Intermolecular coulombic decay in biology: The initial electron detachment from FADH- in DNA photolyases

Journal of Physical Chemistry Letters

Volumn 4, Issue 6, 2013, Pages 943-949

  Harbach, Philipp H P ^a   Schneider, Matthias ^a   Faraji, Shirin ^a   Dreuw, Andreas ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

DNA repair; electronically unbound excited states; energy transfer; free electron generation; quantum chemistry

Indexed keywords

DNA REPAIR; DNA-REPAIR ENZYMES; ELECTRON DETACHMENTS; FLAVIN ADENINE DINUCLEOTIDE; FREE ELECTRON; LOW ENERGY ELECTRONS; OPERATING MECHANISM; QUANTUM-CHEMICAL METHODS;

DNA; ELECTRONS; ENERGY TRANSFER; QUANTUM CHEMISTRY; TISSUE;

REPAIR;

EID: 84875548825     PISSN: None     EISSN: 19487185     Source Type: Journal    
DOI: 10.1021/jz400104h     Document Type: Article

References (56)

1. Cederbaum, L. S.; Zobeley, J.; Tarantelli, F. Giant Intermolecular Decay and Fragmentation of Clusters Phys. Rev. Lett. 1997, 79, 4778-4781
2. Zobeley, J.; Cederbaum, L. S.; Tarantelli, F. Highly Excited Electronic States of Molecular Clusters and Their Decay J. Chem. Phys. 1998, 108, 9737-9751
3. Boudaiffa, B.; Cloutier, P.; Hunting, D.; M. A. Huels, L. S. Resonant Formation of DNA Strand Breaks by Low-Energy (3 to 20 eV) Electrons Science 2000, 287, 1658-1660
4. Mucke, M.; Braune, M.; Barth, S.; Förstel, M.; Lischke, T.; Ulrich, V.; Arion, T.; Becker, U.; Bradshawand, A.; Hergenhahn, U. A Hitherto Unrecognized Source of Low Energy Electrons in Water Nat. Phys. 2012, 6, 143-146
5. Zobeley, J.; Tarantelli, F.; Cederbaum, L. S. Intermolecular Coulombic Decay of Molecular Clusters: Identification of the Decay Mechanism Using a New Hole-Population Analysis J. Phys. Chem. A 1999, 103, 11145-11160
6. Santra, R.; Cederbaum, L. S. Non-Hermitian Electronic Theory and Applications to Clusters Phys. Rep. 2002, 368, 1-117
7. Averbukh, V.; Demekhin, P.; Kolorenc, P.; Scheit, S.; Stoychev, S.; Kuleff, A.; Chiang, Y.-C.; Gokhberg, K.; Kopelke, S.; Sisourat, N.; Cederbaum, L. Interatomic Electronic Decay Processes in Singly and Multiply Ionized Clusters J. Electron Spectrosc. Relat. Phenom. 2011, 183, 36-47
8. Marburger, S.; Kugeler, O.; Hergenhahn, U.; Möller, T. Experimental Evidence for Interatomic Coulombic Decay in Ne Clusters Phys. Rev. Lett. 2003, 90, 203401-203404
9. Jahnke, T.; Czasch, A.; Schöffler, M.; Schössler, S.; Knapp, A.; Käsz, M.; Titze, J.; Wimmer, C.; Kreidi, K.; Grisenti, R.; Staudte, A.; Jagutzki, O.; Hergenhahn, U.; Schmidt-Böcking, H.; Dörner, R. Experimental Observation of Interatomic Coulombic Decay in Neon Dimers Phys. Rev. Lett. 2004, 93, 163401-163404
10. Stoychev, S. D.; Kuleff, A. I.; Cederbaum, L. S. Intermolecular Coulombic Decay in Small Biochemically Relevant Hydrogen-Bonded Systems J. Am. Chem. Soc. 2011, 133, 6817-6824
11. Hergenhahn, U. Interatomic and Intermolecular Coulombic Decay: The Early Years J. Electron Spectrosc. Relat. Phenom. 2011, 184, 78-90
12. Carrier, W. L.; Snyder, R. D.; Regan, J. D. The Science of Photomedicine; Plenum: New York, 1982.
13. Taylor, J.-S. DNA, Sunlight and Skin Cancer Pure Appl. Chem. 1995, 67, 183-190
14. Matsumura, Y.; Ananthaswamy, H. N. Front. Biosci. 2002, 7, D765-783
