Abstract

Analyzing large fluorescence lifetime imaging (FLIM) data is becoming overwhelming; the latest FLIM systems easily produce massive amounts of data, making an efficient analysis more challenging than ever. In this paper we propose the combination of a custom-fit variable projection method, with a Laguerre expansion based deconvolution, to analyze bi-exponential data obtained from time-domain FLIM systems. Unlike nonlinear least squares methods, which require a suitable initial guess from an experienced researcher, the new method is free from manual interventions and hence can support automated analysis. Monte Carlo simulations are carried out on synthesized FLIM data to demonstrate the performance compared to other approaches. The performance is also illustrated on real-life FLIM data obtained from the study of autofluorescence of daisy pollen and the endocytosis of gold nanorods (GNRs) in living cells. In the latter, the fluorescence lifetimes of the GNRs are much shorter than the full width at half maximum of the instrument response function. Overall, our proposed method contains simple steps and shows great promise in realising automated FLIM analysis of large data sets.

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2016 (7)

G. Yahav, A. Hirshberg, O. Salomon, N. Amariglio, L. Trakhtenbrot, and D. Fixler, “Fluorescence lifetime imaging of DAPI-stained nuclei as a novel diagnostic tool for the detection and classification of B-cell chronic lymphocytic leukemia,” Cytometry A 89(7), 644–652 (2016).
[Crossref] [PubMed]

G. Wei, J. Yu, J. Wang, P. Gu, D. J. Birch, and Y. Chen, “Hairpin DNA-functionalized gold nanorods for mRNA detection in homogenous solution,” J. Biomed. Opt. 21(9), 097001 (2016).
[Crossref] [PubMed]

S. P. Poland, A. T. Erdogan, N. Krstajić, J. Levitt, V. Devauges, R. J. Walker, D. D.-U. Li, S. M. Ameer-Beg, and R. K. Henderson, “New high-speed centre of mass method incorporating background subtraction for accurate determination of fluorescence lifetime,” Opt. Express 24(7), 6899–6915 (2016).
[Crossref] [PubMed]

H. A. R. Homulle, F. Powolny, P. L. Stegehuis, J. Dijkstra, D. U. Li, K. Homicsko, D. Rimoldi, K. Muehlethaler, J. O. Prior, R. Sinisi, E. Dubikovskaya, E. Charbon, and C. Bruschini, “Compact solid-state CMOS single-photon detector array for in vivo NIR fluorescence lifetime oncology measurements,” Biomed. Opt. Express 7(5), 1797–1814 (2016).
[Crossref] [PubMed]

G. Wu, T. Nowotny, Y. Zhang, H. Q. Yu, and D. D.-U. Li, “Artificial neural network approaches for fluorescence lifetime imaging techniques,” Opt. Lett. 41(11), 2561–2564 (2016).
[Crossref] [PubMed]

Y. Zhang, Y. Chen, and D. D.-U. Li, “Optimizing Laguerre expansion based deconvolution methods for analysing bi-exponential fluorescence lifetime images,” Opt. Express 24(13), 13894–13905 (2016).
[Crossref] [PubMed]

Y. Zhang, A. A. Khan, G. D. Vigil, and S. S. Howard, “Super-sensitivity multiphoton frequency-domain fluorescence lifetime imaging microscopy,” Opt. Express 24(18), 20862–20867 (2016).
[Crossref] [PubMed]

2015 (6)

S. P. Poland, N. Krstajić, J. Monypenny, S. Coelho, D. Tyndall, R. J. Walker, V. Devauges, J. Richardson, N. Dutton, P. Barber, D. D.-U. Li, K. Suhling, T. Ng, R. K. Henderson, and S. M. Ameer-Beg, “A high speed multifocal multiphoton fluorescence lifetime imaging microscope for live-cell FRET imaging,” Biomed. Opt. Express 6(2), 277–296 (2015).
[Crossref] [PubMed]

D. D.-U. Li, H. Yu, and Y. Chen, “Fast bi-exponential fluorescence lifetime imaging analysis methods,” Opt. Lett. 40(3), 336–339 (2015).
[Crossref] [PubMed]

M. G. Giacomelli, Y. Sheikine, H. Vardeh, J. L. Connolly, and J. G. Fujimoto, “Rapid imaging of surgical breast excisions using direct temporal sampling two photon fluorescent lifetime imaging,” Biomed. Opt. Express 6(11), 4317–4325 (2015).
[Crossref] [PubMed]

J. A. Jo, J. Park, P. Pande, S. Shrestha, M. J. Serafino, J. J. Rico Jimenez, F. Clubb, B. Walton, L. M. Buja, J. E. Phipps, M. D. Feldman, J. Adame, and B. E. Applegate, “Simultaneous morphological and biochemical endogenous optical imaging of atherosclerosis,” Eur. Heart J. Cardiovasc. Imaging 16(8), 910–918 (2015).
[Crossref] [PubMed]

A. Shivalingam, M. A. Izquierdo, A. Le Marois, A. Vyšniauskas, K. Suhling, M. K. Kuimova, and R. Vilar, “The interactions between a small molecule and G-quadruplexes are visualized by fluorescence lifetime imaging microscopy,” Nat. Commun. 6, 8178 (2015).
[Crossref] [PubMed]

Y. Zhang, G. Wei, J. Yu, D. J. S. Birch, and Y. Chen, “Surface plasmon enhanced energy transfer between gold nanorods and fluorophores: application to endocytosis study and RNA detection,” Faraday Discuss. 178, 383–394 (2015).
[Crossref] [PubMed]

2014 (5)

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating NADH and NADPH fluorescence in live cells and tissues using FLIM,” Nat. Commun. 5, 3936 (2014).
[Crossref] [PubMed]

D. M. Kavanagh, A. M. Smyth, K. J. Martin, A. Dun, E. R. Brown, S. Gordon, K. J. Smillie, L. H. Chamberlain, R. S. Wilson, L. Yang, W. Lu, M. A. Cousin, C. Rickman, and R. R. Duncan, “A molecular toggle after exocytosis sequesters the presynaptic syntaxin1a molecules involved in prior vesicle fusion,” Nat. Commun. 5, 5774 (2014).
[Crossref] [PubMed]

R. M. Field, S. Realov, and K. L. Shepard, “A 100 fps, time-correlated single-photon-counting-based fluorescence-lifetime imager in 130 nm CMOS,” IEEE J. Solid-St. Circulation 49, 867–880 (2014).

