Abstract

We established a four-dimensional (4D) microscopy method using structured illumination for optical axial imaging with an electrically tunable lens. With its fast imaging capability, the dynamics of the cardiovascular system of the zebrafish and cerebral vessels were imaged based on the coverage of two stacks (25 layers) per second with lateral /axial resolutions of 0.6 µm and 1.8 µm, respectively. Time lapse imaging clearly shows the contractile–relaxation response of the beating heart at different cardiac phases and with different mobilities of blood vessels in different regions. This new 4D technique will facilitate in vivo imaging of organ function, generation, as well as drug responses in small-sized animals.

© 2020 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2019 (1)

2018 (1)

D. Li, W. Xue, M. Li, M. Dong, J. Wang, X. Wang, X. Li, K. Chen, W. Zhang, and S. Wu, “VCAM-1 + macrophages guide the homing of HSPCs to a vascular niche,” Nature 564(7734), 119–124 (2018).
[Crossref]

2017 (1)

2016 (2)

L. Andrés-Delgado, M. Peralta, N. Mercader, and J. Ripoll, “Dynamic focusing in the zebrafish beating heart,” Proc. SPIE 9717, 971717 (2016).
[Crossref]

K. Ando, S. Fukuhara, N. Izumi, H. Nakajima, H. Fukui, R. N. Kelsh, and N. Mochizuki, “Clarification of mural cell coverage of vascular endothelial cells by live imaging of zebrafish,” Development 143(8), 1328–1339 (2016).
[Crossref]

2015 (4)

D. Li, L. Shao, B. C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “ADVANCED IMAGING. Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref]

R. Galland, G. Grenci, A. Aravind, V. Viasnoff, V. Studer, and J.-B. Sibarita, “3D high-and super-resolution imaging using single-objective SPIM,” Nat. Methods 12(7), 641–644 (2015).
[Crossref]

F. Ströhl and C. F. Kaminski, “A joint Richardson-Lucy deconvolution algorithm for the reconstruction of multifocal structured illumination microscopy data,” Methods Appl. Fluoresc. 3(1), 014002 (2015).
[Crossref]

J. Qian, M. Lei, D. Dan, B. Yao, X. Zhou, Y. Yang, S. H. Yan, J. W. Min, and X. H. Yu, “Full-color structured illumination optical sectioning microscopy,” Sci. Rep. 5(1), 14513 (2015).
[Crossref]

2014 (2)

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. Wu, J.-A. Hammer, and Z. Liu, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref]

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]

2013 (3)

E. Kochhan, A. Lenard, E. Ellertsdottir, L. Herwig, M. Affolter, H.-G. Belting, and A.-F. Siekmann, “Blood flow changes coincide with cellular rearrangements during blood vessel pruning in zebrafish embryos,” PLoS One 8(10), e75060 (2013).
[Crossref]

D. Dan, M. Lei, B. Yao, W. Wang, M. Winterhalder, A. Zumbusch, Y. Qi, L. Xia, S. Yan, Y. Yang, P. Gao, T. Ye, and W. Zhao, “DMD-based LED-illumination super-resolution and optical sectioning microscopy,” Sci. Rep. 3(1), 1116 (2013).
[Crossref]

C. Zuo, Q. Chen, W. Qu, and A. Asundi, “High-speed transport-of-intensity phase microscopy with an electrically tunable lens,” Opt. Express 21(20), 24060–24075 (2013).
[Crossref]

2012 (4)

T. N. Ford, D. Lim, and J. Mertz, “Fast optically sectioned fluorescence HiLo endomicroscopy,” J. Biomed. Opt. 17(2), 021105 (2012).
[Crossref]

K. S. Okuda, J. W. Astin, J. P. Misa, M. V. Flores, K. E. Crosier, and P. S. Crosier, “Lyve1 expression reveals novel lymphatic vessels and new mechanisms for lymphatic vessel development in zebrafish,” Development 139(13), 2381–2391 (2012).
[Crossref]

M. Arigovindan, J. W. Sedat, and D. A. Agard, “Effect of depth dependent spherical aberrations in 3D structured illumination microscopy,” Opt. Express 20(6), 6527–6541 (2012).
[Crossref]

L. Gao, L. Shao, C. D. Higgins, J. S. Poulton, M. Peifer, M. W. Davidson, X. Wu, B. Goldstein, and E. Betzig, “Noninvasive imaging beyond the diffraction limit of 3D dynamics in thickly fluorescent specimens,” Cell 151(6), 1370–1385 (2012).
[Crossref]

2011 (3)

2010 (1)

K. Wicker and R. Heintzmann, “Single-shot optical sectioning using polarization-coded structured illumination,” J. Opt. 12(8), 084010 (2010).
[Crossref]

2009 (1)

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J Biomed Opt. 14(3), 030502 (2009).
[Crossref]

2008 (1)

2007 (2)

2006 (3)

L. D. Covassin, J. A. Villefranc, M. C. Kacergis, B. M. Weinstein, and N. D. Lawson, “Distinct genetic interactions between multiple Vegf receptors are required for development of different blood vessel types in zebrafish,” Proc. Natl. Acad. Sci. 103(17), 6554–6559 (2006).
[Crossref]

K. Yaniv, S. Isogai, D. Castranova, L. Dye, J. Hitomi, and B. M. Weinstein, “Live imaging of lymphatic development in the zebrafish,” Nat. Med. 12(6), 711–716 (2006).
[Crossref]

H. Bauch and J. Schaffer, “Optical sections by means of “structured illumination”: background and application in fluorescence microscopy,” Photonik Int 5, 86–88 (2006).

