Abstract

Development of remote imaging for diagnostic purposes has progressed dramatically since endoscopy began in the 1960’s. The recent advent of a clinically licensed intensity-based fluorescence micro-endoscopic instrument has offered the prospect of real-time cellular resolution imaging. However, interrogating protein-protein interactions deep inside living tissue requires precise fluorescence lifetime measurements to derive the Förster resonance energy transfer between two tagged fluorescent markers. We developed a new instrument combining remote fiber endoscopic cellular-resolution imaging with TCSPC-FLIM technology to interrogate and discriminate mixed fluorochrome labeled beads and expressible GFP/TagRFP tags within live cells. Endoscopic-FLIM (e-FLIM) data was validated by comparison with data acquired via conventional FLIM and e-FLIM was found to be accurate for both bright bead and dim live cell samples. The fiber based micro-endoscope allowed remote imaging of 4 µm and 10 µm beads within a thick Matrigel matrix with confident fluorophore discrimination using lifetime information. More importantly, this new technique enabled us to reliably measure protein-protein interactions in live cells embedded in a 3D matrix, as demonstrated by the dimerization of the fluorescent protein-tagged membrane receptor CXCR4. This cell-based application successfully demonstrated the suitability and great potential of this new technique for in vivo pre-clinical biomedical and possibly human clinical applications.

© 2010 OSA

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2010

R. Maeda-Mamiya, E. Noiri, H. Isobe, W. Nakanishi, K. Okamoto, K. Doi, T. Sugaya, T. Izumi, T. Homma, and E. Nakamura, “In vivo gene delivery by cationic tetraamino fullerene,” Procs. Nat. Acad. Sci. 107(12), 5339–5344 (2010).
[CrossRef]

2009

C. LoPresti, H. Lomas, M. Massignani, T. Smart, and G. Battaglia, “Polymersomes: nature inspired nanometer sized compartments,” J. Mater. Chem. 19(22), 3576–3590 (2009).
[CrossRef]

K. Makrogianneli, L. M. Carlin, M. D. Keppler, D. R. Matthews, E. Ofo, A. Coolen, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, and T. Ng, “Integrating receptor signal inputs that influence small Rho GTPase activation dynamics at the immunological synapse,” Mol. Cell. Biol. 29(11), 2997–3006 (2009).
[CrossRef] [PubMed]

P. R. Barber, S. M. Ameer-Beg, J. Gilbey, L. M. Carlin, M. Keppler, T. Ng, and B. Vojnovic, “Multiphoton time-domain fluorescence lifetime imaging microscopy: practical application to protein–protein interactions using global analysis,” J. R. Soc. Interface 6(0), 93–105 (2009).
[CrossRef]

A. Cobos-Correa, J. B. Trojanek, S. Diemer, M. A. Mall, and C. Schultz, “Membrane-bound FRET probe visualizes MMP12 activity in pulmonary inflammation,” Nat. Chem. Biol. 5(9), 628–630 (2009).
[CrossRef] [PubMed]

2008

H. Lomas, M. Massignani, K. A. Abdullah, I. Canton, C. Lo Presti, S. MacNeil, J. Du, A. Blanazs, J. Madsen, S. P. Armes, A. L. Lewis, and G. Battaglia, “Non-cytotoxic polymer vesicles for rapid and efficient intracellular delivery,” Faraday Discuss. 139, 143–159, discussion 213–228, 419–420 (2008).
[CrossRef] [PubMed]

H. Bar, I. Yacoby, and I. Benhar, “Killing cancer cells by targeted drug-carrying phage nanomedicines,” BMC Biotechnol. 8(1), 37 (2008).
[CrossRef] [PubMed]

Z. Papagatsia, A. Tappuni, T. F. Watson, and R. J. Cook, “Single wavelength micro-endoscopy in non-surgical vascular lesion diagnosis & characterization,” J. Microsc. 230(2), 203–211 (2008).
[CrossRef] [PubMed]

C. Buranachai, D. Kamiyama, A. Chiba, B. D. Williams, and R. M. Clegg, “Rapid frequency-domain FLIM spinning disk confocal microscope: lifetime resolution, image improvement and wavelet analysis,” J. Fluoresc. 18(5), 929–942 (2008).
[CrossRef] [PubMed]

2007

F. Festy, S. M. Ameer-Beg, T. Ng, and K. Suhling, “Imaging proteins in vivo using fluorescence lifetime microscopy,” Mol. Biosyst. 3(6), 381–391 (2007).
[CrossRef] [PubMed]

G. McConnell, J. M. Girkin, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, T. Ng, A. Banerjee, T. F. Watson, and R. J. Cook, “Time-correlated single-photon counting fluorescence lifetime confocal imaging of decayed and sound dental structures with a white-light supercontinuum source,” J. Microsc. 225(2), 126–136 (2007).
[CrossRef] [PubMed]

T. Y. Lee, C. T. Lin, S. Y. Kuo, D. K. Chang, and H. C. Wu, “Peptide-mediated targeting to tumor blood vessels of lung cancer for drug delivery,” Cancer Res. 67(22), 10958–10965 (2007).
[CrossRef] [PubMed]

S. Prag, M. Parsons, M. D. Keppler, S. M. Ameer-Beg, P. Barber, J. Hunt, A. J. Beavil, R. Calvert, M. Arpin, B. Vojnovic, and T. Ng, “Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42,” Mol. Biol. Cell 18(8), 2935–2948 (2007).
[CrossRef] [PubMed]

