Light-driven DNA repair by photolyases

Cellular and Molecular Life Sciences

Volumn 63, Issue 11, 2006, Pages 1266-1277

  Essen, L O ^a   Klar, T ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Base flipping; Blue light reactions; Cyclobutane pyrimidine dimer (CPD); DNA repair; DNA photolyase; Electron transfer; Skin cancer; Ultraviolet radiation

Indexed keywords

CYCLOBUTANE; DEOXYRIBODIPYRIMIDINE PHOTOLYASE; DIMER; DNA BASE; DOUBLE STRANDED DNA; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PYRIMIDINE; PYRIMIDINE PYRIMIDONE PHOTOPRODUCT; PYRIMIDINONE DERIVATIVE; UNCLASSIFIED DRUG;

BLUE LIGHT; CATALYSIS; CATALYST; DNA DAMAGE; DNA REPAIR; ELECTRON TRANSPORT; ENZYME ACTIVITY; HUMAN; LIGHT EXPOSURE; MOLECULAR RECOGNITION; NONHUMAN; PHOTOREACTIVITY; PROTEIN FUNCTION; QUANTUM CHEMISTRY; RADIOSENSITIVITY; REVIEW; SKIN CANCER; SUNLIGHT; SUNLIGHT PROTECTION; TIME; ULTRAVIOLET B RADIATION; ULTRAVIOLET RADIATION;

ANIMALS; DEOXYRIBODIPYRIMIDINE PHOTO-LYASE; DNA; DNA REPAIR; FORECASTING; HUMANS; LIGHT; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PYRIMIDINE DIMERS; SKIN NEOPLASMS; ULTRAVIOLET RAYS;

EUTHERIA;

EID: 33745292138     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-005-5447-y     Document Type: Review

References (76)

