Abstract

We demonstrate diffraction limited multiphoton imaging in a massively parallel, fully addressable time-resolved multi-beam multiphoton microscope capable of producing fluorescence lifetime images with sub-50ps temporal resolution. This imaging platform offers a significant improvement in acquisition speed over single-beam laser scanning FLIM by a factor of 64 without compromising in either the temporal or spatial resolutions of the system. We demonstrate FLIM acquisition at 500 ms with live cells expressing green fluorescent protein. The applicability of the technique to imaging protein-protein interactions in live cells is exemplified by observation of time-dependent FRET between the epidermal growth factor receptor (EGFR) and the adapter protein Grb2 following stimulation with the receptor ligand. Furthermore, ligand-dependent association of HER2-HER3 receptor tyrosine kinases was observed on a similar timescale and involved the internalisation and accumulation or receptor heterodimers within endosomes. These data demonstrate the broad applicability of this novel FLIM technique to the spatio-temporal dynamics of protein-protein interaction.

© 2015 Optical Society of America

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2014 (4)

K. Gala and S. Chandarlapaty, “Molecular Pathways: HER3 Targeted Therapy,” Clin. Cancer Res. 20(6), 1410–1416 (2014).
[Crossref] [PubMed]

Y. Park, H. Jung, M. Choi, W. Chang, Y. Choi, I. Do, J. Ahn, and Y. Im, “Role of HER3 expression and PTEN loss in patients with HER2-overexpressing metastatic breast cancer (MBC) who received taxane plus trastuzumab treatment,” Br. J. Cancer 110(2), 384–391 (2014).
[PubMed]

E. Charbon, “Single-photon imaging in complementary metal oxide semiconductor processes,” Philos. Trans. A. Math Phys. Eng. Sci. 372(2012), 20130100 (2014).
[Crossref] [PubMed]

S. P. Poland, N. Krstajić, R. D. Knight, R. K. Henderson, and S. M. Ameer-Beg, “Development of a doubly weighted Gerchberg-Saxton algorithm for use in multibeam imaging applications,” Opt. Lett. 39(8), 2431–2434 (2014).
[Crossref] [PubMed]

2013 (3)

J. L. Rinnenthal, C. Börnchen, H. Radbruch, V. Andresen, A. Mossakowski, V. Siffrin, T. Seelemann, H. Spiecker, I. Moll, J. Herz, A. E. Hauser, F. Zipp, M. J. Behne, and R. Niesner, “Parallelized TCSPC for dynamic intravital fluorescence lifetime imaging: Quantifying neuronal dysfunction in neuroinflammation,” PLoS ONE 8(4), e60100 (2013).
[Crossref] [PubMed]

S. Antonioli, L. Miari, A. Cuccato, M. Crotti, I. Rech, and M. Ghioni, “8-channel acquisition system for time-correlated single-photon counting,” Rev. Sci. Instrum. 84(6), 064705 (2013).
[Crossref] [PubMed]

X. Michalet, R. A. Colyer, G. Scalia, A. Ingargiola, R. Lin, J. E. Millaud, S. Weiss, O. H. Siegmund, A. S. Tremsin, J. V. Vallerga, A. Cheng, M. Levi, D. Aharoni, K. Arisaka, F. Villa, F. Guerrieri, F. Panzeri, I. Rech, A. Gulinatti, F. Zappa, M. Ghioni, and S. Cova, “Development of new photon-counting detectors for single-molecule fluorescence microscopy,” Philos. Trans. R. Soc. Lond. B Biol. Sci. 368(1611), 20120035 (2013).
[Crossref] [PubMed]

2011 (1)

D. D.-U. Li, J. Arlt, D. Tyndall, R. Walker, J. Richardson, D. Stoppa, E. Charbon, and R. K. Henderson, “Video-rate fluorescence lifetime imaging camera with CMOS single-photon avalanche diode arrays and high-speed imaging algorithm,” J. Biomed. Opt. 16, 096012 (2011).

2010 (1)

2009 (2)

J. R. Morris, C. Boutell, M. Keppler, R. Densham, D. Weekes, A. Alamshah, L. Butler, Y. Galanty, L. Pangon, T. Kiuchi, T. Ng, and E. Solomon, “The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress,” Nature 462(7275), 886–890 (2009).
[Crossref] [PubMed]

P. Barber, S. Ameer-Beg, J. Gilbey, L. 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(Suppl_1), S93–S105 (2009).
[Crossref]

2008 (1)

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]

2007 (4)

2006 (2)

J. Leach, K. Wulff, G. Sinclair, P. Jordan, J. Courtial, L. Thomson, G. Gibson, K. Karunwi, J. Cooper, Z. J. Laczik, and M. Padgett, “Interactive approach to optical tweezers control,” Appl. Opt. 45(5), 897–903 (2006).
[Crossref] [PubMed]

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

2005 (5)

M. Peter, S. M. Ameer-Beg, M. K. 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] [PubMed]

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
[Crossref] [PubMed]

Y. Enari, K. Hayasaka, T. Hokuue, K. Inami, T. Ohshima, N. Sato, M. Akatsu, S. Kawakami, Y. Miyabayashi, H. Tokuda, H. Yanase, H. Shimoi, and T. Fujimori, “Cross-talk of a multi-anode PMT and attainment of a TOF counter,” Nucl. Instrum. Methods Phys. Res. A 547(2-3), 490–503 (2005).
[Crossref]

