Abstract

We present an imaging and image reconstruction pipeline that captures the dynamic three-dimensional beating motion of the live embryonic zebrafish heart at subcellular resolution. Live, intact zebrafish embryos were imaged using 2-photon light sheet microscopy, which offers deep and fast imaging at 70 frames per second, and the individual optical sections were assembled into a full 4D reconstruction of the beating heart using an optimized retrospective image registration algorithm. This imaging and reconstruction platform permitted us to visualize protein expression patterns at endogenous concentrations in zebrafish gene trap lines.

© 2015 Optical Society of America

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  1. J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevedo-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature 421(6919), 172–177 (2003).
    [Crossref] [PubMed]
  2. D. Y. Stainier, “Zebrafish genetics and vertebrate heart formation,” Nat. Rev. Genet. 2(1), 39–48 (2001).
    [Crossref] [PubMed]
  3. A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H. J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312(5774), 751–753 (2006).
    [Crossref] [PubMed]
  4. M. Markl, F. P. Chan, M. T. Alley, K. L. Wedding, M. T. Draney, C. J. Elkins, D. W. Parker, R. Wicker, C. A. Taylor, R. J. Herfkens, and N. J. Pelc, “Time-resolved three-dimensional phase-contrast MRI,” J. Magn. Reson. Imaging 17(4), 499–506 (2003).
    [Crossref] [PubMed]
  5. R. Jerecic, M. Bock, S. Nielles-Vallespin, C. Wacker, W. Bauer, and L. R. Schad, “ECG-gated 23Na-MRI of the human heart using a 3D-radial projection technique with ultra-short echo times,” MAGMA 16(6), 297–302 (2004).
    [Crossref] [PubMed]
  6. J. M. Taylor, C. D. Saunter, G. D. Love, J. M. Girkin, D. J. Henderson, and B. Chaudhry, “Real-time optical gating for three-dimensional beating heart imaging,” J. Biomed. Opt. 16(11), 116021 (2011).
    [Crossref] [PubMed]
  7. J. M. Taylor, “Optically gated beating-heart imaging,” Front Physiol 5, 481 (2014).
    [Crossref] [PubMed]
  8. 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]
  9. J. Ohn, H. J. Tsai, and M. Liebling, “Joint dynamic imaging of morphogenesis and function in the developing heart,” Organogenesis 5(4), 248–255 (2009).
    [Crossref] [PubMed]
  10. T. V. Truong, W. Supatto, D. S. Koos, J. M. Choi, and S. E. Fraser, “Deep and fast live imaging with two-photon scanned light-sheet microscopy,” Nat. Methods 8(9), 757–760 (2011).
    [Crossref] [PubMed]
  11. A. Trinh, T. Hochgreb, M. Graham, D. Wu, F. Ruf-Zamojski, C. S. Jayasena, A. Saxena, R. Hawk, A. Gonzalez-Serricchio, A. Dixson, E. Chow, C. Gonzales, H. Y. Leung, I. Solomon, M. Bronner-Fraser, S. G. Megason, and S. E. Fraser, “A versatile gene trap to visualize and interrogate the function of the vertebrate proteome,” Genes Dev. 25(21), 2306–2320 (2011).
    [Crossref] [PubMed]
  12. A. D. Edelstein, M. A. Tsuchida, N. Amodaj, H. Pinkard, R. D. Vale, and N. Stuurman, “Advanced methods of microscope control using μManager software,” J. Biol. Methods 1(2), 10 (2014).
    [Crossref] [PubMed]
  13. W. C. Skarnes, H. von Melchner, W. Wurst, G. Hicks, A. S. Nord, T. Cox, S. G. Young, P. Ruiz, P. Soriano, M. Tessier-Lavigne, B. R. Conklin, W. L. Stanford, J. Rossant, and International Gene Trap Consortium, “A public gene trap resource for mouse functional genomics,” Nat. Genet. 36(6), 543–544 (2004).
    [Crossref] [PubMed]
  14. W. L. Stanford, J. B. Cohn, and S. P. Cordes, “Gene-trap mutagenesis: past, present and beyond,” Nat. Rev. Genet. 2(10), 756–768 (2001).
    [Crossref] [PubMed]
  15. A. Lisette, L. Maddison, and C. Wenbiao, “Conditional gene-trap mutagenesis in Zebrafish methods,” Mol. Biol. 1101, 393–411 (2014).
  16. M. Westerfield, “The zebrafish book,” University of Oregon Press, Eugene, OR (1994)
  17. M. Mickoleit, B. Schmid, M. Weber, F. O. Fahrbach, S. Hombach, S. Reischauer, and J. Huisken, “High-resolution reconstruction of the beating zebrafish heart,” Nat. Methods 11(9), 919–922 (2014).
    [Crossref] [PubMed]
  18. T. A. Planchon, L. Gao, D. E. Milkie, M. W. Davidson, J. A. Galbraith, C. G. Galbraith, and E. Betzig, “Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination,” Nat. Methods 8(5), 417–423 (2011).
    [Crossref] [PubMed]
  19. O. E. Olarte, J. Licea-Rodriguez, J. A. Palero, E. J. Gualda, D. Artigas, J. Mayer, J. Swoger, J. Sharpe, I. Rocha-Mendoza, R. Rangel-Rojo, and P. Loza-Alvarez, “Image formation by linear and nonlinear digital scanned light-sheet fluorescence microscopy with Gaussian and Bessel beam profiles,” Biomed. Opt. Express 3(7), 1492–1505 (2012).
    [Crossref] [PubMed]
  20. F. O. Fahrbach, V. Gurchenkov, K. Alessandri, P. Nassoy, and A. Rohrbach, “Light-sheet microscopy in thick media using scanned Bessel beams and two-photon fluorescence excitation,” Opt. Express 21(11), 13824–13839 (2013).
    [Crossref] [PubMed]
  21. M. Liebling, A. S. Forouhar, R. Wolleschensky, B. Zimmermann, R. Ankerhold, S. E. Fraser, M. Gharib, and M. E. Dickinson, “Rapid three-dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development,” Dev. Dyn. 235(11), 2940–2948 (2006).
    [Crossref] [PubMed]
  22. M. Liebling, J. Vermot, A. S. Forouhar, M. Gharib, M. E. Dickinson, and S. E. Fraser, “Nonuniform temporal alignment of slice sequences for four-dimensional imaging of cyclically deforming embryonic structures,” Proceedings of the 3rd IEEE International Symposium on Biomedical Imaging: Macro to Nano (ISBI'06), Arlington, VA, USA, April 6–9, 1156–1159 (2006)
    [Crossref]
  23. 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]
  24. I. V. Larina, K. V. Larin, M. E. Dickinson, and M. Liebling, “Sequential turning acquisition and reconstruction (STAR) method for four-dimensional imaging of cyclically moving structures,” Biomed. Opt. Express 3(3), 650–660 (2012).
    [Crossref] [PubMed]
  25. D. W. Staudt, J. Liu, K. S. Thorn, N. Stuurman, M. Liebling, and D. Y. R. Stainier, “High-resolution imaging of cardiomyocyte behavior reveals two distinct steps in ventricular trabeculation,” Development 141(3), 585–593 (2014).
    [Crossref] [PubMed]
  26. A. D. Aguirre, C. Vinegoni, M. Sebas, and R. Weissleder, “Intravital imaging of cardiac function at the single-cell level,” Proc. Natl. Acad. Sci. U.S.A. 111(31), 11257–11262 (2014).
    [Crossref] [PubMed]
  27. P. Mahou, J. Vermot, E. Beaurepaire, and W. Supatto, “Multicolor two-photon light-sheet microscopy,” Nat. Methods 11(6), 600–601 (2014).
    [Crossref] [PubMed]

2014 (7)

J. M. Taylor, “Optically gated beating-heart imaging,” Front Physiol 5, 481 (2014).
[Crossref] [PubMed]

A. D. Edelstein, M. A. Tsuchida, N. Amodaj, H. Pinkard, R. D. Vale, and N. Stuurman, “Advanced methods of microscope control using μManager software,” J. Biol. Methods 1(2), 10 (2014).
[Crossref] [PubMed]

A. Lisette, L. Maddison, and C. Wenbiao, “Conditional gene-trap mutagenesis in Zebrafish methods,” Mol. Biol. 1101, 393–411 (2014).

