Fluorescence lifetime dynamics of enhanced green fluorescent protein in protein aggregates with expanded polyglutamine

Journal of Biomedical Optics

Volumn 15, Issue 1, 2010, Pages

  Ghukasyan, Vladimir ^a   Hsu, Chih Chun ^a   Liu, Chia Rung ^a   Kao, Fu Jen ^a   Cheng, Tzu Hao ^a  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

Aggregation; Enhanced green fluorescent protein; Fluorescence anisotropy imaging; Fluorescence lifetime imaging; F rster resonance energy transfer; Homo FRET; Polyglutamine; Refractive index

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; FLUORESCENCE ANISOTROPY IMAGING; FLUORESCENCE LIFETIME IMAGING; HOMO-FRET; POLYGLUTAMINE;

DISEASE CONTROL; ENERGY TRANSFER; FLUORESCENCE; LIGHT REFRACTION; NEURODEGENERATIVE DISEASES; REFRACTIVE INDEX; REFRACTOMETERS;

PROTEINS;

ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; MULTIPROTEIN COMPLEX; PEPTIDE; POLYGLUTAMINE; PROTEIN;

ANALYSIS OF VARIANCE; ANISOTROPY; ARTICLE; CELL GROWTH; CHEMISTRY; COLOR; FLUORESCENCE MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETICS; METABOLISM; METHODOLOGY; PHYSIOLOGY; REFRACTOMETRY;

ANALYSIS OF VARIANCE; ANISOTROPY; CELL GROWTH PROCESSES; COLOR; FLUORESCENCE RESONANCE ENERGY TRANSFER; GREEN FLUORESCENT PROTEINS; MICROSCOPY, FLUORESCENCE; MULTIPROTEIN COMPLEXES; PEPTIDES; PROTEINS; RECOMBINANT FUSION PROTEINS; REFRACTOMETRY;

EID: 77953140497     PISSN: 10833668     EISSN: 15602281     Source Type: Journal    
DOI: 10.1117/1.3290821     Document Type: Article

References (76)

