Fluorescence lifetime imaging of fluorescent proteins as an effective quantitative tool for noninvasive study of intracellular processes

Svitlana M. Levchenko; Artem Pliss; Junle Qu

doi:10.1142/s1793545817300099

[1] J. R. Lakowicz, Principles of Fluorescence Spectroscopy, 3rd edition, Springer, New York (2006).

[2] A. Ettinger, T. Wittmann, “Fluorescence live cell imaging," Methods Cell. Biol. 123, 77-94 (2014).

[3] J. C. Waters, T. Wittmann, “Quantitative imaging in cell biology: Preface," Methods Cell. Biol. 123, xix xx (2014).

[4] W. Becker, Advanced Time-Correlated Single Photon Counting Techniques, Springer, Berlin (2005).

[5] O. Shimomura, F. H. Johnson, Y. Saiga, “Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea," J. Cell. Comp. Physiol. 59, 223-239 (1962).

[6] D. C. Prasher, V. K. Eckenrode, W. W. Ward, F. G. Prendergast, M. J. Cormier, “Primary structure of the Aequorea victoria green-fluorescent protein," Gene 111, 229-233 (1992).

[7] M. Chalfie, Y. Tu, G. Euskirchen, W. W. Ward, D. C. Prasher, “Green fluorescent protein as a marker for gene-expression," Science 263, 802-805 (1994).

[8] M. Zimmer, “GFP: From jellyfish to the Nobel prize and beyond," Chem. Soc. Rev. 38, 2823-2832 (2009).

[9] M. Ormo, A. B. Cubitt, K. Kallio, L. A. Gross, R. Y. Tsien, S. J. Remington, “Crystal structure of the Aequorea victoria green fluorescent protein," Science 273, 1392-1395 (1996).

[10] R. Heim, D. C. Prasher, R. Y. Tsien, “Wavelength mutations and posttranslational autoxidation of green fluorescent protein," Proc. Natl. Acad. Sci. USA 91, 12501-12504 (1994).

[11] R. Heim, A. B. Cubitt, R. Y. Tsien, “Improved green fluorescence," Nature 373, 663-664 (1995).

[12] G. J. Kremers, S. G. Gilbert, P. J. Cranfill, M. W. Davidson, D. W. Piston, “Fluorescent proteins at a glance," J. Cell. Sci. 124, 157-160 (2011).

[13] A. W. Scruggs, C. L. Flores, R. Wachter, N. W. Woodbury, “Development and characterization of green fluorescent protein mutants with altered lifetimes," Biochemistry 44, 13377-13384 (2005).

[14] A. S. Mishin, F. V. Subach, I. V. Yampolsky, W. King, K. A. Lukyanov, V. V. Verkhusha, “The first mutant of the Aequorea victoria green fluorescent protein that forms a red chromophore," Biochemistry 47, 4666-4673 (2008).

[15] M. V. Matz, A. F. Fradkov, Y. A. Labas, A. P. Savitsky, A. G. Zaraisky, M. L. Markelov, S. A. Lukyanov, “Fluorescent proteins from nonbioluminescent Anthozoa species," Nat. Biotechnol. 17, 969-973 (1999).

[16] N. C. Shaner, R. E. Campbell, P. A. Steinbach, B. N. Giepmans, A. E. Palmer, R. Y. Tsien, “Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein," Nat. Biotechnol. 22, 1567-1572 (2004).

[17] R. Heim, R. Y. Tsien, “Engineering green fluorescent protein for improved brightness, longer wavelengths and fluorescence resonance energy transfer," Curr. Biol. 6, 178-182 (1996).

[18] P. E. Konold, E. Yoon, J. Lee, S. L. Allen, P. P. Chapagain, B. S. Gerstman, C. K. Regmi, K. D. Piatkevich, V. V. Verkhusha, T. Joo, R. Jimenez, “Fluorescence from multiple chromophore hydrogenbonding states in the far-red protein TagRFP675," J. Phys. Chem. Lett. 7, 3046-3051 (2016).

[19] D. S. Bindels, L. Haarbosch, L. van Weeren, M. Postma, K. E. Wiese, M. Mastop, S. Aumonier, G. Gotthard, A. Royant, M. A. Hink, T. W. Gadella, Jr., “mScarlet: A bright monomeric red fluorescent protein for cellular imaging," Nat. Methods 14, 53-56 (2017).

[20] C. P. Toseland, “Fluorescent labeling and modification of proteins," J. Chem. Biol. 6, 85-95 (2013).

