Rational design of an efficient, genetically encodable, protein-encased singlet oxygen photosensitizer

Journal of the American Chemical Society

Volumn 137, Issue 4, 2015, Pages 1632-1642

  Westberg, Michael ^a   Holmegaard, Lotte ^a   Pimenta, Frederico M ^a   Etzerodt, Michael ^b   Ogilby, Peter R ^a  

^a Center for Oxygen Microscopy and Imaging Chemistry Department   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CHROMOPHORES; HYDROGEN BONDS; ISOTOPES; OXYGEN; PHOTOSENSITIZERS; PROTEINS;

AMINO ACID RESIDUES; ELECTRON-TRANSFER REACTIONS; FLAVIN MONO NUCLEOTIDES (FMN); FORMATION KINETICS; MECHANISTIC STUDIES; PHOTOPHYSICAL PARAMETERS; RATIONAL DESIGN; SOLVENT ISOTOPE EFFECTS;

CELL SIGNALING;

AMINO ACID; FLAVINE MONONUCLEOTIDE; PHOTOSENSITIZING AGENT; PROTEIN; SINGLET OXYGEN; FLAVIN MONONUCLEOTIDE SEMIQUINONE; HYBRID PROTEIN; PHOTOTROPIN;

ACCURACY; ARTICLE; CHEMICAL REACTION KINETICS; ELECTRON TRANSPORT; HYDROGEN BOND; MUTATION; SIGNAL TRANSDUCTION; ARABIDOPSIS; CHEMICAL STRUCTURE; CHEMISTRY; ESCHERICHIA COLI; GENETICS; METABOLISM; PROTEIN TERTIARY STRUCTURE; SITE DIRECTED MUTAGENESIS;

ARABIDOPSIS; ESCHERICHIA COLI; FLAVIN MONONUCLEOTIDE; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PHOTOSENSITIZING AGENTS; PHOTOTROPINS; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; SINGLET OXYGEN;

EID: 84922473560     PISSN: 00027863     EISSN: 15205126     Source Type: Journal    
DOI: 10.1021/ja511940j     Document Type: Article

References (81)

