Abstract

Forster resonance energy transfer (FRET) is a nonradiative transfer of energy between two fluorescent molecules (a donor and an acceptor) in nanometer range proximity. FRET imaging methods have been applied to proteomic studies and drug discovery applications based on intermolecular FRET efficiency measurements and stoichiometric measurements of FRET interaction as quantitative parameters of interest. Importantly, FRET provides information about biomolecular interactions at a molecular level, well beyond the diffraction limits of standard microscopy techniques. The application of FRET to small animal imaging will allow biomedical researchers to investigate physiological processes occurring at nanometer range in vivo as well as in situ. In this work a new method for the quantitative reconstruction of FRET measurements in small animals, incorporating a full-field tomographic acquisition system with a Monte Carlo based hierarchical reconstruction scheme, is described and validated in murine models. Our main objective is to estimate the relative concentration of two forms of donor species, i.e., a donor molecule involved in FRETing to an acceptor close by and a nonFRETing donor molecule.

© 2012 OSA

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2012 (2)

J. Chen and X. Intes, “Mesh-based Monte Carlo method in time-domain widefield fluorescence molecular tomography,” J. Biomed. Opt. 17(10), 106009 (2012).
[Crossref]

N. A. Rahim, S. Pelet, R. D. Kamm, and P. T. C. So, “Methodological considerations for global analysis of cellular FLIM/FRET measurements,” J. Biomed. Opt. 17(2), 026013 (2012).
[Crossref] [PubMed]

2011 (7)

J. Chen and X. Intes, “Comparison of Monte Carlo methods for fluorescence molecular tomography-computational efficiency,” Med. Phys. 38(10), 5788–5798 (2011).
[Crossref] [PubMed]

M. Y. Berezin, K. Guo, W. Akers, R. E. Northdurft, J. P. Culver, B. Teng, O. Vasalatiy, K. Barbacow, A. Gandjbakhche, G. L. Griffiths, and S. Achilefu, “Near-infrared fluorescence lifetime pH-sensitive probes,” Biophys. J. 100(8), 2063–2072 (2011).
[Crossref] [PubMed]

N. Gaborit, C. Larbouret, J. Vallaghe, F. Peyrusson, C. Bascoul-Mollevi, E. Crapez, D. Azria, T. Chardès, M.-A. Poul, G. Mathis, H. Bazin, and A. Pèlegrin, “Time-resolved fluorescence resonance energy transfer (TR-FRET) to analyze the disruption of EGFR/HER2 dimers: a new method to evaluate the efficiency of targeted therapy using monoclonal antibodies,” J. Biol. Chem. 286(13), 11337–11345 (2011).
[Crossref] [PubMed]

J. McGinty, D. W. Stuckey, V. Y. Soloviev, R. Laine, M. Wylezinska-Arridge, D. J. Wells, S. R. Arridge, P. M. W. French, J. V. Hajnal, and A. Sardini, “In vivo fluorescence lifetime tomography of a FRET probe expressed in mouse,” Biomed. Opt. Express 2(7), 1907–1917 (2011).
[Crossref] [PubMed]

J. Chen, V. Venugopal, and X. Intes, “Monte Carlo based method for fluorescence tomographic imaging with lifetime multiplexing using time gates,” Biomed. Opt. Express 2(4), 871–886 (2011).
[Crossref] [PubMed]

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. McGinty, H. B. Taylor, L. Chen, L. Bugeon, J. R. Lamb, M. J. Dallman, and P. M. W. French, “In vivo fluorescence lifetime optical projection tomography,” Biomed. Opt. Express 2(5), 1340–1350 (2011).
[Crossref] [PubMed]

2010 (6)

V. Venugopal, J. Chen, and X. Intes, “Development of an optical imaging platform for functional imaging of small animals using wide-field excitation,” Biomed. Opt. Express 1(1), 143–156 (2010).
[Crossref] [PubMed]

S. Bélanger, M. Abran, X. Intes, C. Casanova, and F. Lesage, “Real-time diffuse optical tomography based on structured illumination,” J. Biomed. Opt. 15(1), 016006 (2010).
[Crossref] [PubMed]