M. Mickoleit, B. Schmid, M. Weber, F. O. Fahrbach, S. Hombach, S. Reischauer, and J. Huisken, “High-resolution reconstruction of the beating zebrafish heart,” Nat. Methods 11(9), 919–922 (2014).
[Crossref] [PubMed]

D. W. Staudt, J. Liu, K. S. Thorn, N. Stuurman, M. Liebling, and D. Y. R. Stainier, “High-resolution imaging of cardiomyocyte behavior reveals two distinct steps in ventricular trabeculation,” Development 141(3), 585–593 (2014).
[Crossref] [PubMed]

A. D. Aguirre, C. Vinegoni, M. Sebas, and R. Weissleder, “Intravital imaging of cardiac function at the single-cell level,” Proc. Natl. Acad. Sci. U.S.A. 111(31), 11257–11262 (2014).
[Crossref] [PubMed]

P. Mahou, J. Vermot, E. Beaurepaire, and W. Supatto, “Multicolor two-photon light-sheet microscopy,” Nat. Methods 11(6), 600–601 (2014).
[Crossref] [PubMed]

2013 (2)

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]

F. O. Fahrbach, V. Gurchenkov, K. Alessandri, P. Nassoy, and A. Rohrbach, “Light-sheet microscopy in thick media using scanned Bessel beams and two-photon fluorescence excitation,” Opt. Express 21(11), 13824–13839 (2013).
[Crossref] [PubMed]

2012 (2)

2011 (4)

T. A. Planchon, L. Gao, D. E. Milkie, M. W. Davidson, J. A. Galbraith, C. G. Galbraith, and E. Betzig, “Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination,” Nat. Methods 8(5), 417–423 (2011).
[Crossref] [PubMed]

T. V. Truong, W. Supatto, D. S. Koos, J. M. Choi, and S. E. Fraser, “Deep and fast live imaging with two-photon scanned light-sheet microscopy,” Nat. Methods 8(9), 757–760 (2011).
[Crossref] [PubMed]

A. Trinh, T. Hochgreb, M. Graham, D. Wu, F. Ruf-Zamojski, C. S. Jayasena, A. Saxena, R. Hawk, A. Gonzalez-Serricchio, A. Dixson, E. Chow, C. Gonzales, H. Y. Leung, I. Solomon, M. Bronner-Fraser, S. G. Megason, and S. E. Fraser, “A versatile gene trap to visualize and interrogate the function of the vertebrate proteome,” Genes Dev. 25(21), 2306–2320 (2011).
[Crossref] [PubMed]

J. M. Taylor, C. D. Saunter, G. D. Love, J. M. Girkin, D. J. Henderson, and B. Chaudhry, “Real-time optical gating for three-dimensional beating heart imaging,” J. Biomed. Opt. 16(11), 116021 (2011).
[Crossref] [PubMed]

2009 (1)

J. Ohn, H. J. Tsai, and M. Liebling, “Joint dynamic imaging of morphogenesis and function in the developing heart,” Organogenesis 5(4), 248–255 (2009).
[Crossref] [PubMed]

2006 (2)

A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H. J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312(5774), 751–753 (2006).
[Crossref] [PubMed]

M. Liebling, A. S. Forouhar, R. Wolleschensky, B. Zimmermann, R. Ankerhold, S. E. Fraser, M. Gharib, and M. E. Dickinson, “Rapid three-dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development,” Dev. Dyn. 235(11), 2940–2948 (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 (2)

R. Jerecic, M. Bock, S. Nielles-Vallespin, C. Wacker, W. Bauer, and L. R. Schad, “ECG-gated 23Na-MRI of the human heart using a 3D-radial projection technique with ultra-short echo times,” MAGMA 16(6), 297–302 (2004).
[Crossref] [PubMed]

W. C. Skarnes, H. von Melchner, W. Wurst, G. Hicks, A. S. Nord, T. Cox, S. G. Young, P. Ruiz, P. Soriano, M. Tessier-Lavigne, B. R. Conklin, W. L. Stanford, J. Rossant, and International Gene Trap Consortium, “A public gene trap resource for mouse functional genomics,” Nat. Genet. 36(6), 543–544 (2004).
[Crossref] [PubMed]

2003 (2)

M. Markl, F. P. Chan, M. T. Alley, K. L. Wedding, M. T. Draney, C. J. Elkins, D. W. Parker, R. Wicker, C. A. Taylor, R. J. Herfkens, and N. J. Pelc, “Time-resolved three-dimensional phase-contrast MRI,” J. Magn. Reson. Imaging 17(4), 499–506 (2003).
[Crossref] [PubMed]

J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevedo-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature 421(6919), 172–177 (2003).
[Crossref] [PubMed]

2001 (2)

D. Y. Stainier, “Zebrafish genetics and vertebrate heart formation,” Nat. Rev. Genet. 2(1), 39–48 (2001).
[Crossref] [PubMed]

W. L. Stanford, J. B. Cohn, and S. P. Cordes, “Gene-trap mutagenesis: past, present and beyond,” Nat. Rev. Genet. 2(10), 756–768 (2001).
[Crossref] [PubMed]

Acevedo-Bolton, G.

J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevedo-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature 421(6919), 172–177 (2003).
[Crossref] [PubMed]

Aguirre, A. D.

A. D. Aguirre, C. Vinegoni, M. Sebas, and R. Weissleder, “Intravital imaging of cardiac function at the single-cell level,” Proc. Natl. Acad. Sci. U.S.A. 111(31), 11257–11262 (2014).
[Crossref] [PubMed]

Alessandri, K.

Alley, M. T.

M. Markl, F. P. Chan, M. T. Alley, K. L. Wedding, M. T. Draney, C. J. Elkins, D. W. Parker, R. Wicker, C. A. Taylor, R. J. Herfkens, and N. J. Pelc, “Time-resolved three-dimensional phase-contrast MRI,” J. Magn. Reson. Imaging 17(4), 499–506 (2003).
[Crossref] [PubMed]

Amodaj, N.

A. D. Edelstein, M. A. Tsuchida, N. Amodaj, H. Pinkard, R. D. Vale, and N. Stuurman, “Advanced methods of microscope control using μManager software,” J. Biol. Methods 1(2), 10 (2014).
[Crossref] [PubMed]

Ankerhold, R.

M. Liebling, A. S. Forouhar, R. Wolleschensky, B. Zimmermann, R. Ankerhold, S. E. Fraser, M. Gharib, and M. E. Dickinson, “Rapid three-dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development,” Dev. Dyn. 235(11), 2940–2948 (2006).
[Crossref] [PubMed]

Artigas, D.

Bauer, W.

R. Jerecic, M. Bock, S. Nielles-Vallespin, C. Wacker, W. Bauer, and L. R. Schad, “ECG-gated 23Na-MRI of the human heart using a 3D-radial projection technique with ultra-short echo times,” MAGMA 16(6), 297–302 (2004).
[Crossref] [PubMed]

Beaurepaire, E.

P. Mahou, J. Vermot, E. Beaurepaire, and W. Supatto, “Multicolor two-photon light-sheet microscopy,” Nat. Methods 11(6), 600–601 (2014).
[Crossref] [PubMed]

Betzig, E.

T. A. Planchon, L. Gao, D. E. Milkie, M. W. Davidson, J. A. Galbraith, C. G. Galbraith, and E. Betzig, “Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination,” Nat. Methods 8(5), 417–423 (2011).
[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]

Bock, M.

R. Jerecic, M. Bock, S. Nielles-Vallespin, C. Wacker, W. Bauer, and L. R. Schad, “ECG-gated 23Na-MRI of the human heart using a 3D-radial projection technique with ultra-short echo times,” MAGMA 16(6), 297–302 (2004).
[Crossref] [PubMed]

Bronner-Fraser, M.

A. Trinh, T. Hochgreb, M. Graham, D. Wu, F. Ruf-Zamojski, C. S. Jayasena, A. Saxena, R. Hawk, A. Gonzalez-Serricchio, A. Dixson, E. Chow, C. Gonzales, H. Y. Leung, I. Solomon, M. Bronner-Fraser, S. G. Megason, and S. E. Fraser, “A versatile gene trap to visualize and interrogate the function of the vertebrate proteome,” Genes Dev. 25(21), 2306–2320 (2011).
[Crossref] [PubMed]

Chan, F. P.

M. Markl, F. P. Chan, M. T. Alley, K. L. Wedding, M. T. Draney, C. J. Elkins, D. W. Parker, R. Wicker, C. A. Taylor, R. J. Herfkens, and N. J. Pelc, “Time-resolved three-dimensional phase-contrast MRI,” J. Magn. Reson. Imaging 17(4), 499–506 (2003).
[Crossref] [PubMed]

Chaudhry, B.

J. M. Taylor, C. D. Saunter, G. D. Love, J. M. Girkin, D. J. Henderson, and B. Chaudhry, “Real-time optical gating for three-dimensional beating heart imaging,” J. Biomed. Opt. 16(11), 116021 (2011).
[Crossref] [PubMed]

Choi, J. M.

T. V. Truong, W. Supatto, D. S. Koos, J. M. Choi, and S. E. Fraser, “Deep and fast live imaging with two-photon scanned light-sheet microscopy,” Nat. Methods 8(9), 757–760 (2011).
[Crossref] [PubMed]

Chow, E.

A. Trinh, T. Hochgreb, M. Graham, D. Wu, F. Ruf-Zamojski, C. S. Jayasena, A. Saxena, R. Hawk, A. Gonzalez-Serricchio, A. Dixson, E. Chow, C. Gonzales, H. Y. Leung, I. Solomon, M. Bronner-Fraser, S. G. Megason, and S. E. Fraser, “A versatile gene trap to visualize and interrogate the function of the vertebrate proteome,” Genes Dev. 25(21), 2306–2320 (2011).
[Crossref] [PubMed]

Cohn, J. B.

