Abstract

The understanding of biomechanical regulation of early heart development in genetic mouse models can contribute to improved management of congenital cardiovascular defects and embryonic cardiac failures in humans. The extracellular matrix (ECM), and particularly fibrillar collagen, are central to heart biomechanics, regulating tissue strength, elasticity and contractility. Here, we explore second harmonic generation (SHG) microscopy for visualization of establishing cardiac fibers such as collagen in mouse embryos through the earliest stages of development. We detected significant increase in SHG positive fibrillar content and organization over the first 24 hours after initiation of contractions. SHG microscopy revealed regions of higher fibrillar organization in regions of higher contractility and reduced fibrillar content and organization in mouse Mlc2a model with cardiac contractility defect, suggesting regulatory role of mechanical load in production and organization of structural fibers from the earliest stages. Simultaneous volumetric SHG and two-photon excitation microscopy of vital fluorescent reporter EGFP in the heart was demonstrated. In summary, these data set SHG microscopy as a valuable non-bias imaging tool to investigate mouse embryonic cardiogenesis and biomechanics.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2019 (1)

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
[Crossref] [PubMed]

2018 (2)

S. Masoumi, M. A. Ansari, E. Mohajerani, E. A. Genina, and V. V. Tuchin, “Combination of analytical and experimental optical clearing of rodent specimen for detecting beta-carotene: phantom study,” J. Biomed. Opt. 23(9), 1–7 (2018).
[Crossref] [PubMed]

L. M. Oliveira, M. I. Carvalho, E. M. Nogueira, and V. V. Tuchin, “Skeletal muscle dispersion (400-1000 nm) and kinetics at optical clearing,” J. Biophotonics 11(1), e201700094 (2018).
[Crossref] [PubMed]

2017 (5)

A. Sdobnov, M. E. Darvin, J. Lademann, and V. Tuchin, “A comparative study of ex vivo skin optical clearing using two-photon microscopy,” J. Biophotonics 10(9), 1115–1123 (2017).
[Crossref] [PubMed]

A. S. Piotrowski-Daspit, B. A. Nerger, A. E. Wolf, S. Sundaresan, and C. M. Nelson, “Dynamics of Tissue-Induced Alignment of Fibrous Extracellular Matrix,” Biophys. J. 113(3), 702–713 (2017).
[Crossref] [PubMed]

L. Mostaço-Guidolin, N. L. Rosin, and T.-L. Hackett, “Imaging Collagen in Scar Tissue: Developments in Second Harmonic Generation Microscopy for Biomedical Applications,” Int. J. Mol. Sci. 18(8), 1772 (2017).
[Crossref] [PubMed]

N. H. Green, R. M. Delaine-Smith, H. J. Askew, R. Byers, G. C. Reilly, and S. J. Matcher, “A new mode of contrast in biological second harmonic generation microscopy,” Sci. Rep. 7(1), 13331 (2017).
[Crossref] [PubMed]

M. Midgett, C. S. López, L. David, A. Maloyan, and S. Rugonyi, “Increased Hemodynamic Load in Early Embryonic Stages Alters Myofibril and Mitochondrial Organization in the Myocardium,” Front. Physiol. 8, 631 (2017).
[Crossref] [PubMed]

2016 (2)

J. Liu, W. Yu, Y. Liu, S. Chen, Y. Huang, X. Li, C. Liu, Y. Zhang, Z. Li, J. Du, C. Tang, J. Du, and H. Jin, “Mechanical stretching stimulates collagen synthesis via down-regulating SO2/AAT1 pathway,” Sci. Rep. 6(1), 21112 (2016).
[Crossref] [PubMed]

E. Nam, W. C. Lee, and S. Takeuchi, “Formation of Highly Aligned Collagen Nanofibers by Continuous Cyclic Stretch of a Collagen Hydrogel Sheet,” Macromol. Biosci. 16(7), 995–1000 (2016).
[Crossref] [PubMed]

2015 (3)

A. L. Lopez, S. Wang, K. V. Larin, P. A. Overbeek, and I. V. Larina, “Live four-dimensional optical coherence tomography reveals embryonic cardiac phenotype in mouse mutant,” J. Biomed. Opt. 20(9), 090501 (2015).
[Crossref] [PubMed]

M. D. Garcia, A. L. Lopez, K. V. Larin, and I. V. Larina, “Imaging of cardiovascular development in Mammalian embryos using optical coherence tomography,” Methods Mol. Biol. 1214, 151–161 (2015).
[Crossref] [PubMed]

P. M. Kulkarni, N. Rey-Villamizar, A. Merouane, N. Sudheendran, S. Wang, M. Garcia, I. V. Larina, B. Roysam, and K. V. Larin, “Algorithms for improved 3-D reconstruction of live mammalian embryo vasculature from optical coherence tomography data,” Quant. Imaging Med. Surg. 5(1), 125–135 (2015).
[PubMed]

2014 (7)

S. Dietzel, J. Pircher, A. K. Nekolla, M. Gull, A. W. Brandli, U. Pohl, and M. Rehberg, “Label-free determination of hemodynamic parameters in the microcirculaton with third harmonic generation microscopy,” PLoS ONE 9(6), e99615 (2014).

M. Midgett and S. Rugonyi, “Congenital heart malformations induced by hemodynamic altering surgical interventions,” Front. Physiol. 5, 287 (2014).
[Crossref] [PubMed]

S. V. Biechler, L. Junor, A. N. Evans, J. F. Eberth, R. L. Price, J. D. Potts, M. J. Yost, and R. L. Goodwin, “The impact of flow-induced forces on the morphogenesis of the outflow tract,” Front. Physiol. 5, 225 (2014).
[Crossref] [PubMed]

W. J. Kowalski, K. Pekkan, J. P. Tinney, and B. B. Keller, “Investigating developmental cardiovascular biomechanics and the origins of congenital heart defects,” Front. Physiol. 5, 408 (2014).
[Crossref] [PubMed]

S. E. Lindsey, J. T. Butcher, and H. C. Yalcin, “Mechanical regulation of cardiac development,” Front. Physiol. 5, 318 (2014).
[Crossref] [PubMed]

M. Rienks, A.-P. Papageorgiou, N. G. Frangogiannis, and S. Heymans, “Myocardial Extracellular Matrix,” Circ. Res. 114(5), 872–888 (2014).
[Crossref] [PubMed]

K. Imanaka-Yoshida and H. Aoki, “Tenascin-C and mechanotransduction in the development and diseases of cardiovascular system,” Front. Physiol. 5, 283 (2014).
[Crossref] [PubMed]

2013 (5)

N. K. Weidenhamer and R. T. Tranquillo, “Influence of cyclic mechanical stretch and tissue constraints on cellular and collagen alignment in fibroblast-derived cell sheets,” Tissue Eng. Part C Methods 19(5), 386–395 (2013).
[Crossref] [PubMed]

C. Misra and V. Garg, “Compacting the heart with Notch,” Nat. Med. 19(2), 133–134 (2013).
[Crossref] [PubMed]

J. R. Prigge, J. A. Wiley, E. A. Talago, E. M. Young, L. L. Johns, J. A. Kundert, K. M. Sonsteng, W. P. Halford, M. R. Capecchi, and E. E. Schmidt, “Nuclear double-fluorescent reporter for in vivo and ex vivo analyses of biological transitions in mouse nuclei,” Mamm. Genome 24, 389–399 (2013).

S. Bhat, I. V. Larina, K. V. Larin, M. E. Dickinson, and M. Liebling, “4D reconstruction of the beating embryonic heart from two orthogonal sets of parallel optical coherence tomography slice-sequences,” IEEE Trans. Med. Imaging 32(3), 578–588 (2013).
[Crossref] [PubMed]

D. Zhu, K. V. Larin, Q. Luo, and V. V. Tuchin, “Recent progress in tissue optical clearing,” Laser Photonics Rev. 7(5), 732–757 (2013).
[Crossref] [PubMed]

2012 (2)

J. M. Taylor, J. M. Girkin, and G. D. Love, “High-resolution 3D optical microscopy inside the beating zebrafish heart using prospective optical gating,” Biomed. Opt. Express 3(12), 3043–3053 (2012).
[Crossref] [PubMed]

A. Acharya, S. T. Baek, G. Huang, B. Eskiocak, S. Goetsch, C. Y. Sung, S. Banfi, M. F. Sauer, G. S. Olsen, J. S. Duffield, E. N. Olson, and M. D. Tallquist, “The bHLH transcription factor Tcf21 is required for lineage-specific EMT of cardiac fibroblast progenitors,” Development 139(12), 2139–2149 (2012).
[Crossref] [PubMed]

2011 (4)

M. Rehberg, U. Krombach, F. F. Pohl, S. Pohl, U. F. Dietzel, and S. Dietzel, “Label-free 3D visualization of cellular and tissue structures in intact muscle with second and third harmonic generation microscopy,” PLoS ONE 6(11), e28237 (2011).

W. Supatto, D. T. T. F. Debarre, E. D. D F. Beaurepaire, and E. Beaurepaire, “Advances in multiphoton microscopy for imaging embryos,” Curr. Opin. Genet. Dev. 21(5) 538–548 (2011).

N. Sudheendran, S. H. Syed, M. E. Dickinson, I. V. Larina, and K. V. Larin, “Speckle variance OCT imaging of the vasculature in live mammalian embryos,” Laser Phys. Lett. 8(3), 247–252 (2011).
[Crossref]

S. H. Syed, K. V. Larin, M. E. Dickinson, and I. V. Larina, “Optical coherence tomography for high-resolution imaging of mouse development in utero,” J. Biomed. Opt. 16(4), 046004 (2011).
[Crossref] [PubMed]

2010 (4)

M. W. Jenkins, A. R. Duke, S. Gu, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics 4(9), 623–626 (2010).
[Crossref] [PubMed]

N. Olivier, K. Aptel, F. F. Plamann, M. C. Plamann, K. F. S. Klein, E. S. K. M. F. Beaurepaire, and E. Beaurepaire, “Harmonic microscopy of isotropic and anisotropic microstructure of the human cornea,” Opt. Express 18(5), 5028–5040 (2010).

