Abstract

Interest in time resolved flow cytometry is growing. In this paper, we collect time-resolved flow cytometry data and use it to create polar plots showing distributions that are a function of measured fluorescence decay rates from individual fluorescently-labeled cells and fluorescent microspheres. Phasor, or polar, graphics are commonly used in fluorescence lifetime imaging microscopy (FLIM). In FLIM measurements, the plotted points on a phasor graph represent the phase-shift and demodulation of the frequency-domain fluorescence signal collected by the imaging system for each image pixel. Here, we take a flow cytometry cell counting system, introduce into it frequency-domain optoelectronics, and process the data so that each point on a phasor plot represents the phase shift and demodulation of an individual cell or particle. In order to demonstrate the value of this technique, we show that phasor graphs can be used to discriminate among populations of (i) fluorescent microspheres, which are labeled with one fluorophore type; (ii) Chinese hamster ovary (CHO) cells labeled with one and two different fluorophore types; and (iii) Saccharomyces cerevisiae cells that express combinations of fluorescent proteins with different fluorescence lifetimes. The resulting phasor plots reveal differences in the fluorescence lifetimes within each sample and provide a distribution from which we can infer the number of cells expressing unique single or dual fluorescence lifetimes. These methods should facilitate analysis time resolved flow cytometry data to reveal complex fluorescence decay kinetics.

© 2016 Optical Society of America

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References

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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  5. J. A. Steinkamp and J. F. Keij, “Fluorescence intensity and lifetime measurement of free and particle-bound fluorophore in a sample stream by phase-sensitive flow cytometry,” Rev. Sci. Instrum. 70(12), 4682–4688 (1999).
    [Crossref]
  6. J. P. Houston, M. A. Naivar, P. Jenkins, and J. P. Freyer, “Capture of fluorescence decay times by flow cytometry,” Current Protocols in Cytometry, 1–21 (2012).
    [Crossref]
  7. R. Cao, M. A. Naivar, M. Wilder, and J. P. Houston, “Expanding the potential of standard flow cytometry by extracting fluorescence lifetimes from cytometric pulse shifts,” Cytometry A 85(12), 999–1010 (2014).
    [Crossref] [PubMed]
  8. W. Li, G. Vacca, M. Castillo, K. D. Houston, and J. P. Houston, “Fluorescence lifetime excitation cytometry by kinetic dithering,” Electrophoresis 35(12-13), 1846–1854 (2014).
    [Crossref] [PubMed]
  9. P. Jenkins, M. A. Naivar, and J. P. Houston, “Toward the measurement of multiple fluorescence lifetimes in flow cytometry: maximizing multi-harmonic content from cells and microspheres,” J. Biophotonics 8(11-12), 908–917 (2015).
    [Crossref] [PubMed]
  10. R. Cao, V. Pankayatselvan, and J. P. Houston, “Cytometric sorting based on the fluorescence lifetime of spectrally overlapping signals,” Opt. Express 21(12), 14816–14831 (2013).
    [Crossref] [PubMed]
  11. J. Nedbal, V. Visitkul, E. Ortiz-Zapater, G. Weitsman, P. Chana, D. R. Matthews, T. Ng, and S. M. Ameer-Beg, “Time-domain microfluidic fluorescence lifetime flow cytometry for high-throughput Förster resonance energy transfer screening,” Cytometry A 87(2), 104–118 (2015).
  12. K. M. Dean, L. M. Davis, J. L. Lubbeck, P. Manna, P. Friis, A. E. Palmer, and R. Jimenez, “High-speed multiparameter photophysical analyses of fluorophore libraries,” Anal. Chem. 87(10), 5026–5030 (2015).
    [Crossref] [PubMed]
  13. Y. Lu, J. Lu, J. Zhao, J. Cusido, F. M. Raymo, J. Yuan, S. Yang, R. C. Leif, Y. Huo, J. A. Piper, J. Paul Robinson, E. M. Goldys, and D. Jin, “On-the-fly decoding luminescence lifetimes in the microsecond region for lanthanide-encoded suspension arrays,” Nat. Commun. 5, 3741 (2014).
    [Crossref] [PubMed]
  14. B. Sands, P. Jenkins, W. J. Peria, M. Naivar, J. P. Houston, and R. Brent, “Measuring and sorting cell populations expressing isospectral fluorescent proteins with different fluorescence lifetimes,” PLoS One 9(10), e109940 (2014).
    [Crossref] [PubMed]
  15. A. V. Gohar, R. Cao, P. Jenkins, W. Li, J. P. Houston, and K. D. Houston, “Subcellular localization-dependent changes in EGFP fluorescence lifetime measured by time-resolved flow cytometry,” Biomed. Opt. Express 4(8), 1390–1400 (2013).
    [Crossref] [PubMed]
  16. H. H. Cui, J. G. Valdez, J. A. Steinkamp, and H. A. Crissman, “Fluorescence lifetime-based discrimination and quantification of cellular DNA and RNA with phase-sensitive flow cytometry,” Cytometry A 52(1), 46–55 (2003).
    [Crossref] [PubMed]
  17. J. A. Steinkamp, B. E. Lehnert, and N. M. Lehnert, “Discrimination of damaged/dead cells by propidium iodide uptake in immunofluorescently labeled populations analyzed by phase-sensitive flow cytometry,” J. Immunol. Methods 226(1-2), 59–70 (1999).
    [Crossref] [PubMed]
  18. C. Stringari, A. Cinquin, O. Cinquin, M. A. Digman, P. J. Donovan, and E. Gratton, “Phasor approach to fluorescence lifetime microscopy distinguishes different metabolic states of germ cells in a live tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(33), 13582–13587 (2011).
    [Crossref] [PubMed]
  19. F. Cutrale, A. Salih, and E. Gratton, “Spectral Phasor approach for fingerprinting of photo-activatable fluorescent proteins Dronpa, Kaede and KikGR,” Methods Appl. Fluoresc. 1(3), 035001 (2013).
    [Crossref] [PubMed]
  20. J. S. Basuki, H. T. Duong, A. Macmillan, R. B. Erlich, L. Esser, M. C. Akerfeldt, R. M. Whan, M. Kavallaris, C. Boyer, and T. P. Davis, “Using fluorescence lifetime imaging microscopy to monitor theranostic nanoparticle uptake and intracellular doxorubicin release,” ACS Nano 7(11), 10175–10189 (2013).
    [Crossref] [PubMed]
  21. D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
    [Crossref] [PubMed]
  22. C. Deka, L. S. Cram, R. Habbersett, J. C. Martin, L. A. Sklar, and J. A. Steinkamp, “Simultaneous dual-frequency phase-sensitive flow cytometric measurements for rapid identification of heterogeneous fluorescence decays in fluorochrome-labeled cells and particles,” Cytometry 21(4), 318–328 (1995).
    [Crossref] [PubMed]
  23. G. I. Redford and R. M. Clegg, “Polar plot representation for frequency-domain analysis of fluorescence lifetimes,” J. Fluoresc. 15(5), 805–815 (2005).
    [Crossref] [PubMed]
  24. M. A. Digman, V. R. Caiolfa, M. Zamai, and E. Gratton, “The phasor approach to fluorescence lifetime imaging analysis,” Biophys. J. 94(2), L14–L16 (2008).
    [Crossref] [PubMed]
  25. C. Stringari, A. Cinquin, O. Cinquin, M. A. Digman, P. J. Donovan, and E. Gratton, “Phasor approach to fluorescence lifetime microscopy distinguishes different metabolic states of germ cells in a live tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(33), 13582–13587 (2011).
    [Crossref] [PubMed]
  26. D. U. Campos-Delgado, O. G. Navarro, E. R. Arce-Santana, and J. A. Jo, “Extended output phasor representation of multi-spectral fluorescence lifetime imaging microscopy,” Biomed. Opt. Express 6(6), 2088–2105 (2015).
    [Crossref] [PubMed]
  27. H. Szmacinski, V. Toshchakov, and J. R. Lakowicz, “Application of phasor plot and autofluorescence correction for study of heterogeneous cell population,” J. Biomed. Opt. 19(4), 046017 (2014).
    [Crossref] [PubMed]
  28. R. Pepperkok, A. Squire, S. Geley, and P. I. Bastiaens, “Simultaneous detection of multiple green fluorescent proteins in live cells by fluorescence lifetime imaging microscopy,” Curr. Biol. 9(5), 269–274 (1999).
    [Crossref] [PubMed]
  29. M. Hammer, D. Schweitzer, S. Richter, and E. Königsdörffer, “Sodium fluorescein as a retinal pH indicator?” Physiol. Meas. 26(4), N9–N12 (2005).
    [Crossref] [PubMed]
  30. P. J. Verveer, A. Squire, and P. I. Bastiaens, “Global analysis of fluorescence lifetime imaging microscopy data,” Biophys. J. 78(4), 2127–2137 (2000).
    [Crossref] [PubMed]
  31. C. Deka, B. E. Lehnert, N. M. Lehnert, G. M. Jones, L. A. Sklar, and J. A. Steinkamp, “Analysis of fluorescence lifetime and quenching of FITC-conjugated antibodies on cells by phase-sensitive flow cytometry,” Cytometry 25(3), 271–279 (1996).
    [Crossref] [PubMed]
  32. D. P. Heller and C. L. Greenstock, “Fluorescence lifetime analysis of DNA intercalated ethidium bromide and quenching by free dye,” Biophys. Chem. 50(3), 305–312 (1994).
    [Crossref] [PubMed]
  33. N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
    [Crossref] [PubMed]
  34. C. Stringari, R. A. Edwards, K. T. Pate, M. L. Waterman, P. J. Donovan, and E. Gratton, “Metabolic trajectory of cellular differentiation in small intestine by Phasor Fluorescence Lifetime Microscopy of NADH,” Sci. Rep. 2, 568 (2012).
    [Crossref] [PubMed]

2015 (4)

P. Jenkins, M. A. Naivar, and J. P. Houston, “Toward the measurement of multiple fluorescence lifetimes in flow cytometry: maximizing multi-harmonic content from cells and microspheres,” J. Biophotonics 8(11-12), 908–917 (2015).
[Crossref] [PubMed]

J. Nedbal, V. Visitkul, E. Ortiz-Zapater, G. Weitsman, P. Chana, D. R. Matthews, T. Ng, and S. M. Ameer-Beg, “Time-domain microfluidic fluorescence lifetime flow cytometry for high-throughput Förster resonance energy transfer screening,” Cytometry A 87(2), 104–118 (2015).

