Abstract

Zebrafish has rapidly evolved as a powerful vertebrate model organism for studying human diseases. Here we first demonstrate a new label-free approach for in vivo imaging of microvasculature, based on the recent discovery and detailed characterization of the two-photon excited endogenous fluorescence in the blood plasma of zebrafish. In particular, three-dimensional reconstruction of the microvascular networks was achieved with the depth-resolved two-photon excitation fluorescence (TPEF) imaging. Secondly, the blood flow images, obtained by perpendicularly scanning the focal point across the blood vessel, provided accurate information for characterizing the hemodynamics of the circulatory system. The endogenous fluorescent signals of reduced nicotinamide adenine dinucleotide (NADH) enabled visualization of the circulating granulocytes (neutrophils) in the blood vessel. The development of acute sterile inflammation could be detected by the quantitative counting of circulating neutrophils. Finally, we found that by utilizing a short wavelength excitation at 650 nm, the commonly used fluorescent proteins, such as GFP and DsRed, could be efficiently excited together with the endogenous fluorophores to achieve four-color TPEF imaging of the vascular structures and blood cells. The results demonstrated that the multi-color imaging could potentially yield multiple view angles of important processes in living biological systems.

© 2014 Optical Society of America

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2012 (3)

2011 (3)

W. Zheng, D. Li, Y. Zeng, Y. Luo, and J. Y. Qu, “Two-photon excited hemoglobin fluorescence,” Biomed. Opt. Express2(1), 71–79 (2011).
[CrossRef] [PubMed]

M. Drobizhev, N. S. Makarov, S. E. Tillo, T. E. Hughes, and A. Rebane, “Two-photon absorption properties of fluorescent proteins,” Nat. Methods8(5), 393–399 (2011).
[CrossRef] [PubMed]

V. V. Tuchin, A. Tárnok, and V. P. Zharov, “In vivo flow cytometry: A horizon of opportunities,” Cytometry A79(10), 737–745 (2011).
[CrossRef] [PubMed]

2010 (3)

O. J. Tamplin and L. I. Zon, “Fishing at the cellular level,” Nat. Methods7(8), 600–601 (2010).
[CrossRef] [PubMed]

D. A. Boas and A. K. Dunn, “Laser speckle contrast imaging in biomedical optics,” J. Biomed. Opt.15(1), 011109 (2010).
[CrossRef] [PubMed]

C. Li, R. K. Pastila, C. Pitsillides, J. M. Runnels, M. Puoris’haag, D. Côté, and C. P. Lin, “Imaging leukocyte trafficking in vivo with two-photon-excited endogenous tryptophan fluorescence,” Opt. Express18(2), 988–999 (2010).
[CrossRef] [PubMed]

2009 (3)

I. V. Larina, S. Ivers, S. Syed, M. E. Dickinson, and K. V. Larin, “Hemodynamic measurements from individual blood cells in early mammalian embryos with Doppler swept source OCT,” Opt. Lett.34(7), 986–988 (2009).
[CrossRef] [PubMed]

L. V. Wang, “Multiscale photoacoustic microscopy and computed tomography,” Nat. Photonics3(9), 503–509 (2009).
[CrossRef] [PubMed]

W. Min, S. Lu, S. Chong, R. Roy, G. R. Holtom, and X. S. Xie, “Imaging chromophores with undetectable fluorescence by stimulated emission microscopy,” Nature461(7267), 1105–1109 (2009).
[CrossRef] [PubMed]

2008 (3)

2007 (1)

H. Jin, J. Xu, and Z. Wen, “Migratory path of definitive hematopoietic stem/progenitor cells during zebrafish development,” Blood109(12), 5208–5214 (2007).
[CrossRef] [PubMed]

2006 (2)

E. Murayama, K. Kissa, A. Zapata, E. Mordelet, V. Briolat, H. F. Lin, R. I. Handin, and P. Herbomel, “Tracing Hematopoietic Precursor Migration to Successive Hematopoietic Organs during Zebrafish Development,” Immunity25(6), 963–975 (2006).
[CrossRef] [PubMed]

G. O. Clay, A. C. Millard, C. B. Schaffer, J. Aus-der-Au, P. S. Tsai, J. A. Squier, and D. Kleinfeld, “Spectroscopy of third-harmonic generation: Evidence for resonances in model compounds and ligated hemoglobin,” J. Opt. Soc. Am. B23(5), 932–950 (2006).
[CrossRef]

2003 (1)