T. Mammoto and D. E. Ingber, “Mechanical control of tissue and organ development,” Development 137(9), 1407–1420 (2010).
[Crossref] [PubMed]

J. J. Armstrong, I. V. Larina, M. E. Dickinson, W. E. Zimmer, and K. K. Hirschi, “Characterization of bacterial artificial chromosome transgenic mice expressing mCherry fluorescent protein substituted for the murine smooth muscle alpha-actin gene,” Genesis 48(7), 457–463 (2010).
[Crossref] [PubMed]

2009 (3)

I. V. Larina, W. Shen, O. G. Kelly, A.-K. Hadjantonakis, M. H. Baron, and M. E. Dickinson, “A Membrane Associated mCherry Fluorescent Reporter line for Studying Vascular Remodeling and Cardiac Function During Murine Embryonic Development,” Anat. Rec. (Hoboken) 292(3), 333–341 (2009).
[Crossref] [PubMed]

I. V. Larina, K. Furushima, M. E. Dickinson, R. R. Behringer, and K. V. Larin, “Live imaging of rat embryos with Doppler swept-source optical coherence tomography,” J. Biomed. Opt. 14(5), 050506 (2009).
[Crossref] [PubMed]

S. Bhat, I. V. Larina, K. V. Larin, M. E. Dickinson, and M. Liebling, “Multiple-cardiac-cycle noise reduction in dynamic optical coherence tomography of the embryonic heart and vasculature,” Opt. Lett. 34(23), 3704–3706 (2009).
[Crossref] [PubMed]

2008 (2)

I. V. Larina, E. F. Carbajal, V. V. Tuchin, M. E. Dickinson, and K. V. Larin, “Enhanced OCT imaging of embryonic tissue with optical clearing,” Laser Phys. Lett. 5(6), 476–479 (2008).
[Crossref]

I. V. Larina, N. Sudheendran, M. Ghosn, J. Jiang, A. Cable, K. V. Larin, and M. E. Dickinson, “Live imaging of blood flow in mammalian embryos using Doppler swept-source optical coherence tomography,” J. Biomed. Opt. 13(6), 060506 (2008).
[Crossref] [PubMed]

2007 (1)

M. W. Jenkins, O. Q. Chughtai, A. N. Basavanhally, M. Watanabe, and A. M. Rollins, “In vivo gated 4D imaging of the embryonic heart using optical coherence tomography,” J. Biomed. Opt. 12(3), 030505 (2007).
[Crossref] [PubMed]

2006 (3)

V. Gupta and K. J. Grande-Allen, “Effects of static and cyclic loading in regulating extracellular matrix synthesis by cardiovascular cells,” Cardiovasc. Res. 72(3), 375–383 (2006).
[Crossref] [PubMed]

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the Myosin-Based Source for Second-Harmonic Generation from Muscle Sarcomeres,” Biophys. J. 90(2), 693–703 (2006).
[Crossref] [PubMed]

M. C. Rémond, J. A. Fee, E. L. Elson, and L. A. Taber, “Myosin-based contraction is not necessary for cardiac c-looping in the chick embryo,” Anat. Embryol. (Berl.) 211(5), 443–454 (2006).
[Crossref] [PubMed]

2005 (1)

M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt. 10(5), 054001 (2005).
[Crossref] [PubMed]

2004 (1)

E. G. Stanley, C. Biben, A. Elefanty, L. Barnett, F. Koentgen, L. Robb, and R. P. Harvey, “Efficient Cre-mediated deletion in cardiac progenitor cells conferred by a 3’UTR-ires-Cre allele of the homeobox gene Nkx2-5,” Int. J. Dev. Biol. 46, 431–443 (2004).

2003 (2)

C. Huang, F. Sheikh, M. Hollander, C. Cai, D. Becker, P.-H. Chu, S. Evans, and J. Chen, “Embryonic atrial function is essential for mouse embryogenesis, cardiac morphogenesis and angiogenesis,” Development 130(24), 6111–6119 (2003).
[Crossref] [PubMed]

G. Cox, E. Kable, A. Jones, I. Fraser, F. Manconi, and M. D. Gorrell, “3-Dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol. 141(1), 53–62 (2003).
[Crossref] [PubMed]

2002 (2)

D. E. Ingber, “Mechanical signaling and the Cellular Response to Extracellular Matrix in Angiogenesis and Cardiovascular Physiology,” Circ. Res. 91(10), 877–887 (2002).
[Crossref] [PubMed]

E. A. Jones, D. Crotty, P. M. Kulesa, C. W. Waters, M. H. Baron, S. E. Fraser, and M. E. Dickinson, “Dynamic in vivo imaging of postimplantation mammalian embryos using whole embryo culture,” Genesis 34(4), 228–235 (2002).
[Crossref] [PubMed]

2000 (1)

L. K. Hornberger, S. Singhroy, T. Cavalle-Garrido, W. Tsang, F. Keeley, and M. Rabinovitch, “Synthesis of Extracellular Matrix and Adhesion Through β(1) Integrins are Critical for Fetal Ventricular Myocyte Proliferation,” Circ. Res. 87(6), 508–515 (2000).
[Crossref] [PubMed]

1991 (1)

W. Carver, M. L. Nagpal, M. Nachtigal, T. K. Borg, and L. Terracio, “Collagen expression in mechanically stimulated cardiac fibroblasts,” Circ. Res. 69(1), 116–122 (1991).
[Crossref] [PubMed]

Acharya, A.

A. Acharya, S. T. Baek, G. Huang, B. Eskiocak, S. Goetsch, C. Y. Sung, S. Banfi, M. F. Sauer, G. S. Olsen, J. S. Duffield, E. N. Olson, and M. D. Tallquist, “The bHLH transcription factor Tcf21 is required for lineage-specific EMT of cardiac fibroblast progenitors,” Development 139(12), 2139–2149 (2012).
[Crossref] [PubMed]

Alonso, A.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
[Crossref] [PubMed]

Ansari, M. A.

S. Masoumi, M. A. Ansari, E. Mohajerani, E. A. Genina, and V. V. Tuchin, “Combination of analytical and experimental optical clearing of rodent specimen for detecting beta-carotene: phantom study,” J. Biomed. Opt. 23(9), 1–7 (2018).
[Crossref] [PubMed]

Aoki, H.

K. Imanaka-Yoshida and H. Aoki, “Tenascin-C and mechanotransduction in the development and diseases of cardiovascular system,” Front. Physiol. 5, 283 (2014).
[Crossref] [PubMed]

Aptel, K.

Armstrong, J. J.

J. J. Armstrong, I. V. Larina, M. E. Dickinson, W. E. Zimmer, and K. K. Hirschi, “Characterization of bacterial artificial chromosome transgenic mice expressing mCherry fluorescent protein substituted for the murine smooth muscle alpha-actin gene,” Genesis 48(7), 457–463 (2010).
[Crossref] [PubMed]

Askew, H. J.

N. H. Green, R. M. Delaine-Smith, H. J. Askew, R. Byers, G. C. Reilly, and S. J. Matcher, “A new mode of contrast in biological second harmonic generation microscopy,” Sci. Rep. 7(1), 13331 (2017).
[Crossref] [PubMed]

Baek, S. T.

A. Acharya, S. T. Baek, G. Huang, B. Eskiocak, S. Goetsch, C. Y. Sung, S. Banfi, M. F. Sauer, G. S. Olsen, J. S. Duffield, E. N. Olson, and M. D. Tallquist, “The bHLH transcription factor Tcf21 is required for lineage-specific EMT of cardiac fibroblast progenitors,” Development 139(12), 2139–2149 (2012).
[Crossref] [PubMed]

Banfi, S.

A. Acharya, S. T. Baek, G. Huang, B. Eskiocak, S. Goetsch, C. Y. Sung, S. Banfi, M. F. Sauer, G. S. Olsen, J. S. Duffield, E. N. Olson, and M. D. Tallquist, “The bHLH transcription factor Tcf21 is required for lineage-specific EMT of cardiac fibroblast progenitors,” Development 139(12), 2139–2149 (2012).
[Crossref] [PubMed]

Barnett, L.

E. G. Stanley, C. Biben, A. Elefanty, L. Barnett, F. Koentgen, L. Robb, and R. P. Harvey, “Efficient Cre-mediated deletion in cardiac progenitor cells conferred by a 3’UTR-ires-Cre allele of the homeobox gene Nkx2-5,” Int. J. Dev. Biol. 46, 431–443 (2004).

Baron, M. H.

I. V. Larina, W. Shen, O. G. Kelly, A.-K. Hadjantonakis, M. H. Baron, and M. E. Dickinson, “A Membrane Associated mCherry Fluorescent Reporter line for Studying Vascular Remodeling and Cardiac Function During Murine Embryonic Development,” Anat. Rec. (Hoboken) 292(3), 333–341 (2009).
[Crossref] [PubMed]

E. A. Jones, D. Crotty, P. M. Kulesa, C. W. Waters, M. H. Baron, S. E. Fraser, and M. E. Dickinson, “Dynamic in vivo imaging of postimplantation mammalian embryos using whole embryo culture,” Genesis 34(4), 228–235 (2002).
[Crossref] [PubMed]

Basavanhally, A. N.

M. W. Jenkins, O. Q. Chughtai, A. N. Basavanhally, M. Watanabe, and A. M. Rollins, “In vivo gated 4D imaging of the embryonic heart using optical coherence tomography,” J. Biomed. Opt. 12(3), 030505 (2007).
[Crossref] [PubMed]

Beaurepaire, E.

W. Supatto, D. T. T. F. Debarre, E. D. D F. Beaurepaire, and E. Beaurepaire, “Advances in multiphoton microscopy for imaging embryos,” Curr. Opin. Genet. Dev. 21(5) 538–548 (2011).

N. Olivier, K. Aptel, F. F. Plamann, M. C. Plamann, K. F. S. Klein, E. S. K. M. F. Beaurepaire, and E. Beaurepaire, “Harmonic microscopy of isotropic and anisotropic microstructure of the human cornea,” Opt. Express 18(5), 5028–5040 (2010).

Beaurepaire, E. D. D F.

W. Supatto, D. T. T. F. Debarre, E. D. D F. Beaurepaire, and E. Beaurepaire, “Advances in multiphoton microscopy for imaging embryos,” Curr. Opin. Genet. Dev. 21(5) 538–548 (2011).

Beaurepaire, E. S. K. M. F.

Becker, D.

C. Huang, F. Sheikh, M. Hollander, C. Cai, D. Becker, P.-H. Chu, S. Evans, and J. Chen, “Embryonic atrial function is essential for mouse embryogenesis, cardiac morphogenesis and angiogenesis,” Development 130(24), 6111–6119 (2003).
[Crossref] [PubMed]

Behringer, R. R.