D. Fixler, T. Nayhoz, and K. Ray, “Diffusion reflection and fluorescence lifetime imaging microscopy study of fluorophore-conjugated gold nanoparticles or nanorods in solid phantoms,” ACS Photonics 1(9), 900–905 (2014).
[Crossref] [PubMed]

S. Coda, A. J. Thompson, G. T. Kennedy, K. L. Roche, L. Ayaru, D. S. Bansi, G. W. Stamp, A. V. Thillainayagam, P. M. W. French, and C. Dunsby, “Fluorescence lifetime spectroscopy of tissue autofluorescence in normal and diseased colon measured ex vivo using a fiber-optic probe,” Biomed. Opt. Express 5(2), 515–538 (2014).
[Crossref] [PubMed]

2013 (8)

S. C. Warren, A. Margineanu, D. Alibhai, D. J. Kelly, C. Talbot, Y. Alexandrov, I. Munro, M. Katan, C. Dunsby, and P. M. French, “Rapid global fitting of large fluorescence lifetime imaging microscopy datasets,” PLoS One 8(8), e70687 (2013).
[Crossref] [PubMed]

H. Chen and E. Gratton, “A practical implementation of multifrequency widefield frequency-domain fluorescence lifetime imaging microscopy,” Microsc. Res. Tech. 76(3), 282–289 (2013).
[Crossref] [PubMed]

N. A. Hosny, G. Mohamedi, P. Rademeyer, J. Owen, Y. Wu, M.-X. Tang, R. J. Eckersley, E. Stride, and M. K. Kuimova, “Mapping microbubble viscosity using fluorescence lifetime imaging of molecular rotors,” Proc. Natl. Acad. Sci. U.S.A. 110(23), 9225–9230 (2013).
[Crossref] [PubMed]

Y. Sun, J. E. Phipps, J. Meier, N. Hatami, B. Poirier, D. S. Elson, D. G. Farwell, and L. Marcu, “Endoscopic fluorescence lifetime imaging for in vivo intraoperative diagnosis of oral carcinoma,” Microsc. Microanal. 19(4), 791–798 (2013).
[Crossref] [PubMed]

M. Nobis, E. J. McGhee, J. P. Morton, J. P. Schwarz, S. A. Karim, J. Quinn, M. Edward, A. D. Campbell, L. C. McGarry, T. R. J. Evans, V. G. Brunton, M. C. Frame, N. O. Carragher, Y. Wang, O. J. Sansom, P. Timpson, and K. I. Anderson, “Intravital FLIM-FRET imaging reveals dasatinib-induced spatial control of src in pancreatic cancer,” Cancer Res. 73(15), 4674–4686 (2013).
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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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A. Leray, S. Padilla-Parra, J. Roul, L. Héliot, and M. Tramier, “Spatio-Temporal Quantification of FRET in living cells by fast time-domain FLIM: a comparative study of non-fitting methods [corrected],” PLoS One 8(7), e69335 (2013).
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2012 (5)

J. Liu, Y. Sun, J. Qi, and L. Marcu, “A novel method for fast and robust estimation of fluorescence decay dynamics using constrained least-squares deconvolution with Laguerre expansion,” Phys. Med. Biol. 57(4), 843–865 (2012).
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K. Okabe, N. Inada, C. Gota, Y. Harada, T. Funatsu, and S. Uchiyama, “Intracellular temperature mapping with a fluorescent polymeric thermometer and fluorescence lifetime imaging microscopy,” Nat. Commun. 3, 705 (2012).
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S. R. Stürzenbaum, M. Höckner, A. Panneerselvam, J. Levitt, J. S. Bouillard, S. Taniguchi, L. A. Dailey, R. Ahmad Khanbeigi, E. V. Rosca, M. Thanou, K. Suhling, A. V. Zayats, and M. Green, “Biosynthesis of luminescent quantum dots in an earthworm,” Nat. Nanotechnol. 8(1), 57–60 (2012).
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K. Saha, S. S. Agasti, C. Kim, X. Li, and V. M. Rotello, “Gold nanoparticles in chemical and biological sensing,” Chem. Rev. 112(5), 2739–2779 (2012).
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D. D.-U. Li, S. Ameer-Beg, J. Arlt, D. Tyndall, R. Walker, D. R. Matthews, V. Visitkul, J. Richardson, and R. K. Henderson, “Time-domain fluorescence lifetime imaging techniques suitable for solid-state imaging sensor arrays,” Sensors (Basel) 12(12), 5650–5669 (2012).
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2011 (5)

Y. Zhang, D. J. S. Birch, and Y. Chen, “Two-photon excited surface plasmon enhanced energy transfer between DAPI and gold nanoparticles: Opportunities in intra-cellular imaging and sensing,” Appl. Phys. Lett. 99(10), 103701 (2011).
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G. O. Fruhwirth, L. P. Fernandes, G. Weitsman, G. Patel, M. Kelleher, K. Lawler, A. Brock, S. P. Poland, D. R. Matthews, G. Kéri, P. R. Barber, B. Vojnovic, S. M. Ameer-Beg, A. C. C. Coolen, F. Fraternali, and T. Ng, “How Förster resonance energy transfer imaging improves the understanding of protein interaction networks in cancer biology,” ChemPhysChem 12(3), 442–461 (2011).
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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(9), 096012 (2011).
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P. Pande and J. A. Jo, “Automated analysis of fluorescence lifetime imaging microscopy (FLIM) data based on the Laguerre deconvolution method,” IEEE Trans. Biomed. Eng. 58(1), 172–181 (2011).
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S. Padilla-Parra, N. Auduge, M. Coppey-Moisan, and M. Tramier, “Non fitting based FRET–FLIM analysis approaches applied to quantify protein–protein interactions in live cells,” Biophys. Rev. 3(2), 63–70 (2011).
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2010 (5)

A. Agrawal, B. D. Gallas, C. Parker, K. M. Agrawal, and T. J. Pfefer, “Sensitivity of time-resolved fluorescence analysis methods for disease detection,” IEEE J. Sel. Top. Quant. 16(4), 877–885 (2010).
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J. K. Barral, E. Gudmundson, N. Stikov, M. Etezadi-Amoli, P. Stoica, and D. G. Nishimura, “A robust methodology for in vivo T1 mapping,” Magn. Reson. Med. 64(4), 1057–1067 (2010).
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M. Fritzsche and C.-F. Mandenius, “Fluorescent cell-based sensing approaches for toxicity testing,” Anal. Bioanal. Chem. 398(1), 181–191 (2010).
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D.-U. Li, J. Arlt, J. Richardson, R. Walker, A. Buts, D. Stoppa, E. Charbon, and R. Henderson, “Real-time fluorescence lifetime imaging system with a 32 x 32 0.13 μm CMOS low dark-count single-photon avalanche diode array,” Opt. Express 18(10), 10257–10269 (2010).
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P. R. Barber, S. M. Ameer-Beg, S. Pathmananthan, M. Rowley, and A. C. C. Coolen, “A Bayesian method for single molecule, fluorescence burst analysis,” Biomed. Opt. Express 1(4), 1148–1158 (2010).
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2009 (1)

