Abstract

Förster resonance energy transfer (FRET) imaging is an essential analytical method in biomedical research. The limited photon-budget experimentally available, however, imposes compromises between spatiotemporal and biochemical resolutions, photodamage and phototoxicity. The study of photon-statistics in biochemical imaging is thus important in guiding the efficient design of instrumentation and assays. Here, we show a comparative analysis of photon-statistics in FRET imaging demonstrating how the precision of FRET imaging varies vastly with imaging parameters. Therefore, we provide analytical and numerical tools for assay optimization. Fluorescence lifetime imaging microscopy (FLIM) is a very robust technique with excellent photon-efficiencies. However, we show that also intensity-based FRET imaging can reach high precision by utilizing information from both donor and acceptor fluorophores.

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References

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2019 (3)

2018 (3)

K. J. Martin, E. J. McGhee, J. P. Schwarz, M. Drysdale, S. M. Brachmann, V. Stucke, O. J. Sansom, and K. I. Anderson, “Accepting from the best donor; analysis of long-lifetime donor fluorescent protein pairings to optimise dynamic FLIM-based FRET experiments,” PLoS One 13(1), e0183585 (2018).
[Crossref]

I. M. Antolovic, C. Bruschini, and E. Charbon, “Dynamic range extension for photon counting arrays,” Opt. Express 26(17), 22234–22248 (2018).
[Crossref]

Q. Ni, S. Mehta, and J. Zhang, “Live-cell imaging of cell signaling using genetically encoded fluorescent reporters,” FEBS J. 285(2), 203–219 (2018).
[Crossref]

2017 (3)

J. R. W. Conway, S. C. Warren, and P. Timpson, “Context-dependent intravital imaging of therapeutic response using intramolecular FRET biosensors,” Methods 128, 78–94 (2017).
[Crossref]

A. D. Elliott, N. Bedard, A. Ustione, M. A. Baird, M. W. Davidson, T. Tkaczyk, and D. W. Piston, “Hyperspectral imaging for simultaneous measurements of two FRET biosensors in pancreatic beta-cells,” PLoS One 12(12), e0188789 (2017).
[Crossref]

C. Demeautis, F. Sipieter, J. Roul, C. Chapuis, S. Padilla-Parra, F. B. Riquet, and M. Tramier, “Multiplexing PKA and ERK1&2 kinases FRET biosensors in living cells using single excitation wavelength dual colour FLIM,” Sci. Rep. 7(1), 41026 (2017).
[Crossref]

2016 (3)

S. Isbaner, N. Karedla, D. Ruhlandt, S. C. Stein, A. Chizhik, I. Gregor, and J. Enderlein, “Dead-time correction of fluorescence lifetime measurements and fluorescence lifetime imaging,” Opt. Express 24(9), 9429–9445 (2016).
[Crossref]

M. Raspe, K. M. Kedziora, B. van den Broek, Q. Zhao, S. de Jong, J. Herz, M. Mastop, J. Goedhart, T. W. Gadella, I. T. Young, and K. Jalink, “siFLIM: single-image frequency-domain FLIM provides fast and photon-efficient lifetime data,” Nat. Methods 13(6), 501–504 (2016).
[Crossref]

B. T. Bajar, E. S. Wang, S. Zhang, M. Z. Lin, and J. Chu, “A Guide to Fluorescent Protein FRET Pairs,” Sensors 16(9), 1488 (2016).
[Crossref]

2015 (3)

M. Popleteeva, K. T. Haas, D. Stoppa, L. Pancheri, L. Gasparini, C. F. Kaminski, L. D. Cassidy, A. R. Venkitaraman, and A. Esposito, “Fast and simple spectral FLIM for biochemical and medical imaging,” Opt. Express 23(18), 23511–23525 (2015).
[Crossref]

N. Krstajic, J. Levitt, S. Poland, S. Ameer-Beg, and R. Henderson, “256 × 2 SPAD line sensor for time resolved fluorescence spectroscopy,” Opt. Express 23(5), 5653–5669 (2015).
[Crossref]

J. Klarenbeek, J. Goedhart, A. van Batenburg, D. Groenewald, and K. Jalink, “Fourth-generation epac-based FRET sensors for cAMP feature exceptional brightness, photostability and dynamic range: characterization of dedicated sensors for FLIM, for ratiometry and with high affinity,” PLoS One 10(4), e0122513 (2015).
[Crossref]

2013 (1)

A. Esposito, M. Popleteeva, and A. R. Venkitaraman, “Maximizing the biochemical resolving power of fluorescence microscopy,” PLoS One 8(10), e77392 (2013).
[Crossref]

2012 (3)

F. Fereidouni, A. N. Bader, and H. C. Gerritsen, “Spectral phasor analysis allows rapid and reliable unmixing of fluorescence microscopy spectral images,” Opt. Express 20(12), 12729–12741 (2012).
[Crossref]

A. Zeug, A. Woehler, E. Neher, and E. G. Ponimaskin, “Quantitative intensity-based FRET approaches–a comparative snapshot,” Biophys. J. 103(9), 1821–1827 (2012).
[Crossref]

E. Hirata, H. Yukinaga, Y. Kamioka, Y. Arakawa, S. Miyamoto, T. Okada, E. Sahai, and M. Matsuda, “In vivo fluorescence resonance energy transfer imaging reveals differential activation of Rho-family GTPases in glioblastoma cell invasion,” J. Cell Sci. 125(4), 858–868 (2012).
[Crossref]

2011 (1)

F. Fereidouni, A. Esposito, G. A. Blab, and H. C. Gerritsen, “A modified phasor approach for analyzing time-gated fluorescence lifetime images,” J. Microsc. 244(3), 248–258 (2011).
[Crossref]

2010 (3)

M. Gersbach, R. Trimananda, Y. Maruyama, M. Fishburn, D. Stoppa, J. Richardson, R. Walker, R. K. Henderson, and E. Charbon, “High frame-rate TCSPC-FLIM using a novel SPAD-based image sensor,” P. Soc. Photo. Opt. Ins. 7780, 77801H (2010).
[Crossref]

F. Guerrieri, S. Tisa, A. Tosi, and F. Zappa, “Two-Dimensional SPAD Imaging Camera for Photon Counting,” IEEE Photonics J. 2(5), 759–774 (2010).
[Crossref]

M. Y. Berezin and S. Achilefu, “Fluorescence lifetime measurements and biological imaging,” Chem. Rev. 110(5), 2641–2684 (2010).
[Crossref]

2009 (1)

A. D. Elder, A. Domin, G. S. Kaminski Schierle, C. Lindon, J. Pines, A. Esposito, and C. F. Kaminski, “A quantitative protocol for dynamic measurements of protein interactions by Förster resonance energy transfer-sensitized fluorescence emission,” J. R. Soc. Interface 6(suppl_1), S59–S81 (2009).
[Crossref]

2008 (4)

J. Wlodarczyk, A. Woehler, F. Kobe, E. Ponimaskin, A. Zeug, and E. Neher, “Analysis of FRET signals in the presence of free donors and acceptors,” Biophys. J. 94(3), 986–1000 (2008).
[Crossref]

A. D. Elder, S. Schlachter, and C. F. Kaminski, “Theoretical investigation of the photon efficiency in Frequency-domain FLIM,” J. Opt. Soc. Am. A 25(2), 452–462 (2008).
[Crossref]

M. Digman, V. R. Caiolfa, M. Zamai, and E. Gratton, “The phasor approach to fluorescence lifetime imaging analysis,” Biophys. J. 94(2), L14–16 (2008).
[Crossref]

R. A. Colyer, C. Lee, and E. Gratton, “A novel fluorescence lifetime imaging system that optimizes photon efficiency,” Microsc. Res. Tech. 71(3), 201–213 (2008).
[Crossref]

2007 (2)

A. Esposito, H. C. Gerritsen, and F. S. Wouters, “Optimizing frequency-domain fluorescence lifetime sensing for high-throughput applications: photon economy and acquisition speed,” J. Opt. Soc. Am. A 24(10), 3261–3273 (2007).
[Crossref]

A. I. Iliev and F. S. Wouters, “Application of simple photobleaching microscopy techniques for the determination of the balance between anterograde and retrograde axonal transport,” J. Neurosci. Methods 161(1), 39–46 (2007).
[Crossref]

2006 (5)

S. Pelet, M. J. Previte, D. Kim, K. H. Kim, T. T. Su, and P. T. So, “Frequency domain lifetime and spectral imaging microscopy,” Microsc. Res. Tech. 69(11), 861–874 (2006).
[Crossref]

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]

