RPA physically interacts with the human DNA glycosylase NEIL1 to regulate excision of oxidative DNA base damage in primer-template structures

DNA Repair

Volumn 9, Issue 6, 2010, Pages 643-652

  Theriot, Corey A ^a   Hegde, Muralidhar L ^a   Hazra, Tapas K ^a   Mitra, Sankar ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Base excision repair; DNA glycosylase; NEIL1; Protein protein interaction; Replication associated repair; RPA

Indexed keywords

CYCLINE; DNA BASE; DNA BINDING PROTEIN; DNA GLYCOSYLTRANSFERASE; FLAP ENDONUCLEASE; REPLICATION FACTOR A; SINGLE STRANDED DNA; URACIL; 5-HYDROXYURACIL; DNA; NEIL1 PROTEIN, HUMAN; PRIMER DNA; PROTEIN BINDING;

ANTIGEN ANTIBODY COMPLEX; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; ENZYME ACTIVATION; ESCHERICHIA COLI; EXCISION REPAIR; GENE DELETION; HELA CELL; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; WILD TYPE; ANALOGS AND DERIVATIVES; CELL NUCLEUS; CHEMISTRY; DRUG EFFECTS; ENZYME SPECIFICITY; GEL MOBILITY SHIFT ASSAY; GENETICS; HELA CELL LINE; METABOLISM; NUCLEOTIDE SEQUENCE; SINGLE STRANDED DNA BREAK;

BASE SEQUENCE; CELL NUCLEUS; DNA; DNA BREAKS, SINGLE-STRANDED; DNA DAMAGE; DNA GLYCOSYLASES; DNA PRIMERS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HELA CELLS; HUMANS; OXIDATIVE STRESS; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN BINDING; REPLICATION PROTEIN A; SUBSTRATE SPECIFICITY; URACIL;

ESCHERICHIA COLI;

EID: 77952580830     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2010.02.014     Document Type: Article

References (54)