D. M. McDonald and P. L. Choyke, “Imaging of angiogenesis: From microscope to clinic,” Nat. Med.9(6), 713–725 (2003).
[CrossRef] [PubMed]

2000 (1)

L. Greenbaum, C. Rothmann, R. Lavie, and Z. Malik, “Green fluorescent protein photobleaching: A model for protein damage by endogenous and exogenous singlet oxygen,” Biol. Chem.381(12), 1251–1258 (2000).
[CrossRef] [PubMed]

1998 (1)

D. B. Cines, E. S. Pollak, C. A. Buck, J. Loscalzo, G. A. Zimmerman, R. P. McEver, J. S. Pober, T. M. Wick, B. A. Konkle, B. S. Schwartz, E. S. Barnathan, K. R. McCrae, B. A. Hug, A. M. Schmidt, and D. M. Stern, “Endothelial cells in physiology and in the pathophysiology of vascular disorders,” Blood91(10), 3527–3561 (1998).
[PubMed]

1997 (1)

Z. Lele, S. Engel, and P. H. Krone, “hsp47 and hsp70 gene expression is differentially regulated in a stress- and tissue-specific manner in zebrafish embryos,” Dev. Genet.21(2), 123–133 (1997).
[CrossRef] [PubMed]

1996 (1)

1994 (1)

E. R. Gillan, R. D. Christensen, Y. Suen, R. Ellis, C. van de Ven, and M. S. Cairo, “A randomized, placebo-controlled trial of recombinant human granulocyte colony-stimulating factor administration in newborn infants with presumed sepsis: Significant induction of peripheral and bone marrow neutrophilia,” Blood84(5), 1427–1433 (1994).
[PubMed]

Aus-der-Au, J.

Barnathan, E. S.

D. B. Cines, E. S. Pollak, C. A. Buck, J. Loscalzo, G. A. Zimmerman, R. P. McEver, J. S. Pober, T. M. Wick, B. A. Konkle, B. S. Schwartz, E. S. Barnathan, K. R. McCrae, B. A. Hug, A. M. Schmidt, and D. M. Stern, “Endothelial cells in physiology and in the pathophysiology of vascular disorders,” Blood91(10), 3527–3561 (1998).
[PubMed]

Boas, D. A.

D. A. Boas and A. K. Dunn, “Laser speckle contrast imaging in biomedical optics,” J. Biomed. Opt.15(1), 011109 (2010).
[CrossRef] [PubMed]

Briolat, V.

E. Murayama, K. Kissa, A. Zapata, E. Mordelet, V. Briolat, H. F. Lin, R. I. Handin, and P. Herbomel, “Tracing Hematopoietic Precursor Migration to Successive Hematopoietic Organs during Zebrafish Development,” Immunity25(6), 963–975 (2006).
[CrossRef] [PubMed]

Buck, C. A.

D. B. Cines, E. S. Pollak, C. A. Buck, J. Loscalzo, G. A. Zimmerman, R. P. McEver, J. S. Pober, T. M. Wick, B. A. Konkle, B. S. Schwartz, E. S. Barnathan, K. R. McCrae, B. A. Hug, A. M. Schmidt, and D. M. Stern, “Endothelial cells in physiology and in the pathophysiology of vascular disorders,” Blood91(10), 3527–3561 (1998).
[PubMed]

Cairo, M. S.

E. R. Gillan, R. D. Christensen, Y. Suen, R. Ellis, C. van de Ven, and M. S. Cairo, “A randomized, placebo-controlled trial of recombinant human granulocyte colony-stimulating factor administration in newborn infants with presumed sepsis: Significant induction of peripheral and bone marrow neutrophilia,” Blood84(5), 1427–1433 (1994).
[PubMed]

Chen, Y. S.

Chia, J. S.

Chia, T. H.

Chong, S.

W. Min, S. Lu, S. Chong, R. Roy, G. R. Holtom, and X. S. Xie, “Imaging chromophores with undetectable fluorescence by stimulated emission microscopy,” Nature461(7267), 1105–1109 (2009).
[CrossRef] [PubMed]

Choyke, P. L.

D. M. McDonald and P. L. Choyke, “Imaging of angiogenesis: From microscope to clinic,” Nat. Med.9(6), 713–725 (2003).
[CrossRef] [PubMed]

Christensen, R. D.