2005 (2)

J.-A. Conchello and J. W. Lichtman, “Optical sectioning microscopy,” Nat. Methods 2(12), 920–931 (2005).
[Crossref]

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
[Crossref]

2001 (1)

S. Isogai, M. Horiguchi, and B. M. Weinstein, “The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development,” Dev. Biol. 230(2), 278–301 (2001).
[Crossref]

1998 (1)

M. Neil, R. Juškaitis, and T. Wilson, “Real time 3D fluorescence microscopy by two beam interference illumination,” Opt. Commun. 153(1-3), 1–4 (1998).
[Crossref]

1997 (1)

1996 (1)

D. G. Ransom, P. Haffter, J. Odenthal, A. Brownlie, E. Vogelsang, R. N. Kelsh, M. Van Eeden, F. J. Furutani-Seiki, and M. Makoto Granato, “Characterization of zebrafish mutants with defects in embryonic hematopoiesis,” Development 123, 311–319 (1996).

1993 (1)

A. H. Voie, D. Burns, and F. Spelman, “Orthogonal-plane fluorescence optical sectioning: three - dimensional imaging of macroscopic biological specimens,” J. Microsc. 170(3), 229–236 (1993).
[Crossref]

Affolter, M.

E. Kochhan, A. Lenard, E. Ellertsdottir, L. Herwig, M. Affolter, H.-G. Belting, and A.-F. Siekmann, “Blood flow changes coincide with cellular rearrangements during blood vessel pruning in zebrafish embryos,” PLoS One 8(10), e75060 (2013).
[Crossref]

Agard, D. A.

Ando, K.

K. Ando, S. Fukuhara, N. Izumi, H. Nakajima, H. Fukui, R. N. Kelsh, and N. Mochizuki, “Clarification of mural cell coverage of vascular endothelial cells by live imaging of zebrafish,” Development 143(8), 1328–1339 (2016).
[Crossref]

Andrés-Delgado, L.

L. Andrés-Delgado, M. Peralta, N. Mercader, and J. Ripoll, “Dynamic focusing in the zebrafish beating heart,” Proc. SPIE 9717, 971717 (2016).
[Crossref]

Aravind, A.

R. Galland, G. Grenci, A. Aravind, V. Viasnoff, V. Studer, and J.-B. Sibarita, “3D high-and super-resolution imaging using single-objective SPIM,” Nat. Methods 12(7), 641–644 (2015).
[Crossref]

Arigovindan, M.

Astin, J. W.

K. S. Okuda, J. W. Astin, J. P. Misa, M. V. Flores, K. E. Crosier, and P. S. Crosier, “Lyve1 expression reveals novel lymphatic vessels and new mechanisms for lymphatic vessel development in zebrafish,” Development 139(13), 2381–2391 (2012).
[Crossref]

Asundi, A.

Baird, M. A.

D. Li, L. Shao, B. C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “ADVANCED IMAGING. Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref]

Barberis, A.

Bartoo, A. C.

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J Biomed Opt. 14(3), 030502 (2009).
[Crossref]

Bauch, H.

H. Bauch and J. Schaffer, “Optical sections by means of “structured illumination”: background and application in fluorescence microscopy,” Photonik Int 5, 86–88 (2006).

Beach, J. R.

D. Li, L. Shao, B. C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “ADVANCED IMAGING. Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref]

Belisle, J. M.

Belting, H.-G.

E. Kochhan, A. Lenard, E. Ellertsdottir, L. Herwig, M. Affolter, H.-G. Belting, and A.-F. Siekmann, “Blood flow changes coincide with cellular rearrangements during blood vessel pruning in zebrafish embryos,” PLoS One 8(10), e75060 (2013).
[Crossref]

Betzig, E.

D. Li, L. Shao, B. C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “ADVANCED IMAGING. Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref]

L. Gao, L. Shao, C. D. Higgins, J. S. Poulton, M. Peifer, M. W. Davidson, X. Wu, B. Goldstein, and E. Betzig, “Noninvasive imaging beyond the diffraction limit of 3D dynamics in thickly fluorescent specimens,” Cell 151(6), 1370–1385 (2012).
[Crossref]

Booth, M. J.

Botcherby, E. J.

Bozinovic, N.

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J Biomed Opt. 14(3), 030502 (2009).
[Crossref]

Brownlie, A.

D. G. Ransom, P. Haffter, J. Odenthal, A. Brownlie, E. Vogelsang, R. N. Kelsh, M. Van Eeden, F. J. Furutani-Seiki, and M. Makoto Granato, “Characterization of zebrafish mutants with defects in embryonic hematopoiesis,” Development 123, 311–319 (1996).