J. Chen, V. Venugopal, F. Lesage, and X. Intes, “Time-resolved diffuse optical tomography with patterned-light illumination and detection,” Opt. Lett. 35(13), 2121–2123 (2010).
[Crossref] [PubMed]

V. Gaind, S. Kularatne, P. S. Low, and K. J. Webb, “Deep-tissue imaging of intramolecular fluorescence resonance energy-transfer parameters,” Opt. Lett. 35(9), 1314–1316 (2010).
[Crossref] [PubMed]

N. Valim, J. Brock, and M. Niedre, “Experimental measurement of time-dependent photon scatter for diffuse optical tomography,” J. Biomed. Opt. 15(6), 065006 (2010).
[Crossref] [PubMed]

S. B. Raymond, D. A. Boas, B. J. Bacskai, and A. T. N. Kumar, “Lifetime-based tomographic multiplexing,” J. Biomed. Opt. 15(4), 046011 (2010).
[Crossref] [PubMed]

2009 (3)

2008 (6)

B. Breart, F. Lemaître, S. Celli, and P. Bousso, “Two-photon imaging of intratumoral CD8+ T cell cytotoxic activity during adoptive T cell therapy in mice,” J. Clin. Invest. 118(4), 1390–1397 (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]

J. R. Lakowicz and B. R. Masters, “Principles of fluorescence spectroscopy, third edition,” J. Biomed. Opt. 13(2), 029901 (2008).
[Crossref]

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]

S. Padilla-Parra, N. Audugé, M. Coppey-Moisan, and M. Tramier, “Quantitative FRET analysis by fast acquisition time domain FLIM at high spatial resolution in living cells,” Biophys. J. 95(6), 2976–2988 (2008).
[Crossref] [PubMed]

M. J. Niedre, R. H. de Kleine, E. Aikawa, D. G. Kirsch, R. Weissleder, and V. Ntziachristos, “Early photon tomography allows fluorescence detection of lung carcinomas and disease progression in mice in vivo,” Proc. Natl. Acad. Sci. U.S.A. 105(49), 19126–19131 (2008).
[Crossref] [PubMed]

2006 (5)

H. Wallrabe, Y. Chen, A. Periasamy, and M. Barroso, “Issues in confocal microscopy for quantitative FRET analysis,” Microsc. Res. Tech. 69(3), 196–206 (2006).
[Crossref] [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]

E. A. Jares-Erijman and T. M. Jovin, “Imaging molecular interactions in living cells by FRET microscopy,” Curr. Opin. Chem. Biol. 10(5), 409–416 (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]

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).
[Crossref] [PubMed]

2005 (3)

H. Wallrabe and A. Periasamy, “Imaging protein molecules using FRET and FLIM microscopy,” Curr. Opin. Biotechnol. 16(1), 19–27 (2005).
[Crossref] [PubMed]

V. Ntziachristos, J. Ripoll, L. V. Wang, and R. Weissleder, “Looking and listening to light: the evolution of whole-body photonic imaging,” Nat. Biotechnol. 23(3), 313–320 (2005).
[Crossref] [PubMed]

A. Soubret, J. Ripoll, and V. Ntziachristos, “Accuracy of fluorescent tomography in the presence of heterogeneities: study of the normalized Born ratio,” IEEE Trans. Med. Imaging 24(10), 1377–1386 (2005).
[Crossref] [PubMed]

2002 (2)

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).
[Crossref] [PubMed]

H. Li and Z. M. Qian, “Transferrin/transferrin receptor-mediated drug delivery,” Med. Res. Rev. 22(3), 225–250 (2002).
[Crossref] [PubMed]

2001 (2)

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).
[Crossref] [PubMed]

V. Ntziachristos and R. Weissleder, “Experimental three-dimensional fluorescence reconstruction of diffuse media by use of a normalized Born approximation,” Opt. Lett. 26(12), 893–895 (2001).
[Crossref] [PubMed]

2000 (2)

P. J. Verveer, A. Squire, and P. I. Bastiaens, “Global analysis of fluorescence lifetime imaging microscopy data,” Biophys. J. 78(4), 2127–2137 (2000).
[Crossref] [PubMed]

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).
[Crossref] [PubMed]