K. M. Dean, L. M. Davis, J. L. Lubbeck, P. Manna, P. Friis, A. E. Palmer, and R. Jimenez, “High-speed multiparameter photophysical analyses of fluorophore libraries,” Anal. Chem. 87(10), 5026–5030 (2015).
[Crossref] [PubMed]

D. U. Campos-Delgado, O. G. Navarro, E. R. Arce-Santana, and J. A. Jo, “Extended output phasor representation of multi-spectral fluorescence lifetime imaging microscopy,” Biomed. Opt. Express 6(6), 2088–2105 (2015).
[Crossref] [PubMed]

2014 (5)

H. Szmacinski, V. Toshchakov, and J. R. Lakowicz, “Application of phasor plot and autofluorescence correction for study of heterogeneous cell population,” J. Biomed. Opt. 19(4), 046017 (2014).
[Crossref] [PubMed]

Y. Lu, J. Lu, J. Zhao, J. Cusido, F. M. Raymo, J. Yuan, S. Yang, R. C. Leif, Y. Huo, J. A. Piper, J. Paul Robinson, E. M. Goldys, and D. Jin, “On-the-fly decoding luminescence lifetimes in the microsecond region for lanthanide-encoded suspension arrays,” Nat. Commun. 5, 3741 (2014).
[Crossref] [PubMed]

B. Sands, P. Jenkins, W. J. Peria, M. Naivar, J. P. Houston, and R. Brent, “Measuring and sorting cell populations expressing isospectral fluorescent proteins with different fluorescence lifetimes,” PLoS One 9(10), e109940 (2014).
[Crossref] [PubMed]

R. Cao, M. A. Naivar, M. Wilder, and J. P. Houston, “Expanding the potential of standard flow cytometry by extracting fluorescence lifetimes from cytometric pulse shifts,” Cytometry A 85(12), 999–1010 (2014).
[Crossref] [PubMed]

W. Li, G. Vacca, M. Castillo, K. D. Houston, and J. P. Houston, “Fluorescence lifetime excitation cytometry by kinetic dithering,” Electrophoresis 35(12-13), 1846–1854 (2014).
[Crossref] [PubMed]

2013 (4)

R. Cao, V. Pankayatselvan, and J. P. Houston, “Cytometric sorting based on the fluorescence lifetime of spectrally overlapping signals,” Opt. Express 21(12), 14816–14831 (2013).
[Crossref] [PubMed]

A. V. Gohar, R. Cao, P. Jenkins, W. Li, J. P. Houston, and K. D. Houston, “Subcellular localization-dependent changes in EGFP fluorescence lifetime measured by time-resolved flow cytometry,” Biomed. Opt. Express 4(8), 1390–1400 (2013).
[Crossref] [PubMed]

F. Cutrale, A. Salih, and E. Gratton, “Spectral Phasor approach for fingerprinting of photo-activatable fluorescent proteins Dronpa, Kaede and KikGR,” Methods Appl. Fluoresc. 1(3), 035001 (2013).
[Crossref] [PubMed]

J. S. Basuki, H. T. Duong, A. Macmillan, R. B. Erlich, L. Esser, M. C. Akerfeldt, R. M. Whan, M. Kavallaris, C. Boyer, and T. P. Davis, “Using fluorescence lifetime imaging microscopy to monitor theranostic nanoparticle uptake and intracellular doxorubicin release,” ACS Nano 7(11), 10175–10189 (2013).
[Crossref] [PubMed]

2012 (1)

C. Stringari, R. A. Edwards, K. T. Pate, M. L. Waterman, P. J. Donovan, and E. Gratton, “Metabolic trajectory of cellular differentiation in small intestine by Phasor Fluorescence Lifetime Microscopy of NADH,” Sci. Rep. 2, 568 (2012).
[Crossref] [PubMed]

2011 (2)

C. Stringari, A. Cinquin, O. Cinquin, M. A. Digman, P. J. Donovan, and E. Gratton, “Phasor approach to fluorescence lifetime microscopy distinguishes different metabolic states of germ cells in a live tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(33), 13582–13587 (2011).
[Crossref] [PubMed]

C. Stringari, A. Cinquin, O. Cinquin, M. A. Digman, P. J. Donovan, and E. Gratton, “Phasor approach to fluorescence lifetime microscopy distinguishes different metabolic states of germ cells in a live tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(33), 13582–13587 (2011).
[Crossref] [PubMed]

2010 (1)

J. P. Houston, M. A. Naivar, and J. P. Freyer, “Digital analysis and sorting of fluorescence lifetime by flow cytometry,” Cytometry A 77(9), 861–872 (2010).
[Crossref] [PubMed]

2008 (1)

M. A. Digman, V. R. Caiolfa, M. Zamai, and E. Gratton, “The phasor approach to fluorescence lifetime imaging analysis,” Biophys. J. 94(2), L14–L16 (2008).
[Crossref] [PubMed]

2007 (2)

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
[Crossref] [PubMed]

2005 (2)

G. I. Redford and R. M. Clegg, “Polar plot representation for frequency-domain analysis of fluorescence lifetimes,” J. Fluoresc. 15(5), 805–815 (2005).
[Crossref] [PubMed]

M. Hammer, D. Schweitzer, S. Richter, and E. Königsdörffer, “Sodium fluorescein as a retinal pH indicator?” Physiol. Meas. 26(4), N9–N12 (2005).
[Crossref] [PubMed]

2003 (1)

H. H. Cui, J. G. Valdez, J. A. Steinkamp, and H. A. Crissman, “Fluorescence lifetime-based discrimination and quantification of cellular DNA and RNA with phase-sensitive flow cytometry,” Cytometry A 52(1), 46–55 (2003).
[Crossref] [PubMed]

2000 (1)

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

1999 (3)

R. Pepperkok, A. Squire, S. Geley, and P. I. Bastiaens, “Simultaneous detection of multiple green fluorescent proteins in live cells by fluorescence lifetime imaging microscopy,” Curr. Biol. 9(5), 269–274 (1999).
[Crossref] [PubMed]

J. A. Steinkamp, B. E. Lehnert, and N. M. Lehnert, “Discrimination of damaged/dead cells by propidium iodide uptake in immunofluorescently labeled populations analyzed by phase-sensitive flow cytometry,” J. Immunol. Methods 226(1-2), 59–70 (1999).
[Crossref] [PubMed]

J. A. Steinkamp and J. F. Keij, “Fluorescence intensity and lifetime measurement of free and particle-bound fluorophore in a sample stream by phase-sensitive flow cytometry,” Rev. Sci. Instrum. 70(12), 4682–4688 (1999).
[Crossref]

1996 (1)

C. Deka, B. E. Lehnert, N. M. Lehnert, G. M. Jones, L. A. Sklar, and J. A. Steinkamp, “Analysis of fluorescence lifetime and quenching of FITC-conjugated antibodies on cells by phase-sensitive flow cytometry,” Cytometry 25(3), 271–279 (1996).
[Crossref] [PubMed]

1995 (1)

C. Deka, L. S. Cram, R. Habbersett, J. C. Martin, L. A. Sklar, and J. A. Steinkamp, “Simultaneous dual-frequency phase-sensitive flow cytometric measurements for rapid identification of heterogeneous fluorescence decays in fluorochrome-labeled cells and particles,” Cytometry 21(4), 318–328 (1995).
[Crossref] [PubMed]

1994 (1)

D. P. Heller and C. L. Greenstock, “Fluorescence lifetime analysis of DNA intercalated ethidium bromide and quenching by free dye,” Biophys. Chem. 50(3), 305–312 (1994).
[Crossref] [PubMed]

1993 (2)

J. A. Steinkamp and H. A. Crissman, “Resolution of fluorescence signals from cells labeled with fluorochromes having different lifetimes by phase-sensitive flow cytometry,” Cytometry 14(2), 210–216 (1993).
[Crossref] [PubMed]

B. G. Pinsky, J. J. Ladasky, J. R. Lakowicz, K. Berndt, and R. A. Hoffman, “Phase-resolved fluorescence lifetime measurements for flow cytometry,” Cytometry 14(2), 123–135 (1993).
[Crossref] [PubMed]

Akerfeldt, M. C.

