Reaction mechanisms of DNA photolyase

Current Opinion in Structural Biology

Volumn 20, Issue 6, 2010, Pages 693-701

  Brettel, Klaus ^a,b   Byrdin, Martin ^a,b,c  

^a SERVICE DE CHIMIE BIOORGANIQUE ET DE MARQUAGE   (France)

^b CNRS   (France)

^c CEA GRENOBLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CRYPTOCHROME; DEOXYRIBODIPYRIMIDINE PHOTOLYASE; PYRIMIDINE DIMER; TRYPTOPHAN;

ABSORPTION SPECTROSCOPY; BLUE LIGHT; CATALYSIS; DNA DAMAGE; DNA REPAIR; ELECTRON TRANSPORT; ENZYME KINETICS; ENZYME MECHANISM; HUMAN; LIGHT; NONHUMAN; PHOTOACTIVATION; PHOTOREACTIVITY; PHOTORECEPTOR; PRIORITY JOURNAL; REVIEW; ULTRAVIOLET IRRADIATION;

EID: 78649642414     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2010.07.003     Document Type: Review

References (65)

1. Sancar A. Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chemical Reviews 2003, 103:2203-2237.
2. Thorne R.E., Chinnapen D.J.F., Sekhon G.S., Sen D. A deoxyribozyme, Sero1C, uses light and serotonin to repair diverse pyrimidine dimers in DNA. Journal of Molecular Biology 2009, 388:21-29.
3. 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 and Development 2003, 17:2539-2551.
4. Müller M., Carell T. Structural biology of DNA photolyases and cryptochromes. Current Opinion in Structural Biology 2009, 19:277-285.
5. Glas A.F., Kaya E., Schneider S., Heil K., Fazio D., Maul M.J., Carell T. DNA (6-4) photolyases reduce dewar isomers for isomerization into (6-4) lesions. Journal of the American Chemical Society 2010, 132:3254-3255.
6. Yamamoto J., Hitomi K., Hayashi R., Getzoff E.D., Iwai S. Role of the carbonyl group of the (6-4) photolyase reaction. Biochemistry 2009, 48:9306-9312.
7. 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-A European Journal 2009, 15:10387-10396.
8. Domratcheva T., Schlichting I. Electronic structure of (6-4) DNA photoproduct repair involving a non-oxetane pathway. Journal of the American Chemical Society 2009, 131:17793-17799.
9. Asgatay S., Petermann C., Harakat D., Guillaume D., Taylor J.-S., Clivio P. Evidence that the (6-4) photolyase mechanism can proceed through an oxetane intermediate. Journal of the American Chemical Society 2008, 130:12618-12619.
10. Sancar A. Structure and function of photolyase and in vivo enzymology: 50th anniversary. Journal of Biological Chemistry 2008, 283:32153-32157.
11. Beukers R., Eker A.P.M., Lohman P.H.M. 50 years thymine dimer. DNA Repair 2008, 7:530.
12. Schleicher E., Wenzel R., Ahmad M., Batschauer A., Essen L.-O., Hitomi K., Getzoff E., Bittl R., Weber S., Okafuji A. The electronic state of flavoproteins: investigations with proton electron-nuclear double resonance. Applied Magnetic Resonance 2010, 37:339-352.
13. Boussicault F., Robert M. Electron transfer in DNA and in DNA-related biological processes. Electrochemical insights. Chemical Reviews 2008, 108:2622-2645.
14. Mees A., Klar T., Gnau P., Hennecke U., Eker A.P.M., Carell T., Essen L.O. Crystal structure of a photolyase bound to a CPD-like DNA lesion after in situ repair. Science 2004, 306:1789-1793.
15. Espagne A., Byrdin M., Eker A.P.M., Brettel K. Very fast product release and catalytic turnover of DNA photolyase. ChemBioChem 2009, 10:1777-1780.
16. Thiagarajan V., Villette S., Espagne A., Eker A.P.M., Brettel K., Byrdin M. DNA repair by photolyase: a novel substrate with low background absorption around 265nm for transient absorption studies in the UV. Biochemistry 2010, 49:297-303.