C. Y. Fu, B. K. Ng, and S. G. Razul, “Fluorescence lifetime discrimination using expectation-maximization algorithm with joint deconvolution,” J. Biomed. Opt. 14(6), 064009 (2009).
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2007 (2)

S. Laptenok, K. M. Mullen, J. W. Borst, I. H. van Stokkum, V. V. Apanasovich, and A. Visser, “Fluorescence lifetime imaging microscopy (FLIM) data analysis with TIMP,” J. Stat. Softw. 18(8), 1–20 (2007).
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K. M. Mullen and I. H. Van Stokkum, “TIMP: an R package for modeling multi-way spectroscopic measurements,” J. Stat. Softw. 18(3), 1–46 (2007).
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2006 (1)

J. A. Jo, Q. Fang, T. Papaioannou, J. D. Baker, A. H. Dorafshar, T. Reil, J.-H. Qiao, M. C. Fishbein, J. A. Freischlag, and L. Marcu, “Laguerre-based method for analysis of time-resolved fluorescence data: application to in-vivo characterization and diagnosis of atherosclerotic lesions,” J. Biomed. Opt. 11(2), 021004 (2006).
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2005 (1)

D. B. McCombie, A. T. Reisner, and H. H. Asada, “Laguerre-model blind system identification: cardiovascular dynamics estimated from multiple peripheral circulatory signals,” IEEE Trans. Biomed. Eng. 52(11), 1889–1901 (2005).
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2004 (3)

R. Niesner, B. Peker, P. Schlüsche, and K.-H. Gericke, “Noniterative biexponential fluorescence lifetime imaging in the investigation of cellular metabolism by means of NAD(P)H autofluorescence,” ChemPhysChem 5(8), 1141–1149 (2004).
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A. V. Agronskaia, L. Tertoolen, and H. C. Gerritsen, “Fast fluorescence lifetime imaging of calcium in living cells,” J. Biomed. Opt. 9(6), 1230–1237 (2004).
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S. Pelet, M. J. R. Previte, L. H. Laiho, and P. T. C. So, “A fast global fitting algorithm for fluorescence lifetime imaging microscopy based on image segmentation,” Biophys. J. 87(4), 2807–2817 (2004).
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2003 (1)

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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2002 (1)

M. Elangovan, R. N. Day, and A. Periasamy, “Nanosecond fluorescence resonance energy transfer-fluorescence lifetime imaging microscopy to localize the protein interactions in a single living cell,” J. Microsc. 205(1), 3–14 (2002).
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2001 (2)

K. C. Lee, J. Siegel, S. E. Webb, S. Lévêque-Fort, M. J. Cole, R. Jones, K. Dowling, M. J. Lever, and P. M. French, “Application of the stretched exponential function to fluorescence lifetime imaging,” Biophys. J. 81(3), 1265–1274 (2001).
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C. J. de Grauw and H. C. Gerritsen, “Multiple time-gate module for fluorescence lifetime imaging,” Appl. Spectrosc. 55(6), 670–678 (2001).
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2000 (1)

P. Tinnefeld, V. Buschmann, D.-P. Herten, K.-T. Han, and M. Sauer, “Confocal fluorescence lifetime imaging microscopy (FLIM) at the single molecule level,” Single Mol. 1(3), 215–223 (2000).
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1981 (1)

P. Hall and B. Selinger, “Better estimates of exponential decay parameters,” J. Phys. Chem. 85(20), 2941–2946 (1981).
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1973 (1)

G. H. Golub and V. Pereyra, “The differentiation of pseudo-inverses and nonlinear least squares problems whose variables separate,” SIAM J. Numer. Anal. 10(2), 413–432 (1973).
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1963 (1)

D. Marquardt, “An Algorithm for least-squares estimation of nonlinear parameters,” SIAM J. Appl. Math. 11(2), 431–441 (1963).
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1944 (1)

K. Levenberg, “A method for the solution of certain non-linear problems in least squares,” Q. Appl. Math. 2, 164–168 (1944).

Adame, J.

J. A. Jo, J. Park, P. Pande, S. Shrestha, M. J. Serafino, J. J. Rico Jimenez, F. Clubb, B. Walton, L. M. Buja, J. E. Phipps, M. D. Feldman, J. Adame, and B. E. Applegate, “Simultaneous morphological and biochemical endogenous optical imaging of atherosclerosis,” Eur. Heart J. Cardiovasc. Imaging 16(8), 910–918 (2015).
[Crossref] [PubMed]

Agasti, S. S.

K. Saha, S. S. Agasti, C. Kim, X. Li, and V. M. Rotello, “Gold nanoparticles in chemical and biological sensing,” Chem. Rev. 112(5), 2739–2779 (2012).
[Crossref] [PubMed]

Agrawal, A.

A. Agrawal, B. D. Gallas, C. Parker, K. M. Agrawal, and T. J. Pfefer, “Sensitivity of time-resolved fluorescence analysis methods for disease detection,” IEEE J. Sel. Top. Quant. 16(4), 877–885 (2010).
[Crossref]

Agrawal, K. M.

A. Agrawal, B. D. Gallas, C. Parker, K. M. Agrawal, and T. J. Pfefer, “Sensitivity of time-resolved fluorescence analysis methods for disease detection,” IEEE J. Sel. Top. Quant. 16(4), 877–885 (2010).
[Crossref]

Agronskaia, A. V.

A. V. Agronskaia, L. Tertoolen, and H. C. Gerritsen, “Fast fluorescence lifetime imaging of calcium in living cells,” J. Biomed. Opt. 9(6), 1230–1237 (2004).
[Crossref] [PubMed]

Ahmad Khanbeigi, R.

S. R. Stürzenbaum, M. Höckner, A. Panneerselvam, J. Levitt, J. S. Bouillard, S. Taniguchi, L. A. Dailey, R. Ahmad Khanbeigi, E. V. Rosca, M. Thanou, K. Suhling, A. V. Zayats, and M. Green, “Biosynthesis of luminescent quantum dots in an earthworm,” Nat. Nanotechnol. 8(1), 57–60 (2012).
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Alexandrov, Y.

S. C. Warren, A. Margineanu, D. Alibhai, D. J. Kelly, C. Talbot, Y. Alexandrov, I. Munro, M. Katan, C. Dunsby, and P. M. French, “Rapid global fitting of large fluorescence lifetime imaging microscopy datasets,” PLoS One 8(8), e70687 (2013).
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Alibhai, D.

S. C. Warren, A. Margineanu, D. Alibhai, D. J. Kelly, C. Talbot, Y. Alexandrov, I. Munro, M. Katan, C. Dunsby, and P. M. French, “Rapid global fitting of large fluorescence lifetime imaging microscopy datasets,” PLoS One 8(8), e70687 (2013).
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Amariglio, N.