S. Pelet, M. J. 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]

S. Ganesan, S. M. Ameer beg, T. Ng, B. Vojnovic, and F. S. Wouters, “A YFP-based Resonance Energy Accepting Chromoprotein (REACh) for efficient FRET with GFP,” Proc. Natl. Acad. Sci. U. S. A. 103(11), 4089–4094 (2006).
[Crossref]

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]

2005 (2)

Q. S. Hanley and A. H. Clayton, “AB-plot assisted determination of fluorophore mixtures in a fluorescence lifetime microscope using spectra or quenchers,” J. Microsc. 218(1), 62–67 (2005).
[Crossref]

A. Esposito, T. Oggier, H. C. Gerritsen, F. Lustenberger, and F. S. Wouters, “All-solid-state lock-in imaging for wide-field fluorescence lifetime sensing,” Opt. Express 13(24), 9812–9821 (2005).
[Crossref]

2004 (3)

G. Bunt and F. S. Wouters, “Visualization of molecular activities inside living cells with fluorescent labels,” Int. Rev. Cytol. 237, 205–277 (2004).
[Crossref]

L. P. Watkins and H. Yang, “Information bounds and optimal analysis of dynamic single molecule measurements,” Biophys. J. 86(6), 4015–4029 (2004).
[Crossref]

R. A. Neher and E. Neher, “Applying spectral fingerprinting to the analysis of FRET images,” Microsc. Res. Tech. 64(2), 185–195 (2004).
[Crossref]

2003 (5)

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]

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

C. Berney and G. Danuser, “FRET or no FRET: A quantitative comparison,” Biophys. J. 84(6), 3992–4010 (2003).
[Crossref]

M. Elangovan, H. Wallrabe, Y. Chen, R. N. Day, M. Barroso, and A. Periasamy, “Characterization of one- and two-photon excitation fluorescence resonance energy transfer microscopy,” Methods 29(1), 58–73 (2003).
[Crossref]

J. Philip and K. Carlsson, “Theoretical investigation of the signal-to-noise ratio in fluorescence lifetime imaging,” J. Opt. Soc. Am. A 20(2), 368–379 (2003).
[Crossref]

2002 (3)

A. Hoppe, K. Christensen, and J. A. Swanson, “Fluorescence resonance energy transfer-based stoichiometry in living cells,” Biophys. J. 83(6), 3652–3664 (2002).
[Crossref]

H. C. Gerritsen, M. A. Asselbergs, A. V. Agronskaia, and W. G. Van Sark, “Fluorescence lifetime imaging in scanning microscopes: acquisition speed, photon economy and lifetime resolution,” J. Microsc. 206(3), 218–224 (2002).
[Crossref]

K. Carlsson and J. P. Philip, “Theoretical Investigation of the Signal-To-Noise ratio for different fluorescence lifetime imaging techniques,” Proc. SPIE 4622, 70–74 (2002).
[Crossref]

1998 (1)

G. W. Gordon, G. Berry, X. H. Liang, B. Levine, and B. Herman, “Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy,” Biophys. J. 74(5), 2702–2713 (1998).
[Crossref]

1996 (1)

S. Tyagi and F. R. Kramer, “Molecular beacons: Probes that fluoresce upon hybridization,” Nat. Biotechnol. 14(3), 303–308 (1996).
[Crossref]

1994 (1)

T. W. Gadella, R. M. Clegg, and T. M. Jovin, “Fluorescence lifetime imaging microscopy: pixel-by-pixel analysis of phase-modulation data,” Bioimaging 2(3), 139–159 (1994).
[Crossref]

1992 (1)

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

1991 (2)

Ž. Bajzer, T. M. Therneau, J. C. Sharp, and F. G. Prendergast, “Maximum likelihood method for the analysis of time-resolved fluorescence decay curves,” Eur. Biophys. J. 20(5), 247–262 (1991).
[Crossref]

R. M. Ballew and J. N. Demas, “Error Analysis of the Rapid Lifetime Determination Method for Single Exponential Decays with A Nonzero Base-Line,” Anal. Chim. Acta 245, 121–127 (1991).
[Crossref]

1989 (1)

R. M. Ballew and J. N. Demas, “An Error Analysis of the Rapid Lifetime Determination Method for the Evaluation of Single Exponential Decays,” Anal. Chem. 61(1), 30–33 (1989).
[Crossref]

1984 (1)

H. P. Good, A. J. Kallir, and U. P. Wild, “Comparison of fluorescent lifetime fitting techniques,” J. Phys. Chem. 88(22), 5435–5441 (1984).
[Crossref]

1981 (1)

P. Hall and B. Selinger, “Better estimates of exponential decay parameters,” J. Phys. Chem. 85(20), 2941–2946 (1981).
[Crossref]

1967 (1)

L. Stryer and R. P. Haugland, “Energy Transfer - A Spectroscopic Ruler,” Proc. Natl. Acad. Sci. U. S. A. 58(2), 719–726 (1967).
[Crossref]

1948 (1)

T. Förster, “Zwischenmolekulare Energiewanderung und Fluoreszenz,” Ann. Phys. 437(1-2), 55–75 (1948).
[Crossref]

Achilefu, S.

M. Y. Berezin and S. Achilefu, “Fluorescence lifetime measurements and biological imaging,” Chem. Rev. 110(5), 2641–2684 (2010).
[Crossref]

Agronskaia, A. V.

H. C. Gerritsen, M. A. Asselbergs, A. V. Agronskaia, and W. G. Van Sark, “Fluorescence lifetime imaging in scanning microscopes: acquisition speed, photon economy and lifetime resolution,” J. Microsc. 206(3), 218–224 (2002).
[Crossref]

H. C. Gerritsen, A. V. Agronskaia, A. N. Bader, and A. Esposito, “Time Domain FLIM: theory, Instrumentation and data analysis,” in FRET & FLIM Imaging Techniques, T. W. Gadella, ed. (Elsevier, 2009).

Ameer beg, S. M.

S. Ganesan, S. M. Ameer beg, T. Ng, B. Vojnovic, and F. S. Wouters, “A YFP-based Resonance Energy Accepting Chromoprotein (REACh) for efficient FRET with GFP,” Proc. Natl. Acad. Sci. U. S. A. 103(11), 4089–4094 (2006).
[Crossref]

Ameer-Beg, S.

Anderson, K. I.

K. J. Martin, E. J. McGhee, J. P. Schwarz, M. Drysdale, S. M. Brachmann, V. Stucke, O. J. Sansom, and K. I. Anderson, “Accepting from the best donor; analysis of long-lifetime donor fluorescent protein pairings to optimise dynamic FLIM-based FRET experiments,” PLoS One 13(1), e0183585 (2018).
[Crossref]

Antolovic, I. M.

Arakawa, Y.

E. Hirata, H. Yukinaga, Y. Kamioka, Y. Arakawa, S. Miyamoto, T. Okada, E. Sahai, and M. Matsuda, “In vivo fluorescence resonance energy transfer imaging reveals differential activation of Rho-family GTPases in glioblastoma cell invasion,” J. Cell Sci. 125(4), 858–868 (2012).
[Crossref]

Asselbergs, M. A.

H. C. Gerritsen, M. A. Asselbergs, A. V. Agronskaia, and W. G. Van Sark, “Fluorescence lifetime imaging in scanning microscopes: acquisition speed, photon economy and lifetime resolution,” J. Microsc. 206(3), 218–224 (2002).
[Crossref]

Bader, A. N.

F. Fereidouni, A. N. Bader, and H. C. Gerritsen, “Spectral phasor analysis allows rapid and reliable unmixing of fluorescence microscopy spectral images,” Opt. Express 20(12), 12729–12741 (2012).
[Crossref]

H. C. Gerritsen, A. V. Agronskaia, A. N. Bader, and A. Esposito, “Time Domain FLIM: theory, Instrumentation and data analysis,” in FRET & FLIM Imaging Techniques, T. W. Gadella, ed. (Elsevier, 2009).

Baird, M. A.

A. D. Elliott, N. Bedard, A. Ustione, M. A. Baird, M. W. Davidson, T. Tkaczyk, and D. W. Piston, “Hyperspectral imaging for simultaneous measurements of two FRET biosensors in pancreatic beta-cells,” PLoS One 12(12), e0188789 (2017).
[Crossref]

Bajar, B. T.

B. T. Bajar, E. S. Wang, S. Zhang, M. Z. Lin, and J. Chu, “A Guide to Fluorescent Protein FRET Pairs,” Sensors 16(9), 1488 (2016).
[Crossref]

Bajzer, Ž.