E. M. Merzlyak, J. Goedhart, D. Shcherbo, M. E. Bulina, A. S. Shcheglov, A. F. Fradkov, A. Gaintzeva, K. A. Lukyanov, S. Lukyanov, T. W. Gadella, and D. M. Chudakov, “Bright monomeric red fluorescent protein with an extended fluorescence lifetime,” Nat. Methods 4(7), 555–557 (2007).
[CrossRef] [PubMed]

S. Kumar, C. Dunsby, P. A. A. De Beule, D. M. Owen, U. Anand, P. M. P. Lanigan, R. K. P. Benninger, D. M. Davis, M. A. Neil, P. Anand, C. Benham, A. Naylor, and P. M. French, “Multifocal multiphoton excitation and time correlated single photon counting detection for 3-D fluorescence lifetime imaging,” Opt. Express 15(20), 12548–12561 (2007).
[CrossRef] [PubMed]

2006

S. Pelet, M. J. R. Previte, and P. T. So, “Comparing the quantification of Forster resonance energy transfer measurement accuracies based on intensity, spectral, and lifetime imaging,” J. Biomed. Opt. 11(3), 034017 (2006).
[CrossRef]

2005

M. Parsons, J. Monypenny, S. M. Ameer-Beg, T. H. Millard, L. M. Machesky, M. Peter, M. D. Keppler, G. Schiavo, R. Watson, J. Chernoff, D. Zicha, B. Vojnovic, and T. Ng, “Spatially distinct binding of Cdc42 to PAK1 and N-WASP in breast carcinoma cells,” Mol. Cell. Biol. 25(5), 1680–1695 (2005).
[CrossRef] [PubMed]

M. Peter, S. M. Ameer-Beg, M. K. Y. Hughes, M. D. Keppler, S. Prag, M. Marsh, B. Vojnovic, and T. Ng, “Multiphoton-FLIM quantification of the EGFP-mRFP1 FRET pair for localization of membrane receptor-kinase interactions,” Biophys. J. 88(2), 1224–1237 (2005).
[CrossRef]

K. Suhling, P. M. French, and D. Phillips, “Time-resolved fluorescence microscopy,” Photochem. Photobiol. Sci. 4(1), 13–22 (2005).
[CrossRef]

R. El-Gazzar, M. Macluskey, and G. R. Ogden, “Evidence for a field change effect based on angiogenesis in the oral mucosa? A brief report,” Oral Oncol. 41(1), 25–30 (2005).
[CrossRef]

I. Munro, J. McGinty, N. Galletly, J. Requejo-Isidro, P. M. P. Lanigan, D. S. Elson, C. Dunsby, M. A. Neil, M. J. Lever, G. W. Stamp, and P. M. French, “Toward the clinical application of time-domain fluorescence lifetime imaging,” J. Biomed. Opt. 10(5), 051403 (2005).
[CrossRef] [PubMed]

2004

D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004).
[CrossRef] [PubMed]

R. R. Duncan, A. Bergmann, M. A. Cousin, D. K. Apps, and M. J. Shipston, “Multi-dimensional time-correlated single photon counting (TCSPC) fluorescence lifetime imaging microscopy (FLIM) to detect FRET in cells,” J. Microsc. 215(1), 1–12 (2004).
[CrossRef] [PubMed]

M. Peter and S. M. Ameer-Beg, “Imaging molecular interactions by multiphoton FLIM,” Biol. Cell 96(3), 231–236 (2004).
[CrossRef] [PubMed]

J. Requejo-Isidro, J. McGinty, I. Munro, D. S. Elson, N. P. Galletly, M. J. Lever, M. A. A. Neil, G. W. Stamp, P. M. French, P. A. Kellett, J. D. Hares, and A. K. Dymoke-Bradshaw, “High-speed wide-field time-gated endoscopic fluorescence-lifetime imaging,” Opt. Lett. 29(19), 2249–2251 (2004).
[CrossRef] [PubMed]

2003

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

V. Calleja, S. M. Ameer-Beg, B. Vojnovic, R. Woscholski, J. Downward, and B. Larijani, “Monitoring conformational changes of proteins in cells by fluorescence lifetime imaging microscopy,” Biochem. J. 372(1), 33–40 (2003).
[CrossRef] [PubMed]

G. J. Babcock, M. Farzan, and J. Sodroski, “Ligand-independent dimerization of CXCR4, a principal HIV-1 coreceptor,” J. Biol. Chem. 278(5), 3378–3385 (2003).
[CrossRef]

C. C. Fjeld, W. T. Birdsong, and R. H. Goodman, “Differential binding of NAD+ and NADH allows the transcriptional corepressor carboxyl-terminal binding protein to serve as a metabolic sensor,” Proc. Natl. Acad. Sci. U.S.A. 100(16), 9202–9207 (2003).
[CrossRef] [PubMed]

2001

F. S. Wouters, P. J. Verveer, and P. I. Bastiaens, “Imaging biochemistry inside cells,” Trends Cell Biol. 11(5), 203–211 (2001).
[CrossRef] [PubMed]

2000

1999

A. J. Vila-Coro, J. M. Rodríguez-Frade, A. Martín De Ana, M. C. Moreno-Ortíz, C. Martínez-A, and M. Mellado, “The chemokine SDF-1alpha triggers CXCR4 receptor dimerization and activates the JAK/STAT pathway,” FASEB J. 13(13), 1699–1710 (1999).
[PubMed]

T. Ng, A. Squire, G. Hansra, F. Bornancin, C. Prevostel, A. Hanby, W. Harris, D. Barnes, S. Schmidt, H. Mellor, P. I. Bastiaens, and P. J. Parker, “Imaging protein kinase Calpha activation in cells,” Science 283(5410), 2085–2089 (1999).
[CrossRef] [PubMed]