1. Clennan, E. L.; Pace, A. Tetrahedron 2005, 61, 6665-6691
2. Davies, M. J. Biochem. Biophys. Res. Commun. 2003, 305, 761-770
3. Ogilby, P. R. Chem. Soc. Rev. 2010, 39, 3181-3209
4. Redmond, R. W.; Kochevar, I. E. Photochem. Photobiol. 2006, 82, 1178-1186
5. Klotz, L.-O.; Kröncke, K.-D.; Sies, H. Photochem. Photobiol. Sci. 2003, 2, 88-94
6. Blázquez-Castro, A.; Breitenbach, T.; Ogilby, P. R. Photochem. Photobiol. Sci. 2014, 13, 1235-1240
7. Schweitzer, C.; Schmidt, R. Chem. Rev. 2003, 103, 1685-1757
8. Kim, S.; Tachikawa, T.; Fujitsuka, M.; Majima, T. J. Am. Chem. Soc. 2014, 136, 11707-11715
9. Pedersen, S. K.; Holmehave, J.; Blaikie, F. H.; Gollmer, A.; Breitenbach, T.; Jensen, H. H.; Ogilby, P. R. J. Org. Chem. 2014, 79, 3079-3087
10. Pimenta, F. M.; Jensen, J. K.; Etzerodt, M.; Ogilby, P. R. Photochem. Photobiol. Sci. 2015, 10.1039/c1034pp00408f
11. Bulina, M. E.; Chudakov, D. M.; Britanova, O. V.; Yanushevich, Y. G.; Staroverov, D. B.; Chepurnykh, T. V.; Merzlyak, E. M.; Shkrob, M. A.; Lukyanov, S.; Lukyanov, K. A. Nat. Biotechnol. 2006, 24, 95-99
12. Jimenez-Banzo, A.; Ragas, X.; Abbruzzetti, S.; Viappiani, C.; Campanini, B.; Flors, C.; Nonell, S. Photochem. Photobiol. Sci. 2010, 9, 1336-1341
13. Takemoto, K.; Matsuda, T.; Sakai, N.; Fu, D.; Noda, M.; Uchiyama, S.; Kotera, I.; Arai, Y.; Horiuchi, M.; Fukui, K.; Ayabe, T.; Inagaki, F.; Suzuki, H.; Nagai, T. Sci. Rep. 2013, 3, 2629
14. Shu, X.; Lev-Ram, V.; Deerinck, T. J.; Qi, Y.; Ramko, E. B.; Davidson, M. W.; Jin, Y.; Ellisman, M. H.; Tsien, R. Y. PLoS Biology 2011, 9, e1001041
15. Ragàs, X.; Cooper, L. P.; White, J. H.; Nonell, S.; Flors, C. ChemPhysChem 2011, 12, 161-165
16. Torra, J.; Burgos-Caminal, A.; Endres, S.; Wingen, M.; Drepper, T.; Gensch, T.; Ruiz-González, R.; Nonell, S. Photochem. Photobiol. Sci. 2015, 10.1039/c4PP00338A
17. Vegh, R. B.; Solntsev, K. M.; Kuimova, M. K.; Cho, S.; Liang, Y.; Loo, B. L. W.; Tolbert, L. M.; Bommarius, A. S. Chem. Commun. 2011, 47, 4887-4889
18. Pimenta, F. M.; Jensen, R. L.; Breitenbach, T.; Etzerodt, M.; Ogilby, P. R. Photochem. Photobiol. 2013, 89, 1116-1126
19. Ruiz-González, R.; Cortajarena, A. L.; Mejias, S. H.; Agut, M.; Nonell, S.; Flors, C. J. Am. Chem. Soc. 2013, 135, 9564-9567
20. Görner, H. J. Photochem. Photobiol. B: Biol. 2007, 87, 73-80
21. Heelis, P. F. Chem. Soc. Rev. 1982, 11, 15-39
22. Lu, C.; Lin, W.; Wang, W.; Han, Z.; Yao, S.; Lin, N. Phys. Chem. Chem. Phys. 2000, 2, 329-334
23. Kay, C. W. M.; Schleicher, E.; Kuppig, A.; Hofner, H.; Rudiger, W.; Schleicher, M.; Fischer, M.; Bacher, A.; Weber, S.; Richter, G. J. Biol. Chem. 2003, 278, 10973-10982
24. Lanzl, K.; Sanden-Flohe, M.; Kutta, R.-J.; Dick, B. Phys. Chem. Chem. Phys. 2010, 12, 6594-6604
25. Eisenreich, W.; Fischer, M.; Romisch-Margl, W.; Joshi, M.; Richter, G.; Bacher, A.; Weber, S. Biochem. Soc. Trans. 2009, 37, 382-386
26. Kutta, R. J.; Magerl, K.; Kensy, U.; Dick, B. Photochem. Photobiol. Sci. 2015, 10.1039/c4PP00155a