W. L. Stanford, J. B. Cohn, and S. P. Cordes, “Gene-trap mutagenesis: past, present and beyond,” Nat. Rev. Genet. 2(10), 756–768 (2001).
[Crossref] [PubMed]

Conklin, B. R.

W. C. Skarnes, H. von Melchner, W. Wurst, G. Hicks, A. S. Nord, T. Cox, S. G. Young, P. Ruiz, P. Soriano, M. Tessier-Lavigne, B. R. Conklin, W. L. Stanford, J. Rossant, and International Gene Trap Consortium, “A public gene trap resource for mouse functional genomics,” Nat. Genet. 36(6), 543–544 (2004).
[Crossref] [PubMed]

Cordes, S. P.

W. L. Stanford, J. B. Cohn, and S. P. Cordes, “Gene-trap mutagenesis: past, present and beyond,” Nat. Rev. Genet. 2(10), 756–768 (2001).
[Crossref] [PubMed]

Cox, T.

W. C. Skarnes, H. von Melchner, W. Wurst, G. Hicks, A. S. Nord, T. Cox, S. G. Young, P. Ruiz, P. Soriano, M. Tessier-Lavigne, B. R. Conklin, W. L. Stanford, J. Rossant, and International Gene Trap Consortium, “A public gene trap resource for mouse functional genomics,” Nat. Genet. 36(6), 543–544 (2004).
[Crossref] [PubMed]

Davidson, M. W.

T. A. Planchon, L. Gao, D. E. Milkie, M. W. Davidson, J. A. Galbraith, C. G. Galbraith, and E. Betzig, “Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination,” Nat. Methods 8(5), 417–423 (2011).
[Crossref] [PubMed]

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).
[Crossref] [PubMed]

I. V. Larina, K. V. Larin, M. E. Dickinson, and M. Liebling, “Sequential turning acquisition and reconstruction (STAR) method for four-dimensional imaging of cyclically moving structures,” Biomed. Opt. Express 3(3), 650–660 (2012).
[Crossref] [PubMed]

M. Liebling, A. S. Forouhar, R. Wolleschensky, B. Zimmermann, R. Ankerhold, S. E. Fraser, M. Gharib, and M. E. Dickinson, “Rapid three-dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development,” Dev. Dyn. 235(11), 2940–2948 (2006).
[Crossref] [PubMed]

A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H. J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312(5774), 751–753 (2006).
[Crossref] [PubMed]

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]

M. Liebling, J. Vermot, A. S. Forouhar, M. Gharib, M. E. Dickinson, and S. E. Fraser, “Nonuniform temporal alignment of slice sequences for four-dimensional imaging of cyclically deforming embryonic structures,” Proceedings of the 3rd IEEE International Symposium on Biomedical Imaging: Macro to Nano (ISBI'06), Arlington, VA, USA, April 6–9, 1156–1159 (2006)
[Crossref]

Dixson, A.

A. Trinh, T. Hochgreb, M. Graham, D. Wu, F. Ruf-Zamojski, C. S. Jayasena, A. Saxena, R. Hawk, A. Gonzalez-Serricchio, A. Dixson, E. Chow, C. Gonzales, H. Y. Leung, I. Solomon, M. Bronner-Fraser, S. G. Megason, and S. E. Fraser, “A versatile gene trap to visualize and interrogate the function of the vertebrate proteome,” Genes Dev. 25(21), 2306–2320 (2011).
[Crossref] [PubMed]

Draney, M. T.

M. Markl, F. P. Chan, M. T. Alley, K. L. Wedding, M. T. Draney, C. J. Elkins, D. W. Parker, R. Wicker, C. A. Taylor, R. J. Herfkens, and N. J. Pelc, “Time-resolved three-dimensional phase-contrast MRI,” J. Magn. Reson. Imaging 17(4), 499–506 (2003).
[Crossref] [PubMed]

Edelstein, A. D.

A. D. Edelstein, M. A. Tsuchida, N. Amodaj, H. Pinkard, R. D. Vale, and N. Stuurman, “Advanced methods of microscope control using μManager software,” J. Biol. Methods 1(2), 10 (2014).
[Crossref] [PubMed]

Elkins, C. J.

M. Markl, F. P. Chan, M. T. Alley, K. L. Wedding, M. T. Draney, C. J. Elkins, D. W. Parker, R. Wicker, C. A. Taylor, R. J. Herfkens, and N. J. Pelc, “Time-resolved three-dimensional phase-contrast MRI,” J. Magn. Reson. Imaging 17(4), 499–506 (2003).
[Crossref] [PubMed]

Fahrbach, F. O.

M. Mickoleit, B. Schmid, M. Weber, F. O. Fahrbach, S. Hombach, S. Reischauer, and J. Huisken, “High-resolution reconstruction of the beating zebrafish heart,” Nat. Methods 11(9), 919–922 (2014).
[Crossref] [PubMed]

F. O. Fahrbach, V. Gurchenkov, K. Alessandri, P. Nassoy, and A. Rohrbach, “Light-sheet microscopy in thick media using scanned Bessel beams and two-photon fluorescence excitation,” Opt. Express 21(11), 13824–13839 (2013).
[Crossref] [PubMed]

Forouhar, A. S.

M. Liebling, A. S. Forouhar, R. Wolleschensky, B. Zimmermann, R. Ankerhold, S. E. Fraser, M. Gharib, and M. E. Dickinson, “Rapid three-dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development,” Dev. Dyn. 235(11), 2940–2948 (2006).
[Crossref] [PubMed]

A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H. J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312(5774), 751–753 (2006).
[Crossref] [PubMed]

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]

J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevedo-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature 421(6919), 172–177 (2003).
[Crossref] [PubMed]

M. Liebling, J. Vermot, A. S. Forouhar, M. Gharib, M. E. Dickinson, and S. E. Fraser, “Nonuniform temporal alignment of slice sequences for four-dimensional imaging of cyclically deforming embryonic structures,” Proceedings of the 3rd IEEE International Symposium on Biomedical Imaging: Macro to Nano (ISBI'06), Arlington, VA, USA, April 6–9, 1156–1159 (2006)
[Crossref]

Fraser, S. E.

T. V. Truong, W. Supatto, D. S. Koos, J. M. Choi, and S. E. Fraser, “Deep and fast live imaging with two-photon scanned light-sheet microscopy,” Nat. Methods 8(9), 757–760 (2011).
[Crossref] [PubMed]

A. Trinh, T. Hochgreb, M. Graham, D. Wu, F. Ruf-Zamojski, C. S. Jayasena, A. Saxena, R. Hawk, A. Gonzalez-Serricchio, A. Dixson, E. Chow, C. Gonzales, H. Y. Leung, I. Solomon, M. Bronner-Fraser, S. G. Megason, and S. E. Fraser, “A versatile gene trap to visualize and interrogate the function of the vertebrate proteome,” Genes Dev. 25(21), 2306–2320 (2011).
[Crossref] [PubMed]

A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H. J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312(5774), 751–753 (2006).
[Crossref] [PubMed]

M. Liebling, A. S. Forouhar, R. Wolleschensky, B. Zimmermann, R. Ankerhold, S. E. Fraser, M. Gharib, and M. E. Dickinson, “Rapid three-dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development,” Dev. Dyn. 235(11), 2940–2948 (2006).
[Crossref] [PubMed]

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]

J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevedo-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature 421(6919), 172–177 (2003).
[Crossref] [PubMed]

M. Liebling, J. Vermot, A. S. Forouhar, M. Gharib, M. E. Dickinson, and S. E. Fraser, “Nonuniform temporal alignment of slice sequences for four-dimensional imaging of cyclically deforming embryonic structures,” Proceedings of the 3rd IEEE International Symposium on Biomedical Imaging: Macro to Nano (ISBI'06), Arlington, VA, USA, April 6–9, 1156–1159 (2006)
[Crossref]

Galbraith, C. G.

T. A. Planchon, L. Gao, D. E. Milkie, M. W. Davidson, J. A. Galbraith, C. G. Galbraith, and E. Betzig, “Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination,” Nat. Methods 8(5), 417–423 (2011).
[Crossref] [PubMed]

Galbraith, J. A.

T. A. Planchon, L. Gao, D. E. Milkie, M. W. Davidson, J. A. Galbraith, C. G. Galbraith, and E. Betzig, “Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination,” Nat. Methods 8(5), 417–423 (2011).
[Crossref] [PubMed]

Gao, L.

T. A. Planchon, L. Gao, D. E. Milkie, M. W. Davidson, J. A. Galbraith, C. G. Galbraith, and E. Betzig, “Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination,” Nat. Methods 8(5), 417–423 (2011).
[Crossref] [PubMed]

Gharib, M.

