Physicochemical mechanism of light-driven DNA repair by (6-4) photolyases

Annual Review of Physical Chemistry

Volumn 65, Issue , 2014, Pages 275-292

  Faraji, Shirin ^a   Dreuw, Andreas ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

(6 4) photolesion; DNA photolyase; electron transfer; excited states; proton transfer; pyrimidine dimer

Indexed keywords

DNA; ELECTRON TRANSITIONS; ENERGY TRANSFER; EXCITED STATES; FREE RADICAL REACTIONS; RESTORATION;

(6-4) PHOTOLESION; DNA PHOTOLYASE; ELECTRON TRANSFER; EXCITED-STATES; LIGHT DRIVEN; PHOTO-INDUCED ELECTRON TRANSFER; PHOTOLYASES; PHYSICO-CHEMICAL MECHANISMS; PYRIMIDINE DIMER; SPLITTINGS;

AROMATIC COMPOUNDS;

DEOXYRIBODIPYRIMIDINE PHOTOLYASE; DNA;

ANIMAL; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; DNA REPAIR; GENETICS; HUMAN; LIGHT; METABOLISM;

ANIMALS; BINDING SITES; DEOXYRIBODIPYRIMIDINE PHOTO-LYASE; DNA; DNA REPAIR; HUMANS; LIGHT; MODELS, MOLECULAR;

EID: 84897531334     PISSN: 0066426X     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-physchem-040513-103626     Document Type: Article

References (81)

