Chromophore photoreduction in red fluorescent proteins is responsible for bleaching and phototoxicity

Journal of Physical Chemistry B

Volumn 118, Issue 17, 2014, Pages 4527-4534

  Vegh, Russell B ^a   Bravaya, Ksenia B ^b   Bloch, Dmitry A ^c   Bommarius, Andreas S ^a,d   Tolbert, Laren M ^a   Verkhovsky, Michael ^c   Krylov, Anna I ^b   Solntsev, Kyril M ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF HELSINKI   (Finland)

^d Georgia Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTRONIC STRUCTURE; ENERGY TRANSFER; FLUORESCENCE; PHOTOBLEACHING; PROTEINS;

ELECTRONIC STRUCTURE CALCULATIONS; EXPERIMENTAL EVIDENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; PHOTOINDUCED DYNAMICS; RED FLUORESCENT PROTEINS; SUPER-RESOLUTION MICROSCOPY; TIME-RESOLVED OPTICAL SPECTROSCOPY; TRANSIENT ABSORPTION;

CHROMOPHORES;

PHOTOPROTEIN; RED FLUORESCENT PROTEIN;

BLEACHING; CHEMICAL STRUCTURE; CHEMISTRY; KINETICS; LIGHT; PROTEIN CONFORMATION; THERMODYNAMICS;

KINETICS; LIGHT; LUMINESCENT PROTEINS; MODELS, MOLECULAR; PHOTOBLEACHING; PROTEIN CONFORMATION; THERMODYNAMICS;

EID: 84899830310     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp500919a     Document Type: Article

References (59)