I. V. Larina, K. Furushima, M. E. Dickinson, R. R. Behringer, and K. V. Larin, “Live imaging of rat embryos with Doppler swept-source optical coherence tomography,” J. Biomed. Opt. 14(5), 050506 (2009).
[Crossref] [PubMed]

Benjamin, E. J.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
[Crossref] [PubMed]

Bhat, S.

S. Bhat, I. V. Larina, K. V. Larin, M. E. Dickinson, and M. Liebling, “4D reconstruction of the beating embryonic heart from two orthogonal sets of parallel optical coherence tomography slice-sequences,” IEEE Trans. Med. Imaging 32(3), 578–588 (2013).
[Crossref] [PubMed]

S. Bhat, I. V. Larina, K. V. Larin, M. E. Dickinson, and M. Liebling, “Multiple-cardiac-cycle noise reduction in dynamic optical coherence tomography of the embryonic heart and vasculature,” Opt. Lett. 34(23), 3704–3706 (2009).
[Crossref] [PubMed]

Biben, C.

E. G. Stanley, C. Biben, A. Elefanty, L. Barnett, F. Koentgen, L. Robb, and R. P. Harvey, “Efficient Cre-mediated deletion in cardiac progenitor cells conferred by a 3’UTR-ires-Cre allele of the homeobox gene Nkx2-5,” Int. J. Dev. Biol. 46, 431–443 (2004).

Biechler, S. V.

S. V. Biechler, L. Junor, A. N. Evans, J. F. Eberth, R. L. Price, J. D. Potts, M. J. Yost, and R. L. Goodwin, “The impact of flow-induced forces on the morphogenesis of the outflow tract,” Front. Physiol. 5, 225 (2014).
[Crossref] [PubMed]

Bittencourt, M. S.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
[Crossref] [PubMed]

Borg, T. K.

W. Carver, M. L. Nagpal, M. Nachtigal, T. K. Borg, and L. Terracio, “Collagen expression in mechanically stimulated cardiac fibroblasts,” Circ. Res. 69(1), 116–122 (1991).
[Crossref] [PubMed]

Brandli, A. W.

S. Dietzel, J. Pircher, A. K. Nekolla, M. Gull, A. W. Brandli, U. Pohl, and M. Rehberg, “Label-free determination of hemodynamic parameters in the microcirculaton with third harmonic generation microscopy,” PLoS ONE 9(6), e99615 (2014).

Butcher, J. T.

S. E. Lindsey, J. T. Butcher, and H. C. Yalcin, “Mechanical regulation of cardiac development,” Front. Physiol. 5, 318 (2014).
[Crossref] [PubMed]

Byers, R.

N. H. Green, R. M. Delaine-Smith, H. J. Askew, R. Byers, G. C. Reilly, and S. J. Matcher, “A new mode of contrast in biological second harmonic generation microscopy,” Sci. Rep. 7(1), 13331 (2017).
[Crossref] [PubMed]

Cable, A.

I. V. Larina, N. Sudheendran, M. Ghosn, J. Jiang, A. Cable, K. V. Larin, and M. E. Dickinson, “Live imaging of blood flow in mammalian embryos using Doppler swept-source optical coherence tomography,” J. Biomed. Opt. 13(6), 060506 (2008).
[Crossref] [PubMed]

Cai, C.

C. Huang, F. Sheikh, M. Hollander, C. Cai, D. Becker, P.-H. Chu, S. Evans, and J. Chen, “Embryonic atrial function is essential for mouse embryogenesis, cardiac morphogenesis and angiogenesis,” Development 130(24), 6111–6119 (2003).
[Crossref] [PubMed]

Callaway, C. W.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
[Crossref] [PubMed]

Campagnola, P. J.

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the Myosin-Based Source for Second-Harmonic Generation from Muscle Sarcomeres,” Biophys. J. 90(2), 693–703 (2006).
[Crossref] [PubMed]

Capecchi, M. R.

J. R. Prigge, J. A. Wiley, E. A. Talago, E. M. Young, L. L. Johns, J. A. Kundert, K. M. Sonsteng, W. P. Halford, M. R. Capecchi, and E. E. Schmidt, “Nuclear double-fluorescent reporter for in vivo and ex vivo analyses of biological transitions in mouse nuclei,” Mamm. Genome 24, 389–399 (2013).

Carbajal, E. F.

I. V. Larina, E. F. Carbajal, V. V. Tuchin, M. E. Dickinson, and K. V. Larin, “Enhanced OCT imaging of embryonic tissue with optical clearing,” Laser Phys. Lett. 5(6), 476–479 (2008).
[Crossref]

Carson, A. P.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
[Crossref] [PubMed]

Carvalho, M. I.

L. M. Oliveira, M. I. Carvalho, E. M. Nogueira, and V. V. Tuchin, “Skeletal muscle dispersion (400-1000 nm) and kinetics at optical clearing,” J. Biophotonics 11(1), e201700094 (2018).
[Crossref] [PubMed]

Carver, W.

W. Carver, M. L. Nagpal, M. Nachtigal, T. K. Borg, and L. Terracio, “Collagen expression in mechanically stimulated cardiac fibroblasts,” Circ. Res. 69(1), 116–122 (1991).
[Crossref] [PubMed]

Cavalle-Garrido, T.

L. K. Hornberger, S. Singhroy, T. Cavalle-Garrido, W. Tsang, F. Keeley, and M. Rabinovitch, “Synthesis of Extracellular Matrix and Adhesion Through β(1) Integrins are Critical for Fetal Ventricular Myocyte Proliferation,” Circ. Res. 87(6), 508–515 (2000).
[Crossref] [PubMed]

Chamberlain, A. M.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
[Crossref] [PubMed]

Chang, A. R.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
[Crossref] [PubMed]

Chen, J.

C. Huang, F. Sheikh, M. Hollander, C. Cai, D. Becker, P.-H. Chu, S. Evans, and J. Chen, “Embryonic atrial function is essential for mouse embryogenesis, cardiac morphogenesis and angiogenesis,” Development 130(24), 6111–6119 (2003).
[Crossref] [PubMed]

Chen, S.

J. Liu, W. Yu, Y. Liu, S. Chen, Y. Huang, X. Li, C. Liu, Y. Zhang, Z. Li, J. Du, C. Tang, J. Du, and H. Jin, “Mechanical stretching stimulates collagen synthesis via down-regulating SO2/AAT1 pathway,” Sci. Rep. 6(1), 21112 (2016).
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Cheng, S.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
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Chiel, H. J.

M. W. Jenkins, A. R. Duke, S. Gu, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics 4(9), 623–626 (2010).
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Chu, P.-H.

C. Huang, F. Sheikh, M. Hollander, C. Cai, D. Becker, P.-H. Chu, S. Evans, and J. Chen, “Embryonic atrial function is essential for mouse embryogenesis, cardiac morphogenesis and angiogenesis,” Development 130(24), 6111–6119 (2003).
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Chughtai, O. Q.

M. W. Jenkins, O. Q. Chughtai, A. N. Basavanhally, M. Watanabe, and A. M. Rollins, “In vivo gated 4D imaging of the embryonic heart using optical coherence tomography,” J. Biomed. Opt. 12(3), 030505 (2007).
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G. Cox, E. Kable, A. Jones, I. Fraser, F. Manconi, and M. D. Gorrell, “3-Dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol. 141(1), 53–62 (2003).
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Crotty, D.

E. A. Jones, D. Crotty, P. M. Kulesa, C. W. Waters, M. H. Baron, S. E. Fraser, and M. E. Dickinson, “Dynamic in vivo imaging of postimplantation mammalian embryos using whole embryo culture,” Genesis 34(4), 228–235 (2002).
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Darvin, M. E.

A. Sdobnov, M. E. Darvin, J. Lademann, and V. Tuchin, “A comparative study of ex vivo skin optical clearing using two-photon microscopy,” J. Biophotonics 10(9), 1115–1123 (2017).
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A. Y. Sdobnov, M. E. Darvin, J. Schleusener, J. Lademann, and V. V. Tuchin, “Hydrogen bound water profiles in the skin influenced by optical clearing molecular agents-Quantitative analysis using confocal Raman microscopy,” J. Biophotonics, 201800283 (2018).

Das, S. R.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
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M. Midgett, C. S. López, L. David, A. Maloyan, and S. Rugonyi, “Increased Hemodynamic Load in Early Embryonic Stages Alters Myofibril and Mitochondrial Organization in the Myocardium,” Front. Physiol. 8, 631 (2017).
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W. Supatto, D. T. T. F. Debarre, E. D. D F. Beaurepaire, and E. Beaurepaire, “Advances in multiphoton microscopy for imaging embryos,” Curr. Opin. Genet. Dev. 21(5) 538–548 (2011).

Delaine-Smith, R. M.

N. H. Green, R. M. Delaine-Smith, H. J. Askew, R. Byers, G. C. Reilly, and S. J. Matcher, “A new mode of contrast in biological second harmonic generation microscopy,” Sci. Rep. 7(1), 13331 (2017).
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Delling, F. N.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
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Dickinson, M. E.

