Abstract

We demonstrate the application of fluorescence lifetime optical projection tomography (FLIM-OPT) to in vivo imaging of lysC:GFP transgenic zebrafish embryos (Danio rerio). This method has been applied to unambiguously distinguish between the fluorescent protein (GFP) signal in myeloid cells from background autofluorescence based on the fluorescence lifetime. The combination of FLIM, an inherently ratiometric method, in conjunction with OPT results in a quantitative 3-D tomographic technique that could be used as a robust method for in vivo biological and pharmaceutical research, for example as a readout of Förster resonance energy transfer based interactions.

© 2011 OSA

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2011 (3)

S. Kumar, D. Alibhai, A. Margineanu, R. Laine, G. Kennedy, J. McGinty, S. Warren, D. Kelly, Y. Alexandrov, I. Munro, C. Talbot, D. W. Stuckey, C. Kimberly, B. Viellerobe, F. Lacombe, E. W.-F. Lam, H. Taylor, M. J. Dallman, G. Stamp, E. J. Murray, F. Stuhmeier, A. Sardini, M. Katan, D. S. Elson, M. A. A. Neil, C. Dunsby, and P. M. W. French, “FLIM FRET technology for drug discovery: automated multiwell-plate high-content analysis, multiplexed readouts and application in situ,” ChemPhysChem 12(3), 609–626 (2011).
[CrossRef] [PubMed]

J. I. Agulleiro and J. J. Fernandez, “Fast tomographic reconstruction on multicore computers,” Bioinformatics 27(4), 582–583 (2011).
[CrossRef] [PubMed]

V. Y. Soloviev and S. R. Arridge, “Optical Tomography in weakly scattering media in the presence of highly scattering inclusions,” Biomed. Opt. Express 2(3), 440–451 (2011).
[CrossRef] [PubMed]

2010 (4)

C. Pardo-Martin, T. Y. Chang, B. K. Koo, C. L. Gilleland, S. C. Wasserman, and M. F. Yanik, “High-throughput in vivo vertebrate screening,” Nat. Methods 7(8), 634–636 (2010).
[CrossRef] [PubMed]

A. M. Petzold, V. M. Bedell, N. J. Boczek, J. J. Essner, D. Balciunas, K. J. Clark, and S. C. Ekker, “SCORE imaging: specimen in a corrected optical rotational enclosure,” Zebrafish 7(2), 149–154 (2010).
[CrossRef] [PubMed]

G. T. Kennedy, H. B. Manning, D. S. Elson, M. A. A. Neil, G. W. Stamp, B. Viellerobe, F. Lacombe, C. Dunsby, and P. M. W. French, “A fluorescence lifetime imaging scanning confocal endomicroscope,” J Biophotonics 3(1-2), 103–107 (2010).
[CrossRef] [PubMed]

U. J. Birk, M. Rieckher, N. Konstantinides, A. Darrell, A. Sarasa-Renedo, H. Meyer, N. Tavernarakis, and J. Ripoll, “Correction for specimen movement and rotation errors for in-vivo Optical Projection Tomography,” Biomed. Opt. Express 1(1), 87–96 (2010).
[CrossRef] [PubMed]

2009 (2)

J. R. Mathias, M. E. Dodd, K. B. Walters, S. K. Yoo, E. A. Ranheim, and A. Huttenlocher, “Characterization of zebrafish larval inflammatory macrophages,” Dev. Comp. Immunol. 33(11), 1212–1217 (2009).
[CrossRef] [PubMed]

J. McGinty, J. Requejo-Isidro, I. Munro, C. B. Talbot, P. A. Kellett, J. D. Hares, C. Dunsby, M A A. Neil, and P. M. W. French, “Signal-to-noise characterization of time-gated intensifiers used for wide-field time-domain FLIM,” J. Phys. D Appl. Phys. 42(13), 135103 (2009).
[CrossRef]

2008 (8)

M. J. Boot, C. H. Westerberg, J. Sanz-Ezquerro, J. Cotterell, R. Schweitzer, M. Torres, and J. Sharpe, “In vitro whole-organ imaging: 4D quantification of growing mouse limb buds,” Nat. Methods 5(7), 609–612 (2008).
[CrossRef] [PubMed]

J. McGinty, K. B. Tahir, R. Laine, C. B. Talbot, C. Dunsby, M. A. A. Neil, L. Quintana, J. Swoger, J. Sharpe, and P. M. W. French, “Fluorescence lifetime optical projection tomography,” J Biophotonics 1(5), 390–394 (2008).
[CrossRef] [PubMed]

