Effect of the multifunctional proteins RPA, YB-1, and XPC repair factor on AP site cleavage by DNA glycosylase NEIL1

Journal of Molecular Recognition

Volumn 25, Issue 4, 2012, Pages 224-233

  Pestryakov, Pavel ^a   Zharkov, Dmitry O ^a,b   Grin, Inga ^a,b   Fomina, Elizaveta E ^b   Kim, Ekaterina R ^c   Hamon, Loïc ^d   Eliseeva, Irina A ^c   Petruseva, Irina O ^a   Curmi, Patrick A ^d   Ovchinnikov, Lev P ^c   Lavrik, Olga I ^a,b  

^a INSTITUTE OF CHEMICAL BIOLOGY AND FUNDAMENTAL MEDICINE   (Russian Federation)

^b NOVOSIBIRSK STATE UNIVERSITY   (Russian Federation)

^c INSTITUTE OF PROTEIN RESEARCH   (Russian Federation)

^d UNIVERSITÉ D EVRY VAL D ESSONNE   (France)

Author keywords

AP site; DNA repair; NEIL1; RPA; XPC; YB 1

Indexed keywords

EID: 84858756494     PISSN: 09523499     EISSN: 10991352     Source Type: Journal    
DOI: 10.1002/jmr.2182     Document Type: Article

References (63)