J. S. Basuki, H. T. Duong, A. Macmillan, R. B. Erlich, L. Esser, M. C. Akerfeldt, R. M. Whan, M. Kavallaris, C. Boyer, and T. P. Davis, “Using fluorescence lifetime imaging microscopy to monitor theranostic nanoparticle uptake and intracellular doxorubicin release,” ACS Nano 7(11), 10175–10189 (2013).
[Crossref] [PubMed]

Ameer-Beg, S. M.

J. Nedbal, V. Visitkul, E. Ortiz-Zapater, G. Weitsman, P. Chana, D. R. Matthews, T. Ng, and S. M. Ameer-Beg, “Time-domain microfluidic fluorescence lifetime flow cytometry for high-throughput Förster resonance energy transfer screening,” Cytometry A 87(2), 104–118 (2015).

Ameloot, M.

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

Arce-Santana, E. R.

Basaric, N.

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

Bastiaens, P. I.

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

R. Pepperkok, A. Squire, S. Geley, and P. I. Bastiaens, “Simultaneous detection of multiple green fluorescent proteins in live cells by fluorescence lifetime imaging microscopy,” Curr. Biol. 9(5), 269–274 (1999).
[Crossref] [PubMed]

Basuki, J. S.

J. S. Basuki, H. T. Duong, A. Macmillan, R. B. Erlich, L. Esser, M. C. Akerfeldt, R. M. Whan, M. Kavallaris, C. Boyer, and T. P. Davis, “Using fluorescence lifetime imaging microscopy to monitor theranostic nanoparticle uptake and intracellular doxorubicin release,” ACS Nano 7(11), 10175–10189 (2013).
[Crossref] [PubMed]

Becker, W.

D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
[Crossref] [PubMed]

Bergmann, A.

D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
[Crossref] [PubMed]

Berndt, K.

B. G. Pinsky, J. J. Ladasky, J. R. Lakowicz, K. Berndt, and R. A. Hoffman, “Phase-resolved fluorescence lifetime measurements for flow cytometry,” Cytometry 14(2), 123–135 (1993).
[Crossref] [PubMed]

Birckner, E.

D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
[Crossref] [PubMed]

Boens, N.

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

Boyer, C.

J. S. Basuki, H. T. Duong, A. Macmillan, R. B. Erlich, L. Esser, M. C. Akerfeldt, R. M. Whan, M. Kavallaris, C. Boyer, and T. P. Davis, “Using fluorescence lifetime imaging microscopy to monitor theranostic nanoparticle uptake and intracellular doxorubicin release,” ACS Nano 7(11), 10175–10189 (2013).
[Crossref] [PubMed]

Brent, R.

B. Sands, P. Jenkins, W. J. Peria, M. Naivar, J. P. Houston, and R. Brent, “Measuring and sorting cell populations expressing isospectral fluorescent proteins with different fluorescence lifetimes,” PLoS One 9(10), e109940 (2014).
[Crossref] [PubMed]

Caiolfa, V. R.

M. A. Digman, V. R. Caiolfa, M. Zamai, and E. Gratton, “The phasor approach to fluorescence lifetime imaging analysis,” Biophys. J. 94(2), L14–L16 (2008).
[Crossref] [PubMed]

Campos-Delgado, D. U.

Cao, R.

Castillo, M.

W. Li, G. Vacca, M. Castillo, K. D. Houston, and J. P. Houston, “Fluorescence lifetime excitation cytometry by kinetic dithering,” Electrophoresis 35(12-13), 1846–1854 (2014).
[Crossref] [PubMed]

Chana, P.

J. Nedbal, V. Visitkul, E. Ortiz-Zapater, G. Weitsman, P. Chana, D. R. Matthews, T. Ng, and S. M. Ameer-Beg, “Time-domain microfluidic fluorescence lifetime flow cytometry for high-throughput Förster resonance energy transfer screening,” Cytometry A 87(2), 104–118 (2015).

Cinquin, A.

C. Stringari, A. Cinquin, O. Cinquin, M. A. Digman, P. J. Donovan, and E. Gratton, “Phasor approach to fluorescence lifetime microscopy distinguishes different metabolic states of germ cells in a live tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(33), 13582–13587 (2011).
[Crossref] [PubMed]

C. Stringari, A. Cinquin, O. Cinquin, M. A. Digman, P. J. Donovan, and E. Gratton, “Phasor approach to fluorescence lifetime microscopy distinguishes different metabolic states of germ cells in a live tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(33), 13582–13587 (2011).
[Crossref] [PubMed]

Cinquin, O.

C. Stringari, A. Cinquin, O. Cinquin, M. A. Digman, P. J. Donovan, and E. Gratton, “Phasor approach to fluorescence lifetime microscopy distinguishes different metabolic states of germ cells in a live tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(33), 13582–13587 (2011).
[Crossref] [PubMed]

C. Stringari, A. Cinquin, O. Cinquin, M. A. Digman, P. J. Donovan, and E. Gratton, “Phasor approach to fluorescence lifetime microscopy distinguishes different metabolic states of germ cells in a live tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(33), 13582–13587 (2011).
[Crossref] [PubMed]

Clegg, R. M.

G. I. Redford and R. M. Clegg, “Polar plot representation for frequency-domain analysis of fluorescence lifetimes,” J. Fluoresc. 15(5), 805–815 (2005).
[Crossref] [PubMed]

Cram, L. S.

C. Deka, L. S. Cram, R. Habbersett, J. C. Martin, L. A. Sklar, and J. A. Steinkamp, “Simultaneous dual-frequency phase-sensitive flow cytometric measurements for rapid identification of heterogeneous fluorescence decays in fluorochrome-labeled cells and particles,” Cytometry 21(4), 318–328 (1995).
[Crossref] [PubMed]

Crissman, H. A.

H. H. Cui, J. G. Valdez, J. A. Steinkamp, and H. A. Crissman, “Fluorescence lifetime-based discrimination and quantification of cellular DNA and RNA with phase-sensitive flow cytometry,” Cytometry A 52(1), 46–55 (2003).
[Crossref] [PubMed]

J. A. Steinkamp and H. A. Crissman, “Resolution of fluorescence signals from cells labeled with fluorochromes having different lifetimes by phase-sensitive flow cytometry,” Cytometry 14(2), 210–216 (1993).
[Crossref] [PubMed]

Cui, H. H.

H. H. Cui, J. G. Valdez, J. A. Steinkamp, and H. A. Crissman, “Fluorescence lifetime-based discrimination and quantification of cellular DNA and RNA with phase-sensitive flow cytometry,” Cytometry A 52(1), 46–55 (2003).
[Crossref] [PubMed]

Cusido, J.

Y. Lu, J. Lu, J. Zhao, J. Cusido, F. M. Raymo, J. Yuan, S. Yang, R. C. Leif, Y. Huo, J. A. Piper, J. Paul Robinson, E. M. Goldys, and D. Jin, “On-the-fly decoding luminescence lifetimes in the microsecond region for lanthanide-encoded suspension arrays,” Nat. Commun. 5, 3741 (2014).
[Crossref] [PubMed]

Cutrale, F.

F. Cutrale, A. Salih, and E. Gratton, “Spectral Phasor approach for fingerprinting of photo-activatable fluorescent proteins Dronpa, Kaede and KikGR,” Methods Appl. Fluoresc. 1(3), 035001 (2013).
[Crossref] [PubMed]

Davis, L. M.

K. M. Dean, L. M. Davis, J. L. Lubbeck, P. Manna, P. Friis, A. E. Palmer, and R. Jimenez, “High-speed multiparameter photophysical analyses of fluorophore libraries,” Anal. Chem. 87(10), 5026–5030 (2015).
[Crossref] [PubMed]

Davis, T. P.

J. S. Basuki, H. T. Duong, A. Macmillan, R. B. Erlich, L. Esser, M. C. Akerfeldt, R. M. Whan, M. Kavallaris, C. Boyer, and T. P. Davis, “Using fluorescence lifetime imaging microscopy to monitor theranostic nanoparticle uptake and intracellular doxorubicin release,” ACS Nano 7(11), 10175–10189 (2013).
[Crossref] [PubMed]

Dean, K. M.

K. M. Dean, L. M. Davis, J. L. Lubbeck, P. Manna, P. Friis, A. E. Palmer, and R. Jimenez, “High-speed multiparameter photophysical analyses of fluorophore libraries,” Anal. Chem. 87(10), 5026–5030 (2015).
[Crossref] [PubMed]

Deka, C.

C. Deka, B. E. Lehnert, N. M. Lehnert, G. M. Jones, L. A. Sklar, and J. A. Steinkamp, “Analysis of fluorescence lifetime and quenching of FITC-conjugated antibodies on cells by phase-sensitive flow cytometry,” Cytometry 25(3), 271–279 (1996).
[Crossref] [PubMed]

C. Deka, L. S. Cram, R. Habbersett, J. C. Martin, L. A. Sklar, and J. A. Steinkamp, “Simultaneous dual-frequency phase-sensitive flow cytometric measurements for rapid identification of heterogeneous fluorescence decays in fluorochrome-labeled cells and particles,” Cytometry 21(4), 318–328 (1995).
[Crossref] [PubMed]

Digman, M. A.

