Abstract

For the first time the far red fluorescent protein (FP) E2-Crimson genetically expressed in the exocrine pancreas of adult zebrafish has been non-invasively mapped in 3D in vivo using photoacoustic tomography (PAT). The distribution of E2-Crimson in the exocrine pancreas acquired by PAT was confirmed using epifluorescence imaging and histology, with optical coherence tomography (OCT) providing complementary structural information. This work demonstrates the depth advantage of PAT to resolve FP in an animal model and establishes the value of E2-Crimson for PAT studies of transgenic models, laying the foundation for future longitudinal studies of the zebrafish as a model of diseases affecting inner organs.

© 2013 OSA

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2013 (8)

H. R. Shive, “Zebrafish Models for Human Cancer,” Vet. Pathol.50(3), 468–482 (2013).
[CrossRef] [PubMed]

M. R. Fein and M. Egeblad, “Caught in the act: revealing the metastatic process by live imaging,” Dis. Model. Mech.6(3), 580–593 (2013).
[CrossRef] [PubMed]

C. Lee, S. Han, S. Kim, M. Jeon, M. Y. Jeon, C. Kim, and J. Kim, “Combined photoacoustic and optical coherence tomography using a single near-infrared supercontinuum laser source,” Appl. Opt.52(9), 1824–1828 (2013).
[CrossRef] [PubMed]

X. Cai, Y. Zhang, L. Li, S. W. Choi, M. R. MacEwan, J. Yao, C. Kim, Y. Xia, and L. V. Wang, “Investigation of neovascularization in three-dimensional porous scaffolds in vivo by a combination of multiscale photoacoustic microscopy and optical coherence tomography,” Tissue Eng. Part C Methods19(3), 196–204 (2013).
[CrossRef] [PubMed]

L. Xi, C. Duan, H. Xie, and H. Jiang, “Miniature probe combining optical-resolution photoacoustic microscopy and optical coherence tomography for in vivo microcirculation study,” Appl. Opt.52(9), 1928–1931 (2013).
[CrossRef] [PubMed]

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[CrossRef] [PubMed]

J. Laufer, A. Jathoul, M. Pule, and P. Beard, “Evaluation of genetically expressed absorbing proteins using photoacoustic spectroscopy,” Proc. SPIE8581, 85810X, 85810X-6 (2013).
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A. Kumar, W. Drexler, and R. A. Leitgeb, “Subaperture correlation based digital adaptive optics for full field optical coherence tomography,” Opt. Express21(9), 10850–10866 (2013).
[CrossRef] [PubMed]

2012 (11)

G. S. Filonov, A. Krumholz, J. Xia, J. Yao, L. V. Wang, and V. V. Verkhusha, “Deep-Tissue Photoacoustic Tomography of a Genetically Encoded Near-Infrared Fluorescent Probe,” Angew. Chem.51(6), 1448–1451 (2012).
[CrossRef] [PubMed]

C. Huang, L. Nie, R. W. Schoonover, Z. Guo, C. O. Schirra, M. A. Anastasio, and L. V. Wang, “Aberration correction for transcranial photoacoustic tomography of primates employing adjunct image data,” J. Biomed. Opt.17(6), 066016 (2012).
[CrossRef] [PubMed]

L. Nie, X. Cai, K. Maslov, A. Garcia-Uribe, M. A. Anastasio, and L. V. Wang, “Photoacoustic tomography through a whole adult human skull with a photon recycler,” J. Biomed. Opt.17(11), 110506 (2012).
[CrossRef] [PubMed]

X. Zhang, H. F. Zhang, and S. Jiao, “Optical coherence photoacoustic microscopy: accomplishing optical coherence tomography and photoacoustic microscopy with a single light source,” J. Biomed. Opt.17(3), 030502 (2012).
[CrossRef] [PubMed]

S. Ye, R. Yang, J. Xiong, K. K. Shung, Q. Zhou, C. Li, and Q. Ren, “Label-free imaging of zebrafish larvae in vivo by photoacoustic microscopy,” Biomed. Opt. Express3(2), 360–365 (2012).
[CrossRef] [PubMed]

R. Ma, M. Distel, X. L. Deán-Ben, V. Ntziachristos, and D. Razansky, “Non-invasive whole-body imaging of adult zebrafish with optoacoustic tomography,” Phys. Med. Biol.57(22), 7227–7237 (2012).
[CrossRef] [PubMed]

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[CrossRef] [PubMed]

C. Kizil, J. Kaslin, V. Kroehne, and M. Brand, “Adult neurogenesis and brain regeneration in zebrafish,” Dev. Neurobiol.72(3), 429–461 (2012).
[CrossRef] [PubMed]

J. Laufer, P. Johnson, E. Zhang, B. Treeby, B. Cox, B. Pedley, and P. Beard, “In vivo preclinical photoacoustic imaging of tumor vasculature development and therapy,” J. Biomed. Opt.17(5), 056016 (2012).
[CrossRef] [PubMed]

J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt.17(6), 061220 (2012).
[CrossRef] [PubMed]

B. Cox, J. G. Laufer, S. R. Arridge, and P. C. Beard, “Quantitative spectroscopic photoacoustic imaging: a review,” J. Biomed. Opt.17(6), 061202 (2012).
[CrossRef] [PubMed]

2011 (4)

2010 (3)

A. Alex, B. Považay, B. Hofer, S. Popov, C. Glittenberg, S. Binder, and W. Drexler, “Multispectral in vivo three-dimensional optical coherence tomography of human skin,” J. Biomed. Opt.15(2), 026025 (2010).
[CrossRef] [PubMed]

B. E. Treeby and B. T. Cox, “k-Wave: MATLAB toolbox for the simulation and reconstruction of photoacoustic wave fields,” J. Biomed. Opt.15(2), 021314 (2010).
[CrossRef] [PubMed]

Z. Cao, L. D. Jensen, P. Rouhi, K. Hosaka, T. Länne, J. F. Steffensen, E. Wahlberg, and Y. Cao, “Hypoxia-induced retinopathy model in adult zebrafish,” Nat. Protoc.5(12), 1903–1910 (2010).
[CrossRef] [PubMed]

2009 (5)

J. B. Moss, P. Koustubhan, M. Greenman, M. J. Parsons, I. Walter, and L. G. Moss, “Regeneration of the pancreas in adult zebrafish,” Diabetes58(8), 1844–1851 (2009).
[CrossRef] [PubMed]

B. W. Rice and C. H. Contag, “The importance of being red,” Nat. Biotechnol.27(7), 624–625 (2009).
[CrossRef] [PubMed]

D. Razansky, M. Distel, C. Vinegoni, R. Ma, N. Perrimon, R. W. Köster, and V. Ntziachristos, “Multispectral opto-acoustic tomography of deep-seated fluorescent proteins in vivo,” Nat. Photonics3(7), 412–417 (2009).
[CrossRef]

S. Jiao, Z. Xie, H. F. Zhang, and C. A. Puliafito, “Simultaneous multimodal imaging with integrated photoacoustic microscopy and optical coherence tomography,” Opt. Lett.34(19), 2961–2963 (2009).
[CrossRef] [PubMed]

L. Li, K. Maslov, G. Ku, and L. V. Wang, “Three-dimensional combined photoacoustic and optical coherence microscopy for in vivo microcirculation studies,” Opt. Express17(19), 16450–16455 (2009).
[CrossRef] [PubMed]

2008 (1)

2007 (2)

H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods4(4), 331–336 (2007).
[CrossRef] [PubMed]

K. H. Song and L. V. Wang, “Deep reflection-mode photoacoustic imaging of biological tissue,” J. Biomed. Opt.12(6), 060503 (2007).
[CrossRef] [PubMed]

2006 (3)

H. Wan, S. Korzh, Z. Li, S. P. Mudumana, V. Korzh, Y.-J. Jiang, S. Lin, and Z. Gong, “Analyses of pancreas development by generation of gfp transgenic zebrafish using an exocrine pancreas-specific elastaseA gene promoter,” Exp. Cell Res.312(9), 1526–1539 (2006).
[CrossRef] [PubMed]

N. Furukawa, M. Saito, T. Hakoshima, and K. Kohno, “A Diphtheria Toxin Receptor Deficient in Epidermal Growth Factor-Like Biological Activity,” J. Biochem.140(6), 831–841 (2006).
[CrossRef] [PubMed]

E. Zhang and P. Beard, “Broadband ultrasound field mapping system using a wavelength tuned, optically scanned focused laser beam to address a Fabry Perot polymer film sensor,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control53(7), 1330–1338 (2006).
[CrossRef] [PubMed]

2005 (1)

J. W. Lichtman and J.-A. Conchello, “Fluorescence microscopy,” Nat. Methods2(12), 910–919 (2005).
[CrossRef] [PubMed]

2004 (1)

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical Sectioning Deep Inside Live Embryos by Selective Plane Illumination Microscopy,” Science305(5686), 1007–1009 (2004).
[CrossRef] [PubMed]

2002 (1)

J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson, “Optical projection tomography as a tool for 3D microscopy and gene expression studies,” Science296(5567), 541–545 (2002).
[CrossRef] [PubMed]

Ahlgren, U.