Ž. Bajzer, T. M. Therneau, J. C. Sharp, and F. G. Prendergast, “Maximum likelihood method for the analysis of time-resolved fluorescence decay curves,” Eur. Biophys. J. 20(5), 247–262 (1991).
[Crossref]

Ballew, R. M.

R. M. Ballew and J. N. Demas, “Error Analysis of the Rapid Lifetime Determination Method for Single Exponential Decays with A Nonzero Base-Line,” Anal. Chim. Acta 245, 121–127 (1991).
[Crossref]

R. M. Ballew and J. N. Demas, “An Error Analysis of the Rapid Lifetime Determination Method for the Evaluation of Single Exponential Decays,” Anal. Chem. 61(1), 30–33 (1989).
[Crossref]

Barroso, M.

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]

M. Elangovan, H. Wallrabe, Y. Chen, R. N. Day, M. Barroso, and A. Periasamy, “Characterization of one- and two-photon excitation fluorescence resonance energy transfer microscopy,” Methods 29(1), 58–73 (2003).
[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).
[Crossref]

Bedard, N.

A. D. Elliott, N. Bedard, A. Ustione, M. A. Baird, M. W. Davidson, T. Tkaczyk, and D. W. Piston, “Hyperspectral imaging for simultaneous measurements of two FRET biosensors in pancreatic beta-cells,” PLoS One 12(12), e0188789 (2017).
[Crossref]

Ber, S.

A. L. Trinh, S. Ber, A. Howitt, P. O. Valls, M. W. Fries, A. R. Venkitaraman, and A. Esposito, “Fast single-cell biochemistry: theory, open source microscopy and applications,” Methods Appl. Fluoresc. 7(4), 044001 (2019).
[Crossref]

M. W. Fries, K. T. Haas, S. Ber, J. Saganty, E. K. Richardson, A. R. Venkitaraman, and A. Esposito, “Multiplexed biochemical imaging reveals caspase activation patterns underlying single cell fate,” bioRxiv, 427237 (2018).

Berezin, M. Y.

M. Y. Berezin and S. Achilefu, “Fluorescence lifetime measurements and biological imaging,” Chem. Rev. 110(5), 2641–2684 (2010).
[Crossref]

Berney, C.

C. Berney and G. Danuser, “FRET or no FRET: A quantitative comparison,” Biophys. J. 84(6), 3992–4010 (2003).
[Crossref]

Berry, G.

G. W. Gordon, G. Berry, X. H. Liang, B. Levine, and B. Herman, “Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy,” Biophys. J. 74(5), 2702–2713 (1998).
[Crossref]

Blab, G. A.

F. Fereidouni, A. Esposito, G. A. Blab, and H. C. Gerritsen, “A modified phasor approach for analyzing time-gated fluorescence lifetime images,” J. Microsc. 244(3), 248–258 (2011).
[Crossref]

Bonifacino, J. S.

A. Esposito, F. S. Wouters, J. S. Bonifacino, M. Dasso, J. B. Harford, J. Lippincott-Schwartz, and K. M. Yamada, “Fluorescence Lifetime Imaging Microscopy,” in Current Protocols in Cell Biology (Wiley, 2004).

Bouchet, D.

Brachmann, S. M.

K. J. Martin, E. J. McGhee, J. P. Schwarz, M. Drysdale, S. M. Brachmann, V. Stucke, O. J. Sansom, and K. I. Anderson, “Accepting from the best donor; analysis of long-lifetime donor fluorescent protein pairings to optimise dynamic FLIM-based FRET experiments,” PLoS One 13(1), e0183585 (2018).
[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]

Bruschini, C.

Bunt, G.

G. Bunt and F. S. Wouters, “Visualization of molecular activities inside living cells with fluorescent labels,” Int. Rev. Cytol. 237, 205–277 (2004).
[Crossref]

Caiolfa, V. R.

M. Digman, V. R. Caiolfa, M. Zamai, and E. Gratton, “The phasor approach to fluorescence lifetime imaging analysis,” Biophys. J. 94(2), L14–16 (2008).
[Crossref]

Carlsson, K.

J. Philip and K. Carlsson, “Theoretical investigation of the signal-to-noise ratio in fluorescence lifetime imaging,” J. Opt. Soc. Am. A 20(2), 368–379 (2003).
[Crossref]

K. Carlsson and J. P. Philip, “Theoretical Investigation of the Signal-To-Noise ratio for different fluorescence lifetime imaging techniques,” Proc. SPIE 4622, 70–74 (2002).
[Crossref]

Cassidy, L. D.

Chapuis, C.

C. Demeautis, F. Sipieter, J. Roul, C. Chapuis, S. Padilla-Parra, F. B. Riquet, and M. Tramier, “Multiplexing PKA and ERK1&2 kinases FRET biosensors in living cells using single excitation wavelength dual colour FLIM,” Sci. Rep. 7(1), 41026 (2017).
[Crossref]

Charbon, E.

I. M. Antolovic, C. Bruschini, and E. Charbon, “Dynamic range extension for photon counting arrays,” Opt. Express 26(17), 22234–22248 (2018).
[Crossref]

M. Gersbach, R. Trimananda, Y. Maruyama, M. Fishburn, D. Stoppa, J. Richardson, R. Walker, R. K. Henderson, and E. Charbon, “High frame-rate TCSPC-FLIM using a novel SPAD-based image sensor,” P. Soc. Photo. Opt. Ins. 7780, 77801H (2010).
[Crossref]

Chen, Y.

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]

M. Elangovan, H. Wallrabe, Y. Chen, R. N. Day, M. Barroso, and A. Periasamy, “Characterization of one- and two-photon excitation fluorescence resonance energy transfer microscopy,” Methods 29(1), 58–73 (2003).
[Crossref]

Chizhik, A.

Christensen, K.

A. Hoppe, K. Christensen, and J. A. Swanson, “Fluorescence resonance energy transfer-based stoichiometry in living cells,” Biophys. J. 83(6), 3652–3664 (2002).
[Crossref]

Chu, J.

B. T. Bajar, E. S. Wang, S. Zhang, M. Z. Lin, and J. Chu, “A Guide to Fluorescent Protein FRET Pairs,” Sensors 16(9), 1488 (2016).
[Crossref]

Clayton, A. H.

Q. S. Hanley and A. H. Clayton, “AB-plot assisted determination of fluorophore mixtures in a fluorescence lifetime microscope using spectra or quenchers,” J. Microsc. 218(1), 62–67 (2005).
[Crossref]

Clegg, R. M.

T. W. Gadella, R. M. Clegg, and T. M. Jovin, “Fluorescence lifetime imaging microscopy: pixel-by-pixel analysis of phase-modulation data,” Bioimaging 2(3), 139–159 (1994).
[Crossref]

Colyer, R. A.

R. A. Colyer, C. Lee, and E. Gratton, “A novel fluorescence lifetime imaging system that optimizes photon efficiency,” Microsc. Res. Tech. 71(3), 201–213 (2008).
[Crossref]

Conway, J. R. W.

J. R. W. Conway, S. C. Warren, and P. Timpson, “Context-dependent intravital imaging of therapeutic response using intramolecular FRET biosensors,” Methods 128, 78–94 (2017).
[Crossref]

Danuser, G.

C. Berney and G. Danuser, “FRET or no FRET: A quantitative comparison,” Biophys. J. 84(6), 3992–4010 (2003).
[Crossref]

Dasso, M.

A. Esposito, F. S. Wouters, J. S. Bonifacino, M. Dasso, J. B. Harford, J. Lippincott-Schwartz, and K. M. Yamada, “Fluorescence Lifetime Imaging Microscopy,” in Current Protocols in Cell Biology (Wiley, 2004).

Davidson, M. W.

A. D. Elliott, N. Bedard, A. Ustione, M. A. Baird, M. W. Davidson, T. Tkaczyk, and D. W. Piston, “Hyperspectral imaging for simultaneous measurements of two FRET biosensors in pancreatic beta-cells,” PLoS One 12(12), e0188789 (2017).
[Crossref]

Day, R. N.

M. Elangovan, H. Wallrabe, Y. Chen, R. N. Day, M. Barroso, and A. Periasamy, “Characterization of one- and two-photon excitation fluorescence resonance energy transfer microscopy,” Methods 29(1), 58–73 (2003).
[Crossref]

de Jong, S.

M. Raspe, K. M. Kedziora, B. van den Broek, Q. Zhao, S. de Jong, J. Herz, M. Mastop, J. Goedhart, T. W. Gadella, I. T. Young, and K. Jalink, “siFLIM: single-image frequency-domain FLIM provides fast and photon-efficient lifetime data,” Nat. Methods 13(6), 501–504 (2016).
[Crossref]

Demas, J. N.