S. Bhat, I. V. Larina, K. V. Larin, M. E. Dickinson, and M. Liebling, “4D reconstruction of the beating embryonic heart from two orthogonal sets of parallel optical coherence tomography slice-sequences,” IEEE Trans. Med. Imaging 32(3), 578–588 (2013).
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S. H. Syed, K. V. Larin, M. E. Dickinson, and I. V. Larina, “Optical coherence tomography for high-resolution imaging of mouse development in utero,” J. Biomed. Opt. 16(4), 046004 (2011).
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N. Sudheendran, S. H. Syed, M. E. Dickinson, I. V. Larina, and K. V. Larin, “Speckle variance OCT imaging of the vasculature in live mammalian embryos,” Laser Phys. Lett. 8(3), 247–252 (2011).
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J. J. Armstrong, I. V. Larina, M. E. Dickinson, W. E. Zimmer, and K. K. Hirschi, “Characterization of bacterial artificial chromosome transgenic mice expressing mCherry fluorescent protein substituted for the murine smooth muscle alpha-actin gene,” Genesis 48(7), 457–463 (2010).
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I. V. Larina, W. Shen, O. G. Kelly, A.-K. Hadjantonakis, M. H. Baron, and M. E. Dickinson, “A Membrane Associated mCherry Fluorescent Reporter line for Studying Vascular Remodeling and Cardiac Function During Murine Embryonic Development,” Anat. Rec. (Hoboken) 292(3), 333–341 (2009).
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I. V. Larina, K. Furushima, M. E. Dickinson, R. R. Behringer, and K. V. Larin, “Live imaging of rat embryos with Doppler swept-source optical coherence tomography,” J. Biomed. Opt. 14(5), 050506 (2009).
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S. Bhat, I. V. Larina, K. V. Larin, M. E. Dickinson, and M. Liebling, “Multiple-cardiac-cycle noise reduction in dynamic optical coherence tomography of the embryonic heart and vasculature,” Opt. Lett. 34(23), 3704–3706 (2009).
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I. V. Larina, E. F. Carbajal, V. V. Tuchin, M. E. Dickinson, and K. V. Larin, “Enhanced OCT imaging of embryonic tissue with optical clearing,” Laser Phys. Lett. 5(6), 476–479 (2008).
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I. V. Larina, N. Sudheendran, M. Ghosn, J. Jiang, A. Cable, K. V. Larin, and M. E. Dickinson, “Live imaging of blood flow in mammalian embryos using Doppler swept-source optical coherence tomography,” J. Biomed. Opt. 13(6), 060506 (2008).
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M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt. 10(5), 054001 (2005).
[Crossref] [PubMed]

E. A. Jones, D. Crotty, P. M. Kulesa, C. W. Waters, M. H. Baron, S. E. Fraser, and M. E. Dickinson, “Dynamic in vivo imaging of postimplantation mammalian embryos using whole embryo culture,” Genesis 34(4), 228–235 (2002).
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Dietzel, S.

S. Dietzel, J. Pircher, A. K. Nekolla, M. Gull, A. W. Brandli, U. Pohl, and M. Rehberg, “Label-free determination of hemodynamic parameters in the microcirculaton with third harmonic generation microscopy,” PLoS ONE 9(6), e99615 (2014).

M. Rehberg, U. Krombach, F. F. Pohl, S. Pohl, U. F. Dietzel, and S. Dietzel, “Label-free 3D visualization of cellular and tissue structures in intact muscle with second and third harmonic generation microscopy,” PLoS ONE 6(11), e28237 (2011).

Dietzel, U. F.

M. Rehberg, U. Krombach, F. F. Pohl, S. Pohl, U. F. Dietzel, and S. Dietzel, “Label-free 3D visualization of cellular and tissue structures in intact muscle with second and third harmonic generation microscopy,” PLoS ONE 6(11), e28237 (2011).

Djousse, L.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
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Du, J.

J. Liu, W. Yu, Y. Liu, S. Chen, Y. Huang, X. Li, C. Liu, Y. Zhang, Z. Li, J. Du, C. Tang, J. Du, and H. Jin, “Mechanical stretching stimulates collagen synthesis via down-regulating SO2/AAT1 pathway,” Sci. Rep. 6(1), 21112 (2016).
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J. Liu, W. Yu, Y. Liu, S. Chen, Y. Huang, X. Li, C. Liu, Y. Zhang, Z. Li, J. Du, C. Tang, J. Du, and H. Jin, “Mechanical stretching stimulates collagen synthesis via down-regulating SO2/AAT1 pathway,” Sci. Rep. 6(1), 21112 (2016).
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A. Acharya, S. T. Baek, G. Huang, B. Eskiocak, S. Goetsch, C. Y. Sung, S. Banfi, M. F. Sauer, G. S. Olsen, J. S. Duffield, E. N. Olson, and M. D. Tallquist, “The bHLH transcription factor Tcf21 is required for lineage-specific EMT of cardiac fibroblast progenitors,” Development 139(12), 2139–2149 (2012).
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Duke, A. R.

M. W. Jenkins, A. R. Duke, S. Gu, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics 4(9), 623–626 (2010).
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S. V. Biechler, L. Junor, A. N. Evans, J. F. Eberth, R. L. Price, J. D. Potts, M. J. Yost, and R. L. Goodwin, “The impact of flow-induced forces on the morphogenesis of the outflow tract,” Front. Physiol. 5, 225 (2014).
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Elefanty, A.

E. G. Stanley, C. Biben, A. Elefanty, L. Barnett, F. Koentgen, L. Robb, and R. P. Harvey, “Efficient Cre-mediated deletion in cardiac progenitor cells conferred by a 3’UTR-ires-Cre allele of the homeobox gene Nkx2-5,” Int. J. Dev. Biol. 46, 431–443 (2004).

Elkind, M. S. V.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
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Elson, E. L.

M. C. Rémond, J. A. Fee, E. L. Elson, and L. A. Taber, “Myosin-based contraction is not necessary for cardiac c-looping in the chick embryo,” Anat. Embryol. (Berl.) 211(5), 443–454 (2006).
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Eskiocak, B.

A. Acharya, S. T. Baek, G. Huang, B. Eskiocak, S. Goetsch, C. Y. Sung, S. Banfi, M. F. Sauer, G. S. Olsen, J. S. Duffield, E. N. Olson, and M. D. Tallquist, “The bHLH transcription factor Tcf21 is required for lineage-specific EMT of cardiac fibroblast progenitors,” Development 139(12), 2139–2149 (2012).
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Evans, A. N.

S. V. Biechler, L. Junor, A. N. Evans, J. F. Eberth, R. L. Price, J. D. Potts, M. J. Yost, and R. L. Goodwin, “The impact of flow-induced forces on the morphogenesis of the outflow tract,” Front. Physiol. 5, 225 (2014).
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Evans, S.

C. Huang, F. Sheikh, M. Hollander, C. Cai, D. Becker, P.-H. Chu, S. Evans, and J. Chen, “Embryonic atrial function is essential for mouse embryogenesis, cardiac morphogenesis and angiogenesis,” Development 130(24), 6111–6119 (2003).
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Fee, J. A.

M. C. Rémond, J. A. Fee, E. L. Elson, and L. A. Taber, “Myosin-based contraction is not necessary for cardiac c-looping in the chick embryo,” Anat. Embryol. (Berl.) 211(5), 443–454 (2006).
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Ferguson, J. F.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
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Fornage, M.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
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Forouhar, A. S.

M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt. 10(5), 054001 (2005).
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M. Rienks, A.-P. Papageorgiou, N. G. Frangogiannis, and S. Heymans, “Myocardial Extracellular Matrix,” Circ. Res. 114(5), 872–888 (2014).
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Fraser, I.

G. Cox, E. Kable, A. Jones, I. Fraser, F. Manconi, and M. D. Gorrell, “3-Dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol. 141(1), 53–62 (2003).
[Crossref] [PubMed]

Fraser, S. E.

M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt. 10(5), 054001 (2005).
[Crossref] [PubMed]

E. A. Jones, D. Crotty, P. M. Kulesa, C. W. Waters, M. H. Baron, S. E. Fraser, and M. E. Dickinson, “Dynamic in vivo imaging of postimplantation mammalian embryos using whole embryo culture,” Genesis 34(4), 228–235 (2002).
[Crossref] [PubMed]

Fujioka, H.

M. W. Jenkins, A. R. Duke, S. Gu, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics 4(9), 623–626 (2010).
[Crossref] [PubMed]

Furushima, K.

I. V. Larina, K. Furushima, M. E. Dickinson, R. R. Behringer, and K. V. Larin, “Live imaging of rat embryos with Doppler swept-source optical coherence tomography,” J. Biomed. Opt. 14(5), 050506 (2009).
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Garcia, M.

P. M. Kulkarni, N. Rey-Villamizar, A. Merouane, N. Sudheendran, S. Wang, M. Garcia, I. V. Larina, B. Roysam, and K. V. Larin, “Algorithms for improved 3-D reconstruction of live mammalian embryo vasculature from optical coherence tomography data,” Quant. Imaging Med. Surg. 5(1), 125–135 (2015).
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M. D. Garcia, A. L. Lopez, K. V. Larin, and I. V. Larina, “Imaging of cardiovascular development in Mammalian embryos using optical coherence tomography,” Methods Mol. Biol. 1214, 151–161 (2015).
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C. Misra and V. Garg, “Compacting the heart with Notch,” Nat. Med. 19(2), 133–134 (2013).
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S. Masoumi, M. A. Ansari, E. Mohajerani, E. A. Genina, and V. V. Tuchin, “Combination of analytical and experimental optical clearing of rodent specimen for detecting beta-carotene: phantom study,” J. Biomed. Opt. 23(9), 1–7 (2018).
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Gharib, M.

M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt. 10(5), 054001 (2005).
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Ghosn, M.

I. V. Larina, N. Sudheendran, M. Ghosn, J. Jiang, A. Cable, K. V. Larin, and M. E. Dickinson, “Live imaging of blood flow in mammalian embryos using Doppler swept-source optical coherence tomography,” J. Biomed. Opt. 13(6), 060506 (2008).
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Girkin, J. M.

Goetsch, S.

A. Acharya, S. T. Baek, G. Huang, B. Eskiocak, S. Goetsch, C. Y. Sung, S. Banfi, M. F. Sauer, G. S. Olsen, J. S. Duffield, E. N. Olson, and M. D. Tallquist, “The bHLH transcription factor Tcf21 is required for lineage-specific EMT of cardiac fibroblast progenitors,” Development 139(12), 2139–2149 (2012).
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Goodwin, R. L.

S. V. Biechler, L. Junor, A. N. Evans, J. F. Eberth, R. L. Price, J. D. Potts, M. J. Yost, and R. L. Goodwin, “The impact of flow-induced forces on the morphogenesis of the outflow tract,” Front. Physiol. 5, 225 (2014).
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Gorrell, M. D.

G. Cox, E. Kable, A. Jones, I. Fraser, F. Manconi, and M. D. Gorrell, “3-Dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol. 141(1), 53–62 (2003).
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V. Gupta and K. J. Grande-Allen, “Effects of static and cyclic loading in regulating extracellular matrix synthesis by cardiovascular cells,” Cardiovasc. Res. 72(3), 375–383 (2006).
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N. H. Green, R. M. Delaine-Smith, H. J. Askew, R. Byers, G. C. Reilly, and S. J. Matcher, “A new mode of contrast in biological second harmonic generation microscopy,” Sci. Rep. 7(1), 13331 (2017).
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Gu, S.

M. W. Jenkins, A. R. Duke, S. Gu, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics 4(9), 623–626 (2010).
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Gull, M.

S. Dietzel, J. Pircher, A. K. Nekolla, M. Gull, A. W. Brandli, U. Pohl, and M. Rehberg, “Label-free determination of hemodynamic parameters in the microcirculaton with third harmonic generation microscopy,” PLoS ONE 9(6), e99615 (2014).