G. Yahav, A. Hirshberg, O. Salomon, N. Amariglio, L. Trakhtenbrot, and D. Fixler, “Fluorescence lifetime imaging of DAPI-stained nuclei as a novel diagnostic tool for the detection and classification of B-cell chronic lymphocytic leukemia,” Cytometry A 89(7), 644–652 (2016).
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Ameer-Beg, S.

D. D.-U. Li, S. Ameer-Beg, J. Arlt, D. Tyndall, R. Walker, D. R. Matthews, V. Visitkul, J. Richardson, and R. K. Henderson, “Time-domain fluorescence lifetime imaging techniques suitable for solid-state imaging sensor arrays,” Sensors (Basel) 12(12), 5650–5669 (2012).
[Crossref] [PubMed]

Ameer-Beg, S. M.

Anderson, K. I.

M. Nobis, E. J. McGhee, J. P. Morton, J. P. Schwarz, S. A. Karim, J. Quinn, M. Edward, A. D. Campbell, L. C. McGarry, T. R. J. Evans, V. G. Brunton, M. C. Frame, N. O. Carragher, Y. Wang, O. J. Sansom, P. Timpson, and K. I. Anderson, “Intravital FLIM-FRET imaging reveals dasatinib-induced spatial control of src in pancreatic cancer,” Cancer Res. 73(15), 4674–4686 (2013).
[Crossref] [PubMed]

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).
[Crossref] [PubMed]

Apanasovich, V. V.

S. Laptenok, K. M. Mullen, J. W. Borst, I. H. van Stokkum, V. V. Apanasovich, and A. Visser, “Fluorescence lifetime imaging microscopy (FLIM) data analysis with TIMP,” J. Stat. Softw. 18(8), 1–20 (2007).
[Crossref]

Applegate, B. E.

J. A. Jo, J. Park, P. Pande, S. Shrestha, M. J. Serafino, J. J. Rico Jimenez, F. Clubb, B. Walton, L. M. Buja, J. E. Phipps, M. D. Feldman, J. Adame, and B. E. Applegate, “Simultaneous morphological and biochemical endogenous optical imaging of atherosclerosis,” Eur. Heart J. Cardiovasc. Imaging 16(8), 910–918 (2015).
[Crossref] [PubMed]

Arlt, J.

D. D.-U. Li, S. Ameer-Beg, J. Arlt, D. Tyndall, R. Walker, D. R. Matthews, V. Visitkul, J. Richardson, and R. K. Henderson, “Time-domain fluorescence lifetime imaging techniques suitable for solid-state imaging sensor arrays,” Sensors (Basel) 12(12), 5650–5669 (2012).
[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(9), 096012 (2011).
[Crossref] [PubMed]

D.-U. Li, J. Arlt, J. Richardson, R. Walker, A. Buts, D. Stoppa, E. Charbon, and R. Henderson, “Real-time fluorescence lifetime imaging system with a 32 x 32 0.13 μm CMOS low dark-count single-photon avalanche diode array,” Opt. Express 18(10), 10257–10269 (2010).
[Crossref] [PubMed]

Asada, H. H.

D. B. McCombie, A. T. Reisner, and H. H. Asada, “Laguerre-model blind system identification: cardiovascular dynamics estimated from multiple peripheral circulatory signals,” IEEE Trans. Biomed. Eng. 52(11), 1889–1901 (2005).
[Crossref] [PubMed]

Auduge, N.

S. Padilla-Parra, N. Auduge, M. Coppey-Moisan, and M. Tramier, “Non fitting based FRET–FLIM analysis approaches applied to quantify protein–protein interactions in live cells,” Biophys. Rev. 3(2), 63–70 (2011).
[Crossref]

Ayaru, L.

Bain, A. J.

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating NADH and NADPH fluorescence in live cells and tissues using FLIM,” Nat. Commun. 5, 3936 (2014).
[Crossref] [PubMed]

Baker, J. D.

J. A. Jo, Q. Fang, T. Papaioannou, J. D. Baker, A. H. Dorafshar, T. Reil, J.-H. Qiao, M. C. Fishbein, J. A. Freischlag, and L. Marcu, “Laguerre-based method for analysis of time-resolved fluorescence data: application to in-vivo characterization and diagnosis of atherosclerotic lesions,” J. Biomed. Opt. 11(2), 021004 (2006).
[Crossref] [PubMed]

Bansi, D. S.

Barber, P.

Barber, P. R.

G. O. Fruhwirth, L. P. Fernandes, G. Weitsman, G. Patel, M. Kelleher, K. Lawler, A. Brock, S. P. Poland, D. R. Matthews, G. Kéri, P. R. Barber, B. Vojnovic, S. M. Ameer-Beg, A. C. C. Coolen, F. Fraternali, and T. Ng, “How Förster resonance energy transfer imaging improves the understanding of protein interaction networks in cancer biology,” ChemPhysChem 12(3), 442–461 (2011).
[Crossref] [PubMed]

P. R. Barber, S. M. Ameer-Beg, S. Pathmananthan, M. Rowley, and A. C. C. Coolen, “A Bayesian method for single molecule, fluorescence burst analysis,” Biomed. Opt. Express 1(4), 1148–1158 (2010).
[Crossref] [PubMed]

Barral, J. K.

J. K. Barral, E. Gudmundson, N. Stikov, M. Etezadi-Amoli, P. Stoica, and D. G. Nishimura, “A robust methodology for in vivo T1 mapping,” Magn. Reson. Med. 64(4), 1057–1067 (2010).
[Crossref] [PubMed]

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] [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).
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Birch, D. J.

G. Wei, J. Yu, J. Wang, P. Gu, D. J. Birch, and Y. Chen, “Hairpin DNA-functionalized gold nanorods for mRNA detection in homogenous solution,” J. Biomed. Opt. 21(9), 097001 (2016).
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Birch, D. J. S.

Y. Zhang, G. Wei, J. Yu, D. J. S. Birch, and Y. Chen, “Surface plasmon enhanced energy transfer between gold nanorods and fluorophores: application to endocytosis study and RNA detection,” Faraday Discuss. 178, 383–394 (2015).
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Y. Zhang, D. J. S. Birch, and Y. Chen, “Two-photon excited surface plasmon enhanced energy transfer between DAPI and gold nanoparticles: Opportunities in intra-cellular imaging and sensing,” Appl. Phys. Lett. 99(10), 103701 (2011).
[Crossref]

Blacker, T. S.

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating NADH and NADPH fluorescence in live cells and tissues using FLIM,” Nat. Commun. 5, 3936 (2014).
[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]

Borst, J. W.

S. Laptenok, K. M. Mullen, J. W. Borst, I. H. van Stokkum, V. V. Apanasovich, and A. Visser, “Fluorescence lifetime imaging microscopy (FLIM) data analysis with TIMP,” J. Stat. Softw. 18(8), 1–20 (2007).
[Crossref]

Bouillard, J. S.