1. Vink A. A. and Roza L. (2001) Biological consequences of cyclobutane pyrimidine dimers. J. Photochem. Photobiol. B 65: 101-104
2. Slaper H., Velders G. J., Daniel J. S., Gruijl F. R. de and Leun J. C. van der (1996) Estimates of ozone depletion and skin cancer incidence to examine the Vienna Convention achievements. Nature 384: 256-258
3. Lima-Bessa K. M. and Menck C. F. M. (2005) Skin cancer: lights on genome lesions. Curr. Biol. 15: R58-R61
4. Douki T. and Cadet J. (2001) Individual determination of the yield of the main UV-induced dimeric pyrimidine photoproducts in DNA suggests a high mutagenicity of CC photolesions. Biochemistry 40: 2495-2501
5. Dulbecco R. (1949) Reactivation of ultraviolet-inactivated bacteriophage by visible light. Nature 163: 949-950
6. Kelner A. (1949) Effect Divisible light on the recovery of Streptomyces griseus conidia from ultraviolet-injury. Proc. Natl. Acad. Sci. USA 35: 73-79
7. Minato S. and Werbin H. (1972) Separation of an activator of purified DNA photolyase from baker's yeast. Physiol. Chem. Phys. 4: 467-476
8. Rupert C. S. (1960) Photoreactivation of transforming DNA by an enzyme from bakers' yeast. J. Gen. Physiol. 43: 573-595
9. Heyes D. J., Ruban A. V., Wilks H. M. and Hunter C. N. (2002) Enzymology below 200 K: the kinetics and thermodynamics of the photochemistry catalyzed by protochlorophyllide oxidoreductase. Proc. Natl. Acad. Sci. USA 99: 11145-11150
10. Weber S. (2004) Light-driven enzymatic catalysis of DNA repair: a review of recent biophysical studies on photolyases. Biochem. Biophys. Acta 1707: 1-23
11. Sancar A. (2003) Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chem. Rev. 103: 2203-2237
12. Cockell C. S. and Horneck G. (2001) The history of the UV radiation climate of the Earth - theoretical and space-based observations. Photochem. Photobiol. 73: 447-451
13. Kanai S., Kikuno R., Toh H., Ryo H. and Todo T. (1997) Molecular evolution of the photolyase-blue-light photoreceptor family. J. Mol. Evol. 45: 535-548
14. Kundu L. M., Linne U, Marahiel M. and Carell T. (2004) RNA is more UV resistant than DNA: the formation of UV-induced DNA lesions is strongly sequence and conformation dependent. Chemistry 10: 5697-5705
15. Chinnapen D. J. F. and Sen D. (2004) A deoxyribozyme that harnesses light to repair thymine dimers in DNA. Proc. Natl. Acad. Sci. USA 101: 65-69
16. McCready S. and Marcello E. (2003) Repair of UV damage in Halobacterium salinarum. Biochem. Soc. Trans. 31: 694-698
17. Oconnor K. A., McBride M. J., West M., Yu H., Trinh L., Yuan K. et al. (1996) Photolyase of Myxococcus xanthus, a gram-negative eubacterium, is more similar to photolyases found in Archaea and higher eukaryotes than to photolyases of other Eubacteria. J. Biol. Chem. 271: 6252-6259
18. Bennett C. J., Webb M., Willer D. O. and Evans D. H. (2003) Genetic and phylogenetic characterization of the type II cyclobutane pyrimidine dimer photolyases encoded by Leporipoxviruses. Virology 315: 10-19
19. Srinivasan V., Schnitzlein W. M. and Tripathy D. N. (2001) Fowlpox virus encodes a novel DNA repair enzyme, CPD-photolyase, that restores infectivity of UV light-damaged virus. J. Virol. 75: 1681-1688
20. Slamovits C. H. and Keeling P. J. (2004) Class II photolyase in a microsporidian intracellular parasite. J. Mol. Biol. 341: 713-721
21. Schröder H. C., Krasko A., Gundacker D., Leys S. P., Müller I. M. and Müller W. E. G. (2003) Molecular and functional analysis of the (6-4) photolyase from the hexactinellid Aphrocallistes vastus. Biochem. Biophys. Acta 1651: 41-49
22. Daiyasu H., Ishikawa T., Kuma K., Iwai S., Todo T. and Toh H. (2004) Identification of cryptochrome DASH from vertebrates. Genes Cells 9: 479-495
23. Brudler R., Hitomi K, Daiyasu H., Toh H., Kucho K.-I., Ishiura M. et al. (2003) Identification of a new cryptochrome class: structure, function, and evolution. Mol. Cell 11: 59-67
24. Ozgur S. and Sancar A. (2003) Purification and properties of human blue-light photoreceptor cryptochrome 2. Biochemistry 42: 2926-2932
25. Park H. W., Kim S. T., Sancar A. and Deisenhofer J. (1995) Crystal structure of DNA photolyase from Escherichia coli. Science 268: 1866-1872
26. Tamada T., Kitadokoro K., Higuchi Y., Inaka K., Yasui A., Deruiter P. E. et al. (1997) Crystal structure of DNA photolyase from Anacystis nidulans. Nat. Struct. Biol. 4: 887-891
27. Komori H., Masui R., Kuramitsu S., Yokoyama S., Shibata T., Inoue Y. et al. (2001) Crystal structure of thermostable DNA photolyase: pyrimidine-dimer recognition mechanism. Proc. Natl. Acad. Sci. USA 98: 13560-13565