R. M. Ballew and J. N. Demas, “Error Analysis of the Rapid Lifetime Determination Method for Single Exponential Decays with A Nonzero Base-Line,” Anal. Chim. Acta 245, 121–127 (1991).
[Crossref]

R. M. Ballew and J. N. Demas, “An Error Analysis of the Rapid Lifetime Determination Method for the Evaluation of Single Exponential Decays,” Anal. Chem. 61(1), 30–33 (1989).
[Crossref]

Demeautis, C.

C. Demeautis, F. Sipieter, J. Roul, C. Chapuis, S. Padilla-Parra, F. B. Riquet, and M. Tramier, “Multiplexing PKA and ERK1&2 kinases FRET biosensors in living cells using single excitation wavelength dual colour FLIM,” Sci. Rep. 7(1), 41026 (2017).
[Crossref]

Digman, M.

M. Digman, V. R. Caiolfa, M. Zamai, and E. Gratton, “The phasor approach to fluorescence lifetime imaging analysis,” Biophys. J. 94(2), L14–16 (2008).
[Crossref]

Domin, A.

A. D. Elder, A. Domin, G. S. Kaminski Schierle, C. Lindon, J. Pines, A. Esposito, and C. F. Kaminski, “A quantitative protocol for dynamic measurements of protein interactions by Förster resonance energy transfer-sensitized fluorescence emission,” J. R. Soc. Interface 6(suppl_1), S59–S81 (2009).
[Crossref]

Drysdale, M.

K. J. Martin, E. J. McGhee, J. P. Schwarz, M. Drysdale, S. M. Brachmann, V. Stucke, O. J. Sansom, and K. I. Anderson, “Accepting from the best donor; analysis of long-lifetime donor fluorescent protein pairings to optimise dynamic FLIM-based FRET experiments,” PLoS One 13(1), e0183585 (2018).
[Crossref]

Elangovan, M.

M. Elangovan, H. Wallrabe, Y. Chen, R. N. Day, M. Barroso, and A. Periasamy, “Characterization of one- and two-photon excitation fluorescence resonance energy transfer microscopy,” Methods 29(1), 58–73 (2003).
[Crossref]

Elder, A. D.

A. D. Elder, A. Domin, G. S. Kaminski Schierle, C. Lindon, J. Pines, A. Esposito, and C. F. Kaminski, “A quantitative protocol for dynamic measurements of protein interactions by Förster resonance energy transfer-sensitized fluorescence emission,” J. R. Soc. Interface 6(suppl_1), S59–S81 (2009).
[Crossref]

A. D. Elder, S. Schlachter, and C. F. Kaminski, “Theoretical investigation of the photon efficiency in Frequency-domain FLIM,” J. Opt. Soc. Am. A 25(2), 452–462 (2008).
[Crossref]

Elliott, A. D.

A. D. Elliott, N. Bedard, A. Ustione, M. A. Baird, M. W. Davidson, T. Tkaczyk, and D. W. Piston, “Hyperspectral imaging for simultaneous measurements of two FRET biosensors in pancreatic beta-cells,” PLoS One 12(12), e0188789 (2017).
[Crossref]

Enderlein, J.

Esposito, A.

A. L. Trinh, S. Ber, A. Howitt, P. O. Valls, M. W. Fries, A. R. Venkitaraman, and A. Esposito, “Fast single-cell biochemistry: theory, open source microscopy and applications,” Methods Appl. Fluoresc. 7(4), 044001 (2019).
[Crossref]

M. Popleteeva, K. T. Haas, D. Stoppa, L. Pancheri, L. Gasparini, C. F. Kaminski, L. D. Cassidy, A. R. Venkitaraman, and A. Esposito, “Fast and simple spectral FLIM for biochemical and medical imaging,” Opt. Express 23(18), 23511–23525 (2015).
[Crossref]

A. Esposito, M. Popleteeva, and A. R. Venkitaraman, “Maximizing the biochemical resolving power of fluorescence microscopy,” PLoS One 8(10), e77392 (2013).
[Crossref]

F. Fereidouni, A. Esposito, G. A. Blab, and H. C. Gerritsen, “A modified phasor approach for analyzing time-gated fluorescence lifetime images,” J. Microsc. 244(3), 248–258 (2011).
[Crossref]

A. D. Elder, A. Domin, G. S. Kaminski Schierle, C. Lindon, J. Pines, A. Esposito, and C. F. Kaminski, “A quantitative protocol for dynamic measurements of protein interactions by Förster resonance energy transfer-sensitized fluorescence emission,” J. R. Soc. Interface 6(suppl_1), S59–S81 (2009).
[Crossref]

A. Esposito, H. C. Gerritsen, and F. S. Wouters, “Optimizing frequency-domain fluorescence lifetime sensing for high-throughput applications: photon economy and acquisition speed,” J. Opt. Soc. Am. A 24(10), 3261–3273 (2007).
[Crossref]

A. Esposito, T. Oggier, H. C. Gerritsen, F. Lustenberger, and F. S. Wouters, “All-solid-state lock-in imaging for wide-field fluorescence lifetime sensing,” Opt. Express 13(24), 9812–9821 (2005).
[Crossref]

A. Esposito, H. C. Gerritsen, F. S. Wouters, and U. Resch-Genger, “Fluorescence lifetime imaging microscopy: quality assessment and standards,” in Standardization in Fluorometry: State of the Art and Future Challenges, O. S. Wolfbeis, ed. (Springer, 2007).

M. W. Fries, K. T. Haas, S. Ber, J. Saganty, E. K. Richardson, A. R. Venkitaraman, and A. Esposito, “Multiplexed biochemical imaging reveals caspase activation patterns underlying single cell fate,” bioRxiv, 427237 (2018).

A. Esposito, “Fisher Information and FRET” (2020), retrieved https://github.com/alesposito/FisherInformation

H. C. Gerritsen, A. V. Agronskaia, A. N. Bader, and A. Esposito, “Time Domain FLIM: theory, Instrumentation and data analysis,” in FRET & FLIM Imaging Techniques, T. W. Gadella, ed. (Elsevier, 2009).

A. Esposito, F. S. Wouters, J. S. Bonifacino, M. Dasso, J. B. Harford, J. Lippincott-Schwartz, and K. M. Yamada, “Fluorescence Lifetime Imaging Microscopy,” in Current Protocols in Cell Biology (Wiley, 2004).

Fereidouni, F.

F. Fereidouni, A. N. Bader, and H. C. Gerritsen, “Spectral phasor analysis allows rapid and reliable unmixing of fluorescence microscopy spectral images,” Opt. Express 20(12), 12729–12741 (2012).
[Crossref]

F. Fereidouni, A. Esposito, G. A. Blab, and H. C. Gerritsen, “A modified phasor approach for analyzing time-gated fluorescence lifetime images,” J. Microsc. 244(3), 248–258 (2011).
[Crossref]

Fishburn, M.

M. Gersbach, R. Trimananda, Y. Maruyama, M. Fishburn, D. Stoppa, J. Richardson, R. Walker, R. K. Henderson, and E. Charbon, “High frame-rate TCSPC-FLIM using a novel SPAD-based image sensor,” P. Soc. Photo. Opt. Ins. 7780, 77801H (2010).
[Crossref]

Förster, T.

T. Förster, “Zwischenmolekulare Energiewanderung und Fluoreszenz,” Ann. Phys. 437(1-2), 55–75 (1948).
[Crossref]

Fries, M. W.

A. L. Trinh, S. Ber, A. Howitt, P. O. Valls, M. W. Fries, A. R. Venkitaraman, and A. Esposito, “Fast single-cell biochemistry: theory, open source microscopy and applications,” Methods Appl. Fluoresc. 7(4), 044001 (2019).
[Crossref]

M. W. Fries, K. T. Haas, S. Ber, J. Saganty, E. K. Richardson, A. R. Venkitaraman, and A. Esposito, “Multiplexed biochemical imaging reveals caspase activation patterns underlying single cell fate,” bioRxiv, 427237 (2018).

Gadella, T. W.

M. Raspe, K. M. Kedziora, B. van den Broek, Q. Zhao, S. de Jong, J. Herz, M. Mastop, J. Goedhart, T. W. Gadella, I. T. Young, and K. Jalink, “siFLIM: single-image frequency-domain FLIM provides fast and photon-efficient lifetime data,” Nat. Methods 13(6), 501–504 (2016).
[Crossref]

T. W. Gadella, R. M. Clegg, and T. M. Jovin, “Fluorescence lifetime imaging microscopy: pixel-by-pixel analysis of phase-modulation data,” Bioimaging 2(3), 139–159 (1994).
[Crossref]

Ganesan, S.