S. R. Stürzenbaum, M. Höckner, A. Panneerselvam, J. Levitt, J. S. Bouillard, S. Taniguchi, L. A. Dailey, R. Ahmad Khanbeigi, E. V. Rosca, M. Thanou, K. Suhling, A. V. Zayats, and M. Green, “Biosynthesis of luminescent quantum dots in an earthworm,” Nat. Nanotechnol. 8(1), 57–60 (2012).
[Crossref] [PubMed]

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]

Brock, A.

G. O. Fruhwirth, L. P. Fernandes, G. Weitsman, G. Patel, M. Kelleher, K. Lawler, A. Brock, S. P. Poland, D. R. Matthews, G. Kéri, P. R. Barber, B. Vojnovic, S. M. Ameer-Beg, A. C. C. Coolen, F. Fraternali, and T. Ng, “How Förster resonance energy transfer imaging improves the understanding of protein interaction networks in cancer biology,” ChemPhysChem 12(3), 442–461 (2011).
[Crossref] [PubMed]

Brown, E. R.

D. M. Kavanagh, A. M. Smyth, K. J. Martin, A. Dun, E. R. Brown, S. Gordon, K. J. Smillie, L. H. Chamberlain, R. S. Wilson, L. Yang, W. Lu, M. A. Cousin, C. Rickman, and R. R. Duncan, “A molecular toggle after exocytosis sequesters the presynaptic syntaxin1a molecules involved in prior vesicle fusion,” Nat. Commun. 5, 5774 (2014).
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Brunton, V. G.

M. Nobis, E. J. McGhee, J. P. Morton, J. P. Schwarz, S. A. Karim, J. Quinn, M. Edward, A. D. Campbell, L. C. McGarry, T. R. J. Evans, V. G. Brunton, M. C. Frame, N. O. Carragher, Y. Wang, O. J. Sansom, P. Timpson, and K. I. Anderson, “Intravital FLIM-FRET imaging reveals dasatinib-induced spatial control of src in pancreatic cancer,” Cancer Res. 73(15), 4674–4686 (2013).
[Crossref] [PubMed]

Bruschini, C.

Buja, L. M.

J. A. Jo, J. Park, P. Pande, S. Shrestha, M. J. Serafino, J. J. Rico Jimenez, F. Clubb, B. Walton, L. M. Buja, J. E. Phipps, M. D. Feldman, J. Adame, and B. E. Applegate, “Simultaneous morphological and biochemical endogenous optical imaging of atherosclerosis,” Eur. Heart J. Cardiovasc. Imaging 16(8), 910–918 (2015).
[Crossref] [PubMed]

Buschmann, V.

P. Tinnefeld, V. Buschmann, D.-P. Herten, K.-T. Han, and M. Sauer, “Confocal fluorescence lifetime imaging microscopy (FLIM) at the single molecule level,” Single Mol. 1(3), 215–223 (2000).
[Crossref]

Buts, A.

Campbell, A. D.

M. Nobis, E. J. McGhee, J. P. Morton, J. P. Schwarz, S. A. Karim, J. Quinn, M. Edward, A. D. Campbell, L. C. McGarry, T. R. J. Evans, V. G. Brunton, M. C. Frame, N. O. Carragher, Y. Wang, O. J. Sansom, P. Timpson, and K. I. Anderson, “Intravital FLIM-FRET imaging reveals dasatinib-induced spatial control of src in pancreatic cancer,” Cancer Res. 73(15), 4674–4686 (2013).
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Carragher, N. O.

M. Nobis, E. J. McGhee, J. P. Morton, J. P. Schwarz, S. A. Karim, J. Quinn, M. Edward, A. D. Campbell, L. C. McGarry, T. R. J. Evans, V. G. Brunton, M. C. Frame, N. O. Carragher, Y. Wang, O. J. Sansom, P. Timpson, and K. I. Anderson, “Intravital FLIM-FRET imaging reveals dasatinib-induced spatial control of src in pancreatic cancer,” Cancer Res. 73(15), 4674–4686 (2013).
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Chamberlain, L. H.

D. M. Kavanagh, A. M. Smyth, K. J. Martin, A. Dun, E. R. Brown, S. Gordon, K. J. Smillie, L. H. Chamberlain, R. S. Wilson, L. Yang, W. Lu, M. A. Cousin, C. Rickman, and R. R. Duncan, “A molecular toggle after exocytosis sequesters the presynaptic syntaxin1a molecules involved in prior vesicle fusion,” Nat. Commun. 5, 5774 (2014).
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Charbon, E.

Chen, H.

H. Chen and E. Gratton, “A practical implementation of multifrequency widefield frequency-domain fluorescence lifetime imaging microscopy,” Microsc. Res. Tech. 76(3), 282–289 (2013).
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Chen, Y.

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S. P. Poland, N. Krstajić, J. Monypenny, S. Coelho, D. Tyndall, R. J. Walker, V. Devauges, J. Richardson, N. Dutton, P. Barber, D. D.-U. Li, K. Suhling, T. Ng, R. K. Henderson, and S. M. Ameer-Beg, “A high speed multifocal multiphoton fluorescence lifetime imaging microscope for live-cell FRET imaging,” Biomed. Opt. Express 6(2), 277–296 (2015).
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D. D.-U. Li, S. Ameer-Beg, J. Arlt, D. Tyndall, R. Walker, D. R. Matthews, V. Visitkul, J. Richardson, and R. K. Henderson, “Time-domain fluorescence lifetime imaging techniques suitable for solid-state imaging sensor arrays,” Sensors (Basel) 12(12), 5650–5669 (2012).
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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(9), 096012 (2011).
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K. Okabe, N. Inada, C. Gota, Y. Harada, T. Funatsu, and S. Uchiyama, “Intracellular temperature mapping with a fluorescent polymeric thermometer and fluorescence lifetime imaging microscopy,” Nat. Commun. 3, 705 (2012).
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S. Laptenok, K. M. Mullen, J. W. Borst, I. H. van Stokkum, V. V. Apanasovich, and A. Visser, “Fluorescence lifetime imaging microscopy (FLIM) data analysis with TIMP,” J. Stat. Softw. 18(8), 1–20 (2007).
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K. M. Mullen and I. H. Van Stokkum, “TIMP: an R package for modeling multi-way spectroscopic measurements,” J. Stat. Softw. 18(3), 1–46 (2007).
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Vigil, G. D.