T. Ng, D. Shima, A. Squire, P. I. H. Bastiaens, S. Gschmeissner, M. J. Humphries, and P. J. Parker, “PKCalpha regulates beta1 integrin-dependent cell motility through association and control of integrin traffic,” EMBO J. 18, 3909–3923 (1999).
[CrossRef] [PubMed]

F. S. Wouters and P. I. Bastiaens, “Fluorescence lifetime imaging of receptor tyrosine kinase activity in cells,” Curr. Biol. 9(19), 1127–1130 (1999).
[CrossRef] [PubMed]

W. Becker, H. Hickl, C. Zander, K. H. Drexhage, M. Sauer, S. Siebert, and J. Wolfrum, “Time-resolved detection and identification of single analyte molecules in microcapillaries by time-correlated single photon counting,” Rev. Sci. Instrum. 70(3), 1835–1841 (1999).
[CrossRef]

1993

T. W. J. Gadella, T. M. Jovin, and R. M. Clegg, “Fluorescence lifetime imaging microscopy (FLIM): Spatial resolution of microstructures on the nanosecond time scale,” Biophys. Chem. 48(2), 221–239 (1993).
[CrossRef]

1978

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

1974

H. Morise, O. Shimomura, F. H. Johnson, and J. Winant, “Intermolecular energy transfer in the bioluminescent system of Aequorea,” Biochemistry 13(12), 2656–2662 (1974).
[CrossRef] [PubMed]

1948

T. Förster, “Intermolecular energy migration and fluorescence,” Ann. Phys. 2, 55 (1948).
[CrossRef]

Abdullah, K. A.

H. Lomas, M. Massignani, K. A. Abdullah, I. Canton, C. Lo Presti, S. MacNeil, J. Du, A. Blanazs, J. Madsen, S. P. Armes, A. L. Lewis, and G. Battaglia, “Non-cytotoxic polymer vesicles for rapid and efficient intracellular delivery,” Faraday Discuss. 139, 143–159, discussion 213–228, 419–420 (2008).
[CrossRef] [PubMed]

Ameer-Beg, S. M.

P. R. Barber, S. M. Ameer-Beg, J. Gilbey, L. M. Carlin, M. Keppler, T. Ng, and B. Vojnovic, “Multiphoton time-domain fluorescence lifetime imaging microscopy: practical application to protein–protein interactions using global analysis,” J. R. Soc. Interface 6(0), 93–105 (2009).
[CrossRef]

K. Makrogianneli, L. M. Carlin, M. D. Keppler, D. R. Matthews, E. Ofo, A. Coolen, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, and T. Ng, “Integrating receptor signal inputs that influence small Rho GTPase activation dynamics at the immunological synapse,” Mol. Cell. Biol. 29(11), 2997–3006 (2009).
[CrossRef] [PubMed]

S. Prag, M. Parsons, M. D. Keppler, S. M. Ameer-Beg, P. Barber, J. Hunt, A. J. Beavil, R. Calvert, M. Arpin, B. Vojnovic, and T. Ng, “Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42,” Mol. Biol. Cell 18(8), 2935–2948 (2007).
[CrossRef] [PubMed]

F. Festy, S. M. Ameer-Beg, T. Ng, and K. Suhling, “Imaging proteins in vivo using fluorescence lifetime microscopy,” Mol. Biosyst. 3(6), 381–391 (2007).
[CrossRef] [PubMed]

G. McConnell, J. M. Girkin, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, T. Ng, A. Banerjee, T. F. Watson, and R. J. Cook, “Time-correlated single-photon counting fluorescence lifetime confocal imaging of decayed and sound dental structures with a white-light supercontinuum source,” J. Microsc. 225(2), 126–136 (2007).
[CrossRef] [PubMed]

M. Peter, S. M. Ameer-Beg, M. K. Y. Hughes, M. D. Keppler, S. Prag, M. Marsh, B. Vojnovic, and T. Ng, “Multiphoton-FLIM quantification of the EGFP-mRFP1 FRET pair for localization of membrane receptor-kinase interactions,” Biophys. J. 88(2), 1224–1237 (2005).
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M. Parsons, J. Monypenny, S. M. Ameer-Beg, T. H. Millard, L. M. Machesky, M. Peter, M. D. Keppler, G. Schiavo, R. Watson, J. Chernoff, D. Zicha, B. Vojnovic, and T. Ng, “Spatially distinct binding of Cdc42 to PAK1 and N-WASP in breast carcinoma cells,” Mol. Cell. Biol. 25(5), 1680–1695 (2005).
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M. Peter and S. M. Ameer-Beg, “Imaging molecular interactions by multiphoton FLIM,” Biol. Cell 96(3), 231–236 (2004).
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V. Calleja, S. M. Ameer-Beg, B. Vojnovic, R. Woscholski, J. Downward, and B. Larijani, “Monitoring conformational changes of proteins in cells by fluorescence lifetime imaging microscopy,” Biochem. J. 372(1), 33–40 (2003).
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Anand, U.