1. Breen A.P., and Murphy J.A. Reactions of oxyl radicals with DNA. Free Radic. Biol. Med. 18 (1995) 1033-1077
2. Cadet J.L., and Brannock C. Free radicals and the pathobiology of brain dopamine systems. Neurochem. Int. 32 (1998) 117-131
3. Grisham M.B., Hernandez L.A., and Granger D.N. Xanthine oxidase and neutrophil infiltration in intestinal ischemia. Am. J. Physiol. 251 (1986) G567-574
4. Ames B.N., Shigenaga M.K., and Hagen T.M. Oxidants, antioxidants, and the degenerative diseases of aging. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 7915-7922
5. Bozner P., Grishko V., LeDoux S.P., Wilson G.L., Chyan Y.C., and Pappolla M.A. The amyloid beta protein induces oxidative damage of mitochondrial DNA. J. Neuropathol. Exp. Neurol. 56 (1997) 1356-1362
6. DeWeese T.L., Shipman J.M., Larrier N.A., Buckley N.M., Kidd L.R., Groopman J.D., Cutler R.G., te Riele H., and Nelson W.G. Mouse embryonic stem cells carrying one or two defective Msh2 alleles respond abnormally to oxidative stress inflicted by low-level radiation. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 11915-11920
7. Meyer T.E., Liang H.Q., Buckley A.R., Buckley D.J., Gout P.W., Green E.H., and Bode A.M. Changes in glutathione redox cycling and oxidative stress response in the malignant progression of NB2 lymphoma cells. Int. J. Cancer 77 (1998) 55-63
8. Mukherjee S.K., and Adams Jr. J.D. The effects of aging and neurodegeneration on apoptosis-associated DNA fragmentation and the benefits of nicotinamide. Mol. Chem. Neuropathol. 32 (1997) 59-74
9. Multhaup G., Ruppert T., Schlicksupp A., Hesse L., Beher D., Masters C.L., and Beyreuther K. Reactive oxygen species and Alzheimer's disease. Biochem. Pharmacol. 54 (1997) 533-539
10. Krokan H.E., Nilsen H., Skorpen F., Otterlei M., and Slupphaug G. Base excision repair of DNA in mammalian cells. FEBS Lett. 476 (2000) 73-77
11. Mitra S., Izumi T., Boldogh I., Bhakat K.K., Hill J.W., and Hazra T.K. Choreography of oxidative damage repair in mammalian genomes. Free Radic. Biol. Med. 33 (2002) 15-28
12. Ikeda S., Biswas T., Roy R., Izumi T., Boldogh I., Kurosky A., Sarker A.H., Seki S., and Mitra S. 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 (1998) 21585-21593
13. Radicella J.P., Dherin C., Desmaze C., Fox M.S., and Boiteux S. Cloning and characterization of hOGG1, a human homolog of the OGG1 gene of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 8010-8015
14. Bandaru V., Sunkara S., Wallace S.S., and Bond J.P. A novel human DNA glycosylase that removes oxidative DNA damage and is homologous to Escherichia coli endonuclease VIII. DNA Repair (Amst.) 1 (2002) 517-529
15. Hazra T.K., Izumi T., Boldogh I., Imhoff B., Kow Y.W., Jaruga P., Dizdaroglu M., and Mitra S. 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 (2002) 3523-3528
16. Hazra T.K., Kow Y.W., Hatahet Z., Imhoff B., Boldogh I., Mokkapati S.K., Mitra S., and Izumi T. Identification and characterization of a novel human DNA glycosylase for repair of cytosine-derived lesions. J. Biol. Chem. 277 (2002) 30417-30420
17. Morland I., Rolseth V., Luna L., Rognes T., Bjoras M., and Seeberg E. 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 (2002) 4926-4936
18. Takao M., Kanno S., Kobayashi K., Zhang Q.M., Yonei S., van der Horst G.T., and Yasui A. A back-up glycosylase in Nth1 knock-out mice is a functional Nei (endonuclease VIII) homologue. J. Biol. Chem. 277 (2002) 42205-42213
19. Hill J.W., Hazra T.K., Izumi T., and Mitra S. Stimulation of human 8-oxoguanine-DNA glycosylase by AP-endonuclease: potential coordination of the initial steps in base excision repair. Nucleic Acids Res. 29 (2001) 430-438
20. Wiederhold L., Leppard J.B., Kedar P., Karimi-Busheri F., Rasouli-Nia A., Weinfeld M., Tomkinson A.E., Izumi T., Prasad R., Wilson S.H., Mitra S., and Hazra T.K. AP endonuclease-independent DNA base excision repair in human cells. Mol. Cell 15 (2004) 209-220
21. Tomkinson A.E., Chen L., Dong Z., Leppard J.B., Levin D.S., Mackey Z.B., and Motycka T.A. Completion of base excision repair by mammalian DNA ligases. Prog. Nucleic Acid Res. Mol. Biol. 68 (2001) 151-164
22. Podlutsky A.J., Dianova I.I., Wilson S.H., Bohr V.A., and Dianov G.L. DNA synthesis and dRPase activities of polymerase beta are both essential for single-nucleotide patch base excision repair in mammalian cell extracts. Biochemistry 40 (2001) 809-813
23. Dou H., Mitra S., and Hazra T.K. Repair of oxidized bases in DNA bubble structures by human DNA glycosylases NEIL1 and NEIL2. J. Biol. Chem. 278 (2003) 49679-49684
24. Das A., Boldogh I., Lee J.W., Harrigan J.A., Hegde M.L., Piotrowski J., de Souza Pinto N., Ramos W., Greenberg M.M., Hazra T.K., Mitra S., and Bohr V.A. The human Werner syndrome protein stimulates repair of oxidative DNA base damage by the DNA glycosylase NEIL1. J. Biol. Chem. 282 (2007) 26591-26602
25. Dou H., Theriot C.A., Das A., Hegde M.L., Matsumoto Y., Boldogh I., Hazra T.K., Bhakat K.K., and Mitra S. 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 (2008) 3130-3140
26. Hegde M.L., Theriot C.A., Das A., Hegde P.M., Guo Z., Gary R.K., Hazra T.K., Shen B., and Mitra S. Physical and functional interaction between human oxidized base-specific DNA glycosylase neil1 and flap endonuclease 1. J. Biol. Chem. (2008)
27. Guan X., Bai H., Shi G., Theriot C.A., Hazra T.K., Mitra S., and Lu A.L. The human checkpoint sensor Rad9-Rad1-Hus1 interacts with and stimulates NEIL1 glycosylase. Nucleic Acids Res. 35 (2007) 2463-2472