1. F. Chiti and C. M. Dobson, "Protein misfolding, functional amyloid, and human disease", Annu. Rev. Biochem. 75, 333-366 (2006). (Pubitemid 44118036)
2. P. S. Reddy and D. E. Housman, "The complex pathology of trinucleotide repeats", Curr. Opin. Cell Biol. 9(3), 364-372 (1997). (Pubitemid 27263178)
3. K. Mitsui, H. Doi, and N. Nukina, "Proteomics of polyglutamine aggregates", Methods Enzymol. 412, 63-76 (2006). (Pubitemid 44548574)
4. A. J. Williams and H. L. Paulson, "Polyglutamine neurodegeneration: protein misfolding revisited", Trends Neurosci. 31(10), 521-528 (2008).
5. H. Y. Zoghbi and H. T. Orr, "Glutamine repeats and neurodegeneration", Annu. Rev. Neurosci. 23, 217-247 (2000). (Pubitemid 30350043)
6. J. K. Cooper, G. Schilling, M. F. Peters, W. J. Herring, A. H. Sharp, Z. Kaminsky, J. Masone, F. A. Khan, M. Delanoy, D. R. Borchelt, V. L. Dawson, T. M. Dawson, and C. A. Ross, "Truncated N-terminal fragments of huntingtin with expanded glutamine repeats from nuclear and cytoplasmic aggregates in cell culture", Hum. Mol. Genet. 7(5), 783-790 (1998). (Pubitemid 28221240)
7. S. H. Li and X. J. Li, "Aggregation of N-terminal huntingtin is dependent on the length of its glutamine repeats", Hum. Mol. Genet. 7(5), 777-782 (1998).
8. S. Krobitsch and S. Lindquist, "Aggregation of huntingtin in yeast varies with the length of the polyglutamine expansion and the expression of chaperone proteins", Proc. Natl. Acad. Sci. U. S. A. 97(4), 1589-1594 (2000). (Pubitemid 30118486)
9. G. Huntington's Disease Collaborative Research, "A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes", Cell 72, 971-983 (1993).
10. A. J. Tobin and E. R. Signer, "Huntington's disease: the challenge for cell biologists", Trends Cell Biol. 10, 531-536 (2000).
11. R. M. Bonelli, G. K. Wenning, "Pharmacological management of Huntington's disease: an evidence-based review", Curr. Pharm. Des. 12(21), 2701-2720 (2006).
12. B. Meriin, X. Zhang, N. B. Miliaras, A. Kazantsev, Y. O. Chernoff, J. M. McCaffery, B. Wendland, and M. Y. Sherman, "Aggregation of expanded polyglutamine domain in yeast leads to defects in endocytosis", Mol. Cell. Biol. 23(21), 7554-7565 (2003). (Pubitemid 37271456)
13. S. L. Crick, M. Jayaraman, C. Frieden, R. Wetzel, and R. V. Pappu, "Fluorescence correlation spectroscopy shows that monomeric polyglutamine molecules form collapsed structures in aqueous solutions", Proc. Natl. Acad. Sci. U. S. A. 103(45), 16764 (2006).
14. Y. Takahashi, Y. Okamoto, H. A. Popiel, N. Fujikake, T. Toda, M. Kinjo, and Y. Nagai, "Detection of polyglutamine protein oligomers in cells by fluorescence correlation spectroscopy", J. Biol. Chem. 282(33), 24039 (2007).
15. H. R. Brignull, F. E. Moore, S. J. Tang, and R. I. Morimoto, "Polyglutamine proteins at the pathogenic threshold display neuronspecific aggregation in a pan-neuronal Caenorhabditis elegans model", J. Neurosci. 26(29), 7597-7606 (2006). (Pubitemid 44315179)
16. S. K. Pollitt, J. Pallos, J. Shao, U. A. Desai, A. A. Ma, L. M. Thompson, J. L. Marsh, and M. I. Diamond, "A rapid cellular FRET assay of polyglutamine aggregation identifies a novel inhibitor", Neuron 40, 685-694 (2003). (Pubitemid 37431030)
17. R. S. Rajan, M. E. Illing, N. F. Bence, and R. P. Kopito, "Specificity in intracellular protein aggregation and inclusion body formation", Proc. Natl. Acad. Sci. U. S. A. 98(23), 13060-13065 (2001). (Pubitemid 33051317)
18. A. Weiss, D. Abramowski, M. Bibel, R. Bodner, V. Chopra, M. Di-Figlia, J. Fox, K. Kegel, C. Klein, S. Grueninger, S. Hersch, D. Housman, E. Régulier, H. D. Rosas, M. Stefani, S. Zeitlin, G. Bilbe, and P. Paganetti, "Single-step detection of mutant huntingtin in animal and human tissues: a bioassay for Huntington's disease", Anal. Biochem. 395, 8-15 (2009).
19. T. Takahashi, S. Kikuchi, S. Katada, Y. Nagai, M. Nishizawa, and O. Onodera, "Soluble polyglutamine oligomers formed prior to inclusion body formation are cytotoxic", Hum. Mol. Genet. 17(3), 345-356 (2008).