J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson, “Optical projection tomography as a tool for 3D microscopy and gene expression studies,” Science296(5567), 541–545 (2002).
[CrossRef] [PubMed]

Alex, A.

A. Alex, J. Weingast, M. Weinigel, M. Kellner-Höfer, R. Nemecek, M. Binder, H. Pehamberger, K. König, and W. Drexler, “Three-dimensional multiphoton/optical coherence tomography for diagnostic applications in dermatology,” J Biophotonics6(4), 352–362 (2013).
[CrossRef] [PubMed]

E. Z. Zhang, B. Povazay, J. Laufer, A. Alex, B. Hofer, B. Pedley, C. Glittenberg, B. Treeby, B. Cox, P. Beard, and W. Drexler, “Multimodal photoacoustic and optical coherence tomography scanner using an all optical detection scheme for 3D morphological skin imaging,” Biomed. Opt. Express2(8), 2202–2215 (2011).
[CrossRef] [PubMed]

A. Alex, B. Považay, B. Hofer, S. Popov, C. Glittenberg, S. Binder, and W. Drexler, “Multispectral in vivo three-dimensional optical coherence tomography of human skin,” J. Biomed. Opt.15(2), 026025 (2010).
[CrossRef] [PubMed]

Anastasio, M. A.

C. Huang, L. Nie, R. W. Schoonover, Z. Guo, C. O. Schirra, M. A. Anastasio, and L. V. Wang, “Aberration correction for transcranial photoacoustic tomography of primates employing adjunct image data,” J. Biomed. Opt.17(6), 066016 (2012).
[CrossRef] [PubMed]

L. Nie, X. Cai, K. Maslov, A. Garcia-Uribe, M. A. Anastasio, and L. V. Wang, “Photoacoustic tomography through a whole adult human skull with a photon recycler,” J. Biomed. Opt.17(11), 110506 (2012).
[CrossRef] [PubMed]

Arridge, S. R.

B. Cox, J. G. Laufer, S. R. Arridge, and P. C. Beard, “Quantitative spectroscopic photoacoustic imaging: a review,” J. Biomed. Opt.17(6), 061202 (2012).
[CrossRef] [PubMed]

Baldock, R.

J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson, “Optical projection tomography as a tool for 3D microscopy and gene expression studies,” Science296(5567), 541–545 (2002).
[CrossRef] [PubMed]

Beard, P.

J. Laufer, A. Jathoul, M. Pule, and P. Beard, “Evaluation of genetically expressed absorbing proteins using photoacoustic spectroscopy,” Proc. SPIE8581, 85810X, 85810X-6 (2013).
[CrossRef]

J. Laufer, P. Johnson, E. Zhang, B. Treeby, B. Cox, B. Pedley, and P. Beard, “In vivo preclinical photoacoustic imaging of tumor vasculature development and therapy,” J. Biomed. Opt.17(5), 056016 (2012).
[CrossRef] [PubMed]

J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt.17(6), 061220 (2012).
[CrossRef] [PubMed]

P. Beard, “Biomedical photoacoustic imaging,” Interface Focus1(4), 602–631 (2011).
[CrossRef] [PubMed]

E. Z. Zhang, B. Povazay, J. Laufer, A. Alex, B. Hofer, B. Pedley, C. Glittenberg, B. Treeby, B. Cox, P. Beard, and W. Drexler, “Multimodal photoacoustic and optical coherence tomography scanner using an all optical detection scheme for 3D morphological skin imaging,” Biomed. Opt. Express2(8), 2202–2215 (2011).
[CrossRef] [PubMed]

E. Zhang, J. Laufer, and P. Beard, “Backward-mode multiwavelength photoacoustic scanner using a planar Fabry-Perot polymer film ultrasound sensor for high-resolution three-dimensional imaging of biological tissues,” Appl. Opt.47(4), 561–577 (2008).
[CrossRef] [PubMed]

E. Zhang and P. Beard, “Broadband ultrasound field mapping system using a wavelength tuned, optically scanned focused laser beam to address a Fabry Perot polymer film sensor,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control53(7), 1330–1338 (2006).
[CrossRef] [PubMed]

Beard, P. C.

B. Cox, J. G. Laufer, S. R. Arridge, and P. C. Beard, “Quantitative spectroscopic photoacoustic imaging: a review,” J. Biomed. Opt.17(6), 061202 (2012).
[CrossRef] [PubMed]

Becker, K.

H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods4(4), 331–336 (2007).
[CrossRef] [PubMed]

Binder, M.

A. Alex, J. Weingast, M. Weinigel, M. Kellner-Höfer, R. Nemecek, M. Binder, H. Pehamberger, K. König, and W. Drexler, “Three-dimensional multiphoton/optical coherence tomography for diagnostic applications in dermatology,” J Biophotonics6(4), 352–362 (2013).
[CrossRef] [PubMed]

Binder, S.

A. Alex, B. Považay, B. Hofer, S. Popov, C. Glittenberg, S. Binder, and W. Drexler, “Multispectral in vivo three-dimensional optical coherence tomography of human skin,” J. Biomed. Opt.15(2), 026025 (2010).
[CrossRef] [PubMed]

Brand, M.

C. Kizil, J. Kaslin, V. Kroehne, and M. Brand, “Adult neurogenesis and brain regeneration in zebrafish,” Dev. Neurobiol.72(3), 429–461 (2012).
[CrossRef] [PubMed]

Bugeon, L.

Cai, X.

X. Cai, Y. Zhang, L. Li, S. W. Choi, M. R. MacEwan, J. Yao, C. Kim, Y. Xia, and L. V. Wang, “Investigation of neovascularization in three-dimensional porous scaffolds in vivo by a combination of multiscale photoacoustic microscopy and optical coherence tomography,” Tissue Eng. Part C Methods19(3), 196–204 (2013).
[CrossRef] [PubMed]

L. Nie, X. Cai, K. Maslov, A. Garcia-Uribe, M. A. Anastasio, and L. V. Wang, “Photoacoustic tomography through a whole adult human skull with a photon recycler,” J. Biomed. Opt.17(11), 110506 (2012).
[CrossRef] [PubMed]

Cao, Y.

Z. Cao, L. D. Jensen, P. Rouhi, K. Hosaka, T. Länne, J. F. Steffensen, E. Wahlberg, and Y. Cao, “Hypoxia-induced retinopathy model in adult zebrafish,” Nat. Protoc.5(12), 1903–1910 (2010).
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Cao, Z.

Z. Cao, L. D. Jensen, P. Rouhi, K. Hosaka, T. Länne, J. F. Steffensen, E. Wahlberg, and Y. Cao, “Hypoxia-induced retinopathy model in adult zebrafish,” Nat. Protoc.5(12), 1903–1910 (2010).
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Chen, L.

Choi, S. W.