1. Bandaru V, Zhao X, Newton MR, Burrows CJ, Wallace SS,. 2007. Human endonuclease VIII-like (NEIL) proteins in the giant DNA Mimivirus. DNA Repair (Amst). 6: 1629-1641. (Pubitemid 47610757)
2. Belousova EA, Lavrik OI,. 2010. DNA polymerases β and λ, and their roles in the DNA replication and repair. Mol Biol (Mosk). 44: 839-855.
3. Choi JY, Lim S, Kim EJ, Jo A, Guengerich FP,. 2010. Translesion synthesis across abasic lesions by human B-family and Y-family DNA polymerases α, δ, η, ι, κ, and REV1. J. Mol. Biol. 404: 34-44.
4. Clement FC, Camenisch U, Fei J, Kaczmarek N, Mathieu N, Naegeli H,. 2010. Dynamic two-stage mechanism of versatile DNA damage recognition by xeroderma pigmentosum group C protein. Mutat. Res. 685: 21-28.
5. Cohen SB, Ma W, Valova VA, Algie M, Harfoot R, Woolley AG, Robinson PJ, Braithwaite AW,. 2010. Genotoxic stress-induced nuclear localization of oncoprotein YB-1 in the absence of proteolytic processing. Oncogene 29: 403-410.
6. Das S, Chattopadhyay R, Bhakat KK, Boldogh I, Kohno LK, Prasad R, Wilson SH, Hazra TK,. 2007. Stimulation of NEIL2-mediated oxidized base excision repair via YB-1 interaction during oxidative stress. J. Biol. Chem. 282: 28474-28484. (Pubitemid 47606000)
7. D'Errico M, Parlanti E, Teson M, de Jesus BM, Degan P, Calcagnile A, Jaruga P, BjørÃ¥s M, Crescenzi M, Pedrini AM, Egly JM, Zambruno G, Stefanini M, Dizdaroglu M, Dogliotti E,. 2006. New functions of XPC in the protection of human skin cells from oxidative damage. EMBO J. 25: 4305-4315. (Pubitemid 44435228)
8. Dianov GL, Allinson SL,. 2007. DNA base damage recognition and processing. Genome Dyn Stab. 1: 287-314. (Pubitemid 44592841)
9. Dou H, Mitra S, Hazra TK,. 2003. Repair of oxidized bases in DNA bubble structures by human DNA glycosylases NEIL1 and NEIL2. J. Biol. Chem. 278: 49679-49684. (Pubitemid 37548799)
10. Dou H, Theriot CA, Das A, Hegde ML, Matsumoto Y, Boldogh I, Hazra TK, Bhakat KK, Mitra S,. 2008. Interaction of the human DNA glycosylase NEIL1 with proliferating cell nuclear antigen: the potential for replication-associated repair of oxidized bases in mammalian genomes. J. Biol. Chem. 283: 3130-3140.
11. Eliseeva IA, Kim ER, Guryanov SG, Ovchinnikov LP, Lyabin DN,. 2011. Y-box-binding protein 1 (YB-1) and its functions. Biochemistry (Mosc.) 76: 1402-1433. DOI: 10.1134/S0006297911130049.
12. Evdokimov AN, Petruseva IO, Pestryakov PE, Lavrik OI,. 2011. Photoactivated DNA analogs of substrates of the nucleotide excision repair system and their interaction with proteins of NER-competent extract of HeLa cells. Synthesis and application of long model DNA. Biochemistry (Mosc.) 76: 157-166.
13. Evdokimova VM, Kovrigina EA, Nashchekin DV, Davydova EK, Hershey JW, Ovchinnikov LP,. 1998. The major core protein of messenger ribonucleoprotein particles (p50) promotes initiation of protein biosynthesis in vitro. J. Biol. Chem. 273: 3574-3581. (Pubitemid 28109781)
14. Fan J, Matsumoto Y, Wilson DM III,. 2006. Nucleotide sequence and DNA secondary structure, as well as replication protein A, modulate the single-stranded abasic endonuclease activity of APE1. J. Biol. Chem. 281: 3889-3898. (Pubitemid 43847812)
15. Fortune JM, Stith CM, Kissling GE, Burgers PM, Kunkel TA,. 2006. RPA and PCNA suppress formation of large deletion errors by yeast DNA polymerase δ. Nucleic Acids Res. 34: 4335-4341. (Pubitemid 44567033)
16. Gaudreault I, Guay D, Lebel M,. 2004. YB-1 promotes strand separation in vitro of duplex DNA containing either mispaired bases or cisplatin modifications, exhibits endonucleolytic activities and binds several DNA repair proteins. Nucleic Acids Res. 32: 316-327. (Pubitemid 38228631)