20. C. Behrends, C. A. Langer, R. Boteva, U. M. Böttcher, M. J. Stemp, G. Schaffar, B. V. Rao, A. Giese, H. Kretzschmar, K. Siegers, and F. U. Hartl, "Chaperonin TRiC promotes the assembly of polyQ expansion proteins into nontoxic oligomers", Mol. Cell 23, 887-897 (2006). (Pubitemid 44363048)
21. W. Fecke, M. Gianfriddo, G. Gaviraghi, G. C. Terstappen, and F. Heitz, "Small molecule drug discovery for Huntington's disease", Drug Discovery Today 14(9-10), 453-364 (2009).
22. S. S. Vogel, C. Thaler, and S. V. Koushik, "Fanciful FRET", Sci. STKE 2006(331), 2-9 (2006).
23. B. Valeur, Molecular Fluorescence: Principles and Applications, Wiley, Weinheim, New York, Chichester, Brisbane, Singapore, Toronto (2001).
24. K. Suhling, K. Siegel, D. Phillips, P. M. W. French, S. Leveque-Fort, S. E. D. Webb, and D. M. Davis, "Imaging the environment of green fluorescent protein", Biophys. J. 83, 3589-3595 (2002). (Pubitemid 36041976)
25. T. Nakabayashi, H. P. Wang, M. Kinjo, and N. Ohta, "Application of fluorescence lifetime imaging of enhanced green fluorescent protein to intracellular pH measurements", Photochem. Photobiol. Sci. 7(6), 668-670 (2008). (Pubitemid 351798459)
26. 2+ based on green fluorescent proteins and calmodulin", Nature (London) 388, 882-887 (1997). (Pubitemid 27377061)
27. C. M. Dooley, T. M. Dore, G. T. Hanson, W. C. Jackson, S. J. Remington, and R. Y. Tsien, "Imaging dynamic redox changes in mammalian cells with green fluorescent protein indicators", J. Biol. Chem. 219, 22284-22293 (2004). (Pubitemid 38679425)
28. A. Miyawaki, "Visualization of the spatial and temporal dynamics of intracellular signaling", Dev. Cell 4(3), 295-305 (2003). (Pubitemid 36342356)
29. H. Wallrabe and A. Periasamy, "Imaging protein molecules using FRET and FLIM microscopy", Curr. Opin. Biotechnol. 16(1), 19-27 (2005). (Pubitemid 40249755)
30. V. Calleja, S. M. Ameer-Beg, B. Vojnovic, R. Woscholski, J. Downward, and B. Larijani, "Monitoring conformational changes of proteins in cells by fluorescence lifetime imaging microscopy", Biochem. J. 372, 33-40 (2003). (Pubitemid 36609604)
31. J. Klucken, T. F. Outeiro, P. Nguyen, P. J. McLean, and B. T. Hyman, "Detection of novel intracellular {alpha}-synuclein oligomeric species by fluorescence lifetime imaging", FASEB J. 20(12), 2050-2057 (2006). (Pubitemid 44953904)
32. O. Berezovska, B. J. Bacskai, and B. T. Hyman, "Monitoring proteins in intact cells", Sci. Aging Knowl. Environ. 2003(23), pe14 (2003).
33. V. N. Uversky, "Nanoimaging in protein-misfolding and conformational diseases", Nanomedicine 2(5), 615-643 (2007).
34. R. Y. Tsien, "The green fluorescent protein", Annu. Rev. Biochem. 67, 509-544 (1998). (Pubitemid 28411137)
35. M. Zimmer, "Green fluorescent protein: applications, structure, and related photophysical behavior", Chem. Rev. (Washington, D. C) 102, 759-781 (2002). (Pubitemid 35377613)
36. W. Cody, D. C. Prasher, W. M. Westler, F. G. Prendergast, and W. W. Ward, "Chemical structure of the hexapeptide chromophore of the Aequorea green-fluorescent protein", Biochemistry 32(5), 1212-1218 (1993). (Pubitemid 23070642)
37. H. Katayama, A. Yamamoto, N. Mizushima, T. Yoshimori, and A. Myawaki, "GFP-like proteins stably accumulate in lysosomes", Cell Struct. Funct 33, 1-12 (2008). (Pubitemid 351860896)
38. R. Heim, A. B. Cubitt, and R. Y. Tsien, "Improved green fluorescence", Nature (London) 373(6516), 663-664 (1995).
39. T. T. Yang, L. Cheng, and S. R. Kain, "Optimized codon usage and chromophore mutations provide enhanced sensitivity with the green fluorescent protein", Nucleic Acids Res. 24(22), 4592-4593 (1996). (Pubitemid 26388650)
40. A. B. Meriin, X. Zhang, X. He, G. P. Newnam, Y. O. Chernoff, and M. Y. Sherman, "Huntingtin toxicity in yeast model depends on polyglutamine aggregation mediated by a prion-like protein Rnq1", J. Cell Biol. 157, 997-1004 (2002). (Pubitemid 34839774)
41. U. Guldener, S. Heck, T. Fielder, J. Beinhauer, and J. H. Hegemann, "A new efficient gene disruption cassette for repeated use in budding yeast", Nucleic Acids Res. 24(13), 2519-2524 (1996). (Pubitemid 26237149)