Burns, D.

A. H. Voie, D. Burns, and F. Spelman, “Orthogonal-plane fluorescence optical sectioning: three - dimensional imaging of macroscopic biological specimens,” J. Microsc. 170(3), 229–236 (1993).
[Crossref]

Castranova, D.

K. Yaniv, S. Isogai, D. Castranova, L. Dye, J. Hitomi, and B. M. Weinstein, “Live imaging of lymphatic development in the zebrafish,” Nat. Med. 12(6), 711–716 (2006).
[Crossref]

Cha, Y. R.

Y. R. Cha and B. M. Weinstein, “Visualization and experimental analysis of blood vessel formation using transgenic zebrafish,” Birth Defects Res., Part C 81(4), 286–296 (2007).
[Crossref]

Chen, B. C.

D. Li, L. Shao, B. C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “ADVANCED IMAGING. Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref]

Chen, B.-C.

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. Wu, J.-A. Hammer, and Z. Liu, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref]

Chen, K.

D. Li, W. Xue, M. Li, M. Dong, J. Wang, X. Wang, X. Li, K. Chen, W. Zhang, and S. Wu, “VCAM-1 + macrophages guide the homing of HSPCs to a vascular niche,” Nature 564(7734), 119–124 (2018).
[Crossref]

Chen, Q.

Chu, K. K.

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J Biomed Opt. 14(3), 030502 (2009).
[Crossref]

Conchello, J.-A.

J.-A. Conchello and J. W. Lichtman, “Optical sectioning microscopy,” Nat. Methods 2(12), 920–931 (2005).
[Crossref]

Costantino, S.

Covassin, L. D.

L. D. Covassin, J. A. Villefranc, M. C. Kacergis, B. M. Weinstein, and N. D. Lawson, “Distinct genetic interactions between multiple Vegf receptors are required for development of different blood vessel types in zebrafish,” Proc. Natl. Acad. Sci. 103(17), 6554–6559 (2006).
[Crossref]

Crosier, K. E.

K. S. Okuda, J. W. Astin, J. P. Misa, M. V. Flores, K. E. Crosier, and P. S. Crosier, “Lyve1 expression reveals novel lymphatic vessels and new mechanisms for lymphatic vessel development in zebrafish,” Development 139(13), 2381–2391 (2012).
[Crossref]

Crosier, P. S.

K. S. Okuda, J. W. Astin, J. P. Misa, M. V. Flores, K. E. Crosier, and P. S. Crosier, “Lyve1 expression reveals novel lymphatic vessels and new mechanisms for lymphatic vessel development in zebrafish,” Development 139(13), 2381–2391 (2012).
[Crossref]

Dan, D.

J. Qian, M. Lei, D. Dan, B. Yao, X. Zhou, Y. Yang, S. H. Yan, J. W. Min, and X. H. Yu, “Full-color structured illumination optical sectioning microscopy,” Sci. Rep. 5(1), 14513 (2015).
[Crossref]

D. Dan, M. Lei, B. Yao, W. Wang, M. Winterhalder, A. Zumbusch, Y. Qi, L. Xia, S. Yan, Y. Yang, P. Gao, T. Ye, and W. Zhao, “DMD-based LED-illumination super-resolution and optical sectioning microscopy,” Sci. Rep. 3(1), 1116 (2013).
[Crossref]

Davidson, M. W.

D. Li, L. Shao, B. C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “ADVANCED IMAGING. Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref]

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. Wu, J.-A. Hammer, and Z. Liu, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref]

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B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. Wu, J.-A. Hammer, and Z. Liu, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref]

L. Gao, L. Shao, C. D. Higgins, J. S. Poulton, M. Peifer, M. W. Davidson, X. Wu, B. Goldstein, and E. Betzig, “Noninvasive imaging beyond the diffraction limit of 3D dynamics in thickly fluorescent specimens,” Cell 151(6), 1370–1385 (2012).
[Crossref]

Sibarita, J.-B.

R. Galland, G. Grenci, A. Aravind, V. Viasnoff, V. Studer, and J.-B. Sibarita, “3D high-and super-resolution imaging using single-objective SPIM,” Nat. Methods 12(7), 641–644 (2015).
[Crossref]

Siekmann, A.-F.

E. Kochhan, A. Lenard, E. Ellertsdottir, L. Herwig, M. Affolter, H.-G. Belting, and A.-F. Siekmann, “Blood flow changes coincide with cellular rearrangements during blood vessel pruning in zebrafish embryos,” PLoS One 8(10), e75060 (2013).
[Crossref]

Singh, K.

Singh, S. K.

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J Biomed Opt. 14(3), 030502 (2009).
[Crossref]

Spelman, F.

A. H. Voie, D. Burns, and F. Spelman, “Orthogonal-plane fluorescence optical sectioning: three - dimensional imaging of macroscopic biological specimens,” J. Microsc. 170(3), 229–236 (1993).
[Crossref]

St Croix, C. M.