X. Cai, Y. Zhang, L. Li, S. W. Choi, M. R. MacEwan, J. Yao, C. Kim, Y. Xia, and L. V. Wang, “Investigation of neovascularization in three-dimensional porous scaffolds in vivo by a combination of multiscale photoacoustic microscopy and optical coherence tomography,” Tissue Eng. Part C Methods19(3), 196–204 (2013).
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J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt.17(6), 061220 (2012).
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J. W. Lichtman and J.-A. Conchello, “Fluorescence microscopy,” Nat. Methods2(12), 910–919 (2005).
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B. W. Rice and C. H. Contag, “The importance of being red,” Nat. Biotechnol.27(7), 624–625 (2009).
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J. Laufer, P. Johnson, E. Zhang, B. Treeby, B. Cox, B. Pedley, and P. Beard, “In vivo preclinical photoacoustic imaging of tumor vasculature development and therapy,” J. Biomed. Opt.17(5), 056016 (2012).
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J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt.17(6), 061220 (2012).
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B. Cox, J. G. Laufer, S. R. Arridge, and P. C. Beard, “Quantitative spectroscopic photoacoustic imaging: a review,” J. Biomed. Opt.17(6), 061202 (2012).
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E. Z. Zhang, B. Povazay, J. Laufer, A. Alex, B. Hofer, B. Pedley, C. Glittenberg, B. Treeby, B. Cox, P. Beard, and W. Drexler, “Multimodal photoacoustic and optical coherence tomography scanner using an all optical detection scheme for 3D morphological skin imaging,” Biomed. Opt. Express2(8), 2202–2215 (2011).
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B. E. Treeby and B. T. Cox, “k-Wave: MATLAB toolbox for the simulation and reconstruction of photoacoustic wave fields,” J. Biomed. Opt.15(2), 021314 (2010).
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Davidson, D.

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R. Ma, M. Distel, X. L. Deán-Ben, V. Ntziachristos, and D. Razansky, “Non-invasive whole-body imaging of adult zebrafish with optoacoustic tomography,” Phys. Med. Biol.57(22), 7227–7237 (2012).
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H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods4(4), 331–336 (2007).
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J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical Sectioning Deep Inside Live Embryos by Selective Plane Illumination Microscopy,” Science305(5686), 1007–1009 (2004).
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H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods4(4), 331–336 (2007).
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R. Ma, M. Distel, X. L. Deán-Ben, V. Ntziachristos, and D. Razansky, “Non-invasive whole-body imaging of adult zebrafish with optoacoustic tomography,” Phys. Med. Biol.57(22), 7227–7237 (2012).
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D. Razansky, M. Distel, C. Vinegoni, R. Ma, N. Perrimon, R. W. Köster, and V. Ntziachristos, “Multispectral opto-acoustic tomography of deep-seated fluorescent proteins in vivo,” Nat. Photonics3(7), 412–417 (2009).
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H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods4(4), 331–336 (2007).
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A. Alex, J. Weingast, M. Weinigel, M. Kellner-Höfer, R. Nemecek, M. Binder, H. Pehamberger, K. König, and W. Drexler, “Three-dimensional multiphoton/optical coherence tomography for diagnostic applications in dermatology,” J Biophotonics6(4), 352–362 (2013).
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A. Alex, B. Považay, B. Hofer, S. Popov, C. Glittenberg, S. Binder, and W. Drexler, “Multispectral in vivo three-dimensional optical coherence tomography of human skin,” J. Biomed. Opt.15(2), 026025 (2010).
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Duan, C.

Eder, M.

H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods4(4), 331–336 (2007).
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M. R. Fein and M. Egeblad, “Caught in the act: revealing the metastatic process by live imaging,” Dis. Model. Mech.6(3), 580–593 (2013).
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Fein, M. R.

M. R. Fein and M. Egeblad, “Caught in the act: revealing the metastatic process by live imaging,” Dis. Model. Mech.6(3), 580–593 (2013).
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Filonov, G. S.

G. S. Filonov, A. Krumholz, J. Xia, J. Yao, L. V. Wang, and V. V. Verkhusha, “Deep-Tissue Photoacoustic Tomography of a Genetically Encoded Near-Infrared Fluorescent Probe,” Angew. Chem.51(6), 1448–1451 (2012).
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French, P. M.

Furukawa, N.

N. Furukawa, M. Saito, T. Hakoshima, and K. Kohno, “A Diphtheria Toxin Receptor Deficient in Epidermal Growth Factor-Like Biological Activity,” J. Biochem.140(6), 831–841 (2006).
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Garcia-Uribe, A.

L. Nie, X. Cai, K. Maslov, A. Garcia-Uribe, M. A. Anastasio, and L. V. Wang, “Photoacoustic tomography through a whole adult human skull with a photon recycler,” J. Biomed. Opt.17(11), 110506 (2012).
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Glittenberg, C.

Gong, Z.

H. Wan, S. Korzh, Z. Li, S. P. Mudumana, V. Korzh, Y.-J. Jiang, S. Lin, and Z. Gong, “Analyses of pancreas development by generation of gfp transgenic zebrafish using an exocrine pancreas-specific elastaseA gene promoter,” Exp. Cell Res.312(9), 1526–1539 (2006).
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Greenman, M.

J. B. Moss, P. Koustubhan, M. Greenman, M. J. Parsons, I. Walter, and L. G. Moss, “Regeneration of the pancreas in adult zebrafish,” Diabetes58(8), 1844–1851 (2009).
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Guo, Z.

C. Huang, L. Nie, R. W. Schoonover, Z. Guo, C. O. Schirra, M. A. Anastasio, and L. V. Wang, “Aberration correction for transcranial photoacoustic tomography of primates employing adjunct image data,” J. Biomed. Opt.17(6), 066016 (2012).
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Hakoshima, T.

N. Furukawa, M. Saito, T. Hakoshima, and K. Kohno, “A Diphtheria Toxin Receptor Deficient in Epidermal Growth Factor-Like Biological Activity,” J. Biochem.140(6), 831–841 (2006).
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Han, S.

Hecksher-Sørensen, J.

J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson, “Optical projection tomography as a tool for 3D microscopy and gene expression studies,” Science296(5567), 541–545 (2002).
[CrossRef] [PubMed]

Hill, B.

J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson, “Optical projection tomography as a tool for 3D microscopy and gene expression studies,” Science296(5567), 541–545 (2002).
[CrossRef] [PubMed]

Hofer, B.

Hosaka, K.

Z. Cao, L. D. Jensen, P. Rouhi, K. Hosaka, T. Länne, J. F. Steffensen, E. Wahlberg, and Y. Cao, “Hypoxia-induced retinopathy model in adult zebrafish,” Nat. Protoc.5(12), 1903–1910 (2010).
[CrossRef] [PubMed]

Huang, C.

C. Huang, L. Nie, R. W. Schoonover, Z. Guo, C. O. Schirra, M. A. Anastasio, and L. V. Wang, “Aberration correction for transcranial photoacoustic tomography of primates employing adjunct image data,” J. Biomed. Opt.17(6), 066016 (2012).
[CrossRef] [PubMed]

Huisken, J.

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical Sectioning Deep Inside Live Embryos by Selective Plane Illumination Microscopy,” Science305(5686), 1007–1009 (2004).
[CrossRef] [PubMed]

Jährling, N.

H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods4(4), 331–336 (2007).
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Jathoul, A.

J. Laufer, A. Jathoul, M. Pule, and P. Beard, “Evaluation of genetically expressed absorbing proteins using photoacoustic spectroscopy,” Proc. SPIE8581, 85810X, 85810X-6 (2013).
[CrossRef]

Jensen, L. D.

Z. Cao, L. D. Jensen, P. Rouhi, K. Hosaka, T. Länne, J. F. Steffensen, E. Wahlberg, and Y. Cao, “Hypoxia-induced retinopathy model in adult zebrafish,” Nat. Protoc.5(12), 1903–1910 (2010).
[CrossRef] [PubMed]

Jeon, M.

Jeon, M. Y.

Jiang, H.

Jiang, Y.-J.

H. Wan, S. Korzh, Z. Li, S. P. Mudumana, V. Korzh, Y.-J. Jiang, S. Lin, and Z. Gong, “Analyses of pancreas development by generation of gfp transgenic zebrafish using an exocrine pancreas-specific elastaseA gene promoter,” Exp. Cell Res.312(9), 1526–1539 (2006).
[CrossRef] [PubMed]

Jiao, S.

X. Zhang, H. F. Zhang, and S. Jiao, “Optical coherence photoacoustic microscopy: accomplishing optical coherence tomography and photoacoustic microscopy with a single light source,” J. Biomed. Opt.17(3), 030502 (2012).
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S. Jiao, Z. Xie, H. F. Zhang, and C. A. Puliafito, “Simultaneous multimodal imaging with integrated photoacoustic microscopy and optical coherence tomography,” Opt. Lett.34(19), 2961–2963 (2009).
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Johnson, P.