42. W. Becker, Advanced Time-Correlated Single Photon Counting Techniques, Springer, Berlin, Heidelberg (2005).
43. L. S. Weisman, R. Bacallao, and W. Wickner, "Multiple methods of visualizing the yeast vacuole permit evaluation of its morphology and inheritance during the cell cycle", J. Cell Biol. 105(4), 1539-1547 (1987).
44. P. J. Muchowski, G. Schaffar, A. Sittler, E. E. Wanker, M. K. Hayer-Hartl, and F. U. Hartl, "Hsp70 and hsp40 chaperones can inhibit self-assembly of polyglutamine proteins into amyloid-like fibrils", Proc. Natl. Acad. Sci. U. S. A. 97, 7841-7846 (2000). (Pubitemid 30460735)
45. P. J. Muchowski, K. Ning, C. D'Souza-Schorey, and S. Fields, "Requirement of an intact microtubule cytoskeleton for aggregation and inclusion body formation by a mutant huntingtin fragment", Proc. Natl. Acad. Sci. U. S. A. 99, 727-732 (2002). (Pubitemid 34106578)
46. T. Shimohata, A. Sato, J. R. Burke, W. J. Strittmatter, S. Tsuji, and O. Onodera, "Expanded polyglutamine stretches form an 'aggresome'", Neurosci. Lett. 323, 215-218 (2002). (Pubitemid 34311915)
47. Y. P. Bao, L. J. Cook, D. O'Donovan, E. Uyama, and D. C. Rubinsztein, "Mammalian, yeast, bacterial, and chemical chaperones reduce aggregate formation and death in a cell model of oculopharyngeal muscular dystrophy", J. Biol. Chem. 277(14), 12263-12269 (2002). (Pubitemid 34952794)
48. A. Wyttenbach, J. Carmichael, J. Swartz, R. A. Furlong, Y. Narain, J. Rankin, and D. C. Rubinsztein, "Effects of heat shock, heat shock protein 40 (HDJ-2), and proteasome inhibition on protein aggregation in cellular models of Huntington's disease", Proc. Natl. Acad. Sci. U. S. A. 97(6), 2898-2903 (2000). (Pubitemid 30159269)
49. J. Shorter and S. Lindquist, "Hsp104 catalyzes formation and elimination of self-replicating Sup35 prion conformers", Science 304, (5678), 1793-1797 (2004). (Pubitemid 38787894)
50. D. A. Hattendorf and S. L. Lindquist, "Cooperative kinetics of both Hsp104 ATPase domains and interdomain communication revealed by AAA sensor-1 mutants", EMBO J. 21(1-2), 12-21 (2002). (Pubitemid 34087070)
51. E. W. Jones and G. R. Fink, "Regulation of amino acid and nucleotide biosynthesis in yeast", in The Molecular Biology of the Yeast Saccharomyces: Metabolism and Gene Expression, pp. 181-299, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1982).
52. G. Moat, C. N. Wilkins, and H. Friedman, "A role for biotin in purine biosynthesis", J. Biol. Chem. 223(2), 985-991 (1956).
53. A. Ciechanover, "Intracellular protein degradation: from a vague idea, through the lysosome and the ubiquitin-proteasome system, and onto human diseases and drug targeting (Nobel lecture)", Angew. Chem. 44(37), 5944-5967 (2005). (Pubitemid 41345912)
54. B. Ravikumar, R. Duden, and D. C. Rubinsztein, "Aggregate-prone proteins with polyglutamine and polyalanine expansions are degraded by autophagy", Hum. Mol. Genet. 11(9), 1107-1117 (2002). (Pubitemid 34521091)
55. S. V. Koushik and S. S. Vogel, "Energy migration alters the fluorescence lifetime of cerulean: implications for fluorescence lifetime imaging Forster resonance transfer measurements", J. Biomed. Opt. 13(3), 031204 (2008).
56. R. Luchowski, E. G. Matveeva, I. Gryczynski, E. A. Terpetsching, L. Patsenker, G. Laczko, J. Borejdo, and Z. Gryczynski, "Single molecule studies of multiple fluorophore-labeled antibodies. Effect of Homo-FRET on the number of photons available before photobleaching", Curr. Pharm. Biotechnol. 9, 411-420 (2008).
57. S. S. Vogel, C. Thaler, P. S. Blank, and S. Koushik, "Time-resolved fluorescence anisotropy", Chap. 10 in FLIM Microscopy in Biology and Medicine, A. Periasamy and R. M. Clegg, Eds., pp. 245-288, CRC Press, Boca Raton, FL (2009).
58. M. Tramier, T. Piolot, I. Gautier, V. Mignotte, J. Coppey, K. Kemnitz, C. Durieux, and M. Coppey-Moisan, "Homo-FRET versus hetero-FRET to probe homodimers in living cells", Chap. 25 in Methods in Enzymology, Vol. 360, part A, G. Marriott and I. Parker, Eds., pp. 580-597, Academic Press, San Diego, CA (2003). (Pubitemid 36207284)