S. C. Watkins, S. Maniar, M. Mosher, B. L. Roman, M. Tsang, and C. M. St Croix, “High resolution imaging of vascular function in zebrafish,” PloS One7(8), e44018 (2012).
[Crossref]

Stelzer, E. H.

P. J. Keller, A. D. Schmidt, J. Wittbrodt, and E. H. Stelzer, “Digital scanned laser light-sheet fluorescence microscopy (DSLM) of zebrafish and Drosophila embryonic development,” Cold Spring Harbor Protocols 2011(10), pdb.prot065839 (2011).
[Crossref]

Ströhl, F.

F. Ströhl and C. F. Kaminski, “A joint Richardson-Lucy deconvolution algorithm for the reconstruction of multifocal structured illumination microscopy data,” Methods Appl. Fluoresc. 3(1), 014002 (2015).
[Crossref]

Studer, V.

R. Galland, G. Grenci, A. Aravind, V. Viasnoff, V. Studer, and J.-B. Sibarita, “3D high-and super-resolution imaging using single-objective SPIM,” Nat. Methods 12(7), 641–644 (2015).
[Crossref]

Tsang, M.

S. C. Watkins, S. Maniar, M. Mosher, B. L. Roman, M. Tsang, and C. M. St Croix, “High resolution imaging of vascular function in zebrafish,” PloS One7(8), e44018 (2012).
[Crossref]

Van Eeden, M.

D. G. Ransom, P. Haffter, J. Odenthal, A. Brownlie, E. Vogelsang, R. N. Kelsh, M. Van Eeden, F. J. Furutani-Seiki, and M. Makoto Granato, “Characterization of zebrafish mutants with defects in embryonic hematopoiesis,” Development 123, 311–319 (1996).

van’t Hoff, M.

Viasnoff, V.

R. Galland, G. Grenci, A. Aravind, V. Viasnoff, V. Studer, and J.-B. Sibarita, “3D high-and super-resolution imaging using single-objective SPIM,” Nat. Methods 12(7), 641–644 (2015).
[Crossref]

Villefranc, J. A.

L. D. Covassin, J. A. Villefranc, M. C. Kacergis, B. M. Weinstein, and N. D. Lawson, “Distinct genetic interactions between multiple Vegf receptors are required for development of different blood vessel types in zebrafish,” Proc. Natl. Acad. Sci. 103(17), 6554–6559 (2006).
[Crossref]

Vogelsang, E.

D. G. Ransom, P. Haffter, J. Odenthal, A. Brownlie, E. Vogelsang, R. N. Kelsh, M. Van Eeden, F. J. Furutani-Seiki, and M. Makoto Granato, “Characterization of zebrafish mutants with defects in embryonic hematopoiesis,” Development 123, 311–319 (1996).

Voie, A. H.

A. H. Voie, D. Burns, and F. Spelman, “Orthogonal-plane fluorescence optical sectioning: three - dimensional imaging of macroscopic biological specimens,” J. Microsc. 170(3), 229–236 (1993).
[Crossref]

Voigt, F. F.

Wang, J.

D. Li, W. Xue, M. Li, M. Dong, J. Wang, X. Wang, X. Li, K. Chen, W. Zhang, and S. Wu, “VCAM-1 + macrophages guide the homing of HSPCs to a vascular niche,” Nature 564(7734), 119–124 (2018).
[Crossref]

Wang, K.

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. Wu, J.-A. Hammer, and Z. Liu, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref]

Wang, W.

D. Dan, M. Lei, B. Yao, W. Wang, M. Winterhalder, A. Zumbusch, Y. Qi, L. Xia, S. Yan, Y. Yang, P. Gao, T. Ye, and W. Zhao, “DMD-based LED-illumination super-resolution and optical sectioning microscopy,” Sci. Rep. 3(1), 1116 (2013).
[Crossref]

Wang, X.

D. Li, W. Xue, M. Li, M. Dong, J. Wang, X. Wang, X. Li, K. Chen, W. Zhang, and S. Wu, “VCAM-1 + macrophages guide the homing of HSPCs to a vascular niche,” Nature 564(7734), 119–124 (2018).
[Crossref]

Watkins, S. C.

S. C. Watkins, S. Maniar, M. Mosher, B. L. Roman, M. Tsang, and C. M. St Croix, “High resolution imaging of vascular function in zebrafish,” PloS One7(8), e44018 (2012).
[Crossref]

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]

Weinstein, B. M.

Y. R. Cha and B. M. Weinstein, “Visualization and experimental analysis of blood vessel formation using transgenic zebrafish,” Birth Defects Res., Part C 81(4), 286–296 (2007).
[Crossref]

L. D. Covassin, J. A. Villefranc, M. C. Kacergis, B. M. Weinstein, and N. D. Lawson, “Distinct genetic interactions between multiple Vegf receptors are required for development of different blood vessel types in zebrafish,” Proc. Natl. Acad. Sci. 103(17), 6554–6559 (2006).
[Crossref]

K. Yaniv, S. Isogai, D. Castranova, L. Dye, J. Hitomi, and B. M. Weinstein, “Live imaging of lymphatic development in the zebrafish,” Nat. Med. 12(6), 711–716 (2006).
[Crossref]

S. Isogai, M. Horiguchi, and B. M. Weinstein, “The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development,” Dev. Biol. 230(2), 278–301 (2001).
[Crossref]

Wicker, K.