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A. Shivalingam, M. A. Izquierdo, A. Le Marois, A. Vyšniauskas, K. Suhling, M. K. Kuimova, and R. Vilar, “The interactions between a small molecule and G-quadruplexes are visualized by fluorescence lifetime imaging microscopy,” Nat. Commun. 6, 8178 (2015).
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G. O. Fruhwirth, L. P. Fernandes, G. Weitsman, G. Patel, M. Kelleher, K. Lawler, A. Brock, S. P. Poland, D. R. Matthews, G. Kéri, P. R. Barber, B. Vojnovic, S. M. Ameer-Beg, A. C. C. Coolen, F. Fraternali, and T. Ng, “How Förster resonance energy transfer imaging improves the understanding of protein interaction networks in cancer biology,” ChemPhysChem 12(3), 442–461 (2011).
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Vyšniauskas, A.

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D. D.-U. Li, S. Ameer-Beg, J. Arlt, D. Tyndall, R. Walker, D. R. Matthews, V. Visitkul, J. Richardson, and R. K. Henderson, “Time-domain fluorescence lifetime imaging techniques suitable for solid-state imaging sensor arrays,” Sensors (Basel) 12(12), 5650–5669 (2012).
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Y. Zhang, G. Wei, J. Yu, D. J. S. Birch, and Y. Chen, “Surface plasmon enhanced energy transfer between gold nanorods and fluorophores: application to endocytosis study and RNA detection,” Faraday Discuss. 178, 383–394 (2015).
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G. Wei, J. Yu, J. Wang, P. Gu, D. J. Birch, and Y. Chen, “Hairpin DNA-functionalized gold nanorods for mRNA detection in homogenous solution,” J. Biomed. Opt. 21(9), 097001 (2016).
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Y. Zhang, G. Wei, J. Yu, D. J. S. Birch, and Y. Chen, “Surface plasmon enhanced energy transfer between gold nanorods and fluorophores: application to endocytosis study and RNA detection,” Faraday Discuss. 178, 383–394 (2015).
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S. R. Stürzenbaum, M. Höckner, A. Panneerselvam, J. Levitt, J. S. Bouillard, S. Taniguchi, L. A. Dailey, R. Ahmad Khanbeigi, E. V. Rosca, M. Thanou, K. Suhling, A. V. Zayats, and M. Green, “Biosynthesis of luminescent quantum dots in an earthworm,” Nat. Nanotechnol. 8(1), 57–60 (2012).
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G. Wu, T. Nowotny, Y. Zhang, H. Q. Yu, and D. D.-U. Li, “Artificial neural network approaches for fluorescence lifetime imaging techniques,” Opt. Lett. 41(11), 2561–2564 (2016).
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Y. Zhang, Y. Chen, and D. D.-U. Li, “Optimizing Laguerre expansion based deconvolution methods for analysing bi-exponential fluorescence lifetime images,” Opt. Express 24(13), 13894–13905 (2016).
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Y. Zhang, A. A. Khan, G. D. Vigil, and S. S. Howard, “Super-sensitivity multiphoton frequency-domain fluorescence lifetime imaging microscopy,” Opt. Express 24(18), 20862–20867 (2016).
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Y. Zhang, G. Wei, J. Yu, D. J. S. Birch, and Y. Chen, “Surface plasmon enhanced energy transfer between gold nanorods and fluorophores: application to endocytosis study and RNA detection,” Faraday Discuss. 178, 383–394 (2015).
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Y. Zhang, D. J. S. Birch, and Y. Chen, “Two-photon excited surface plasmon enhanced energy transfer between DAPI and gold nanoparticles: Opportunities in intra-cellular imaging and sensing,” Appl. Phys. Lett. 99(10), 103701 (2011).
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T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating NADH and NADPH fluorescence in live cells and tissues using FLIM,” Nat. Commun. 5, 3936 (2014).
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Zipp, F.

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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ACS Photonics (1)

D. Fixler, T. Nayhoz, and K. Ray, “Diffusion reflection and fluorescence lifetime imaging microscopy study of fluorophore-conjugated gold nanoparticles or nanorods in solid phantoms,” ACS Photonics 1(9), 900–905 (2014).
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Anal. Bioanal. Chem. (1)

M. Fritzsche and C.-F. Mandenius, “Fluorescent cell-based sensing approaches for toxicity testing,” Anal. Bioanal. Chem. 398(1), 181–191 (2010).
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Appl. Phys. Lett. (1)

Y. Zhang, D. J. S. Birch, and Y. Chen, “Two-photon excited surface plasmon enhanced energy transfer between DAPI and gold nanoparticles: Opportunities in intra-cellular imaging and sensing,” Appl. Phys. Lett. 99(10), 103701 (2011).
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Biomed. Opt. Express (5)

P. R. Barber, S. M. Ameer-Beg, S. Pathmananthan, M. Rowley, and A. C. C. Coolen, “A Bayesian method for single molecule, fluorescence burst analysis,” Biomed. Opt. Express 1(4), 1148–1158 (2010).
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S. Coda, A. J. Thompson, G. T. Kennedy, K. L. Roche, L. Ayaru, D. S. Bansi, G. W. Stamp, A. V. Thillainayagam, P. M. W. French, and C. Dunsby, “Fluorescence lifetime spectroscopy of tissue autofluorescence in normal and diseased colon measured ex vivo using a fiber-optic probe,” Biomed. Opt. Express 5(2), 515–538 (2014).
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S. P. Poland, N. Krstajić, J. Monypenny, S. Coelho, D. Tyndall, R. J. Walker, V. Devauges, J. Richardson, N. Dutton, P. Barber, D. D.-U. Li, K. Suhling, T. Ng, R. K. Henderson, and S. M. Ameer-Beg, “A high speed multifocal multiphoton fluorescence lifetime imaging microscope for live-cell FRET imaging,” Biomed. Opt. Express 6(2), 277–296 (2015).
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M. G. Giacomelli, Y. Sheikine, H. Vardeh, J. L. Connolly, and J. G. Fujimoto, “Rapid imaging of surgical breast excisions using direct temporal sampling two photon fluorescent lifetime imaging,” Biomed. Opt. Express 6(11), 4317–4325 (2015).
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H. A. R. Homulle, F. Powolny, P. L. Stegehuis, J. Dijkstra, D. U. Li, K. Homicsko, D. Rimoldi, K. Muehlethaler, J. O. Prior, R. Sinisi, E. Dubikovskaya, E. Charbon, and C. Bruschini, “Compact solid-state CMOS single-photon detector array for in vivo NIR fluorescence lifetime oncology measurements,” Biomed. Opt. Express 7(5), 1797–1814 (2016).
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Biophys. J. (2)

S. Pelet, M. J. R. Previte, L. H. Laiho, and P. T. C. So, “A fast global fitting algorithm for fluorescence lifetime imaging microscopy based on image segmentation,” Biophys. J. 87(4), 2807–2817 (2004).
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K. C. Lee, J. Siegel, S. E. Webb, S. Lévêque-Fort, M. J. Cole, R. Jones, K. Dowling, M. J. Lever, and P. M. French, “Application of the stretched exponential function to fluorescence lifetime imaging,” Biophys. J. 81(3), 1265–1274 (2001).
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Biophys. Rev. (1)