T. P. Barros, W. K. Alderton, H. M. Reynolds, A. G. Roach, and S. Berghmans, “Zebrafish: an emerging technology for in vivo pharmacological assessment to identify potential safety liabilities in early drug discovery,” Br. J. Pharmacol. 154(7), 1400–1413 (2008).
[CrossRef] [PubMed]

C. Vinegoni, C. Pitsouli, D. Razansky, N. Perrimon, and V. Ntziachristos, “In vivo imaging of Drosophila melanogaster pupae with mesoscopic fluorescence tomography,” Nat. Methods 5(1), 45–47 (2008).
[CrossRef] [PubMed]

M. Oldham, H. S. Sakhalkar, T. Oliver, G. Allan Johnson, and M. Dewhirst, “Optical clearing of unsectioned specimens for three-dimensional imaging via optical transmission and emission tomography,” J. Biomed. Opt. 13(2), 021113 (2008).
[CrossRef] [PubMed]

C. Dunsby, “Optically sectioned imaging by oblique plane microscopy,” Opt. Express 16(25), 20306–20316 (2008).
[CrossRef] [PubMed]

T. Nishioka, K. Aoki, K. Hikake, H. Yoshizaki, E. Kiyokawa, and M. Matsuda, “Rapid turnover rate of phosphoinositides at the front of migrating MDCK cells,” Mol. Biol. Cell 19(10), 4213–4223 (2008).
[CrossRef] [PubMed]

C. B. Talbot, J. McGinty, D. M. Grant, E. J. McGhee, D. M. Owen, W. Zhang, T. D. Bunney, I. Munro, B. Isherwood, R. Eagle, A. Hargreaves, C. Dunsby, M. A. Neil, and P. M. W. French, “High speed unsupervised fluorescence lifetime imaging confocal multiwell plate reader for high content analysis,” J Biophotonics 1(6), 514–521 (2008).
[CrossRef] [PubMed]

2007 (8)

H. S. Sakhalkar, M. Dewhirst, T. Oliver, Y. Cao, and M. Oldham, “Functional imaging in bulk tissue specimens using optical emission tomography: fluorescence preservation during optical clearing,” Phys. Med. Biol. 52(8), 2035–2054 (2007).
[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. Methods 4(4), 331–336 (2007).
[CrossRef] [PubMed]

M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
[CrossRef] [PubMed]

J. Huisken and D. Y. R. Stainier, “Even fluorescence excitation by multidirectional selective plane illumination microscopy (mSPIM),” Opt. Lett. 32(17), 2608–2610 (2007).
[CrossRef] [PubMed]

C. Hall, M. V. Flores, T. Storm, K. Crosier, and P. Crosier, “The zebrafish lysozyme C promoter drives myeloid-specific expression in transgenic fish,” BMC Dev. Biol. 7(1), 42 (2007).
[CrossRef] [PubMed]

G. Kari, U. Rodeck, and A. P. Dicker, “Zebrafish: an emerging model system for human disease and drug discovery,” Clin. Pharmacol. Ther. 82(1), 70–80 (2007).
[CrossRef] [PubMed]

D. Castaño Díez, H. Mueller, and A. S. Frangakis, “Implementation and performance evaluation of reconstruction algorithms on graphics processors,” J. Struct. Biol. 157(1), 288–295 (2007).
[CrossRef] [PubMed]

J. R. Walls, J. G. Sled, J. Sharpe, and R. M. Henkelman, “Resolution improvement in emission optical projection tomography,” Phys. Med. Biol. 52(10), 2775–2790 (2007).
[CrossRef] [PubMed]

2006 (7)

D. M. Owen, P. M. P. Lanigan, C. Dunsby, I. Munro, D. Grant, M. A. A. Neil, P. M. W. French, and A. I. Magee, “Fluorescence lifetime imaging provides enhanced contrast when imaging the phase-sensitive dye di-4-ANEPPDHQ in model membranes and live cells,” Biophys. J. 90(11), L80–L82 (2006).
[CrossRef] [PubMed]

A. Esposito, H. C. Gerritsen, T. Oggier, F. Lustenberger, and F. S. Wouters, “Innovating lifetime microscopy: a compact and simple tool for life sciences, screening, and diagnostics,” J. Biomed. Opt. 11(3), 034016 (2006).
[CrossRef] [PubMed]