J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt.17(6), 061220 (2012).
[CrossRef] [PubMed]

J. Laufer, P. Johnson, E. Zhang, B. Treeby, B. Cox, B. Pedley, and P. Beard, “In vivo preclinical photoacoustic imaging of tumor vasculature development and therapy,” J. Biomed. Opt.17(5), 056016 (2012).
[CrossRef] [PubMed]

Kaslin, J.

C. Kizil, J. Kaslin, V. Kroehne, and M. Brand, “Adult neurogenesis and brain regeneration in zebrafish,” Dev. Neurobiol.72(3), 429–461 (2012).
[CrossRef] [PubMed]

Kellner-Höfer, M.

A. Alex, J. Weingast, M. Weinigel, M. Kellner-Höfer, R. Nemecek, M. Binder, H. Pehamberger, K. König, and W. Drexler, “Three-dimensional multiphoton/optical coherence tomography for diagnostic applications in dermatology,” J Biophotonics6(4), 352–362 (2013).
[CrossRef] [PubMed]

Kim, C.

X. Cai, Y. Zhang, L. Li, S. W. Choi, M. R. MacEwan, J. Yao, C. Kim, Y. Xia, and L. V. Wang, “Investigation of neovascularization in three-dimensional porous scaffolds in vivo by a combination of multiscale photoacoustic microscopy and optical coherence tomography,” Tissue Eng. Part C Methods19(3), 196–204 (2013).
[CrossRef] [PubMed]

C. Lee, S. Han, S. Kim, M. Jeon, M. Y. Jeon, C. Kim, and J. Kim, “Combined photoacoustic and optical coherence tomography using a single near-infrared supercontinuum laser source,” Appl. Opt.52(9), 1824–1828 (2013).
[CrossRef] [PubMed]

Kim, J.

Kim, S.

Kizil, C.

C. Kizil, J. Kaslin, V. Kroehne, and M. Brand, “Adult neurogenesis and brain regeneration in zebrafish,” Dev. Neurobiol.72(3), 429–461 (2012).
[CrossRef] [PubMed]

Kohno, K.

N. Furukawa, M. Saito, T. Hakoshima, and K. Kohno, “A Diphtheria Toxin Receptor Deficient in Epidermal Growth Factor-Like Biological Activity,” J. Biochem.140(6), 831–841 (2006).
[CrossRef] [PubMed]

König, K.

A. Alex, J. Weingast, M. Weinigel, M. Kellner-Höfer, R. Nemecek, M. Binder, H. Pehamberger, K. König, and W. Drexler, “Three-dimensional multiphoton/optical coherence tomography for diagnostic applications in dermatology,” J Biophotonics6(4), 352–362 (2013).
[CrossRef] [PubMed]

Korzh, S.

H. Wan, S. Korzh, Z. Li, S. P. Mudumana, V. Korzh, Y.-J. Jiang, S. Lin, and Z. Gong, “Analyses of pancreas development by generation of gfp transgenic zebrafish using an exocrine pancreas-specific elastaseA gene promoter,” Exp. Cell Res.312(9), 1526–1539 (2006).
[CrossRef] [PubMed]

Korzh, V.

H. Wan, S. Korzh, Z. Li, S. P. Mudumana, V. Korzh, Y.-J. Jiang, S. Lin, and Z. Gong, “Analyses of pancreas development by generation of gfp transgenic zebrafish using an exocrine pancreas-specific elastaseA gene promoter,” Exp. Cell Res.312(9), 1526–1539 (2006).
[CrossRef] [PubMed]

Köster, R. W.

D. Razansky, M. Distel, C. Vinegoni, R. Ma, N. Perrimon, R. W. Köster, and V. Ntziachristos, “Multispectral opto-acoustic tomography of deep-seated fluorescent proteins in vivo,” Nat. Photonics3(7), 412–417 (2009).
[CrossRef]

Koustubhan, P.

J. B. Moss, P. Koustubhan, M. Greenman, M. J. Parsons, I. Walter, and L. G. Moss, “Regeneration of the pancreas in adult zebrafish,” Diabetes58(8), 1844–1851 (2009).
[CrossRef] [PubMed]

Kroehne, V.

C. Kizil, J. Kaslin, V. Kroehne, and M. Brand, “Adult neurogenesis and brain regeneration in zebrafish,” Dev. Neurobiol.72(3), 429–461 (2012).
[CrossRef] [PubMed]

Krumholz, A.

G. S. Filonov, A. Krumholz, J. Xia, J. Yao, L. V. Wang, and V. V. Verkhusha, “Deep-Tissue Photoacoustic Tomography of a Genetically Encoded Near-Infrared Fluorescent Probe,” Angew. Chem.51(6), 1448–1451 (2012).
[CrossRef] [PubMed]

Ku, G.

Kumar, A.

Lamb, J. R.

Länne, T.

Z. Cao, L. D. Jensen, P. Rouhi, K. Hosaka, T. Länne, J. F. Steffensen, E. Wahlberg, and Y. Cao, “Hypoxia-induced retinopathy model in adult zebrafish,” Nat. Protoc.5(12), 1903–1910 (2010).
[CrossRef] [PubMed]

Laufer, J.

J. Laufer, A. Jathoul, M. Pule, and P. Beard, “Evaluation of genetically expressed absorbing proteins using photoacoustic spectroscopy,” Proc. SPIE8581, 85810X, 85810X-6 (2013).
[CrossRef]

J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt.17(6), 061220 (2012).
[CrossRef] [PubMed]

J. Laufer, P. Johnson, E. Zhang, B. Treeby, B. Cox, B. Pedley, and P. Beard, “In vivo preclinical photoacoustic imaging of tumor vasculature development and therapy,” J. Biomed. Opt.17(5), 056016 (2012).
[CrossRef] [PubMed]

E. Z. Zhang, B. Povazay, J. Laufer, A. Alex, B. Hofer, B. Pedley, C. Glittenberg, B. Treeby, B. Cox, P. Beard, and W. Drexler, “Multimodal photoacoustic and optical coherence tomography scanner using an all optical detection scheme for 3D morphological skin imaging,” Biomed. Opt. Express2(8), 2202–2215 (2011).
[CrossRef] [PubMed]

E. Zhang, J. Laufer, and P. Beard, “Backward-mode multiwavelength photoacoustic scanner using a planar Fabry-Perot polymer film ultrasound sensor for high-resolution three-dimensional imaging of biological tissues,” Appl. Opt.47(4), 561–577 (2008).
[CrossRef] [PubMed]

Laufer, J. G.

B. Cox, J. G. Laufer, S. R. Arridge, and P. C. Beard, “Quantitative spectroscopic photoacoustic imaging: a review,” J. Biomed. Opt.17(6), 061202 (2012).
[CrossRef] [PubMed]

Leach, S. D.

S. Liu and S. D. Leach, “Screening pancreatic oncogenes in zebrafish using the Gal4/UAS system,” Methods Cell Biol.105, 367–381 (2011).
[CrossRef] [PubMed]

Lee, C.

Leischner, U.

H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods4(4), 331–336 (2007).
[CrossRef] [PubMed]

Leitgeb, R. A.

Li, C.

Li, L.

X. Cai, Y. Zhang, L. Li, S. W. Choi, M. R. MacEwan, J. Yao, C. Kim, Y. Xia, and L. V. Wang, “Investigation of neovascularization in three-dimensional porous scaffolds in vivo by a combination of multiscale photoacoustic microscopy and optical coherence tomography,” Tissue Eng. Part C Methods19(3), 196–204 (2013).
[CrossRef] [PubMed]

L. Li, K. Maslov, G. Ku, and L. V. Wang, “Three-dimensional combined photoacoustic and optical coherence microscopy for in vivo microcirculation studies,” Opt. Express17(19), 16450–16455 (2009).
[CrossRef] [PubMed]

Li, Z.

H. Wan, S. Korzh, Z. Li, S. P. Mudumana, V. Korzh, Y.-J. Jiang, S. Lin, and Z. Gong, “Analyses of pancreas development by generation of gfp transgenic zebrafish using an exocrine pancreas-specific elastaseA gene promoter,” Exp. Cell Res.312(9), 1526–1539 (2006).
[CrossRef] [PubMed]

Lichtman, J. W.