Gupta, V.

V. Gupta and K. J. Grande-Allen, “Effects of static and cyclic loading in regulating extracellular matrix synthesis by cardiovascular cells,” Cardiovasc. Res. 72(3), 375–383 (2006).
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L. Mostaço-Guidolin, N. L. Rosin, and T.-L. Hackett, “Imaging Collagen in Scar Tissue: Developments in Second Harmonic Generation Microscopy for Biomedical Applications,” Int. J. Mol. Sci. 18(8), 1772 (2017).
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Hadjantonakis, A.-K.

I. V. Larina, W. Shen, O. G. Kelly, A.-K. Hadjantonakis, M. H. Baron, and M. E. Dickinson, “A Membrane Associated mCherry Fluorescent Reporter line for Studying Vascular Remodeling and Cardiac Function During Murine Embryonic Development,” Anat. Rec. (Hoboken) 292(3), 333–341 (2009).
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Halford, W. P.

J. R. Prigge, J. A. Wiley, E. A. Talago, E. M. Young, L. L. Johns, J. A. Kundert, K. M. Sonsteng, W. P. Halford, M. R. Capecchi, and E. E. Schmidt, “Nuclear double-fluorescent reporter for in vivo and ex vivo analyses of biological transitions in mouse nuclei,” Mamm. Genome 24, 389–399 (2013).

Harvey, R. P.

E. G. Stanley, C. Biben, A. Elefanty, L. Barnett, F. Koentgen, L. Robb, and R. P. Harvey, “Efficient Cre-mediated deletion in cardiac progenitor cells conferred by a 3’UTR-ires-Cre allele of the homeobox gene Nkx2-5,” Int. J. Dev. Biol. 46, 431–443 (2004).

Heymans, S.

M. Rienks, A.-P. Papageorgiou, N. G. Frangogiannis, and S. Heymans, “Myocardial Extracellular Matrix,” Circ. Res. 114(5), 872–888 (2014).
[Crossref] [PubMed]

Hirschi, K. K.

J. J. Armstrong, I. V. Larina, M. E. Dickinson, W. E. Zimmer, and K. K. Hirschi, “Characterization of bacterial artificial chromosome transgenic mice expressing mCherry fluorescent protein substituted for the murine smooth muscle alpha-actin gene,” Genesis 48(7), 457–463 (2010).
[Crossref] [PubMed]

Hollander, M.

C. Huang, F. Sheikh, M. Hollander, C. Cai, D. Becker, P.-H. Chu, S. Evans, and J. Chen, “Embryonic atrial function is essential for mouse embryogenesis, cardiac morphogenesis and angiogenesis,” Development 130(24), 6111–6119 (2003).
[Crossref] [PubMed]

Hornberger, L. K.

L. K. Hornberger, S. Singhroy, T. Cavalle-Garrido, W. Tsang, F. Keeley, and M. Rabinovitch, “Synthesis of Extracellular Matrix and Adhesion Through β(1) Integrins are Critical for Fetal Ventricular Myocyte Proliferation,” Circ. Res. 87(6), 508–515 (2000).
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Huang, C.

C. Huang, F. Sheikh, M. Hollander, C. Cai, D. Becker, P.-H. Chu, S. Evans, and J. Chen, “Embryonic atrial function is essential for mouse embryogenesis, cardiac morphogenesis and angiogenesis,” Development 130(24), 6111–6119 (2003).
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Huang, G.

A. Acharya, S. T. Baek, G. Huang, B. Eskiocak, S. Goetsch, C. Y. Sung, S. Banfi, M. F. Sauer, G. S. Olsen, J. S. Duffield, E. N. Olson, and M. D. Tallquist, “The bHLH transcription factor Tcf21 is required for lineage-specific EMT of cardiac fibroblast progenitors,” Development 139(12), 2139–2149 (2012).
[Crossref] [PubMed]

Huang, Y.

J. Liu, W. Yu, Y. Liu, S. Chen, Y. Huang, X. Li, C. Liu, Y. Zhang, Z. Li, J. Du, C. Tang, J. Du, and H. Jin, “Mechanical stretching stimulates collagen synthesis via down-regulating SO2/AAT1 pathway,” Sci. Rep. 6(1), 21112 (2016).
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Imanaka-Yoshida, K.

K. Imanaka-Yoshida and H. Aoki, “Tenascin-C and mechanotransduction in the development and diseases of cardiovascular system,” Front. Physiol. 5, 283 (2014).
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Ingber, D. E.

T. Mammoto and D. E. Ingber, “Mechanical control of tissue and organ development,” Development 137(9), 1407–1420 (2010).
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D. E. Ingber, “Mechanical signaling and the Cellular Response to Extracellular Matrix in Angiogenesis and Cardiovascular Physiology,” Circ. Res. 91(10), 877–887 (2002).
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Jansen, E. D.

M. W. Jenkins, A. R. Duke, S. Gu, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics 4(9), 623–626 (2010).
[Crossref] [PubMed]

Jenkins, M. W.

M. W. Jenkins, A. R. Duke, S. Gu, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics 4(9), 623–626 (2010).
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M. W. Jenkins, O. Q. Chughtai, A. N. Basavanhally, M. Watanabe, and A. M. Rollins, “In vivo gated 4D imaging of the embryonic heart using optical coherence tomography,” J. Biomed. Opt. 12(3), 030505 (2007).
[Crossref] [PubMed]

Jiang, J.

I. V. Larina, N. Sudheendran, M. Ghosn, J. Jiang, A. Cable, K. V. Larin, and M. E. Dickinson, “Live imaging of blood flow in mammalian embryos using Doppler swept-source optical coherence tomography,” J. Biomed. Opt. 13(6), 060506 (2008).
[Crossref] [PubMed]

Jin, H.

J. Liu, W. Yu, Y. Liu, S. Chen, Y. Huang, X. Li, C. Liu, Y. Zhang, Z. Li, J. Du, C. Tang, J. Du, and H. Jin, “Mechanical stretching stimulates collagen synthesis via down-regulating SO2/AAT1 pathway,” Sci. Rep. 6(1), 21112 (2016).
[Crossref] [PubMed]

Johns, L. L.

J. R. Prigge, J. A. Wiley, E. A. Talago, E. M. Young, L. L. Johns, J. A. Kundert, K. M. Sonsteng, W. P. Halford, M. R. Capecchi, and E. E. Schmidt, “Nuclear double-fluorescent reporter for in vivo and ex vivo analyses of biological transitions in mouse nuclei,” Mamm. Genome 24, 389–399 (2013).

Jones, A.

G. Cox, E. Kable, A. Jones, I. Fraser, F. Manconi, and M. D. Gorrell, “3-Dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol. 141(1), 53–62 (2003).
[Crossref] [PubMed]

Jones, E. A.

E. A. Jones, D. Crotty, P. M. Kulesa, C. W. Waters, M. H. Baron, S. E. Fraser, and M. E. Dickinson, “Dynamic in vivo imaging of postimplantation mammalian embryos using whole embryo culture,” Genesis 34(4), 228–235 (2002).
[Crossref] [PubMed]

Jordan, L. C.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
[Crossref] [PubMed]

Junor, L.

S. V. Biechler, L. Junor, A. N. Evans, J. F. Eberth, R. L. Price, J. D. Potts, M. J. Yost, and R. L. Goodwin, “The impact of flow-induced forces on the morphogenesis of the outflow tract,” Front. Physiol. 5, 225 (2014).
[Crossref] [PubMed]

Kable, E.

G. Cox, E. Kable, A. Jones, I. Fraser, F. Manconi, and M. D. Gorrell, “3-Dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol. 141(1), 53–62 (2003).
[Crossref] [PubMed]

Keeley, F.

L. K. Hornberger, S. Singhroy, T. Cavalle-Garrido, W. Tsang, F. Keeley, and M. Rabinovitch, “Synthesis of Extracellular Matrix and Adhesion Through β(1) Integrins are Critical for Fetal Ventricular Myocyte Proliferation,” Circ. Res. 87(6), 508–515 (2000).
[Crossref] [PubMed]

Keller, B. B.

W. J. Kowalski, K. Pekkan, J. P. Tinney, and B. B. Keller, “Investigating developmental cardiovascular biomechanics and the origins of congenital heart defects,” Front. Physiol. 5, 408 (2014).
[Crossref] [PubMed]

Kelly, O. G.

I. V. Larina, W. Shen, O. G. Kelly, A.-K. Hadjantonakis, M. H. Baron, and M. E. Dickinson, “A Membrane Associated mCherry Fluorescent Reporter line for Studying Vascular Remodeling and Cardiac Function During Murine Embryonic Development,” Anat. Rec. (Hoboken) 292(3), 333–341 (2009).
[Crossref] [PubMed]

Khan, S. S.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
[Crossref] [PubMed]

Kissela, B. M.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
[Crossref] [PubMed]

Klein, K. F. S.

Knutson, K. L.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
[Crossref] [PubMed]

Koentgen, F.

E. G. Stanley, C. Biben, A. Elefanty, L. Barnett, F. Koentgen, L. Robb, and R. P. Harvey, “Efficient Cre-mediated deletion in cardiac progenitor cells conferred by a 3’UTR-ires-Cre allele of the homeobox gene Nkx2-5,” Int. J. Dev. Biol. 46, 431–443 (2004).

Kowalski, W. J.

W. J. Kowalski, K. Pekkan, J. P. Tinney, and B. B. Keller, “Investigating developmental cardiovascular biomechanics and the origins of congenital heart defects,” Front. Physiol. 5, 408 (2014).
[Crossref] [PubMed]

Krombach, U.

M. Rehberg, U. Krombach, F. F. Pohl, S. Pohl, U. F. Dietzel, and S. Dietzel, “Label-free 3D visualization of cellular and tissue structures in intact muscle with second and third harmonic generation microscopy,” PLoS ONE 6(11), e28237 (2011).

Kulesa, P. M.

E. A. Jones, D. Crotty, P. M. Kulesa, C. W. Waters, M. H. Baron, S. E. Fraser, and M. E. Dickinson, “Dynamic in vivo imaging of postimplantation mammalian embryos using whole embryo culture,” Genesis 34(4), 228–235 (2002).
[Crossref] [PubMed]

Kulkarni, P. M.