D. Beis and D. Y. R. Stainier, “In vivo cell biology: following the zebrafish trend,” Trends Cell Biol. 16(2), 105–112 (2006).
[CrossRef] [PubMed]

P. J. Keller, F. Pampaloni, and E. H. K. Stelzer, “Life sciences require the third dimension,” Curr. Opin. Cell Biol. 18(1), 117–124 (2006).
[CrossRef] [PubMed]

A. Nezu, A. Tanimura, T. Morita, A. Shitara, and Y. Tojyo, “A novel fluorescent method employing the FRET-based biosensor “LIBRA” for the identification of ligands of the inositol 1,4,5-trisphosphate receptors,” Biochim. Biophys. Acta 1760(8), 1274–1280 (2006).
[PubMed]

I. T. Li, E. Pham, and K. Truong, “Protein biosensors based on the principle of fluorescence resonance energy transfer for monitoring cellular dynamics,” Biotechnol. Lett. 28(24), 1971–1982 (2006).
[CrossRef] [PubMed]

M. Mank, D. F. Reiff, N. Heim, M. W. Friedrich, A. Borst, and O. Griesbeck, “A FRET-based calcium biosensor with fast signal kinetics and high fluorescence change,” Biophys. J. 90(5), 1790–1796 (2006).
[CrossRef] [PubMed]

2005 (3)

C. G. Burns, D. J. Milan, E. J. Grande, W. Rottbauer, C. A. MacRae, and M. C. Fishman, “High-throughput assay for small molecules that modulate zebrafish embryonic heart rate,” Nat. Chem. Biol. 1(5), 263–264 (2005).
[CrossRef] [PubMed]

D. Stockholm, M. Bartoli, G. Sillon, N. Bourg, J. Davoust, and I. Richard, “Imaging calpain protease activity by multiphoton FRET in living mice,” J. Mol. Biol. 346(1), 215–222 (2005).
[CrossRef] [PubMed]

A. J. Hill, H. Teraoka, W. Heideman, and R. E. Peterson, “Zebrafish as a model vertebrate for investigating chemical toxicity,” Toxicol. Sci. 86(1), 6–19 (2005).
[CrossRef] [PubMed]

2004 (2)

C. Dunsby, P. M. P. Lanigan, J. McGinty, D. S. Elson, J. Requejo-Isidro, I. Munro, N. Galletly, F. McCann, B. Treanor, B. Onfelt, D. M. Davis, M. A. A. Neil, and P. M. W. French, “An electronically tunable ultrafast laser source applied to fluorescence imaging and fluorescence lifetime imaging microscopy,” J. Phys. D Appl. Phys. 37(23), 3296–3303 (2004).
[CrossRef]

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,” Science 305(5686), 1007–1009 (2004).
[CrossRef] [PubMed]

2003 (4)

E. A. Jares-Erijman and T. M. Jovin, “FRET imaging,” Nat. Biotechnol. 21(11), 1387–1395 (2003).
[CrossRef] [PubMed]

R. Weissleder and V. Ntziachristos, “Shedding light onto live molecular targets,” Nat. Med. 9(1), 123–128 (2003).
[CrossRef] [PubMed]

A. Abbott, “Cell culture: biology’s new dimension,” Nature 424(6951), 870–872 (2003).
[CrossRef] [PubMed]

L. K. van Geest and K. W. J. Stoop, “FLIM on a wide field fluorescence microscope,” Lett. Pept. Sci. 10(5-6), 501–510 (2003).
[CrossRef]

2002 (3)

H. Ueyama, M. Takagi, and S. Takenaka, “A novel potassium sensing in aqueous media with a synthetic oligonucleotide derivative. Fluorescence resonance energy transfer associated with Guanine quartet-potassium ion complex formation,” J. Am. Chem. Soc. 124(48), 14286–14287 (2002).
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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,” Science 296(5567), 541–545 (2002).
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2001 (1)

N. Mochizuki, S. Yamashita, K. Kurokawa, Y. Ohba, T. Nagai, A. Miyawaki, and M. Matsuda, “Spatio-temporal images of growth-factor-induced activation of Ras and Rap1,” Nature 411(6841), 1065–1068 (2001).
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2000 (1)

T. Kuner and G. J. Augustine, “A genetically encoded ratiometric indicator for chloride: capturing chloride transients in cultured hippocampal neurons,” Neuron 27(3), 447–459 (2000).
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1999 (1)