C. Stringari, A. Cinquin, O. Cinquin, M. A. Digman, P. J. Donovan, and E. Gratton, “Phasor approach to fluorescence lifetime microscopy distinguishes different metabolic states of germ cells in a live tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(33), 13582–13587 (2011).
[Crossref] [PubMed]

C. Stringari, A. Cinquin, O. Cinquin, M. A. Digman, P. J. Donovan, and E. Gratton, “Phasor approach to fluorescence lifetime microscopy distinguishes different metabolic states of germ cells in a live tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(33), 13582–13587 (2011).
[Crossref] [PubMed]

M. A. Digman, V. R. Caiolfa, M. Zamai, and E. Gratton, “The phasor approach to fluorescence lifetime imaging analysis,” Biophys. J. 94(2), L14–L16 (2008).
[Crossref] [PubMed]

Donovan, P. J.

C. Stringari, R. A. Edwards, K. T. Pate, M. L. Waterman, P. J. Donovan, and E. Gratton, “Metabolic trajectory of cellular differentiation in small intestine by Phasor Fluorescence Lifetime Microscopy of NADH,” Sci. Rep. 2, 568 (2012).
[Crossref] [PubMed]

C. Stringari, A. Cinquin, O. Cinquin, M. A. Digman, P. J. Donovan, and E. Gratton, “Phasor approach to fluorescence lifetime microscopy distinguishes different metabolic states of germ cells in a live tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(33), 13582–13587 (2011).
[Crossref] [PubMed]

C. Stringari, A. Cinquin, O. Cinquin, M. A. Digman, P. J. Donovan, and E. Gratton, “Phasor approach to fluorescence lifetime microscopy distinguishes different metabolic states of germ cells in a live tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(33), 13582–13587 (2011).
[Crossref] [PubMed]

Duong, H. T.

J. S. Basuki, H. T. Duong, A. Macmillan, R. B. Erlich, L. Esser, M. C. Akerfeldt, R. M. Whan, M. Kavallaris, C. Boyer, and T. P. Davis, “Using fluorescence lifetime imaging microscopy to monitor theranostic nanoparticle uptake and intracellular doxorubicin release,” ACS Nano 7(11), 10175–10189 (2013).
[Crossref] [PubMed]

Edwards, R. A.

C. Stringari, R. A. Edwards, K. T. Pate, M. L. Waterman, P. J. Donovan, and E. Gratton, “Metabolic trajectory of cellular differentiation in small intestine by Phasor Fluorescence Lifetime Microscopy of NADH,” Sci. Rep. 2, 568 (2012).
[Crossref] [PubMed]

Engelborghs, Y.

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

Erlich, R. B.

J. S. Basuki, H. T. Duong, A. Macmillan, R. B. Erlich, L. Esser, M. C. Akerfeldt, R. M. Whan, M. Kavallaris, C. Boyer, and T. P. Davis, “Using fluorescence lifetime imaging microscopy to monitor theranostic nanoparticle uptake and intracellular doxorubicin release,” ACS Nano 7(11), 10175–10189 (2013).
[Crossref] [PubMed]

Esser, L.

J. S. Basuki, H. T. Duong, A. Macmillan, R. B. Erlich, L. Esser, M. C. Akerfeldt, R. M. Whan, M. Kavallaris, C. Boyer, and T. P. Davis, “Using fluorescence lifetime imaging microscopy to monitor theranostic nanoparticle uptake and intracellular doxorubicin release,” ACS Nano 7(11), 10175–10189 (2013).
[Crossref] [PubMed]

Freyer, J. P.

J. P. Houston, M. A. Naivar, and J. P. Freyer, “Digital analysis and sorting of fluorescence lifetime by flow cytometry,” Cytometry A 77(9), 861–872 (2010).
[Crossref] [PubMed]

Friis, P.

K. M. Dean, L. M. Davis, J. L. Lubbeck, P. Manna, P. Friis, A. E. Palmer, and R. Jimenez, “High-speed multiparameter photophysical analyses of fluorophore libraries,” Anal. Chem. 87(10), 5026–5030 (2015).
[Crossref] [PubMed]

Geley, S.

R. Pepperkok, A. Squire, S. Geley, and P. I. Bastiaens, “Simultaneous detection of multiple green fluorescent proteins in live cells by fluorescence lifetime imaging microscopy,” Curr. Biol. 9(5), 269–274 (1999).
[Crossref] [PubMed]

Gohar, A. V.

Goldys, E. M.

Y. Lu, J. Lu, J. Zhao, J. Cusido, F. M. Raymo, J. Yuan, S. Yang, R. C. Leif, Y. Huo, J. A. Piper, J. Paul Robinson, E. M. Goldys, and D. Jin, “On-the-fly decoding luminescence lifetimes in the microsecond region for lanthanide-encoded suspension arrays,” Nat. Commun. 5, 3741 (2014).
[Crossref] [PubMed]

Gratton, E.

F. Cutrale, A. Salih, and E. Gratton, “Spectral Phasor approach for fingerprinting of photo-activatable fluorescent proteins Dronpa, Kaede and KikGR,” Methods Appl. Fluoresc. 1(3), 035001 (2013).
[Crossref] [PubMed]

C. Stringari, R. A. Edwards, K. T. Pate, M. L. Waterman, P. J. Donovan, and E. Gratton, “Metabolic trajectory of cellular differentiation in small intestine by Phasor Fluorescence Lifetime Microscopy of NADH,” Sci. Rep. 2, 568 (2012).
[Crossref] [PubMed]

C. Stringari, A. Cinquin, O. Cinquin, M. A. Digman, P. J. Donovan, and E. Gratton, “Phasor approach to fluorescence lifetime microscopy distinguishes different metabolic states of germ cells in a live tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(33), 13582–13587 (2011).
[Crossref] [PubMed]

C. Stringari, A. Cinquin, O. Cinquin, M. A. Digman, P. J. Donovan, and E. Gratton, “Phasor approach to fluorescence lifetime microscopy distinguishes different metabolic states of germ cells in a live tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(33), 13582–13587 (2011).
[Crossref] [PubMed]

M. A. Digman, V. R. Caiolfa, M. Zamai, and E. Gratton, “The phasor approach to fluorescence lifetime imaging analysis,” Biophys. J. 94(2), L14–L16 (2008).
[Crossref] [PubMed]

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

Greenstock, C. L.

D. P. Heller and C. L. Greenstock, “Fluorescence lifetime analysis of DNA intercalated ethidium bromide and quenching by free dye,” Biophys. Chem. 50(3), 305–312 (1994).
[Crossref] [PubMed]

Gryczynski, I.

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

Habbersett, R.

C. Deka, L. S. Cram, R. Habbersett, J. C. Martin, L. A. Sklar, and J. A. Steinkamp, “Simultaneous dual-frequency phase-sensitive flow cytometric measurements for rapid identification of heterogeneous fluorescence decays in fluorochrome-labeled cells and particles,” Cytometry 21(4), 318–328 (1995).
[Crossref] [PubMed]

Hammer, M.

D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
[Crossref] [PubMed]

M. Hammer, D. Schweitzer, S. Richter, and E. Königsdörffer, “Sodium fluorescein as a retinal pH indicator?” Physiol. Meas. 26(4), N9–N12 (2005).
[Crossref] [PubMed]

Heller, D. P.

D. P. Heller and C. L. Greenstock, “Fluorescence lifetime analysis of DNA intercalated ethidium bromide and quenching by free dye,” Biophys. Chem. 50(3), 305–312 (1994).
[Crossref] [PubMed]

Hoffman, R. A.

B. G. Pinsky, J. J. Ladasky, J. R. Lakowicz, K. Berndt, and R. A. Hoffman, “Phase-resolved fluorescence lifetime measurements for flow cytometry,” Cytometry 14(2), 123–135 (1993).
[Crossref] [PubMed]

Hofkens, J.

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

Houston, J. P.

P. Jenkins, M. A. Naivar, and J. P. Houston, “Toward the measurement of multiple fluorescence lifetimes in flow cytometry: maximizing multi-harmonic content from cells and microspheres,” J. Biophotonics 8(11-12), 908–917 (2015).
[Crossref] [PubMed]

W. Li, G. Vacca, M. Castillo, K. D. Houston, and J. P. Houston, “Fluorescence lifetime excitation cytometry by kinetic dithering,” Electrophoresis 35(12-13), 1846–1854 (2014).
[Crossref] [PubMed]

R. Cao, M. A. Naivar, M. Wilder, and J. P. Houston, “Expanding the potential of standard flow cytometry by extracting fluorescence lifetimes from cytometric pulse shifts,” Cytometry A 85(12), 999–1010 (2014).
[Crossref] [PubMed]

B. Sands, P. Jenkins, W. J. Peria, M. Naivar, J. P. Houston, and R. Brent, “Measuring and sorting cell populations expressing isospectral fluorescent proteins with different fluorescence lifetimes,” PLoS One 9(10), e109940 (2014).
[Crossref] [PubMed]

R. Cao, V. Pankayatselvan, and J. P. Houston, “Cytometric sorting based on the fluorescence lifetime of spectrally overlapping signals,” Opt. Express 21(12), 14816–14831 (2013).
[Crossref] [PubMed]

A. V. Gohar, R. Cao, P. Jenkins, W. Li, J. P. Houston, and K. D. Houston, “Subcellular localization-dependent changes in EGFP fluorescence lifetime measured by time-resolved flow cytometry,” Biomed. Opt. Express 4(8), 1390–1400 (2013).
[Crossref] [PubMed]

J. P. Houston, M. A. Naivar, and J. P. Freyer, “Digital analysis and sorting of fluorescence lifetime by flow cytometry,” Cytometry A 77(9), 861–872 (2010).
[Crossref] [PubMed]

Houston, K. D.

Huo, Y.