J. W. Lichtman and J.-A. Conchello, “Fluorescence microscopy,” Nat. Methods2(12), 910–919 (2005).
[CrossRef] [PubMed]

Lin, S.

H. Wan, S. Korzh, Z. Li, S. P. Mudumana, V. Korzh, Y.-J. Jiang, S. Lin, and Z. Gong, “Analyses of pancreas development by generation of gfp transgenic zebrafish using an exocrine pancreas-specific elastaseA gene promoter,” Exp. Cell Res.312(9), 1526–1539 (2006).
[CrossRef] [PubMed]

Liu, S.

S. Liu and S. D. Leach, “Screening pancreatic oncogenes in zebrafish using the Gal4/UAS system,” Methods Cell Biol.105, 367–381 (2011).
[CrossRef] [PubMed]

Lythgoe, M.

J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt.17(6), 061220 (2012).
[CrossRef] [PubMed]

Ma, R.

R. Ma, M. Distel, X. L. Deán-Ben, V. Ntziachristos, and D. Razansky, “Non-invasive whole-body imaging of adult zebrafish with optoacoustic tomography,” Phys. Med. Biol.57(22), 7227–7237 (2012).
[CrossRef] [PubMed]

D. Razansky, M. Distel, C. Vinegoni, R. Ma, N. Perrimon, R. W. Köster, and V. Ntziachristos, “Multispectral opto-acoustic tomography of deep-seated fluorescent proteins in vivo,” Nat. Photonics3(7), 412–417 (2009).
[CrossRef]

MacEwan, M. R.

X. Cai, Y. Zhang, L. Li, S. W. Choi, M. R. MacEwan, J. Yao, C. Kim, Y. Xia, and L. V. Wang, “Investigation of neovascularization in three-dimensional porous scaffolds in vivo by a combination of multiscale photoacoustic microscopy and optical coherence tomography,” Tissue Eng. Part C Methods19(3), 196–204 (2013).
[CrossRef] [PubMed]

Maslov, K.

L. Nie, X. Cai, K. Maslov, A. Garcia-Uribe, M. A. Anastasio, and L. V. Wang, “Photoacoustic tomography through a whole adult human skull with a photon recycler,” J. Biomed. Opt.17(11), 110506 (2012).
[CrossRef] [PubMed]

L. Li, K. Maslov, G. Ku, and L. V. Wang, “Three-dimensional combined photoacoustic and optical coherence microscopy for in vivo microcirculation studies,” Opt. Express17(19), 16450–16455 (2009).
[CrossRef] [PubMed]

Mauch, C. P.

H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods4(4), 331–336 (2007).
[CrossRef] [PubMed]

McGinty, J.

Moss, J. B.

J. B. Moss, P. Koustubhan, M. Greenman, M. J. Parsons, I. Walter, and L. G. Moss, “Regeneration of the pancreas in adult zebrafish,” Diabetes58(8), 1844–1851 (2009).
[CrossRef] [PubMed]

Moss, L. G.

J. B. Moss, P. Koustubhan, M. Greenman, M. J. Parsons, I. Walter, and L. G. Moss, “Regeneration of the pancreas in adult zebrafish,” Diabetes58(8), 1844–1851 (2009).
[CrossRef] [PubMed]

Mudumana, S. P.

H. Wan, S. Korzh, Z. Li, S. P. Mudumana, V. Korzh, Y.-J. Jiang, S. Lin, and Z. Gong, “Analyses of pancreas development by generation of gfp transgenic zebrafish using an exocrine pancreas-specific elastaseA gene promoter,” Exp. Cell Res.312(9), 1526–1539 (2006).
[CrossRef] [PubMed]

Nemecek, R.

A. Alex, J. Weingast, M. Weinigel, M. Kellner-Höfer, R. Nemecek, M. Binder, H. Pehamberger, K. König, and W. Drexler, “Three-dimensional multiphoton/optical coherence tomography for diagnostic applications in dermatology,” J Biophotonics6(4), 352–362 (2013).
[CrossRef] [PubMed]

Nie, L.

L. Nie, X. Cai, K. Maslov, A. Garcia-Uribe, M. A. Anastasio, and L. V. Wang, “Photoacoustic tomography through a whole adult human skull with a photon recycler,” J. Biomed. Opt.17(11), 110506 (2012).
[CrossRef] [PubMed]

C. Huang, L. Nie, R. W. Schoonover, Z. Guo, C. O. Schirra, M. A. Anastasio, and L. V. Wang, “Aberration correction for transcranial photoacoustic tomography of primates employing adjunct image data,” J. Biomed. Opt.17(6), 066016 (2012).
[CrossRef] [PubMed]

Norris, F.

J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt.17(6), 061220 (2012).
[CrossRef] [PubMed]

Ntziachristos, V.

R. Ma, M. Distel, X. L. Deán-Ben, V. Ntziachristos, and D. Razansky, “Non-invasive whole-body imaging of adult zebrafish with optoacoustic tomography,” Phys. Med. Biol.57(22), 7227–7237 (2012).
[CrossRef] [PubMed]

D. Razansky, M. Distel, C. Vinegoni, R. Ma, N. Perrimon, R. W. Köster, and V. Ntziachristos, “Multispectral opto-acoustic tomography of deep-seated fluorescent proteins in vivo,” Nat. Photonics3(7), 412–417 (2009).
[CrossRef]

Parsons, M. J.

J. B. Moss, P. Koustubhan, M. Greenman, M. J. Parsons, I. Walter, and L. G. Moss, “Regeneration of the pancreas in adult zebrafish,” Diabetes58(8), 1844–1851 (2009).
[CrossRef] [PubMed]

Pedley, B.

Pehamberger, H.

A. Alex, J. Weingast, M. Weinigel, M. Kellner-Höfer, R. Nemecek, M. Binder, H. Pehamberger, K. König, and W. Drexler, “Three-dimensional multiphoton/optical coherence tomography for diagnostic applications in dermatology,” J Biophotonics6(4), 352–362 (2013).
[CrossRef] [PubMed]

Perrimon, N.

D. Razansky, M. Distel, C. Vinegoni, R. Ma, N. Perrimon, R. W. Köster, and V. Ntziachristos, “Multispectral opto-acoustic tomography of deep-seated fluorescent proteins in vivo,” Nat. Photonics3(7), 412–417 (2009).
[CrossRef]

Perry, P.

J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson, “Optical projection tomography as a tool for 3D microscopy and gene expression studies,” Science296(5567), 541–545 (2002).
[CrossRef] [PubMed]

Popov, S.

A. Alex, B. Považay, B. Hofer, S. Popov, C. Glittenberg, S. Binder, and W. Drexler, “Multispectral in vivo three-dimensional optical coherence tomography of human skin,” J. Biomed. Opt.15(2), 026025 (2010).
[CrossRef] [PubMed]

Poss, K. D.

W. Y. Choi and K. D. Poss, “Cardiac regeneration,” Curr. Top. Dev. Biol.100, 319–344 (2012).
[CrossRef] [PubMed]

Povazay, B.

Považay, B.

A. Alex, B. Považay, B. Hofer, S. Popov, C. Glittenberg, S. Binder, and W. Drexler, “Multispectral in vivo three-dimensional optical coherence tomography of human skin,” J. Biomed. Opt.15(2), 026025 (2010).
[CrossRef] [PubMed]

Pule, M.

J. Laufer, A. Jathoul, M. Pule, and P. Beard, “Evaluation of genetically expressed absorbing proteins using photoacoustic spectroscopy,” Proc. SPIE8581, 85810X, 85810X-6 (2013).
[CrossRef]

Puliafito, C. A.

Razansky, D.

R. Ma, M. Distel, X. L. Deán-Ben, V. Ntziachristos, and D. Razansky, “Non-invasive whole-body imaging of adult zebrafish with optoacoustic tomography,” Phys. Med. Biol.57(22), 7227–7237 (2012).
[CrossRef] [PubMed]

D. Razansky, M. Distel, C. Vinegoni, R. Ma, N. Perrimon, R. W. Köster, and V. Ntziachristos, “Multispectral opto-acoustic tomography of deep-seated fluorescent proteins in vivo,” Nat. Photonics3(7), 412–417 (2009).
[CrossRef]

Ren, Q.

