XRCC1 coordinates disparate responses and multiprotein repair complexes depending on the nature and context of the DNA damage

Environmental and Molecular Mutagenesis

Volumn 52, Issue 8, 2011, Pages 623-635

  Hanssen Bauer, Audun ^a   Solvang Garten, Karin ^a   Sundheim, Ottar ^a   Peña Diaz, Javier ^a   Andersen, Sonja ^a   Slupphaug, Geir ^a   Krokan, Hans E ^a   Wilson, David M ^b   Akbari, Mansour ^a   Otterlei, Marit ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

Base excision repair; DNA repair complexes; Micro irradiation; PARP inhibitors; PCNA

Indexed keywords

CELL EXTRACT; CYCLINE; DNA DIRECTED DNA POLYMERASE BETA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; XRCC1 PROTEIN;

ARTICLE; CONFOCAL MICROSCOPY; DNA DAMAGE; DNA PROTEIN COMPLEX; DNA REPLICATION; EXCISION REPAIR; GEL FILTRATION; GENETIC TRANSFECTION; IMMUNOPRECIPITATION; PROTEIN LOCALIZATION; ULTRAVIOLET IRRADIATION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELL CULTURE TECHNIQUES; CHO CELLS; CRICETINAE; CRICETULUS; DNA BREAKS, SINGLE-STRANDED; DNA POLYMERASE BETA; DNA REPAIR; DNA-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, RADIATION; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; LASERS; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; POLY(ADP-RIBOSE) POLYMERASES; POLYNUCLEOTIDE 5'-HYDROXYL-KINASE; PROLIFERATING CELL NUCLEAR ANTIGEN; RECOMBINANT FUSION PROTEINS; TRANSFECTION;

EID: 80053648571     PISSN: 08936692     EISSN: 10982280     Source Type: Journal    
DOI: 10.1002/em.20663     Document Type: Article

References (54)