Q. S. Hanley, K. A. Lidke, R. Heintzmann, D. J. Arndt-Jovin, and T. M. Jovin, “Fluorescence lifetime imaging in an optically sectioning programmable array microscope (PAM),” Cytometry A 67(2), 112–118 (2005).
[Crossref] [PubMed]

M. vandeVen, M. Ameloot, B. Valeur, and N. Boens, “Pitfalls and their remedies in time-resolved fluorescence spectroscopy and microscopy,” J. Fluoresc. 15(3), 377–413 (2005).
[Crossref] [PubMed]

2004 (4)

J. Kalisz, “Review of methods for time interval measurements with picosecond resolution,” Metrologia 41(1), 17–32 (2004).
[Crossref]

E. Van Munster and T. W. Gadella, “φFLIM: a new method to avoid aliasing in frequency‐domain fluorescence lifetime imaging microscopy,” J Microsc. 213(1), 29–38 (2004).
[Crossref]

E. B. van Munster and T. W. Gadella., “Suppression of photobleaching-induced artifacts in frequency-domain FLIM by permutation of the recording order,” Cytometry A 58(2), 185–194 (2004).
[Crossref] [PubMed]

J. Requejo-Isidro, J. McGinty, I. Munro, D. S. Elson, N. P. Galletly, M. J. Lever, M. 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 (5)

L. Sacconi, E. Froner, R. Antolini, M. R. Taghizadeh, A. Choudhury, and F. S. Pavone, “Multiphoton multifocal microscopy exploiting a diffractive optical element,” Opt. Lett. 28(20), 1918–1920 (2003).
[Crossref] [PubMed]

A. Agronskaia, L. Tertoolen, and H. Gerritsen, “High frame rate fluorescence lifetime imaging,” J. Phys. D Appl. Phys. 36(14), 1655–1662 (2003).
[Crossref]

E. Gratton, S. Breusegem, J. Sutin, Q. Ruan, and N. Barry, “Fluorescence lifetime imaging for the two-photon microscope: time-domain and frequency-domain methods,” J. Biomed. Opt. 8(3), 381–390 (2003).
[Crossref] [PubMed]

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref] [PubMed]

S. Yamasaki, K. Nishida, Y. Yoshida, M. Itoh, M. Hibi, and T. Hirano, “Gab1 is required for EGF receptor signaling and the transformation by activated ErbB2,” Oncogene 22(10), 1546–1556 (2003).
[Crossref] [PubMed]

2001 (4)

Q. S. Hanley, V. Subramaniam, D. J. Arndt-Jovin, and T. M. Jovin, “Fluorescence lifetime imaging: multi-point calibration, minimum resolvable differences, and artifact suppression,” Cytometry 43(4), 248–260 (2001).
[Crossref] [PubMed]

E. B. Brown, R. B. Campbell, Y. Tsuzuki, L. Xu, P. Carmeliet, D. Fukumura, and R. K. Jain, “In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy,” Nat. Med. 7(9), 1069 (2001).
[Crossref]

T. Nielsen, M. Fricke, D. Hellweg, and P. Andresen, “High efficiency beam splitter for multifocal multiphoton microscopy,” J. Microsc. 201(3), 368–376 (2001).
[Crossref] [PubMed]

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 (2)

P. I. Bastiaens and R. Pepperkok, “Observing proteins in their natural habitat: the living cell,” Trends Biochem. Sci. 25(12), 631–637 (2000).
[Crossref] [PubMed]

M.-F. Carlier, P. Nioche, I. Broutin-L’Hermite, R. Boujemaa, C. Le Clainche, C. Egile, C. Garbay, A. Ducruix, P. Sansonetti, and D. Pantaloni, “GRB2 links signaling to actin assembly by enhancing interaction of neural Wiskott-Aldrich syndrome protein (N-WASp) with actin-related protein (ARP2/3) complex,” J. Biol. Chem. 275(29), 21946–21952 (2000).
[Crossref] [PubMed]

1999 (2)

A. Miyawaki, O. Griesbeck, R. Heim, and R. Y. Tsien, “Dynamic and quantitative Ca2+ measurements using improved cameleons,” Proc. Natl. Acad. Sci. U.S.A. 96(5), 2135–2140 (1999).
[Crossref] [PubMed]

K. K. Sharman, A. Periasamy, H. Ashworth, and J. N. Demas, “Error analysis of the rapid lifetime determination method for double-exponential decays and new windowing schemes,” Anal. Chem. 71(5), 947–952 (1999).
[Crossref] [PubMed]

1998 (2)

A. Buist, M. Müller, J. Squier, and G. Brakenhoff, “Real time two-photon absorption microscopy using multi point excitation,” J. Microsc. 192(2), 217–226 (1998).
[Crossref]

J. Bewersdorf, R. Pick, and S. W. Hell, “Multifocal multiphoton microscopy,” Opt. Lett. 23(9), 655–657 (1998).
[Crossref] [PubMed]

1997 (1)

P. C. Schneider and R. M. Clegg, “Rapid acquisition, analysis, and display of fluorescence lifetime-resolved images for real-time applications,” Rev. Sci. Instrum. 68(11), 4107–4119 (1997).
[Crossref]