17. Girard PM, Guibourt N, Boiteux S,. 1997. The Ogg1 protein of Saccharomyces cerevisiae: a 7,8-dihydro-8-oxoguanine DNA glycosylase/AP lyase whose lysine 241 is a critical residue for catalytic activity. Nucleic Acids Res. 25: 3204-3211. (Pubitemid 27338677)
18. Grin IR, Khodyreva SN, Nevinsky GA, Zharkov DO,. 2006. Deoxyribophosphate lyase activity of mammalian endonuclease VIII-like proteins. FEBS Lett. 580: 4916-4922. (Pubitemid 44286857)
19. Guay D, Garand C, Reddy S, Schmutte C, Lebel M,. 2008. The human endonuclease III enzyme is a relevant target to potentiate cisplatin cytotoxicity in Y-box-binding protein-1 overexpressing tumor cells. Cancer Sci. 99: 762-769. (Pubitemid 351448081)
20. Hagen L, Kavli B, Sousa MM, Torseth K, Liabakk NB, Sundheim O, Pena-Diaz J, Otterlei M, Hørning O, Jensen ON, Krokan HE, Slupphaug G,. 2008. Cell cycle-specific UNG2 phosphorylations regulate protein turnover, activity and association with RPA. EMBO J. 27: 51-61.
21. Haring SJ, Mason AC, Binz SK, Wold MS,. 2008. Cellular functions of human RPA1. Multiple roles of domains in replication, repair, and checkpoints. J. Biol. Chem. 283: 19095-19111.
22. Hasegawa SL, Doetsch PW, Hamilton KK, Martin AM, Okenquist SA, Lenz J, Boss JM,. 1991. DNA binding properties of YB-1 and dbpA: binding to double-stranded, single-stranded, and abasic site containing DNAs. Nucleic Acids Res. 19: 4915-4920. (Pubitemid 21912876)
23. Hazra TK, Izumi T, Boldogh I, Imhoff B, Kow YW, Jaruga P, Dizdaroglu M, Mitra S,. 2002. Identification and characterization of a human DNA glycosylase for repair of modified bases in oxidatively damaged DNA. Proc Natl Acad Sci U S A 99: 3523-3528. (Pubitemid 34252141)
24. Hegde ML, Theriot CA, Das A, Hegde PM, Guo Z, Gary RK, Hazra TK, Shen B, Mitra S,. 2008. Physical and functional interaction between human oxidized base-specific DNA glycosylase NEIL1 and flap endonuclease 1. J. Biol. Chem. 283: 27028-27037.
25. Hey T, Lipps G, Sugasawa K, Iwai S, Hanaoka F, Krauss G,. 2002. The XPC-HR23B complex displays high affinity and specificity for damaged DNA in a true-equilibrium fluorescence assay. Biochemistry 41: 6583-6587. (Pubitemid 34547348)
26. Iftode C, Daniely Y, Borowiec JA,. 1999. Replication protein A (RPA): the eukaryotic SSB. Crit. Rev. Biochem. Mol. Biol. 34: 141-180. (Pubitemid 29326003)
27. Ikeda S, Biswas T, Roy R, Izumi T, Boldogh I, Kurosky A, Sarker AH, Seki S, Mitra S,. 1998. Purification and characterization of human NTH1, a homolog of Escherichia coli endonuclease III. Direct identification of Lys-212 as the active nucleophilic residue. J. Biol. Chem. 273: 21585-21593. (Pubitemid 28405328)
28. Ilina ES, Lavrik OI, Khodyreva SN,. 2008. Ku antigen interacts with abasic sites. Biochim. Biophys. Acta 1784: 1777-1785.
29. Ise T, Nagatani G, Imamura T, Kato K, Takano H, Nomoto M, Izumi H, Ohmori H, Okamoto T, Ohga T, Uchiumi T, Kuwano M, Kohno K,. 1999. Transcription factor Y-box binding protein 1 binds preferentially to cisplatin-modified DNA and interacts with proliferating cell nuclear antigen. Cancer Res. 59: 342-346. (Pubitemid 29048865)
30. Izumi H, Imamura T, Nagatani G, Ise T, Murakami T, Uramoto H, Torigoe T, Ishiguchi H, Yoshida Y, Nomoto M, Okamoto T, Uchiumi T, Kuwano M, Funa K, Kohnoa K,. 2001. Y box-binding protein-1 binds preferentially to single-stranded nucleic acids and exhibits 3′ → 5′ exonuclease activity. Nucleic Acids Res. 29: 1200-1207. (Pubitemid 32186206)