K. Wicker and R. Heintzmann, “Single-shot optical sectioning using polarization-coded structured illumination,” J. Opt. 12(8), 084010 (2010).
[Crossref]

Wilson, T.

Winterhalder, M.

D. Dan, M. Lei, B. Yao, W. Wang, M. Winterhalder, A. Zumbusch, Y. Qi, L. Xia, S. Yan, Y. Yang, P. Gao, T. Ye, and W. Zhao, “DMD-based LED-illumination super-resolution and optical sectioning microscopy,” Sci. Rep. 3(1), 1116 (2013).
[Crossref]

Wittbrodt, J.

P. J. Keller, A. D. Schmidt, J. Wittbrodt, and E. H. Stelzer, “Digital scanned laser light-sheet fluorescence microscopy (DSLM) of zebrafish and Drosophila embryonic development,” Cold Spring Harbor Protocols 2011(10), pdb.prot065839 (2011).
[Crossref]

Wu, S.

D. Li, W. Xue, M. Li, M. Dong, J. Wang, X. Wang, X. Li, K. Chen, W. Zhang, and S. Wu, “VCAM-1 + macrophages guide the homing of HSPCs to a vascular niche,” Nature 564(7734), 119–124 (2018).
[Crossref]

Wu, X.

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. Wu, J.-A. Hammer, and Z. Liu, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref]

L. Gao, L. Shao, C. D. Higgins, J. S. Poulton, M. Peifer, M. W. Davidson, X. Wu, B. Goldstein, and E. Betzig, “Noninvasive imaging beyond the diffraction limit of 3D dynamics in thickly fluorescent specimens,” Cell 151(6), 1370–1385 (2012).
[Crossref]

Xia, L.

D. Dan, M. Lei, B. Yao, W. Wang, M. Winterhalder, A. Zumbusch, Y. Qi, L. Xia, S. Yan, Y. Yang, P. Gao, T. Ye, and W. Zhao, “DMD-based LED-illumination super-resolution and optical sectioning microscopy,” Sci. Rep. 3(1), 1116 (2013).
[Crossref]

Xu, P.

D. Li, L. Shao, B. C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “ADVANCED IMAGING. Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref]

Xue, W.

D. Li, W. Xue, M. Li, M. Dong, J. Wang, X. Wang, X. Li, K. Chen, W. Zhang, and S. Wu, “VCAM-1 + macrophages guide the homing of HSPCs to a vascular niche,” Nature 564(7734), 119–124 (2018).
[Crossref]

Yan, S.

D. Dan, M. Lei, B. Yao, W. Wang, M. Winterhalder, A. Zumbusch, Y. Qi, L. Xia, S. Yan, Y. Yang, P. Gao, T. Ye, and W. Zhao, “DMD-based LED-illumination super-resolution and optical sectioning microscopy,” Sci. Rep. 3(1), 1116 (2013).
[Crossref]

Yan, S. H.

J. Qian, M. Lei, D. Dan, B. Yao, X. Zhou, Y. Yang, S. H. Yan, J. W. Min, and X. H. Yu, “Full-color structured illumination optical sectioning microscopy,” Sci. Rep. 5(1), 14513 (2015).
[Crossref]

Yang, Y.

J. Qian, M. Lei, D. Dan, B. Yao, X. Zhou, Y. Yang, S. H. Yan, J. W. Min, and X. H. Yu, “Full-color structured illumination optical sectioning microscopy,” Sci. Rep. 5(1), 14513 (2015).
[Crossref]

D. Dan, M. Lei, B. Yao, W. Wang, M. Winterhalder, A. Zumbusch, Y. Qi, L. Xia, S. Yan, Y. Yang, P. Gao, T. Ye, and W. Zhao, “DMD-based LED-illumination super-resolution and optical sectioning microscopy,” Sci. Rep. 3(1), 1116 (2013).
[Crossref]

Yaniv, K.

K. Yaniv, S. Isogai, D. Castranova, L. Dye, J. Hitomi, and B. M. Weinstein, “Live imaging of lymphatic development in the zebrafish,” Nat. Med. 12(6), 711–716 (2006).
[Crossref]

Yao, B.

J. Qian, M. Lei, D. Dan, B. Yao, X. Zhou, Y. Yang, S. H. Yan, J. W. Min, and X. H. Yu, “Full-color structured illumination optical sectioning microscopy,” Sci. Rep. 5(1), 14513 (2015).
[Crossref]

D. Dan, M. Lei, B. Yao, W. Wang, M. Winterhalder, A. Zumbusch, Y. Qi, L. Xia, S. Yan, Y. Yang, P. Gao, T. Ye, and W. Zhao, “DMD-based LED-illumination super-resolution and optical sectioning microscopy,” Sci. Rep. 3(1), 1116 (2013).
[Crossref]

Ye, T.