1996 (3)

L. Wong and G. R. Johnson, “Epidermal growth factor induces coupling of protein-tyrosine phosphatase 1D to GRB2 via the COOH-terminal SH3 domain of GRB2,” J. Biol. Chem. 271(35), 20981–20984 (1996).
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K. Suhling, D. McLoskey, and D. Birch, “Multiplexed single‐photon counting. II. The statistical theory of time‐correlated measurements,” Rev. Sci. Instrum. 67(6), 2238–2246 (1996).
[Crossref]

D. McLoskey, D. J. Birch, A. Sanderson, K. Suhling, E. Welch, and P. Hicks, “Multiplexed single‐photon counting. I. A time‐correlated fluorescence lifetime camera,” Rev. Sci. Instrum. 67(6), 2228–2237 (1996).
[Crossref]

1993 (2)

S. E. Egan, B. W. Giddings, M. W. Brooks, L. Buday, A. M. Sizeland, and R. A. Weinberg, “Association of Sos Ras exchange protein with Grb2 is implicated in tyrosine kinase signal transduction and transformation,” Nature 363(6424), 45–51 (1993).
[Crossref] [PubMed]

J. P. Olivier, T. Raabe, M. Henkemeyer, B. Dickson, G. Mbamalu, B. Margolis, J. Schlessinger, E. Hafen, and T. Pawson, “A Drosophila SH2-SH3 adaptor protein implicated in coupling the sevenless tyrosine kinase to an activator of Ras guanine nucleotide exchange, Sos,” Cell 73(1), 179–191 (1993).
[Crossref] [PubMed]

1992 (1)

M. Köllner and J. Wolfrum, “How many photons are necessary for fluorescence-lifetime measurements?” Chem. Phys. Lett. 200(1-2), 199–204 (1992).
[Crossref]

1990 (1)

W. Denk, J. H. Strickler, and W. W. Webb, “Two-Photon Laser Scanning Fluorescence Microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

Agronskaia, A.

A. Agronskaia, L. Tertoolen, and H. Gerritsen, “High frame rate fluorescence lifetime imaging,” J. Phys. D Appl. Phys. 36(14), 1655–1662 (2003).
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Aharoni, D.

X. Michalet, R. A. Colyer, G. Scalia, A. Ingargiola, R. Lin, J. E. Millaud, S. Weiss, O. H. Siegmund, A. S. Tremsin, J. V. Vallerga, A. Cheng, M. Levi, D. Aharoni, K. Arisaka, F. Villa, F. Guerrieri, F. Panzeri, I. Rech, A. Gulinatti, F. Zappa, M. Ghioni, and S. Cova, “Development of new photon-counting detectors for single-molecule fluorescence microscopy,” Philos. Trans. R. Soc. Lond. B Biol. Sci. 368(1611), 20120035 (2013).
[Crossref] [PubMed]

Ahn, J.

Y. Park, H. Jung, M. Choi, W. Chang, Y. Choi, I. Do, J. Ahn, and Y. Im, “Role of HER3 expression and PTEN loss in patients with HER2-overexpressing metastatic breast cancer (MBC) who received taxane plus trastuzumab treatment,” Br. J. Cancer 110(2), 384–391 (2014).
[PubMed]

Akatsu, M.

Y. Enari, K. Hayasaka, T. Hokuue, K. Inami, T. Ohshima, N. Sato, M. Akatsu, S. Kawakami, Y. Miyabayashi, H. Tokuda, H. Yanase, H. Shimoi, and T. Fujimori, “Cross-talk of a multi-anode PMT and attainment of a TOF counter,” Nucl. Instrum. Methods Phys. Res. A 547(2-3), 490–503 (2005).
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Alamshah, A.

J. R. Morris, C. Boutell, M. Keppler, R. Densham, D. Weekes, A. Alamshah, L. Butler, Y. Galanty, L. Pangon, T. Kiuchi, T. Ng, and E. Solomon, “The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress,” Nature 462(7275), 886–890 (2009).
[Crossref] [PubMed]

Ameer-Beg, S.

P. Barber, S. Ameer-Beg, J. Gilbey, L. 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(Suppl_1), S93–S105 (2009).
[Crossref]

Ameer-Beg, S. M.

S. P. Poland, N. Krstajić, R. D. Knight, R. K. Henderson, and S. M. Ameer-Beg, “Development of a doubly weighted Gerchberg-Saxton algorithm for use in multibeam imaging applications,” Opt. Lett. 39(8), 2431–2434 (2014).
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M. Peter, S. M. Ameer-Beg, M. K. 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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Ameloot, M.

M. vandeVen, M. Ameloot, B. Valeur, and N. Boens, “Pitfalls and their remedies in time-resolved fluorescence spectroscopy and microscopy,” J. Fluoresc. 15(3), 377–413 (2005).
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Anand, P.

Anand, U.

Andresen, P.

T. Nielsen, M. Fricke, D. Hellweg, and P. Andresen, “High efficiency beam splitter for multifocal multiphoton microscopy,” J. Microsc. 201(3), 368–376 (2001).
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Andresen, V.