S. Ganesan, S. M. Ameer beg, T. Ng, B. Vojnovic, and F. S. Wouters, “A YFP-based Resonance Energy Accepting Chromoprotein (REACh) for efficient FRET with GFP,” Proc. Natl. Acad. Sci. U. S. A. 103(11), 4089–4094 (2006).
[Crossref]

Gasparini, L.

Gerritsen, H. C.

F. Fereidouni, A. N. Bader, and H. C. Gerritsen, “Spectral phasor analysis allows rapid and reliable unmixing of fluorescence microscopy spectral images,” Opt. Express 20(12), 12729–12741 (2012).
[Crossref]

F. Fereidouni, A. Esposito, G. A. Blab, and H. C. Gerritsen, “A modified phasor approach for analyzing time-gated fluorescence lifetime images,” J. Microsc. 244(3), 248–258 (2011).
[Crossref]

A. Esposito, H. C. Gerritsen, and F. S. Wouters, “Optimizing frequency-domain fluorescence lifetime sensing for high-throughput applications: photon economy and acquisition speed,” J. Opt. Soc. Am. A 24(10), 3261–3273 (2007).
[Crossref]

A. Esposito, T. Oggier, H. C. Gerritsen, F. Lustenberger, and F. S. Wouters, “All-solid-state lock-in imaging for wide-field fluorescence lifetime sensing,” Opt. Express 13(24), 9812–9821 (2005).
[Crossref]

H. C. Gerritsen, M. A. Asselbergs, A. V. Agronskaia, and W. G. Van Sark, “Fluorescence lifetime imaging in scanning microscopes: acquisition speed, photon economy and lifetime resolution,” J. Microsc. 206(3), 218–224 (2002).
[Crossref]

H. C. Gerritsen, A. V. Agronskaia, A. N. Bader, and A. Esposito, “Time Domain FLIM: theory, Instrumentation and data analysis,” in FRET & FLIM Imaging Techniques, T. W. Gadella, ed. (Elsevier, 2009).

A. Esposito, H. C. Gerritsen, F. S. Wouters, and U. Resch-Genger, “Fluorescence lifetime imaging microscopy: quality assessment and standards,” in Standardization in Fluorometry: State of the Art and Future Challenges, O. S. Wolfbeis, ed. (Springer, 2007).

Gersbach, M.

M. Gersbach, R. Trimananda, Y. Maruyama, M. Fishburn, D. Stoppa, J. Richardson, R. Walker, R. K. Henderson, and E. Charbon, “High frame-rate TCSPC-FLIM using a novel SPAD-based image sensor,” P. Soc. Photo. Opt. Ins. 7780, 77801H (2010).
[Crossref]

Goedhart, J.

M. Raspe, K. M. Kedziora, B. van den Broek, Q. Zhao, S. de Jong, J. Herz, M. Mastop, J. Goedhart, T. W. Gadella, I. T. Young, and K. Jalink, “siFLIM: single-image frequency-domain FLIM provides fast and photon-efficient lifetime data,” Nat. Methods 13(6), 501–504 (2016).
[Crossref]

J. Klarenbeek, J. Goedhart, A. van Batenburg, D. Groenewald, and K. Jalink, “Fourth-generation epac-based FRET sensors for cAMP feature exceptional brightness, photostability and dynamic range: characterization of dedicated sensors for FLIM, for ratiometry and with high affinity,” PLoS One 10(4), e0122513 (2015).
[Crossref]

Good, H. P.

H. P. Good, A. J. Kallir, and U. P. Wild, “Comparison of fluorescent lifetime fitting techniques,” J. Phys. Chem. 88(22), 5435–5441 (1984).
[Crossref]

Gordon, G. W.

G. W. Gordon, G. Berry, X. H. Liang, B. Levine, and B. Herman, “Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy,” Biophys. J. 74(5), 2702–2713 (1998).
[Crossref]

Gratton, E.

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[Crossref]

Timpson, P.

J. R. W. Conway, S. C. Warren, and P. Timpson, “Context-dependent intravital imaging of therapeutic response using intramolecular FRET biosensors,” Methods 128, 78–94 (2017).
[Crossref]

Tisa, S.

F. Guerrieri, S. Tisa, A. Tosi, and F. Zappa, “Two-Dimensional SPAD Imaging Camera for Photon Counting,” IEEE Photonics J. 2(5), 759–774 (2010).
[Crossref]

Tkaczyk, T.

A. D. Elliott, N. Bedard, A. Ustione, M. A. Baird, M. W. Davidson, T. Tkaczyk, and D. W. Piston, “Hyperspectral imaging for simultaneous measurements of two FRET biosensors in pancreatic beta-cells,” PLoS One 12(12), e0188789 (2017).
[Crossref]

Tosi, A.

F. Guerrieri, S. Tisa, A. Tosi, and F. Zappa, “Two-Dimensional SPAD Imaging Camera for Photon Counting,” IEEE Photonics J. 2(5), 759–774 (2010).
[Crossref]

Tramier, M.

C. Demeautis, F. Sipieter, J. Roul, C. Chapuis, S. Padilla-Parra, F. B. Riquet, and M. Tramier, “Multiplexing PKA and ERK1&2 kinases FRET biosensors in living cells using single excitation wavelength dual colour FLIM,” Sci. Rep. 7(1), 41026 (2017).
[Crossref]

Trimananda, R.

M. Gersbach, R. Trimananda, Y. Maruyama, M. Fishburn, D. Stoppa, J. Richardson, R. Walker, R. K. Henderson, and E. Charbon, “High frame-rate TCSPC-FLIM using a novel SPAD-based image sensor,” P. Soc. Photo. Opt. Ins. 7780, 77801H (2010).
[Crossref]

Trinh, A. L.

A. L. Trinh, S. Ber, A. Howitt, P. O. Valls, M. W. Fries, A. R. Venkitaraman, and A. Esposito, “Fast single-cell biochemistry: theory, open source microscopy and applications,” Methods Appl. Fluoresc. 7(4), 044001 (2019).
[Crossref]

Tyagi, S.

S. Tyagi and F. R. Kramer, “Molecular beacons: Probes that fluoresce upon hybridization,” Nat. Biotechnol. 14(3), 303–308 (1996).
[Crossref]

Ustione, A.

A. D. Elliott, N. Bedard, A. Ustione, M. A. Baird, M. W. Davidson, T. Tkaczyk, and D. W. Piston, “Hyperspectral imaging for simultaneous measurements of two FRET biosensors in pancreatic beta-cells,” PLoS One 12(12), e0188789 (2017).
[Crossref]

Valls, P. O.

A. L. Trinh, S. Ber, A. Howitt, P. O. Valls, M. W. Fries, A. R. Venkitaraman, and A. Esposito, “Fast single-cell biochemistry: theory, open source microscopy and applications,” Methods Appl. Fluoresc. 7(4), 044001 (2019).
[Crossref]

van Batenburg, A.

J. Klarenbeek, J. Goedhart, A. van Batenburg, D. Groenewald, and K. Jalink, “Fourth-generation epac-based FRET sensors for cAMP feature exceptional brightness, photostability and dynamic range: characterization of dedicated sensors for FLIM, for ratiometry and with high affinity,” PLoS One 10(4), e0122513 (2015).
[Crossref]

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M. Raspe, K. M. Kedziora, B. van den Broek, Q. Zhao, S. de Jong, J. Herz, M. Mastop, J. Goedhart, T. W. Gadella, I. T. Young, and K. Jalink, “siFLIM: single-image frequency-domain FLIM provides fast and photon-efficient lifetime data,” Nat. Methods 13(6), 501–504 (2016).
[Crossref]

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H. C. Gerritsen, M. A. Asselbergs, A. V. Agronskaia, and W. G. Van Sark, “Fluorescence lifetime imaging in scanning microscopes: acquisition speed, photon economy and lifetime resolution,” J. Microsc. 206(3), 218–224 (2002).
[Crossref]

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A. L. Trinh, S. Ber, A. Howitt, P. O. Valls, M. W. Fries, A. R. Venkitaraman, and A. Esposito, “Fast single-cell biochemistry: theory, open source microscopy and applications,” Methods Appl. Fluoresc. 7(4), 044001 (2019).
[Crossref]

M. Popleteeva, K. T. Haas, D. Stoppa, L. Pancheri, L. Gasparini, C. F. Kaminski, L. D. Cassidy, A. R. Venkitaraman, and A. Esposito, “Fast and simple spectral FLIM for biochemical and medical imaging,” Opt. Express 23(18), 23511–23525 (2015).
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A. Esposito, M. Popleteeva, and A. R. Venkitaraman, “Maximizing the biochemical resolving power of fluorescence microscopy,” PLoS One 8(10), e77392 (2013).
[Crossref]

M. W. Fries, K. T. Haas, S. Ber, J. Saganty, E. K. Richardson, A. R. Venkitaraman, and A. Esposito, “Multiplexed biochemical imaging reveals caspase activation patterns underlying single cell fate,” bioRxiv, 427237 (2018).