31. Jaruga P, Birincioglu M, Rosenquist TA, Dizdaroglu M,. 2004. Mouse NEIL1 protein is specific for excision of 2,6-diamino-4-hydroxy-5-formamidopyrimidine and 4,6-diamino-5-formamidopyrimidine from oxidatively damaged DNA. Biochemistry 43: 15909-15914. (Pubitemid 39665090)
32. Jaruga P, Xiao Y, Vartanian V, Lloyd RS, Dizdaroglu M,. 2010. Evidence for the involvement of DNA repair enzyme NEIL1 in nucleotide excision repair of (5'R)- and (5'S)-8,5'-cyclo-2'-deoxyadenosines. Biochemistry 49: 1053-1055.
33. Kim C, Paulus BF, Wold MS,. 1994. Interactions of human replication protein A with oligonucleotides. Biochemistry 33: 14197-14206. (Pubitemid 24382365)
34. Kohno K, Izumi H, Uchiumi T, Ashizuka M, Kuwano M,. 2003. The pleiotropic functions of the Y-box-binding protein, YB-1. Bioessays 25: 691-698. (Pubitemid 36850797)
35. Koike K, Uchiumi T, Ohga T, Toh S, Wada M, Kohno K, Kuwano M,. 1997. Nuclear translocation of the Y-box binding protein by ultraviolet irradiation. FEBS Lett. 417: 390-394. (Pubitemid 27511629)
36. Krasikova YS, Belousova EA, Lebedeva NA, Pestryakov PE, Lavrik OI,. 2008. Interaction between DNA polymerase λ and RPA during translesion synthesis. Biochemistry (Mosc.) 73: 1042-1046.
37. Krishnamurthy N, Zhao X, Burrows CJ, David SS,. 2008. Superior removal of hydantoin lesions relative to other oxidized bases by the human DNA glycosylase hNEIL1. Biochemistry 47: 7137-7146. (Pubitemid 351956362)
38. de Laat WL, Appeldoorn E, Sugasawa K, Weterings E, Jaspers NG, Hoeijmakers JH,. 1998. DNA-binding polarity of human replication protein A positions nucleases in nucleotide excision repair. Genes Dev. 12: 2598-2609. (Pubitemid 28406961)
39. Lindahl T,. 1993. Instability and decay of the primary structure of DNA. Nature 362: 709-715. (Pubitemid 23125973)
40. Maga G, Frouin I, Spadari S, Hubscher U,. 2001. Replication protein A as a "fidelity clamp" for DNA polymerase α. J. Biol. Chem. 276: 18235-18242.
41. Maga G, Villani G, Crespan E, Wimmer U, Ferrari E, Bertocci B, Hübscher U,. 2007. 8-oxo-guanine bypass by human DNA polymerases in the presence of auxiliary proteins. Nature 447: 606-608. (Pubitemid 46868042)
42. Marenstein DR, Ocampo MT, Chan MK, Altamirano A, Basu AK, Boorstein RJ, Cunningham RP, Teebor GW,. 2001. Stimulation of human endonuclease III by Y box-binding protein 1 (DNA-binding protein B). Interaction between a base excision repair enzyme and a transcription factor. J. Biol. Chem. 276: 21242-21249.
43. Morland I, Rolseth V, Luna L, Rognes T, BjørÃ¥s M, Seeberg E,. 2002. Human DNA glycosylases of the bacterial Fpg/MutM superfamily: an alternative pathway for the repair of 8-oxoguanine and other oxidation products in DNA. Nucleic Acids Res. 30: 4926-4936. (Pubitemid 35414653)
44. Ohga T, Koike K, Ono M, Makino Y, Itagaki Y, Tanimoto M, Kuwano M, Kohno K,. 1996. Role of the human Y box-binding protein YB-1 in cellular sensitivity to the DNA-damaging agents cisplatin, mitomycin C, and ultraviolet light. Cancer Res. 56: 4224-4228. (Pubitemid 26305020)
45. Parker A, Gu Y, Mahoney W, Lee SH, Singh KK, Lu AL,. 2001. Human homolog of the MutY repair protein (hMYH) physically interacts with proteins involved in long patch DNA base excision repair. J. Biol. Chem. 276: 5547-5555.
46. Parsons JL, Zharkov DO, Dianov GL,. 2005. NEIL1 excises 3' end proximal oxidative DNA lesions resistant to cleavage by NTH1 and OGG1. Nucleic Acids Res. 33: 4849-4856. (Pubitemid 41418884)
47. Prasad R, Liu Y, Deterding LJ, Poltoratsky VP, Kedar PS, Horton JK, Kanno S-I, Asagoshi K, Hou EW, Khodyreva SN, Lavrik OI, Tomer KB, Yasui A, Wilson SH,. 2007. HMGB1 is a cofactor in mammalian base excision repair. Mol. Cell 27: 829-841. (Pubitemid 47333218)