J. L. Rinnenthal, C. Börnchen, H. Radbruch, V. Andresen, A. Mossakowski, V. Siffrin, T. Seelemann, H. Spiecker, I. Moll, J. Herz, A. E. Hauser, F. Zipp, M. J. Behne, and R. Niesner, “Parallelized TCSPC for dynamic intravital fluorescence lifetime imaging: Quantifying neuronal dysfunction in neuroinflammation,” PLoS ONE 8(4), e60100 (2013).
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Antolini, R.

Antonioli, S.

S. Antonioli, L. Miari, A. Cuccato, M. Crotti, I. Rech, and M. Ghioni, “8-channel acquisition system for time-correlated single-photon counting,” Rev. Sci. Instrum. 84(6), 064705 (2013).
[Crossref] [PubMed]

Arisaka, K.

X. Michalet, R. A. Colyer, G. Scalia, A. Ingargiola, R. Lin, J. E. Millaud, S. Weiss, O. H. Siegmund, A. S. Tremsin, J. V. Vallerga, A. Cheng, M. Levi, D. Aharoni, K. Arisaka, F. Villa, F. Guerrieri, F. Panzeri, I. Rech, A. Gulinatti, F. Zappa, M. Ghioni, and S. Cova, “Development of new photon-counting detectors for single-molecule fluorescence microscopy,” Philos. Trans. R. Soc. Lond. B Biol. Sci. 368(1611), 20120035 (2013).
[Crossref] [PubMed]

Arlt, J.

D. D.-U. Li, J. Arlt, D. Tyndall, R. Walker, J. Richardson, D. Stoppa, E. Charbon, and R. K. Henderson, “Video-rate fluorescence lifetime imaging camera with CMOS single-photon avalanche diode arrays and high-speed imaging algorithm,” J. Biomed. Opt. 16, 096012 (2011).

Arndt-Jovin, D. J.

Q. S. Hanley, K. A. Lidke, R. Heintzmann, D. J. Arndt-Jovin, and T. M. Jovin, “Fluorescence lifetime imaging in an optically sectioning programmable array microscope (PAM),” Cytometry A 67(2), 112–118 (2005).
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Q. S. Hanley, V. Subramaniam, D. J. Arndt-Jovin, and T. M. Jovin, “Fluorescence lifetime imaging: multi-point calibration, minimum resolvable differences, and artifact suppression,” Cytometry 43(4), 248–260 (2001).
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Ashworth, H.

K. K. Sharman, A. Periasamy, H. Ashworth, and J. N. Demas, “Error analysis of the rapid lifetime determination method for double-exponential decays and new windowing schemes,” Anal. Chem. 71(5), 947–952 (1999).
[Crossref] [PubMed]

Audugé, N.

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]

Barber, P.

P. Barber, S. Ameer-Beg, J. Gilbey, L. 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(Suppl_1), S93–S105 (2009).
[Crossref]

Barry, N.

E. Gratton, S. Breusegem, J. Sutin, Q. Ruan, and N. Barry, “Fluorescence lifetime imaging for the two-photon microscope: time-domain and frequency-domain methods,” J. Biomed. Opt. 8(3), 381–390 (2003).
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Bastiaens, P. I.

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

P. I. Bastiaens and R. Pepperkok, “Observing proteins in their natural habitat: the living cell,” Trends Biochem. Sci. 25(12), 631–637 (2000).
[Crossref] [PubMed]

Behne, M. J.

J. L. Rinnenthal, C. Börnchen, H. Radbruch, V. Andresen, A. Mossakowski, V. Siffrin, T. Seelemann, H. Spiecker, I. Moll, J. Herz, A. E. Hauser, F. Zipp, M. J. Behne, and R. Niesner, “Parallelized TCSPC for dynamic intravital fluorescence lifetime imaging: Quantifying neuronal dysfunction in neuroinflammation,” PLoS ONE 8(4), e60100 (2013).
[Crossref] [PubMed]

Benham, C.

Benninger, R. K. P.

Bewersdorf, J.

Birch, D.

K. Suhling, D. McLoskey, and D. Birch, “Multiplexed single‐photon counting. II. The statistical theory of time‐correlated measurements,” Rev. Sci. Instrum. 67(6), 2238–2246 (1996).
[Crossref]

Birch, D. J.

D. McLoskey, D. J. Birch, A. Sanderson, K. Suhling, E. Welch, and P. Hicks, “Multiplexed single‐photon counting. I. A time‐correlated fluorescence lifetime camera,” Rev. Sci. Instrum. 67(6), 2228–2237 (1996).
[Crossref]

Boens, N.

M. vandeVen, M. Ameloot, B. Valeur, and N. Boens, “Pitfalls and their remedies in time-resolved fluorescence spectroscopy and microscopy,” J. Fluoresc. 15(3), 377–413 (2005).
[Crossref] [PubMed]

Börnchen, C.

J. L. Rinnenthal, C. Börnchen, H. Radbruch, V. Andresen, A. Mossakowski, V. Siffrin, T. Seelemann, H. Spiecker, I. Moll, J. Herz, A. E. Hauser, F. Zipp, M. J. Behne, and R. Niesner, “Parallelized TCSPC for dynamic intravital fluorescence lifetime imaging: Quantifying neuronal dysfunction in neuroinflammation,” PLoS ONE 8(4), e60100 (2013).
[Crossref] [PubMed]

Boujemaa, R.