E. R. Gillan, R. D. Christensen, Y. Suen, R. Ellis, C. van de Ven, and M. S. Cairo, “A randomized, placebo-controlled trial of recombinant human granulocyte colony-stimulating factor administration in newborn infants with presumed sepsis: Significant induction of peripheral and bone marrow neutrophilia,” Blood84(5), 1427–1433 (1994).
[PubMed]

Cines, D. B.

D. B. Cines, E. S. Pollak, C. A. Buck, J. Loscalzo, G. A. Zimmerman, R. P. McEver, J. S. Pober, T. M. Wick, B. A. Konkle, B. S. Schwartz, E. S. Barnathan, K. R. McCrae, B. A. Hug, A. M. Schmidt, and D. M. Stern, “Endothelial cells in physiology and in the pathophysiology of vascular disorders,” Blood91(10), 3527–3561 (1998).
[PubMed]

Clay, G. O.

Côté, D.

Dickinson, M. E.

Drobizhev, M.

M. Drobizhev, N. S. Makarov, S. E. Tillo, T. E. Hughes, and A. Rebane, “Two-photon absorption properties of fluorescent proteins,” Nat. Methods8(5), 393–399 (2011).
[CrossRef] [PubMed]

Dunn, A. K.

D. A. Boas and A. K. Dunn, “Laser speckle contrast imaging in biomedical optics,” J. Biomed. Opt.15(1), 011109 (2010).
[CrossRef] [PubMed]

Ellis, R.

E. R. Gillan, R. D. Christensen, Y. Suen, R. Ellis, C. van de Ven, and M. S. Cairo, “A randomized, placebo-controlled trial of recombinant human granulocyte colony-stimulating factor administration in newborn infants with presumed sepsis: Significant induction of peripheral and bone marrow neutrophilia,” Blood84(5), 1427–1433 (1994).
[PubMed]

Engel, S.

Z. Lele, S. Engel, and P. H. Krone, “hsp47 and hsp70 gene expression is differentially regulated in a stress- and tissue-specific manner in zebrafish embryos,” Dev. Genet.21(2), 123–133 (1997).
[CrossRef] [PubMed]

Gillan, E. R.

E. R. Gillan, R. D. Christensen, Y. Suen, R. Ellis, C. van de Ven, and M. S. Cairo, “A randomized, placebo-controlled trial of recombinant human granulocyte colony-stimulating factor administration in newborn infants with presumed sepsis: Significant induction of peripheral and bone marrow neutrophilia,” Blood84(5), 1427–1433 (1994).
[PubMed]

Greenbaum, L.

L. Greenbaum, C. Rothmann, R. Lavie, and Z. Malik, “Green fluorescent protein photobleaching: A model for protein damage by endogenous and exogenous singlet oxygen,” Biol. Chem.381(12), 1251–1258 (2000).
[CrossRef] [PubMed]

Handin, R. I.

E. Murayama, K. Kissa, A. Zapata, E. Mordelet, V. Briolat, H. F. Lin, R. I. Handin, and P. Herbomel, “Tracing Hematopoietic Precursor Migration to Successive Hematopoietic Organs during Zebrafish Development,” Immunity25(6), 963–975 (2006).
[CrossRef] [PubMed]

Herbomel, P.

E. Murayama, K. Kissa, A. Zapata, E. Mordelet, V. Briolat, H. F. Lin, R. I. Handin, and P. Herbomel, “Tracing Hematopoietic Precursor Migration to Successive Hematopoietic Organs during Zebrafish Development,” Immunity25(6), 963–975 (2006).
[CrossRef] [PubMed]

Holtom, G. R.

W. Min, S. Lu, S. Chong, R. Roy, G. R. Holtom, and X. S. Xie, “Imaging chromophores with undetectable fluorescence by stimulated emission microscopy,” Nature461(7267), 1105–1109 (2009).
[CrossRef] [PubMed]

Hsieh, T. Y.

Hug, B. A.

D. B. Cines, E. S. Pollak, C. A. Buck, J. Loscalzo, G. A. Zimmerman, R. P. McEver, J. S. Pober, T. M. Wick, B. A. Konkle, B. S. Schwartz, E. S. Barnathan, K. R. McCrae, B. A. Hug, A. M. Schmidt, and D. M. Stern, “Endothelial cells in physiology and in the pathophysiology of vascular disorders,” Blood91(10), 3527–3561 (1998).
[PubMed]

Hughes, T. E.

M. Drobizhev, N. S. Makarov, S. E. Tillo, T. E. Hughes, and A. Rebane, “Two-photon absorption properties of fluorescent proteins,” Nat. Methods8(5), 393–399 (2011).
[CrossRef] [PubMed]

Ivers, S.