D. Dan, M. Lei, B. Yao, W. Wang, M. Winterhalder, A. Zumbusch, Y. Qi, L. Xia, S. Yan, Y. Yang, P. Gao, T. Ye, and W. Zhao, “DMD-based LED-illumination super-resolution and optical sectioning microscopy,” Sci. Rep. 3(1), 1116 (2013).
[Crossref]

Yu, X. H.

J. Qian, M. Lei, D. Dan, B. Yao, X. Zhou, Y. Yang, S. H. Yan, J. W. Min, and X. H. Yu, “Full-color structured illumination optical sectioning microscopy,” Sci. Rep. 5(1), 14513 (2015).
[Crossref]

Zhang, H.

Zhang, M.

D. Li, L. Shao, B. C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “ADVANCED IMAGING. Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref]

Zhang, W.

D. Li, W. Xue, M. Li, M. Dong, J. Wang, X. Wang, X. Li, K. Chen, W. Zhang, and S. Wu, “VCAM-1 + macrophages guide the homing of HSPCs to a vascular niche,” Nature 564(7734), 119–124 (2018).
[Crossref]

Zhang, X.

D. Li, L. Shao, B. C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “ADVANCED IMAGING. Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref]

Zhao, W.

D. Dan, M. Lei, B. Yao, W. Wang, M. Winterhalder, A. Zumbusch, Y. Qi, L. Xia, S. Yan, Y. Yang, P. Gao, T. Ye, and W. Zhao, “DMD-based LED-illumination super-resolution and optical sectioning microscopy,” Sci. Rep. 3(1), 1116 (2013).
[Crossref]

Zhou, X.

J. Qian, M. Lei, D. Dan, B. Yao, X. Zhou, Y. Yang, S. H. Yan, J. W. Min, and X. H. Yu, “Full-color structured illumination optical sectioning microscopy,” Sci. Rep. 5(1), 14513 (2015).
[Crossref]

Zumbusch, A.

D. Dan, M. Lei, B. Yao, W. Wang, M. Winterhalder, A. Zumbusch, Y. Qi, L. Xia, S. Yan, Y. Yang, P. Gao, T. Ye, and W. Zhao, “DMD-based LED-illumination super-resolution and optical sectioning microscopy,” Sci. Rep. 3(1), 1116 (2013).
[Crossref]

Zuo, C.

Žurauskas, M.

Biomed. Opt. Express (1)

Birth Defects Res., Part C (1)

Y. R. Cha and B. M. Weinstein, “Visualization and experimental analysis of blood vessel formation using transgenic zebrafish,” Birth Defects Res., Part C 81(4), 286–296 (2007).
[Crossref]

Cell (1)

L. Gao, L. Shao, C. D. Higgins, J. S. Poulton, M. Peifer, M. W. Davidson, X. Wu, B. Goldstein, and E. Betzig, “Noninvasive imaging beyond the diffraction limit of 3D dynamics in thickly fluorescent specimens,” Cell 151(6), 1370–1385 (2012).
[Crossref]

Cold Spring Harbor Protocols (1)

P. J. Keller, A. D. Schmidt, J. Wittbrodt, and E. H. Stelzer, “Digital scanned laser light-sheet fluorescence microscopy (DSLM) of zebrafish and Drosophila embryonic development,” Cold Spring Harbor Protocols 2011(10), pdb.prot065839 (2011).
[Crossref]

Dev. Biol. (1)

S. Isogai, M. Horiguchi, and B. M. Weinstein, “The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development,” Dev. Biol. 230(2), 278–301 (2001).
[Crossref]

Development (3)

K. S. Okuda, J. W. Astin, J. P. Misa, M. V. Flores, K. E. Crosier, and P. S. Crosier, “Lyve1 expression reveals novel lymphatic vessels and new mechanisms for lymphatic vessel development in zebrafish,” Development 139(13), 2381–2391 (2012).
[Crossref]

K. Ando, S. Fukuhara, N. Izumi, H. Nakajima, H. Fukui, R. N. Kelsh, and N. Mochizuki, “Clarification of mural cell coverage of vascular endothelial cells by live imaging of zebrafish,” Development 143(8), 1328–1339 (2016).
[Crossref]

D. G. Ransom, P. Haffter, J. Odenthal, A. Brownlie, E. Vogelsang, R. N. Kelsh, M. Van Eeden, F. J. Furutani-Seiki, and M. Makoto Granato, “Characterization of zebrafish mutants with defects in embryonic hematopoiesis,” Development 123, 311–319 (1996).