Rice, B. W.

B. W. Rice and C. H. Contag, “The importance of being red,” Nat. Biotechnol.27(7), 624–625 (2009).
[CrossRef] [PubMed]

Ross, A.

J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson, “Optical projection tomography as a tool for 3D microscopy and gene expression studies,” Science296(5567), 541–545 (2002).
[CrossRef] [PubMed]

Rouhi, P.

Z. Cao, L. D. Jensen, P. Rouhi, K. Hosaka, T. Länne, J. F. Steffensen, E. Wahlberg, and Y. Cao, “Hypoxia-induced retinopathy model in adult zebrafish,” Nat. Protoc.5(12), 1903–1910 (2010).
[CrossRef] [PubMed]

Saito, M.

N. Furukawa, M. Saito, T. Hakoshima, and K. Kohno, “A Diphtheria Toxin Receptor Deficient in Epidermal Growth Factor-Like Biological Activity,” J. Biochem.140(6), 831–841 (2006).
[CrossRef] [PubMed]

Scambler, P.

J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt.17(6), 061220 (2012).
[CrossRef] [PubMed]

Schierloh, A.

H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods4(4), 331–336 (2007).
[CrossRef] [PubMed]

Schirra, C. O.

C. Huang, L. Nie, R. W. Schoonover, Z. Guo, C. O. Schirra, M. A. Anastasio, and L. V. Wang, “Aberration correction for transcranial photoacoustic tomography of primates employing adjunct image data,” J. Biomed. Opt.17(6), 066016 (2012).
[CrossRef] [PubMed]

Schoonover, R. W.

C. Huang, L. Nie, R. W. Schoonover, Z. Guo, C. O. Schirra, M. A. Anastasio, and L. V. Wang, “Aberration correction for transcranial photoacoustic tomography of primates employing adjunct image data,” J. Biomed. Opt.17(6), 066016 (2012).
[CrossRef] [PubMed]

Sharpe, J.

J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson, “Optical projection tomography as a tool for 3D microscopy and gene expression studies,” Science296(5567), 541–545 (2002).
[CrossRef] [PubMed]

Shive, H. R.

H. R. Shive, “Zebrafish Models for Human Cancer,” Vet. Pathol.50(3), 468–482 (2013).
[CrossRef] [PubMed]

Shung, K. K.

Song, K. H.

K. H. Song and L. V. Wang, “Deep reflection-mode photoacoustic imaging of biological tissue,” J. Biomed. Opt.12(6), 060503 (2007).
[CrossRef] [PubMed]

Steffensen, J. F.

Z. Cao, L. D. Jensen, P. Rouhi, K. Hosaka, T. Länne, J. F. Steffensen, E. Wahlberg, and Y. Cao, “Hypoxia-induced retinopathy model in adult zebrafish,” Nat. Protoc.5(12), 1903–1910 (2010).
[CrossRef] [PubMed]

Stelzer, E. H. K.

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical Sectioning Deep Inside Live Embryos by Selective Plane Illumination Microscopy,” Science305(5686), 1007–1009 (2004).
[CrossRef] [PubMed]

Swoger, J.

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical Sectioning Deep Inside Live Embryos by Selective Plane Illumination Microscopy,” Science305(5686), 1007–1009 (2004).
[CrossRef] [PubMed]

Taylor, H. B.

Treeby, B.

J. Laufer, P. Johnson, E. Zhang, B. Treeby, B. Cox, B. Pedley, and P. Beard, “In vivo preclinical photoacoustic imaging of tumor vasculature development and therapy,” J. Biomed. Opt.17(5), 056016 (2012).
[CrossRef] [PubMed]

J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt.17(6), 061220 (2012).
[CrossRef] [PubMed]

E. Z. Zhang, B. Povazay, J. Laufer, A. Alex, B. Hofer, B. Pedley, C. Glittenberg, B. Treeby, B. Cox, P. Beard, and W. Drexler, “Multimodal photoacoustic and optical coherence tomography scanner using an all optical detection scheme for 3D morphological skin imaging,” Biomed. Opt. Express2(8), 2202–2215 (2011).
[CrossRef] [PubMed]

Treeby, B. E.

B. E. Treeby and B. T. Cox, “k-Wave: MATLAB toolbox for the simulation and reconstruction of photoacoustic wave fields,” J. Biomed. Opt.15(2), 021314 (2010).
[CrossRef] [PubMed]

Verkhusha, V. V.

G. S. Filonov, A. Krumholz, J. Xia, J. Yao, L. V. Wang, and V. V. Verkhusha, “Deep-Tissue Photoacoustic Tomography of a Genetically Encoded Near-Infrared Fluorescent Probe,” Angew. Chem.51(6), 1448–1451 (2012).
[CrossRef] [PubMed]

Vinegoni, C.

D. Razansky, M. Distel, C. Vinegoni, R. Ma, N. Perrimon, R. W. Köster, and V. Ntziachristos, “Multispectral opto-acoustic tomography of deep-seated fluorescent proteins in vivo,” Nat. Photonics3(7), 412–417 (2009).
[CrossRef]

Wahlberg, E.

Z. Cao, L. D. Jensen, P. Rouhi, K. Hosaka, T. Länne, J. F. Steffensen, E. Wahlberg, and Y. Cao, “Hypoxia-induced retinopathy model in adult zebrafish,” Nat. Protoc.5(12), 1903–1910 (2010).
[CrossRef] [PubMed]

Walter, I.

J. B. Moss, P. Koustubhan, M. Greenman, M. J. Parsons, I. Walter, and L. G. Moss, “Regeneration of the pancreas in adult zebrafish,” Diabetes58(8), 1844–1851 (2009).
[CrossRef] [PubMed]

Wan, H.

H. Wan, S. Korzh, Z. Li, S. P. Mudumana, V. Korzh, Y.-J. Jiang, S. Lin, and Z. Gong, “Analyses of pancreas development by generation of gfp transgenic zebrafish using an exocrine pancreas-specific elastaseA gene promoter,” Exp. Cell Res.312(9), 1526–1539 (2006).
[CrossRef] [PubMed]

Wang, L. V.

X. Cai, Y. Zhang, L. Li, S. W. Choi, M. R. MacEwan, J. Yao, C. Kim, Y. Xia, and L. V. Wang, “Investigation of neovascularization in three-dimensional porous scaffolds in vivo by a combination of multiscale photoacoustic microscopy and optical coherence tomography,” Tissue Eng. Part C Methods19(3), 196–204 (2013).
[CrossRef] [PubMed]

G. S. Filonov, A. Krumholz, J. Xia, J. Yao, L. V. Wang, and V. V. Verkhusha, “Deep-Tissue Photoacoustic Tomography of a Genetically Encoded Near-Infrared Fluorescent Probe,” Angew. Chem.51(6), 1448–1451 (2012).
[CrossRef] [PubMed]

C. Huang, L. Nie, R. W. Schoonover, Z. Guo, C. O. Schirra, M. A. Anastasio, and L. V. Wang, “Aberration correction for transcranial photoacoustic tomography of primates employing adjunct image data,” J. Biomed. Opt.17(6), 066016 (2012).
[CrossRef] [PubMed]

L. Nie, X. Cai, K. Maslov, A. Garcia-Uribe, M. A. Anastasio, and L. V. Wang, “Photoacoustic tomography through a whole adult human skull with a photon recycler,” J. Biomed. Opt.17(11), 110506 (2012).
[CrossRef] [PubMed]

L. Li, K. Maslov, G. Ku, and L. V. Wang, “Three-dimensional combined photoacoustic and optical coherence microscopy for in vivo microcirculation studies,” Opt. Express17(19), 16450–16455 (2009).
[CrossRef] [PubMed]

K. H. Song and L. V. Wang, “Deep reflection-mode photoacoustic imaging of biological tissue,” J. Biomed. Opt.12(6), 060503 (2007).
[CrossRef] [PubMed]

Weingast, J.

A. Alex, J. Weingast, M. Weinigel, M. Kellner-Höfer, R. Nemecek, M. Binder, H. Pehamberger, K. König, and W. Drexler, “Three-dimensional multiphoton/optical coherence tomography for diagnostic applications in dermatology,” J Biophotonics6(4), 352–362 (2013).
[CrossRef] [PubMed]

Weinigel, M.