M. Liebling, A. S. Forouhar, R. Wolleschensky, B. Zimmermann, R. Ankerhold, S. E. Fraser, M. Gharib, and M. E. Dickinson, “Rapid three-dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development,” Dev. Dyn. 235(11), 2940–2948 (2006).
[Crossref] [PubMed]

A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H. J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312(5774), 751–753 (2006).
[Crossref] [PubMed]

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]

J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevedo-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature 421(6919), 172–177 (2003).
[Crossref] [PubMed]

M. Liebling, J. Vermot, A. S. Forouhar, M. Gharib, M. E. Dickinson, and S. E. Fraser, “Nonuniform temporal alignment of slice sequences for four-dimensional imaging of cyclically deforming embryonic structures,” Proceedings of the 3rd IEEE International Symposium on Biomedical Imaging: Macro to Nano (ISBI'06), Arlington, VA, USA, April 6–9, 1156–1159 (2006)
[Crossref]

Girkin, J. M.

J. M. Taylor, C. D. Saunter, G. D. Love, J. M. Girkin, D. J. Henderson, and B. Chaudhry, “Real-time optical gating for three-dimensional beating heart imaging,” J. Biomed. Opt. 16(11), 116021 (2011).
[Crossref] [PubMed]

Gonzales, C.

A. Trinh, T. Hochgreb, M. Graham, D. Wu, F. Ruf-Zamojski, C. S. Jayasena, A. Saxena, R. Hawk, A. Gonzalez-Serricchio, A. Dixson, E. Chow, C. Gonzales, H. Y. Leung, I. Solomon, M. Bronner-Fraser, S. G. Megason, and S. E. Fraser, “A versatile gene trap to visualize and interrogate the function of the vertebrate proteome,” Genes Dev. 25(21), 2306–2320 (2011).
[Crossref] [PubMed]

Gonzalez-Serricchio, A.

A. Trinh, T. Hochgreb, M. Graham, D. Wu, F. Ruf-Zamojski, C. S. Jayasena, A. Saxena, R. Hawk, A. Gonzalez-Serricchio, A. Dixson, E. Chow, C. Gonzales, H. Y. Leung, I. Solomon, M. Bronner-Fraser, S. G. Megason, and S. E. Fraser, “A versatile gene trap to visualize and interrogate the function of the vertebrate proteome,” Genes Dev. 25(21), 2306–2320 (2011).
[Crossref] [PubMed]

Graham, M.

A. Trinh, T. Hochgreb, M. Graham, D. Wu, F. Ruf-Zamojski, C. S. Jayasena, A. Saxena, R. Hawk, A. Gonzalez-Serricchio, A. Dixson, E. Chow, C. Gonzales, H. Y. Leung, I. Solomon, M. Bronner-Fraser, S. G. Megason, and S. E. Fraser, “A versatile gene trap to visualize and interrogate the function of the vertebrate proteome,” Genes Dev. 25(21), 2306–2320 (2011).
[Crossref] [PubMed]

Gualda, E. J.

Gurchenkov, V.

Hawk, R.

A. Trinh, T. Hochgreb, M. Graham, D. Wu, F. Ruf-Zamojski, C. S. Jayasena, A. Saxena, R. Hawk, A. Gonzalez-Serricchio, A. Dixson, E. Chow, C. Gonzales, H. Y. Leung, I. Solomon, M. Bronner-Fraser, S. G. Megason, and S. E. Fraser, “A versatile gene trap to visualize and interrogate the function of the vertebrate proteome,” Genes Dev. 25(21), 2306–2320 (2011).
[Crossref] [PubMed]

Henderson, D. J.

J. M. Taylor, C. D. Saunter, G. D. Love, J. M. Girkin, D. J. Henderson, and B. Chaudhry, “Real-time optical gating for three-dimensional beating heart imaging,” J. Biomed. Opt. 16(11), 116021 (2011).
[Crossref] [PubMed]

Herfkens, R. J.

M. Markl, F. P. Chan, M. T. Alley, K. L. Wedding, M. T. Draney, C. J. Elkins, D. W. Parker, R. Wicker, C. A. Taylor, R. J. Herfkens, and N. J. Pelc, “Time-resolved three-dimensional phase-contrast MRI,” J. Magn. Reson. Imaging 17(4), 499–506 (2003).
[Crossref] [PubMed]

Hickerson, A.

A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H. J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312(5774), 751–753 (2006).
[Crossref] [PubMed]

Hicks, G.

W. C. Skarnes, H. von Melchner, W. Wurst, G. Hicks, A. S. Nord, T. Cox, S. G. Young, P. Ruiz, P. Soriano, M. Tessier-Lavigne, B. R. Conklin, W. L. Stanford, J. Rossant, and International Gene Trap Consortium, “A public gene trap resource for mouse functional genomics,” Nat. Genet. 36(6), 543–544 (2004).
[Crossref] [PubMed]

Hochgreb, T.

A. Trinh, T. Hochgreb, M. Graham, D. Wu, F. Ruf-Zamojski, C. S. Jayasena, A. Saxena, R. Hawk, A. Gonzalez-Serricchio, A. Dixson, E. Chow, C. Gonzales, H. Y. Leung, I. Solomon, M. Bronner-Fraser, S. G. Megason, and S. E. Fraser, “A versatile gene trap to visualize and interrogate the function of the vertebrate proteome,” Genes Dev. 25(21), 2306–2320 (2011).
[Crossref] [PubMed]

Hombach, S.

M. Mickoleit, B. Schmid, M. Weber, F. O. Fahrbach, S. Hombach, S. Reischauer, and J. Huisken, “High-resolution reconstruction of the beating zebrafish heart,” Nat. Methods 11(9), 919–922 (2014).
[Crossref] [PubMed]

Hove, J. R.

A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H. J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312(5774), 751–753 (2006).
[Crossref] [PubMed]

J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevedo-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature 421(6919), 172–177 (2003).
[Crossref] [PubMed]

Huisken, J.

M. Mickoleit, B. Schmid, M. Weber, F. O. Fahrbach, S. Hombach, S. Reischauer, and J. Huisken, “High-resolution reconstruction of the beating zebrafish heart,” Nat. Methods 11(9), 919–922 (2014).
[Crossref] [PubMed]

Jayasena, C. S.

A. Trinh, T. Hochgreb, M. Graham, D. Wu, F. Ruf-Zamojski, C. S. Jayasena, A. Saxena, R. Hawk, A. Gonzalez-Serricchio, A. Dixson, E. Chow, C. Gonzales, H. Y. Leung, I. Solomon, M. Bronner-Fraser, S. G. Megason, and S. E. Fraser, “A versatile gene trap to visualize and interrogate the function of the vertebrate proteome,” Genes Dev. 25(21), 2306–2320 (2011).
[Crossref] [PubMed]

Jerecic, R.

R. Jerecic, M. Bock, S. Nielles-Vallespin, C. Wacker, W. Bauer, and L. R. Schad, “ECG-gated 23Na-MRI of the human heart using a 3D-radial projection technique with ultra-short echo times,” MAGMA 16(6), 297–302 (2004).
[Crossref] [PubMed]

Koos, D. S.

T. V. Truong, W. Supatto, D. S. Koos, J. M. Choi, and S. E. Fraser, “Deep and fast live imaging with two-photon scanned light-sheet microscopy,” Nat. Methods 8(9), 757–760 (2011).
[Crossref] [PubMed]

Köster, R. W.

J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevedo-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature 421(6919), 172–177 (2003).
[Crossref] [PubMed]

Larin, K. V.

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]

I. V. Larina, K. V. Larin, M. E. Dickinson, and M. Liebling, “Sequential turning acquisition and reconstruction (STAR) method for four-dimensional imaging of cyclically moving structures,” Biomed. Opt. Express 3(3), 650–660 (2012).
[Crossref] [PubMed]

Larina, I. V.

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]

I. V. Larina, K. V. Larin, M. E. Dickinson, and M. Liebling, “Sequential turning acquisition and reconstruction (STAR) method for four-dimensional imaging of cyclically moving structures,” Biomed. Opt. Express 3(3), 650–660 (2012).
[Crossref] [PubMed]

Leung, H. Y.

A. Trinh, T. Hochgreb, M. Graham, D. Wu, F. Ruf-Zamojski, C. S. Jayasena, A. Saxena, R. Hawk, A. Gonzalez-Serricchio, A. Dixson, E. Chow, C. Gonzales, H. Y. Leung, I. Solomon, M. Bronner-Fraser, S. G. Megason, and S. E. Fraser, “A versatile gene trap to visualize and interrogate the function of the vertebrate proteome,” Genes Dev. 25(21), 2306–2320 (2011).
[Crossref] [PubMed]

Licea-Rodriguez, J.

Liebling, M.