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R. R. Duncan, A. Bergmann, M. A. Cousin, D. K. Apps, and M. J. Shipston, “Multi-dimensional time-correlated single photon counting (TCSPC) fluorescence lifetime imaging microscopy (FLIM) to detect FRET in cells,” J. Microsc. 215(1), 1–12 (2004).
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S. Prag, M. Parsons, M. D. Keppler, S. M. Ameer-Beg, P. Barber, J. Hunt, A. J. Beavil, R. Calvert, M. Arpin, B. Vojnovic, and T. Ng, “Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42,” Mol. Biol. Cell 18(8), 2935–2948 (2007).
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G. J. Babcock, M. Farzan, and J. Sodroski, “Ligand-independent dimerization of CXCR4, a principal HIV-1 coreceptor,” J. Biol. Chem. 278(5), 3378–3385 (2003).
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S. Prag, M. Parsons, M. D. Keppler, S. M. Ameer-Beg, P. Barber, J. Hunt, A. J. Beavil, R. Calvert, M. Arpin, B. Vojnovic, and T. Ng, “Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42,” Mol. Biol. Cell 18(8), 2935–2948 (2007).
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K. Makrogianneli, L. M. Carlin, M. D. Keppler, D. R. Matthews, E. Ofo, A. Coolen, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, and T. Ng, “Integrating receptor signal inputs that influence small Rho GTPase activation dynamics at the immunological synapse,” Mol. Cell. Biol. 29(11), 2997–3006 (2009).
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P. R. Barber, S. M. Ameer-Beg, J. Gilbey, L. M. Carlin, M. Keppler, T. Ng, and B. Vojnovic, “Multiphoton time-domain fluorescence lifetime imaging microscopy: practical application to protein–protein interactions using global analysis,” J. R. Soc. Interface 6(0), 93–105 (2009).
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G. McConnell, J. M. Girkin, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, T. Ng, A. Banerjee, T. F. Watson, and R. J. Cook, “Time-correlated single-photon counting fluorescence lifetime confocal imaging of decayed and sound dental structures with a white-light supercontinuum source,” J. Microsc. 225(2), 126–136 (2007).
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F. S. Wouters and P. I. Bastiaens, “Fluorescence lifetime imaging of receptor tyrosine kinase activity in cells,” Curr. Biol. 9(19), 1127–1130 (1999).
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T. Ng, D. Shima, A. Squire, P. I. H. Bastiaens, S. Gschmeissner, M. J. Humphries, and P. J. Parker, “PKCalpha regulates beta1 integrin-dependent cell motility through association and control of integrin traffic,” EMBO J. 18, 3909–3923 (1999).
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H. Lomas, M. Massignani, K. A. Abdullah, I. Canton, C. Lo Presti, S. MacNeil, J. Du, A. Blanazs, J. Madsen, S. P. Armes, A. L. Lewis, and G. Battaglia, “Non-cytotoxic polymer vesicles for rapid and efficient intracellular delivery,” Faraday Discuss. 139, 143–159, discussion 213–228, 419–420 (2008).
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S. Prag, M. Parsons, M. D. Keppler, S. M. Ameer-Beg, P. Barber, J. Hunt, A. J. Beavil, R. Calvert, M. Arpin, B. Vojnovic, and T. Ng, “Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42,” Mol. Biol. Cell 18(8), 2935–2948 (2007).
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H. Bar, I. Yacoby, and I. Benhar, “Killing cancer cells by targeted drug-carrying phage nanomedicines,” BMC Biotechnol. 8(1), 37 (2008).
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Bergmann, A.