1. Aas PA, Otterlei M, Falnes PO, Vagbo CB, Skorpen F, Akbari M, Sundheim O, Bjoras M, Slupphaug G, Seeberg E, Krokan HE. 2003. Human and bacterial oxidative demethylases repair alkylation damage in both RNA, DNA. Nature 421: 859-863.
2. Abdelkarim GE, Gertz K, Harms C, Katchanov J, Dirnagl U, Szabo C, Endres M. 2001. Protective effects of PJ34, a novel, potent inhibitor of poly(ADP-ribose) polymerase (PARP) in in vitro and in vivo models of stroke. Int J Mol Med 7: 255-260.
3. Akbari M, Otterlei M, Pena-Diaz J, Aas PA, Kavli B, Liabakk NB, Hagen L, Imai K, Durandy A, Slupphaug G, Krokan HE. 2004. Repair of U/G and U/A in DNA by UNG2-associated repair complexes takes place predominantly by short-patch repair both in proliferating and growth-arrested cells. Nucleic Acids Res 32: 5486-5498.
4. Akbari M, Solvang-Garten K, Hanssen-Bauer A, Lieske NV, Pettersen HS, Pettersen GK, Wilson DMIII, Krokan HE, Otterlei M. 2010. Direct interaction between XRCC1 and UNG2 facilitates rapid repair of uracil in DNA by XRCC1 complexes. DNA Repair (Amst) 9: 785-795.
5. Bedard K, Krause KH. 2007. The NOX family of ROS-generating NADPH oxidases: Physiology and pathophysiology. Physiol Rev 87: 245-313.
6. Beernink PT, Hwang M, Ramirez M, Murphy MB, Doyle SA, Thelen MP. 2005. Specificity of protein interactions mediated by BRCT domains of the XRCC1 DNA repair protein. J Biol Chem 280: 30206-30213.
7. Bekker-Jensen S, Lukas C, Kitagawa R, Melander F, Kastan MB, Bartek J, Lukas J. 2006. Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J Cell Biol 173: 195-206.
8. Caldecott KW. 2001. Mammalian DNA single-strand break repair: An X-ra(y)ted affair. Bioessays 23: 447-455.
9. Caldecott KW, McKeown CK, Tucker JD, Ljungquist S, Thompson LH. 1994. An interaction between the mammalian DNA repair protein XRCC1 and DNA ligase III. Mol Cell Biol 14: 68-76.
10. Caldecott KW, Aoufouchi S, Johnson P, Shall S. 1996. XRCC1 polypeptide interacts with DNA polymerase beta and possibly poly (ADP-ribose) polymerase, and DNA ligase III is a novel molecular 'nick-sensor' in vitro. Nucleic Acids Res 24: 4387-4394.
11. Campalans A, Marsin S, Nakabeppu Y, O'Connor TR, Boiteux S, Radicella JP. 2005. XRCC1 interactions with multiple DNA glycosylases: A model for its recruitment to base excision repair. DNA Repair (Amst) 4: 826-835.
12. El-Khamisy SF, Saifi GM, Weinfeld M, Johansson F, Helleday T, Lupski JR, Caldecott KW. 2005. Defective DNA single-strand break repair in spinocerebellar ataxia with axonal neuropathy-1. Nature 434: 108-113.
13. Fan J, Wilson DMIII. 2005. Protein-protein interactions and posttranslational modifications in mammalian base excision repair. Free Radic Biol Med 38: 1121-1138.
14. Fan J, Otterlei M, Wong HK, Tomkinson AE, Wilson DMIII. 2004. XRCC1 co-localizes and physically interacts with PCNA. Nucleic Acids Res 32: 2193-2201.
15. Frosina G, Cappelli E, Fortini P, Dogliotti E. 1999. In vitro base excision repair assay using mammalian cell extracts. Methods Mol Biol 113: 301-315.
16. Godon C, Cordelieres FP, Biard D, Giocanti N, Megnin-Chanet F, Hall J, Favaudon V. 2008. PARP inhibition versus PARP-1 silencing: different outcomes in terms of single-strand break repair and radiation susceptibility. Nucleic Acids Res 36: 4454-4464.
17. Ha YJ, Seul HJ, Lee JR. 2011. Ligation of CD40 receptor in human B lymphocytes triggers the 5-lipoxygenase pathway to produce reactive oxygen species and activate p38 MAPK. Exp Mol Med 41: 101-110.
18. Hagen L, Kavli B, Sousa MM, Torseth K, Liabakk NB, Sundheim O, Pena-Diaz J, Otterlei M, Horning 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.
19. Heacock ML, Stefanick DF, Horton JK, Wilson SH. 2010. Alkylation DNA damage in combination with PARP inhibition results in formation of S-phase-dependent double-strand breaks. DNA Repair (Amst) 9: 929-936.