28. Brautigam C. A., Smith B. S., Ma Z., Palnitkar M., Tomchick D. R., Machius M. et al. (2004) Structure of the photolyase-like domain of cryptochrome 1 from Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 101: 12142-12147
29. Heelis P. F. and Sancar A. (1986) Photochemical properties of Escherichia coli DNA photolyase: a flash photolysis study. Biochemistry 25: 8163-8166
30. Strassner J., Furholz A., Macheroux P., Amrhein N. and Schaller A. (1999) A homolog of old yellow enzyme in tomato - spectral properties and substrate specificity of the recombinant protein. J. Biol. Chem. 274: 35067-35073
31. Aubert C., Vos M. H., Matthis P., Eker A. P. M. and Brettel K. (2000) Intraprotein radical transfer during photoactivation of DNA photolyase. Nature 405: 586-590
32. Aubert C., Mathis P., Eker A. P. M. and Brettel K. (1999) Intraprotein electron transfer between tyrosine and tryptophan in DNA photolyase from Anacystis nidulans. Proc. Natl. Acad. Sci. USA 96: 5423-5427
33. Weber S., Kay C. W., Mogling H., Mobius K., Hitomi K. and Todo T. (2002) Photoactivation of the flavin cofactor in Xenopus laevis (6-4) photolyase: observation of a transient tyrosyl radical by time-resolved electron paramagnetic resonance. Proc. Natl. Acad. Sci. USA 99: 1319-1322
34. Giovani B., Byrdin M., Ahmad M. and Brettel K. (2003) Light-induced electron transfer in a cryptochrome blue-light photoreceptor. Nat. Struct. Biol. 10: 489-491
35. Saxena C., Sancar A. and Zhong D. P. (2004) Femtosecond dynamics of DNA photolyase: energy transfer of antenna initiation and electron transfer of cofactor reduction. J. Phys. Chem. B 108: 18026-18033
36. Zeugner A., Byrdin M., Bouly J.-P., Bakrim N., Giovani B., Brettel K. et al. (2005) Light-induced electron transfer in Arabidopsis cryptochrome-1 correlates in vivo function. J. Biol. Chem. 280: 19437-19440
37. Kort R., Komori H., Adachi S., Miki K. and Eker A. P. M. (2004) DNA apophotolyase from Anacystis nidulans: 1.8 Å structure, 8-HDF reconstitution and X-ray-induced FAD reduction. Acta Crystallogr. D 60: 1205-1213
38. Mees A., Klar T., Hennecke U., Eker A. P. M., Carell T. and Essen L.-O. (2004) Crystal structure of a photolyase bound to a CPD-like DNA lesion after in situ repair. Science 306: 1789-1793
39. Kleiner O., Butenandt L., Carell T. and Batschauer A. (1999) Class II DNA photolyase from Arabidopsis thaliana contains FAD as a cofactor. Eur. J. Biochem. 264: 161-167
40. Hada M., Iida Y. and Takeuchi Y. (2000) Action spectra of DNA photolyases for photorepair of cyclobutane pyrimidine dimers in sorghum and cucumber. Plant Cell Physiol. 41: 644-648
41. Ikenaga M., Kondo S. and Fujii T. (1974) Action spectrum for enzymatic photoreactivation in maize. Photochem. Photobiol. 19: 109-113
42. Malhotra K., Kim S. T. and Sancar A. (1994) Characterization of a medium wavelength type DNA photolyase: purification and properties of photolyase from Bacillus firmus. Biochemistry 33: 8712-8718
43. Henry A. A., Jimenez R., Hanway D. and Romesberg F. E. (2004) Preliminary characterization of light harvesting in E. coli DNA photolyase. ChemBioChem 5: 1088-1094
44. Kim S. T., Heelis P. F. and Sancar A. (1992) Energy transfer (deazaflavin → FADH2) and electron transfer (FADH2 → T <> T) kinetics in Anacystis nidulans photolyase. Biochemistry 31: 11244-11248
45. Thoma F. (2005) Repair of UV lesions in nucleosomes - intrinsic properties and remodeling. DNA Repair 4: 855-869
46. Ueda T., Kato A., Ogawa Y., Torizawa T., Kuramitsu S., Iwai S. et al. (2004) NMR study of repair mechanism of DNA photolyase by FAD-induced paramagnetic relaxation enhancement. J. Biol. Chem. 279: 52574-52579
47. Torizawa T., Ueda T., Kuramitsu S., Hitomi K., Todo T., Iwai S. et al. (2004) Investigation of the cyclobutane pyrimidine dimer (CPD) photolyase DNA recognition mechanism by NMR analyses. J. Biol. Chem. 279: 32950-32956
48. Noort J. van, Orsini E, Eker A., Wyman C., Grooth B. de and Greve J. (1999) DNA bending by photolyase in specific and non-specific complexes studied by atomic force microscopy. Nucleic Acids Res. 27: 3875-3880
49. Husain I., Griffith J. and Sancar A. (1988) Thymine dimers bind DNA. Proc. Natl. Acad. Sci. USA 85: 2558-2562
50. Park H., Zhang K., Ren Y., Nadji S., Sinha N., Taylor J.-S. et al. (2002) Crystal structure of a DNA decamer containing a cis-syn thymine dimer. Proc. Natl. Acad. Sci. USA 99: 15965-15970
51. Harrison C. B., O'Neil L. L. and Wiest O. (2005) Computational studies of DNA photolyase. J. Phys. Chem. A 109: 7001-7012