J Biomed Opt. (1)

S. Santos, K. K. Chu, D. Lim, N. Bozinovic, T. N. Ford, C. Hourtoule, A. C. Bartoo, S. K. Singh, and J. Mertz, “Optically sectioned fluorescence endomicroscopy with hybrid-illumination imaging through a flexible fiber bundle,” J Biomed Opt. 14(3), 030502 (2009).
[Crossref]

J. Biomed. Opt. (1)

T. N. Ford, D. Lim, and J. Mertz, “Fast optically sectioned fluorescence HiLo endomicroscopy,” J. Biomed. Opt. 17(2), 021105 (2012).
[Crossref]

J. Microsc. (1)

A. H. Voie, D. Burns, and F. Spelman, “Orthogonal-plane fluorescence optical sectioning: three - dimensional imaging of macroscopic biological specimens,” J. Microsc. 170(3), 229–236 (1993).
[Crossref]

J. Opt. (1)

K. Wicker and R. Heintzmann, “Single-shot optical sectioning using polarization-coded structured illumination,” J. Opt. 12(8), 084010 (2010).
[Crossref]

Methods Appl. Fluoresc. (1)

F. Ströhl and C. F. Kaminski, “A joint Richardson-Lucy deconvolution algorithm for the reconstruction of multifocal structured illumination microscopy data,” Methods Appl. Fluoresc. 3(1), 014002 (2015).
[Crossref]

Nat. Med. (1)

K. Yaniv, S. Isogai, D. Castranova, L. Dye, J. Hitomi, and B. M. Weinstein, “Live imaging of lymphatic development in the zebrafish,” Nat. Med. 12(6), 711–716 (2006).
[Crossref]

Nat. Methods (4)

J.-A. Conchello and J. W. Lichtman, “Optical sectioning microscopy,” Nat. Methods 2(12), 920–931 (2005).
[Crossref]

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
[Crossref]

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]

R. Galland, G. Grenci, A. Aravind, V. Viasnoff, V. Studer, and J.-B. Sibarita, “3D high-and super-resolution imaging using single-objective SPIM,” Nat. Methods 12(7), 641–644 (2015).
[Crossref]

Nature (1)

D. Li, W. Xue, M. Li, M. Dong, J. Wang, X. Wang, X. Li, K. Chen, W. Zhang, and S. Wu, “VCAM-1 + macrophages guide the homing of HSPCs to a vascular niche,” Nature 564(7734), 119–124 (2018).
[Crossref]

Opt. Commun. (1)

M. Neil, R. Juškaitis, and T. Wilson, “Real time 3D fluorescence microscopy by two beam interference illumination,” Opt. Commun. 153(1-3), 1–4 (1998).
[Crossref]

Opt. Express (5)

Opt. Lett. (1)

Optica (2)

Photonik Int (1)

H. Bauch and J. Schaffer, “Optical sections by means of “structured illumination”: background and application in fluorescence microscopy,” Photonik Int 5, 86–88 (2006).

PLoS One (1)

E. Kochhan, A. Lenard, E. Ellertsdottir, L. Herwig, M. Affolter, H.-G. Belting, and A.-F. Siekmann, “Blood flow changes coincide with cellular rearrangements during blood vessel pruning in zebrafish embryos,” PLoS One 8(10), e75060 (2013).
[Crossref]

Proc. Natl. Acad. Sci. (1)

L. D. Covassin, J. A. Villefranc, M. C. Kacergis, B. M. Weinstein, and N. D. Lawson, “Distinct genetic interactions between multiple Vegf receptors are required for development of different blood vessel types in zebrafish,” Proc. Natl. Acad. Sci. 103(17), 6554–6559 (2006).
[Crossref]

Proc. SPIE (1)

L. Andrés-Delgado, M. Peralta, N. Mercader, and J. Ripoll, “Dynamic focusing in the zebrafish beating heart,” Proc. SPIE 9717, 971717 (2016).
[Crossref]

Sci. Rep. (2)

D. Dan, M. Lei, B. Yao, W. Wang, M. Winterhalder, A. Zumbusch, Y. Qi, L. Xia, S. Yan, Y. Yang, P. Gao, T. Ye, and W. Zhao, “DMD-based LED-illumination super-resolution and optical sectioning microscopy,” Sci. Rep. 3(1), 1116 (2013).
[Crossref]

J. Qian, M. Lei, D. Dan, B. Yao, X. Zhou, Y. Yang, S. H. Yan, J. W. Min, and X. H. Yu, “Full-color structured illumination optical sectioning microscopy,” Sci. Rep. 5(1), 14513 (2015).
[Crossref]

Science (2)

B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. Wu, J.-A. Hammer, and Z. Liu, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346(6208), 1257998 (2014).
[Crossref]

D. Li, L. Shao, B. C. Chen, X. Zhang, M. Zhang, B. Moses, D. E. Milkie, J. R. Beach, J. A. Hammer, M. Pasham, T. Kirchhausen, M. A. Baird, M. W. Davidson, P. Xu, and E. Betzig, “ADVANCED IMAGING. Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics,” Science 349(6251), aab3500 (2015).
[Crossref]

Other (1)

S. C. Watkins, S. Maniar, M. Mosher, B. L. Roman, M. Tsang, and C. M. St Croix, “High resolution imaging of vascular function in zebrafish,” PloS One7(8), e44018 (2012).
[Crossref]

Supplementary Material (7)