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C. C. Fjeld, W. T. Birdsong, and R. H. Goodman, “Differential binding of NAD+ and NADH allows the transcriptional corepressor carboxyl-terminal binding protein to serve as a metabolic sensor,” Proc. Natl. Acad. Sci. U.S.A. 100(16), 9202–9207 (2003).
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H. Lomas, M. Massignani, K. A. Abdullah, I. Canton, C. Lo Presti, S. MacNeil, J. Du, A. Blanazs, J. Madsen, S. P. Armes, A. L. Lewis, and G. Battaglia, “Non-cytotoxic polymer vesicles for rapid and efficient intracellular delivery,” Faraday Discuss. 139, 143–159, discussion 213–228, 419–420 (2008).
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T. Ng, A. Squire, G. Hansra, F. Bornancin, C. Prevostel, A. Hanby, W. Harris, D. Barnes, S. Schmidt, H. Mellor, P. I. Bastiaens, and P. J. Parker, “Imaging protein kinase Calpha activation in cells,” Science 283(5410), 2085–2089 (1999).
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E. M. Merzlyak, J. Goedhart, D. Shcherbo, M. E. Bulina, A. S. Shcheglov, A. F. Fradkov, A. Gaintzeva, K. A. Lukyanov, S. Lukyanov, T. W. Gadella, and D. M. Chudakov, “Bright monomeric red fluorescent protein with an extended fluorescence lifetime,” Nat. Methods 4(7), 555–557 (2007).
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C. Buranachai, D. Kamiyama, A. Chiba, B. D. Williams, and R. M. Clegg, “Rapid frequency-domain FLIM spinning disk confocal microscope: lifetime resolution, image improvement and wavelet analysis,” J. Fluoresc. 18(5), 929–942 (2008).
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V. Calleja, S. M. Ameer-Beg, B. Vojnovic, R. Woscholski, J. Downward, and B. Larijani, “Monitoring conformational changes of proteins in cells by fluorescence lifetime imaging microscopy,” Biochem. J. 372(1), 33–40 (2003).
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S. Prag, M. Parsons, M. D. Keppler, S. M. Ameer-Beg, P. Barber, J. Hunt, A. J. Beavil, R. Calvert, M. Arpin, B. Vojnovic, and T. Ng, “Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42,” Mol. Biol. Cell 18(8), 2935–2948 (2007).
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H. Lomas, M. Massignani, K. A. Abdullah, I. Canton, C. Lo Presti, S. MacNeil, J. Du, A. Blanazs, J. Madsen, S. P. Armes, A. L. Lewis, and G. Battaglia, “Non-cytotoxic polymer vesicles for rapid and efficient intracellular delivery,” Faraday Discuss. 139, 143–159, discussion 213–228, 419–420 (2008).
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P. R. Barber, S. M. Ameer-Beg, J. Gilbey, L. M. Carlin, M. Keppler, T. Ng, and B. Vojnovic, “Multiphoton time-domain fluorescence lifetime imaging microscopy: practical application to protein–protein interactions using global analysis,” J. R. Soc. Interface 6(0), 93–105 (2009).
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K. Makrogianneli, L. M. Carlin, M. D. Keppler, D. R. Matthews, E. Ofo, A. Coolen, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, and T. Ng, “Integrating receptor signal inputs that influence small Rho GTPase activation dynamics at the immunological synapse,” Mol. Cell. Biol. 29(11), 2997–3006 (2009).
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T. Y. Lee, C. T. Lin, S. Y. Kuo, D. K. Chang, and H. C. Wu, “Peptide-mediated targeting to tumor blood vessels of lung cancer for drug delivery,” Cancer Res. 67(22), 10958–10965 (2007).
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C. Buranachai, D. Kamiyama, A. Chiba, B. D. Williams, and R. M. Clegg, “Rapid frequency-domain FLIM spinning disk confocal microscope: lifetime resolution, image improvement and wavelet analysis,” J. Fluoresc. 18(5), 929–942 (2008).
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E. M. Merzlyak, J. Goedhart, D. Shcherbo, M. E. Bulina, A. S. Shcheglov, A. F. Fradkov, A. Gaintzeva, K. A. Lukyanov, S. Lukyanov, T. W. Gadella, and D. M. Chudakov, “Bright monomeric red fluorescent protein with an extended fluorescence lifetime,” Nat. Methods 4(7), 555–557 (2007).
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C. Buranachai, D. Kamiyama, A. Chiba, B. D. Williams, and R. M. Clegg, “Rapid frequency-domain FLIM spinning disk confocal microscope: lifetime resolution, image improvement and wavelet analysis,” J. Fluoresc. 18(5), 929–942 (2008).
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T. W. J. Gadella, T. M. Jovin, and R. M. Clegg, “Fluorescence lifetime imaging microscopy (FLIM): Spatial resolution of microstructures on the nanosecond time scale,” Biophys. Chem. 48(2), 221–239 (1993).
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A. Cobos-Correa, J. B. Trojanek, S. Diemer, M. A. Mall, and C. Schultz, “Membrane-bound FRET probe visualizes MMP12 activity in pulmonary inflammation,” Nat. Chem. Biol. 5(9), 628–630 (2009).
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Z. Papagatsia, A. Tappuni, T. F. Watson, and R. J. Cook, “Single wavelength micro-endoscopy in non-surgical vascular lesion diagnosis & characterization,” J. Microsc. 230(2), 203–211 (2008).
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K. Makrogianneli, L. M. Carlin, M. D. Keppler, D. R. Matthews, E. Ofo, A. Coolen, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, and T. Ng, “Integrating receptor signal inputs that influence small Rho GTPase activation dynamics at the immunological synapse,” Mol. Cell. Biol. 29(11), 2997–3006 (2009).
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R. R. Duncan, A. Bergmann, M. A. Cousin, D. K. Apps, and M. J. Shipston, “Multi-dimensional time-correlated single photon counting (TCSPC) fluorescence lifetime imaging microscopy (FLIM) to detect FRET in cells,” J. Microsc. 215(1), 1–12 (2004).
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D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004).
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De Beule, P. A. A.

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A. Cobos-Correa, J. B. Trojanek, S. Diemer, M. A. Mall, and C. Schultz, “Membrane-bound FRET probe visualizes MMP12 activity in pulmonary inflammation,” Nat. Chem. Biol. 5(9), 628–630 (2009).
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R. Maeda-Mamiya, E. Noiri, H. Isobe, W. Nakanishi, K. Okamoto, K. Doi, T. Sugaya, T. Izumi, T. Homma, and E. Nakamura, “In vivo gene delivery by cationic tetraamino fullerene,” Procs. Nat. Acad. Sci. 107(12), 5339–5344 (2010).
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V. Calleja, S. M. Ameer-Beg, B. Vojnovic, R. Woscholski, J. Downward, and B. Larijani, “Monitoring conformational changes of proteins in cells by fluorescence lifetime imaging microscopy,” Biochem. J. 372(1), 33–40 (2003).
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W. Becker, H. Hickl, C. Zander, K. H. Drexhage, M. Sauer, S. Siebert, and J. Wolfrum, “Time-resolved detection and identification of single analyte molecules in microcapillaries by time-correlated single photon counting,” Rev. Sci. Instrum. 70(3), 1835–1841 (1999).
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H. Lomas, M. Massignani, K. A. Abdullah, I. Canton, C. Lo Presti, S. MacNeil, J. Du, A. Blanazs, J. Madsen, S. P. Armes, A. L. Lewis, and G. Battaglia, “Non-cytotoxic polymer vesicles for rapid and efficient intracellular delivery,” Faraday Discuss. 139, 143–159, discussion 213–228, 419–420 (2008).
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R. R. Duncan, A. Bergmann, M. A. Cousin, D. K. Apps, and M. J. Shipston, “Multi-dimensional time-correlated single photon counting (TCSPC) fluorescence lifetime imaging microscopy (FLIM) to detect FRET in cells,” J. Microsc. 215(1), 1–12 (2004).
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El-Gazzar, R.