Y. Lu, J. Lu, J. Zhao, J. Cusido, F. M. Raymo, J. Yuan, S. Yang, R. C. Leif, Y. Huo, J. A. Piper, J. Paul Robinson, E. M. Goldys, and D. Jin, “On-the-fly decoding luminescence lifetimes in the microsecond region for lanthanide-encoded suspension arrays,” Nat. Commun. 5, 3741 (2014).
[Crossref] [PubMed]

Jenkins, P.

P. Jenkins, M. A. Naivar, and J. P. Houston, “Toward the measurement of multiple fluorescence lifetimes in flow cytometry: maximizing multi-harmonic content from cells and microspheres,” J. Biophotonics 8(11-12), 908–917 (2015).
[Crossref] [PubMed]

B. Sands, P. Jenkins, W. J. Peria, M. Naivar, J. P. Houston, and R. Brent, “Measuring and sorting cell populations expressing isospectral fluorescent proteins with different fluorescence lifetimes,” PLoS One 9(10), e109940 (2014).
[Crossref] [PubMed]

A. V. Gohar, R. Cao, P. Jenkins, W. Li, J. P. Houston, and K. D. Houston, “Subcellular localization-dependent changes in EGFP fluorescence lifetime measured by time-resolved flow cytometry,” Biomed. Opt. Express 4(8), 1390–1400 (2013).
[Crossref] [PubMed]

Jentsch, S.

D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
[Crossref] [PubMed]

Jimenez, R.

K. M. Dean, L. M. Davis, J. L. Lubbeck, P. Manna, P. Friis, A. E. Palmer, and R. Jimenez, “High-speed multiparameter photophysical analyses of fluorophore libraries,” Anal. Chem. 87(10), 5026–5030 (2015).
[Crossref] [PubMed]

Jin, D.

Y. Lu, J. Lu, J. Zhao, J. Cusido, F. M. Raymo, J. Yuan, S. Yang, R. C. Leif, Y. Huo, J. A. Piper, J. Paul Robinson, E. M. Goldys, and D. Jin, “On-the-fly decoding luminescence lifetimes in the microsecond region for lanthanide-encoded suspension arrays,” Nat. Commun. 5, 3741 (2014).
[Crossref] [PubMed]

Jo, J. A.

Jones, G. M.

C. Deka, B. E. Lehnert, N. M. Lehnert, G. M. Jones, L. A. Sklar, and J. A. Steinkamp, “Analysis of fluorescence lifetime and quenching of FITC-conjugated antibodies on cells by phase-sensitive flow cytometry,” Cytometry 25(3), 271–279 (1996).
[Crossref] [PubMed]

Kavallaris, M.

J. S. Basuki, H. T. Duong, A. Macmillan, R. B. Erlich, L. Esser, M. C. Akerfeldt, R. M. Whan, M. Kavallaris, C. Boyer, and T. P. Davis, “Using fluorescence lifetime imaging microscopy to monitor theranostic nanoparticle uptake and intracellular doxorubicin release,” ACS Nano 7(11), 10175–10189 (2013).
[Crossref] [PubMed]

Keij, J. F.

J. A. Steinkamp and J. F. Keij, “Fluorescence intensity and lifetime measurement of free and particle-bound fluorophore in a sample stream by phase-sensitive flow cytometry,” Rev. Sci. Instrum. 70(12), 4682–4688 (1999).
[Crossref]

Königsdörffer, E.

M. Hammer, D. Schweitzer, S. Richter, and E. Königsdörffer, “Sodium fluorescein as a retinal pH indicator?” Physiol. Meas. 26(4), N9–N12 (2005).
[Crossref] [PubMed]

Krajcarski, D. T.

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

Ladasky, J. J.

B. G. Pinsky, J. J. Ladasky, J. R. Lakowicz, K. Berndt, and R. A. Hoffman, “Phase-resolved fluorescence lifetime measurements for flow cytometry,” Cytometry 14(2), 123–135 (1993).
[Crossref] [PubMed]

Lakowicz, J. R.

H. Szmacinski, V. Toshchakov, and J. R. Lakowicz, “Application of phasor plot and autofluorescence correction for study of heterogeneous cell population,” J. Biomed. Opt. 19(4), 046017 (2014).
[Crossref] [PubMed]

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

B. G. Pinsky, J. J. Ladasky, J. R. Lakowicz, K. Berndt, and R. A. Hoffman, “Phase-resolved fluorescence lifetime measurements for flow cytometry,” Cytometry 14(2), 123–135 (1993).
[Crossref] [PubMed]

Lefèvre, J.-P.

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

Lehnert, B. E.

J. A. Steinkamp, B. E. Lehnert, and N. M. Lehnert, “Discrimination of damaged/dead cells by propidium iodide uptake in immunofluorescently labeled populations analyzed by phase-sensitive flow cytometry,” J. Immunol. Methods 226(1-2), 59–70 (1999).
[Crossref] [PubMed]

C. Deka, B. E. Lehnert, N. M. Lehnert, G. M. Jones, L. A. Sklar, and J. A. Steinkamp, “Analysis of fluorescence lifetime and quenching of FITC-conjugated antibodies on cells by phase-sensitive flow cytometry,” Cytometry 25(3), 271–279 (1996).
[Crossref] [PubMed]

Lehnert, N. M.

J. A. Steinkamp, B. E. Lehnert, and N. M. Lehnert, “Discrimination of damaged/dead cells by propidium iodide uptake in immunofluorescently labeled populations analyzed by phase-sensitive flow cytometry,” J. Immunol. Methods 226(1-2), 59–70 (1999).
[Crossref] [PubMed]

C. Deka, B. E. Lehnert, N. M. Lehnert, G. M. Jones, L. A. Sklar, and J. A. Steinkamp, “Analysis of fluorescence lifetime and quenching of FITC-conjugated antibodies on cells by phase-sensitive flow cytometry,” Cytometry 25(3), 271–279 (1996).
[Crossref] [PubMed]

Leif, R. C.

Y. Lu, J. Lu, J. Zhao, J. Cusido, F. M. Raymo, J. Yuan, S. Yang, R. C. Leif, Y. Huo, J. A. Piper, J. Paul Robinson, E. M. Goldys, and D. Jin, “On-the-fly decoding luminescence lifetimes in the microsecond region for lanthanide-encoded suspension arrays,” Nat. Commun. 5, 3741 (2014).
[Crossref] [PubMed]

Li, W.

Lu, J.

Y. Lu, J. Lu, J. Zhao, J. Cusido, F. M. Raymo, J. Yuan, S. Yang, R. C. Leif, Y. Huo, J. A. Piper, J. Paul Robinson, E. M. Goldys, and D. Jin, “On-the-fly decoding luminescence lifetimes in the microsecond region for lanthanide-encoded suspension arrays,” Nat. Commun. 5, 3741 (2014).
[Crossref] [PubMed]

Lu, Y.

Y. Lu, J. Lu, J. Zhao, J. Cusido, F. M. Raymo, J. Yuan, S. Yang, R. C. Leif, Y. Huo, J. A. Piper, J. Paul Robinson, E. M. Goldys, and D. Jin, “On-the-fly decoding luminescence lifetimes in the microsecond region for lanthanide-encoded suspension arrays,” Nat. Commun. 5, 3741 (2014).
[Crossref] [PubMed]

Lubbeck, J. L.

K. M. Dean, L. M. Davis, J. L. Lubbeck, P. Manna, P. Friis, A. E. Palmer, and R. Jimenez, “High-speed multiparameter photophysical analyses of fluorophore libraries,” Anal. Chem. 87(10), 5026–5030 (2015).
[Crossref] [PubMed]

Macmillan, A.

J. S. Basuki, H. T. Duong, A. Macmillan, R. B. Erlich, L. Esser, M. C. Akerfeldt, R. M. Whan, M. Kavallaris, C. Boyer, and T. P. Davis, “Using fluorescence lifetime imaging microscopy to monitor theranostic nanoparticle uptake and intracellular doxorubicin release,” ACS Nano 7(11), 10175–10189 (2013).
[Crossref] [PubMed]

Malak, H.

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

Manna, P.

K. M. Dean, L. M. Davis, J. L. Lubbeck, P. Manna, P. Friis, A. E. Palmer, and R. Jimenez, “High-speed multiparameter photophysical analyses of fluorophore libraries,” Anal. Chem. 87(10), 5026–5030 (2015).
[Crossref] [PubMed]

Martin, J. C.

C. Deka, L. S. Cram, R. Habbersett, J. C. Martin, L. A. Sklar, and J. A. Steinkamp, “Simultaneous dual-frequency phase-sensitive flow cytometric measurements for rapid identification of heterogeneous fluorescence decays in fluorochrome-labeled cells and particles,” Cytometry 21(4), 318–328 (1995).
[Crossref] [PubMed]

Matthews, D. R.

J. Nedbal, V. Visitkul, E. Ortiz-Zapater, G. Weitsman, P. Chana, D. R. Matthews, T. Ng, and S. M. Ameer-Beg, “Time-domain microfluidic fluorescence lifetime flow cytometry for high-throughput Förster resonance energy transfer screening,” Cytometry A 87(2), 104–118 (2015).

Miura, A.

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

Naivar, M.

B. Sands, P. Jenkins, W. J. Peria, M. Naivar, J. P. Houston, and R. Brent, “Measuring and sorting cell populations expressing isospectral fluorescent proteins with different fluorescence lifetimes,” PLoS One 9(10), e109940 (2014).
[Crossref] [PubMed]

Naivar, M. A.