A. Alex, J. Weingast, M. Weinigel, M. Kellner-Höfer, R. Nemecek, M. Binder, H. Pehamberger, K. König, and W. Drexler, “Three-dimensional multiphoton/optical coherence tomography for diagnostic applications in dermatology,” J Biophotonics6(4), 352–362 (2013).
[CrossRef] [PubMed]

Wittbrodt, J.

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical Sectioning Deep Inside Live Embryos by Selective Plane Illumination Microscopy,” Science305(5686), 1007–1009 (2004).
[CrossRef] [PubMed]

Xi, L.

Xia, J.

G. S. Filonov, A. Krumholz, J. Xia, J. Yao, L. V. Wang, and V. V. Verkhusha, “Deep-Tissue Photoacoustic Tomography of a Genetically Encoded Near-Infrared Fluorescent Probe,” Angew. Chem.51(6), 1448–1451 (2012).
[CrossRef] [PubMed]

Xia, Y.

X. Cai, Y. Zhang, L. Li, S. W. Choi, M. R. MacEwan, J. Yao, C. Kim, Y. Xia, and L. V. Wang, “Investigation of neovascularization in three-dimensional porous scaffolds in vivo by a combination of multiscale photoacoustic microscopy and optical coherence tomography,” Tissue Eng. Part C Methods19(3), 196–204 (2013).
[CrossRef] [PubMed]

Xie, H.

Xie, Z.

Xiong, J.

Yang, R.

Yao, J.

X. Cai, Y. Zhang, L. Li, S. W. Choi, M. R. MacEwan, J. Yao, C. Kim, Y. Xia, and L. V. Wang, “Investigation of neovascularization in three-dimensional porous scaffolds in vivo by a combination of multiscale photoacoustic microscopy and optical coherence tomography,” Tissue Eng. Part C Methods19(3), 196–204 (2013).
[CrossRef] [PubMed]

G. S. Filonov, A. Krumholz, J. Xia, J. Yao, L. V. Wang, and V. V. Verkhusha, “Deep-Tissue Photoacoustic Tomography of a Genetically Encoded Near-Infrared Fluorescent Probe,” Angew. Chem.51(6), 1448–1451 (2012).
[CrossRef] [PubMed]

Ye, S.

Zhang, E.

J. Laufer, P. Johnson, E. Zhang, B. Treeby, B. Cox, B. Pedley, and P. Beard, “In vivo preclinical photoacoustic imaging of tumor vasculature development and therapy,” J. Biomed. Opt.17(5), 056016 (2012).
[CrossRef] [PubMed]

J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt.17(6), 061220 (2012).
[CrossRef] [PubMed]

E. Zhang, J. Laufer, and P. Beard, “Backward-mode multiwavelength photoacoustic scanner using a planar Fabry-Perot polymer film ultrasound sensor for high-resolution three-dimensional imaging of biological tissues,” Appl. Opt.47(4), 561–577 (2008).
[CrossRef] [PubMed]

E. Zhang and P. Beard, “Broadband ultrasound field mapping system using a wavelength tuned, optically scanned focused laser beam to address a Fabry Perot polymer film sensor,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control53(7), 1330–1338 (2006).
[CrossRef] [PubMed]

Zhang, E. Z.

Zhang, H. F.

X. Zhang, H. F. Zhang, and S. Jiao, “Optical coherence photoacoustic microscopy: accomplishing optical coherence tomography and photoacoustic microscopy with a single light source,” J. Biomed. Opt.17(3), 030502 (2012).
[CrossRef] [PubMed]

S. Jiao, Z. Xie, H. F. Zhang, and C. A. Puliafito, “Simultaneous multimodal imaging with integrated photoacoustic microscopy and optical coherence tomography,” Opt. Lett.34(19), 2961–2963 (2009).
[CrossRef] [PubMed]

Zhang, X.

X. Zhang, H. F. Zhang, and S. Jiao, “Optical coherence photoacoustic microscopy: accomplishing optical coherence tomography and photoacoustic microscopy with a single light source,” J. Biomed. Opt.17(3), 030502 (2012).
[CrossRef] [PubMed]

Zhang, Y.

X. Cai, Y. Zhang, L. Li, S. W. Choi, M. R. MacEwan, J. Yao, C. Kim, Y. Xia, and L. V. Wang, “Investigation of neovascularization in three-dimensional porous scaffolds in vivo by a combination of multiscale photoacoustic microscopy and optical coherence tomography,” Tissue Eng. Part C Methods19(3), 196–204 (2013).
[CrossRef] [PubMed]

Zhou, Q.

Zieglgänsberger, W.

H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods4(4), 331–336 (2007).
[CrossRef] [PubMed]

Angew. Chem. (1)

G. S. Filonov, A. Krumholz, J. Xia, J. Yao, L. V. Wang, and V. V. Verkhusha, “Deep-Tissue Photoacoustic Tomography of a Genetically Encoded Near-Infrared Fluorescent Probe,” Angew. Chem.51(6), 1448–1451 (2012).
[CrossRef] [PubMed]

Appl. Opt. (3)

Biomed. Opt. Express (3)

Curr. Top. Dev. Biol. (1)

W. Y. Choi and K. D. Poss, “Cardiac regeneration,” Curr. Top. Dev. Biol.100, 319–344 (2012).
[CrossRef] [PubMed]

Dev. Neurobiol. (1)

C. Kizil, J. Kaslin, V. Kroehne, and M. Brand, “Adult neurogenesis and brain regeneration in zebrafish,” Dev. Neurobiol.72(3), 429–461 (2012).
[CrossRef] [PubMed]

Diabetes (1)

J. B. Moss, P. Koustubhan, M. Greenman, M. J. Parsons, I. Walter, and L. G. Moss, “Regeneration of the pancreas in adult zebrafish,” Diabetes58(8), 1844–1851 (2009).
[CrossRef] [PubMed]

Dis. Model. Mech. (1)

M. R. Fein and M. Egeblad, “Caught in the act: revealing the metastatic process by live imaging,” Dis. Model. Mech.6(3), 580–593 (2013).
[CrossRef] [PubMed]

Exp. Cell Res. (1)

H. Wan, S. Korzh, Z. Li, S. P. Mudumana, V. Korzh, Y.-J. Jiang, S. Lin, and Z. Gong, “Analyses of pancreas development by generation of gfp transgenic zebrafish using an exocrine pancreas-specific elastaseA gene promoter,” Exp. Cell Res.312(9), 1526–1539 (2006).
[CrossRef] [PubMed]

IEEE Trans. Ultrason. Ferroelectr. Freq. Control (1)

E. Zhang and P. Beard, “Broadband ultrasound field mapping system using a wavelength tuned, optically scanned focused laser beam to address a Fabry Perot polymer film sensor,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control53(7), 1330–1338 (2006).
[CrossRef] [PubMed]

Interface Focus (1)

P. Beard, “Biomedical photoacoustic imaging,” Interface Focus1(4), 602–631 (2011).
[CrossRef] [PubMed]

J Biophotonics (1)

A. Alex, J. Weingast, M. Weinigel, M. Kellner-Höfer, R. Nemecek, M. Binder, H. Pehamberger, K. König, and W. Drexler, “Three-dimensional multiphoton/optical coherence tomography for diagnostic applications in dermatology,” J Biophotonics6(4), 352–362 (2013).
[CrossRef] [PubMed]

J. Biochem. (1)

N. Furukawa, M. Saito, T. Hakoshima, and K. Kohno, “A Diphtheria Toxin Receptor Deficient in Epidermal Growth Factor-Like Biological Activity,” J. Biochem.140(6), 831–841 (2006).
[CrossRef] [PubMed]

J. Biomed. Opt. (9)

B. E. Treeby and B. T. Cox, “k-Wave: MATLAB toolbox for the simulation and reconstruction of photoacoustic wave fields,” J. Biomed. Opt.15(2), 021314 (2010).
[CrossRef] [PubMed]

A. Alex, B. Považay, B. Hofer, S. Popov, C. Glittenberg, S. Binder, and W. Drexler, “Multispectral in vivo three-dimensional optical coherence tomography of human skin,” J. Biomed. Opt.15(2), 026025 (2010).
[CrossRef] [PubMed]