Vojnovic, B.

S. Ganesan, S. M. Ameer beg, T. Ng, B. Vojnovic, and F. S. Wouters, “A YFP-based Resonance Energy Accepting Chromoprotein (REACh) for efficient FRET with GFP,” Proc. Natl. Acad. Sci. U. S. A. 103(11), 4089–4094 (2006).
[Crossref]

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M. Gersbach, R. Trimananda, Y. Maruyama, M. Fishburn, D. Stoppa, J. Richardson, R. Walker, R. K. Henderson, and E. Charbon, “High frame-rate TCSPC-FLIM using a novel SPAD-based image sensor,” P. Soc. Photo. Opt. Ins. 7780, 77801H (2010).
[Crossref]

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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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M. Elangovan, H. Wallrabe, Y. Chen, R. N. Day, M. Barroso, and A. Periasamy, “Characterization of one- and two-photon excitation fluorescence resonance energy transfer microscopy,” Methods 29(1), 58–73 (2003).
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B. T. Bajar, E. S. Wang, S. Zhang, M. Z. Lin, and J. Chu, “A Guide to Fluorescent Protein FRET Pairs,” Sensors 16(9), 1488 (2016).
[Crossref]

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J. R. W. Conway, S. C. Warren, and P. Timpson, “Context-dependent intravital imaging of therapeutic response using intramolecular FRET biosensors,” Methods 128, 78–94 (2017).
[Crossref]

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L. P. Watkins and H. Yang, “Information bounds and optimal analysis of dynamic single molecule measurements,” Biophys. J. 86(6), 4015–4029 (2004).
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H. P. Good, A. J. Kallir, and U. P. Wild, “Comparison of fluorescent lifetime fitting techniques,” J. Phys. Chem. 88(22), 5435–5441 (1984).
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J. Wlodarczyk, A. Woehler, F. Kobe, E. Ponimaskin, A. Zeug, and E. Neher, “Analysis of FRET signals in the presence of free donors and acceptors,” Biophys. J. 94(3), 986–1000 (2008).
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A. Zeug, A. Woehler, E. Neher, and E. G. Ponimaskin, “Quantitative intensity-based FRET approaches–a comparative snapshot,” Biophys. J. 103(9), 1821–1827 (2012).
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J. Wlodarczyk, A. Woehler, F. Kobe, E. Ponimaskin, A. Zeug, and E. Neher, “Analysis of FRET signals in the presence of free donors and acceptors,” Biophys. J. 94(3), 986–1000 (2008).
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A. Esposito, H. C. Gerritsen, and F. S. Wouters, “Optimizing frequency-domain fluorescence lifetime sensing for high-throughput applications: photon economy and acquisition speed,” J. Opt. Soc. Am. A 24(10), 3261–3273 (2007).
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A. I. Iliev and F. S. Wouters, “Application of simple photobleaching microscopy techniques for the determination of the balance between anterograde and retrograde axonal transport,” J. Neurosci. Methods 161(1), 39–46 (2007).
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S. Ganesan, S. M. Ameer beg, T. Ng, B. Vojnovic, and F. S. Wouters, “A YFP-based Resonance Energy Accepting Chromoprotein (REACh) for efficient FRET with GFP,” Proc. Natl. Acad. Sci. U. S. A. 103(11), 4089–4094 (2006).
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A. Esposito, T. Oggier, H. C. Gerritsen, F. Lustenberger, and F. S. Wouters, “All-solid-state lock-in imaging for wide-field fluorescence lifetime sensing,” Opt. Express 13(24), 9812–9821 (2005).
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G. Bunt and F. S. Wouters, “Visualization of molecular activities inside living cells with fluorescent labels,” Int. Rev. Cytol. 237, 205–277 (2004).
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A. Esposito, F. S. Wouters, J. S. Bonifacino, M. Dasso, J. B. Harford, J. Lippincott-Schwartz, and K. M. Yamada, “Fluorescence Lifetime Imaging Microscopy,” in Current Protocols in Cell Biology (Wiley, 2004).

A. Esposito, H. C. Gerritsen, F. S. Wouters, and U. Resch-Genger, “Fluorescence lifetime imaging microscopy: quality assessment and standards,” in Standardization in Fluorometry: State of the Art and Future Challenges, O. S. Wolfbeis, ed. (Springer, 2007).

Yamada, K. M.

A. Esposito, F. S. Wouters, J. S. Bonifacino, M. Dasso, J. B. Harford, J. Lippincott-Schwartz, and K. M. Yamada, “Fluorescence Lifetime Imaging Microscopy,” in Current Protocols in Cell Biology (Wiley, 2004).

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M. Raspe, K. M. Kedziora, B. van den Broek, Q. Zhao, S. de Jong, J. Herz, M. Mastop, J. Goedhart, T. W. Gadella, I. T. Young, and K. Jalink, “siFLIM: single-image frequency-domain FLIM provides fast and photon-efficient lifetime data,” Nat. Methods 13(6), 501–504 (2016).
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E. Hirata, H. Yukinaga, Y. Kamioka, Y. Arakawa, S. Miyamoto, T. Okada, E. Sahai, and M. Matsuda, “In vivo fluorescence resonance energy transfer imaging reveals differential activation of Rho-family GTPases in glioblastoma cell invasion,” J. Cell Sci. 125(4), 858–868 (2012).
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M. Digman, V. R. Caiolfa, M. Zamai, and E. Gratton, “The phasor approach to fluorescence lifetime imaging analysis,” Biophys. J. 94(2), L14–16 (2008).
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F. Guerrieri, S. Tisa, A. Tosi, and F. Zappa, “Two-Dimensional SPAD Imaging Camera for Photon Counting,” IEEE Photonics J. 2(5), 759–774 (2010).
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A. Zeug, A. Woehler, E. Neher, and E. G. Ponimaskin, “Quantitative intensity-based FRET approaches–a comparative snapshot,” Biophys. J. 103(9), 1821–1827 (2012).
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Q. Ni, S. Mehta, and J. Zhang, “Live-cell imaging of cell signaling using genetically encoded fluorescent reporters,” FEBS J. 285(2), 203–219 (2018).
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B. T. Bajar, E. S. Wang, S. Zhang, M. Z. Lin, and J. Chu, “A Guide to Fluorescent Protein FRET Pairs,” Sensors 16(9), 1488 (2016).
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M. Raspe, K. M. Kedziora, B. van den Broek, Q. Zhao, S. de Jong, J. Herz, M. Mastop, J. Goedhart, T. W. Gadella, I. T. Young, and K. Jalink, “siFLIM: single-image frequency-domain FLIM provides fast and photon-efficient lifetime data,” Nat. Methods 13(6), 501–504 (2016).
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M. Digman, V. R. Caiolfa, M. Zamai, and E. Gratton, “The phasor approach to fluorescence lifetime imaging analysis,” Biophys. J. 94(2), L14–16 (2008).
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Q. Ni, S. Mehta, and J. Zhang, “Live-cell imaging of cell signaling using genetically encoded fluorescent reporters,” FEBS J. 285(2), 203–219 (2018).
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F. Guerrieri, S. Tisa, A. Tosi, and F. Zappa, “Two-Dimensional SPAD Imaging Camera for Photon Counting,” IEEE Photonics J. 2(5), 759–774 (2010).
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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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H. C. Gerritsen, M. A. Asselbergs, A. V. Agronskaia, and W. G. Van Sark, “Fluorescence lifetime imaging in scanning microscopes: acquisition speed, photon economy and lifetime resolution,” J. Microsc. 206(3), 218–224 (2002).
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A. L. Trinh, S. Ber, A. Howitt, P. O. Valls, M. W. Fries, A. R. Venkitaraman, and A. Esposito, “Fast single-cell biochemistry: theory, open source microscopy and applications,” Methods Appl. Fluoresc. 7(4), 044001 (2019).
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M. Raspe, K. M. Kedziora, B. van den Broek, Q. Zhao, S. de Jong, J. Herz, M. Mastop, J. Goedhart, T. W. Gadella, I. T. Young, and K. Jalink, “siFLIM: single-image frequency-domain FLIM provides fast and photon-efficient lifetime data,” Nat. Methods 13(6), 501–504 (2016).
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M. Gersbach, R. Trimananda, Y. Maruyama, M. Fishburn, D. Stoppa, J. Richardson, R. Walker, R. K. Henderson, and E. Charbon, “High frame-rate TCSPC-FLIM using a novel SPAD-based image sensor,” P. Soc. Photo. Opt. Ins. 7780, 77801H (2010).
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A. Esposito, M. Popleteeva, and A. R. Venkitaraman, “Maximizing the biochemical resolving power of fluorescence microscopy,” PLoS One 8(10), e77392 (2013).
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J. Klarenbeek, J. Goedhart, A. van Batenburg, D. Groenewald, and K. Jalink, “Fourth-generation epac-based FRET sensors for cAMP feature exceptional brightness, photostability and dynamic range: characterization of dedicated sensors for FLIM, for ratiometry and with high affinity,” PLoS One 10(4), e0122513 (2015).
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A. D. Elliott, N. Bedard, A. Ustione, M. A. Baird, M. W. Davidson, T. Tkaczyk, and D. W. Piston, “Hyperspectral imaging for simultaneous measurements of two FRET biosensors in pancreatic beta-cells,” PLoS One 12(12), e0188789 (2017).
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S. Ganesan, S. M. Ameer beg, T. Ng, B. Vojnovic, and F. S. Wouters, “A YFP-based Resonance Energy Accepting Chromoprotein (REACh) for efficient FRET with GFP,” Proc. Natl. Acad. Sci. U. S. A. 103(11), 4089–4094 (2006).
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C. Demeautis, F. Sipieter, J. Roul, C. Chapuis, S. Padilla-Parra, F. B. Riquet, and M. Tramier, “Multiplexing PKA and ERK1&2 kinases FRET biosensors in living cells using single excitation wavelength dual colour FLIM,” Sci. Rep. 7(1), 41026 (2017).
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B. T. Bajar, E. S. Wang, S. Zhang, M. Z. Lin, and J. Chu, “A Guide to Fluorescent Protein FRET Pairs,” Sensors 16(9), 1488 (2016).
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A. Esposito, F. S. Wouters, J. S. Bonifacino, M. Dasso, J. B. Harford, J. Lippincott-Schwartz, and K. M. Yamada, “Fluorescence Lifetime Imaging Microscopy,” in Current Protocols in Cell Biology (Wiley, 2004).