P. Jenkins, M. A. Naivar, and J. P. Houston, “Toward the measurement of multiple fluorescence lifetimes in flow cytometry: maximizing multi-harmonic content from cells and microspheres,” J. Biophotonics 8(11-12), 908–917 (2015).
[Crossref] [PubMed]

R. Cao, M. A. Naivar, M. Wilder, and J. P. Houston, “Expanding the potential of standard flow cytometry by extracting fluorescence lifetimes from cytometric pulse shifts,” Cytometry A 85(12), 999–1010 (2014).
[Crossref] [PubMed]

J. P. Houston, M. A. Naivar, and J. P. Freyer, “Digital analysis and sorting of fluorescence lifetime by flow cytometry,” Cytometry A 77(9), 861–872 (2010).
[Crossref] [PubMed]

Navarro, O. G.

Nedbal, J.

J. Nedbal, V. Visitkul, E. Ortiz-Zapater, G. Weitsman, P. Chana, D. R. Matthews, T. Ng, and S. M. Ameer-Beg, “Time-domain microfluidic fluorescence lifetime flow cytometry for high-throughput Förster resonance energy transfer screening,” Cytometry A 87(2), 104–118 (2015).

Ng, T.

J. Nedbal, V. Visitkul, E. Ortiz-Zapater, G. Weitsman, P. Chana, D. R. Matthews, T. Ng, and S. M. Ameer-Beg, “Time-domain microfluidic fluorescence lifetime flow cytometry for high-throughput Förster resonance energy transfer screening,” Cytometry A 87(2), 104–118 (2015).

Ortiz-Zapater, E.

J. Nedbal, V. Visitkul, E. Ortiz-Zapater, G. Weitsman, P. Chana, D. R. Matthews, T. Ng, and S. M. Ameer-Beg, “Time-domain microfluidic fluorescence lifetime flow cytometry for high-throughput Förster resonance energy transfer screening,” Cytometry A 87(2), 104–118 (2015).

Palmer, A. E.

K. M. Dean, L. M. Davis, J. L. Lubbeck, P. Manna, P. Friis, A. E. Palmer, and R. Jimenez, “High-speed multiparameter photophysical analyses of fluorophore libraries,” Anal. Chem. 87(10), 5026–5030 (2015).
[Crossref] [PubMed]

Pankayatselvan, V.

Pate, K. T.

C. Stringari, R. A. Edwards, K. T. Pate, M. L. Waterman, P. J. Donovan, and E. Gratton, “Metabolic trajectory of cellular differentiation in small intestine by Phasor Fluorescence Lifetime Microscopy of NADH,” Sci. Rep. 2, 568 (2012).
[Crossref] [PubMed]

Paul Robinson, J.

Y. Lu, J. Lu, J. Zhao, J. Cusido, F. M. Raymo, J. Yuan, S. Yang, R. C. Leif, Y. Huo, J. A. Piper, J. Paul Robinson, E. M. Goldys, and D. Jin, “On-the-fly decoding luminescence lifetimes in the microsecond region for lanthanide-encoded suspension arrays,” Nat. Commun. 5, 3741 (2014).
[Crossref] [PubMed]

Pepperkok, R.

R. Pepperkok, A. Squire, S. Geley, and P. I. Bastiaens, “Simultaneous detection of multiple green fluorescent proteins in live cells by fluorescence lifetime imaging microscopy,” Curr. Biol. 9(5), 269–274 (1999).
[Crossref] [PubMed]

Peria, W. J.

B. Sands, P. Jenkins, W. J. Peria, M. Naivar, J. P. Houston, and R. Brent, “Measuring and sorting cell populations expressing isospectral fluorescent proteins with different fluorescence lifetimes,” PLoS One 9(10), e109940 (2014).
[Crossref] [PubMed]

Phillips, D.

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

Pinsky, B. G.

B. G. Pinsky, J. J. Ladasky, J. R. Lakowicz, K. Berndt, and R. A. Hoffman, “Phase-resolved fluorescence lifetime measurements for flow cytometry,” Cytometry 14(2), 123–135 (1993).
[Crossref] [PubMed]

Piper, J. A.

Y. Lu, J. Lu, J. Zhao, J. Cusido, F. M. Raymo, J. Yuan, S. Yang, R. C. Leif, Y. Huo, J. A. Piper, J. Paul Robinson, E. M. Goldys, and D. Jin, “On-the-fly decoding luminescence lifetimes in the microsecond region for lanthanide-encoded suspension arrays,” Nat. Commun. 5, 3741 (2014).
[Crossref] [PubMed]

Pouget, J.

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

Qin, W.

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

Raymo, F. M.

Y. Lu, J. Lu, J. Zhao, J. Cusido, F. M. Raymo, J. Yuan, S. Yang, R. C. Leif, Y. Huo, J. A. Piper, J. Paul Robinson, E. M. Goldys, and D. Jin, “On-the-fly decoding luminescence lifetimes in the microsecond region for lanthanide-encoded suspension arrays,” Nat. Commun. 5, 3741 (2014).
[Crossref] [PubMed]

Redford, G. I.

G. I. Redford and R. M. Clegg, “Polar plot representation for frequency-domain analysis of fluorescence lifetimes,” J. Fluoresc. 15(5), 805–815 (2005).
[Crossref] [PubMed]

Richter, S.

M. Hammer, D. Schweitzer, S. Richter, and E. Königsdörffer, “Sodium fluorescein as a retinal pH indicator?” Physiol. Meas. 26(4), N9–N12 (2005).
[Crossref] [PubMed]

Rumbles, G.

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

Salih, A.

F. Cutrale, A. Salih, and E. Gratton, “Spectral Phasor approach for fingerprinting of photo-activatable fluorescent proteins Dronpa, Kaede and KikGR,” Methods Appl. Fluoresc. 1(3), 035001 (2013).
[Crossref] [PubMed]

Sands, B.

B. Sands, P. Jenkins, W. J. Peria, M. Naivar, J. P. Houston, and R. Brent, “Measuring and sorting cell populations expressing isospectral fluorescent proteins with different fluorescence lifetimes,” PLoS One 9(10), e109940 (2014).
[Crossref] [PubMed]

Schenke, S.

D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
[Crossref] [PubMed]

Schweitzer, D.

D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
[Crossref] [PubMed]

M. Hammer, D. Schweitzer, S. Richter, and E. Königsdörffer, “Sodium fluorescein as a retinal pH indicator?” Physiol. Meas. 26(4), N9–N12 (2005).
[Crossref] [PubMed]

Schweitzer, F.

D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
[Crossref] [PubMed]

Sillen, A.

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

Silva, N. D.

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

Sklar, L. A.

C. Deka, B. E. Lehnert, N. M. Lehnert, G. M. Jones, L. A. Sklar, and J. A. Steinkamp, “Analysis of fluorescence lifetime and quenching of FITC-conjugated antibodies on cells by phase-sensitive flow cytometry,” Cytometry 25(3), 271–279 (1996).
[Crossref] [PubMed]

C. Deka, L. S. Cram, R. Habbersett, J. C. Martin, L. A. Sklar, and J. A. Steinkamp, “Simultaneous dual-frequency phase-sensitive flow cytometric measurements for rapid identification of heterogeneous fluorescence decays in fluorochrome-labeled cells and particles,” Cytometry 21(4), 318–328 (1995).
[Crossref] [PubMed]

Squire, A.

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

R. Pepperkok, A. Squire, S. Geley, and P. I. Bastiaens, “Simultaneous detection of multiple green fluorescent proteins in live cells by fluorescence lifetime imaging microscopy,” Curr. Biol. 9(5), 269–274 (1999).
[Crossref] [PubMed]

Steinkamp, J. A.

H. H. Cui, J. G. Valdez, J. A. Steinkamp, and H. A. Crissman, “Fluorescence lifetime-based discrimination and quantification of cellular DNA and RNA with phase-sensitive flow cytometry,” Cytometry A 52(1), 46–55 (2003).
[Crossref] [PubMed]

J. A. Steinkamp, B. E. Lehnert, and N. M. Lehnert, “Discrimination of damaged/dead cells by propidium iodide uptake in immunofluorescently labeled populations analyzed by phase-sensitive flow cytometry,” J. Immunol. Methods 226(1-2), 59–70 (1999).
[Crossref] [PubMed]

J. A. Steinkamp and J. F. Keij, “Fluorescence intensity and lifetime measurement of free and particle-bound fluorophore in a sample stream by phase-sensitive flow cytometry,” Rev. Sci. Instrum. 70(12), 4682–4688 (1999).
[Crossref]

C. Deka, B. E. Lehnert, N. M. Lehnert, G. M. Jones, L. A. Sklar, and J. A. Steinkamp, “Analysis of fluorescence lifetime and quenching of FITC-conjugated antibodies on cells by phase-sensitive flow cytometry,” Cytometry 25(3), 271–279 (1996).
[Crossref] [PubMed]

C. Deka, L. S. Cram, R. Habbersett, J. C. Martin, L. A. Sklar, and J. A. Steinkamp, “Simultaneous dual-frequency phase-sensitive flow cytometric measurements for rapid identification of heterogeneous fluorescence decays in fluorochrome-labeled cells and particles,” Cytometry 21(4), 318–328 (1995).
[Crossref] [PubMed]

J. A. Steinkamp and H. A. Crissman, “Resolution of fluorescence signals from cells labeled with fluorochromes having different lifetimes by phase-sensitive flow cytometry,” Cytometry 14(2), 210–216 (1993).
[Crossref] [PubMed]

Stringari, C.