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I. Munro, J. McGinty, N. Galletly, J. Requejo-Isidro, P. M. P. Lanigan, D. S. Elson, C. Dunsby, M. A. Neil, M. J. Lever, G. W. Stamp, and P. M. French, “Toward the clinical application of time-domain fluorescence lifetime imaging,” J. Biomed. Opt. 10(5), 051403 (2005).
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J. Requejo-Isidro, J. McGinty, I. Munro, D. S. Elson, N. P. Galletly, M. J. Lever, M. A. A. Neil, G. W. Stamp, P. M. French, P. A. Kellett, J. D. Hares, and A. K. Dymoke-Bradshaw, “High-speed wide-field time-gated endoscopic fluorescence-lifetime imaging,” Opt. Lett. 29(19), 2249–2251 (2004).
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G. J. Babcock, M. Farzan, and J. Sodroski, “Ligand-independent dimerization of CXCR4, a principal HIV-1 coreceptor,” J. Biol. Chem. 278(5), 3378–3385 (2003).
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F. Festy, S. M. Ameer-Beg, T. Ng, and K. Suhling, “Imaging proteins in vivo using fluorescence lifetime microscopy,” Mol. Biosyst. 3(6), 381–391 (2007).
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C. C. Fjeld, W. T. Birdsong, and R. H. Goodman, “Differential binding of NAD+ and NADH allows the transcriptional corepressor carboxyl-terminal binding protein to serve as a metabolic sensor,” Proc. Natl. Acad. Sci. U.S.A. 100(16), 9202–9207 (2003).
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E. M. Merzlyak, J. Goedhart, D. Shcherbo, M. E. Bulina, A. S. Shcheglov, A. F. Fradkov, A. Gaintzeva, K. A. Lukyanov, S. Lukyanov, T. W. Gadella, and D. M. Chudakov, “Bright monomeric red fluorescent protein with an extended fluorescence lifetime,” Nat. Methods 4(7), 555–557 (2007).
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French, P.

D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004).
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French, P. M.

Gadella, T. W.

E. M. Merzlyak, J. Goedhart, D. Shcherbo, M. E. Bulina, A. S. Shcheglov, A. F. Fradkov, A. Gaintzeva, K. A. Lukyanov, S. Lukyanov, T. W. Gadella, and D. M. Chudakov, “Bright monomeric red fluorescent protein with an extended fluorescence lifetime,” Nat. Methods 4(7), 555–557 (2007).
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Gadella, T. W. J.

T. W. J. Gadella, T. M. Jovin, and R. M. Clegg, “Fluorescence lifetime imaging microscopy (FLIM): Spatial resolution of microstructures on the nanosecond time scale,” Biophys. Chem. 48(2), 221–239 (1993).
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E. M. Merzlyak, J. Goedhart, D. Shcherbo, M. E. Bulina, A. S. Shcheglov, A. F. Fradkov, A. Gaintzeva, K. A. Lukyanov, S. Lukyanov, T. W. Gadella, and D. M. Chudakov, “Bright monomeric red fluorescent protein with an extended fluorescence lifetime,” Nat. Methods 4(7), 555–557 (2007).
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I. Munro, J. McGinty, N. Galletly, J. Requejo-Isidro, P. M. P. Lanigan, D. S. Elson, C. Dunsby, M. A. Neil, M. J. Lever, G. W. Stamp, and P. M. French, “Toward the clinical application of time-domain fluorescence lifetime imaging,” J. Biomed. Opt. 10(5), 051403 (2005).
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Galletly, N. P.

Gilbey, J.

P. R. Barber, S. M. Ameer-Beg, J. Gilbey, L. M. Carlin, M. Keppler, T. Ng, and B. Vojnovic, “Multiphoton time-domain fluorescence lifetime imaging microscopy: practical application to protein–protein interactions using global analysis,” J. R. Soc. Interface 6(0), 93–105 (2009).
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G. McConnell, J. M. Girkin, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, T. Ng, A. Banerjee, T. F. Watson, and R. J. Cook, “Time-correlated single-photon counting fluorescence lifetime confocal imaging of decayed and sound dental structures with a white-light supercontinuum source,” J. Microsc. 225(2), 126–136 (2007).
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Goedhart, J.

E. M. Merzlyak, J. Goedhart, D. Shcherbo, M. E. Bulina, A. S. Shcheglov, A. F. Fradkov, A. Gaintzeva, K. A. Lukyanov, S. Lukyanov, T. W. Gadella, and D. M. Chudakov, “Bright monomeric red fluorescent protein with an extended fluorescence lifetime,” Nat. Methods 4(7), 555–557 (2007).
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C. C. Fjeld, W. T. Birdsong, and R. H. Goodman, “Differential binding of NAD+ and NADH allows the transcriptional corepressor carboxyl-terminal binding protein to serve as a metabolic sensor,” Proc. Natl. Acad. Sci. U.S.A. 100(16), 9202–9207 (2003).
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[CrossRef] [PubMed]

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[CrossRef] [PubMed]

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R. Maeda-Mamiya, E. Noiri, H. Isobe, W. Nakanishi, K. Okamoto, K. Doi, T. Sugaya, T. Izumi, T. Homma, and E. Nakamura, “In vivo gene delivery by cationic tetraamino fullerene,” Procs. Nat. Acad. Sci. 107(12), 5339–5344 (2010).
[CrossRef]

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R. Maeda-Mamiya, E. Noiri, H. Isobe, W. Nakanishi, K. Okamoto, K. Doi, T. Sugaya, T. Izumi, T. Homma, and E. Nakamura, “In vivo gene delivery by cationic tetraamino fullerene,” Procs. Nat. Acad. Sci. 107(12), 5339–5344 (2010).
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Neil, M.