48. Reardon JT, Mu D, Sancar A,. 1996. Overproduction, purification, and characterization of the XPC subunit of the human DNA repair excision nuclease. J. Biol. Chem. 271: 19451-19456. (Pubitemid 26271618)
49. Rieger RA, Zaika EI, Xie W, Johnson F, Grollman AP, Iden CR, Zharkov DO,. 2006. Proteomic approach to identification of proteins reactive for abasic sites in DNA. Mol. Cell. Proteomics 5: 858-867. (Pubitemid 43792795)
50. Roche Y, Zhang D, Segers-Nolten GM, Vermeulen W, Wyman C, Sugasawa K, Hoeijmakers J, Otto C,. 2008. Fluorescence correlation spectroscopy of the binding of nucleotide excision repair protein XPC-hHr23B with DNA substrates. J. Fluoresc. 18: 987-995.
51. Rosenquist TA, Zharkov DO, Grollman AP,. 1997. Cloning and characterization of a mammalian 8-oxoguanine DNA glycosylase. Proc Natl Acad Sci U S A 94: 7429-7434. (Pubitemid 27345332)
52. Rosenquist TA, Zaika E, Fernandes AS, Zharkov DO, Miller H, Grollman AP,. 2003. The novel DNA glycosylase, NEIL1, protects mammalian cells from radiation-mediated cell death. DNA Repair (Amst). 2: 581-591. (Pubitemid 36507126)
53. Shimizu Y, Iwai S, Hanaoka F, Sugasawa K,. 2003. Xeroderma pigmentosum group C protein interacts physically and functionally with thymine DNA glycosylase. EMBO J. 22: 164-173. (Pubitemid 36091279)
54. Shimizu Y, Uchimura Y, Dohmae N, Saitoh H, Hanaoka F, Sugasawa K,. 2010. Stimulation of DNA glycosylase activities by XPC protein complex: roles of protein-protein interactions. J Nucleic Acids. 2010. pii: 805698. DOI: 10.4061/2010/805698.
55. de Souza-Pinto NC, Mason PA, Hashiguchi K, Weissman L, Tian J, Guay D, Lebel M, Stevnsner TV, Rasmussen LJ, Bohr VA,. 2009. Novel DNA mismatch-repair activity involving YB-1 in human mitochondria. DNA Repair (Amst). 8: 704-719.
56. Sugasawa K, Shimizu Y, Iwai S, Hanaoka F,. 2002. A molecular mechanism for DNA damage recognition by the xeroderma pigmentosum group C protein complex. DNA Repair (Amst). 1: 95-107. (Pubitemid 34475695)
57. Takao M, Kanno S, Kobayashi K, Zhang QM, Yonei S, van der Horst GT, Yasui A,. 2002. A back-up glycosylase in Nth1 knock-out mice is a functional Nei (endonuclease VIII) homologue. J. Biol. Chem. 277: 42205-42213. (Pubitemid 35257539)
58. Theriot CA, Hegde ML, Hazra TK, Mitra S,. 2010. RPA physically interacts with the human DNA glycosylase NEIL1 to regulate excision of oxidative DNA base damage in primer-template structures. DNA Repair (Amst). 9: 643-652.
59. Weisshart K, Pestryakov P, Smith RW, Hartmann H, Kremmer E, Lavrik O, Nasheuer HP,. 2004. Coordinated regulation of replication protein A activities by its subunits p14 and p32. J. Biol. Chem. 279: 35368-35376. (Pubitemid 39100536)
60. Wiederhold L, Leppard JB, Kedar P, Karimi-Busheri F, Rasouli-Nia A, Weinfeld M, Tomkinson AE, Izumi T, Prasad R, Wilson SH, Mitra S, Hazra TK,. 2004. AP endonuclease-independent DNA base excision repair in human cells. Mol. Cell 15: 209-220. (Pubitemid 38950968)
61. Wilson DM III, Barsky D,. 2001. The major human abasic endonuclease: formation, consequences and repair of abasic lesions in DNA. Mutat. Res. 485: 283-307. (Pubitemid 32406284)
62. Zasedateleva OA, Krylov AS, Prokopenko DV, Skabkin MA, Ovchinnikov LP, Kolchinsky A, Mirzabekov AD,. 2002. Specificity of mammalian Y-box binding protein p50 in interaction with ss and ds DNA analyzed with generic oligonucleotide microchip. J. Mol. Biol. 324: 73-87. (Pubitemid 35352181)
63. Zhao X, Krishnamurthy N, Burrows CJ, David SS,. 2010. Mutation versus repair: NEIL1 removal of hydantoin lesions in single-stranded, bulge, bubble, and duplex DNA contexts. Biochemistry 49: 1658-1666.