X. Zhang, H. F. Zhang, and S. Jiao, “Optical coherence photoacoustic microscopy: accomplishing optical coherence tomography and photoacoustic microscopy with a single light source,” J. Biomed. Opt.17(3), 030502 (2012).
[CrossRef] [PubMed]

J. Laufer, P. Johnson, E. Zhang, B. Treeby, B. Cox, B. Pedley, and P. Beard, “In vivo preclinical photoacoustic imaging of tumor vasculature development and therapy,” J. Biomed. Opt.17(5), 056016 (2012).
[CrossRef] [PubMed]

J. Laufer, F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, “In vivo photoacoustic imaging of mouse embryos,” J. Biomed. Opt.17(6), 061220 (2012).
[CrossRef] [PubMed]

B. Cox, J. G. Laufer, S. R. Arridge, and P. C. Beard, “Quantitative spectroscopic photoacoustic imaging: a review,” J. Biomed. Opt.17(6), 061202 (2012).
[CrossRef] [PubMed]

K. H. Song and L. V. Wang, “Deep reflection-mode photoacoustic imaging of biological tissue,” J. Biomed. Opt.12(6), 060503 (2007).
[CrossRef] [PubMed]

C. Huang, L. Nie, R. W. Schoonover, Z. Guo, C. O. Schirra, M. A. Anastasio, and L. V. Wang, “Aberration correction for transcranial photoacoustic tomography of primates employing adjunct image data,” J. Biomed. Opt.17(6), 066016 (2012).
[CrossRef] [PubMed]

L. Nie, X. Cai, K. Maslov, A. Garcia-Uribe, M. A. Anastasio, and L. V. Wang, “Photoacoustic tomography through a whole adult human skull with a photon recycler,” J. Biomed. Opt.17(11), 110506 (2012).
[CrossRef] [PubMed]

Methods Cell Biol. (1)

S. Liu and S. D. Leach, “Screening pancreatic oncogenes in zebrafish using the Gal4/UAS system,” Methods Cell Biol.105, 367–381 (2011).
[CrossRef] [PubMed]

Nat. Biotechnol. (1)

B. W. Rice and C. H. Contag, “The importance of being red,” Nat. Biotechnol.27(7), 624–625 (2009).
[CrossRef] [PubMed]

Nat. Methods (2)

J. W. Lichtman and J.-A. Conchello, “Fluorescence microscopy,” Nat. Methods2(12), 910–919 (2005).
[CrossRef] [PubMed]

H. U. Dodt, U. Leischner, A. Schierloh, N. Jährling, C. P. Mauch, K. Deininger, J. M. Deussing, M. Eder, W. Zieglgänsberger, and K. Becker, “Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain,” Nat. Methods4(4), 331–336 (2007).
[CrossRef] [PubMed]

Nat. Photonics (1)

D. Razansky, M. Distel, C. Vinegoni, R. Ma, N. Perrimon, R. W. Köster, and V. Ntziachristos, “Multispectral opto-acoustic tomography of deep-seated fluorescent proteins in vivo,” Nat. Photonics3(7), 412–417 (2009).
[CrossRef]

Nat. Protoc. (1)

Z. Cao, L. D. Jensen, P. Rouhi, K. Hosaka, T. Länne, J. F. Steffensen, E. Wahlberg, and Y. Cao, “Hypoxia-induced retinopathy model in adult zebrafish,” Nat. Protoc.5(12), 1903–1910 (2010).
[CrossRef] [PubMed]

Opt. Express (2)

Opt. Lett. (1)

Phys. Med. Biol. (1)

R. Ma, M. Distel, X. L. Deán-Ben, V. Ntziachristos, and D. Razansky, “Non-invasive whole-body imaging of adult zebrafish with optoacoustic tomography,” Phys. Med. Biol.57(22), 7227–7237 (2012).
[CrossRef] [PubMed]

Proc. SPIE (1)

J. Laufer, A. Jathoul, M. Pule, and P. Beard, “Evaluation of genetically expressed absorbing proteins using photoacoustic spectroscopy,” Proc. SPIE8581, 85810X, 85810X-6 (2013).
[CrossRef]

Science (2)

J. Sharpe, U. Ahlgren, P. Perry, B. Hill, A. Ross, J. Hecksher-Sørensen, R. Baldock, and D. Davidson, “Optical projection tomography as a tool for 3D microscopy and gene expression studies,” Science296(5567), 541–545 (2002).
[CrossRef] [PubMed]

J. Huisken, J. Swoger, F. Del Bene, J. Wittbrodt, and E. H. K. Stelzer, “Optical Sectioning Deep Inside Live Embryos by Selective Plane Illumination Microscopy,” Science305(5686), 1007–1009 (2004).
[CrossRef] [PubMed]

Tissue Eng. Part C Methods (1)

X. Cai, Y. Zhang, L. Li, S. W. Choi, M. R. MacEwan, J. Yao, C. Kim, Y. Xia, and L. V. Wang, “Investigation of neovascularization in three-dimensional porous scaffolds in vivo by a combination of multiscale photoacoustic microscopy and optical coherence tomography,” Tissue Eng. Part C Methods19(3), 196–204 (2013).
[CrossRef] [PubMed]

Vet. Pathol. (1)

H. R. Shive, “Zebrafish Models for Human Cancer,” Vet. Pathol.50(3), 468–482 (2013).
[CrossRef] [PubMed]

Other (3)

L. V. Wang and H.-i. Wu, Biomedical Optics: Principles and Imaging (Wiley-Interscience, Hoboken, N.J., 2007).

M. Westerfield, The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio Rerio). 4th ed. (Eugene: University of Oregon Press, 2000).

American National Standards Institute, “American National Standard for Safe Use of Lasers,” ANSI Z136.1 2007–1 (2007).

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Figures (6)

Fig. 1
Fig. 1

(a) Schematic of the PAT system. AI: analog input; AO: analog output; SCB 68: the connector block for NI PCIe 6323; FPI: Fabry-Perot interferometer polymer film sensor; PD: photodiode; C: circulator; CM: concave mirror; CL: collimator; L1: focusing lens for OPO output; L2: objective lens; F: multimode fiber delivering the excitation laser beam; M: mirror. (b) A photograph of the scanning unit of the PAT system. (c) A reconstructed cross section of the inked fiber imaged using the PAT system with z axis being the depth dimension and x axis the lateral dimension. (d) A plot through the center of the inked fiber shown in (c). Gaussian fitting to the raw data points was performed and the full width at half maximum (FWHM) of the fitted curve represents the lateral resolution of the system. (e) Similar to (d), but in the axial direction.

Fig. 2
Fig. 2

Photoacoustic spectra of E2-Crimson and mCherry, adapted from [36].

Fig. 3
Fig. 3

Maximum amplitude projection (MAP) images of the E2-Crimson expressing zebrafish acquired at 611 nm (a) and 640 nm (b) displayed over 18 dB dynamic range. (c) is an SD-OCT MAP image of the E2-Crimson expressing fish. (d) and (e) are MAP images of a negative control fish imaged at 611 nm and 640 nm, respectively.

Fig. 4
Fig. 4

(a) E2-Crimson distribution (blue) acquired by spectroscopic PAT. (b) Epifluorescence photo of the adult zebrafish showing E2-Crimson (red). (c) Overlay of (a) and (b).

Fig. 5
Fig. 5

Sagittal sections of the zebrafish using PAT at five representative depths. Left and middle columns use the data acquired at 611 nm and 640 nm, respectively. The right column shows the multispectral processed results with the exocrine pancreas labeled by E2-Crimson. E: eye; G: gills; FP: fluorescent protein labeled exocrine pancreas; L: liver; AV: aorta and vein.

Fig. 6
Fig. 6

(a) & (c): PAT images acquired at the depths of 804 µm and 1176 µm, respectively with the FP labeled exocrine pancreas processed from spectroscopic PAT overlaid in red. (b) & (d): Histological sections at approximate depths as (a) and (c), respectively. (e) is an SD-OCT B-mode image of the zebrafish at approximately corresponding depth to (c). (f) is a zoomed-in display of the dashed region in (d). EP: exocrine pancreas; M: muscle; DF: dorsal fin; PF: pectoral fin; E: eye; AV: aorta and vein; G: gills; I: intersegmental vessels; VC: vertebral column; SB: swim bladder; O: ovary; IT: intestinal tracts; L: liver.

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