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

Key Laboratory of Optoelectronic Devices and Systems of Guangdong Province, College of Optoelectronic Engineering, Shenzhen University, Shenzhen, Guangdong Province 518060, P. R. China

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Artem Pliss

http://orcid.org/0000-0003-4867-4074

Institute for Lasers, Photonics and Biophotonics, University at Buffalo, State University of New York, Buffalo, NY 14260-3000, USA

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, and

Junle Qu

Key Laboratory of Optoelectronic Devices and Systems of Guangdong Province, College of Optoelectronic Engineering, Shenzhen University, Shenzhen, Guangdong Province 518060, P. R. China

E-mail Address: jlqu@szu.edu.cn

Corresponding author.

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https://doi.org/10.1142/S1793545817300099Cited by:19 (Source: Crossref)

Abstract

Fluorescence lifetime imaging (FLIM) is an effective noninvasive bioanalytical tool based on measuring fluorescent lifetime of fluorophores. A growing number of FLIM studies utilizes genetically engineered fluorescent proteins targeted to specific subcellular structures to probe local molecular environment, which opens new directions in cell science. This paper highlights the unconventional applications of FLIM for studies of molecular processes in diverse organelles of live cultured cells.

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References

1. J. R. Lakowicz, Principles of Fluorescence Spectroscopy, 3rd edition, Springer, New York (2006). Crossref, Google Scholar
2. A. Ettinger, T. Wittmann, “Fluorescence live cell imaging,” Methods Cell. Biol. 123, 77–94 (2014). Crossref, Web of Science, Google Scholar
3. J. C. Waters, T. Wittmann, “Quantitative imaging in cell biology: Preface,” Methods Cell. Biol. 123, xix–xx (2014). Crossref, Web of Science, Google Scholar
4. W. Becker, Advanced Time-Correlated Single Photon Counting Techniques, Springer, Berlin (2005). Crossref, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
8. M. Zimmer, “GFP: From jellyfish to the Nobel prize and beyond,” Chem. Soc. Rev. 38, 2823–2832 (2009). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
11. R. Heim, A. B. Cubitt, R. Y. Tsien, “Improved green fluorescence,” Nature 373, 663–664 (1995). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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 hydrogen-bonding states in the far-red protein TagRFP675,” J. Phys. Chem. Lett. 7, 3046–3051 (2016). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
20. C. P. Toseland, “Fluorescent labeling and modification of proteins,” J. Chem. Biol. 6, 85–95 (2013). Crossref, Google Scholar
21. M. Modesti, “Fluorescent labeling of proteins,” Methods Mol. Biol. 783, 101–120 (2011). Crossref, Google Scholar
22. K. M. Dean, A. E. Palmer, “Advances in fluorescence labeling strategies for dynamic cellular imaging,” Nat. Chem. Biol. 10, 512–523 (2014). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
25. E. Hemmer, A. Benayas, F. Legare, F. Vetrone, “Exploiting the biological windows: Current perspectives on fluorescent bioprobes emitting above 1000nm,” Nanoscale Horiz. 1, 168–184 (2016). Crossref, Web of Science, Google Scholar
26. D. M. Shcherbakova, V. V. Verkhusha, “Near-infrared fluorescent proteins for multicolor in vivo imaging,” Nat. Methods 10, 751–754 (2013). Crossref, Web of Science, Google Scholar
27. G. Crivat, J. W. Taraska, “Imaging proteins inside cells with fluorescent tags,” Trends Biotechnol. 30, 8–16 (2012). Crossref, Web of Science, Google Scholar
28. E. Snapp, “Design and use of fluorescent fusion proteins in cell biology,” Curr. Protoc. Cell Biol. 21, 21–24 (2005). Google Scholar
29. R. Ebrecht, C. Don Paul, F. S. Wouters, “Fluorescence lifetime imaging microscopy in the medical sciences,” Protoplasma 251, 293–305 (2014). Crossref, Web of Science, Google Scholar
30. J. A. Levitt, D. R. Matthews, S. M. Ameer-Beg, K. Suhling, “Fluorescence lifetime and polarization-resolved imaging in cell biology,” Curr. Opin. Biotechnol. 20, 28–36 (2009). Crossref, Web of Science, Google Scholar
31. A. Periasamy, R. M. Clegg, FLIM Microscopy in Biology and Medicine, Taylor & Francis, Boca Raton (2010). Google Scholar
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). Crossref, Web of Science, Google Scholar
33. M. Y. Berezin, S. Achilefu, “Fluorescence lifetime measurements and biological imaging,” Chem. Rev. 110, 2641–2684 (2010). Crossref, Web of Science, Google Scholar
34. A. Le Marois, S. Labouesse, K. Suhling, R. Heintzmann, “Noise-Corrected Principal Component Analysis of fluorescence lifetime imaging data,” J. Biophoton. (2016). Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
45. M. Bencina, “Illumination of the spatial order of intracellular pH by genetically encoded pH-sensitive sensors,” Sensors 13, 16736–16758 (2013). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
50. H. Ogawa, S. Inouye, F. I. Tsuji, K. Yasuda, K. Umesono, “Localization, trafficking, and temperature-dependence of the Aequorea green fluorescent protein in cultured vertebrate cells,” Proc. Natl. Acad. Sci. USA 92, 11899–11903 (1995). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar
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). Crossref, Web of Science, Google Scholar

Vol. 11, No. 01

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Received 16 April 2017

Accepted 7 June 2017

Published: 19 July 2017

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This is an Open Access article published by World Scientific Publishing Company. It is distributed under the terms of the Creative Commons Attribution 4.0 (CC-BY) License. Further distribution of this work is permitted, provided the original work is properly cited.

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

Abstract

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