27. Yagi, K.; Ohishi, N.; Nishimoto, K.; Choi, J. D.; Song, P. S. Biochemistry 1980, 19, 1553-1557
28. Miura, R. Chem. Rec. 2001, 1, 183-194
29. Raffelberg, S.; Mansurova, M.; Gärtner, W.; Losi, A. J. Am. Chem. Soc. 2011, 133, 5346-5356
30. Valle, L.; Vieyra, F. E. M.; Borsarelli, C. D. Photochem. Photobiol. Sci. 2012, 11, 1051-1061
31. Nishimoto, K.; Fukumaga, H.; Yagi, K. J. Biochem. 1986, 100, 1647-1653
32. Nonell, S.; Gonzalez, M.; Trull, F. R. Afinidad 1993, 448, 445-450
33. Available at: http://www.tsienlab.ucsd.edu/Samples/Constructs.htm.
34. Arnbjerg, J.; Johnsen, M.; Frederiksen, P. K.; Braslavsky, S. E.; Ogilby, P. R. J. Phys. Chem. A 2006, 110, 7375-7385
35. Salice, P.; Arnbjerg, J.; Pedersen, B. W.; Toftegaard, R.; Beverina, L.; Pagani, G. A.; Ogilby, P. R. J. Phys. Chem. A 2010, 114, 2518-2525
36. Bazin, M.; Ebbesen, T. W. Photochem. Photobiol. 1983, 37, 675-678
37. Arnold, K.; Bordoli, L.; Kopp, J.; Schwede, T. Bioinformatics 2006, 22, 195-201
38. Christie, J. M.; Hitomi, K.; Arvai, A. S.; Hartfield, K. A.; Mettlen, M.; Pratt, A. J.; Tainer, J. A.; Getzoff, E. D. J. Biol. Chem. 2012, 287, 22295-22304
39. Losi, A.; Gärtner, W. Photochem. Photobiol. 2011, 87, 491-510
40. List, N. H.; Pimenta, F. M.; Holmegaard, L.; Jensen, R. L.; Etzerodt, M.; Schwabe, T.; Kongsted, J.; Ogilby, P. R.; Christiansen, O. Phys. Chem. Chem. Phys. 2014, 16, 9950-9959
41. Salomon, M.; Christie, J. M.; Knieb, E.; Lempert, U.; Briggs, W. R. Biochemistry 2000, 39, 9401-9410
42. Jones, M. A.; Feeney, K. A.; Kelly, S. M.; Christie, J. M. J. Biol. Chem. 2007, 282, 6405-6414
43. Zayner, J. P.; Antoniou, C.; French, A. R.; Hause, R. J.; Sosnick, T. R. Biophys. J. 2013, 105, 1027-1036
44. Schüttrigkeit, T. A.; Kompa, C. K.; Salomon, M.; Rüdiger, W.; Michel-Beyerle, M. E. Chem. Phys. 2003, 294, 501-508
45. Klaumünzer, B.; Kröner, D.; Saalfrank, P. J. Phys. Chem. B 2010, 114, 10826-10834
46. Wingen, M.; Potzkei, J.; Endres, S.; Casini, G.; Rupprecht, C.; Fahlke, C.; Krauss, U.; Jaeger, K.-E.; Drepper, T.; Gensch, T. Photochem. Photobiol. Sci. 2014, 13, 875-883
47. Nash, A. I.; Ko, W.-H.; Harper, S. M.; Gardner, K. H. Biochemistry 2008, 47, 13842-13849
48. Nozaki, D.; Iwata, T.; Ishikawa, T.; Todo, T.; Tokutomi, S.; Kandori, H. Biochemistry 2004, 43, 8373-8379
49. Massey, V. Biochem. Soc. Trans. 2000, 28, 283-296
50. Li, H.; Melø, T. B.; Naqvi, K. R. J. Photochem. Photobiol., B 2012, 106, 34-39
51. Walrant, P.; Santus, R. Photochem. Photobiol. 1974, 19, 411-417
52. Fukunaga, Y.; Katsuragi, Y.; Izumi, T.; Sakiyama, F. J. Biochem. 1982, 92, 129-141
53. IUPAC Solubility Data Series; Battino, R., Ed.; Pergamon Press: Oxford, 1981; Vol. 7: Oxygen and Ozone.
54. Montalti, M.; Credi, A.; Prodi, L.; Gandolfi, M. T. Handbook of Photochemistry; 3 rd ed.; CRC Press: Boca Raton, 2006.
55. Bauer, C.; Rabi, C.-R.; Heberle, J.; Kottke, T. Photochem. Photobiol. 2011, 87, 548-553