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[CrossRef] [PubMed]

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S. Kumar, C. Dunsby, P. A. A. De Beule, D. M. Owen, U. Anand, P. M. P. Lanigan, R. K. P. Benninger, D. M. Davis, M. A. Neil, P. Anand, C. Benham, A. Naylor, and P. M. French, “Multifocal multiphoton excitation and time correlated single photon counting detection for 3-D fluorescence lifetime imaging,” Opt. Express 15(20), 12548–12561 (2007).
[CrossRef] [PubMed]

I. Munro, J. McGinty, N. Galletly, J. Requejo-Isidro, P. M. P. Lanigan, D. S. Elson, C. Dunsby, M. A. Neil, M. J. Lever, G. W. Stamp, and P. M. French, “Toward the clinical application of time-domain fluorescence lifetime imaging,” J. Biomed. Opt. 10(5), 051403 (2005).
[CrossRef] [PubMed]

Neil, M. A. A.

Ng, T.

K. Makrogianneli, L. M. Carlin, M. D. Keppler, D. R. Matthews, E. Ofo, A. Coolen, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, and T. Ng, “Integrating receptor signal inputs that influence small Rho GTPase activation dynamics at the immunological synapse,” Mol. Cell. Biol. 29(11), 2997–3006 (2009).
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P. R. Barber, S. M. Ameer-Beg, J. Gilbey, L. M. Carlin, M. Keppler, T. Ng, and B. Vojnovic, “Multiphoton time-domain fluorescence lifetime imaging microscopy: practical application to protein–protein interactions using global analysis,” J. R. Soc. Interface 6(0), 93–105 (2009).
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F. Festy, S. M. Ameer-Beg, T. Ng, and K. Suhling, “Imaging proteins in vivo using fluorescence lifetime microscopy,” Mol. Biosyst. 3(6), 381–391 (2007).
[CrossRef] [PubMed]

G. McConnell, J. M. Girkin, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, T. Ng, A. Banerjee, T. F. Watson, and R. J. Cook, “Time-correlated single-photon counting fluorescence lifetime confocal imaging of decayed and sound dental structures with a white-light supercontinuum source,” J. Microsc. 225(2), 126–136 (2007).
[CrossRef] [PubMed]

S. Prag, M. Parsons, M. D. Keppler, S. M. Ameer-Beg, P. Barber, J. Hunt, A. J. Beavil, R. Calvert, M. Arpin, B. Vojnovic, and T. Ng, “Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42,” Mol. Biol. Cell 18(8), 2935–2948 (2007).
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M. Peter, S. M. Ameer-Beg, M. K. Y. Hughes, M. D. Keppler, S. Prag, M. Marsh, B. Vojnovic, and T. Ng, “Multiphoton-FLIM quantification of the EGFP-mRFP1 FRET pair for localization of membrane receptor-kinase interactions,” Biophys. J. 88(2), 1224–1237 (2005).
[CrossRef]

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[CrossRef] [PubMed]

T. Ng, D. Shima, A. Squire, P. I. H. Bastiaens, S. Gschmeissner, M. J. Humphries, and P. J. Parker, “PKCalpha regulates beta1 integrin-dependent cell motility through association and control of integrin traffic,” EMBO J. 18, 3909–3923 (1999).
[CrossRef] [PubMed]

T. Ng, A. Squire, G. Hansra, F. Bornancin, C. Prevostel, A. Hanby, W. Harris, D. Barnes, S. Schmidt, H. Mellor, P. I. Bastiaens, and P. J. Parker, “Imaging protein kinase Calpha activation in cells,” Science 283(5410), 2085–2089 (1999).
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R. El-Gazzar, M. Macluskey, and G. R. Ogden, “Evidence for a field change effect based on angiogenesis in the oral mucosa? A brief report,” Oral Oncol. 41(1), 25–30 (2005).
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Papagatsia, Z.

Z. Papagatsia, A. Tappuni, T. F. Watson, and R. J. Cook, “Single wavelength micro-endoscopy in non-surgical vascular lesion diagnosis & characterization,” J. Microsc. 230(2), 203–211 (2008).
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T. Ng, D. Shima, A. Squire, P. I. H. Bastiaens, S. Gschmeissner, M. J. Humphries, and P. J. Parker, “PKCalpha regulates beta1 integrin-dependent cell motility through association and control of integrin traffic,” EMBO J. 18, 3909–3923 (1999).
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S. Prag, M. Parsons, M. D. Keppler, S. M. Ameer-Beg, P. Barber, J. Hunt, A. J. Beavil, R. Calvert, M. Arpin, B. Vojnovic, and T. Ng, “Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42,” Mol. Biol. Cell 18(8), 2935–2948 (2007).
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M. Peter, S. M. Ameer-Beg, M. K. Y. Hughes, M. D. Keppler, S. Prag, M. Marsh, B. Vojnovic, and T. Ng, “Multiphoton-FLIM quantification of the EGFP-mRFP1 FRET pair for localization of membrane receptor-kinase interactions,” Biophys. J. 88(2), 1224–1237 (2005).
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S. Pelet, M. J. R. Previte, and P. T. So, “Comparing the quantification of Forster resonance energy transfer measurement accuracies based on intensity, spectral, and lifetime imaging,” J. Biomed. Opt. 11(3), 034017 (2006).
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T. Ng, A. Squire, G. Hansra, F. Bornancin, C. Prevostel, A. Hanby, W. Harris, D. Barnes, S. Schmidt, H. Mellor, P. I. Bastiaens, and P. J. Parker, “Imaging protein kinase Calpha activation in cells,” Science 283(5410), 2085–2089 (1999).
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D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004).
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Schultz, C.