52. Wiest O. (1999) Structure and [2+2] cycloreversion of the cyclobutane radical cation. J. Phys. Chem. 103: 7907-7911
53. Hahn J., Michel-Beyerle M. E. and Rösch N. (1999) Binding of pyrimidine model dimers to the photolyase enzyme: a molecular dynamics study. J. Phys. Chem. B 103: 2001-2007
54. Gindt Y. M., Schelvis J. P. M., Thoren K. L. and Huang T. H. (2005) Substrate binding modulates the reduction potential of DNA photolyase. J. Am. Chem. Soc. 127: 10472-10473
55. Kapentanaki S. M., Ramsey M., Gindt Y. M. and Schelvis J. P. M. (2004) Substrate electric dipole moment exerts a pH-dependent effect on electron transfer in Escherichia coli photolyase. J. Am. Chem. Soc. 126: 6214-6215
56. Husain I., Sancar G. B., Holbrook S. R. and Sancar A. (1987) Mechanism of damage recognition by Escherichia coli DNA photolyase. J. Biol. Chem. 262: 13188-13197
57. Kiener A., Husain I., Sancar A. and Walsh C. (1989) Purification and properties of Methanobacterium thermoautotrophicum DNA photolyase. J. Biol. Chem. 264: 13880-13887
58. Vande Berg B. J. and Sancar G. B. (1998) Evidence for dinucleotide flipping by DNA photolyase. J. Biol. Chem. 273: 20276-20284
59. McAteer K., Jing Y., Kao J., Taylor J.-S. and Kennedy M.-A. (1998) Solution-state structure of a DNA dodecamer duplex containing a cis-syn thymine cyclobutane dimer, the major UV photoproduct of DNA. J. Mol. Biol. 282: 1013-1032
60. Fuxreiter M., Luo N., Jedlovszky P., Simon I. and Osman R. (2002) Role of base flipping in specific recognition of damaged DNA by repair enzymes. J. Mol. Biol. 323: 823-834
61. Heelis P. F., Hartman R. F. and Rose S. D. (1995) Photoenzymic repair of UV-damaged DNA - a chemists perspective. Chem. Soc. Rev. 24
62. Kao Y.-T., Saxena C., Wang L., Sancar A. and Zhong D. (2005) Direct observation of thymine dimer repair in DNA by photolyase. Proc. Natl. Acad. Sci. USA 102: 16128-16132
63. MacFarlane A. W. and Stanley R. J. (2003) Cis-syn thymidine dimer repair by DNA photolyase in real time. Biochemistry 42: 8558-8568
64. MacFarlane A. W. and Stanley R. J. (2001) Evidence of powerful substrate electric fields in DNA photolyase: implications for thymidine dimer repair. Biochemistry 40: 15203-15214
65. Kavakli I. H. and Sancar A. (2004) Analysis of the role of intraprotein electron transfer in photoreactivation by DNA photolyase in vivo. Biochemistry 43: 15103-15110
66. Rak J., Voityuk A. A., Michel-Beyerle M.-E. and Rösch N. (1999) Effect of proton transfer on the anionic and cationic pathways of pyrimidine photodimer cleavage, a computational study. J. Phys. Chem. A 103: 3569-3574
67. Kim S. T. and Sancar A. (1991) Effect of base, pentose, and phosphodiester backbone structures on binding and repair of pyrimidine dimers by Escherichia coli DNA photolyase. Biochemistry 30: 8623-8630
68. Schleicher E., Heßling B., Illarionova V., Bacher A., Weber S., Richter G. et al. (2005) Light-induced reactions of Escherichia coli DNA photolyase monitored by Fourier transform infrared spectroscopy. FEBS J. 272: 1-12
69. Kleine T., Lockhart P. and Batschauer A. (2003) An Arabidopsis protein closely related to Synechocystis cryptochrome is targeted to organelles. Plant J. 35: 93-103
70. Kim S. T., Malhotra K., Smith C. A., Taylor J. S. and Sancar A. (1994) Characterization of (6-4) photoproduct DNA photolyase. J. Biol. Chem. 269: 8535-8540
71. Hitomi K., Nakamura H., Kim S. T., Mizukoshi T., Ishikawa T., Iwai S. et al. (2001) Role of two histidines in the (6-4) photolyase reaction. J. Biol. Chem. 276: 10103-10109
72. Schul W., Jans J., Rijksen Y. M. A., Klemann K. H. M., Eker A. P. M., Wit J. N. de, et al. (2002) Enhanced repair of cyclobutane pyrimidine dimers and improved UV resistance in photolyase transgenic mice. EMBO J. 21: 4719-4729
73. Jans J., Schul W., Sert Y. G., Rijksen Y., Rebel H., Eker A. P. M. et al. (2005) Powerful skin cancer protection by a CPD-photolyase transgene. Curr. Biol. 15: 105-115
74. Stege H., Roza L., Vink A. A., Grewe M., Ruzicka T., Grether-Beck S. et al. (2000) Enzyme plus light therapy to repair DNA damage in ultraviolet-B-irradiated human skin. Proc. Natl. Acad. Sci. USA 97: 1790-1795
75. Nakajima S., Lan L., Kanno S., Takao M., Yamamoto K., Eker A. P. M. et al. (2004) Light-induced DNA damage and tolerance for the survival of nucleotide excision repair-deficient human cells. J. Biol. Chem. 279: 46674-46677
76. Zhao X., Liu J., Hsu D. S., Zhao S., Taylor J. S. and Sancar A. (1997) Reaction mechanism of (6-4) photolyase. J. Biol. Chem. 272: 32580-32590