1998 (3)

S. R. Arridge and W. R. B. Lionheart, “Nonuniqueness in diffusion-based optical tomography,” Opt. Lett. 23(11), 882–884 (1998).
[Crossref] [PubMed]

A. H. Hielscher, R. E. Alcouffe, and R. L. Barbour, “Comparison of finite-difference transport and diffusion calculations for photon migration in homogeneous and heterogeneous tissues,” Phys. Med. Biol. 43(5), 1285–1302 (1998).
[Crossref] [PubMed]

A. K. Kenworthy and M. Edidin, “Distribution of a glycosylphosphatidylinositol-anchored protein at the apical surface of MDCK cells examined at a resolution of <100 A using imaging fluorescence resonance energy transfer,” J. Cell Biol. 142(1), 69–84 (1998).
[Crossref] [PubMed]

1997 (1)

A. Miyawaki, J. Llopis, R. Heim, J. M. McCaffery, J. A. Adams, M. Ikura, and R. Y. Tsien, “Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin,” Nature 388(6645), 882–887 (1997).
[Crossref] [PubMed]

1996 (1)

1990 (1)

K. M. Yoo, F. Liu, and R. R. Alfano, “When does the diffusion approximation fail to describe photon transport in random media?” Phys. Rev. Lett. 64(22), 2647–2650 (1990).
[Crossref] [PubMed]

1978 (1)

L. Stryer, “Fluorescence energy transfer as a spectroscopic ruler,” Annu. Rev. Biochem. 47(1), 819–846 (1978).
[Crossref] [PubMed]

Abran, M.

S. Bélanger, M. Abran, X. Intes, C. Casanova, and F. Lesage, “Real-time diffuse optical tomography based on structured illumination,” J. Biomed. Opt. 15(1), 016006 (2010).
[Crossref] [PubMed]

Achilefu, S.

M. Y. Berezin, K. Guo, W. Akers, R. E. Northdurft, J. P. Culver, B. Teng, O. Vasalatiy, K. Barbacow, A. Gandjbakhche, G. L. Griffiths, and S. Achilefu, “Near-infrared fluorescence lifetime pH-sensitive probes,” Biophys. J. 100(8), 2063–2072 (2011).
[Crossref] [PubMed]

Adams, J. A.

A. Miyawaki, J. Llopis, R. Heim, J. M. McCaffery, J. A. Adams, M. Ikura, and R. Y. Tsien, “Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin,” Nature 388(6645), 882–887 (1997).
[Crossref] [PubMed]

Aikawa, E.

M. J. Niedre, R. H. de Kleine, E. Aikawa, D. G. Kirsch, R. Weissleder, and V. Ntziachristos, “Early photon tomography allows fluorescence detection of lung carcinomas and disease progression in mice in vivo,” Proc. Natl. Acad. Sci. U.S.A. 105(49), 19126–19131 (2008).
[Crossref] [PubMed]

Akers, W.

M. Y. Berezin, K. Guo, W. Akers, R. E. Northdurft, J. P. Culver, B. Teng, O. Vasalatiy, K. Barbacow, A. Gandjbakhche, G. L. Griffiths, and S. Achilefu, “Near-infrared fluorescence lifetime pH-sensitive probes,” Biophys. J. 100(8), 2063–2072 (2011).
[Crossref] [PubMed]

Alcouffe, R. E.

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Chen, L.

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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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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).
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S. Padilla-Parra, N. Audugé, M. Coppey-Moisan, and M. Tramier, “Quantitative FRET analysis by fast acquisition time domain FLIM at high spatial resolution in living cells,” Biophys. J. 95(6), 2976–2988 (2008).
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Curr. Opin. Biotechnol. (1)

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J. Am. Chem. Soc. (1)

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J. Biol. Chem. (1)