1. Tsien, R. Y. The green fluorescent protein Annu. Rev. Biochem. 1998, 67, 509-544
2. Verkhusha, V. V.; Lukyanov, K. A. The molecular properties and applications of anthozoa fluorescent proteins and chromoproteins Nat. Biotechnol. 2004, 22, 289-296
3. Subach, F. V.; Verkhusha, V. V. Chromophore transformations in red fluorescent proteins Chem. Rev. 2012, 112, 4308-4327
4. Lecoq, J.; Schnitzer, M. J. An infrared fluorescent protein for deeper imaging Nat. Biotechnol. 2011, 29, 715716
5. Giepmans, B. N. G.; Adams, S. R.; Ellisman, M. H.; Tsien, R. Y. The fluorescent toolbox for assessing protein location and function Science 2006, 312, 217
6. Chalfie, M.; Tu, Y.; Euskirchen, G.; Ward, W. W.; Prasher, D. C. Green fluorescent protein as a marker for gene expression Science 1994, 263, 802-805
7. Kneen, M.; Farinas, J.; Li, Y.; Verkman, A. S. Green fluorescent protein as a noninvasive intracellular pH indicator Biophys. J. 1998, 74, 1591-1599
8. 2+ sensors with increased dynamic range BMC Biotechnol. 2007, 7, 37
9. Barondeau, D. P.; Kassmann, C. J.; Tainer, J. A.; Getzoff, E. D. Structural chemistry of a green fluorescent protein zn biosensor J. Am. Chem. Soc. 2002, 124, 3522-3524
10. Meyer, A. J.; Dick, T. P. Fluorescent protein-based redox probes Antioxid. Redox Signal. 2010, 13, 621-650
11. Lukyanov, K. A.; Belousov, V. V. Genetically encoded fluorescent redox sensors Biochim. Biophys. Acta 2014, 1840, 745-756
12. Belousov, V. V.; Fradkov, A. F.; Lukyanov, K. A.; Staroverov, D. B.; Shakhbazov, K. S.; Terskikh, A. V.; Lukyanov, S. Genetically encoded fluorescent indicator for intracellular hydrogen peroxide Nat. Methods 2006, 3, 281-286
13. McLean, M. A.; Rajfur, Z.; Chen, Z.; Humphrey, D.; Yang, B.; Sligar, S. G.; Jacobson, K. Mechanism of chromophore assisted laser inactivation employing fluorescent proteins Anal. Chem. 2009, 81, 1755-1761
14. Bulina, M. E.; Chudakov, D. M.; Britanova, O. V.; Yanushevich, Y. G.; Shkrob, M. A.; Lukyanov, S.; Lukyanov, K. A. A genetically encoded photosensitizer Nat. Biotechnol. 2006, 24, 95-99
15. Dean, K. M.; Lubbeck, J. L.; Binder, J. K.; Schwall, L. R.; Jimenez, R.; Palmer, A. E. Analysis of red-fluorescent proteins provides insight into dark-state conversion and photodegradation Biophys. J. 2011, 101, 961-969
16. Schenk, S.; Ivanchenko, S.; Röcker, C.; Wiedenmann, J.; Nienhaus, G. U. Photodynamics of red fluorescent proteins studied by fluorescence correlation spectroscopy Biophys. J. 2004, 86, 384-394
17. Ha, T.; Tinnefeld, P. Photophysics of fluorescent probes for single-molecule biophysics and super-resolution and imaging Annu. Rev. Phys. Chem. 2012, 63, 595-617
18. Adam, V.; Carpentier, P.; Violot, S.; Lelimousin, M.; Darnault, C.; Nienhaus, G. U.; Bougeois, D. Structural basis of X-ray induced transient photobleaching in a photactivable green fluorescent protein J. Am. Chem. Soc. 2009, 131, 18063-18065
19. Roy, A.; Field, M. J.; Adam, V.; Bourgeois, D. The nature of transient dark states in photoactivatable fluorescent protein J. Am. Chem. Soc. 2011, 133, 18586-18589
20. Pletnev, S.; Gurskaya, N. G.; Pletneva, N. V.; Lukyanov, K. A.; Chudakov, D. M.; Martynov, V. I.; Popov, V. O.; Kovalchuk, M. V.; Wlodawer, A.; Dauter, Z. Structural basis for phototoxicity of the genetically encoded photosensitizer KillerRed J. Biol. Chem. 2009, 284, 32028-32039
21. Carpentier, P.; Violot, S.; Blanchoin, L.; Bourgeois, D. Structural basis for the phototoxicity of the fluorescent protein killerred FEBS Lett. 2009, 583, 2839-2842
22. Bogdanov, A. M.; Mishin, A. S.; Yampolsky, I. V.; Belousov, V. V.; Chudakov, D. M.; Subach, F. V.; Verkhusha, V. V.; Lukyanov, S.; Lukyanov, K. A. Green fluorescent proteins are light-induced electron donors Nat. Chem. Biol. 2009, 5, 459-461