A. Cobos-Correa, J. B. Trojanek, S. Diemer, M. A. Mall, and C. Schultz, “Membrane-bound FRET probe visualizes MMP12 activity in pulmonary inflammation,” Nat. Chem. Biol. 5(9), 628–630 (2009).
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T. Ng, D. Shima, A. Squire, P. I. H. Bastiaens, S. Gschmeissner, M. J. Humphries, and P. J. Parker, “PKCalpha regulates beta1 integrin-dependent cell motility through association and control of integrin traffic,” EMBO J. 18, 3909–3923 (1999).
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W. Becker, H. Hickl, C. Zander, K. H. Drexhage, M. Sauer, S. Siebert, and J. Wolfrum, “Time-resolved detection and identification of single analyte molecules in microcapillaries by time-correlated single photon counting,” Rev. Sci. Instrum. 70(3), 1835–1841 (1999).
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T. Ng, D. Shima, A. Squire, P. I. H. Bastiaens, S. Gschmeissner, M. J. Humphries, and P. J. Parker, “PKCalpha regulates beta1 integrin-dependent cell motility through association and control of integrin traffic,” EMBO J. 18, 3909–3923 (1999).
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D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004).
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F. Festy, S. M. Ameer-Beg, T. Ng, and K. Suhling, “Imaging proteins in vivo using fluorescence lifetime microscopy,” Mol. Biosyst. 3(6), 381–391 (2007).
[CrossRef] [PubMed]

K. Suhling, P. M. French, and D. Phillips, “Time-resolved fluorescence microscopy,” Photochem. Photobiol. Sci. 4(1), 13–22 (2005).
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D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004).
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D. Elson, J. Requejo-Isidro, I. Munro, F. Reavell, J. Siegel, K. Suhling, P. Tadrous, R. Benninger, P. Lanigan, J. McGinty, C. Talbot, B. Treanor, S. Webb, A. Sandison, A. Wallace, D. Davis, J. Lever, M. Neil, D. Phillips, G. Stamp, and P. French, “Time-domain fluorescence lifetime imaging applied to biological tissue,” Photochem. Photobiol. Sci. 3(8), 795–801 (2004).
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Z. Papagatsia, A. Tappuni, T. F. Watson, and R. J. Cook, “Single wavelength micro-endoscopy in non-surgical vascular lesion diagnosis & characterization,” J. Microsc. 230(2), 203–211 (2008).
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K. Makrogianneli, L. M. Carlin, M. D. Keppler, D. R. Matthews, E. Ofo, A. Coolen, S. M. Ameer-Beg, P. R. Barber, B. Vojnovic, and T. Ng, “Integrating receptor signal inputs that influence small Rho GTPase activation dynamics at the immunological synapse,” Mol. Cell. Biol. 29(11), 2997–3006 (2009).
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S. Prag, M. Parsons, M. D. Keppler, S. M. Ameer-Beg, P. Barber, J. Hunt, A. J. Beavil, R. Calvert, M. Arpin, B. Vojnovic, and T. Ng, “Activated ezrin promotes cell migration through recruitment of the GEF Dbl to lipid rafts and preferential downstream activation of Cdc42,” Mol. Biol. Cell 18(8), 2935–2948 (2007).
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M. Parsons, J. Monypenny, S. M. Ameer-Beg, T. H. Millard, L. M. Machesky, M. Peter, M. D. Keppler, G. Schiavo, R. Watson, J. Chernoff, D. Zicha, B. Vojnovic, and T. Ng, “Spatially distinct binding of Cdc42 to PAK1 and N-WASP in breast carcinoma cells,” Mol. Cell. Biol. 25(5), 1680–1695 (2005).
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Figures (3)

Fig. 1
Fig. 1

Schematic drawing of the experimental setup. (A) Main components of the setup are shown including a magnified reflection image of the front of the fiber bundle. The fiber cores have a diameter of 2.28 ± 0.48 µm and are spaced 2.80 ± 0.21 µm apart, leading to an optical resolution of about 5 µm. (B) Illustration of how the fiber bundle is coupled to the objective. The laser beam is scanned over the polished fiber bundle, which is aligned precisely with the focal plane.

Fig. 2
Fig. 2

Comparison of wide-field intensity and single-photon TCSPC FLIM measurements of small beads using either fluorescence lifetime microscopy or endoscopy through a coherent fiber bundle. (A) 10 µm and 4 µm microspheres were immersed alone (top and middle panels, respectively) or as a mixture in a clear 3D matrix and the bottom layer was imaged using a 20-fold objective (0.5 NA, 2.1 mm WD). From the single photon intensity FLIM images the fluorescence lifetime maps were calculated by applying mono-exponential fitting. The right column shows the corresponding fluorescence lifetime histograms. (B) The same samples were used for fluorescence lifetime endoscopy through a coherent fiber bundle of 2 m length and the data are shown as described for (A). Scale bars are 50 µm.

Fig. 3
Fig. 3

Fluorescence lifetime endoscopy of living mammalian cells. Wide-field and single-photon TCSPC images of cells expressing CXCR4-GFP and CXCR4-RFP together or CXCR4-GFP alone (control) are shown. The cells expressing both receptors show FRET between GFP and RFP due to receptor dimerization. Fluorescence lifetime maps are calculated from single-photon intensity images and the corresponding histograms are shown next to the fluorescence lifetime maps. (A) Images acquired in the microscopic mode. (B) Images acquired in the endoscopy mode. Scale bars are 20µm.

Equations (1)

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F R E T E f f = 1 τ D A τ D

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