D. W. Staudt, J. Liu, K. S. Thorn, N. Stuurman, M. Liebling, and D. Y. R. Stainier, “High-resolution imaging of cardiomyocyte behavior reveals two distinct steps in ventricular trabeculation,” Development 141(3), 585–593 (2014).
[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]

I. V. Larina, K. V. Larin, M. E. Dickinson, and M. Liebling, “Sequential turning acquisition and reconstruction (STAR) method for four-dimensional imaging of cyclically moving structures,” Biomed. Opt. Express 3(3), 650–660 (2012).
[Crossref] [PubMed]

J. Ohn, H. J. Tsai, and M. Liebling, “Joint dynamic imaging of morphogenesis and function in the developing heart,” Organogenesis 5(4), 248–255 (2009).
[Crossref] [PubMed]

A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H. J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312(5774), 751–753 (2006).
[Crossref] [PubMed]

M. Liebling, A. S. Forouhar, R. Wolleschensky, B. Zimmermann, R. Ankerhold, S. E. Fraser, M. Gharib, and M. E. Dickinson, “Rapid three-dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development,” Dev. Dyn. 235(11), 2940–2948 (2006).
[Crossref] [PubMed]

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]

M. Liebling, J. Vermot, A. S. Forouhar, M. Gharib, M. E. Dickinson, and S. E. Fraser, “Nonuniform temporal alignment of slice sequences for four-dimensional imaging of cyclically deforming embryonic structures,” Proceedings of the 3rd IEEE International Symposium on Biomedical Imaging: Macro to Nano (ISBI'06), Arlington, VA, USA, April 6–9, 1156–1159 (2006)
[Crossref]

Lisette, A.

A. Lisette, L. Maddison, and C. Wenbiao, “Conditional gene-trap mutagenesis in Zebrafish methods,” Mol. Biol. 1101, 393–411 (2014).

Liu, J.

D. W. Staudt, J. Liu, K. S. Thorn, N. Stuurman, M. Liebling, and D. Y. R. Stainier, “High-resolution imaging of cardiomyocyte behavior reveals two distinct steps in ventricular trabeculation,” Development 141(3), 585–593 (2014).
[Crossref] [PubMed]

Love, G. D.

J. M. Taylor, C. D. Saunter, G. D. Love, J. M. Girkin, D. J. Henderson, and B. Chaudhry, “Real-time optical gating for three-dimensional beating heart imaging,” J. Biomed. Opt. 16(11), 116021 (2011).
[Crossref] [PubMed]

Loza-Alvarez, P.

Maddison, L.

A. Lisette, L. Maddison, and C. Wenbiao, “Conditional gene-trap mutagenesis in Zebrafish methods,” Mol. Biol. 1101, 393–411 (2014).

Mahou, P.

P. Mahou, J. Vermot, E. Beaurepaire, and W. Supatto, “Multicolor two-photon light-sheet microscopy,” Nat. Methods 11(6), 600–601 (2014).
[Crossref] [PubMed]

Markl, M.

M. Markl, F. P. Chan, M. T. Alley, K. L. Wedding, M. T. Draney, C. J. Elkins, D. W. Parker, R. Wicker, C. A. Taylor, R. J. Herfkens, and N. J. Pelc, “Time-resolved three-dimensional phase-contrast MRI,” J. Magn. Reson. Imaging 17(4), 499–506 (2003).
[Crossref] [PubMed]

Mayer, J.

Megason, S. G.

A. Trinh, T. Hochgreb, M. Graham, D. Wu, F. Ruf-Zamojski, C. S. Jayasena, A. Saxena, R. Hawk, A. Gonzalez-Serricchio, A. Dixson, E. Chow, C. Gonzales, H. Y. Leung, I. Solomon, M. Bronner-Fraser, S. G. Megason, and S. E. Fraser, “A versatile gene trap to visualize and interrogate the function of the vertebrate proteome,” Genes Dev. 25(21), 2306–2320 (2011).
[Crossref] [PubMed]

Mickoleit, M.

M. Mickoleit, B. Schmid, M. Weber, F. O. Fahrbach, S. Hombach, S. Reischauer, and J. Huisken, “High-resolution reconstruction of the beating zebrafish heart,” Nat. Methods 11(9), 919–922 (2014).
[Crossref] [PubMed]

Milkie, D. E.

T. A. Planchon, L. Gao, D. E. Milkie, M. W. Davidson, J. A. Galbraith, C. G. Galbraith, and E. Betzig, “Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination,” Nat. Methods 8(5), 417–423 (2011).
[Crossref] [PubMed]

Nasiraei-Moghaddam, A.

A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H. J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312(5774), 751–753 (2006).
[Crossref] [PubMed]

Nassoy, P.

Nielles-Vallespin, S.

R. Jerecic, M. Bock, S. Nielles-Vallespin, C. Wacker, W. Bauer, and L. R. Schad, “ECG-gated 23Na-MRI of the human heart using a 3D-radial projection technique with ultra-short echo times,” MAGMA 16(6), 297–302 (2004).
[Crossref] [PubMed]

Nord, A. S.

W. C. Skarnes, H. von Melchner, W. Wurst, G. Hicks, A. S. Nord, T. Cox, S. G. Young, P. Ruiz, P. Soriano, M. Tessier-Lavigne, B. R. Conklin, W. L. Stanford, J. Rossant, and International Gene Trap Consortium, “A public gene trap resource for mouse functional genomics,” Nat. Genet. 36(6), 543–544 (2004).
[Crossref] [PubMed]

Ohn, J.

J. Ohn, H. J. Tsai, and M. Liebling, “Joint dynamic imaging of morphogenesis and function in the developing heart,” Organogenesis 5(4), 248–255 (2009).
[Crossref] [PubMed]

Olarte, O. E.

Palero, J. A.

Parker, D. W.

M. Markl, F. P. Chan, M. T. Alley, K. L. Wedding, M. T. Draney, C. J. Elkins, D. W. Parker, R. Wicker, C. A. Taylor, R. J. Herfkens, and N. J. Pelc, “Time-resolved three-dimensional phase-contrast MRI,” J. Magn. Reson. Imaging 17(4), 499–506 (2003).
[Crossref] [PubMed]

Pelc, N. J.

M. Markl, F. P. Chan, M. T. Alley, K. L. Wedding, M. T. Draney, C. J. Elkins, D. W. Parker, R. Wicker, C. A. Taylor, R. J. Herfkens, and N. J. Pelc, “Time-resolved three-dimensional phase-contrast MRI,” J. Magn. Reson. Imaging 17(4), 499–506 (2003).
[Crossref] [PubMed]

Pinkard, H.

A. D. Edelstein, M. A. Tsuchida, N. Amodaj, H. Pinkard, R. D. Vale, and N. Stuurman, “Advanced methods of microscope control using μManager software,” J. Biol. Methods 1(2), 10 (2014).
[Crossref] [PubMed]

Planchon, T. A.

T. A. Planchon, L. Gao, D. E. Milkie, M. W. Davidson, J. A. Galbraith, C. G. Galbraith, and E. Betzig, “Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination,” Nat. Methods 8(5), 417–423 (2011).
[Crossref] [PubMed]

Rangel-Rojo, R.

Reischauer, S.

M. Mickoleit, B. Schmid, M. Weber, F. O. Fahrbach, S. Hombach, S. Reischauer, and J. Huisken, “High-resolution reconstruction of the beating zebrafish heart,” Nat. Methods 11(9), 919–922 (2014).
[Crossref] [PubMed]

Rocha-Mendoza, I.

Rohrbach, A.

Rossant, J.

W. C. Skarnes, H. von Melchner, W. Wurst, G. Hicks, A. S. Nord, T. Cox, S. G. Young, P. Ruiz, P. Soriano, M. Tessier-Lavigne, B. R. Conklin, W. L. Stanford, J. Rossant, and International Gene Trap Consortium, “A public gene trap resource for mouse functional genomics,” Nat. Genet. 36(6), 543–544 (2004).
[Crossref] [PubMed]

Ruf-Zamojski, F.

A. Trinh, T. Hochgreb, M. Graham, D. Wu, F. Ruf-Zamojski, C. S. Jayasena, A. Saxena, R. Hawk, A. Gonzalez-Serricchio, A. Dixson, E. Chow, C. Gonzales, H. Y. Leung, I. Solomon, M. Bronner-Fraser, S. G. Megason, and S. E. Fraser, “A versatile gene trap to visualize and interrogate the function of the vertebrate proteome,” Genes Dev. 25(21), 2306–2320 (2011).
[Crossref] [PubMed]

Ruiz, P.

W. C. Skarnes, H. von Melchner, W. Wurst, G. Hicks, A. S. Nord, T. Cox, S. G. Young, P. Ruiz, P. Soriano, M. Tessier-Lavigne, B. R. Conklin, W. L. Stanford, J. Rossant, and International Gene Trap Consortium, “A public gene trap resource for mouse functional genomics,” Nat. Genet. 36(6), 543–544 (2004).
[Crossref] [PubMed]

Saunter, C. D.

J. M. Taylor, C. D. Saunter, G. D. Love, J. M. Girkin, D. J. Henderson, and B. Chaudhry, “Real-time optical gating for three-dimensional beating heart imaging,” J. Biomed. Opt. 16(11), 116021 (2011).
[Crossref] [PubMed]

Saxena, A.

A. Trinh, T. Hochgreb, M. Graham, D. Wu, F. Ruf-Zamojski, C. S. Jayasena, A. Saxena, R. Hawk, A. Gonzalez-Serricchio, A. Dixson, E. Chow, C. Gonzales, H. Y. Leung, I. Solomon, M. Bronner-Fraser, S. G. Megason, and S. E. Fraser, “A versatile gene trap to visualize and interrogate the function of the vertebrate proteome,” Genes Dev. 25(21), 2306–2320 (2011).
[Crossref] [PubMed]

Schad, L. R.