Jin, H.

H. Jin, J. Xu, and Z. Wen, “Migratory path of definitive hematopoietic stem/progenitor cells during zebrafish development,” Blood109(12), 5208–5214 (2007).
[CrossRef] [PubMed]

Kissa, K.

E. Murayama, K. Kissa, A. Zapata, E. Mordelet, V. Briolat, H. F. Lin, R. I. Handin, and P. Herbomel, “Tracing Hematopoietic Precursor Migration to Successive Hematopoietic Organs during Zebrafish Development,” Immunity25(6), 963–975 (2006).
[CrossRef] [PubMed]

Kleinfeld, D.

Konkle, B. A.

D. B. Cines, E. S. Pollak, C. A. Buck, J. Loscalzo, G. A. Zimmerman, R. P. McEver, J. S. Pober, T. M. Wick, B. A. Konkle, B. S. Schwartz, E. S. Barnathan, K. R. McCrae, B. A. Hug, A. M. Schmidt, and D. M. Stern, “Endothelial cells in physiology and in the pathophysiology of vascular disorders,” Blood91(10), 3527–3561 (1998).
[PubMed]

Krone, P. H.

Z. Lele, S. Engel, and P. H. Krone, “hsp47 and hsp70 gene expression is differentially regulated in a stress- and tissue-specific manner in zebrafish embryos,” Dev. Genet.21(2), 123–133 (1997).
[CrossRef] [PubMed]

Larin, K. V.

Larina, I. V.

Lavie, R.

L. Greenbaum, C. Rothmann, R. Lavie, and Z. Malik, “Green fluorescent protein photobleaching: A model for protein damage by endogenous and exogenous singlet oxygen,” Biol. Chem.381(12), 1251–1258 (2000).
[CrossRef] [PubMed]

Lele, Z.

Z. Lele, S. Engel, and P. H. Krone, “hsp47 and hsp70 gene expression is differentially regulated in a stress- and tissue-specific manner in zebrafish embryos,” Dev. Genet.21(2), 123–133 (1997).
[CrossRef] [PubMed]

Levene, M. J.

Li, C.

Li, D.

Li, L.

Y. Zeng, J. Xu, D. Li, L. Li, Z. Wen, and J. Y. Qu, “Label-free in vivo flow cytometry in zebrafish using two-photon autofluorescence imaging,” Opt. Lett.37(13), 2490–2492 (2012).
[CrossRef] [PubMed]

L. Li, B. Yan, Y. Q. Shi, W. Q. Zhang, and Z. L. Wen, “Live imaging reveals differing roles of macrophages and neutrophils during zebrafish tail fin regeneration,” J. Biol. Chem.287(30), 25353–25360 (2012).
[CrossRef] [PubMed]

Lin, C. P.

Lin, H. F.

E. Murayama, K. Kissa, A. Zapata, E. Mordelet, V. Briolat, H. F. Lin, R. I. Handin, and P. Herbomel, “Tracing Hematopoietic Precursor Migration to Successive Hematopoietic Organs during Zebrafish Development,” Immunity25(6), 963–975 (2006).
[CrossRef] [PubMed]

Lin, W. L.

Liu, H. W.

Liu, T. M.

Loscalzo, J.

D. B. Cines, E. S. Pollak, C. A. Buck, J. Loscalzo, G. A. Zimmerman, R. P. McEver, J. S. Pober, T. M. Wick, B. A. Konkle, B. S. Schwartz, E. S. Barnathan, K. R. McCrae, B. A. Hug, A. M. Schmidt, and D. M. Stern, “Endothelial cells in physiology and in the pathophysiology of vascular disorders,” Blood91(10), 3527–3561 (1998).
[PubMed]

Lu, S.

W. Min, S. Lu, S. Chong, R. Roy, G. R. Holtom, and X. S. Xie, “Imaging chromophores with undetectable fluorescence by stimulated emission microscopy,” Nature461(7267), 1105–1109 (2009).
[CrossRef] [PubMed]

Luo, Y.

Makarov, N. S.

M. Drobizhev, N. S. Makarov, S. E. Tillo, T. E. Hughes, and A. Rebane, “Two-photon absorption properties of fluorescent proteins,” Nat. Methods8(5), 393–399 (2011).
[CrossRef] [PubMed]

Malik, Z.

L. Greenbaum, C. Rothmann, R. Lavie, and Z. Malik, “Green fluorescent protein photobleaching: A model for protein damage by endogenous and exogenous singlet oxygen,” Biol. Chem.381(12), 1251–1258 (2000).
[CrossRef] [PubMed]

McCrae, K. R.