1. Sinha RP, Hader D-P. 2002. UV-induced DNA damage and repair: A review. Photochem. Photobiol. Sci. 1:225-36
2. Essen LO, Klar T. 2006. Light-driven DNA repair by photolyases. Cell. Mol. Life Sci. 63:1266-77
3. Weber S. 2005. Light-driven enzymatic catalysis of DNA repair: A review of recent biophysical studies on photolyase. Biochim. Biophys. Acta 1707:1-23
4. Kamiya H, Iwai S, Kasai H. 1998. The (6-4) photoproduct of thymine-Thymine induces targeted substitution mutations in mammalian cells. Nucleic Acids Res. 26:2611-17
5. Carrier WL, Snyder RD, Regan JD. 1982. The Science of Photomedicine. New York: Plenum
6. Taylor J-S. 1995. DNA, sunlight and skin cancer. Pure Appl. Chem. 67:183-90
7. Matsumura Y, Ananthaswamy H. 2002. Molecular mechanisms of photocarcinogenesis. Front. Biosci. 7:D765-83
8. Sanders DB, Wiest O. 2010. A model for the enzyme-substrate complex of DNA photolyase and photodamaged DNA. J. Am. Chem. Soc. 121:5127-34
9. Büchi G, Inman CG, Lipinsky ES. 1954. Light-catalyzed organic reactions. I. The reaction of carbonyl compounds with 2-methyl-2-butene in the presence of ultraviolet light. J. Am. Chem. Soc. 76:4327-31
10. Baccarelli I, Bald I, Gianturco FA, Illenberger E, Kopyra J. 2011. Electron-induced damage of DNA and its components: Experiments and theoretical models. Phys. Rep. 508:1-44
11. Glas AF, Schneider S, Maul MJ, Hennecke U, Carell T. 2009. Crystal structure of the T(6-4)C lesion in complex with a (6-4) DNA photolyase and repair of UV-induced (6-4) and Dewar photolesions. Eur. J. Chem. 15:10387-96
12. Wang Y, Gaspar PP, Taylor JS. 2000. Quantum chemical study of the electron-Transfer-catalyzed splitting of oxetane and azetidine intermediates proposed in the photoenzymatic repair of (6-4) photoproducts of DNA. J. Am. Chem. Soc. 122:5510-19
13. Faraji S, Wirz L, Dreuw A. 2013. Quantum chemical study of the enzymatic repair of T(6-4)C/C(6-4)T UV photolesions by DNA photolyases. Chem. Phys. Chem. 14:2817-24
14. May NL, Egly J, Coin F. 2010. True lies: The double life of the nucleotide excision repair factors in transcription and DNA repair. J. Nucleic Acids 2010:616342
15. Reardon JT, Sancar A. 2003. Recognition and repair of the cyclobutane thymine dimer, a major cause of skin cancers, by the human excision nuclease. Genes Dev. 17:2539-51
16. Liu Y, Prasad R, Beard WA, Kedar PS, Hou EW, et al. 2007. Coordination of steps in single-nucleotide base excision repair mediated by apurinic/apyrimidinic endonuclease 1 and DNA polymerase. J. Biol. Chem. 282:13532-41
17. SelbyCP, Sancar A. 2006.Acryptochrome/photolyase class of enzymes with single-strandedDNA-specific photolyase activity. Proc. Natl. Acad. Sci. USA 103:17696-700
18. Sancar A. 2003. Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chem. Rev. 103:2203-37
19. Zhao X, Liu J, Hsu DS, Zhao S, Taylor JS, Sancar A. 1997. Reaction mechanism of (6-4) photolyase. J. Biol. Chem. 272:32580-90
20. Okamura T, Sancar A, Heelis P, Begley T, Hirata Y, Mataga N. 1991. Picosecond laser photolysis studies on the photorepair of pyrimidine dimers by DNA photolyase. 1. Laser photolysis of photolyase-2-deoxyuridine dinucleotide photodimer complex. J. Am. Chem. Soc. 113:3143-45
21. Todo T, Takemori H, Ryo H, Ihara M, Matsunaga T, et al. 1993. A new photoreactivating enzyme that specifically repairs ultraviolet light-induced (6-4) photoproducts. Nature 361:371-74
22. Rupert CS, Goodgal SH, Herriott RM. 1958. Photoreactivation in vitro of ultraviolet-inactivated Hemophilus influenzae transforming factor. J. Gen. Physiol. 41:451-71
23. Sancar A. 2008. Structure and function of photolyase and in vivo enzymology: 50th anniversary. J. Biol. Chem. 283:32153-57
24. Hahn J, Michel-Beyerle ME, Rösch N. 1998. Conformation of the flavin adenine dinucleotide cofactor FAD in DNA-photolyase: A molecular dynamics study. Mol. Model. Annu. 4:73-82
25. Kao Y-T, Saxena C, He T-F, Guo L, Wang L, et al. 2008. Ultrafast dynamics of flavins in five redox states. J. Am. Chem. Soc. 130:13132-39
26. Malhotra K, Kim ST, WalshC, Sancar A. 1992. Roles of FADand 8-hydroxy-5-deazaflavin chromophores in photoreactivation by Anacystis nidulans DNA photolyase. J. Biol. Chem. 267:15406-11
27. Kao Y-T, Tan C, Song S-H, Oztrk N, Li J, et al. 2008. Ultrafast dynamics and anionic active states of the flavin cofactor in cryptochrome and photolyase. J. Am. Chem. Soc. 130:7695-701