R. Jerecic, M. Bock, S. Nielles-Vallespin, C. Wacker, W. Bauer, and L. R. Schad, “ECG-gated 23Na-MRI of the human heart using a 3D-radial projection technique with ultra-short echo times,” MAGMA 16(6), 297–302 (2004).
[Crossref] [PubMed]

Schmid, B.

M. Mickoleit, B. Schmid, M. Weber, F. O. Fahrbach, S. Hombach, S. Reischauer, and J. Huisken, “High-resolution reconstruction of the beating zebrafish heart,” Nat. Methods 11(9), 919–922 (2014).
[Crossref] [PubMed]

Sebas, M.

A. D. Aguirre, C. Vinegoni, M. Sebas, and R. Weissleder, “Intravital imaging of cardiac function at the single-cell level,” Proc. Natl. Acad. Sci. U.S.A. 111(31), 11257–11262 (2014).
[Crossref] [PubMed]

Sharpe, J.

Skarnes, W. C.

W. C. Skarnes, H. von Melchner, W. Wurst, G. Hicks, A. S. Nord, T. Cox, S. G. Young, P. Ruiz, P. Soriano, M. Tessier-Lavigne, B. R. Conklin, W. L. Stanford, J. Rossant, and International Gene Trap Consortium, “A public gene trap resource for mouse functional genomics,” Nat. Genet. 36(6), 543–544 (2004).
[Crossref] [PubMed]

Solomon, I.

A. Trinh, T. Hochgreb, M. Graham, D. Wu, F. Ruf-Zamojski, C. S. Jayasena, A. Saxena, R. Hawk, A. Gonzalez-Serricchio, A. Dixson, E. Chow, C. Gonzales, H. Y. Leung, I. Solomon, M. Bronner-Fraser, S. G. Megason, and S. E. Fraser, “A versatile gene trap to visualize and interrogate the function of the vertebrate proteome,” Genes Dev. 25(21), 2306–2320 (2011).
[Crossref] [PubMed]

Soriano, P.

W. C. Skarnes, H. von Melchner, W. Wurst, G. Hicks, A. S. Nord, T. Cox, S. G. Young, P. Ruiz, P. Soriano, M. Tessier-Lavigne, B. R. Conklin, W. L. Stanford, J. Rossant, and International Gene Trap Consortium, “A public gene trap resource for mouse functional genomics,” Nat. Genet. 36(6), 543–544 (2004).
[Crossref] [PubMed]

Stainier, D. Y.

D. Y. Stainier, “Zebrafish genetics and vertebrate heart formation,” Nat. Rev. Genet. 2(1), 39–48 (2001).
[Crossref] [PubMed]

Stainier, D. Y. R.

D. W. Staudt, J. Liu, K. S. Thorn, N. Stuurman, M. Liebling, and D. Y. R. Stainier, “High-resolution imaging of cardiomyocyte behavior reveals two distinct steps in ventricular trabeculation,” Development 141(3), 585–593 (2014).
[Crossref] [PubMed]

Stanford, W. L.

W. C. Skarnes, H. von Melchner, W. Wurst, G. Hicks, A. S. Nord, T. Cox, S. G. Young, P. Ruiz, P. Soriano, M. Tessier-Lavigne, B. R. Conklin, W. L. Stanford, J. Rossant, and International Gene Trap Consortium, “A public gene trap resource for mouse functional genomics,” Nat. Genet. 36(6), 543–544 (2004).
[Crossref] [PubMed]

W. L. Stanford, J. B. Cohn, and S. P. Cordes, “Gene-trap mutagenesis: past, present and beyond,” Nat. Rev. Genet. 2(10), 756–768 (2001).
[Crossref] [PubMed]

Staudt, D. W.

D. W. Staudt, J. Liu, K. S. Thorn, N. Stuurman, M. Liebling, and D. Y. R. Stainier, “High-resolution imaging of cardiomyocyte behavior reveals two distinct steps in ventricular trabeculation,” Development 141(3), 585–593 (2014).
[Crossref] [PubMed]

Stuurman, N.

D. W. Staudt, J. Liu, K. S. Thorn, N. Stuurman, M. Liebling, and D. Y. R. Stainier, “High-resolution imaging of cardiomyocyte behavior reveals two distinct steps in ventricular trabeculation,” Development 141(3), 585–593 (2014).
[Crossref] [PubMed]

A. D. Edelstein, M. A. Tsuchida, N. Amodaj, H. Pinkard, R. D. Vale, and N. Stuurman, “Advanced methods of microscope control using μManager software,” J. Biol. Methods 1(2), 10 (2014).
[Crossref] [PubMed]

Supatto, W.

P. Mahou, J. Vermot, E. Beaurepaire, and W. Supatto, “Multicolor two-photon light-sheet microscopy,” Nat. Methods 11(6), 600–601 (2014).
[Crossref] [PubMed]

T. V. Truong, W. Supatto, D. S. Koos, J. M. Choi, and S. E. Fraser, “Deep and fast live imaging with two-photon scanned light-sheet microscopy,” Nat. Methods 8(9), 757–760 (2011).
[Crossref] [PubMed]

Swoger, J.

Taylor, C. A.

M. Markl, F. P. Chan, M. T. Alley, K. L. Wedding, M. T. Draney, C. J. Elkins, D. W. Parker, R. Wicker, C. A. Taylor, R. J. Herfkens, and N. J. Pelc, “Time-resolved three-dimensional phase-contrast MRI,” J. Magn. Reson. Imaging 17(4), 499–506 (2003).
[Crossref] [PubMed]

Taylor, J. M.

J. M. Taylor, “Optically gated beating-heart imaging,” Front Physiol 5, 481 (2014).
[Crossref] [PubMed]

J. M. Taylor, C. D. Saunter, G. D. Love, J. M. Girkin, D. J. Henderson, and B. Chaudhry, “Real-time optical gating for three-dimensional beating heart imaging,” J. Biomed. Opt. 16(11), 116021 (2011).
[Crossref] [PubMed]

Tessier-Lavigne, M.

W. C. Skarnes, H. von Melchner, W. Wurst, G. Hicks, A. S. Nord, T. Cox, S. G. Young, P. Ruiz, P. Soriano, M. Tessier-Lavigne, B. R. Conklin, W. L. Stanford, J. Rossant, and International Gene Trap Consortium, “A public gene trap resource for mouse functional genomics,” Nat. Genet. 36(6), 543–544 (2004).
[Crossref] [PubMed]

Thorn, K. S.

D. W. Staudt, J. Liu, K. S. Thorn, N. Stuurman, M. Liebling, and D. Y. R. Stainier, “High-resolution imaging of cardiomyocyte behavior reveals two distinct steps in ventricular trabeculation,” Development 141(3), 585–593 (2014).
[Crossref] [PubMed]

Trinh, A.

A. Trinh, T. Hochgreb, M. Graham, D. Wu, F. Ruf-Zamojski, C. S. Jayasena, A. Saxena, R. Hawk, A. Gonzalez-Serricchio, A. Dixson, E. Chow, C. Gonzales, H. Y. Leung, I. Solomon, M. Bronner-Fraser, S. G. Megason, and S. E. Fraser, “A versatile gene trap to visualize and interrogate the function of the vertebrate proteome,” Genes Dev. 25(21), 2306–2320 (2011).
[Crossref] [PubMed]

Truong, T. V.

T. V. Truong, W. Supatto, D. S. Koos, J. M. Choi, and S. E. Fraser, “Deep and fast live imaging with two-photon scanned light-sheet microscopy,” Nat. Methods 8(9), 757–760 (2011).
[Crossref] [PubMed]

Tsai, H. J.

J. Ohn, H. J. Tsai, and M. Liebling, “Joint dynamic imaging of morphogenesis and function in the developing heart,” Organogenesis 5(4), 248–255 (2009).
[Crossref] [PubMed]

A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H. J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312(5774), 751–753 (2006).
[Crossref] [PubMed]

Tsuchida, M. A.

A. D. Edelstein, M. A. Tsuchida, N. Amodaj, H. Pinkard, R. D. Vale, and N. Stuurman, “Advanced methods of microscope control using μManager software,” J. Biol. Methods 1(2), 10 (2014).
[Crossref] [PubMed]

Vale, R. D.

A. D. Edelstein, M. A. Tsuchida, N. Amodaj, H. Pinkard, R. D. Vale, and N. Stuurman, “Advanced methods of microscope control using μManager software,” J. Biol. Methods 1(2), 10 (2014).
[Crossref] [PubMed]

Vermot, J.

P. Mahou, J. Vermot, E. Beaurepaire, and W. Supatto, “Multicolor two-photon light-sheet microscopy,” Nat. Methods 11(6), 600–601 (2014).
[Crossref] [PubMed]

M. Liebling, J. Vermot, A. S. Forouhar, M. Gharib, M. E. Dickinson, and S. E. Fraser, “Nonuniform temporal alignment of slice sequences for four-dimensional imaging of cyclically deforming embryonic structures,” Proceedings of the 3rd IEEE International Symposium on Biomedical Imaging: Macro to Nano (ISBI'06), Arlington, VA, USA, April 6–9, 1156–1159 (2006)
[Crossref]

Vinegoni, C.