P. I. H. Bastiaens and A. Squire, “Fluorescence lifetime imaging microscopy: spatial resolution of biochemical processes in the cell,” Trends Cell Biol. 9(2), 48–52 (1999).
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1998 (2)

1997 (1)

K. Dowling, S. C. W. Hyde, J. C. Dainty, P. W. W. French, and J. D. Hares, “2-D fluorescence lifetime imaging using a time-gated image intensifier,” Opt. Commun. 135(1-3), 27–31 (1997).
[CrossRef]

1992 (2)

E. P. Buurman, R. Sanders, A. Draaijer, H. C. Gerritsen, J. J. F. Vanveen, P. M. Houpt, and Y. K. Levine, “Fluorescence lifetime imaging using a confocal laser scanning microscope,” Scanning 14, 155–159 (1992).

X. F. Wang, A. Periasamy, B. Herman, and D. M. Coleman, “Fluorescence lifetime imaging microscopy (FLIM): instrumentation and applications,” Crit. Rev. Anal. Chem. 23(5), 369–395 (1992).
[CrossRef]

1989 (1)

R. M. Ballew and J. N. Demas, “An error analysis of the rapid lifetime determination method for the evaluation of single exponential decay,” Anal. Chem. 61(1), 30–33 (1989).
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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,” Science 296(5567), 541–545 (2002).
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T. P. Barros, W. K. Alderton, H. M. Reynolds, A. G. Roach, and S. Berghmans, “Zebrafish: an emerging technology for in vivo pharmacological assessment to identify potential safety liabilities in early drug discovery,” Br. J. Pharmacol. 154(7), 1400–1413 (2008).
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Alibhai, D.

S. Kumar, D. Alibhai, A. Margineanu, R. Laine, G. Kennedy, J. McGinty, S. Warren, D. Kelly, Y. Alexandrov, I. Munro, C. Talbot, D. W. Stuckey, C. Kimberly, B. Viellerobe, F. Lacombe, E. W.-F. Lam, H. Taylor, M. J. Dallman, G. Stamp, E. J. Murray, F. Stuhmeier, A. Sardini, M. Katan, D. S. Elson, M. A. A. Neil, C. Dunsby, and P. M. W. French, “FLIM FRET technology for drug discovery: automated multiwell-plate high-content analysis, multiplexed readouts and application in situ,” ChemPhysChem 12(3), 609–626 (2011).
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Allan Johnson, G.

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Arridge, S. R.

Augustine, G. J.

T. Kuner and G. J. Augustine, “A genetically encoded ratiometric indicator for chloride: capturing chloride transients in cultured hippocampal neurons,” Neuron 27(3), 447–459 (2000).
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Balciunas, D.

A. M. Petzold, V. M. Bedell, N. J. Boczek, J. J. Essner, D. Balciunas, K. J. Clark, and S. C. Ekker, “SCORE imaging: specimen in a corrected optical rotational enclosure,” Zebrafish 7(2), 149–154 (2010).
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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,” Science 296(5567), 541–545 (2002).
[CrossRef] [PubMed]

Ballew, R. M.

R. M. Ballew and J. N. Demas, “An error analysis of the rapid lifetime determination method for the evaluation of single exponential decay,” Anal. Chem. 61(1), 30–33 (1989).
[CrossRef]

Barros, T. P.

T. P. Barros, W. K. Alderton, H. M. Reynolds, A. G. Roach, and S. Berghmans, “Zebrafish: an emerging technology for in vivo pharmacological assessment to identify potential safety liabilities in early drug discovery,” Br. J. Pharmacol. 154(7), 1400–1413 (2008).
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Bartoli, M.

D. Stockholm, M. Bartoli, G. Sillon, N. Bourg, J. Davoust, and I. Richard, “Imaging calpain protease activity by multiphoton FRET in living mice,” J. Mol. Biol. 346(1), 215–222 (2005).
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Bastiaens, P. I. H.

P. I. H. Bastiaens and A. Squire, “Fluorescence lifetime imaging microscopy: spatial resolution of biochemical processes in the cell,” Trends Cell Biol. 9(2), 48–52 (1999).
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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. Methods 4(4), 331–336 (2007).
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A. M. Petzold, V. M. Bedell, N. J. Boczek, J. J. Essner, D. Balciunas, K. J. Clark, and S. C. Ekker, “SCORE imaging: specimen in a corrected optical rotational enclosure,” Zebrafish 7(2), 149–154 (2010).
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D. Beis and D. Y. R. Stainier, “In vivo cell biology: following the zebrafish trend,” Trends Cell Biol. 16(2), 105–112 (2006).
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Berghmans, S.