M.-F. Carlier, P. Nioche, I. Broutin-L’Hermite, R. Boujemaa, C. Le Clainche, C. Egile, C. Garbay, A. Ducruix, P. Sansonetti, and D. Pantaloni, “GRB2 links signaling to actin assembly by enhancing interaction of neural Wiskott-Aldrich syndrome protein (N-WASp) with actin-related protein (ARP2/3) complex,” J. Biol. Chem. 275(29), 21946–21952 (2000).
[Crossref] [PubMed]

Boutell, C.

J. R. Morris, C. Boutell, M. Keppler, R. Densham, D. Weekes, A. Alamshah, L. Butler, Y. Galanty, L. Pangon, T. Kiuchi, T. Ng, and E. Solomon, “The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress,” Nature 462(7275), 886–890 (2009).
[Crossref] [PubMed]

Brakenhoff, G.

A. Buist, M. Müller, J. Squier, and G. Brakenhoff, “Real time two-photon absorption microscopy using multi point excitation,” J. Microsc. 192(2), 217–226 (1998).
[Crossref]

Breusegem, S.

E. Gratton, S. Breusegem, J. Sutin, Q. Ruan, and N. Barry, “Fluorescence lifetime imaging for the two-photon microscope: time-domain and frequency-domain methods,” J. Biomed. Opt. 8(3), 381–390 (2003).
[Crossref] [PubMed]

Brooks, M. W.

S. E. Egan, B. W. Giddings, M. W. Brooks, L. Buday, A. M. Sizeland, and R. A. Weinberg, “Association of Sos Ras exchange protein with Grb2 is implicated in tyrosine kinase signal transduction and transformation,” Nature 363(6424), 45–51 (1993).
[Crossref] [PubMed]

Broutin-L’Hermite, I.

M.-F. Carlier, P. Nioche, I. Broutin-L’Hermite, R. Boujemaa, C. Le Clainche, C. Egile, C. Garbay, A. Ducruix, P. Sansonetti, and D. Pantaloni, “GRB2 links signaling to actin assembly by enhancing interaction of neural Wiskott-Aldrich syndrome protein (N-WASp) with actin-related protein (ARP2/3) complex,” J. Biol. Chem. 275(29), 21946–21952 (2000).
[Crossref] [PubMed]

Brown, E. B.

E. B. Brown, R. B. Campbell, Y. Tsuzuki, L. Xu, P. Carmeliet, D. Fukumura, and R. K. Jain, “In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy,” Nat. Med. 7(9), 1069 (2001).
[Crossref]

Buday, L.

S. E. Egan, B. W. Giddings, M. W. Brooks, L. Buday, A. M. Sizeland, and R. A. Weinberg, “Association of Sos Ras exchange protein with Grb2 is implicated in tyrosine kinase signal transduction and transformation,” Nature 363(6424), 45–51 (1993).
[Crossref] [PubMed]

Buist, A.

A. Buist, M. Müller, J. Squier, and G. Brakenhoff, “Real time two-photon absorption microscopy using multi point excitation,” J. Microsc. 192(2), 217–226 (1998).
[Crossref]

Bunney, T. D.

Butler, L.

J. R. Morris, C. Boutell, M. Keppler, R. Densham, D. Weekes, A. Alamshah, L. Butler, Y. Galanty, L. Pangon, T. Kiuchi, T. Ng, and E. Solomon, “The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress,” Nature 462(7275), 886–890 (2009).
[Crossref] [PubMed]

Campbell, R. B.

E. B. Brown, R. B. Campbell, Y. Tsuzuki, L. Xu, P. Carmeliet, D. Fukumura, and R. K. Jain, “In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy,” Nat. Med. 7(9), 1069 (2001).
[Crossref]

Carlier, M.-F.

M.-F. Carlier, P. Nioche, I. Broutin-L’Hermite, R. Boujemaa, C. Le Clainche, C. Egile, C. Garbay, A. Ducruix, P. Sansonetti, and D. Pantaloni, “GRB2 links signaling to actin assembly by enhancing interaction of neural Wiskott-Aldrich syndrome protein (N-WASp) with actin-related protein (ARP2/3) complex,” J. Biol. Chem. 275(29), 21946–21952 (2000).
[Crossref] [PubMed]

Carlin, L.

P. Barber, S. Ameer-Beg, J. Gilbey, L. 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(Suppl_1), S93–S105 (2009).
[Crossref]

Carmeliet, P.

E. B. Brown, R. B. Campbell, Y. Tsuzuki, L. Xu, P. Carmeliet, D. Fukumura, and R. K. Jain, “In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy,” Nat. Med. 7(9), 1069 (2001).
[Crossref]

Chandarlapaty, S.

K. Gala and S. Chandarlapaty, “Molecular Pathways: HER3 Targeted Therapy,” Clin. Cancer Res. 20(6), 1410–1416 (2014).
[Crossref] [PubMed]

Chang, W.

Y. Park, H. Jung, M. Choi, W. Chang, Y. Choi, I. Do, J. Ahn, and Y. Im, “Role of HER3 expression and PTEN loss in patients with HER2-overexpressing metastatic breast cancer (MBC) who received taxane plus trastuzumab treatment,” Br. J. Cancer 110(2), 384–391 (2014).
[PubMed]

Charbon, E.