D. B. Cines, E. S. Pollak, C. A. Buck, J. Loscalzo, G. A. Zimmerman, R. P. McEver, J. S. Pober, T. M. Wick, B. A. Konkle, B. S. Schwartz, E. S. Barnathan, K. R. McCrae, B. A. Hug, A. M. Schmidt, and D. M. Stern, “Endothelial cells in physiology and in the pathophysiology of vascular disorders,” Blood91(10), 3527–3561 (1998).
[PubMed]

McDonald, D. M.

D. M. McDonald and P. L. Choyke, “Imaging of angiogenesis: From microscope to clinic,” Nat. Med.9(6), 713–725 (2003).
[CrossRef] [PubMed]

McEver, R. P.

D. B. Cines, E. S. Pollak, C. A. Buck, J. Loscalzo, G. A. Zimmerman, R. P. McEver, J. S. Pober, T. M. Wick, B. A. Konkle, B. S. Schwartz, E. S. Barnathan, K. R. McCrae, B. A. Hug, A. M. Schmidt, and D. M. Stern, “Endothelial cells in physiology and in the pathophysiology of vascular disorders,” Blood91(10), 3527–3561 (1998).
[PubMed]

Millard, A. C.

Min, W.

W. Min, S. Lu, S. Chong, R. Roy, G. R. Holtom, and X. S. Xie, “Imaging chromophores with undetectable fluorescence by stimulated emission microscopy,” Nature461(7267), 1105–1109 (2009).
[CrossRef] [PubMed]

Mordelet, E.

E. Murayama, K. Kissa, A. Zapata, E. Mordelet, V. Briolat, H. F. Lin, R. I. Handin, and P. Herbomel, “Tracing Hematopoietic Precursor Migration to Successive Hematopoietic Organs during Zebrafish Development,” Immunity25(6), 963–975 (2006).
[CrossRef] [PubMed]

Murayama, E.

E. Murayama, K. Kissa, A. Zapata, E. Mordelet, V. Briolat, H. F. Lin, R. I. Handin, and P. Herbomel, “Tracing Hematopoietic Precursor Migration to Successive Hematopoietic Organs during Zebrafish Development,” Immunity25(6), 963–975 (2006).
[CrossRef] [PubMed]

Pastila, R. K.

Pitsillides, C.

Pober, J. S.

D. B. Cines, E. S. Pollak, C. A. Buck, J. Loscalzo, G. A. Zimmerman, R. P. McEver, J. S. Pober, T. M. Wick, B. A. Konkle, B. S. Schwartz, E. S. Barnathan, K. R. McCrae, B. A. Hug, A. M. Schmidt, and D. M. Stern, “Endothelial cells in physiology and in the pathophysiology of vascular disorders,” Blood91(10), 3527–3561 (1998).
[PubMed]

Pollak, E. S.

D. B. Cines, E. S. Pollak, C. A. Buck, J. Loscalzo, G. A. Zimmerman, R. P. McEver, J. S. Pober, T. M. Wick, B. A. Konkle, B. S. Schwartz, E. S. Barnathan, K. R. McCrae, B. A. Hug, A. M. Schmidt, and D. M. Stern, “Endothelial cells in physiology and in the pathophysiology of vascular disorders,” Blood91(10), 3527–3561 (1998).
[PubMed]

Puoris’haag, M.

Qu, J. Y.

Rebane, A.

M. Drobizhev, N. S. Makarov, S. E. Tillo, T. E. Hughes, and A. Rebane, “Two-photon absorption properties of fluorescent proteins,” Nat. Methods8(5), 393–399 (2011).
[CrossRef] [PubMed]

Rothmann, C.

L. Greenbaum, C. Rothmann, R. Lavie, and Z. Malik, “Green fluorescent protein photobleaching: A model for protein damage by endogenous and exogenous singlet oxygen,” Biol. Chem.381(12), 1251–1258 (2000).
[CrossRef] [PubMed]

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W. Min, S. Lu, S. Chong, R. Roy, G. R. Holtom, and X. S. Xie, “Imaging chromophores with undetectable fluorescence by stimulated emission microscopy,” Nature461(7267), 1105–1109 (2009).
[CrossRef] [PubMed]

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Schaffer, C. B.

Schmidt, A. M.