[21] M. Modesti, “Fluorescent labeling of proteins," Methods Mol. Biol. 783, 101-120 (2011).

[22] K. M. Dean, A. E. Palmer, “Advances in fluorescence labeling strategies for dynamic cellular imaging," Nat. Chem. Biol. 10, 512-523 (2014).

[23] G. S. Filonov, K. D. Piatkevich, L. M. Ting, J. Zhang, K. Kim, V. V. Verkhusha, “Bright and stable near-infrared fluorescent protein for in vivo imaging," Nat. Biotechnol. 29, 757-761 (2011).

[24] K. G. Chernov, T. A. Redchuk, E. S. Omelina, V. V. Verkhusha, “Near-infrared fluorescent proteins, biosensors, and optogenetic tools engineered from phytochromes," Chem. Rev. 117, 6423-6446 (2017).

[25] E. Hemmer, A. Benayas, F. Legare, F. Vetrone, “Exploiting the biological windows: Current perspectives on fluorescent bioprobes emitting above 1000 nm," Nanoscale Horiz. 1, 168-184 (2016).

[26] D. M. Shcherbakova, V. V. Verkhusha, “Nearinfrared fluorescent proteins for multicolor in vivo imaging," Nat. Methods 10, 751-754 (2013).

[27] G. Crivat, J. W. Taraska, “Imaging proteins inside cells with fluorescent tags," Trends Biotechnol. 30, 8-16 (2012).

[28] E. Snapp, “Design and use of fluorescent fusion proteins in cell biology," Curr. Protoc. Cell Biol. 21, 21-24 (2005).

[29] R. Ebrecht, C. Don Paul, F. S. Wouters, “Fluorescence lifetime imaging microscopy in the medical sciences," Protoplasma 251, 293-305 (2014).

[30] J. A. Levitt, D. R. Matthews, S. M. Ameer-Beg, K. Suhling, “Fluorescence lifetime and polarizationresolved imaging in cell biology," Curr. Opin. Biotechnol. 20, 28-36 (2009).

[31] A. Periasamy, R. M. Clegg, FLIM Microscopy in Biology and Medicine, Taylor & Francis, Boca Raton (2010).

[32] K. Suhling, L. M. Hirvonen, J. A. Levitt, P.-H. Chung, C. Tregidgo, A. Le Marois, D. A. Rusakov, K. Zheng, S. Ameer-Beg, S. Poland, “Fluorescence lifetime imaging (FLIM): Basic concepts and some recent developments," Med. Photonics 27, 3-40 (2015).

[33] M. Y. Berezin, S. Achilefu, “Fluorescence lifetime measurements and biological imaging," Chem. Rev. 110, 2641-2684 (2010).

[34] A. Le Marois, S. Labouesse, K. Suhling, R. Heintzmann, “Noise-Corrected Principal Component Analysis of fluorescence lifetime imaging data," J. Biophoton. (2016).

[35] A. C. Sohnel, W. Kohl, I. Gregor, J. Enderlein, B. Rieger, K. B. Busch, “Probing of protein localization and shuttling in mitochondrial microcompartments by FLIM with sub-diffraction resolution," Biochim. Biophys. Acta 1857, 1290-1299 (2016).

[36] K. Suhling, J. Siegel, D. Phillips, P. M. French, S. Leveque-Fort, S. E. Webb, D. M. Davis, “Imaging the environment of green fluorescent protein," Biophys. J. 83, 3589-3595 (2002).

[37] T. Niehorster, A. Loschberger, I. Gregor, B. Kramer, H. J. Rahn, M. Patting, F. Koberling, J. Enderlein, M. Sauer, “Multi-target spectrally resolved fluorescence lifetime imaging microscopy," Nat. Methods 13, 257-262 (2016).

[38] H. Anton, N. Taha, E. Boutant, L. Richert, H. Khatter, B. Klaholz, P. Ronde, E. Real, H. de Rocquigny, Y. Mely, “Investigating the cellular distribution and interactions of HIV-1 nucleocapsid protein by quantitative fluorescence microscopy," PLoS One 10, e0116921 (2015).

[39] M. Kneen, J. Farinas, Y. Li, A. S. Verkman, “Green fluorescent protein as a noninvasive intracellular pH indicator," Biophys. J. 74, 1591-1599 (1998).

[40] M. F. Abad, G. Di Benedetto, P. J. Magalhaes, L. Filippin, T. Pozzan, “Mitochondrial pH monitored by a new engineered green fluorescent protein mutant," J. Biol. Chem. 279, 11521-11529 (2004).