N. Gaborit, C. Larbouret, J. Vallaghe, F. Peyrusson, C. Bascoul-Mollevi, E. Crapez, D. Azria, T. Chardès, M.-A. Poul, G. Mathis, H. Bazin, and A. Pèlegrin, “Time-resolved fluorescence resonance energy transfer (TR-FRET) to analyze the disruption of EGFR/HER2 dimers: a new method to evaluate the efficiency of targeted therapy using monoclonal antibodies,” J. Biol. Chem. 286(13), 11337–11345 (2011).
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H. Wallrabe, Y. Chen, A. Periasamy, and M. Barroso, “Issues in confocal microscopy for quantitative FRET analysis,” Microsc. Res. Tech. 69(3), 196–206 (2006).
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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).
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V. Ntziachristos, J. Ripoll, L. V. Wang, and R. Weissleder, “Looking and listening to light: the evolution of whole-body photonic imaging,” Nat. Biotechnol. 23(3), 313–320 (2005).
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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).
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Supplementary Material (1)

» Media 1: AVI (4636 KB)     

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Figures (6)

Fig. 1
Fig. 1

a, Schematic of the tomographic imaging platform. b, Excerpt from video showing imaging protocol for wide-field time-resolved tomography (Media 1) c, Hierarchical reconstruction scheme flowchart.

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Fig. 2
Fig. 2

NIR FRET pair. a, Fluorescence spectra of the Alexa Fluor 700 (donor) and Alexa Fluor 750 (acceptor) dyes. b, Temporal measurements acquired upon direct imaging of multiple mixtures of acceptor and donor fluorophores in varying ratios. c, Fraction of FRETing donor molecules in multiple mixtures with varying Acceptor:Donor (A:D) ratios.

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Fig. 3
Fig. 3

a, Design of murine phantom with four inclusions carrying mixtures with different acceptor to donor ratios (Red- 1:4, Green-1:2, Cyan-2:1 and Blue-4:1). The orange boundary indicates the area of full-field excitation. b, An example of the normalized temporal measurements acquired at detectors directly above the four inclusions when excited by a full-field excitation pattern. c, Histogram of the value of shorter lifetime (FRETing donor) component for all detectors above signal threshold for all excitation patterns.

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Fig. 4
Fig. 4

a, 50% iso volume of total reconstructed fluorescence yield. b, Reconstructed quantum yield of the shorter component thresholded at 50% of maximum value at the slice at depth of 11 mm. c, Quantitative comparison of tomographic estimates of FRETing donor fraction from above reconstruction.

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Fig. 5
Fig. 5

a, 3D rendering of the CT images of the mouse model showing the location of two capillary tubes carrying donor acceptor mixtures with A:D ratio of 1:4 (green) and 4:1 (blue). The black border represents the registered field of view on the optical imaging platform. b, An example of the temporal measurements acquired at detectors directly above the four inclusions when excited by a full-field excitation pattern. c, Histogram of the value of shorter lifetime (FRETing donor) component for all detectors above signal threshold for all excitation patterns.

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Fig. 6
Fig. 6

a, 50% iso-volumes of total reconstructed donor quantum yield. b, The relative reconstructed quantum yield of the shorter component thresholded at 50% of maximum value overlaid on the corresponding slice from the CT volume. c, Quantitative comparison of tomographic estimates of FRETing donor fraction from above reconstruction.

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Equations (5)

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

η ( r ) = μ a f x ( r ) ϕ μ a x ( r )
W f l u o ( t ) = ∫ 0 t d t ' W a ( t ' ) e − ( t − t ' ) / τ
Φ = M i m ( t ) M i x = α U i x [ ∫ d 3 r W i F R E T ( t ) η F R E T + ∫ d 3 r W i n o n F R E T ( t ) η n o n F R E T ]
[ Φ 1 ⋮ Φ K ] = [ β 1 W 1 , 1 F R E T ⋯ β 1 W 1 , J F R E T β 1 W 1 , 1 , n o n F R E T ⋯ β 1 W 1 , J n o n F R E T ⋮ ⋱ ⋮ ⋮ ⋱ ⋮ β K W K , 1 F R E T ⋯ β K W K , J F R E T β K W K , 1 n o n F R E T ⋯ β K W K , J n o n F R E T ] [ η 1 F R E T ⋮ η J F R E T η 1 n o n F R E T ⋮ η J n o n F R E T ]
Γ e m ( t ) = I R F ( t ) ∗ ( N + A F R E T e − t / τ F R E T + A n o n F R E T e − t / τ n o n F R E T )

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