T. P. Barros, W. K. Alderton, H. M. Reynolds, A. G. Roach, and S. Berghmans, “Zebrafish: an emerging technology for in vivo pharmacological assessment to identify potential safety liabilities in early drug discovery,” Br. J. Pharmacol. 154(7), 1400–1413 (2008).
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Birk, U. J.

Boczek, N. J.

A. M. Petzold, V. M. Bedell, N. J. Boczek, J. J. Essner, D. Balciunas, K. J. Clark, and S. C. Ekker, “SCORE imaging: specimen in a corrected optical rotational enclosure,” Zebrafish 7(2), 149–154 (2010).
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Boot, M. J.

M. J. Boot, C. H. Westerberg, J. Sanz-Ezquerro, J. Cotterell, R. Schweitzer, M. Torres, and J. Sharpe, “In vitro whole-organ imaging: 4D quantification of growing mouse limb buds,” Nat. Methods 5(7), 609–612 (2008).
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M. Mank, D. F. Reiff, N. Heim, M. W. Friedrich, A. Borst, and O. Griesbeck, “A FRET-based calcium biosensor with fast signal kinetics and high fluorescence change,” Biophys. J. 90(5), 1790–1796 (2006).
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Bourg, N.

D. Stockholm, M. Bartoli, G. Sillon, N. Bourg, J. Davoust, and I. Richard, “Imaging calpain protease activity by multiphoton FRET in living mice,” J. Mol. Biol. 346(1), 215–222 (2005).
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Bunney, T. D.

C. B. Talbot, J. McGinty, D. M. Grant, E. J. McGhee, D. M. Owen, W. Zhang, T. D. Bunney, I. Munro, B. Isherwood, R. Eagle, A. Hargreaves, C. Dunsby, M. A. Neil, and P. M. W. French, “High speed unsupervised fluorescence lifetime imaging confocal multiwell plate reader for high content analysis,” J Biophotonics 1(6), 514–521 (2008).
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Burns, C. G.

C. G. Burns, D. J. Milan, E. J. Grande, W. Rottbauer, C. A. MacRae, and M. C. Fishman, “High-throughput assay for small molecules that modulate zebrafish embryonic heart rate,” Nat. Chem. Biol. 1(5), 263–264 (2005).
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Buurman, E. P.

E. P. Buurman, R. Sanders, A. Draaijer, H. C. Gerritsen, J. J. F. Vanveen, P. M. Houpt, and Y. K. Levine, “Fluorescence lifetime imaging using a confocal laser scanning microscope,” Scanning 14, 155–159 (1992).

Cao, Y.

H. S. Sakhalkar, M. Dewhirst, T. Oliver, Y. Cao, and M. Oldham, “Functional imaging in bulk tissue specimens using optical emission tomography: fluorescence preservation during optical clearing,” Phys. Med. Biol. 52(8), 2035–2054 (2007).
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D. Castaño Díez, H. Mueller, and A. S. Frangakis, “Implementation and performance evaluation of reconstruction algorithms on graphics processors,” J. Struct. Biol. 157(1), 288–295 (2007).
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Chang, T. Y.

C. Pardo-Martin, T. Y. Chang, B. K. Koo, C. L. Gilleland, S. C. Wasserman, and M. F. Yanik, “High-throughput in vivo vertebrate screening,” Nat. Methods 7(8), 634–636 (2010).
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Clark, K. J.

A. M. Petzold, V. M. Bedell, N. J. Boczek, J. J. Essner, D. Balciunas, K. J. Clark, and S. C. Ekker, “SCORE imaging: specimen in a corrected optical rotational enclosure,” Zebrafish 7(2), 149–154 (2010).
[CrossRef] [PubMed]

Coleman, D. M.

X. F. Wang, A. Periasamy, B. Herman, and D. M. Coleman, “Fluorescence lifetime imaging microscopy (FLIM): instrumentation and applications,” Crit. Rev. Anal. Chem. 23(5), 369–395 (1992).
[CrossRef]

Cotterell, J.