A. D. Aguirre, C. Vinegoni, M. Sebas, and R. Weissleder, “Intravital imaging of cardiac function at the single-cell level,” Proc. Natl. Acad. Sci. U.S.A. 111(31), 11257–11262 (2014).
[Crossref] [PubMed]

von Melchner, H.

W. C. Skarnes, H. von Melchner, W. Wurst, G. Hicks, A. S. Nord, T. Cox, S. G. Young, P. Ruiz, P. Soriano, M. Tessier-Lavigne, B. R. Conklin, W. L. Stanford, J. Rossant, and International Gene Trap Consortium, “A public gene trap resource for mouse functional genomics,” Nat. Genet. 36(6), 543–544 (2004).
[Crossref] [PubMed]

Wacker, C.

R. Jerecic, M. Bock, S. Nielles-Vallespin, C. Wacker, W. Bauer, and L. R. Schad, “ECG-gated 23Na-MRI of the human heart using a 3D-radial projection technique with ultra-short echo times,” MAGMA 16(6), 297–302 (2004).
[Crossref] [PubMed]

Weber, M.

M. Mickoleit, B. Schmid, M. Weber, F. O. Fahrbach, S. Hombach, S. Reischauer, and J. Huisken, “High-resolution reconstruction of the beating zebrafish heart,” Nat. Methods 11(9), 919–922 (2014).
[Crossref] [PubMed]

Wedding, K. L.

M. Markl, F. P. Chan, M. T. Alley, K. L. Wedding, M. T. Draney, C. J. Elkins, D. W. Parker, R. Wicker, C. A. Taylor, R. J. Herfkens, and N. J. Pelc, “Time-resolved three-dimensional phase-contrast MRI,” J. Magn. Reson. Imaging 17(4), 499–506 (2003).
[Crossref] [PubMed]

Weissleder, R.

A. D. Aguirre, C. Vinegoni, M. Sebas, and R. Weissleder, “Intravital imaging of cardiac function at the single-cell level,” Proc. Natl. Acad. Sci. U.S.A. 111(31), 11257–11262 (2014).
[Crossref] [PubMed]

Wenbiao, C.

A. Lisette, L. Maddison, and C. Wenbiao, “Conditional gene-trap mutagenesis in Zebrafish methods,” Mol. Biol. 1101, 393–411 (2014).

Wicker, R.

M. Markl, F. P. Chan, M. T. Alley, K. L. Wedding, M. T. Draney, C. J. Elkins, D. W. Parker, R. Wicker, C. A. Taylor, R. J. Herfkens, and N. J. Pelc, “Time-resolved three-dimensional phase-contrast MRI,” J. Magn. Reson. Imaging 17(4), 499–506 (2003).
[Crossref] [PubMed]

Wolleschensky, R.

M. Liebling, A. S. Forouhar, R. Wolleschensky, B. Zimmermann, R. Ankerhold, S. E. Fraser, M. Gharib, and M. E. Dickinson, “Rapid three-dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development,” Dev. Dyn. 235(11), 2940–2948 (2006).
[Crossref] [PubMed]

Wu, D.

A. Trinh, T. Hochgreb, M. Graham, D. Wu, F. Ruf-Zamojski, C. S. Jayasena, A. Saxena, R. Hawk, A. Gonzalez-Serricchio, A. Dixson, E. Chow, C. Gonzales, H. Y. Leung, I. Solomon, M. Bronner-Fraser, S. G. Megason, and S. E. Fraser, “A versatile gene trap to visualize and interrogate the function of the vertebrate proteome,” Genes Dev. 25(21), 2306–2320 (2011).
[Crossref] [PubMed]

Wurst, W.

W. C. Skarnes, H. von Melchner, W. Wurst, G. Hicks, A. S. Nord, T. Cox, S. G. Young, P. Ruiz, P. Soriano, M. Tessier-Lavigne, B. R. Conklin, W. L. Stanford, J. Rossant, and International Gene Trap Consortium, “A public gene trap resource for mouse functional genomics,” Nat. Genet. 36(6), 543–544 (2004).
[Crossref] [PubMed]

Young, S. G.

W. C. Skarnes, H. von Melchner, W. Wurst, G. Hicks, A. S. Nord, T. Cox, S. G. Young, P. Ruiz, P. Soriano, M. Tessier-Lavigne, B. R. Conklin, W. L. Stanford, J. Rossant, and International Gene Trap Consortium, “A public gene trap resource for mouse functional genomics,” Nat. Genet. 36(6), 543–544 (2004).
[Crossref] [PubMed]

Zimmermann, B.

M. Liebling, A. S. Forouhar, R. Wolleschensky, B. Zimmermann, R. Ankerhold, S. E. Fraser, M. Gharib, and M. E. Dickinson, “Rapid three-dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development,” Dev. Dyn. 235(11), 2940–2948 (2006).
[Crossref] [PubMed]

Biomed. Opt. Express (2)

Dev. Dyn. (1)

M. Liebling, A. S. Forouhar, R. Wolleschensky, B. Zimmermann, R. Ankerhold, S. E. Fraser, M. Gharib, and M. E. Dickinson, “Rapid three-dimensional imaging and analysis of the beating embryonic heart reveals functional changes during development,” Dev. Dyn. 235(11), 2940–2948 (2006).
[Crossref] [PubMed]

Development (1)

D. W. Staudt, J. Liu, K. S. Thorn, N. Stuurman, M. Liebling, and D. Y. R. Stainier, “High-resolution imaging of cardiomyocyte behavior reveals two distinct steps in ventricular trabeculation,” Development 141(3), 585–593 (2014).
[Crossref] [PubMed]

Front Physiol (1)

J. M. Taylor, “Optically gated beating-heart imaging,” Front Physiol 5, 481 (2014).
[Crossref] [PubMed]

Genes Dev. (1)

A. Trinh, T. Hochgreb, M. Graham, D. Wu, F. Ruf-Zamojski, C. S. Jayasena, A. Saxena, R. Hawk, A. Gonzalez-Serricchio, A. Dixson, E. Chow, C. Gonzales, H. Y. Leung, I. Solomon, M. Bronner-Fraser, S. G. Megason, and S. E. Fraser, “A versatile gene trap to visualize and interrogate the function of the vertebrate proteome,” Genes Dev. 25(21), 2306–2320 (2011).
[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).
[Crossref] [PubMed]

J. Biol. Methods (1)

A. D. Edelstein, M. A. Tsuchida, N. Amodaj, H. Pinkard, R. D. Vale, and N. Stuurman, “Advanced methods of microscope control using μManager software,” J. Biol. Methods 1(2), 10 (2014).
[Crossref] [PubMed]

J. Biomed. Opt. (2)

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]

J. M. Taylor, C. D. Saunter, G. D. Love, J. M. Girkin, D. J. Henderson, and B. Chaudhry, “Real-time optical gating for three-dimensional beating heart imaging,” J. Biomed. Opt. 16(11), 116021 (2011).
[Crossref] [PubMed]

J. Magn. Reson. Imaging (1)

M. Markl, F. P. Chan, M. T. Alley, K. L. Wedding, M. T. Draney, C. J. Elkins, D. W. Parker, R. Wicker, C. A. Taylor, R. J. Herfkens, and N. J. Pelc, “Time-resolved three-dimensional phase-contrast MRI,” J. Magn. Reson. Imaging 17(4), 499–506 (2003).
[Crossref] [PubMed]

MAGMA (1)

R. Jerecic, M. Bock, S. Nielles-Vallespin, C. Wacker, W. Bauer, and L. R. Schad, “ECG-gated 23Na-MRI of the human heart using a 3D-radial projection technique with ultra-short echo times,” MAGMA 16(6), 297–302 (2004).
[Crossref] [PubMed]

Mol. Biol. (1)

A. Lisette, L. Maddison, and C. Wenbiao, “Conditional gene-trap mutagenesis in Zebrafish methods,” Mol. Biol. 1101, 393–411 (2014).