15. Reardon, J. T.; Sancar, A. Recognition and Repair of the Cyclobutane Thymine Dimer, a Major Cause of Skin Cancers, by the Human Excision Nuclease Genes Dev. 2003, 17, 2539-2551
16. Sancar, A. Structure and Function of DNA Photolyase and Cryptochrome Blue-Light Photoreceptors Chem. Rev. 2003, 103, 2203-2237
17. Lin, C.; Todo, T. The Cryptochromes Genome Biol. 2005, 6, 220-228
18. Todo, T.; Kim, S. T.; Hitomi, K.; Otoshi, E.; Inui, T.; Morioka, H.; Kobayashi, H.; Ohtsuka, E.; Toh, H.; Ikenaga, M. Flavin Adenine Dinucleotide as a Chromophore of the Xenopus (6-4) Photolyase Nucleic Adic Res. 1997, 25, 764-768
19. Yi, Y.; Yi, C.; Qian, L.; Min, L.; Long, C.; Linhan, B.; Zhirong, Y.; Dairong, Q. Cloning and Sequence Analysis of the Gene Encoding (6-4) Photolyase from Dunaliella Salina Biotechnol. Lett. 2006, 28, 309-314
20. Glas, A. F.; Schneider, S.; Maul, M. J.; Hennecke, U.; Carell, T. 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 Chemistry 2009, 15, 10387-10396
21. Klar, T.; Kaiser, G.; Hennecke, U.; Carell, T.; Batschauer, A.; Essen, L.-O. Natural and Non-Natural Antenna Chromophores in the DNA Photolyase from Thermus Thermophilus Chem. Biol. Chem. 2006, 7, 1798-1806
22. Malhotra, K.; Kim, S. T.; Walsh, C.; Sancar, A. Roles of FAD and 8-Hydroxy-5-deazaflavin Chromophores in Photoreactivation byAnacystis Nidulans DNA Photolyase J. Biol. Chem. 1992, 267, 15406-15411
23. Heelis, P. F.; Hartman, R. F.; Rose, S. D. Energy and Electron Transfer Processes in Flavoprotein-Mediated DNA Repair J. Photochem. Photobiol., A 1996, 95, 89-98
24. Cheung, M. S.; Daizadeh, I.; Stuchebrukhov, A. A.; Heelis, P. F. Pathways of Electron Transfer in Escherichia coli DNA Photolyase: Trp306 to FADH Biophys. J. 1999, 76, 1241-1249
25. -) in DNA Photolyase J. Phys. Chem. Lett. 2010, 1, 743-747
26. Woiczikowski, P. B.; Steinbrecher, T.; Kumar, T.; Elstner, M. Nonadiabatic QM/MM Simulations of Fast Charge Transfer in Escherichia coli DNA Photolyase J. Phys. Chem. B 2011, 115, 9846-9863
27. Liu, Z.; Guo, X.; Tan, C.; Li, J.; Kao, Y.-T.; Wang, L.; Sancar, A.; Zhong, D. Electron Tunneling Pathways and Role of Adenine in Repair of Cyclobutane Pyrimidine Dimer by DNA Photolyase J. Am. Chem. Soc. 2012, 134, 8104-8114
28. Sancar, A. Structure and Function of Photolyase and In Vivo Enzymology: 50th Anniversary J. Biol. Chem. 2008, 283, 32153-32157
29. Carell, T.; Burgdorf, L. T.; Kundu, L. M.; Cichon, M. The Mechanism of Action of Photolyase Curr. Opin. Chem. Biol. 2001, 5, 491-498
30. Essen, L.-O.; Klar, T. Light Driven DNA Repair by Photolyases Cell. Mol. Life Sci. 2006, 63, 1266-1277
31. Yamamoto, J.; Hitomi, K.; Hayashi, R.; Getzoff, E. D.; Iwai, S. Role of the Carbonyl Group of the (6-4) Photoproduct in the (6-4) Photolyase Reaction Biochemistry 2009, 48, 9306-9312
32. Borg, O. A.; Eriksson, L. A.; Durbeej, B. Electron-Transfer Induced Repair of 6-4 Photoproducts in DNA: A Computational Study J. Phys. Chem. A 2007, 111, 2351-2361
33. Domratcheva, T.; Schlichting, I. Electronic Structure of (6-4) DNA Photoproduct Repair Involving a Non-Oxetane Pathway J. Am. Chem. Soc. 2009, 131, 17793-17799
34. Sadeghian, K.; Bocola, M.; Merz, T.; Schütz, M. Theoretical Study on the Repair Mechanism of the (6-4) Photolesion by the (6-4) Photolyase J. Am. Chem. Soc. 2012, 132, 16285-16295