M. J. Boot, C. H. Westerberg, J. Sanz-Ezquerro, J. Cotterell, R. Schweitzer, M. Torres, and J. Sharpe, “In vitro whole-organ imaging: 4D quantification of growing mouse limb buds,” Nat. Methods 5(7), 609–612 (2008).
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C. Hall, M. V. Flores, T. Storm, K. Crosier, and P. Crosier, “The zebrafish lysozyme C promoter drives myeloid-specific expression in transgenic fish,” BMC Dev. Biol. 7(1), 42 (2007).
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Crosier, P.

C. Hall, M. V. Flores, T. Storm, K. Crosier, and P. Crosier, “The zebrafish lysozyme C promoter drives myeloid-specific expression in transgenic fish,” BMC Dev. Biol. 7(1), 42 (2007).
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Dainty, J. C.

K. Dowling, S. C. W. Hyde, J. C. Dainty, P. W. W. French, and J. D. Hares, “2-D fluorescence lifetime imaging using a time-gated image intensifier,” Opt. Commun. 135(1-3), 27–31 (1997).
[CrossRef]

Dallman, M. J.

S. Kumar, D. Alibhai, A. Margineanu, R. Laine, G. Kennedy, J. McGinty, S. Warren, D. Kelly, Y. Alexandrov, I. Munro, C. Talbot, D. W. Stuckey, C. Kimberly, B. Viellerobe, F. Lacombe, E. W.-F. Lam, H. Taylor, M. J. Dallman, G. Stamp, E. J. Murray, F. Stuhmeier, A. Sardini, M. Katan, D. S. Elson, M. A. A. Neil, C. Dunsby, and P. M. W. French, “FLIM FRET technology for drug discovery: automated multiwell-plate high-content analysis, multiplexed readouts and application in situ,” ChemPhysChem 12(3), 609–626 (2011).
[CrossRef] [PubMed]

Darrell, A.

Davidson, D.

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,” Science 296(5567), 541–545 (2002).
[CrossRef] [PubMed]

Davis, D. M.

C. Dunsby, P. M. P. Lanigan, J. McGinty, D. S. Elson, J. Requejo-Isidro, I. Munro, N. Galletly, F. McCann, B. Treanor, B. Onfelt, D. M. Davis, M. A. A. Neil, and P. M. W. French, “An electronically tunable ultrafast laser source applied to fluorescence imaging and fluorescence lifetime imaging microscopy,” J. Phys. D Appl. Phys. 37(23), 3296–3303 (2004).
[CrossRef]

Davoust, J.

D. Stockholm, M. Bartoli, G. Sillon, N. Bourg, J. Davoust, and I. Richard, “Imaging calpain protease activity by multiphoton FRET in living mice,” J. Mol. Biol. 346(1), 215–222 (2005).
[CrossRef] [PubMed]

Dayel, M. J.

Deininger, 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. Methods 4(4), 331–336 (2007).
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Del Bene, F.

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,” Science 305(5686), 1007–1009 (2004).
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Demas, J. N.

R. M. Ballew and J. N. Demas, “An error analysis of the rapid lifetime determination method for the evaluation of single exponential decay,” Anal. Chem. 61(1), 30–33 (1989).
[CrossRef]

Deussing, J. 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. Methods 4(4), 331–336 (2007).
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Dewhirst, M.

M. Oldham, H. S. Sakhalkar, T. Oliver, G. Allan Johnson, and M. Dewhirst, “Optical clearing of unsectioned specimens for three-dimensional imaging via optical transmission and emission tomography,” J. Biomed. Opt. 13(2), 021113 (2008).
[CrossRef] [PubMed]

H. S. Sakhalkar, M. Dewhirst, T. Oliver, Y. Cao, and M. Oldham, “Functional imaging in bulk tissue specimens using optical emission tomography: fluorescence preservation during optical clearing,” Phys. Med. Biol. 52(8), 2035–2054 (2007).
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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. Methods 4(4), 331–336 (2007).
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Dowling, K.

K. Dowling, M. J. Dayel, M. J. Lever, P. M. W. French, J. D. Hares, and A. K. L. Dymoke-Bradshaw, “Fluorescence lifetime imaging with picosecond resolution for biomedical applications,” Opt. Lett. 23(10), 810–812 (1998).
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K. Dowling, S. C. W. Hyde, J. C. Dainty, P. W. W. French, and J. D. Hares, “2-D fluorescence lifetime imaging using a time-gated image intensifier,” Opt. Commun. 135(1-3), 27–31 (1997).
[CrossRef]

Draaijer, A.