H. C. Gerritsen, A. V. Agronskaia, A. N. Bader, and A. Esposito, “Time Domain FLIM: theory, Instrumentation and data analysis,” in FRET & FLIM Imaging Techniques, T. W. Gadella, ed. (Elsevier, 2009).

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M. W. Fries, K. T. Haas, S. Ber, J. Saganty, E. K. Richardson, A. R. Venkitaraman, and A. Esposito, “Multiplexed biochemical imaging reveals caspase activation patterns underlying single cell fate,” bioRxiv, 427237 (2018).

A. Esposito, H. C. Gerritsen, F. S. Wouters, and U. Resch-Genger, “Fluorescence lifetime imaging microscopy: quality assessment and standards,” in Standardization in Fluorometry: State of the Art and Future Challenges, O. S. Wolfbeis, ed. (Springer, 2007).

Supplementary Material (1)

NameDescription
» Code 1       Code to compute Fisher information and CRLB

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Figures (5)

Fig. 1.
Fig. 1. Quantification of FRET by FLIM and seFRET. Excitation light pumps a population of excited fluorophores, here represented as blue (donor) or yellow (acceptor) buckets. In an ideal system, the light source (blue tap) excites only the pool of donor fluorophores directly (a). Excitation energy then is either transferred non-radiatively to the acceptor or emitted as photons and collected by detectors, here represented by the bottom blue (IDD) and yellow (IDA) plates. The ratio of IDA and IDD can be used to estimate FRET. In practice, direct excitation of the acceptor (DE) and spectral bleed-through from donor to acceptor (SBT) contaminate the FRET signal. FLIM (b) avoids cross-talks between donor and acceptor by estimating the presence of FRET by the time a fluorophore spends in its excited state. Quantitative implementations of seFRET requires the estimation of cross-talks using a third image (IAA in c) from which correction factors (AER in d, and DER in e) can be estimated. These parameters are used to subtract spill-over contributions from the FRET-sensitized acceptor emission (f, cFRET). FRET efficiency (E) can be then estimated by normalizing cFRET to the donor (dFRET) or acceptor emission (aFRET) that would have been measured with E = 0 or E = 1, respectively.
Fig. 2.
Fig. 2. Photon-economy in FRET estimation by TCSPC. The $\tilde{\sigma }$ values were obtained numerically. The mock curve in (a) exemplifies how the $\tilde{\sigma }$ values can be used. Divided by NP0.5, $\tilde{\sigma }$ returns the expected standard deviation on the FRET estimate. When squared and divided by the maximum variance that might be targeted in an experiment, $\tilde{\sigma }$ provide an estimate of the minimum number of photons that should be collected (ND). Numerical estimations of the standard deviations of FRET estimates measured with FLIM, for an ideal system (b) with Dirac-like IRF for τ0=1ns (blue), 3ns (black lines and yellow area) and 10ns (magenta) or with a finite IRF of 38ps fwhm (c). Curves of the same color show f = 10%, 50% and ∼90% from top to bottom. (d) Simulations for τ0=3ns, with an uncorrelated background that must be estimated, with values of 0 (magenta), 100 (black curves and yellow area) and 1,000 photons (blue).
Fig. 3.
Fig. 3. seFRET in the absence of background. The dFRET (a) and the aFRET (b) estimators are unbiased in the absence of background signals and, as expected they estimate the quantities fDE and fAE, respectively. The intensity-normalized standard deviations for dFRET (c) and aFRET (d) vary with a sweep of the parameters (nDA, nD, nA and E) albeit in a narrow SNR area (gray) and with a perfect match between the analytical solutions (dark gray curves) and the numerical simulations (circles). In yellow, the reference area explored by TCSPC from Fig. 2(b) is shown.
Fig. 4.
Fig. 4. seFRET in the presence of spectral bleed-through. dFRET (a) and aFRET (b) are unbiased estimators as shown using the cross-talk reported in Table 1 for a representative configuration of a confocal (system 1, red) and a wide-field (system 2, blue) microscope. Crosstalk causes a significant deterioration of SNR values for dFRET (c,e) and aFRET estimators (d,f). The loss of SNR is shown in (c-d) and its dependency on DER, AER and the fraction of interacting donor/acceptor fluorophores is further illustrated in (e-f) where the SNR regions for fD=fA=1 (grey), fD=0.1 and fA=1 (red) or fD=1 and fA=0.1 (blue) are shown by varying DER and AER from 0 to 1. In yellow, we show also the TCSPC reference area from Fig. 2(c).
Fig. 5.
Fig. 5. seFRET in the presence of background. The dFRET (a) and aFRET (b) are not accurate estimators of fDE and fAE in the presence of background (simulated background-to-signal ratio of 0%, black; 20%, yellow; 40%, orange and 60%, red). The analytical solutions (solid lines) describing the noise in dFRET (c) and aFRET (d) match the numerical simulations (solid circles) also in the presence of a background signal. We compare the noise for the systems also shown in Fig. 3, i.e. system 1 (confocal, 0% (red) and 20% (orange) background), system 2 (wide-field, 0% (blue) and 20% (cyan) background) and the reference ideal case (0% (black) and 20% (dark gray) background). The SNR range explored by TCSPC from Fig. 2(d) is shown in yellow.

Tables (5)

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Table 1. Examples of photon-budget required to attain a standard deviation of 5% in FRET efficiency.