23. Epifanovsky, E.; Polyakov, I.; Grigorenko, B. L.; Nemukhin, A. V.; Krylov, A. I. The effect of oxidation on the electronic structure of the green fluorescent protein chromophore J. Chem. Phys. 2010, 132, 115104
24. Bravaya, K.; Khrenova, M. G.; Grigorenko, B. L.; Nemukhin, A. V.; Krylov, A. I. The effect of protein environment on electronically excited and ionized states of the green fluorescent protein chromophore J. Phys. Chem. B 2011, 8, 8296-8303
25. Vegh, R. B.; Solntsev, K. M.; Kuimova, M. K.; Cho, S.; Liang, Y.; Loo, B. L. W.; Tolbert, L. M.; Bommarius, A. S. Reactive oxygen species in photochemistry of the red fluorescent protein "Killer Red" Chem. Commun. 2011, 47, 4887-4889
26. Bulina, M. E.; Lukyanov, K. A.; Britanova, O. V.; Onichtchouk, D.; Lukyanov, S.; Chudakov, D. M. Chromophore-assisted light inactivation (CALI) using the phototoxic fluorescent protein KillerRed Nat. Protoc. 2006, 1, 947-953
27. Grigorenko, B. L.; Nemukhin, A. V.; Morozov, D. I.; Polyakov, I.; Bravaya, K. B.; Krylov, A. I. Towards molecular-level characterization of photo-induced decarboxylation of the green fluorescent protein: Accessibility of the charge-transfer states J. Chem. Theory Comput. 2012, 8, 1912-1920
28. Ding, L.; Chung, L. W.; Morokuma, K. Reaction mechanism of photoinduced decarboxylation of the photoactivatable green fluorescent protein: an ONIOM(QM:MM) study J. Phys. Chem. B 2013, 117, 1075-1084
29. van Thor, J. J.; Gensch, T.; Hellingwerf, K. J.; Johnson, L. N. Phototransformation of green fluoresecent protein with UV and visible light leads to decarboxilation of glutamate 222 Nat. Struct. Biol. 2002, 9, 37-41
30. Bell, A. F.; Stoner-Ma, D.; Wachter, R. M.; Tonge, P. J. Light-driven decarboxylation of wild-type green fluorescent protein J. Am. Chem. Soc. 2003, 125, 6919-6926
31. Habuchi, S.; Cotlet, M.; Gensch, T.; Bednarz, T.; Haber-Pohlmeier, S.; Rozenski, J.; Dirix, G.; Michiels, J.; Vanderleyden, J.; Heberle, J. Evidence for the isomerization and decarboxylation in the photoconversion of the red fluorescent protein dsred J. Am. Chem. Soc. 2005, 127, 8977-8984
32. Chapagain, P. P.; Regmi, C.; Castillo, W. Fluorescent protein barrel fluctuations and oxygen diffusion pathways in mCherry J. Chem. Phys. 2011, 135, 235101
33. Laurent, A. D.; Mironov, V. A.; Chapagain, P. P.; Nemukhin, A. V.; Krylov, A. I. Exploring structural and optical properties of fluorescent proteins by squeezing: Modeling high-pressure effects on the mStrawberry and mCherry red fluorescent proteins J. Phys. Chem. B 2012, 116, 12426-12440
34. Hales, J. M.; Cozzuol, M.; Screen, T. E. O.; Anderson, H. L.; Perry, J. W. Metalloporphyrin polymer with temporally agile, broadband nonlinear absorption for optical limiting in the near infrared Opt. Exp. 2009, 17, 18478-18488
35. Belevich, I.; Gorbikova, E.; Belevich, N. P.; Rauhamäki, V.; Wikström, M.; Verkhovsky, M. I. Initiation of the proton pump of cytochrome c oxidase Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 18469-18474
36. Borisov, V. B.; Belevich, I.; Bloch, D. A.; Mogi, T.; Verkhovsky, M. I. Glutamate 107 in subunit i of cytochrome bd from Escherichia coli is part of a transmembrane intraprotein pathway conducting protons from the cytoplasm to the heme b(595)/heme d active site Biochemistry 2008, 47, 7907-7914
37. Belevich, I.; Bloch, D. A.; Belevich, N.; Wikström, M.; Verkhovsky, M. I. Exploring the proton pump mechanism of cytochrome c oxidase in real time Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 2685-2690
38. Bravaya, K. B.; Subach, O.; Korovina, N.; Verkhusha, V. V.; Krylov, A. I. An insight into the common mechanism of the chromophore formation in the red fluorescent proteins: The elusive blue intermediate revealed J. Am. Chem. Soc. 2012, 134, 2807-2814