NameDescription
» Visualization 1       Visualization of the vein in zebrafish cardiovascular
» Visualization 2       Visualization of the artery in zebrafish cardiovascular
» Visualization 3       The shape of the four components of the zebrafish cardiovascular
» Visualization 4       Cardiac images at different phases of the cardiac cycle
» Visualization 5       Reconstruction of zebrafish vessels in the head region
» Visualization 6       Optical sectioning SIM time-lapse recording of zebrafish vessels in the head region
» Visualization 7       Dynamic three-dimensional visualization of the intersegmental and peri-intestinal vessels in zebrafish

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Figures (6)

Fig. 1.
Fig. 1. (a) Schematic of the imaging system (DMD, digital micromirror device; L1,L2,L3, Optical Lenses; M1, M2, mirrors; DM, dichroic mirror; ETL, electrically tunable lens; OBJ, objective lens. The illustration in the upper right corner is a schematic view of the ETL. (b) Control sequence diagram of the system. FPGA output two signals to trigger the start of camera (light blue) and ETL focus change (red); DMD loads two opposite structural patterns at each plane and turned off between them; the green area represents the camera's read-out time while the yellow area represents the exposure time only when the DMD turned on; 8 ms is ETL settling time).
Fig. 2.
Fig. 2. Principle of the optical sectioning algorithm. (a) Flow chart of the algorithm. Three main steps consisting deconvolution, HiLo and inverted Gaussian attenuation were marked in different colors. (HP filter, high pass filter; LP filter, low pass filter; FT, Fourier transform; iFT, inverse Fourier transform). (b) Principle of inverted Gaussian attenuation to decrease the out-of-focus signal in spectrum domain. (WF, wide field). (c) Demonstration of the optical section capability with a pumpkin stem slices sample. Lower panel shows the normalized intensity along the dotted lines. (OS, optical sectioning image; Scale bar: 1 µm)
Fig. 3.
Fig. 3. Calibration of various system parameters. (a) Relationship between the focal plane position and the voltage for different objective lenses. (b) Relationship between the relative magnification and imaging depth with 40× objective. The magnification was characterized by measuring distances between two beads. (c) Evaluation of the spatial resolutions using 200 nm red fluorescent beads. Scale bar: 7 µm. (d) Enlarged image of fluorescent beads. Scale bar: 2 µm. (e) Axial images of the beads. Scale bar: 2 µm. (f, g) Fitted curves for grayscale values of horizontal and axial images.
Fig. 4.
Fig. 4. Images of the cardiovascular system of the zebrafish. (a) Two-dimensional (2D) zebrafish image with the use of a 4× objective lens, Scale bar: 200 µm. (b) Schematic of the heart of the zebrafish. The illustration in the upper right corner marks the location of the zebrafish heart. (c, d) Blood vessels connected to the heart. Scale bar: 10 µm. (e) Static heart image acquired with a 40× objective. Scale bar: 20 µm. (f-h) Cardiac images at different phases of the cardiac cycle. The yellow dotted line indicates the shape of the heart. Scale bar: 10 µm.
Fig. 5.
Fig. 5. Three-dimensional (3D) imaging of cerebral blood vessels in the zebrafish. (a) Vessel image acquired with a 40× objective lens (yellow box area shown in Fig. 4(a).) Scale bar: 20 µm. (b-d) Cross-sectional image at different time points in the yellow box in (a). The yellow arrows indicate the locations of the obvious movements. (e) Deep vascular imaging with a 40× objective lens, (green box area shown in Fig. 4(a)). Scale bar: 20 µm. (f) Depth-coding maximum intensity projection (MIP) images. Scale bar: 20 µm. (g) Quantitative measurement of vessel movement from the beginning to the end-time point, Scale bar: 2 µm.
Fig. 6.
Fig. 6. Intersegmental and peri-intestinal vessels. (a) White and yellow boxes indicate the intersegmental and peri-intestinal vessels, respectively. Scale bar: 20 µm. (b) 3D view of intersegmental vessel. (c) Images of the peri- intestinal blood vessels at two time points showing obvious movements. Scale bar: 20 µm.

Tables (1)

Tables Icon

Table 1. Parameters in Fig. 4–Fig. 6

Equations (6)

Equations on this page are rendered with MathJax. Learn more.

T i m e = E x p o s u r e _ t i m e × L a y e r s × 2 + R o w s × 7.74 u s × L a y e r s + 8 m s × L a y e r s ,
O T F = { π 2 [ c o s 1 ( k ) k 1 k 2 ] , | k | k c 0 , | k | k c
R ( k ) = F T [ 2 × r 1 / ( r 1 + r 2 ) ] ,
C ( x , y ) = [ R + ( x , y ) R + ( x , y ) ]   .
I h i l o ( x , y ) = I h p ( x , y ) + η I l p ( x , y ) = H P [ ( r 1 + r 2 ) / 2 ] + η L P [ R + ( x , y ) R + ( x , y ) × ( r 1 + r 2 ) / 2 ] ,
I o s = i F T [ F T ( I h i l o ) × G a u s s A t t ( a , σ 2 ) ] ,