E. Charbon, “Single-photon imaging in complementary metal oxide semiconductor processes,” Philos. Trans. A. Math Phys. Eng. Sci. 372(2012), 20130100 (2014).
[Crossref] [PubMed]

D. D.-U. Li, J. Arlt, D. Tyndall, R. Walker, J. Richardson, D. Stoppa, E. Charbon, and R. K. Henderson, “Video-rate fluorescence lifetime imaging camera with CMOS single-photon avalanche diode arrays and high-speed imaging algorithm,” J. Biomed. Opt. 16, 096012 (2011).

Cheng, A.

X. Michalet, R. A. Colyer, G. Scalia, A. Ingargiola, R. Lin, J. E. Millaud, S. Weiss, O. H. Siegmund, A. S. Tremsin, J. V. Vallerga, A. Cheng, M. Levi, D. Aharoni, K. Arisaka, F. Villa, F. Guerrieri, F. Panzeri, I. Rech, A. Gulinatti, F. Zappa, M. Ghioni, and S. Cova, “Development of new photon-counting detectors for single-molecule fluorescence microscopy,” Philos. Trans. R. Soc. Lond. B Biol. Sci. 368(1611), 20120035 (2013).
[Crossref] [PubMed]

Choi, M.

Y. Park, H. Jung, M. Choi, W. Chang, Y. Choi, I. Do, J. Ahn, and Y. Im, “Role of HER3 expression and PTEN loss in patients with HER2-overexpressing metastatic breast cancer (MBC) who received taxane plus trastuzumab treatment,” Br. J. Cancer 110(2), 384–391 (2014).
[PubMed]

Choi, Y.

Y. Park, H. Jung, M. Choi, W. Chang, Y. Choi, I. Do, J. Ahn, and Y. Im, “Role of HER3 expression and PTEN loss in patients with HER2-overexpressing metastatic breast cancer (MBC) who received taxane plus trastuzumab treatment,” Br. J. Cancer 110(2), 384–391 (2014).
[PubMed]

Choudhury, A.

Clegg, R. M.

P. C. Schneider and R. M. Clegg, “Rapid acquisition, analysis, and display of fluorescence lifetime-resolved images for real-time applications,” Rev. Sci. Instrum. 68(11), 4107–4119 (1997).
[Crossref]

Colyer, R. A.

X. Michalet, R. A. Colyer, G. Scalia, A. Ingargiola, R. Lin, J. E. Millaud, S. Weiss, O. H. Siegmund, A. S. Tremsin, J. V. Vallerga, A. Cheng, M. Levi, D. Aharoni, K. Arisaka, F. Villa, F. Guerrieri, F. Panzeri, I. Rech, A. Gulinatti, F. Zappa, M. Ghioni, and S. Cova, “Development of new photon-counting detectors for single-molecule fluorescence microscopy,” Philos. Trans. R. Soc. Lond. B Biol. Sci. 368(1611), 20120035 (2013).
[Crossref] [PubMed]

R. A. Colyer, G. Scalia, I. Rech, A. Gulinatti, M. Ghioni, S. Cova, S. Weiss, and X. Michalet, “High-throughput FCS using an LCOS spatial light modulator and an 8 × 1 SPAD array,” Biomed. Opt. Express 1(5), 1408–1431 (2010).
[Crossref] [PubMed]

Cooper, J.

Coppey-Moisan, M.

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]

Courtial, J.

Courtney, P.

Cova, S.

X. Michalet, R. A. Colyer, G. Scalia, A. Ingargiola, R. Lin, J. E. Millaud, S. Weiss, O. H. Siegmund, A. S. Tremsin, J. V. Vallerga, A. Cheng, M. Levi, D. Aharoni, K. Arisaka, F. Villa, F. Guerrieri, F. Panzeri, I. Rech, A. Gulinatti, F. Zappa, M. Ghioni, and S. Cova, “Development of new photon-counting detectors for single-molecule fluorescence microscopy,” Philos. Trans. R. Soc. Lond. B Biol. Sci. 368(1611), 20120035 (2013).
[Crossref] [PubMed]

R. A. Colyer, G. Scalia, I. Rech, A. Gulinatti, M. Ghioni, S. Cova, S. Weiss, and X. Michalet, “High-throughput FCS using an LCOS spatial light modulator and an 8 × 1 SPAD array,” Biomed. Opt. Express 1(5), 1408–1431 (2010).
[Crossref] [PubMed]

Crotti, M.

S. Antonioli, L. Miari, A. Cuccato, M. Crotti, I. Rech, and M. Ghioni, “8-channel acquisition system for time-correlated single-photon counting,” Rev. Sci. Instrum. 84(6), 064705 (2013).
[Crossref] [PubMed]

Cuccato, A.

S. Antonioli, L. Miari, A. Cuccato, M. Crotti, I. Rech, and M. Ghioni, “8-channel acquisition system for time-correlated single-photon counting,” Rev. Sci. Instrum. 84(6), 064705 (2013).
[Crossref] [PubMed]

Davis, D. M.

De Beule, P. A. A.

Demas, J. N.

K. K. Sharman, A. Periasamy, H. Ashworth, and J. N. Demas, “Error analysis of the rapid lifetime determination method for double-exponential decays and new windowing schemes,” Anal. Chem. 71(5), 947–952 (1999).
[Crossref] [PubMed]

Denk, W.