S. Padilla-Parra, N. Auduge, M. Coppey-Moisan, and M. Tramier, “Non fitting based FRET–FLIM analysis approaches applied to quantify protein–protein interactions in live cells,” Biophys. Rev. 3(2), 63–70 (2011).
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Cancer Res. (1)

M. Nobis, E. J. McGhee, J. P. Morton, J. P. Schwarz, S. A. Karim, J. Quinn, M. Edward, A. D. Campbell, L. C. McGarry, T. R. J. Evans, V. G. Brunton, M. C. Frame, N. O. Carragher, Y. Wang, O. J. Sansom, P. Timpson, and K. I. Anderson, “Intravital FLIM-FRET imaging reveals dasatinib-induced spatial control of src in pancreatic cancer,” Cancer Res. 73(15), 4674–4686 (2013).
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Chem. Rev. (1)

K. Saha, S. S. Agasti, C. Kim, X. Li, and V. M. Rotello, “Gold nanoparticles in chemical and biological sensing,” Chem. Rev. 112(5), 2739–2779 (2012).
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ChemPhysChem (2)

G. O. Fruhwirth, L. P. Fernandes, G. Weitsman, G. Patel, M. Kelleher, K. Lawler, A. Brock, S. P. Poland, D. R. Matthews, G. Kéri, P. R. Barber, B. Vojnovic, S. M. Ameer-Beg, A. C. C. Coolen, F. Fraternali, and T. Ng, “How Förster resonance energy transfer imaging improves the understanding of protein interaction networks in cancer biology,” ChemPhysChem 12(3), 442–461 (2011).
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R. Niesner, B. Peker, P. Schlüsche, and K.-H. Gericke, “Noniterative biexponential fluorescence lifetime imaging in the investigation of cellular metabolism by means of NAD(P)H autofluorescence,” ChemPhysChem 5(8), 1141–1149 (2004).
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Comput. Optim. Appl. (1)

D. P. O’Leary and B. W. Rust, “Variable projection for nonlinear least squares problems,” Comput. Optim. Appl. 54(3), 579–593 (2013).
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Cytometry A (1)

G. Yahav, A. Hirshberg, O. Salomon, N. Amariglio, L. Trakhtenbrot, and D. Fixler, “Fluorescence lifetime imaging of DAPI-stained nuclei as a novel diagnostic tool for the detection and classification of B-cell chronic lymphocytic leukemia,” Cytometry A 89(7), 644–652 (2016).
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Eur. Heart J. Cardiovasc. Imaging (1)

J. A. Jo, J. Park, P. Pande, S. Shrestha, M. J. Serafino, J. J. Rico Jimenez, F. Clubb, B. Walton, L. M. Buja, J. E. Phipps, M. D. Feldman, J. Adame, and B. E. Applegate, “Simultaneous morphological and biochemical endogenous optical imaging of atherosclerosis,” Eur. Heart J. Cardiovasc. Imaging 16(8), 910–918 (2015).
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Faraday Discuss. (1)

Y. Zhang, G. Wei, J. Yu, D. J. S. Birch, and Y. Chen, “Surface plasmon enhanced energy transfer between gold nanorods and fluorophores: application to endocytosis study and RNA detection,” Faraday Discuss. 178, 383–394 (2015).
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IEEE J. Sel. Top. Quant. (1)

A. Agrawal, B. D. Gallas, C. Parker, K. M. Agrawal, and T. J. Pfefer, “Sensitivity of time-resolved fluorescence analysis methods for disease detection,” IEEE J. Sel. Top. Quant. 16(4), 877–885 (2010).
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IEEE J. Solid-St. Circulation (1)

R. M. Field, S. Realov, and K. L. Shepard, “A 100 fps, time-correlated single-photon-counting-based fluorescence-lifetime imager in 130 nm CMOS,” IEEE J. Solid-St. Circulation 49, 867–880 (2014).

IEEE Trans. Biomed. Eng. (2)

P. Pande and J. A. Jo, “Automated analysis of fluorescence lifetime imaging microscopy (FLIM) data based on the Laguerre deconvolution method,” IEEE Trans. Biomed. Eng. 58(1), 172–181 (2011).
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J. Biomed. Opt. (6)

J. A. Jo, Q. Fang, T. Papaioannou, J. D. Baker, A. H. Dorafshar, T. Reil, J.-H. Qiao, M. C. Fishbein, J. A. Freischlag, and L. Marcu, “Laguerre-based method for analysis of time-resolved fluorescence data: application to in-vivo characterization and diagnosis of atherosclerotic lesions,” J. Biomed. Opt. 11(2), 021004 (2006).
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C. Y. Fu, B. K. Ng, and S. G. Razul, “Fluorescence lifetime discrimination using expectation-maximization algorithm with joint deconvolution,” J. Biomed. Opt. 14(6), 064009 (2009).
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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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A. V. Agronskaia, L. Tertoolen, and H. C. Gerritsen, “Fast fluorescence lifetime imaging of calcium in living cells,” J. Biomed. Opt. 9(6), 1230–1237 (2004).
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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(9), 096012 (2011).
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G. Wei, J. Yu, J. Wang, P. Gu, D. J. Birch, and Y. Chen, “Hairpin DNA-functionalized gold nanorods for mRNA detection in homogenous solution,” J. Biomed. Opt. 21(9), 097001 (2016).
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J. Microsc. (1)

M. Elangovan, R. N. Day, and A. Periasamy, “Nanosecond fluorescence resonance energy transfer-fluorescence lifetime imaging microscopy to localize the protein interactions in a single living cell,” J. Microsc. 205(1), 3–14 (2002).
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J. Stat. Softw. (2)

S. Laptenok, K. M. Mullen, J. W. Borst, I. H. van Stokkum, V. V. Apanasovich, and A. Visser, “Fluorescence lifetime imaging microscopy (FLIM) data analysis with TIMP,” J. Stat. Softw. 18(8), 1–20 (2007).
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K. M. Mullen and I. H. Van Stokkum, “TIMP: an R package for modeling multi-way spectroscopic measurements,” J. Stat. Softw. 18(3), 1–46 (2007).
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Magn. Reson. Med. (1)

J. K. Barral, E. Gudmundson, N. Stikov, M. Etezadi-Amoli, P. Stoica, and D. G. Nishimura, “A robust methodology for in vivo T1 mapping,” Magn. Reson. Med. 64(4), 1057–1067 (2010).
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Microsc. Microanal. (1)