28. Melendy T., and Stillman B. An interaction between replication protein A and SV40 T antigen appears essential for primosome assembly during SV40 DNA replication. J. Biol. Chem. 268 (1993) 3389-3395
29. Stillman B., Bell S.P., Dutta A., and Marahrens Y. DNA replication and the cell cycle. Ciba Found. Symp. 170 (1992) 147-156 (discussion 156-160)
30. Waga S., Bauer G., and Stillman B. Reconstitution of complete SV40 DNA replication with purified replication factors. J. Biol. Chem. 269 (1994) 10923-10934
31. Deng X., Habel J.E., Kabaleeswaran V., Snell E.H., Wold M.S., and Borgstahl G.E. Structure of the full-length human RPA14/32 complex gives insights into the mechanism of DNA binding and complex formation. J. Mol. Biol. 374 (2007) 865-876
32. Richard D.J., Bolderson E., Cubeddu L., Wadsworth R.I., Savage K., Sharma G.G., Nicolette M.L., Tsvetanov S., McIlwraith M.J., Pandita R.K., Takeda S., Hay R.T., Gautier J., West S.C., Paull T.T., Pandita T.K., White M.F., and Khanna K.K. Single-stranded DNA-binding protein hSSB1 is critical for genomic stability. Nature 453 (2008) 677-681
33. Binz S.K., Sheehan A.M., and Wold M.S. Replication protein A phosphorylation and the cellular response to DNA damage. DNA Repair (Amst.) 3 (2004) 1015-1024
34. Gomes X.V., and Wold M.S. Functional domains of the 70-kilodalton subunit of human replication protein A. Biochemistry 35 (1996) 10558-10568
35. de Laat W.L., Appeldoorn E., Sugasawa K., Weterings E., Jaspers N.G., and Hoeijmakers J.H. DNA-binding polarity of human replication protein A positions nucleases in nucleotide excision repair. Genes Dev. 12 (1998) 2598-2609
36. Iftode C., and Borowiec J.A. 5′ → 3′ molecular polarity of human replication protein A (hRPA) binding to pseudo-origin DNA substrates. Biochemistry 39 (2000) 11970-11981
37. Bastin-Shanower S.A., and Brill S.J. Functional analysis of the four DNA binding domains of replication protein A. The role of RPA2 in ssDNA binding. J. Biol. Chem. 276 (2001) 36446-36453
38. Arunkumar A.I., Stauffer M.E., Bochkareva E., Bochkarev A., and Chazin W.J. Independent and coordinated functions of replication protein A tandem high affinity single-stranded DNA binding domains. J. Biol. Chem. 278 (2003) 41077-41082
39. Wyka I.M., Dhar K., Binz S.K., and Wold M.S. Replication protein A interactions with DNA: differential binding of the core domains and analysis of the DNA interaction surface. Biochemistry 42 (2003) 12909-12918
40. Jiang X., Klimovich V., Arunkumar A.I., Hysinger E.B., Wang Y., Ott R.D., Guler G.D., Weiner B., Chazin W.J., and Fanning E. Structural mechanism of RPA loading on DNA during activation of a simple pre-replication complex. EMBO J. 25 (2006) 5516-5526
41. Haring S.J., Mason A.C., Binz S.K., and Wold M.S. Cellular functions of human RPA1. Multiple roles of domains in replication, repair, and checkpoints. J. Biol. Chem. 283 (2008) 19095-19111
42. Zou Y., Liu Y., Wu X., and Shell S.M. Functions of human replication protein A (RPA): from DNA replication to DNA damage and stress responses. J. Cell. Physiol. 208 (2006) 267-273
43. Fan J., Matsumoto Y., and Wilson III D.M. 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 (2006) 3889-3898
44. Otterlei M., Warbrick E., Nagelhus T.A., Haug T., Slupphaug G., Akbari M., Aas P.A., Steinsbekk K., Bakke O., and Krokan H.E. Post-replicative base excision repair in replication foci. EMBO J. 18 (1999) 3834-3844
45. Hagen L., Kavli B., Sousa M.M., Torseth K., Liabakk N.B., Sundheim O., Pena-Diaz J., Otterlei M., Horning O., Jensen O.N., Krokan H.E., and Slupphaug G. Cell cycle-specific UNG2 phosphorylations regulate protein turnover, activity and association with RPA. EMBO J. 27 (2008) 51-61
46. Sukhodolets K.E., Hickman A.B., Agarwal S.K., Sukhodolets M.V., Obungu V.H., Novotny E.A., Crabtree J.S., Chandrasekharappa S.C., Collins F.S., Spiegel A.M., Burns A.L., and Marx S.J. The 32-kilodalton subunit of replication protein A interacts with menin, the product of the MEN1 tumor suppressor gene. Mol. Cell. Biol. 23 (2003) 493-509
47. Hazra T.K., and Mitra S. Purification and characterization of NEIL1 and NEIL2, members of a distinct family of mammalian DNA glycosylases for repair of oxidized bases. Methods Enzymol. 408 (2006) 33-48
48. Das A., Wiederhold L., Leppard J.B., Kedar P., Prasad R., Wang H., Boldogh I., Karimi-Busheri F., Weinfeld M., Tomkinson A.E., Wilson S.H., Mitra S., and Hazra T.K. NEIL2-initiated, APE-independent repair of oxidized bases in DNA: Evidence for a repair complex in human cells. DNA Repair (Amst.) 5 (2006) 1439-1448
49. Kolpashchikov D.M., Khodyreva S.N., Khlimankov D.Y., Wold M.S., Favre A., and Lavrik O.I. Polarity of human replication protein A binding to DNA. Nucleic Acids Res. 29 (2001) 373-379
50. Fanning E., Klimovich V., and Nager A.R. A dynamic model for replication protein A (RPA) function in DNA processing pathways. Nucleic Acids Res. 34 (2006) 4126-4137
51. Cai L., Roginskaya M., Qu Y., Yang Z., Xu Y., and Zou Y. Structural characterization of human RPA sequential binding to single-stranded DNA using ssDNA as a molecular ruler. Biochemistry 46 (2007) 8226-8233
52. Wold M.S. Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu. Rev. Biochem. 66 (1997) 61-92
53. Bochkareva E., Korolev S., Lees-Miller S.P., and Bochkarev A. Structure of the RPA trimerization core and its role in the multistep DNA-binding mechanism of RPA. EMBO J. 21 (2002) 1855-1863
54. Wood R.D. DNA damage recognition during nucleotide excision repair in mammalian cells. Biochimie 81 (1999) 39-44