E. P. Buurman, R. Sanders, A. Draaijer, H. C. Gerritsen, J. J. F. Vanveen, P. M. Houpt, and Y. K. Levine, “Fluorescence lifetime imaging using a confocal laser scanning microscope,” Scanning 14, 155–159 (1992).

Dunsby, C.

S. Kumar, D. Alibhai, A. Margineanu, R. Laine, G. Kennedy, J. McGinty, S. Warren, D. Kelly, Y. Alexandrov, I. Munro, C. Talbot, D. W. Stuckey, C. Kimberly, B. Viellerobe, F. Lacombe, E. W.-F. Lam, H. Taylor, M. J. Dallman, G. Stamp, E. J. Murray, F. Stuhmeier, A. Sardini, M. Katan, D. S. Elson, M. A. A. Neil, C. Dunsby, and P. M. W. French, “FLIM FRET technology for drug discovery: automated multiwell-plate high-content analysis, multiplexed readouts and application in situ,” ChemPhysChem 12(3), 609–626 (2011).
[CrossRef] [PubMed]

G. T. Kennedy, H. B. Manning, D. S. Elson, M. A. A. Neil, G. W. Stamp, B. Viellerobe, F. Lacombe, C. Dunsby, and P. M. W. French, “A fluorescence lifetime imaging scanning confocal endomicroscope,” J Biophotonics 3(1-2), 103–107 (2010).
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J. McGinty, J. Requejo-Isidro, I. Munro, C. B. Talbot, P. A. Kellett, J. D. Hares, C. Dunsby, M A A. Neil, and P. M. W. French, “Signal-to-noise characterization of time-gated intensifiers used for wide-field time-domain FLIM,” J. Phys. D Appl. Phys. 42(13), 135103 (2009).
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J. McGinty, K. B. Tahir, R. Laine, C. B. Talbot, C. Dunsby, M. A. A. Neil, L. Quintana, J. Swoger, J. Sharpe, and P. M. W. French, “Fluorescence lifetime optical projection tomography,” J Biophotonics 1(5), 390–394 (2008).
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C. Dunsby, “Optically sectioned imaging by oblique plane microscopy,” Opt. Express 16(25), 20306–20316 (2008).
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C. B. Talbot, J. McGinty, D. M. Grant, E. J. McGhee, D. M. Owen, W. Zhang, T. D. Bunney, I. Munro, B. Isherwood, R. Eagle, A. Hargreaves, C. Dunsby, M. A. Neil, and P. M. W. French, “High speed unsupervised fluorescence lifetime imaging confocal multiwell plate reader for high content analysis,” J Biophotonics 1(6), 514–521 (2008).
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D. M. Owen, P. M. P. Lanigan, C. Dunsby, I. Munro, D. Grant, M. A. A. Neil, P. M. W. French, and A. I. Magee, “Fluorescence lifetime imaging provides enhanced contrast when imaging the phase-sensitive dye di-4-ANEPPDHQ in model membranes and live cells,” Biophys. J. 90(11), L80–L82 (2006).
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C. Dunsby, P. M. P. Lanigan, J. McGinty, D. S. Elson, J. Requejo-Isidro, I. Munro, N. Galletly, F. McCann, B. Treanor, B. Onfelt, D. M. Davis, M. A. A. Neil, and P. M. W. French, “An electronically tunable ultrafast laser source applied to fluorescence imaging and fluorescence lifetime imaging microscopy,” J. Phys. D Appl. Phys. 37(23), 3296–3303 (2004).
[CrossRef]

Dymoke-Bradshaw, A. K. L.

Eagle, R.

C. B. Talbot, J. McGinty, D. M. Grant, E. J. McGhee, D. M. Owen, W. Zhang, T. D. Bunney, I. Munro, B. Isherwood, R. Eagle, A. Hargreaves, C. Dunsby, M. A. Neil, and P. M. W. French, “High speed unsupervised fluorescence lifetime imaging confocal multiwell plate reader for high content analysis,” J Biophotonics 1(6), 514–521 (2008).
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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. Methods 4(4), 331–336 (2007).
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Eickhoff, J.

M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
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Ekker, S. C.

A. M. Petzold, V. M. Bedell, N. J. Boczek, J. J. Essner, D. Balciunas, K. J. Clark, and S. C. Ekker, “SCORE imaging: specimen in a corrected optical rotational enclosure,” Zebrafish 7(2), 149–154 (2010).
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Eliceiri, K. W.

M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
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Elson, D. S.