[41] M. Tantama, Y. P. Hung, G. Yellen, “Imaging intracellular pH in live cells with a genetically encoded red fluorescent protein sensor," J. Am. Chem. Soc. 133, 10034-10037 (2011).

[42] J. S. Donner, S. A. Thompson, M. P. Kreuzer, G. Baffou, R. Quidant, “Mapping intracellular temperature using green fluorescent protein," Nano Lett. 12, 2107-2111 (2012).

[43] A. Pliss, L. Zhao, T. Y. Ohulchanskyy, J. Qu, P. N. Prasad, “Fluorescence lifetime of fluorescent proteins as an intracellular environment probe sensing the cell cycle progression," ACS Chem. Biol. 7, 1385-1392 (2012).

[44] A. Pliss, X. Peng, L. Liu, A. Kuzmin, Y. Wang, J. Qu, Y. Li, P. N. Prasad, “Single cell assay for molecular diagnostics and medicine: Monitoring intracellular concentrations of macromolecules by two-photon fluorescence lifetime imaging," Theranostics 5, 919-930 (2015).

[45] M. Bencina, “Illumination of the spatial order of intracellular pH by genetically encoded pH-sensitive sensors," Sensors 13, 16736-16758 (2013).

[46] T. Nakabayashi, S. Oshita, R. Sumikawa, F. Sun, M. Kinjo, N. Ohta, “pH dependence of the fluorescence lifetime of enhanced yellow fluorescent protein in solution and cells," J. Photochem. Photobiol. A 235, 65-71 (2012).

[47] F. J. Schmitt, B. Thaa, C. Junghans, M. Vitali, M. Veit, T. Friedrich, “eGFP-pHsens as a highly sensitive fluorophore for cellular pH determination by fluorescence lifetime imaging microscopy (FLIM)," Biochem. Biophys. Acta 1837, 1581-1593 (2014).

[48] T. Nakabayashi, H. P. Wang, M. Kinjo, N. Ohta, “Application of fluorescence lifetime imaging of enhanced green fluorescent protein to intracellular pH measurements," Photochem. Photobiol. Sci. 7, 668-670 (2008).

[49] S. Poea-Guyon, H. Pasquier, F. Merola, N. Morel, M. Erard, “The enhanced cyan fluorescent protein: A sensitive pH sensor for fluorescence lifetime imaging," Anal. Bioanal. Chem. 405, 3983-3987 (2013).

[50] H. Ogawa, S. Inouye, F. I. Tsuji, K. Yasuda, K. Umesono, “Localization, tra±cking, and temperaturedependence of the Aequorea green fluorescent protein in cultured vertebrate cells," Proc. Natl. Acad. Sci. USA 92, 11899-11903 (1995).

[51] S. Kiyonaka, T. Kajimoto, R. Sakaguchi, D. Shinmi, M. Omatsu-Kanbe, H. Matsuura, H. Imamura, T. Yoshizaki, I. Hamachi, T. Morii, Y. Mori, “Genetically encoded fluorescent thermosensors visualize subcellular thermoregulation in living cells," Nat. Methods 10, 1232-1238 (2013).

[52] M. Nakano, Y. Arai, I. Kotera, K. Okabe, Y. Kamei, T. Nagai, “Genetically encoded ratiometric fluorescent thermometer with wide range and rapid response," PLoS One 12, e0172344 (2017).

[53] K. Deepankumar, S. P. Nadarajan, D. H. Bae, K. H. Baek, K. Y. Choi, H. Yun, “Temperature sensing using red fluorescent protein," Biotechnol. Bioprocess. Eng. 20, 67-72 (2015).

[54] H. Itoh, S. Arai, T. Sudhaharan, S. C. Lee, Y. T. Chang, S. Ishiwata, M. Suzuki, E. B. Lane, “Direct organelle thermometry with fluorescence lifetime imaging microscopy in single myotubes," Chem. Commun. (Camb.) 52, 4458-4461 (2016).

[55] K. Okabe, N. Inada, C. Gota, Y. Harada, T. Funatsu, S. Uchiyama, “Intracellular temperature mapping with a fluorescent polymeric thermometer and fluorescence lifetime imaging microscopy," Nat. Commun. 3, 705 (2012).

[56] B. Treanor, P. M. Lanigan, K. Suhling, T. Schreiber, I. Munro, M. A. Neil, D. Phillips, D. M. Davis, P. M. French, “Imaging fluorescence lifetime heterogeneity applied to GFP-tagged MHC protein at an immunological synapse," J. Microsc. 217, 36-43 (2005).