59. D. M. Jameson, J. C. Croney, and P. D. J. Moens, "Fluorescence: basic concepts, practical aspects, some anecdotes", Chap. 1 in Methods in Enzymology, Vol. 360, part A, G. Marriott and I. Parker, Eds., pp. 1-44, Academic Press (2003).
60. S. T. Hess, E. D. Sheets, A. Wagenknecht-Wiesner, and A. Heikal, "Quantitative analysis of the fluorescence properties of intrinsically fluorescent proteins in living cells", Biophys. J. 85, 2566-2580 (2003). (Pubitemid 37210802)
61. I. Gautier, M. Tramier, C. Durieux, J. Coppey, R. B. Pansu, J.-C. Nicolas, K. Kemnitz, and M. Coppey-Moisan, "Homo-FRET microscopy in living cells to measure monomer-dimer transition of GFP-tagged proteins", Biophys. J. 80, 3000-3008 (2001). (Pubitemid 32536682)
62. J. P. Vonsattel and M. DiFiglia, "Huntington disease", J. Neuropathol. Exp. Neurol. 57, 369-384 (1998). (Pubitemid 28237321)
63. T. de Cristofaro, A. Affaitati, A. Feliciello, E. V. Avvedimento, and S. Varrone, "Polyglutamine-mediated aggregation and cell death", Biochem. Biophys. Res. Commun. 272, 816-821 (2000). (Pubitemid 30420720)
64. S. Sokolov, A. Pozniakovsky, N. Bocharova, D. Knorre, and F. Severin, "Expression of an expanded polyglutamine domain in yeast causes death with apoptotic markers", Biochim. Biophys. Acta 1757, 660-666 (2006). (Pubitemid 43993870)
65. H. W. Wang, V. Gukassyan, C. T. Chen, Y. H. Wei, H. W. Guo, J. S. Yu, and F. J. Kao, "Differentiation of apoptosis from necrosis by dynamic changes of reduced nicotinamide adenine dinucleotide fluorescence lifetime in live cells", J. Biomed. Opt. 13, 054011 (2008).
66. V. Ghukasyan, Y. Y. Hsu, S. H. Kung, and F. J. Kao, "Application of fluorescence resonance energy transfer resolved by fluorescence lifetime imaging microscopy for the detection of enterovirus 71 infection in cells", J. Biomed. Opt. 12, 024016 (2007).
67. S. J. Strickler and R. A. Berg, "Relationship between absorption intensity and fluorescence lifetime of molecules", J. Chem. Phys. 37, 814-822 (1962).
68. C. L. Curl, C. J. Bellair, T. Harris, B. E. Allman, P. J. Harris, A. G. Stewart, A. Roberts, K. A. Nugent, and L. M. D. Delbridge, "Refractive index measurement in viable cells using quantitative phaseamplitude microscopy and confocal microscopy", Cytometry, Part A 65 A, 88-92 (2005). (Pubitemid 40604991)
69. W. Choi, C. Fang-Yen, K. Badizadegan, S. Oh, N. Lue, R. R. Dasari, and M. S. Feld, "Tomographic phase microscopy", Nat. Med. 4(9), 717-720 (2007).
70. S. Johnsen and E. A. Widder, "The physical basis of transparency in biological tissue: ultrastructure and the minimization of light scattering", J. Theor. Biol. 199(2), 181-198 (1999). (Pubitemid 29366544)
71. J. Beuthan, O. Minet, J. Helfmann, M. Herrig, and G. Muller, "The spatial variation of the refractive index in biological cells", Phys. Med. Biol. 41(3), 369-382 (1996). (Pubitemid 26098980)
72. B. Treanor, P. M. P. Lanigan, K. Suhling, T. Schreiber, I. Munro, M. A. A. Neil, D. Phillips, D. M. Davis, and P. M. W. French, "Imaging fluorescence lifetime heterogeneity applied to GFP-tagged MHC protein at an immunological synapse", J. Microsc. 217(1), 36-43 (2005). (Pubitemid 40188358)
73. C. Tregidgo, J. A. Levitt, and K. Suhling, "Effect of refractive index on the fluorescence lifetime of green fluorescent protein", J. Biomed. Opt. 13, 031218 (2008).
74. H. J. van Manen, P. Verkuijlen, P. Wittendorp, V. Subramaniam, T. K. van den Berg, D. Roos, and C. Otto, "Refractive index sensing of green fluorescent proteins in living cells using fluorescence lifetime imaging microscopy", Biophys. J. 94(8), 67-69 (2008).
75. D. Toptygin, R. S. Savtchenko, N. D. Meadow, S. Roseman, and L. Brand, "Effect of the solvent refractive index on the excited-state lifetime of a single tryptophan residue in a protein", J. Phys. Chem. B 106(14), 3724-3734 (2002). (Pubitemid 35295426)
76. M. M. G. Krishna and N. Periasamy, "Fluorescence of organic dyes in lipid membranes: site of solubilization and effects of viscosity and refractive index on lifetimes", J. Fluoresc. 8(1), 81-91 (1998). (Pubitemid 128696616)