Nat. Genet. (1)

W. C. Skarnes, H. von Melchner, W. Wurst, G. Hicks, A. S. Nord, T. Cox, S. G. Young, P. Ruiz, P. Soriano, M. Tessier-Lavigne, B. R. Conklin, W. L. Stanford, J. Rossant, and International Gene Trap Consortium, “A public gene trap resource for mouse functional genomics,” Nat. Genet. 36(6), 543–544 (2004).
[Crossref] [PubMed]

Nat. Methods (4)

M. Mickoleit, B. Schmid, M. Weber, F. O. Fahrbach, S. Hombach, S. Reischauer, and J. Huisken, “High-resolution reconstruction of the beating zebrafish heart,” Nat. Methods 11(9), 919–922 (2014).
[Crossref] [PubMed]

T. A. Planchon, L. Gao, D. E. Milkie, M. W. Davidson, J. A. Galbraith, C. G. Galbraith, and E. Betzig, “Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination,” Nat. Methods 8(5), 417–423 (2011).
[Crossref] [PubMed]

T. V. Truong, W. Supatto, D. S. Koos, J. M. Choi, and S. E. Fraser, “Deep and fast live imaging with two-photon scanned light-sheet microscopy,” Nat. Methods 8(9), 757–760 (2011).
[Crossref] [PubMed]

P. Mahou, J. Vermot, E. Beaurepaire, and W. Supatto, “Multicolor two-photon light-sheet microscopy,” Nat. Methods 11(6), 600–601 (2014).
[Crossref] [PubMed]

Nat. Rev. Genet. (2)

W. L. Stanford, J. B. Cohn, and S. P. Cordes, “Gene-trap mutagenesis: past, present and beyond,” Nat. Rev. Genet. 2(10), 756–768 (2001).
[Crossref] [PubMed]

D. Y. Stainier, “Zebrafish genetics and vertebrate heart formation,” Nat. Rev. Genet. 2(1), 39–48 (2001).
[Crossref] [PubMed]

Nature (1)

J. R. Hove, R. W. Köster, A. S. Forouhar, G. Acevedo-Bolton, S. E. Fraser, and M. Gharib, “Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis,” Nature 421(6919), 172–177 (2003).
[Crossref] [PubMed]

Opt. Express (1)

Organogenesis (1)

J. Ohn, H. J. Tsai, and M. Liebling, “Joint dynamic imaging of morphogenesis and function in the developing heart,” Organogenesis 5(4), 248–255 (2009).
[Crossref] [PubMed]

Proc. Natl. Acad. Sci. U.S.A. (1)

A. D. Aguirre, C. Vinegoni, M. Sebas, and R. Weissleder, “Intravital imaging of cardiac function at the single-cell level,” Proc. Natl. Acad. Sci. U.S.A. 111(31), 11257–11262 (2014).
[Crossref] [PubMed]

Science (1)

A. S. Forouhar, M. Liebling, A. Hickerson, A. Nasiraei-Moghaddam, H. J. Tsai, J. R. Hove, S. E. Fraser, M. E. Dickinson, and M. Gharib, “The embryonic vertebrate heart tube is a dynamic suction pump,” Science 312(5774), 751–753 (2006).
[Crossref] [PubMed]

Other (2)

M. Westerfield, “The zebrafish book,” University of Oregon Press, Eugene, OR (1994)

M. Liebling, J. Vermot, A. S. Forouhar, M. Gharib, M. E. Dickinson, and S. E. Fraser, “Nonuniform temporal alignment of slice sequences for four-dimensional imaging of cyclically deforming embryonic structures,” Proceedings of the 3rd IEEE International Symposium on Biomedical Imaging: Macro to Nano (ISBI'06), Arlington, VA, USA, April 6–9, 1156–1159 (2006)
[Crossref]

Supplementary Material (7)

» Media 1: MOV (4094 KB)     
» Media 2: MOV (1960 KB)     
» Media 3: MOV (2731 KB)     
» Media 4: MOV (720 KB)     
» Media 5: MOV (2165 KB)     
» Media 6: MOV (2413 KB)     
» Media 7: MOV (6693 KB)     

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Figures (5)

Fig. 1
Fig. 1 Live 4D imaging of the embryonic heart with 2-photon light sheet microscopy. (A) Schematic of the orthogonal illumination and detection pathways of the imaging setup. (B) Successive movies of the beating heart were collected with the light sheet parked at different z positions. (C) Schematic overview of the retrospective synchronization algorithm using the movies collected at successive z positions. Time points t1, t2…, tM denote distinct states of contractions of the heart as captured by our imaging protocol. (D) The FlipTrap vector inserts a Citrine coding sequence (green) into the intron of genes randomly. Active expression of a trapped gene leads to splicing of the citrine exon, yielding full-length fluorescent fusion protein expressed at endogenous level in the embryo. Bottom: wide field fluorescent image of Gt(Tpm4-citrine)ct31a /+. (E) 3D-rendered view of a single time point in the 4D reconstructed image series of the beating heart (transgenic line Gt(Tpm4-citrine)ct31a /+ at 84 hpf). See Media 1 and Media 2 for the full 4D depiction of the reconstructed image series. The fluorescent fusion construct labels the cytoplasm of myocardial cells. The arrows indicate nuclei visible by negative contrast, in different cross-sections, demonstrating the quality of resolution achieved with our 2p light sheet imaging. Trabeculating myocardium (arrowhead) can be easily visualized owing to the image quality and synchronization efficiency.

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Fig. 2
Fig. 2 Photobleaching of the sample. For a typical movie of the beating heart at a certain z-depth (A), the normalized signal intensity integrated over the entire image is plotted as a function of time (B). The periodic time-structure of the signal intensity comes from the beating of the heart, as different parts of the heart periodically crossed the imaging focal plane. Dashed black line segments show the signal intensity averaged over the time window of one local maximum to the next, revealing a decrease of ~35% over the first ~1 second, and remaining nearly constant after that. We use the near-constant intensity portion of each movie for subsequent image processing and reconstruction.

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Fig. 3
Fig. 3 Characterization of imaging performance of 1p-SPIM and 2p-SPIM. (A) Resolution estimates from imaging 170nm-diameter fluorescent beads embedded in agarose. Images show the maximum intensity projection (MIP) along the xy and xz planes, for the same bead imaged by the two modalities. Plot shows the signal line profiles along the axial z-axis (solid line) and lateral x-axis (dashed line) over the bead images, showing FWHM axial resolution of ~1.5 µm and lateral resolution of ~0.5 µm. (B, C) Comparison of penetration depth of 1p-SPIM and 2p-SPIM in imaging the heart of a 60-hpf transgenic zebrafish, Tg(kdrl:GFP) s843, where the endocardium cell layer is labeled with GFP. The heart beating was stopped with a high concentration of anesthetic, allowing conventional z-stack imaging to capture the 3D structure. (B) MIPs of the 2p-SPIM data set along the three principal Cartesian planes are shown to aid the visualization of the anatomy of the heart. (C) Orthogonal views of the 3D data sets, showing single image slices at particular planes (designated by dashed green lines in the central image panels), to demonstrate the penetration depth of 1p-SPIM and 2p-SPIM. 3D images were taken with either uni-directional (light sheet coming from side 1 or side 2) or bidirectional (light sheets coming from both sides simultaneously) excitation. To facilitate fair comparison between the two imaging modalities, best effort was made to show the same planes within the heart for each data set (with the constraint that the live sample did shift slightly between data sets), with linear display contrast minimum and maximum set equal to the minimum and maximum pixel value, respectively, in each of the presented image slice. Overall, we see that 1p-SPIM and 2p-SPIM performs equally well in resolving the endocardium wall closer to the outer surface of the embryo, but 2p-SPIM performs better at capturing cardiac structures deeper inside the animal, as highlighted by structures marked with green arrowheads.

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Fig. 4
Fig. 4 Results of 4D capture of the beating heart. (A-D) Fluorescent images of the heart in different transgenic lines at representative time points during its beating cycle. Images are from a single optical section in (A) Gt(Tpm4-citrine)ct31a /+ and (C) Tg(kdrl:GFP)s843. (B) 3D-rendered images of Tg(kdrl:GFP) s843 heart, at 84 hours post-fertilization (hpf), from two viewing angles demonstrating the resolution achieved with 2p-SPIM. (D) 3D rendered image of an Ct(ctnna-citrine)ct3a/+ embryonic heart at 84 hpf permits visualization of cellular boundaries at two time points in the heart beating cycle. The high image quality allows segmentation of cells through the entire cardiac cycle. (E) Endocardial cells in Tg(kdrl:GFP) s843, when tracked over time (right), return to their initial position (due to periodicity of the heart motion), verifying the accuracy of the reconstruction algorithm. (F) Iso-surface rendering of Gt(Tpm4-citrine)ct31a /+ at 84 hpf and digitally cropped showing the heart tubular topology, shown in 2 different time points during the beating. The surface morphology of the inside of the myocardium is clearly visualized, revealing the trabeculating ventricle. Movie versions of the data sets shown in (A-F) are found in Media 1, Media 2, Media 3, Media 4, Media 5, Media 6, and Media 7.

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Fig. 5
Fig. 5 (A) Trabeculating myocardium during cardiac beating cycle. Optical sections of the reconstructed beating heart of the transgenic line Gt(Tpm4-citrine) Gt31a /+, at 84 hpf, shown at 4 distinct time points during the beating cycle, and at 2 different z-sections. The fluorescent fusion construct labels the cytoplasm of myocardial cells. The arrows indicate the spongiform structure (trabeculae) formed by the inner lining of the ventricular myocardium. The nuclei are visible by negative contrast, in different cross-sections. (B) Iso-surface rendering of the same reconstructed data set, shown at 4 distinct phase points and digitally cropped showing that the heart remains topologically equivalent to the cylindroid it started as. Not only can trabeculating ventricle be easily seen in the isosurface view but also the surface morphology of the inside of the myocardium is clearly visualized.

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Tables (1)

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Table 1 Imaging parameters for all the presented data

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