28. Cederbaum LS, Zobeley J, Tarantelli F. 1997. Giant intermolecular decay and fragmentation of clusters. Phys. Rev. Lett. 79:4778-81
29. Santra R, Cederbaum L. 2002. Non-Hermitian electronic theory and applications to clusters. Phys. Rep. 368:1-117
30. Förster T. 1948. Zwischenmolekulare Energiewanderung und Fluoreszenz. Ann. Phys. 437:55-75
31. Li J, Liu Z, Tan C, Guo X, Wang L, et al. 2010. Dynamics andmechanism of repair of ultraviolet-induced (6-4) photoproduct by photolyase. Nature 466:887-90
32. 2-TT) kinetics in Anacystis nidulans photolyase. Biochemistry 31:11244-48
33. Carell T, Burgdorf LT, Kundu LM, Cichon M. 2001. The mechanism of action of DNA photolyases. Curr. Opin. Chem. Biol. 5:491-98
34. Maul MJ, BarendsTRM, Glas AF, Cryle MJ, Domratcheva T, et al. 2008. Crystal structure andmechanism of a DNA (6-4) photolyase. Angew. Chem. Int. Ed. Engl. 47:10076-80
35. Liu Z, Tan C, Guo X, Kao Y-T, Li J, et al. 2011. Dynamics and mechanism of cyclobutane pyrimidine dimer repair by DNA photolyase. Proc. Natl. Acad. Sci. USA 108:14831-36
36. Liu Z, Guo X, Tan C, Li J, Kao Y-T, et al. 2012. Electron tunneling pathways and role of adenine in repair of cyclobutane pyrimidine dimer by DNA photolyase. J. Am. Chem. Soc. 134:8104-14
37. Chang C-W, Guo L, Kao Y-T, Li J, Tan C, et al. 2010. Ultrafast solvation dynamics at binding and active sites of photolyases. Proc. Natl. Acad. Sci. USA 107:2914-19
38. Kim ST, Heelis PF, Okamura T, Hirata Y, Mataga N, Sancar A. 1991. Determination of rates and yields of interchromophore (folate→flavin) energy transfer and intermolecular (flavin?DNA) electron transfer in Escherichia coli photolyase by time-resolved fluorescence and absorption spectroscopy. Biochemistry 30:11262-70
39. Yamamoto J, Martin R, Iwai S, Plaza P, Brettel K. 2013. Repair of the (6-4) photoproduct by DNA photolyase requires two photons. Angew. Chem. Int. Ed. Engl. 52:7432-36
40. Harbach PHP, Borowka J, Bohnwagner M-V, Dreuw A. 2010. DNA (6-4) photolesion repair occurs in the electronic ground state of the TT dinucleotide dimer radical anion. J. Phys. Chem. Lett. 1:2556-60
41. Harbach PHP, Schneider M, Faraji S, Dreuw A. 2013. Intermolecular Coulombic decay in biology: The initial electron detachment from FADH- in DNA photolyases. J. Phys. Chem. Lett. 4:943-49
42. Sadeghian K, Bocola M, Merz T, SchützM. 2010. Theoretical study on the repair mechanism of the (6-4) photolesion by the (6-4) photolyase. J. Am. Chem. Soc. 132:16285-95
43. Masson F, Laino T, Rothlisberger U, Hutter J. 2009. A QM/MM investigation of thymine dimer radical anion splitting catalyzed by DNA photolyase. J. Chem. Phys. Phys. Chem. 10:400-10
44. Zheng X, Garcia J, Stuchebrukhov AA. 2008. Theoretical study of excitation energy transfer in DNA photolyase. J. Phys. Chem. B 112:8724-29
45. Antony J, Medvedev DM, Stuchebrukhov AA. 2000. Theoretical study of electron transfer between the photolyase catalytic cofactor FADH- and DNA thymine dimer. J. Am. Chem. Soc. 122:1057-65
46. Durbeej B, Eriksson LA. 2000. Thermodynamics of the photoenzymic repair mechanism studied by density functional theory. J. Am. Chem. Soc. 122:10126-32
47. Borg OA, Eriksson LA, Durbeej B. 2007. Electron-Transfer induced repair of 6-4 photoproducts in DNA: A computational study. J. Phys. Chem. A 111:2351-61
48. Harrison CB, O'Neil LL, Wiest O. 2005. Computational studies of DNA photolyase. J. Phys. Chem. A 109:7001-12
49. Č ondić-Jurkić K, Smith A-S, ZipseH, SmithDM.2012. The protonation states of the active-site histidines in (6-4) photolyase. J. Chem. Theory Comput. 8:1078-91
50. Hassanali AA, ZhongD, Singer SJ. 2011. An AIMD study of theCPD repair mechanism in water: Reaction free energy surface and mechanistic implications. J. Phys. Chem. B 115:3848-59
51. Domratcheva T. 2011. Neutral histidine and photoinduced electron transfer in DNA photolyases. J. Am. Chem. Soc. 133:18172-82
52. Yamamoto J, Hitomi K, Hayashi R, Getzoff ED, Iwai S. 2009. Role of the carbonyl group of the (6-4) photoproduct in the (6-4) photolyase reaction. Biochemistry 48:9306-12
53. Faraji S, Dreuw A. 2012. Proton-Transfer-steered mechanisms of photolesion repair by (6-4) photolyases. J. Phys. Chem. Lett. 3:227-30
54. Masson F, Laino T, Tavernelli I, Rothlisberger U, Hutter J. 2008. Computational study of thymine dimer radical anion splitting in the self-repair process of duplex DNA. J. Am. Chem. Soc. 130:3443-50