35. Harbach, P. H. P.; Borowka, J.; Bohnwagner, M.-V.; Dreuw, A. Photolesion Repair Occurs in the Electronic Ground State of the TT Dinucleotide Dimer Radical Anion J. Phys. Chem. Lett. 2010, 1, 2556-2560
36. Li, J.; Liu, Z.; Guo, X.; Wang, L.; Sancar, A.; Zhong, D. Dynamics and Mechanism of Repair of Ultraviolet-Induced (6-4) Photoproduct by Photolyase Nature 2010, 466, 887-890
37. Faraji, S.; Dreuw, A. Proton-Transfer-Steered Mechanism of Photolesion Repair by (6-4)-Photolyases J. Phys. Chem. Lett. 2012, 3, 227-230
38. Jung, Y.; Lochan, R. C.; Dutoi, A. D.; Head-Gordon, M. Scaled Opposite-Spin Second Order Møller-Plesset Correlation Energy: an Economical Electronic Structure Method J. Chem. Phys. 2004, 121, 9793-9803
39. Tapia, O.; Goscinski, O. Self-Consistent Reaction Field Theory of Solvent Effects Mol. Phys. 1975, 29, 1653-1661
40. Schutz, C. N.; Warshel, A. What Are the Dielectric Constants of Proteins and How to Validate Electrostatic Models? Proteins 2001, 44, 400-417
41. Dreuw, A.; Head-Gordon, M. Single-Reference Ab Initio Methods for the Calculation of Excited States of Large Molecules Chem. Rev. 2005, 105, 4009-4037
42. Harbach, P. H. P.; Dreuw, A. In Molecular Modeling; Wiley-VCH: Weinheim, Germany, 2011; p 29.
43. Rokita, S. E.; Walsh, C. T. Flavin and 5-Deazaflavin Photosensitized Cleavage of Thymine Dimer: A Model of in Vivo Light-Requiring DNA Repair J. Am. Chem. Soc. 1984, 106, 4589-4595
44. Todo, T.; Takemori, H.; Ryo, H.; Ihara, M.; Matsunaga, T.; Nikaido, O.; Sato, K.; Nomura, T. A New Photoreactivating Enzyme That Specifically Repairs Ultraviolet Light-Induced (6-4) Photoproducts Nature 1993, 361, 371-374
45. Zheng, X.; Garcia, J.; Stuchebrukhov, A. A. Theoretical Study of Excitation Energy Transfer in DNA Photolyase J. Phys. Chem. B 2008, 112, 8724-8729
46. Nuttall, J.; Cohen, H. L. Method of Complex Coordinates for Three-Body Calculations above the Breakup Threshold Phys. Rev. 1969, 188, 1542-1544
47. Balslev, E.; Combes, J. M. Spectral Properties of Many-Body Schrödinger Operators with Dilatation-Analytic Interactions Commun. Math. Phys. 1971, 22, 280-294
48. Simon, B. Quadratic Form Techniques and the Balslev-Combes Theorem Commun. Math. Phys. 1972, 27, 1-9
49. Riss, U. V.; Meyer, H.-D. Calculation of Resonance Energies and Widths Using the Complex Absorbing Potential Method J. Phys. B 1993, 26, 4503-4513
50. Riss, U. V.; Meyer, H.-D. Reflection-Free Complex Absorbing Potentials J. Phys. B 1995, 28, 1475-1488
51. Santra, R.; Cederbaum, L. S.; Meyer, H.-D. Electronic Decay of Molecular Clusters: Non-Stationary States Computed by Standard Quantum Chemistry Methods Chem. Phys. Lett. 1999, 303, 413-419
52. - J. Chem. Phys. 1967, 47, 2165-2178
53. Volobuev, Y. L.; Truhlar, D. G. An MIMD Strategy for Quantum Mechanical Reactive Scattering Comput. Phys. Commun. 2000, 128, 516-526
54. Krueger, B. P.; Scholes, G. D.; Fleming, G. R. Calculation of Couplings and Energy Transfer Pathways Between the Pigments of LH2 by the Ab Initio Transition Density Cube Method J. Phys. Chem. B 1998, 102, 5378-5386
55. 2 → T<>T) Kinetics in Anacystic nidulans Photolyase Biochemistry 1992, 31, 11244-11248
56. Kim, S. T.; Heelis, P. F.; Okamura, T.; Hirata, Y.; Mataga, N.; Sancar, A. 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 1991, 30, 11262-11270