D. B. Cines, E. S. Pollak, C. A. Buck, J. Loscalzo, G. A. Zimmerman, R. P. McEver, J. S. Pober, T. M. Wick, B. A. Konkle, B. S. Schwartz, E. S. Barnathan, K. R. McCrae, B. A. Hug, A. M. Schmidt, and D. M. Stern, “Endothelial cells in physiology and in the pathophysiology of vascular disorders,” Blood91(10), 3527–3561 (1998).
[PubMed]

Schwartz, B. S.

D. B. Cines, E. S. Pollak, C. A. Buck, J. Loscalzo, G. A. Zimmerman, R. P. McEver, J. S. Pober, T. M. Wick, B. A. Konkle, B. S. Schwartz, E. S. Barnathan, K. R. McCrae, B. A. Hug, A. M. Schmidt, and D. M. Stern, “Endothelial cells in physiology and in the pathophysiology of vascular disorders,” Blood91(10), 3527–3561 (1998).
[PubMed]

Shi, Y. Q.

L. Li, B. Yan, Y. Q. Shi, W. Q. Zhang, and Z. L. Wen, “Live imaging reveals differing roles of macrophages and neutrophils during zebrafish tail fin regeneration,” J. Biol. Chem.287(30), 25353–25360 (2012).
[CrossRef] [PubMed]

Spencer, D. D.

Squier, J. A.

Stern, D. M.

D. B. Cines, E. S. Pollak, C. A. Buck, J. Loscalzo, G. A. Zimmerman, R. P. McEver, J. S. Pober, T. M. Wick, B. A. Konkle, B. S. Schwartz, E. S. Barnathan, K. R. McCrae, B. A. Hug, A. M. Schmidt, and D. M. Stern, “Endothelial cells in physiology and in the pathophysiology of vascular disorders,” Blood91(10), 3527–3561 (1998).
[PubMed]

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E. R. Gillan, R. D. Christensen, Y. Suen, R. Ellis, C. van de Ven, and M. S. Cairo, “A randomized, placebo-controlled trial of recombinant human granulocyte colony-stimulating factor administration in newborn infants with presumed sepsis: Significant induction of peripheral and bone marrow neutrophilia,” Blood84(5), 1427–1433 (1994).
[PubMed]

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Tamplin, O. J.

O. J. Tamplin and L. I. Zon, “Fishing at the cellular level,” Nat. Methods7(8), 600–601 (2010).
[CrossRef] [PubMed]

Tárnok, A.

V. V. Tuchin, A. Tárnok, and V. P. Zharov, “In vivo flow cytometry: A horizon of opportunities,” Cytometry A79(10), 737–745 (2011).
[CrossRef] [PubMed]

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M. Drobizhev, N. S. Makarov, S. E. Tillo, T. E. Hughes, and A. Rebane, “Two-photon absorption properties of fluorescent proteins,” Nat. Methods8(5), 393–399 (2011).
[CrossRef] [PubMed]

Tsai, C. K.

Tsai, P. S.

Tuchin, V. V.

V. V. Tuchin, A. Tárnok, and V. P. Zharov, “In vivo flow cytometry: A horizon of opportunities,” Cytometry A79(10), 737–745 (2011).
[CrossRef] [PubMed]

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E. R. Gillan, R. D. Christensen, Y. Suen, R. Ellis, C. van de Ven, and M. S. Cairo, “A randomized, placebo-controlled trial of recombinant human granulocyte colony-stimulating factor administration in newborn infants with presumed sepsis: Significant induction of peripheral and bone marrow neutrophilia,” Blood84(5), 1427–1433 (1994).
[PubMed]

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L. V. Wang, “Multiscale photoacoustic microscopy and computed tomography,” Nat. Photonics3(9), 503–509 (2009).
[CrossRef] [PubMed]

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Y. Zeng, J. Xu, D. Li, L. Li, Z. Wen, and J. Y. Qu, “Label-free in vivo flow cytometry in zebrafish using two-photon autofluorescence imaging,” Opt. Lett.37(13), 2490–2492 (2012).
[CrossRef] [PubMed]

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[CrossRef] [PubMed]

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L. Li, B. Yan, Y. Q. Shi, W. Q. Zhang, and Z. L. Wen, “Live imaging reveals differing roles of macrophages and neutrophils during zebrafish tail fin regeneration,” J. Biol. Chem.287(30), 25353–25360 (2012).
[CrossRef] [PubMed]

Wick, T. M.