55. Park H, Kim S, Sancar A, Deisenhofer J. 1995. Crystal structure of DNA photolyase from Escherichia coli. Science 268:1866-72
56. Mees A, Klar T, Gnau P, Hennecke U, Eker APM, et al. 2004. Crystal structure of a photolyase bound to a CPD-like DNA lesion after in situ repair. Science 306:1789-93
57. Friederl MG, Cichon MK, Carell T. 2005. Model compounds for (6-4) photolyases: A comparative flavin induced cleavage study of oxetanes and thietanes. Org. Biomol. Chem. 3:1937-41
58. Hitomi K, Nakamura H, Kim S, Mizukoshi T, Ishikawa T, et al. 2001. Role of two histidines in the (6-4) photolyase reaction. J. Biol. Chem. 276:10103-9
59. Schleicher E, Hitomi K, Kay CWM, Getzoff ED, Takeshi T, Weber S. 2007. Electron nuclear double resonance differentiates complementary roles for active site histidines in (6-4) photolyase. J. Biol. Chem. 16:4738-47
60. Liu Z, Tan C, Guo X, Kao Y-T, Li J, et al. 2011. Dynamics and mechanism of cyclobutane pyrimidine dimer repair by DNA photolyase. Proc. Natl. Acad. Sci. USA 108:14831-36
61. Kao Y-T, Song Q-H, Saxena C, Wang L, Zhong D. 2012. Dynamics and mechanism of DNA repair in a biomimetic system: Flavin-Thymine dimer adduct. J. Am. Chem. Soc. 134:1501-3
62. Harris CB, Ippen EP, Mourou GA, Zewail AH. 1990. Ultrafast Phenomena VII. Berlin: Springer-Verlag
63. Zewail AH. 1994. Femtochemistry: Ultrafast Dynamics of the Chemical Bond. Singapore: World Sci
64. Domratcheva T, Schlichting I. 2009. Electronic structure of (6-4) DNA photoproduct repair involving a non-oxetane pathway. J. Am. Chem. Soc. 131:17793-99
65. Dreuw A. 2006. Quantum chemical methods for the investigation of photoinitiated processes in biological systems: Theory and applications. ChemPhysChem 7:2259-74
66. Grimme S. 2004. Calculation of the electronic spectra of large molecules. In Reviews in Computational Chemistry, ed. KB Lipkowitz, R Larter, TR Cundari, pp. 153-18. New York: Wiley
67. Köppel H, Domcke W, Cederbaum LS. 1984. Multimode molecular dynamics beyond the Born-Oppenheimer approximation. Adv. Chem. Phys. 57:59-246
68. Domcke W, Yarkony DR, Köppel H, eds. 2004. Conical Intersections: Electronic Structure, Dynamics and Spectroscopy. Singapore: Word Sci
69. Senn HM, Thiel W. 2009. QM/MM methods for biomolecular systems. Angew. Chem. Int. Ed. Engl. 48:1198-229
70. Warshel A, Levitt M. 1976. Theoretical studies of enzymic reactions: Dielectric, electrostatic and steric stabilization of the carbonium ion in the reaction of lysozyme. J. Mol. Biol. 103:227-49
71. Day PN, Jensen JH, Gordon MS, Webb SP, Stevens WJ, et al. 1996. An effective fragment method for modeling solvent effects in quantum mechanical calculations. J. Chem. Phys. 105:1968-86
72. Gordon MS, Fedorov DG, Pruitt SR, Slipchenko LV. 2012. Fragmentation methods: A route to accurate calculations on large systems. Chem. Rev. 112:632-72
73. Klamt A, Schuurmann G. 1993. COSMO: A new approach to dielectric screening in solvents with explicit expressions for the screening energy and its gradient. J. Chem. Soc. Perkin Trans. 2 1993:799-805
74. TapiaO, GoscinskiO. 1975. Self-consistent reaction field theory of solvent effects. Mol. Phys. 29:1653-61
75. Liao R, ThielW. 2012. Comparison of QM-only and QM/MM models for the mechanism of tungstendependent acetylene hydratase. J. Chem. Theory Comput. 8:3793-803
76. Woiczikowski PB, Steinbrecher T, Kubar T, Elstner M. 2011. Nonadiabatic QM/MM simulations of fast charge transfer in Escherichia coli DNA photolyase. J. Phys. Chem. B 115:9846-63
77. Hassanali AA, Zhong D, Singer SJ. 2011. An AIMD study of CPD repair mechanism in water: Role of solvent in ring splitting. J. Phys. Chem. B 115:3860-71
78. Asgatay S, Petermann C, Harakat D, Guillaume D, Taylor JS, Pascale C. 2008. Evidence that the (6-4) photolyase mechanism can proceed through an oxetane intermediate. J. Am. Chem. Soc. 130:12618-19
79. Faraji S, Groenhof G, Dreuw A. 2013. A combined QM/MM investigation on the light-driven electroninduced repair of the (6-4) thymine dimer catalyzed by DNA photolyase. J. Phys. Chem. B 117:10071-79
80. Kozuch S, Shaik S. 2011. How to conceptualize catalytic cycles? The energetic span model. Acc. Chem. Res. 44:101-10
81. Dreuw A, Faraji S. 2013. A quantum chemical perspective on (6-4) photolesion repair by photolyases. Phys. Chem. Chem. Phys. 15:19957-69