P. M. Kulkarni, N. Rey-Villamizar, A. Merouane, N. Sudheendran, S. Wang, M. Garcia, I. V. Larina, B. Roysam, and K. V. Larin, “Algorithms for improved 3-D reconstruction of live mammalian embryo vasculature from optical coherence tomography data,” Quant. Imaging Med. Surg. 5(1), 125–135 (2015).
[PubMed]

Kundert, J. A.

J. R. Prigge, J. A. Wiley, E. A. Talago, E. M. Young, L. L. Johns, J. A. Kundert, K. M. Sonsteng, W. P. Halford, M. R. Capecchi, and E. E. Schmidt, “Nuclear double-fluorescent reporter for in vivo and ex vivo analyses of biological transitions in mouse nuclei,” Mamm. Genome 24, 389–399 (2013).

Kwan, T. W.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
[Crossref] [PubMed]

Lackland, D. T.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
[Crossref] [PubMed]

Lademann, J.

A. Sdobnov, M. E. Darvin, J. Lademann, and V. Tuchin, “A comparative study of ex vivo skin optical clearing using two-photon microscopy,” J. Biophotonics 10(9), 1115–1123 (2017).
[Crossref] [PubMed]

A. Y. Sdobnov, M. E. Darvin, J. Schleusener, J. Lademann, and V. V. Tuchin, “Hydrogen bound water profiles in the skin influenced by optical clearing molecular agents-Quantitative analysis using confocal Raman microscopy,” J. Biophotonics, 201800283 (2018).

Larin, K. V.

M. D. Garcia, A. L. Lopez, K. V. Larin, and I. V. Larina, “Imaging of cardiovascular development in Mammalian embryos using optical coherence tomography,” Methods Mol. Biol. 1214, 151–161 (2015).
[Crossref] [PubMed]

P. M. Kulkarni, N. Rey-Villamizar, A. Merouane, N. Sudheendran, S. Wang, M. Garcia, I. V. Larina, B. Roysam, and K. V. Larin, “Algorithms for improved 3-D reconstruction of live mammalian embryo vasculature from optical coherence tomography data,” Quant. Imaging Med. Surg. 5(1), 125–135 (2015).
[PubMed]

A. L. Lopez, S. Wang, K. V. Larin, P. A. Overbeek, and I. V. Larina, “Live four-dimensional optical coherence tomography reveals embryonic cardiac phenotype in mouse mutant,” J. Biomed. Opt. 20(9), 090501 (2015).
[Crossref] [PubMed]

S. Bhat, I. V. Larina, K. V. Larin, M. E. Dickinson, and M. Liebling, “4D reconstruction of the beating embryonic heart from two orthogonal sets of parallel optical coherence tomography slice-sequences,” IEEE Trans. Med. Imaging 32(3), 578–588 (2013).
[Crossref] [PubMed]

D. Zhu, K. V. Larin, Q. Luo, and V. V. Tuchin, “Recent progress in tissue optical clearing,” Laser Photonics Rev. 7(5), 732–757 (2013).
[Crossref] [PubMed]

S. H. Syed, K. V. Larin, M. E. Dickinson, and I. V. Larina, “Optical coherence tomography for high-resolution imaging of mouse development in utero,” J. Biomed. Opt. 16(4), 046004 (2011).
[Crossref] [PubMed]

N. Sudheendran, S. H. Syed, M. E. Dickinson, I. V. Larina, and K. V. Larin, “Speckle variance OCT imaging of the vasculature in live mammalian embryos,” Laser Phys. Lett. 8(3), 247–252 (2011).
[Crossref]

I. V. Larina, K. Furushima, M. E. Dickinson, R. R. Behringer, and K. V. Larin, “Live imaging of rat embryos with Doppler swept-source optical coherence tomography,” J. Biomed. Opt. 14(5), 050506 (2009).
[Crossref] [PubMed]

S. Bhat, I. V. Larina, K. V. Larin, M. E. Dickinson, and M. Liebling, “Multiple-cardiac-cycle noise reduction in dynamic optical coherence tomography of the embryonic heart and vasculature,” Opt. Lett. 34(23), 3704–3706 (2009).
[Crossref] [PubMed]

I. V. Larina, E. F. Carbajal, V. V. Tuchin, M. E. Dickinson, and K. V. Larin, “Enhanced OCT imaging of embryonic tissue with optical clearing,” Laser Phys. Lett. 5(6), 476–479 (2008).
[Crossref]

I. V. Larina, N. Sudheendran, M. Ghosn, J. Jiang, A. Cable, K. V. Larin, and M. E. Dickinson, “Live imaging of blood flow in mammalian embryos using Doppler swept-source optical coherence tomography,” J. Biomed. Opt. 13(6), 060506 (2008).
[Crossref] [PubMed]

Larina, I. V.

M. D. Garcia, A. L. Lopez, K. V. Larin, and I. V. Larina, “Imaging of cardiovascular development in Mammalian embryos using optical coherence tomography,” Methods Mol. Biol. 1214, 151–161 (2015).
[Crossref] [PubMed]

P. M. Kulkarni, N. Rey-Villamizar, A. Merouane, N. Sudheendran, S. Wang, M. Garcia, I. V. Larina, B. Roysam, and K. V. Larin, “Algorithms for improved 3-D reconstruction of live mammalian embryo vasculature from optical coherence tomography data,” Quant. Imaging Med. Surg. 5(1), 125–135 (2015).
[PubMed]

A. L. Lopez, S. Wang, K. V. Larin, P. A. Overbeek, and I. V. Larina, “Live four-dimensional optical coherence tomography reveals embryonic cardiac phenotype in mouse mutant,” J. Biomed. Opt. 20(9), 090501 (2015).
[Crossref] [PubMed]

S. Bhat, I. V. Larina, K. V. Larin, M. E. Dickinson, and M. Liebling, “4D reconstruction of the beating embryonic heart from two orthogonal sets of parallel optical coherence tomography slice-sequences,” IEEE Trans. Med. Imaging 32(3), 578–588 (2013).
[Crossref] [PubMed]

S. H. Syed, K. V. Larin, M. E. Dickinson, and I. V. Larina, “Optical coherence tomography for high-resolution imaging of mouse development in utero,” J. Biomed. Opt. 16(4), 046004 (2011).
[Crossref] [PubMed]

N. Sudheendran, S. H. Syed, M. E. Dickinson, I. V. Larina, and K. V. Larin, “Speckle variance OCT imaging of the vasculature in live mammalian embryos,” Laser Phys. Lett. 8(3), 247–252 (2011).
[Crossref]

J. J. Armstrong, I. V. Larina, M. E. Dickinson, W. E. Zimmer, and K. K. Hirschi, “Characterization of bacterial artificial chromosome transgenic mice expressing mCherry fluorescent protein substituted for the murine smooth muscle alpha-actin gene,” Genesis 48(7), 457–463 (2010).
[Crossref] [PubMed]

I. V. Larina, W. Shen, O. G. Kelly, A.-K. Hadjantonakis, M. H. Baron, and M. E. Dickinson, “A Membrane Associated mCherry Fluorescent Reporter line for Studying Vascular Remodeling and Cardiac Function During Murine Embryonic Development,” Anat. Rec. (Hoboken) 292(3), 333–341 (2009).
[Crossref] [PubMed]

I. V. Larina, K. Furushima, M. E. Dickinson, R. R. Behringer, and K. V. Larin, “Live imaging of rat embryos with Doppler swept-source optical coherence tomography,” J. Biomed. Opt. 14(5), 050506 (2009).
[Crossref] [PubMed]

S. Bhat, I. V. Larina, K. V. Larin, M. E. Dickinson, and M. Liebling, “Multiple-cardiac-cycle noise reduction in dynamic optical coherence tomography of the embryonic heart and vasculature,” Opt. Lett. 34(23), 3704–3706 (2009).
[Crossref] [PubMed]

I. V. Larina, N. Sudheendran, M. Ghosn, J. Jiang, A. Cable, K. V. Larin, and M. E. Dickinson, “Live imaging of blood flow in mammalian embryos using Doppler swept-source optical coherence tomography,” J. Biomed. Opt. 13(6), 060506 (2008).
[Crossref] [PubMed]

I. V. Larina, E. F. Carbajal, V. V. Tuchin, M. E. Dickinson, and K. V. Larin, “Enhanced OCT imaging of embryonic tissue with optical clearing,” Laser Phys. Lett. 5(6), 476–479 (2008).
[Crossref]

Lee, W. C.

E. Nam, W. C. Lee, and S. Takeuchi, “Formation of Highly Aligned Collagen Nanofibers by Continuous Cyclic Stretch of a Collagen Hydrogel Sheet,” Macromol. Biosci. 16(7), 995–1000 (2016).
[Crossref] [PubMed]

Lewis, T. T.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
[Crossref] [PubMed]

Li, X.

J. Liu, W. Yu, Y. Liu, S. Chen, Y. Huang, X. Li, C. Liu, Y. Zhang, Z. Li, J. Du, C. Tang, J. Du, and H. Jin, “Mechanical stretching stimulates collagen synthesis via down-regulating SO2/AAT1 pathway,” Sci. Rep. 6(1), 21112 (2016).
[Crossref] [PubMed]

Li, Z.

J. Liu, W. Yu, Y. Liu, S. Chen, Y. Huang, X. Li, C. Liu, Y. Zhang, Z. Li, J. Du, C. Tang, J. Du, and H. Jin, “Mechanical stretching stimulates collagen synthesis via down-regulating SO2/AAT1 pathway,” Sci. Rep. 6(1), 21112 (2016).
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E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
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E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
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A. Acharya, S. T. Baek, G. Huang, B. Eskiocak, S. Goetsch, C. Y. Sung, S. Banfi, M. F. Sauer, G. S. Olsen, J. S. Duffield, E. N. Olson, and M. D. Tallquist, “The bHLH transcription factor Tcf21 is required for lineage-specific EMT of cardiac fibroblast progenitors,” Development 139(12), 2139–2149 (2012).
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Tranquillo, R. T.

N. K. Weidenhamer and R. T. Tranquillo, “Influence of cyclic mechanical stretch and tissue constraints on cellular and collagen alignment in fibroblast-derived cell sheets,” Tissue Eng. Part C Methods 19(5), 386–395 (2013).
[Crossref] [PubMed]

Tsang, W.

L. K. Hornberger, S. Singhroy, T. Cavalle-Garrido, W. Tsang, F. Keeley, and M. Rabinovitch, “Synthesis of Extracellular Matrix and Adhesion Through β(1) Integrins are Critical for Fetal Ventricular Myocyte Proliferation,” Circ. Res. 87(6), 508–515 (2000).
[Crossref] [PubMed]

Tsao, C. W.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
[Crossref] [PubMed]

Tuchin, V.