56. Lee, C.-T.; Malzahn, E.; Brunner, M.; Mayer, M. P. J. Mol. Biol. 2014, 426, 601-610
57. Cioni, P.; Strambini, G. B. Biophys. J. 2002, 82, 3246-3253
58. Parker, M. J.; Clarke, A. R. Biochemistry 1997, 36, 5786-5794
59. Katz, J. J.; Crespi, H. L. In Isotope Effects in Chemical Reactions (ACS Monograph 167); Collins, C. J.; Bowman, N. S., Eds.; Van Nostrand Reinhold: New York, 1970; p 286-363.
60. Ogilby, P. R.; Foote, C. S. J. Am. Chem. Soc. 1983, 105, 3423-3430
61. Ermolaev, V. L.; Sveshnikova, E. B. J. Lumin. 1979, 20, 387-395
62. Beeby, A.; Parker, A. W.; Simpson, M. S. C.; Phillips, D. J. Photochem. Photobiol., B 1992, 16, 73-81
63. Nitzan, A. Chemical Dynamics in Condensed Phases: Relaxation, Transfer, and Reactions in Condensed Molecular Systems; Oxford University Press: Oxford, 2006.
64. Klán, P.; Wirz, J. Photochemisrtry of Organic Compounds; Wiley: Chichester, 2009.
65. Siebrand, W. J. Chem. Phys. 1967, 47, 2411-2422
66. Yang, H.; Luo, G.; Karnchanaphanurach, P.; Louie, T.-M.; Rech, I.; Cova, S.; Xun, L.; Xie, X. S. Science 2003, 302, 262-266
67. Liu, X.; Jiang, L.; Li, J.; Wang, L.; Yu, Y.; Zhou, Q.; Lu, X.; Gong, W.; Lu, Y.; Wang, J. J. Am. Chem. Soc. 2014, 136, 13094-13097
68. Pimenta, F. M.; Jensen, R. L.; Holmegaard, L.; Esipova, T. V.; Westberg, M.; Breitenbach, T.; Ogilby, P. R. J. Phys. Chem. B 2012, 116, 10234-10246
69. Jensen, R. L.; Arnbjerg, J.; Ogilby, P. R. J. Am. Chem. Soc. 2012, 134, 9820-9826
70. Lepeshkevich, S. V.; Parkhats, M. V.; Stasheuski, A. S.; Britikov, V. V.; Jarnikova, E. S.; Usanov, S. A.; Dzhagarov, B. M. J. Phys. Chem. A 2014, 118, 1864-1878
71. Scurlock, R. D.; Mártire, D. O.; Ogilby, P. R.; Taylor, V. L.; Clough, R. L. Macromolecules 1994, 27, 4787-4794
72. Marti, C.; Jürgens, O.; Cuenca, O.; Casals, M.; Nonell, S. J. Photochem. Photobiol., A 1996, 97, 11-18
73. Baier, J.; Maisch, T.; Maier, M.; Engel, E.; Landthaler, M.; Bäumler, W. Biophys. J. 2006, 91, 1452-1459
74. Gomes, A.; Fernandes, E.; Lima, J. L. F. C. J. Biochem. Biophys. Methods 2005, 65, 45-80
75. Bilski, P. J.; Karriker, B.; Chignell, C. F. Chem. Phys. Lett. 2009, 475, 116-119
76. Bindokas, V. P.; Jordan, J.; Lee, C. C.; Miller, R. J. J. Neurosci. 1996, 16, 1324-1336
77. To, T.-L.; Fadul, M. J.; Shu, X. Nat. Comm. 2014, 5, 4072
78. Wilkinson, F.; Helman, W. P.; Ross, A. B. J. Phys. Chem. Ref. Data 1995, 24, 663-1021
79. Heelis, P. F.; Parsons, B. J.; Phillips, G. O.; McKellar, J. F. Photochem. Photobiol. 1978, 28, 169-173
80. Lin, J. Y.; Sann, S. B.; Zhou, K.; Nabavi, S.; Proulx, C. D.; Malinow, R.; Jin, Y.; Tsien, R. Y. Neuron 2013, 79, 241-253
81. Ryumina, A. P.; Serebrovskaya, E. O.; Shirmanova, M. V.; Snopova, L. B.; Kuznetsova, M. M.; Turchin, I. V.; Ignatova, N. I.; Klementieva, N. V.; Fradkov, A. F.; Shaklov, B. E.; Zagaynova, E. V.; Lukyanov, K. A.; Lukyanov, S. A. Biochem. Biophys. Acta 2013, 1830, 5059-5067