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Table 2. properties of FRET pairs relevant to seFRET

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Table 3. Conversion of nomenclature from Elder et al. [14]

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Table 4. Conversion of nomenclature from this work

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Table 5. Conversion of nomenclature from Hoppe et al. [15]

Equations (37)

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σ E i 2 = ( J i F R E T 1 ) 11 = N P 1 ( σ ~ B 2 + σ ~ S B T 2 + σ ~ E 2 )
L = i = 1 m 1 / N i ! [ F ( i U ) F ( ( i 1 ) U ) ] N i e [ F ( i U ) F ( ( i 1 ) U ) ]
F ( u , q ) = 0 u f ( υ , q ) d υ
f ( u , q ) = k e x T S ( u ) ζ ( q )
j i j = E [ 2 l n f ( u , q ) q i q j ] u
j j k = T i = 1 m k i S i ( u ) ζ i ( q ) ζ i ( q ) q j ζ i ( q ) q k
f ( λ , E , n D , n A , n D A ) = k e x T { S D ( λ ) [ n D + n D A ( 1 E ) ] + n D A S S E ( λ ) E + n A S D E ( λ ) }
F ( λ ) = k e x T { [ n D + n D A ( 1 E ) ] 0 λ S D ( λ ) d λ + n D A E 0 λ S S E ( λ ) d λ + n A 0 λ S D E ( λ ) d λ }
I D D = F ( λ d 2 ) F ( λ d 1 ) = k e x T S D D [ n D + n D A ( 1 E ) ]
λ d 1 λ d 2 S D ( λ ) d λ = S D D ; λ d 1 λ d 2 S S E ( λ ) d λ = 0 ; λ d 1 λ d 2 S D E ( λ ) d λ = 0 ;
I D D = k e x T { S D D [ n D + n D A ( 1 E ) ] + B D D } = k e x T { S D D N D [ 1 f D E ] + B D D }
I D D ( f D E ) = k e x T [ S D D N D ( 1 f D E ) + B D D ] I D D ( f A E ) = k e x T [ S D D N D S D D N A f A E + B D D ]
I D A = k e x T { [ n D + n D A ( 1 E ) ] S D D D E R + [ n D A E + ( n A + n D A ) ε A E R ] S A A + B D A }
λ a 1 λ a 2 S D ( λ ) d λ = S D D D E R ; λ a 1 λ a 2 S S E ( λ ) d λ = S A A ; λ a 1 λ a 2 S D E ( λ ) d λ = ε S A A A E R
I D A ( f D E ) = k e x T { N D ( S A A S D D D E R ) f D E + S A A N A ε A E R + S D D N D D E R + B D A } I D A ( f A E ) = k e x T { N A ( S A A S D D D E R ) f A E + S A A N A ε A E R + S D D N D D E R + B D A }
I A A = k e x T ε ( S A A N A + B A A )
{ I D D ( E D , C D ) = N P [ C D ( 1 E D ) + B D D ] I D D ( E A , C D , C A ) = N P [ C D η C A E A + B D D ] I D A ( E D , C D , C A ) = N P [ ( η 1 D E R ) C D E D + C A ε A E R + C D D E R + B D A ] I D A ( E A , C D , C A ) = N P [ ( 1 D E R η ) C A E A + C A ε A E R + C D D E R + B D A ] I A A ( C A ) = N P ε [ C A + B A A ]
{ I D D ( E D , C D , C A ) = F D D [ ( 1 β D D 1 ) ζ D D ( E D , C D , C A ) + β D D 1 ] F D D = N P ( 1 + B D D ) β D D = ( 1 + B D D ) B D D 1 ζ D D ( E D , C D , C A ) = C D ( 1 E D )
{ I D D ( E A , C D , C A ) = F D D [ ( 1 β D D 1 ) ζ D D ( E A , C D , C A ) + β D D 1 ] F D D = N P ( 1 + B D D ) β D D = ( 1 + B D D ) B D D 1 ζ D D ( E A , C D , C A ) = C D η C A E A
{ I D A ( E D , C D , C A ) = F D A [ ( 1 β D A 1 ) ζ D A ( E D , C D , C A ) + β D A 1 ] F D A = N P ( 1 + B D A ) β D A = ( 1 + B D A ) B D A 1 ζ D A ( E D , C D , C A ) = ( η 1 D E R ) C D E D + C A ε A E R + C D D E R
{ I D A ( E A , C D , C A ) = F D A [ ( 1 β D A 1 ) ζ D A ( E A , C D , C A ) + β D A 1 ] F D A = N P ( 1 + B D A ) β D A = ( 1 + B D A ) B D A 1 ζ D A ( E A , C D , C A ) = ( 1 D E R η ) C A E A + C A ε A E R + C D D E R
{ I A A ( C A ) = F A A [ ( 1 β A A 1 ) ζ A A ( C A ) + β A A 1 ] F A A = ε N P ( 1 + B A A ) β A A = ( 1 + B A A ) B A A 1 ζ A A ( C A ) = C A
( ζ D D E D ζ D D C D ζ D D C A ζ D A E D ζ D A C D ζ D A C A ζ A A E D ζ A A C D ζ A A C A ) = ( C D 1 0 ( η 1 D E R ) C D D E R ( η 1 D E R ) E D ε A E R 0 0 1 )
( ζ D D E A ζ D D C D ζ D D C A ζ D A E A ζ D A C D ζ D A C A ζ A A E A ζ A A C D ζ A A C A ) = ( η C A 1 η E A ( 1 D E R η ) C A D E R ε A E R + ( 1 D E R η ) E A 0 0 1 )
J 11 = N P C D 2 [ 1 C D ( 1 E D ) + B D D + η 1 D E R ( η 1 D E R ) C D E D + C A ε A E R + C D D E R + B D A ]
J 12 = J 21 = N P C D [ 1 C D ( 1 E D ) + B D D + ( η 1 D E R ) C D [ D E R ( η 1 D E R ) E D ] ( η 1 D E R ) C D E D + C A ε A E R + C D D E R + B D A ]
J 13 = J 13 = N P C D ( η 1 D E R ) ε A E R ( η 1 D E R ) C D E D + C A ε A E R + C D D E R + B D A
J 22 = N P { 1 C D ( 1 E D ) + B D D + [ D E R ( η 1 D E R ) E D ] 2 ( η 1 D E R ) C D E D + C A ε A E R + C D D E R + B D A }
J 23 = J 32 = N P { [ D E R ( η 1 D E R ) E D ] ε A E R ( η 1 D E R ) C D E D + C A ε A E R + C D D E R + B D A }
J 33 = N P ( C A + B A A ) 1
σ E 2 ( d F R E T ) = N P 1 { B D D [ D E R η ( 1 E D ) + E D ] 2 C D 2 + B D A [ η ( 1 E D ) ] 2 C D 2 + B A A [ A E R η ( 1 E D ) ] 2 C D 2 ε + A E R ( A E R + 1 ) [ C A ( 1 E D ) 2 η 2 ] C D 2 ε + D E R [ ( D E R + 1 ) ( 1 E D ) η + 2 E D ] [ ( 1 E D ) 2 η ] C D 1 + E D ( 1 E D ) [ E D ( 1 η ) + η ] C D 1 }
{ σ ~ B 2 ( d F R E T ) = σ ~ B D D 2 ( d F R E T ) + σ ~ B D A 2 ( d F R E T ) + σ ~ B A A 2 ( d F R E T ) σ ~ B D D 2 ( d F R E T ) = B D D [ D E R η ( 1 E D ) + E D ] 2 C D 2 σ ~ B D A 2 ( d F R E T ) = B D A [ η ( 1 E D ) ] 2 C D 2 σ ~ B A A 2 ( d F R E T ) = B A A [ A E R η ( 1 E D ) ] 2 C D 2 ε
{ σ ~ S B T 2 ( d F R E T ) = σ ~ D E R 2 ( d F R E T ) + σ ~ A E R 2 ( d F R E T ) σ ~ D E R 2 ( d F R E T ) = A E R ( A E R + 1 ) [ C A ( 1 E D ) 2 η 2 ] C D 2 ε σ ~ A E R 2 ( d F R E T ) = D E R [ ( D E R + 1 ) ( 1 E D ) η + 2 E D ] [ ( 1 E D ) 2 η ] C D 1
σ ~ E 2 ( d F R E T ) = E D ( 1 E D ) [ E D ( 1 η ) + η ] C D 1
{ σ ~ B 2 ( a F R E T ) = σ ~ B D D 2 ( a F R E T ) + σ ~ B D A 2 ( a F R E T ) + σ ~ B A A 2 ( a F R E T ) σ ~ B D D 2 ( a F R E T ) = B D D D E R C A 2 σ ~ B D A 2 ( a F R E T ) = B D A C A 2 σ ~ B A A 2 ( a F R E T ) = B A A [ ε A E R E A ] 2 C D 2 ε 1
{ σ ~ S B T 2 ( a F R E T ) = σ ~ D E R 2 ( a F R E T ) + σ ~ A E R 2 ( a F R E T ) σ ~ D E R 2 ( a F R E T ) = D E R ( D E R + 1 ) [ C D C A E A η ] C A 2 σ ~ A E R 2 ( a F R E T ) = A E R [ ( A E R + 1 ) ε + 2 E A ] C A 1
σ ~ E 2 ( a F R E T ) = E A ( 1 + ε 1 A ) C A 1