D. B. Cines, E. S. Pollak, C. A. Buck, J. Loscalzo, G. A. Zimmerman, R. P. McEver, J. S. Pober, T. M. Wick, B. A. Konkle, B. S. Schwartz, E. S. Barnathan, K. R. McCrae, B. A. Hug, A. M. Schmidt, and D. M. Stern, “Endothelial cells in physiology and in the pathophysiology of vascular disorders,” Blood91(10), 3527–3561 (1998).
[PubMed]

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Wu, P. C.

Wu, Y. C.

W. Zheng, Y. C. Wu, D. Li, and J. Y. Qu, “Autofluorescence of epithelial tissue: Single-photon versus two-photon excitation,” J. Biomed. Opt.13(5), 054010 (2008).
[CrossRef] [PubMed]

Xie, X. S.

W. Min, S. Lu, S. Chong, R. Roy, G. R. Holtom, and X. S. Xie, “Imaging chromophores with undetectable fluorescence by stimulated emission microscopy,” Nature461(7267), 1105–1109 (2009).
[CrossRef] [PubMed]

Xu, C.

Xu, J.

Y. Zeng, J. Xu, D. Li, L. Li, Z. Wen, and J. Y. Qu, “Label-free in vivo flow cytometry in zebrafish using two-photon autofluorescence imaging,” Opt. Lett.37(13), 2490–2492 (2012).
[CrossRef] [PubMed]

H. Jin, J. Xu, and Z. Wen, “Migratory path of definitive hematopoietic stem/progenitor cells during zebrafish development,” Blood109(12), 5208–5214 (2007).
[CrossRef] [PubMed]

Yan, B.

L. Li, B. Yan, Y. Q. Shi, W. Q. Zhang, and Z. L. Wen, “Live imaging reveals differing roles of macrophages and neutrophils during zebrafish tail fin regeneration,” J. Biol. Chem.287(30), 25353–25360 (2012).
[CrossRef] [PubMed]

Yeh, C. Y.

Zapata, A.

E. Murayama, K. Kissa, A. Zapata, E. Mordelet, V. Briolat, H. F. Lin, R. I. Handin, and P. Herbomel, “Tracing Hematopoietic Precursor Migration to Successive Hematopoietic Organs during Zebrafish Development,” Immunity25(6), 963–975 (2006).
[CrossRef] [PubMed]

Zeng, Y.

Zhang, W. Q.

L. Li, B. Yan, Y. Q. Shi, W. Q. Zhang, and Z. L. Wen, “Live imaging reveals differing roles of macrophages and neutrophils during zebrafish tail fin regeneration,” J. Biol. Chem.287(30), 25353–25360 (2012).
[CrossRef] [PubMed]

Zharov, V. P.

V. V. Tuchin, A. Tárnok, and V. P. Zharov, “In vivo flow cytometry: A horizon of opportunities,” Cytometry A79(10), 737–745 (2011).
[CrossRef] [PubMed]

Zheng, W.

Zimmerman, G. A.

D. B. Cines, E. S. Pollak, C. A. Buck, J. Loscalzo, G. A. Zimmerman, R. P. McEver, J. S. Pober, T. M. Wick, B. A. Konkle, B. S. Schwartz, E. S. Barnathan, K. R. McCrae, B. A. Hug, A. M. Schmidt, and D. M. Stern, “Endothelial cells in physiology and in the pathophysiology of vascular disorders,” Blood91(10), 3527–3561 (1998).
[PubMed]

Zon, L. I.

O. J. Tamplin and L. I. Zon, “Fishing at the cellular level,” Nat. Methods7(8), 600–601 (2010).
[CrossRef] [PubMed]

Biol. Chem. (1)

L. Greenbaum, C. Rothmann, R. Lavie, and Z. Malik, “Green fluorescent protein photobleaching: A model for protein damage by endogenous and exogenous singlet oxygen,” Biol. Chem.381(12), 1251–1258 (2000).
[CrossRef] [PubMed]

Biomed. Opt. Express (2)

Blood (3)

E. R. Gillan, R. D. Christensen, Y. Suen, R. Ellis, C. van de Ven, and M. S. Cairo, “A randomized, placebo-controlled trial of recombinant human granulocyte colony-stimulating factor administration in newborn infants with presumed sepsis: Significant induction of peripheral and bone marrow neutrophilia,” Blood84(5), 1427–1433 (1994).
[PubMed]