A. Sdobnov, M. E. Darvin, J. Lademann, and V. Tuchin, “A comparative study of ex vivo skin optical clearing using two-photon microscopy,” J. Biophotonics 10(9), 1115–1123 (2017).
[Crossref] [PubMed]

Tuchin, V. V.

S. Masoumi, M. A. Ansari, E. Mohajerani, E. A. Genina, and V. V. Tuchin, “Combination of analytical and experimental optical clearing of rodent specimen for detecting beta-carotene: phantom study,” J. Biomed. Opt. 23(9), 1–7 (2018).
[Crossref] [PubMed]

L. M. Oliveira, M. I. Carvalho, E. M. Nogueira, and V. V. Tuchin, “Skeletal muscle dispersion (400-1000 nm) and kinetics at optical clearing,” J. Biophotonics 11(1), e201700094 (2018).
[Crossref] [PubMed]

D. Zhu, K. V. Larin, Q. Luo, and V. V. Tuchin, “Recent progress in tissue optical clearing,” Laser Photonics Rev. 7(5), 732–757 (2013).
[Crossref] [PubMed]

I. V. Larina, E. F. Carbajal, V. V. Tuchin, M. E. Dickinson, and K. V. Larin, “Enhanced OCT imaging of embryonic tissue with optical clearing,” Laser Phys. Lett. 5(6), 476–479 (2008).
[Crossref]

A. Y. Sdobnov, M. E. Darvin, J. Schleusener, J. Lademann, and V. V. Tuchin, “Hydrogen bound water profiles in the skin influenced by optical clearing molecular agents-Quantitative analysis using confocal Raman microscopy,” J. Biophotonics, 201800283 (2018).

Turakhia, M. P.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
[Crossref] [PubMed]

VanWagner, L. B.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
[Crossref] [PubMed]

Virani, S. S.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
[Crossref] [PubMed]

Wang, S.

A. L. Lopez, S. Wang, K. V. Larin, P. A. Overbeek, and I. V. Larina, “Live four-dimensional optical coherence tomography reveals embryonic cardiac phenotype in mouse mutant,” J. Biomed. Opt. 20(9), 090501 (2015).
[Crossref] [PubMed]

P. M. Kulkarni, N. Rey-Villamizar, A. Merouane, N. Sudheendran, S. Wang, M. Garcia, I. V. Larina, B. Roysam, and K. V. Larin, “Algorithms for improved 3-D reconstruction of live mammalian embryo vasculature from optical coherence tomography data,” Quant. Imaging Med. Surg. 5(1), 125–135 (2015).
[PubMed]

Watanabe, M.

M. W. Jenkins, A. R. Duke, S. Gu, H. J. Chiel, H. Fujioka, M. Watanabe, E. D. Jansen, and A. M. Rollins, “Optical pacing of the embryonic heart,” Nat. Photonics 4(9), 623–626 (2010).
[Crossref] [PubMed]

M. W. Jenkins, O. Q. Chughtai, A. N. Basavanhally, M. Watanabe, and A. M. Rollins, “In vivo gated 4D imaging of the embryonic heart using optical coherence tomography,” J. Biomed. Opt. 12(3), 030505 (2007).
[Crossref] [PubMed]

Waters, C. W.

E. A. Jones, D. Crotty, P. M. Kulesa, C. W. Waters, M. H. Baron, S. E. Fraser, and M. E. Dickinson, “Dynamic in vivo imaging of postimplantation mammalian embryos using whole embryo culture,” Genesis 34(4), 228–235 (2002).
[Crossref] [PubMed]

Weidenhamer, N. K.

N. K. Weidenhamer and R. T. Tranquillo, “Influence of cyclic mechanical stretch and tissue constraints on cellular and collagen alignment in fibroblast-derived cell sheets,” Tissue Eng. Part C Methods 19(5), 386–395 (2013).
[Crossref] [PubMed]

Wiley, J. A.

J. R. Prigge, J. A. Wiley, E. A. Talago, E. M. Young, L. L. Johns, J. A. Kundert, K. M. Sonsteng, W. P. Halford, M. R. Capecchi, and E. E. Schmidt, “Nuclear double-fluorescent reporter for in vivo and ex vivo analyses of biological transitions in mouse nuclei,” Mamm. Genome 24, 389–399 (2013).

Wilkins, J. T.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
[Crossref] [PubMed]

Wolf, A. E.

A. S. Piotrowski-Daspit, B. A. Nerger, A. E. Wolf, S. Sundaresan, and C. M. Nelson, “Dynamics of Tissue-Induced Alignment of Fibrous Extracellular Matrix,” Biophys. J. 113(3), 702–713 (2017).
[Crossref] [PubMed]

Wong, S. S.

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
[Crossref] [PubMed]

Yalcin, H. C.

S. E. Lindsey, J. T. Butcher, and H. C. Yalcin, “Mechanical regulation of cardiac development,” Front. Physiol. 5, 318 (2014).
[Crossref] [PubMed]

Yost, M. J.

S. V. Biechler, L. Junor, A. N. Evans, J. F. Eberth, R. L. Price, J. D. Potts, M. J. Yost, and R. L. Goodwin, “The impact of flow-induced forces on the morphogenesis of the outflow tract,” Front. Physiol. 5, 225 (2014).
[Crossref] [PubMed]

Young, E. M.

J. R. Prigge, J. A. Wiley, E. A. Talago, E. M. Young, L. L. Johns, J. A. Kundert, K. M. Sonsteng, W. P. Halford, M. R. Capecchi, and E. E. Schmidt, “Nuclear double-fluorescent reporter for in vivo and ex vivo analyses of biological transitions in mouse nuclei,” Mamm. Genome 24, 389–399 (2013).

Yu, W.

J. Liu, W. Yu, Y. Liu, S. Chen, Y. Huang, X. Li, C. Liu, Y. Zhang, Z. Li, J. Du, C. Tang, J. Du, and H. Jin, “Mechanical stretching stimulates collagen synthesis via down-regulating SO2/AAT1 pathway,” Sci. Rep. 6(1), 21112 (2016).
[Crossref] [PubMed]

Zhang, Y.

J. Liu, W. Yu, Y. Liu, S. Chen, Y. Huang, X. Li, C. Liu, Y. Zhang, Z. Li, J. Du, C. Tang, J. Du, and H. Jin, “Mechanical stretching stimulates collagen synthesis via down-regulating SO2/AAT1 pathway,” Sci. Rep. 6(1), 21112 (2016).
[Crossref] [PubMed]

Zhu, D.

D. Zhu, K. V. Larin, Q. Luo, and V. V. Tuchin, “Recent progress in tissue optical clearing,” Laser Photonics Rev. 7(5), 732–757 (2013).
[Crossref] [PubMed]

Zimmer, W. E.

J. J. Armstrong, I. V. Larina, M. E. Dickinson, W. E. Zimmer, and K. K. Hirschi, “Characterization of bacterial artificial chromosome transgenic mice expressing mCherry fluorescent protein substituted for the murine smooth muscle alpha-actin gene,” Genesis 48(7), 457–463 (2010).
[Crossref] [PubMed]

Anat. Embryol. (Berl.) (1)

M. C. Rémond, J. A. Fee, E. L. Elson, and L. A. Taber, “Myosin-based contraction is not necessary for cardiac c-looping in the chick embryo,” Anat. Embryol. (Berl.) 211(5), 443–454 (2006).
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Anat. Rec. (Hoboken) (1)

I. V. Larina, W. Shen, O. G. Kelly, A.-K. Hadjantonakis, M. H. Baron, and M. E. Dickinson, “A Membrane Associated mCherry Fluorescent Reporter line for Studying Vascular Remodeling and Cardiac Function During Murine Embryonic Development,” Anat. Rec. (Hoboken) 292(3), 333–341 (2009).
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Biomed. Opt. Express (1)

Biophys. J. (2)

A. S. Piotrowski-Daspit, B. A. Nerger, A. E. Wolf, S. Sundaresan, and C. M. Nelson, “Dynamics of Tissue-Induced Alignment of Fibrous Extracellular Matrix,” Biophys. J. 113(3), 702–713 (2017).
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S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the Myosin-Based Source for Second-Harmonic Generation from Muscle Sarcomeres,” Biophys. J. 90(2), 693–703 (2006).
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V. Gupta and K. J. Grande-Allen, “Effects of static and cyclic loading in regulating extracellular matrix synthesis by cardiovascular cells,” Cardiovasc. Res. 72(3), 375–383 (2006).
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Circ. Res. (4)

L. K. Hornberger, S. Singhroy, T. Cavalle-Garrido, W. Tsang, F. Keeley, and M. Rabinovitch, “Synthesis of Extracellular Matrix and Adhesion Through β(1) Integrins are Critical for Fetal Ventricular Myocyte Proliferation,” Circ. Res. 87(6), 508–515 (2000).
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W. Carver, M. L. Nagpal, M. Nachtigal, T. K. Borg, and L. Terracio, “Collagen expression in mechanically stimulated cardiac fibroblasts,” Circ. Res. 69(1), 116–122 (1991).
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D. E. Ingber, “Mechanical signaling and the Cellular Response to Extracellular Matrix in Angiogenesis and Cardiovascular Physiology,” Circ. Res. 91(10), 877–887 (2002).
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M. Rienks, A.-P. Papageorgiou, N. G. Frangogiannis, and S. Heymans, “Myocardial Extracellular Matrix,” Circ. Res. 114(5), 872–888 (2014).
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Circulation (1)

E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong, S. S. Virani, and American Heart Association Council on Epidemiology and Prevention Statistics Committee and Stroke Statistics Subcommittee, “Heart Disease and Stroke Statistics-2019 Update: A Report From the American Heart Association,” Circulation 139(10), 56–528 (2019).
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Curr. Opin. Genet. Dev. (1)

W. Supatto, D. T. T. F. Debarre, E. D. D F. Beaurepaire, and E. Beaurepaire, “Advances in multiphoton microscopy for imaging embryos,” Curr. Opin. Genet. Dev. 21(5) 538–548 (2011).