S. Kumar, D. Alibhai, A. Margineanu, R. Laine, G. Kennedy, J. McGinty, S. Warren, D. Kelly, Y. Alexandrov, I. Munro, C. Talbot, D. W. Stuckey, C. Kimberly, B. Viellerobe, F. Lacombe, E. W.-F. Lam, H. Taylor, M. J. Dallman, G. Stamp, E. J. Murray, F. Stuhmeier, A. Sardini, M. Katan, D. S. Elson, M. A. A. Neil, C. Dunsby, and P. M. W. French, “FLIM FRET technology for drug discovery: automated multiwell-plate high-content analysis, multiplexed readouts and application in situ,” ChemPhysChem 12(3), 609–626 (2011).
[CrossRef] [PubMed]

G. T. Kennedy, H. B. Manning, D. S. Elson, M. A. A. Neil, G. W. Stamp, B. Viellerobe, F. Lacombe, C. Dunsby, and P. M. W. French, “A fluorescence lifetime imaging scanning confocal endomicroscope,” J Biophotonics 3(1-2), 103–107 (2010).
[CrossRef] [PubMed]

C. Dunsby, P. M. P. Lanigan, J. McGinty, D. S. Elson, J. Requejo-Isidro, I. Munro, N. Galletly, F. McCann, B. Treanor, B. Onfelt, D. M. Davis, M. A. A. Neil, and P. M. W. French, “An electronically tunable ultrafast laser source applied to fluorescence imaging and fluorescence lifetime imaging microscopy,” J. Phys. D Appl. Phys. 37(23), 3296–3303 (2004).
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Esposito, A.

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Essner, J. J.

A. M. Petzold, V. M. Bedell, N. J. Boczek, J. J. Essner, D. Balciunas, K. J. Clark, and S. C. Ekker, “SCORE imaging: specimen in a corrected optical rotational enclosure,” Zebrafish 7(2), 149–154 (2010).
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Fernandez, J. J.

J. I. Agulleiro and J. J. Fernandez, “Fast tomographic reconstruction on multicore computers,” Bioinformatics 27(4), 582–583 (2011).
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Fishman, M. C.

C. G. Burns, D. J. Milan, E. J. Grande, W. Rottbauer, C. A. MacRae, and M. C. Fishman, “High-throughput assay for small molecules that modulate zebrafish embryonic heart rate,” Nat. Chem. Biol. 1(5), 263–264 (2005).
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Supplementary Material (6)

» Media 1: AVI (852 KB)     
» Media 2: AVI (592 KB)     
» Media 3: AVI (469 KB)     
» Media 4: AVI (299 KB)     
» Media 5: AVI (329 KB)     
» Media 6: AVI (329 KB)     

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Figures (5)

Fig. 1
Fig. 1

Single frames from videos showing (a) a live zebrafish embryo (Media 1) mounted in the OPT system and (b) an intensity-based in vivo OPT acquisition (Media 2) of a lysC:GFP zebrafish embryo. Scale bar 500 μm.

Fig. 2
Fig. 2

(a) Schematic of OPT system. O – objective, AP – aperture, L1 – condenser lens, F1 – excitation filter, DM – dichroic mirror, L2 – tube lens, F2 – emission filter, M – mirror. (b) Photograph of custom built chamber.

Fig. 3
Fig. 3

(a) An OPT raw data set comprises a set of wide-field images as a function of rotation. Reconstruction is performed using the sinograms (r-θ planes) for each row of pixels. (b) Single frame showing the reconstruction of a single slice from 90 fluorescence projections (Media 3). Scale bar 500 μm.

Fig. 4
Fig. 4

(a) A 3-D fluorescence intensity reconstruction and (b) a single frame showing combined fluorescence (red) and transmitted light (grey) intensity reconstructions of a live lysC:GFP transgenic zebrafish embryo 3 days post-fertilization (Media 4). Scale bar 500 μm.

Fig. 5
Fig. 5

Single frames showing 3-D fluorescence lifetime reconstructions on a (a) continuous (Media 5) and (b) discrete color scale (Media 6) of a live lysC:GFP transgenic zebrafish embryo 3 days post-fertilization. (c) A fluorescence lifetime histogram showing two clear populations corresponding to GFP and autofluorescence. Scale bar 500 μm.

Equations (1)

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I ( x , z ) = 1 2 0 2 π [ S θ ( w ) | w | e 2 π i w r d w ] d θ

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