D. B. Cines, E. S. Pollak, C. A. Buck, J. Loscalzo, G. A. Zimmerman, R. P. McEver, J. S. Pober, T. M. Wick, B. A. Konkle, B. S. Schwartz, E. S. Barnathan, K. R. McCrae, B. A. Hug, A. M. Schmidt, and D. M. Stern, “Endothelial cells in physiology and in the pathophysiology of vascular disorders,” Blood91(10), 3527–3561 (1998).
[PubMed]

H. Jin, J. Xu, and Z. Wen, “Migratory path of definitive hematopoietic stem/progenitor cells during zebrafish development,” Blood109(12), 5208–5214 (2007).
[CrossRef] [PubMed]

Cytometry A (1)

V. V. Tuchin, A. Tárnok, and V. P. Zharov, “In vivo flow cytometry: A horizon of opportunities,” Cytometry A79(10), 737–745 (2011).
[CrossRef] [PubMed]

Dev. Genet. (1)

Z. Lele, S. Engel, and P. H. Krone, “hsp47 and hsp70 gene expression is differentially regulated in a stress- and tissue-specific manner in zebrafish embryos,” Dev. Genet.21(2), 123–133 (1997).
[CrossRef] [PubMed]

Immunity (1)

E. Murayama, K. Kissa, A. Zapata, E. Mordelet, V. Briolat, H. F. Lin, R. I. Handin, and P. Herbomel, “Tracing Hematopoietic Precursor Migration to Successive Hematopoietic Organs during Zebrafish Development,” Immunity25(6), 963–975 (2006).
[CrossRef] [PubMed]

J. Biol. Chem. (1)

L. Li, B. Yan, Y. Q. Shi, W. Q. Zhang, and Z. L. Wen, “Live imaging reveals differing roles of macrophages and neutrophils during zebrafish tail fin regeneration,” J. Biol. Chem.287(30), 25353–25360 (2012).
[CrossRef] [PubMed]

J. Biomed. Opt. (2)

W. Zheng, Y. C. Wu, D. Li, and J. Y. Qu, “Autofluorescence of epithelial tissue: Single-photon versus two-photon excitation,” J. Biomed. Opt.13(5), 054010 (2008).
[CrossRef] [PubMed]

D. A. Boas and A. K. Dunn, “Laser speckle contrast imaging in biomedical optics,” J. Biomed. Opt.15(1), 011109 (2010).
[CrossRef] [PubMed]

J. Opt. Soc. Am. B (2)

Nat. Med. (1)

D. M. McDonald and P. L. Choyke, “Imaging of angiogenesis: From microscope to clinic,” Nat. Med.9(6), 713–725 (2003).
[CrossRef] [PubMed]

Nat. Methods (2)

M. Drobizhev, N. S. Makarov, S. E. Tillo, T. E. Hughes, and A. Rebane, “Two-photon absorption properties of fluorescent proteins,” Nat. Methods8(5), 393–399 (2011).
[CrossRef] [PubMed]

O. J. Tamplin and L. I. Zon, “Fishing at the cellular level,” Nat. Methods7(8), 600–601 (2010).
[CrossRef] [PubMed]

Nat. Photonics (1)

L. V. Wang, “Multiscale photoacoustic microscopy and computed tomography,” Nat. Photonics3(9), 503–509 (2009).
[CrossRef] [PubMed]

Nature (1)

W. Min, S. Lu, S. Chong, R. Roy, G. R. Holtom, and X. S. Xie, “Imaging chromophores with undetectable fluorescence by stimulated emission microscopy,” Nature461(7267), 1105–1109 (2009).
[CrossRef] [PubMed]

Opt. Express (2)

Opt. Lett. (3)

Other (7)

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J. K. Li, Dynamics of the vascular system (World scientific, 2004).

M. Westerfield, The zebrafish book: a guide for the laboratory use of zebrafish (Daniorerio) (University of Oregon Press, 2000).

V. Kumar, A. K. Abbas, N. Fausto, and J. Aster, Robbins and cotran: pathologic basis of disease (Elsevier, 2009).

A. V. Gore, K. Monzo, Y. R. Cha, W. Pan, and B. M. Weinstein, “Vascular development in the zebrafish,” Cold Spring Harbor Perspectives in Medicine 2, (2012).

F. H. Martini, M. J. Timmons, and B. Tallitsch, Human Anatomy (Pearson Education, 2003)

G. E. Davis, A. N. Stratman, A. Sacharidou, and W. Koh, “Molecular basis for endothelial lumen formation and tubulogenesis during vasculogenesis and angiogenic sprouting,” International Review of Cell and Molecular Biology208 (2011) Chap. 3.

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