C. Stringari, R. A. Edwards, K. T. Pate, M. L. Waterman, P. J. Donovan, and E. Gratton, “Metabolic trajectory of cellular differentiation in small intestine by Phasor Fluorescence Lifetime Microscopy of NADH,” Sci. Rep. 2, 568 (2012).
[Crossref] [PubMed]

C. Stringari, A. Cinquin, O. Cinquin, M. A. Digman, P. J. Donovan, and E. Gratton, “Phasor approach to fluorescence lifetime microscopy distinguishes different metabolic states of germ cells in a live tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(33), 13582–13587 (2011).
[Crossref] [PubMed]

C. Stringari, A. Cinquin, O. Cinquin, M. A. Digman, P. J. Donovan, and E. Gratton, “Phasor approach to fluorescence lifetime microscopy distinguishes different metabolic states of germ cells in a live tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(33), 13582–13587 (2011).
[Crossref] [PubMed]

Szabo, A. G.

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

Szmacinski, H.

H. Szmacinski, V. Toshchakov, and J. R. Lakowicz, “Application of phasor plot and autofluorescence correction for study of heterogeneous cell population,” J. Biomed. Opt. 19(4), 046017 (2014).
[Crossref] [PubMed]

Tamai, N.

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

Toshchakov, V.

H. Szmacinski, V. Toshchakov, and J. R. Lakowicz, “Application of phasor plot and autofluorescence correction for study of heterogeneous cell population,” J. Biomed. Opt. 19(4), 046017 (2014).
[Crossref] [PubMed]

Vacca, G.

W. Li, G. Vacca, M. Castillo, K. D. Houston, and J. P. Houston, “Fluorescence lifetime excitation cytometry by kinetic dithering,” Electrophoresis 35(12-13), 1846–1854 (2014).
[Crossref] [PubMed]

Valdez, J. G.

H. H. Cui, J. G. Valdez, J. A. Steinkamp, and H. A. Crissman, “Fluorescence lifetime-based discrimination and quantification of cellular DNA and RNA with phase-sensitive flow cytometry,” Cytometry A 52(1), 46–55 (2003).
[Crossref] [PubMed]

Valeur, B.

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

van Hoek, A.

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

vandeVen, M.

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

Verveer, P. J.

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

Visitkul, V.

J. Nedbal, V. Visitkul, E. Ortiz-Zapater, G. Weitsman, P. Chana, D. R. Matthews, T. Ng, and S. M. Ameer-Beg, “Time-domain microfluidic fluorescence lifetime flow cytometry for high-throughput Förster resonance energy transfer screening,” Cytometry A 87(2), 104–118 (2015).

Visser, A. J.

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

Waterman, M. L.

C. Stringari, R. A. Edwards, K. T. Pate, M. L. Waterman, P. J. Donovan, and E. Gratton, “Metabolic trajectory of cellular differentiation in small intestine by Phasor Fluorescence Lifetime Microscopy of NADH,” Sci. Rep. 2, 568 (2012).
[Crossref] [PubMed]

Weitsman, G.

J. Nedbal, V. Visitkul, E. Ortiz-Zapater, G. Weitsman, P. Chana, D. R. Matthews, T. Ng, and S. M. Ameer-Beg, “Time-domain microfluidic fluorescence lifetime flow cytometry for high-throughput Förster resonance energy transfer screening,” Cytometry A 87(2), 104–118 (2015).

Whan, R. M.

J. S. Basuki, H. T. Duong, A. Macmillan, R. B. Erlich, L. Esser, M. C. Akerfeldt, R. M. Whan, M. Kavallaris, C. Boyer, and T. P. Davis, “Using fluorescence lifetime imaging microscopy to monitor theranostic nanoparticle uptake and intracellular doxorubicin release,” ACS Nano 7(11), 10175–10189 (2013).
[Crossref] [PubMed]

Wilder, M.

R. Cao, M. A. Naivar, M. Wilder, and J. P. Houston, “Expanding the potential of standard flow cytometry by extracting fluorescence lifetimes from cytometric pulse shifts,” Cytometry A 85(12), 999–1010 (2014).
[Crossref] [PubMed]

Willaert, K.

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

Yang, S.

Y. Lu, J. Lu, J. Zhao, J. Cusido, F. M. Raymo, J. Yuan, S. Yang, R. C. Leif, Y. Huo, J. A. Piper, J. Paul Robinson, E. M. Goldys, and D. Jin, “On-the-fly decoding luminescence lifetimes in the microsecond region for lanthanide-encoded suspension arrays,” Nat. Commun. 5, 3741 (2014).
[Crossref] [PubMed]

Yuan, J.

Y. Lu, J. Lu, J. Zhao, J. Cusido, F. M. Raymo, J. Yuan, S. Yang, R. C. Leif, Y. Huo, J. A. Piper, J. Paul Robinson, E. M. Goldys, and D. Jin, “On-the-fly decoding luminescence lifetimes in the microsecond region for lanthanide-encoded suspension arrays,” Nat. Commun. 5, 3741 (2014).
[Crossref] [PubMed]

Zamai, M.

M. A. Digman, V. R. Caiolfa, M. Zamai, and E. Gratton, “The phasor approach to fluorescence lifetime imaging analysis,” Biophys. J. 94(2), L14–L16 (2008).
[Crossref] [PubMed]

Zhao, J.

Y. Lu, J. Lu, J. Zhao, J. Cusido, F. M. Raymo, J. Yuan, S. Yang, R. C. Leif, Y. Huo, J. A. Piper, J. Paul Robinson, E. M. Goldys, and D. Jin, “On-the-fly decoding luminescence lifetimes in the microsecond region for lanthanide-encoded suspension arrays,” Nat. Commun. 5, 3741 (2014).
[Crossref] [PubMed]

ACS Nano (1)

J. S. Basuki, H. T. Duong, A. Macmillan, R. B. Erlich, L. Esser, M. C. Akerfeldt, R. M. Whan, M. Kavallaris, C. Boyer, and T. P. Davis, “Using fluorescence lifetime imaging microscopy to monitor theranostic nanoparticle uptake and intracellular doxorubicin release,” ACS Nano 7(11), 10175–10189 (2013).
[Crossref] [PubMed]

Anal. Chem. (2)

N. Boens, W. Qin, N. Basarić, J. Hofkens, M. Ameloot, J. Pouget, J.-P. Lefèvre, B. Valeur, E. Gratton, M. vandeVen, N. D. Silva, Y. Engelborghs, K. Willaert, A. Sillen, G. Rumbles, D. Phillips, A. J. Visser, A. van Hoek, J. R. Lakowicz, H. Malak, I. Gryczynski, A. G. Szabo, D. T. Krajcarski, N. Tamai, and A. Miura, “Fluorescence lifetime standards for time and frequency domain fluorescence spectroscopy,” Anal. Chem. 79(5), 2137–2149 (2007).
[Crossref] [PubMed]

K. M. Dean, L. M. Davis, J. L. Lubbeck, P. Manna, P. Friis, A. E. Palmer, and R. Jimenez, “High-speed multiparameter photophysical analyses of fluorophore libraries,” Anal. Chem. 87(10), 5026–5030 (2015).
[Crossref] [PubMed]

Biomed. Opt. Express (2)

Biophys. Chem. (1)

D. P. Heller and C. L. Greenstock, “Fluorescence lifetime analysis of DNA intercalated ethidium bromide and quenching by free dye,” Biophys. Chem. 50(3), 305–312 (1994).
[Crossref] [PubMed]

Biophys. J. (2)

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

M. A. Digman, V. R. Caiolfa, M. Zamai, and E. Gratton, “The phasor approach to fluorescence lifetime imaging analysis,” Biophys. J. 94(2), L14–L16 (2008).
[Crossref] [PubMed]

Curr. Biol. (1)

R. Pepperkok, A. Squire, S. Geley, and P. I. Bastiaens, “Simultaneous detection of multiple green fluorescent proteins in live cells by fluorescence lifetime imaging microscopy,” Curr. Biol. 9(5), 269–274 (1999).
[Crossref] [PubMed]

Cytometry (4)

C. Deka, B. E. Lehnert, N. M. Lehnert, G. M. Jones, L. A. Sklar, and J. A. Steinkamp, “Analysis of fluorescence lifetime and quenching of FITC-conjugated antibodies on cells by phase-sensitive flow cytometry,” Cytometry 25(3), 271–279 (1996).
[Crossref] [PubMed]

C. Deka, L. S. Cram, R. Habbersett, J. C. Martin, L. A. Sklar, and J. A. Steinkamp, “Simultaneous dual-frequency phase-sensitive flow cytometric measurements for rapid identification of heterogeneous fluorescence decays in fluorochrome-labeled cells and particles,” Cytometry 21(4), 318–328 (1995).
[Crossref] [PubMed]

J. A. Steinkamp and H. A. Crissman, “Resolution of fluorescence signals from cells labeled with fluorochromes having different lifetimes by phase-sensitive flow cytometry,” Cytometry 14(2), 210–216 (1993).
[Crossref] [PubMed]

B. G. Pinsky, J. J. Ladasky, J. R. Lakowicz, K. Berndt, and R. A. Hoffman, “Phase-resolved fluorescence lifetime measurements for flow cytometry,” Cytometry 14(2), 123–135 (1993).
[Crossref] [PubMed]

Cytometry A (4)

J. P. Houston, M. A. Naivar, and J. P. Freyer, “Digital analysis and sorting of fluorescence lifetime by flow cytometry,” Cytometry A 77(9), 861–872 (2010).
[Crossref] [PubMed]

R. Cao, M. A. Naivar, M. Wilder, and J. P. Houston, “Expanding the potential of standard flow cytometry by extracting fluorescence lifetimes from cytometric pulse shifts,” Cytometry A 85(12), 999–1010 (2014).
[Crossref] [PubMed]

H. H. Cui, J. G. Valdez, J. A. Steinkamp, and H. A. Crissman, “Fluorescence lifetime-based discrimination and quantification of cellular DNA and RNA with phase-sensitive flow cytometry,” Cytometry A 52(1), 46–55 (2003).
[Crossref] [PubMed]

J. Nedbal, V. Visitkul, E. Ortiz-Zapater, G. Weitsman, P. Chana, D. R. Matthews, T. Ng, and S. M. Ameer-Beg, “Time-domain microfluidic fluorescence lifetime flow cytometry for high-throughput Förster resonance energy transfer screening,” Cytometry A 87(2), 104–118 (2015).