17. Kao Y.T., Saxena C., Wang L., Sancar A., Zhong D. Direct observation of thymine dimer repair in DNA by photolyase. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:16128-16132.
18. MacFarlane A.W., Stanley R.J. Cis-Syn thymidine dimer repair by DNA photolyase in real time. Biochemistry 2003, 42:8558-8568.
19. Chang C.W., Kao Y.T., Li J., Tan C., Li T.P., Saxena C., Liu Z.Y., Wang L.J., Sancar A., Zhong D.P. Ultrafast solvation dynamics at binding and active sites of photolyases. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:2914-2919.
20. - and DNA thymine dimer. Journal of the American Chemical Society 2000, 122:1057-1065.
21. Masson F., Laino T., Rothlisberger U., Hutter J. A QM/MM investigation of thymine dimer radical anion splitting catalyzed by DNA photolyase. ChemPhysChem 2009, 10:400-410.
22. Boussicault F., Krüger O., Robert M., Wille U. Dissociative electron transfer to and from pyrimidine cyclobutane dimers: an electrochemical study. Organic and Biomolecular Chemistry 2004, 2:2742-2750.
23. Xu L., Mu W., Ding Y., Luo Z., Han Q., Bi F., Wang Y., Song Q. Active site of Escherichia coli DNA photolyase: Asn378 is crucial both for stabilizing the neutral flavin radical cofactor and for DNA repair. Biochemistry 2008, 47:8736-8743.
24. Yeh S.R., Falvey D.E. Model studies of DNA photorepair: energetic requirements for the radical anion mechanism determined by fluorescence quenching. Journal of the American Chemical Society 1992, 114:7313-7314.
25. Chatgilialoglu C., Guerra M., Kaloudis P., Houee-Levin C., Marignier J.L., Swaminathan V.N., Carell T. Ring opening of the cyclobutane in a thymine dimer radical anion. Chemistry-A European Journal 2007, 13:8979-8984.
26. Song Q.-H., Tang W.-J., Ji X.-B., Wang H.-B., Guo Q.-X. Do photolyases need to provide considerable activation energy for the splitting of cyclobutane pyrimidine dimer radical anions?. Chemistry-A European Journal 2007, 13:7762-7770.
27. Langenbacher T., Zhao X.D., Bieser G., Heelis P.F., Sancar A., MichelBeyerle M.E. Substrate and temperature dependence of DNA photolyase repair activity examined with ultrafast spectroscopy. Journal of the American Chemical Society 1997, 119:10532-10536.
28. Harrison C.B., O'Neil L.L., Wiest O. Computational studies of DNA photolyase. The Journal of Physical Chemistry A 2005, 109:7001-7012.
29. Masson F., Laino T., Tavernelli I., Rothlisberger U., Hutter J. Computational study of thymine dimer radical anion splitting in the self-repair process of duplex DNA. Journal of the American Chemical Society 2008, 130:3443-3450.
30. Tachikawa H., Kawabata H. Interaction between thymine dimer and flavin-adenine dinucleotide: a DFT and direct ab initio molecular dynamics study. The Journal of Physical Chemistry B 2008, 112:7315-7319.
31. Prytkova T.R., Beratan D.N., Skourtis S.S. Photoselected electron transfer pathways in DNA photolyase. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:802-807.
32. Acocella A., Jones G.A., Zerbetto F. What is adenine doing in photolyase?. The Journal of Physical Chemistry B 2010, 114:4101-4106.
33. Zheng X., Garcia J., Stuchebrukhov A.A. Theoretical study of excitation energy transfer in DNA photolyase. The Journal of Physical Chemistry B 2008, 112:8724-8729.
34. Murphy A.K., Tammaro M., Cortazar F., Gindt Y.M., Schelvis J.P.M. Effect of the cyclobutane cytidine dimer on the properties of Escherichia coli DNA photolyase. The Journal of Physical Chemistry B 2008, 112:15217-15226.