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
[Crossref] [PubMed]

W. Denk, J. H. Strickler, and W. W. Webb, “Two-Photon Laser Scanning Fluorescence Microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

Densham, R.

J. R. Morris, C. Boutell, M. Keppler, R. Densham, D. Weekes, A. Alamshah, L. Butler, Y. Galanty, L. Pangon, T. Kiuchi, T. Ng, and E. Solomon, “The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress,” Nature 462(7275), 886–890 (2009).
[Crossref] [PubMed]

Dickson, B.

J. P. Olivier, T. Raabe, M. Henkemeyer, B. Dickson, G. Mbamalu, B. Margolis, J. Schlessinger, E. Hafen, and T. Pawson, “A Drosophila SH2-SH3 adaptor protein implicated in coupling the sevenless tyrosine kinase to an activator of Ras guanine nucleotide exchange, Sos,” Cell 73(1), 179–191 (1993).
[Crossref] [PubMed]

Do, I.

Y. Park, H. Jung, M. Choi, W. Chang, Y. Choi, I. Do, J. Ahn, and Y. Im, “Role of HER3 expression and PTEN loss in patients with HER2-overexpressing metastatic breast cancer (MBC) who received taxane plus trastuzumab treatment,” Br. J. Cancer 110(2), 384–391 (2014).
[PubMed]

Ducruix, A.

M.-F. Carlier, P. Nioche, I. Broutin-L’Hermite, R. Boujemaa, C. Le Clainche, C. Egile, C. Garbay, A. Ducruix, P. Sansonetti, and D. Pantaloni, “GRB2 links signaling to actin assembly by enhancing interaction of neural Wiskott-Aldrich syndrome protein (N-WASp) with actin-related protein (ARP2/3) complex,” J. Biol. Chem. 275(29), 21946–21952 (2000).
[Crossref] [PubMed]

Dunsby, C.

Dymoke-Bradshaw, A. K.

Egan, S. E.

S. E. Egan, B. W. Giddings, M. W. Brooks, L. Buday, A. M. Sizeland, and R. A. Weinberg, “Association of Sos Ras exchange protein with Grb2 is implicated in tyrosine kinase signal transduction and transformation,” Nature 363(6424), 45–51 (1993).
[Crossref] [PubMed]

Egile, C.

M.-F. Carlier, P. Nioche, I. Broutin-L’Hermite, R. Boujemaa, C. Le Clainche, C. Egile, C. Garbay, A. Ducruix, P. Sansonetti, and D. Pantaloni, “GRB2 links signaling to actin assembly by enhancing interaction of neural Wiskott-Aldrich syndrome protein (N-WASp) with actin-related protein (ARP2/3) complex,” J. Biol. Chem. 275(29), 21946–21952 (2000).
[Crossref] [PubMed]

Elferink, L. A.

N. Li, M. Lorinczi, K. Ireton, and L. A. Elferink, “Specific Grb2-mediated interactions regulate clathrin-dependent endocytosis of the cMet-tyrosine kinase,” J. Biol. Chem. 282(23), 16764–16775 (2007).
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D. D.-U. Li, J. Arlt, D. Tyndall, R. Walker, J. Richardson, D. Stoppa, E. Charbon, and R. K. Henderson, “Video-rate fluorescence lifetime imaging camera with CMOS single-photon avalanche diode arrays and high-speed imaging algorithm,” J. Biomed. Opt. 16, 096012 (2011).

Webb, W. W.

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
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Wulff, K.

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S. Yamasaki, K. Nishida, Y. Yoshida, M. Itoh, M. Hibi, and T. Hirano, “Gab1 is required for EGF receptor signaling and the transformation by activated ErbB2,” Oncogene 22(10), 1546–1556 (2003).
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Nat. Med. (1)

E. B. Brown, R. B. Campbell, Y. Tsuzuki, L. Xu, P. Carmeliet, D. Fukumura, and R. K. Jain, “In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy,” Nat. Med. 7(9), 1069 (2001).
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S. Yamasaki, K. Nishida, Y. Yoshida, M. Itoh, M. Hibi, and T. Hirano, “Gab1 is required for EGF receptor signaling and the transformation by activated ErbB2,” Oncogene 22(10), 1546–1556 (2003).
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Supplementary Material (4)

» Media 1: AVI (31003 KB)     
» Media 2: AVI (17041 KB)     
» Media 3: AVI (12379 KB)     
» Media 4: AVI (17596 KB)     

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Figures (13)

Fig. 1
Fig. 1

Operational schematic of the multifocal multiphoton system.

Fig. 2
Fig. 2

A flow chart detailing the Megaframe camera internal architecture, consisting of the motherboard PCB holding the Megaframe camera and programmable logic (FPGA). The FPGA controls the Megaframe camera readout and forwards the data to PC via USB2.0 link.

Fig. 3
Fig. 3

Comparing raw data with a DNL corrected histogram for a 7x7 detector array. Correction of the DNL gives a marked reduction of the intensity variation of the transient.

Fig. 4
Fig. 4

Presents data on the 7 × 7 detector array used for imaging (a) the temporal bin size of each detector in the 7 × 7 array. Average temporal resolution of the 7 × 7 array is 52.5 +/− 0.7ps. Variation in the temporal bin sizes are due to minor discrepancies between individual SPADs caused in the fabrication process of the chip. (b) Presents a histogram of the distribution of bin sizes of the 7 × 7 detector array.