Electrophoresis (1)

W. Li, G. Vacca, M. Castillo, K. D. Houston, and J. P. Houston, “Fluorescence lifetime excitation cytometry by kinetic dithering,” Electrophoresis 35(12-13), 1846–1854 (2014).
[Crossref] [PubMed]

J. Biomed. Opt. (1)

H. Szmacinski, V. Toshchakov, and J. R. Lakowicz, “Application of phasor plot and autofluorescence correction for study of heterogeneous cell population,” J. Biomed. Opt. 19(4), 046017 (2014).
[Crossref] [PubMed]

J. Biophotonics (1)

P. Jenkins, M. A. Naivar, and J. P. Houston, “Toward the measurement of multiple fluorescence lifetimes in flow cytometry: maximizing multi-harmonic content from cells and microspheres,” J. Biophotonics 8(11-12), 908–917 (2015).
[Crossref] [PubMed]

J. Fluoresc. (1)

G. I. Redford and R. M. Clegg, “Polar plot representation for frequency-domain analysis of fluorescence lifetimes,” J. Fluoresc. 15(5), 805–815 (2005).
[Crossref] [PubMed]

J. Immunol. Methods (1)

J. A. Steinkamp, B. E. Lehnert, and N. M. Lehnert, “Discrimination of damaged/dead cells by propidium iodide uptake in immunofluorescently labeled populations analyzed by phase-sensitive flow cytometry,” J. Immunol. Methods 226(1-2), 59–70 (1999).
[Crossref] [PubMed]

Methods Appl. Fluoresc. (1)

F. Cutrale, A. Salih, and E. Gratton, “Spectral Phasor approach for fingerprinting of photo-activatable fluorescent proteins Dronpa, Kaede and KikGR,” Methods Appl. Fluoresc. 1(3), 035001 (2013).
[Crossref] [PubMed]

Microsc. Res. Tech. (1)

D. Schweitzer, S. Schenke, M. Hammer, F. Schweitzer, S. Jentsch, E. Birckner, W. Becker, and A. Bergmann, “Towards metabolic mapping of the human retina,” Microsc. Res. Tech. 70(5), 410–419 (2007).
[Crossref] [PubMed]

Nat. Commun. (1)

Y. Lu, J. Lu, J. Zhao, J. Cusido, F. M. Raymo, J. Yuan, S. Yang, R. C. Leif, Y. Huo, J. A. Piper, J. Paul Robinson, E. M. Goldys, and D. Jin, “On-the-fly decoding luminescence lifetimes in the microsecond region for lanthanide-encoded suspension arrays,” Nat. Commun. 5, 3741 (2014).
[Crossref] [PubMed]

Opt. Express (1)

Physiol. Meas. (1)

M. Hammer, D. Schweitzer, S. Richter, and E. Königsdörffer, “Sodium fluorescein as a retinal pH indicator?” Physiol. Meas. 26(4), N9–N12 (2005).
[Crossref] [PubMed]

PLoS One (1)

B. Sands, P. Jenkins, W. J. Peria, M. Naivar, J. P. Houston, and R. Brent, “Measuring and sorting cell populations expressing isospectral fluorescent proteins with different fluorescence lifetimes,” PLoS One 9(10), e109940 (2014).
[Crossref] [PubMed]

Proc. Natl. Acad. Sci. U.S.A. (2)

C. Stringari, A. Cinquin, O. Cinquin, M. A. Digman, P. J. Donovan, and E. Gratton, “Phasor approach to fluorescence lifetime microscopy distinguishes different metabolic states of germ cells in a live tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(33), 13582–13587 (2011).
[Crossref] [PubMed]

C. Stringari, A. Cinquin, O. Cinquin, M. A. Digman, P. J. Donovan, and E. Gratton, “Phasor approach to fluorescence lifetime microscopy distinguishes different metabolic states of germ cells in a live tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(33), 13582–13587 (2011).
[Crossref] [PubMed]

Rev. Sci. Instrum. (1)

J. A. Steinkamp and J. F. Keij, “Fluorescence intensity and lifetime measurement of free and particle-bound fluorophore in a sample stream by phase-sensitive flow cytometry,” Rev. Sci. Instrum. 70(12), 4682–4688 (1999).
[Crossref]

Sci. Rep. (1)

C. Stringari, R. A. Edwards, K. T. Pate, M. L. Waterman, P. J. Donovan, and E. Gratton, “Metabolic trajectory of cellular differentiation in small intestine by Phasor Fluorescence Lifetime Microscopy of NADH,” Sci. Rep. 2, 568 (2012).
[Crossref] [PubMed]

Other (2)

J. P. Houston, M. A. Naivar, P. Jenkins, and J. P. Freyer, “Capture of fluorescence decay times by flow cytometry,” Current Protocols in Cytometry, 1–21 (2012).
[Crossref]

C. Deka and J. A. Steinkamp, “Time-resolved fluorescence decay measurements for flowing particles,” (Google Patents, 1999).

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Figures (6)

Fig. 1
Fig. 1 Frequency-domain flow cytometry system used for the generation of phasor plots. A laser-excited sample is driven by pressurized fluidics. The samples (depicted by circles and ovals) transit the laser beam (represented by blue dashed line), which is modulated by a function generator. Fluorescence (yellow dashed line directed to PMT2) and side scattering signals (blue dashed line before PMT1) are focused onto the side of two similar PMTs (Hamamatsu, San Diego, model R1477-04). The full cytometry waveforms are collected with a 250 MSPS high-speed Innovative data acquisition system. After collection of the full waveforms, MATLAB was used to build phasor plots for analyses of multiple lifetime components.
Fig. 2
Fig. 2 Modulated flow cytometry waveform (a) and the resulting frequency spectrum output (b) after applying a discrete Fourier transform to the data. In this example the modulation frequency was 1 MHz.
Fig. 3
Fig. 3 The transfer from a raw data of an event (a) to one dot in the phasor plot where the dots located on semicircle indicate single lifetimes (b). The location [1, 0] represents 0 ns, and the location of origin [0, 0] represents an infinite lifetime. Fluorescence lifetimes along the semicircle increase counter-clockwise to the left. In this coordinate system the measured value is the intensity-weighted average of the lifetime components. The magnitude of the vector equals the demodulation of the measured event m, and the angle between x-axis and vector equals the phase shift ϕ. The line joining the lifetime components notes the location of the measured event. In this example, the measured event is located in the middle of the line joining single lifetimes of 4 ns and 19 ns. The plot reveals the event consists of an equivalent fraction of 4 ns and 19 ns components. The solid lines represent the phase shift and demodulation vector for the dual-lifetime simulation, and the dashed lines represent single lifetime component vectors thereof.
Fig. 4
Fig. 4 Phasor plot representations from fluorescence data on single fluorophore-labeled microspheres. The red population is data from fluorescein microspheres and the blue is of PI microspheres, with the calculated value of their respective fluorescent lifetimes shown by the open marker on the semicircle.
Fig. 5
Fig. 5 Phasor plot representation of cells labeled with FITC (red dots), EB (blue dots), and a combination of FITC and EB (brown dots), with the open markers being the calculated values of the fluorescent lifetimes of FITC and EB on the phasor semicircle.
Fig. 6
Fig. 6 Phasor plot representations of yeast cells expressing different fluorescent protein constructs. (a), (b), and (c) are the phasor plots of cells producing TFP, TFP linked to dark citrine fluorescence protein, and an equal mixture of cells that express either TFP or TFP-dCit, respectively. (d) is a dot plot of two parameters (side scatter and fluorescence intensity) where the blue dots represent TFP-dCit expressing cells and the red dots represent the TFP expressing cells.

Equations (10)

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

E(t)= E 0 + E ω cos(ωt+ ϕ E ),
F(t)= F 0 + F ω cos(ωt+ ϕ F ),
ω τ ϕ =tanϕ,
and, m= 1 1+ (ω τ m ) 2 ,
( 1 m 2 1) 1 2 = sinϕ cosϕ ,
x=mcosϕ,
y=msinϕ,
y x = ( 1 x 2 + y 2 1 ) 1 2 ,
x 2 + y 2 =x.
r measure =a r a +b r b ,

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