35. -) in DNA photolyase. The Journal of Physical Chemistry Letters 2010, 1:743-747.
36. Byrdin M., Sartor V., Eker A.P.M., Vos M.H., Aubert C., Brettel K., Mathis P. Intraprotein electron transfer and proton dynamics during photoactivation of DNA photolyase from E. coli: review and new insights from an "inverse" deuterium isotope effect. Biochimica et Biophysica Acta 2004, 1655:64-70.
37. Kavakli I.H., Sancar A. Analysis of the role of intraprotein electron transfer in photoreactivation by DNA photolyase in vivo. Biochemistry 2004, 43:15103-15110.
38. Li Y.F., Heelis P.F., Sancar A. Active site of DNA photolyase: tryptophan-306 is the intrinsic hydrogen atom donor essential for flavin radical photoreduction and DNA repair in vitro. Biochemistry 1991, 30:6322-6329.
39. Cheung M.S., Daizadeh I., Stuchebrukhov A.A., Heelis P.F. Pathways of electron transfer in Escherichia coli DNA photolyase: Trp306 to FADH. Biophysical Journal 1999, 76:1241-1249.
40. Aubert C., Vos M.H., Mathis P., Eker A.P.M., Brettel K. Intraprotein radical transfer during photoactivation of DNA photolyase. Nature 2000, 405:586-590.
41. Byrdin M., Eker A.P.M., Vos M.H., Brettel K. Dissection of the triple tryptophan electron transfer chain in Escherichia coli DNA photolyase: Trp382 is the primary donor in photoactivation. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:8676-8681.
42. Byrdin M., Villette S., Eker A.P.M., Brettel K. Observation of an intermediate tryptophanyl radical in W306F mutant DNA photolyase from Escherichia coli supports electron hopping along the triple tryptophan chain. Biochemistry 2007, 46:10072-10077.
43. Lukacs A., Eker A.P.M., Byrdin M., Villette S., Pan J., Brettel K., Vos M.H. Role of the middle residue in the triple tryptophan electron transfer chain of DNA photolyase: ultrafast spectroscopy of a Trp->Phe mutant. The Journal of Physical Chemistry B 2006, 110:15654-15658.
44. Byrdin M., Villette S., Espagne A., Eker A.P.M., Brettel K. Polarized transient absorption to resolve electron transfer between tryptophans in DNA photolyase. The Journal of Physical Chemistry B 2008, 112:6866-6871.
45. Lukacs A., Eker A.P.M., Byrdin M., Brettel K., Vos M.H. Electron hopping through the 15Å Triple tryptophan molecular wire in DNA photolyase occurs within 30ps. Journal of the American Chemical Society 2008, 130:14394-14395.
46. Byrdin M., Lukacs A., Thiagarajan V., Eker A.P.M., Brettel K., Vos M.H. Quantum yield measurements of short-lived photoactivation intermediates in DNA photolyase: toward a detailed understanding of the triple tryptophan electron transfer chain. The Journal of Physical Chemistry A 2010, 114:3207-3214.
47. Aubert C., Mathis P., Eker A.P.M., Brettel K. Intraprotein electron transfer between tyrosine and tryptophan in DNA photolyase from Anacystis nidulans. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:5423-5427.
48. Popovic D.M., Zmiric A., Zaric S.D., Knapp E.W. Energetics of radical transfer in DNA photolyase. Journal of the American Chemical Society 2002, 124:3775-3782.
49. Selby C.P., Sancar A. A cryptochrome/photolyase class of enzymes with single-stranded DNA-specific photolyase activity. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:17696-17700.