Y. Sun, J. E. Phipps, J. Meier, N. Hatami, B. Poirier, D. S. Elson, D. G. Farwell, and L. Marcu, “Endoscopic fluorescence lifetime imaging for in vivo intraoperative diagnosis of oral carcinoma,” Microsc. Microanal. 19(4), 791–798 (2013).
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Microsc. Res. Tech. (1)

H. Chen and E. Gratton, “A practical implementation of multifrequency widefield frequency-domain fluorescence lifetime imaging microscopy,” Microsc. Res. Tech. 76(3), 282–289 (2013).
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Nat. Commun. (4)

T. S. Blacker, Z. F. Mann, J. E. Gale, M. Ziegler, A. J. Bain, G. Szabadkai, and M. R. Duchen, “Separating NADH and NADPH fluorescence in live cells and tissues using FLIM,” Nat. Commun. 5, 3936 (2014).
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D. M. Kavanagh, A. M. Smyth, K. J. Martin, A. Dun, E. R. Brown, S. Gordon, K. J. Smillie, L. H. Chamberlain, R. S. Wilson, L. Yang, W. Lu, M. A. Cousin, C. Rickman, and R. R. Duncan, “A molecular toggle after exocytosis sequesters the presynaptic syntaxin1a molecules involved in prior vesicle fusion,” Nat. Commun. 5, 5774 (2014).
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K. Okabe, N. Inada, C. Gota, Y. Harada, T. Funatsu, and S. Uchiyama, “Intracellular temperature mapping with a fluorescent polymeric thermometer and fluorescence lifetime imaging microscopy,” Nat. Commun. 3, 705 (2012).
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A. Shivalingam, M. A. Izquierdo, A. Le Marois, A. Vyšniauskas, K. Suhling, M. K. Kuimova, and R. Vilar, “The interactions between a small molecule and G-quadruplexes are visualized by fluorescence lifetime imaging microscopy,” Nat. Commun. 6, 8178 (2015).
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Nat. Nanotechnol. (1)

S. R. Stürzenbaum, M. Höckner, A. Panneerselvam, J. Levitt, J. S. Bouillard, S. Taniguchi, L. A. Dailey, R. Ahmad Khanbeigi, E. V. Rosca, M. Thanou, K. Suhling, A. V. Zayats, and M. Green, “Biosynthesis of luminescent quantum dots in an earthworm,” Nat. Nanotechnol. 8(1), 57–60 (2012).
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Opt. Express (4)

Opt. Lett. (2)

Phys. Med. Biol. (1)

J. Liu, Y. Sun, J. Qi, and L. Marcu, “A novel method for fast and robust estimation of fluorescence decay dynamics using constrained least-squares deconvolution with Laguerre expansion,” Phys. Med. Biol. 57(4), 843–865 (2012).
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PLoS One (3)

A. Leray, S. Padilla-Parra, J. Roul, L. Héliot, and M. Tramier, “Spatio-Temporal Quantification of FRET in living cells by fast time-domain FLIM: a comparative study of non-fitting methods [corrected],” PLoS One 8(7), e69335 (2013).
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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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[Crossref] [PubMed]

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[Crossref] [PubMed]

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[Crossref] [PubMed]

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[Crossref]

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[Crossref]

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Figures (6)

Fig. 1
Fig. 1

(a), (c), and (e), Bias and (b), (d), and (f) F plots for different methods, K = 1,000, and N = 256.

Fig. 2
Fig. 2

(a), (c), and (e) Bias and (b), (d), and (f) F plots for different methods, K = 50, and N = 256.

Fig. 3
Fig. 3

(a) Normalized bias and (b) F plots for τave = 1 + (1– a)τ2 when K = 1000. (c) Normalized bias and (d) F plots for τave when K = 50.

Fig. 4
Fig. 4

Measured IRF, measured and fitted histograms.

Fig. 5
Fig. 5

(a) Intensity, (b) τave, (c) a, and (d) τ2 images; (e) a, (f) τ2, (g) τ1, and (h) τave histograms. obtained by DE-VPM

Fig. 6
Fig. 6

(a) τave map, (b) a map, (c) τ2 map at the pixels showing τ2 < 100ps and a > 0.95, (d) lifetime (τ1,τ2, τave) vs a histograms showing one brighter cluster with τ1 < 100ps and 2.0 < τ2 < 4.4ns and one dimmer cluster with 100ps <τ1 < 1.2ns and 0.5 < τ2 < 2.5ns, (e) intensity vs (a,τ1, τ2) histograms indicate that the brighter pixels have shorter τ2 and higher a (suggesting Cy5 is strongly quenched).

Tables (1)

Tables Icon

Table 1 Average fitting time of 16 decays for different methods.

Equations (7)

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S( K,a, τ 1 , τ 2 )= j=1 N [ y j f( t j ) ] 2 .
S( A,B, τ 1 ,τ 2 )= A 2 j=1 N e 2 t j / τ 1 + B 2 j=1 N e 2 t j / τ 2 2A j=1 N y j e t j / τ 1 2B j=1 N y j e t j / τ 2 +2AB j=1 N e t j / τ 1 t j / τ 2 + j=1 N y j 2 =γ( τ 1 ) [ Aα( B, τ 1 , τ 2 ) ] 2 +δ( τ 1 , τ 2 ) [ Bβ( τ 1 , τ 2 ) ] 2 +η( τ 1 , τ 2 )+ j=1 N y j 2
γ( τ 1 )= j=1 N e 2 t j / τ 1 , δ( τ 1 , τ 2 )= j=1 N e 2 t j / τ 2 γ 1 ( τ 1 ) ( j=1 N e t j / τ 1 t j / τ 2 ) 2 , α( B, τ 1 , τ 2 )= γ 1 ( τ 1 )( j=1 N y j e t j / τ 1 B j=1 N e t j / τ 1 t j / τ 2 ), β( τ 1 , τ 2 )=δ ( τ 1 , τ 2 ) 1 [ j=1 N y j e t j / τ 2 γ 1 ( τ 1 )( j=1 N y j e t j / τ 1 )( j=1 N e t j / τ 1 t j / τ 2 ) ], η( τ 1 , τ 2 )=δ( τ 1 , τ 2 ) β 2 ( τ 1 , τ 2 ) γ 1 ( τ 1 ) ( j=1 N y j e t j / τ 1 ) 2 .
( τ 1 , τ 2 )= minimize τ MIN < τ 1 , τ 2 < τ MAX [ η( τ 1 , τ 2 ) ], B=β( τ 1 , τ 2 ),A=α( B, τ 1 , τ 2 ).
y( t )=I( t )f( t )+ε( t ),0tT,
y( t j )= i=1 j I( t j t i ) f( t i )+ε( t j ), j=1,2,...,N.
S( K,a, τ 1 , τ 2 )= j=1 N [ y j i=1 j I( t j t i ) f( t i ) ] 2 .

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