Fig. 5
Fig. 5

Presents resolution imaging performance of the microscope across all beamlets which were calculated by imaging sub-resolution (100 nm dia.) fluorescent beads. (a) A typical lateral PSF of a single bead. (b) A typical axial PSF of a single bead. (c) The average lateral resolutions per detector for 5 × 5 detector array (d) The average axial resolutions per detector for a 5 × 5 array.

Fig. 6
Fig. 6

Comparing lifetime analysis techniques for image acquisition of live cells at high speed. MCF-7 human breast carcinoma cells were transiently transfected with EGFP only and data sets were acquired for a 7 × 7 array for 500 milliseconds and 5 seconds. In a 256 × 256 data set, a maximum of 200 photons and 2000 photons were collected per pixel at 500 milliseconds and 5 second acquisitions respectively. In order to simulate the analysis of time gated camera to compare with Levenberg-Marquardt (L-M) fitting using Tri2 we used the 2 gated Rapid Lifetime Determination (RLD) approach for single exponential decays with 2 ns gate size. Lifetime images are displayed for both techniques with no binning and 5 × 5 circular binning for both 500 milliseconds and 5second acquisitions and their histograms compared. L-M clearly outperforms the RLD in all data analysis performed giving a much more accurate determination of the lifetime. The average calculated lifetimes for 500 ms acquisitions are: RLD no binning = 2.12 +/− 0.83 ns, RLD 5 × 5 circ. binning = 2.30 ± 0.46 ns, L-M no binning = 2.25 ± 0.39 ns and L-M 5 × 5 circ. binning = 2.23 ± 0.07 ns. The average calculated lifetimes for 5 s acquisitions are: RLD no binning = 2.31 ± 0.49 ns, RLD 5 × 5 circ. binning = 2.28 ± 0.29 ns, L-M no binning = 2.23 ± 0.12 ns and L-M 5 × 5 circ. binning = 2.24 ± 0.06 ns.

Fig. 7
Fig. 7

(a) Comparing widefield fluorescence, MP intensity and fluorescence lifetime data sets of test MCF-7 cells expressing EGFR-EGFP (control vs EGFR-EGFP & Grb2-mCherry, pre and post treated with EGF ligand. Acquisition time per frame is 15 seconds and all images have an 87.5µm x 87.5µm field of view. (b) Statistical analysis comparing FRET efficiencies of control MCF-7 cells expressing HER2-EGFP with MCF-7 cells coexpressing HER2-EGFP & HER3-mRFP1, both pre and post addition of neuregulin ligand. In order to compare two different populations (control vs. test) for statistical significance, two-tailed unpaired Student t-test was used. For the same populations (pre vs. post treatment) paired t-test was used. *** between populations denotes a highly significant difference in lifetime values (p<0.0001).

Fig. 8
Fig. 8

(a) Fluorescence widefield image highlighting the relative abundance of donor (green) and acceptor (red) regions in each cell. (b) A composite of Intensity and lifetime images are presented highlighting the ROIs chosen for the cells which were examined before and after neuregulin ligand was added. (c) Average FRET efficiencies values of the ROIs are presented in the accompanying graph with 0 seconds indicating the moment that neuregulin addition occurs. Cells were imaged every 15s for 40 minutes.

Fig. 9
Fig. 9

Intensity, lifetime and composite images for a four frames in the time lapse (Media 1).

Fig. 10
Fig. 10

(a) Comparing widefield fluorescence, MP intensity and fluorescence lifetime data sets of control MCF-7 cells expressing EGFR-EGFP vs test MCF-7 cells expressing EGFR-EGFP & Grb2-mCherry, pre and post treated with EGF ligand. Acquisition time per frame is 10 seconds and all images have an 87.5µm x 87.5µm field of view.(b) Statistical analysis comparing control MCF-7 cells expressing EGFR-EGFP with MCF-7 cells coexpressing EGFR-EGFP & Grb2-mCherry, both pre and post addition of EGF ligand. In order to compare two different populations (control vs. test) for significance two-tailed unpaired Student t-test was used. For the same populations (pre vs. post treatment) paired t-test was used. *** between populations denotes a highly significant difference in lifetime values (p<0.0001).

Fig. 11
Fig. 11

(a) Fluorescence widefield image highlighting the relative abundance of donor (green) and acceptor (red) in each cell. (b) A composite of intensity and lifetime images are presented highlighting the ROIs chosen for the two cells which were examined before and after EGF ligand was added. (c) Average FRET efficiency values of the region of interest (ROI) are presented in the accompanying graph with 0 seconds indicating the moment that EGF addition occurs (Media 2).

Fig. 12
Fig. 12

3D-image stack of a 40 z-sections acquired in 400 s (1 section/10s) of an MCF-7 cell, taken pre and post EGF addition (Media 3). Data taken before and after the time lapse data had been acquired.

Fig. 13
Fig. 13

Data from Fig. 11 reanalysed by biexponential global analysis to determine the fraction of EGFR-EGFP interacting by FRET with Grb2-mCherry. (a) Presents the total fraction of FRET interacting species, pre and post EGF addition. (b) Histograms comparing fractional contributions of FRET interaction species for pre and post EGF ligand addition (Media 4).

Metrics