39. Bravaya, K.; Grigorenko, B. L.; Nemukhin, A. V.; Krylov, A. I. Quantum chemistry behind bioimaging: Insights from ab initio studies of fluorescent proteins and their chromophores Acc. Chem. Res. 2012, 45, 265-275
40. PROPKA, http://propka.ki.ku.dk.
41. Hess, B.; Kutzner, C.; van der Spoel, D.; Lindahl, E. GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 2008, 4, 435447
42. Bussi, G.; Donadio, D.; Parrinello, M. Canonical sampling through velocity rescaling J. Chem. Phys. 2007, 126, 014101
43. Nosé, S.; Klein, M. L. Constant pressure molecular dynamics for molecular systems Mol. Phys. 1983, 50, 10551076
44. Chai, J.-D.; Head-Gordon, M. Long-range corrected hybrid density functionals with damped atom-atom dispersion interactions Phys. Chem. Chem. Phys. 2008, 10, 6615-6620
45. Glendening, E. D.; Badenhoop, J. K.; Reed, A. E.; Carpenter, J. E.; Weinhold, F. NBO 4.0; Theoretical Chemistry Institute, University of Wisconsin: Madison, WI, USA, 1996.
46. Reuter, N.; Lin, H.; Thiel, W. Green fluorescent proteins: Empirical force field for the neutral and deprotonated forms of the chromophore. Molecular dynamics simulations of the wild type and S65T mutant J. Phys. Chem. B 2002, 106, 6310-6321
47. Rhee, Y. M.; Head-Gordon, M. Scaled second order perturbation corrections to configuration interaction singles: efficient and reliable excitation energy methods J. Phys. Chem. A 2007, 111, 5314-5326
48. Grigorenko, B. L.; Nemukhin, A. V.; Polyakov, I.; Krylov, A. I. Triple-decker motif for red-shifted fluorescent protein mutants J. Phys. Chem. Lett. 2013, 4, 11815-11822
49. Grigorenko, B. L.; Nemukhin, A. V.; Polyakov, I.; Morozov, D.; Krylov, A. I. First-principle characterization of the energy landscape and optical spectra of the green fluorescent protein along A-I-B proton transfer route J. Am. Chem. Soc. 2013, 135, 11541-11549
50. Bravaya, K. B.; Epifanovsky, E.; Krylov, A. I. Four bases score a run: Ab initio calculations quantify a cooperative effect of h-bonding and pi-stacking on ionization energy of adenine in the AATT tetramer J. Phys. Chem. Lett. 2012, 3, 2726-2732
51. Shao, Y.; Fusti-Molnar, L.; Jung, Y.; Kussmann, J.; Ochsenfeld, C.; Brown, S.; Gilbert, A. T. B.; Slipchenko, L. V.; Levchenko, S. V.; O'Neill, D. P. Advances in methods and algorithms in a modern quantum chemistry program package Phys. Chem. Chem. Phys. 2006, 8, 3172-3191
52. Malvezzi-Campeggi, F.; Jahnz, M.; Heinze, K. G.; Dittrich, P.; Schwille, P. Light-induced flickering of dsred provides evidence for distinct and interconvertible fluorescent states Biophys. J. 2001, 81, 1776-1785
53. Hendrix, J.; Flors, C.; Dedecker, P.; Hofkens, J.; Engelbroghs, Y. Dark states of monomeric red fluorescent proteins studies by fluorescence correlation and single molecule spectroscopy Biophys. J. 2008, 94, 4103-4113
54. Close, D. M. Calculated vertical ionization energies of the common r-amino acids in the gas phase and in solution J. Phys. Chem. A 2009, 115, 2900-2912
55. Larsen, D. Private communication.
56. Wilson, K. R.; Jimenez-Cruz, M.; Nicolas, C.; Belau, L.; Leone, S. R.; Ahmed, M. Thermal vaporization of biological nanoparticles: fragment-free vacuum untraviolet photoionization mass spectra of tryptophan, phenylalanine-glycine- glycine, and β-carotene J. Phys. Chem. A 2006, 110, 2106-2113
57. Vogelsang, J.; Kasper, R.; Steinhauer, C.; Person, B.; Heilemann, M.; Sauer, M.; Tinnefeld, P. A reducing and oxidizing system minimizes photobleaching and blinking of fluorescent dyes Angew. Chem. Int. Ed. 2008, 47, 5456-5469
58. Greenbaum, L.; Lavie, C.; Rothmann, R.; Malik, Z. Green fluorescent protein photobleaching: a model for protein damage by endogenous and exogenous singlet oxygen Biol. Chem. 2000, 381, 12511258
59. Besley, N. A.; Gilbert, A. T. B.; Gill, P. M. W. Self-consistent-field calculations of core excited states J. Chem. Phys. 2009, 130, 124308