50. Pokorny R., Klar T., Hennecke U., Carell T., Batschauer A., Essen L.-O. Recognition and repair of UV lesions in loop structures of duplex DNA by DASH-type cryptochrome. Proceedings of the National Academy of Sciences 2008, 105:21023-21027.
51. Lin C.T., Todo T. The cryptochromes. Genome Biology 2005, 6.
52. Balland V., Byrdin M., Eker A.P.M., Ahmad M., Brettel K. What makes the difference between a cryptochrome and DNA photolyase? A spectroelectrochemical comparison of the flavin redox transitions. Journal of the American Chemical Society 2009, 131:426-427.
53. Damiani M.J., Yalloway G.N., Lu J., McLeod N.R., O'Neill M.A. Kinetic stability of the flavin semiquinone in photolyase and cryptochrome-DASH. Biochemistry 2009, 48:11399-11411.
54. Giovani B., Byrdin M., Ahmad M., Brettel K. Light-induced electron transfer in a cryptochrome blue-light photoreceptor. Nature Structural Biology 2003, 10:489-490.
55. Zeugner A., Byrdin M., Bouly J.P., Bakrim N., Giovani B., Brettel K., Ahmad M. Light-induced electron transfer in Arabidopsis cryptochrome-1 correlates with in vivo function. The Journal of Biological Chemistry 2005, 280:19437-19440.
56. Langenbacher T., Immeln D., Dick B., Kottke T. Microsecond light-induced proton transfer to flavin in the blue light sensor plant cryptochrome. Journal of the American Chemical Society 2009, 131:14274-14280.
57. Berndt A., Kottke T., Breitkreuz H., Dvorsky R., Hennig S., Alexander M., Wolf E. A novel photoreaction mechanism for the circadian blue light photoreceptor drosophila cryptochrome. The Journal of Biological Chemistry 2007, 282:13011-13021.
58. Song S.-H., Ozturk N., Denaro T.R., Arat N.O., Kao Y.-T., Zhu H., Zhong D., Reppert S.M., Sancar A. Formation and function of flavin anion radical in cryptochrome 1 blue-light photoreceptor of monarch butterfly. The Journal of Biological Chemistry 2007, 282:17608-17612.
59. Ozturk N., Song S.-H., Selby C.P., Sancar A. Animal type 1 cryptochromes: analysis of the redox state of the flavin cofactor by site-directed mutagenesis. The Journal of Biological Chemistry 2008, 283:3256-3263.
60. Kao Y.-T., Tan C., Song S.-H., Öztürk N., Li J., Wang L., Sancar A., Zhong D. Ultrafast dynamics and anionic active states of the flavin cofactor in cryptochrome and photolyase. Journal of the American Chemical Society 2008, 130:7695-7701.
61. Brazard J., Usman A., Lacombat F., Ley C., Martin M.M., Plaza P., Mony L., Heijde M., Zabulon G., Bowler C. Spectro-temporal characterization of the photoactivation mechanism of two new oxidized cryptochrome/photolyase photoreceptors. Journal of the American Chemical Society 2010, 132:4935-4945.
62. Kodali G., Siddiqui S.U., Stanley R.J. Charge redistribution in oxidized and semiquinone E. coli DNA photolyase upon photoexcitation: Stark spectroscopy reveals a rationale for the position of Trp382. Journal of the American Chemical Society 2009, 131:4795-4807.
63. Journal of the Royal Society Interface 2010, 7 Suppl. 2.
64. Byrdin M., Thiagarajan V., Villette S., Espagne A., Brettel K. Use of ruthenium dyes for subnanosecond detector fidelity testing in real time transient absorption. Review of Scientific Instruments 2009, 80:043102.
65. Sokolowsky K., Newton M., Lucero C., Wertheim B., Freedman J., Cortazar F., Czochor J., Schelvis J.P.M., Gindt Y.M. Spectroscopic and thermodynamic comparisons of Escherichia coli DNA photolyase and vibrio cholerae cryptochrome 1. The Journal of Physical Chemistry B 2010, 114:7121-7130.