20. Hegde ML, Hazra TK, Mitra S. 2008. Early steps in the DNA base excision/single-strand interruption repair pathway in mammalian cells. Cell Res 18: 27-47.
21. Herrlich P, Karin M, Weiss C. 2008. Supreme EnLIGHTenment: Damage recognition and signaling in the mammalian UV response. Mol Cell 29: 279-290.
22. Hirano M, Yamamoto A, Mori T, Lan L, Iwamoto TA, Aoki M, Shimada K, Furiya Y, Kariya S, Asai H, Yasui A, Nishiwaki T, Imoto K, Kobayashi N, Kiriyama T, Nagata T, Konishi N, Itoyama Y, Ueno S. 2007. DNA single-strand break repair is impaired in aprataxin-related ataxia. Ann Neurol 61: 162-174.
23. Jelezcova E, Trivedi RN, Wang XH, Tang JB, Brown AR, Goellner EM, Schamus S, Fornsaglio JL, Sobol RW. 2010. Parp1 activation in mouse embryonic fibroblasts promotes Pol beta-dependent cellular hypersensitivity to alkylation damage. Mutat Res 686: 57-67.
24. Kedar PS, Kim SJ, Robertson A, Hou E, Prasad R, Horton JK, Wilson SH. 2002. Direct interaction between mammalian DNA polymerase β and proliferating cell nuclear antigen. J Biol Chem 277: 31115-31123.
25. Kim K, Biade S, Matsumoto Y. 1998. Involvement of flap endonuclease 1 in base excision DNA repair. J Biol Chem 273: 8842-8848.
26. Kong X, Mohanty SK, Stephens J, Heale JT, Gomez-Godinez V, Shi LZ, Kim JS, Yokomori K, Berns MW. 2009. Comparative analysis of different laser systems to study cellular responses to DNA damage in mammalian cells. Nucleic Acids Res 37: e68.
27. Krokan H, Schaffer P, DePamphilis ML. 1979. Involvement of eucaryotic deoxyribonucleic acid polymerases alpha and gamma in the replication of cellular and viral deoxyribonucleic acid. Biochemistry 18: 4431-4443.
28. Lan L, Nakajima S, Oohata Y, Takao M, Okano S, Masutani M, Wilson SH, Yasui A. 2004. In situ analysis of repair processes for oxidative DNA damage in mammalian cells. Proc Natl Acad Sci USA 101: 13738-13743.
29. Leonhardt H, Rahn HP, Weinzierl P, Sporbert A, Cremer T, Zink D, Cardoso MC. 2000. Dynamics of DNA replication factories in living cells. J Cell Biol 149: 271-280.
30. Lonn P, van der Heide LP, Dahl M, Hellman U, Heldin CH, Moustakas A. 2010. PARP-1 attenuates Smad-mediated transcription. Mol Cell 40: 521-532.
31. Luo H, Chan DW, Yang T, Rodriguez M, Chen BP, Leng M, Mu JJ, Chen D, Songyang Z, Wang Y, Qin J. 2004. A new XRCC1-containing complex and its role in cellular survival of methyl methanesulfonate treatment. Mol Cell Biol 24: 8356-8365.
32. Marsin S, Vidal AE, Sossou M, Menissier-de Murcia J, Le Page F, Boiteux S, de Murcia G, Radicella JP. 2003. Role of XRCC1 in the coordination and stimulation of oxidative DNA damage repair initiated by the DNA glycosylase hOGG1. J Biol Chem 278: 44068-44074.
33. Masson M, Niedergang C, Schreiber V, Muller S, Menissier-de Murcia J, de Murcia G. 1998. XRCC1 is specifically associated with poly(ADP-ribose) polymerase and negatively regulates its activity following DNA damage. Mol Cell Biol 18: 3563-3571.
34. Megnin-Chanet F, Bollet MA, Hall J. 2010. Targeting poly(ADP-ribose) polymerase activity for cancer therapy. Cell Mol Life Sci 67: 3649-3662.
35. Mortusewicz O, Leonhardt H. 2007. XRCC1 and PCNA are loading platforms with distinct kinetic properties and different capacities to respond to multiple DNA lesions. BMC Mol Biol 8: 81.
36. Mortusewicz O, Rothbauer U, Cardoso MC, Leonhardt H. 2006. Differential recruitment of DNA Ligase I, III to DNA repair sites. Nucleic Acids Res 34: 3523-3532.
37. Mortusewicz O, Ame JC, Schreiber V, Leonhardt H. 2007. Feedback-regulated poly(ADP-ribosyl)ation by PARP-1 is required for rapid response to DNA damage in living cells. Nucleic Acids Res 35: 7665-7675.