Development (3)

C. Huang, F. Sheikh, M. Hollander, C. Cai, D. Becker, P.-H. Chu, S. Evans, and J. Chen, “Embryonic atrial function is essential for mouse embryogenesis, cardiac morphogenesis and angiogenesis,” Development 130(24), 6111–6119 (2003).
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T. Mammoto and D. E. Ingber, “Mechanical control of tissue and organ development,” Development 137(9), 1407–1420 (2010).
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A. Acharya, S. T. Baek, G. Huang, B. Eskiocak, S. Goetsch, C. Y. Sung, S. Banfi, M. F. Sauer, G. S. Olsen, J. S. Duffield, E. N. Olson, and M. D. Tallquist, “The bHLH transcription factor Tcf21 is required for lineage-specific EMT of cardiac fibroblast progenitors,” Development 139(12), 2139–2149 (2012).
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Front. Physiol. (6)

K. Imanaka-Yoshida and H. Aoki, “Tenascin-C and mechanotransduction in the development and diseases of cardiovascular system,” Front. Physiol. 5, 283 (2014).
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S. V. Biechler, L. Junor, A. N. Evans, J. F. Eberth, R. L. Price, J. D. Potts, M. J. Yost, and R. L. Goodwin, “The impact of flow-induced forces on the morphogenesis of the outflow tract,” Front. Physiol. 5, 225 (2014).
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M. Midgett, C. S. López, L. David, A. Maloyan, and S. Rugonyi, “Increased Hemodynamic Load in Early Embryonic Stages Alters Myofibril and Mitochondrial Organization in the Myocardium,” Front. Physiol. 8, 631 (2017).
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W. J. Kowalski, K. Pekkan, J. P. Tinney, and B. B. Keller, “Investigating developmental cardiovascular biomechanics and the origins of congenital heart defects,” Front. Physiol. 5, 408 (2014).
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S. E. Lindsey, J. T. Butcher, and H. C. Yalcin, “Mechanical regulation of cardiac development,” Front. Physiol. 5, 318 (2014).
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M. Midgett and S. Rugonyi, “Congenital heart malformations induced by hemodynamic altering surgical interventions,” Front. Physiol. 5, 287 (2014).
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Genesis (2)

E. A. Jones, D. Crotty, P. M. Kulesa, C. W. Waters, M. H. Baron, S. E. Fraser, and M. E. Dickinson, “Dynamic in vivo imaging of postimplantation mammalian embryos using whole embryo culture,” Genesis 34(4), 228–235 (2002).
[Crossref] [PubMed]

J. J. Armstrong, I. V. Larina, M. E. Dickinson, W. E. Zimmer, and K. K. Hirschi, “Characterization of bacterial artificial chromosome transgenic mice expressing mCherry fluorescent protein substituted for the murine smooth muscle alpha-actin gene,” Genesis 48(7), 457–463 (2010).
[Crossref] [PubMed]

IEEE Trans. Med. Imaging (1)

S. Bhat, I. V. Larina, K. V. Larin, M. E. Dickinson, and M. Liebling, “4D reconstruction of the beating embryonic heart from two orthogonal sets of parallel optical coherence tomography slice-sequences,” IEEE Trans. Med. Imaging 32(3), 578–588 (2013).
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Int. J. Dev. Biol. (1)

E. G. Stanley, C. Biben, A. Elefanty, L. Barnett, F. Koentgen, L. Robb, and R. P. Harvey, “Efficient Cre-mediated deletion in cardiac progenitor cells conferred by a 3’UTR-ires-Cre allele of the homeobox gene Nkx2-5,” Int. J. Dev. Biol. 46, 431–443 (2004).

Int. J. Mol. Sci. (1)

L. Mostaço-Guidolin, N. L. Rosin, and T.-L. Hackett, “Imaging Collagen in Scar Tissue: Developments in Second Harmonic Generation Microscopy for Biomedical Applications,” Int. J. Mol. Sci. 18(8), 1772 (2017).
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J. Biomed. Opt. (7)

A. L. Lopez, S. Wang, K. V. Larin, P. A. Overbeek, and I. V. Larina, “Live four-dimensional optical coherence tomography reveals embryonic cardiac phenotype in mouse mutant,” J. Biomed. Opt. 20(9), 090501 (2015).
[Crossref] [PubMed]

I. V. Larina, N. Sudheendran, M. Ghosn, J. Jiang, A. Cable, K. V. Larin, and M. E. Dickinson, “Live imaging of blood flow in mammalian embryos using Doppler swept-source optical coherence tomography,” J. Biomed. Opt. 13(6), 060506 (2008).
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I. V. Larina, K. Furushima, M. E. Dickinson, R. R. Behringer, and K. V. Larin, “Live imaging of rat embryos with Doppler swept-source optical coherence tomography,” J. Biomed. Opt. 14(5), 050506 (2009).
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M. W. Jenkins, O. Q. Chughtai, A. N. Basavanhally, M. Watanabe, and A. M. Rollins, “In vivo gated 4D imaging of the embryonic heart using optical coherence tomography,” J. Biomed. Opt. 12(3), 030505 (2007).
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S. H. Syed, K. V. Larin, M. E. Dickinson, and I. V. Larina, “Optical coherence tomography for high-resolution imaging of mouse development in utero,” J. Biomed. Opt. 16(4), 046004 (2011).
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M. Liebling, A. S. Forouhar, M. Gharib, S. E. Fraser, and M. E. Dickinson, “Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences,” J. Biomed. Opt. 10(5), 054001 (2005).
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S. Masoumi, M. A. Ansari, E. Mohajerani, E. A. Genina, and V. V. Tuchin, “Combination of analytical and experimental optical clearing of rodent specimen for detecting beta-carotene: phantom study,” J. Biomed. Opt. 23(9), 1–7 (2018).
[Crossref] [PubMed]

J. Biophotonics (2)

L. M. Oliveira, M. I. Carvalho, E. M. Nogueira, and V. V. Tuchin, “Skeletal muscle dispersion (400-1000 nm) and kinetics at optical clearing,” J. Biophotonics 11(1), e201700094 (2018).
[Crossref] [PubMed]

A. Sdobnov, M. E. Darvin, J. Lademann, and V. Tuchin, “A comparative study of ex vivo skin optical clearing using two-photon microscopy,” J. Biophotonics 10(9), 1115–1123 (2017).
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J. Struct. Biol. (1)

G. Cox, E. Kable, A. Jones, I. Fraser, F. Manconi, and M. D. Gorrell, “3-Dimensional imaging of collagen using second harmonic generation,” J. Struct. Biol. 141(1), 53–62 (2003).
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Laser Photonics Rev. (1)

D. Zhu, K. V. Larin, Q. Luo, and V. V. Tuchin, “Recent progress in tissue optical clearing,” Laser Photonics Rev. 7(5), 732–757 (2013).
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Laser Phys. Lett. (2)

I. V. Larina, E. F. Carbajal, V. V. Tuchin, M. E. Dickinson, and K. V. Larin, “Enhanced OCT imaging of embryonic tissue with optical clearing,” Laser Phys. Lett. 5(6), 476–479 (2008).
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N. Sudheendran, S. H. Syed, M. E. Dickinson, I. V. Larina, and K. V. Larin, “Speckle variance OCT imaging of the vasculature in live mammalian embryos,” Laser Phys. Lett. 8(3), 247–252 (2011).
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Macromol. Biosci. (1)

E. Nam, W. C. Lee, and S. Takeuchi, “Formation of Highly Aligned Collagen Nanofibers by Continuous Cyclic Stretch of a Collagen Hydrogel Sheet,” Macromol. Biosci. 16(7), 995–1000 (2016).
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Mamm. Genome (1)

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Supplementary Material (4)

NameDescription
» Visualization 1       The Visualization 1 is referenced in Figure 2 caption and the results section of the manuscript.
» Visualization 2       The Visualization 2 is referenced in Figure 3 caption and the results section of the manuscript.
» Visualization 3       The Visualization 3 is referenced in Figure 4 caption and the results section of the manuscript.
» Visualization 4       The Visualization 4 is referenced in Figure 5 caption and the results section of the manuscript.

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Figures (5)

Fig. 1
Fig. 1 Validation of SHG nature of cardiac fibrillar structures. Images of a single plane within an E8.5 heart ventricle wall at illumination wavelengths between 770 and 840 nm with 10 nm increment acquired through a narrowband emission filter 405 ± 10 nm. The illumination wavelength is labeled in the top left corner of each image. The detection and visualization were performed using the same settings for all images.
Fig. 2
Fig. 2 SHG positive cardiac fibers develop quickly after beginning of heart contraction. (A-C) Brightfield images of mouse embryos focused on cardiac region at 3-4, 5-6, and 6-7 somite stages, respectively. (D-F) Corresponding 3-D SHG images of the same embryonic hearts as in (A-C). The image acquisition, rendering, and visualization were performed at the same settings. Visualization 1 shows volumetric details of SHG images in panels (D-F).
Fig. 3
Fig. 3 SHG positive cardiac fibers show regional difference. (A) 3-D SHG imaging of the embryonic heart at E8.5 10-somite stage showing a ventricle and an outflow tract; the volumetric view is presented in Visualization 2. (B-C) Corresponding cross-sectional views through the heart at the planes labeled in (A). (D-F) Magnified view of the corresponding areas labeled in panel (A). (D) Magnified view of the outflow tract region labeled in panel (A). (E) Magnified view of the ventricle region labeled in panel (A). (F) The same region of the ventricle as shown in panel (E), but with a clipping plane at 15 um below the heart surface.
Fig. 4
Fig. 4 SHG microscopy in a heart of a mouse mutant with reduced contractility. (A-D) Images of the control embryo. (E-H) Images of the Mlc2a KO embryo at the same developmental stage. (A and E) Brightfield microscopic image of the extracted heats and (B and F) of the whole control and Mlc2a KO embryos, respectively. (C and G) Corresponding 3-D SHG microscopy of the atria in the same control and Mlc2a KO embryos, respectively. Visualization 3 shows details of the fibrillar network 3-D organization within the atria. (D and H) quantitative visualization of SHF positive fibrillar networks in the control and Mlc2a KO embryos, respectively. The histograms show corresponding count distributions of segmented fiber lengths at the same scale. The image acquisition, rendering, visualization, and analysis for the control and the mutant embryos were performed at the same settings.
Fig. 5
Fig. 5 Simultaneous detection of SHG and two-photon excitation imaging of EGFP in the embryonic heart. 3-D reconstruction of the cardiac wall at E9.5 (A) SHG microscopy, (B) two-photon excitation microscopy of EGFP, and (C) merged images. The volumetric view of the same area is presented in Visualization 4.

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