38. Nguyen LH, Barsky D, Erzberger JP, Wilson DMIII. 2000. Mapping the protein-DNA interface and the metal-binding site of the major human apurinic/apyrimidinic endonuclease. J Mol Biol 298: 447-459.
39. Opresko PL, Otterlei M, Graakjaer J, Bruheim P, Dawut L, Kolvraa S, May A, Seidman MM, Bohr VA. 2004. The Werner syndrome helicase and exonuclease cooperate to resolve telomeric D loops in a manner regulated by TRF1 and TRF2. Mol Cell 14: 763-774.
40. Parlanti E, Locatelli G, Maga G, Dogliotti E. 2007. Human base excision repair complex is physically associated to DNA replication and cell cycle regulatory proteins. Nucleic Acids Res 35: 1569-1577.
41. Parsons JL, Dianova II, Allinson SL, Dianov GL. 2005a. DNA Polymerase β promotes recruitment of DNA ligase IIIα-XRCC1 to sites of base excision repair. Biochemistry 44: 10613-10619.
42. Parsons JL, Dianova II, Allinson SL, Dianov GL. 2005b. Poly(ADP-ribose) polymerase-1 protects excessive DNA strand breaks from deterioration during repair in human cell extracts. FEBS J 272: 2012-2021.
43. Prasad R, Liu Y, Deterding LJ, Poltoratsky VP, Kedar PS, Horton JK, Kanno S, 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.
44. Schreiber V, Ame JC, Dolle P, Schultz I, Rinaldi B, Fraulob V, Menissier-de Murcia J, de Murcia G. 2002. Poly(ADP-ribose) polymerase-2 (PARP-2) is required for efficient base excision DNA repair in association with PARP-1 and XRCC1. J Biol Chem 277: 23028-23036.
45. Sharma S, Otterlei M, Sommers JA, Driscoll HC, Dianov GL, Kao HI, Bambara RA, Brosh RM, Jr. 2004. WRN helicase and FEN-1 form a complex upon replication arrest and together process branchmigrating DNA structures associated with the replication fork. Mol Biol Cell 15: 734-750.
46. Slupphaug G, Eftedal I, Kavli B, Bharati S, Helle NM, Haug T, Levine DW, Krokan HE. 1995. Properties of a recombinant human uracil-DNA glycosylase from the UNG gene and evidence that UNG encodes the major uracil-DNA glycosylase. Biochemistry 34: 128-138.
47. Stilmann M, Hinz M, Arslan SC, Zimmer A, Schreiber V, Scheidereit C. 2009. A nuclear poly(ADP-ribose)-dependent signalosome confers DNA damage-induced IkappaB kinase activation. Mol Cell 36: 365-378.
48. Strom CE, Johansson F, Uhlen M, Al-Khalili Szigyarto C, Erixon K, Helleday T. 2011. Poly (ADP-ribose) polymerase (PARP) is not involved in base excision repair but PARP inhibition traps a single-strand intermediate. Nucleic Acids Res 39:3166-3175.
49. Tebbs RS, Flannery ML, Meneses JJ, Hartmann A, Tucker JD, Thompson LH, Cleaver JE, Pedersen RA. 1999. Requirement for the Xrcc1 DNA base excision repair gene during early mouse development. Dev Biol 208: 513-529.
50. Vidal AE, Boiteux S, Hickson ID, Radicella JP. 2001. XRCC1 coordinates the initial and late stages of DNA abasic site repair through protein-protein interactions. EMBO J 20: 6530-6539.
51. Vodenicharov MD, Sallmann FR, Satoh MS, Poirier GG. 2000. Base excision repair is efficient in cells lacking poly(ADP-ribose) polymerase 1. Nucleic Acids Res 28: 3887-3896.
52. von Kobbe C, Harrigan JA, May A, Opresko PL, Dawut L, Cheng WH, Bohr VA. 2003. Central role for the Werner syndrome protein/poly(ADP-ribose) polymerase 1 complex in the poly (ADP-ribosyl)ation pathway after DNA damage. Mol Cell Biol 23: 8601-8613.
53. Whitehouse CJ, Taylor RM, Thistlethwaite A, Zhang H, Karimi-Busheri F, Lasko DD, Weinfeld M, Caldecott KW. 2001. XRCC1 stimulates human polynucleotide kinase activity at damaged DNA termini and accelerates DNA single-strand break repair. Cell 104: 107-117.
54. Yalcin S, Marinkovic D, Mungamuri SK, Zhang X, Tong W, Sellers R, Ghaffari S. 2010. ROS-mediated amplification of AKT/mTOR signalling pathway leads to myeloproliferative syndrome in Foxo3(-/-) mice. EMBO J 29: 4118-4131.