Interaction with OGG1 is required for efficient recruitment of XRCC1 to base excision repair and maintenance of genetic stability after exposure to oxidative stress

Molecular and Cellular Biology

Volumn 35, Issue 9, 2015, Pages 1648-1658

  Campalans, Anna ^a,b,c,d   Moritz, Eva ^e   Kortulewski, Thierry ^a,b,c,d   Biard, Denis ^f   Epe, Bernd ^e   Radicellaa, J Pablo ^a,b,c,d  

^a INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^b INSERM   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d UNIVERSITÉ PARIS SACLAY   (France)

^e JOHANNES GUTENBERG UNIVERSITY   (Germany)

^f CEA DSV iMETI SEPIA   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DNA GLYCOSYLTRANSFERASE; OGG1 PROTEIN; UNCLASSIFIED DRUG; XRCC1 PROTEIN; DNA BINDING PROTEIN; OXOGUANINE GLYCOSYLASE 1, HUMAN; X-RAY REPAIR CROSS COMPLEMENTING PROTEIN 1;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EXCISION REPAIR; FEMALE; GENETIC STABILITY; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; MICRONUCLEUS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN POLYMORPHISM; PROTEIN PROTEIN INTERACTION; ANIMAL; CELL LINE; CHO CELL LINE; CRICETULUS; DNA REPAIR; GENE DELETION; GENETICS; METABOLISM; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; CELL LINE; CHO CELLS; CRICETULUS; DNA GLYCOSYLASES; DNA REPAIR; DNA-BINDING PROTEINS; GENE DELETION; HUMANS; OXIDATIVE STRESS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN INTERACTION MAPS;

EID: 84929152639     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00134-15     Document Type: Article

References (57)

1. Cadet J, Delatour T, Douki T, Gasparutto D, Pouget JP, Ravanat JL, Sauvaigo S. 1999. Hydroxyl radicals and DNA base damage. Mutat Res 424:9-21. http://dx.doi.org/10.1016/S0027-5107(99)00004-4.
2. Radicella JP, Dherin C, Desmaze C, Fox MS, Boiteux S. 1997. Cloning and characterization of hOGG1, a human homolog of the OGG1 gene of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 94:8010-8015. http://dx.doi.org/10.1073/pnas.94.15.8010.
3. Barnes DE, Lindahl T. 2004. Repair and genetic consequences of endogenous DNA base damage in mammalian cells. Annu Rev Genet 38:445-476. http://dx.doi.org/10.1146/annurev.genet.38.072902.092448.
4. Tebbs RS, Flannery ML, Meneses JJ, Hartmann A, Tucker JD, Thomp-son LH, Cleaver JE, Pedersen RA. 1999. Requirement for the Xrcc1 DNA base excision repair gene during early mouse development. Dev Biol 208: 513-529. http://dx.doi.org/10.1006/dbio.1999.9232.
5. Caldecott KW. 2003. XRCC1 and DNA strand break repair. DNA Repair (Amst) 2:955-969. http://dx.doi.org/10.1016/S1568-7864(03)00118-6.
6. 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 theDNAglycosylase hOGG1. J Biol Chem 278:44068-44074. http://dx.doi.org/10.1074/jbc. M306160200.
7. Caldecott KW. 2003. Protein-protein interactions during mammalian DNA single-strand break repair. Biochem Soc Trans 31:247-251.
8. Nazarkina ZK, Khodyreva SN, Marsin S, Lavrik OI, Radicella JP. 2007. XRCC1 interactions with base excision repair DNA intermediates. DNA Repair (Amst) 6:254-264. http://dx.doi.org/10.1016/j.dnarep.2006.10.002.
9. Wilson SH, Kunkel TA. 2000. Passing the baton in base excision repair. Nat Struct Biol 7:176-178. http://dx.doi.org/10.1038/73260.
10. Marintchev A, Robertson A, Dimitriadis EK, Prasad R, Wilson SH, Mullen GP. 2000. Domain specific interaction in the XRCC1-DNA polymerase beta complex. Nucleic Acids Res 28:2049-2059. http://dx.doi.org/10.1093/nar/28.10.2049.
11. 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. http://dx.doi.org/10.1093/nar/24.22.4387.
12. Kubota Y, Nash RA, Klungland A, Schar P, Barnes DE, Lindahl T. 1996. Reconstitution of DNA base excision-repair with purified human proteins: interaction between DNA polymerase beta and the XRCC1 protein. EMBO J 15:6662-6670.
13. Masson M, Niedergang C, Schreiber V, Muller S, Menissier-De Murcia J, De Murcia G. 1998. XRCC1 is specifically associated with poly(ADPribose) polymerase and negatively regulates its activity following DNA damage. Mol Cell Biol 18:3563-3571.
14. Nash RA, Caldecott KW, Barnes DE, Lindahl T. 1997. XRCC1 protein interacts with one of two distinct forms of DNA ligase III. Biochemistry 36:5207-5211. http://dx.doi.org/10.1021/bi962281m.
15. Taylor RM, Wickstead B, Cronin S, Caldecott KW. 1998. Role of a BRCT domain in the interaction of DNA ligase III-alpha with the DNA repair protein XRCC1. Curr Biol 8:877-880. http://dx.doi.org/10.1016/S0960-9822(07)00350-8.
16. El-Khamisy SF, Masutani M, Suzuki H, Caldecott KW. 2003. A requirement for PARP-1 for the assembly or stability of XRCC1 nuclear foci at sites of oxidative DNA damage. Nucleic Acids Res 31:5526-5533. http://dx.doi.org/10.1093/nar/gkg761.
17. Okano S, Lan L, Caldecott KW, Mori T, Yasui A. 2003. Spatial and temporal cellular responses to single-strand breaks in human cells. Mol Cell Biol 23:3974-3981. http://dx.doi.org/10.1128/MCB.23.11.3974-3981.2003.
18. Campalans A, Kortulewski T, Amouroux R, Menoni H, Vermeulen W, Radicella JP. 2013. Distinct spatiotemporal patterns and PARP dependence of XRCC1 recruitment to single-strand break and base excision repair. Nucleic Acids Res 41:3115-3129. http://dx.doi.org/10.1093/nar/gkt025.
19. 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 U S A 101:13738-13743. http://dx.doi.org/10.1073/pnas.0406048101.
20. Dianova II, Sleeth KM, Allinson SL, Parsons JL, Breslin C, Caldecott KW, Dianov GL. 2004. XRCC1-DNA polymerase beta interaction is required for efficient base excision repair. Nucleic Acids Res 32:2550-2555. http://dx.doi.org/10.1093/nar/gkh567.
21. Campalans A, Marsin S, Nakabeppu Y, O'Connor RT, 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. http://dx.doi.org/10.1016/j.dnarep.2005.04.014.
22. Vidal AE, Boiteux S, Hickson ID, Radicella JP. 2001. XRCC1 coordinates the initial and late stages of DNA abasic site repair through proteinprotein interactions. EMBO J 20:6530-6539. http://dx.doi.org/10.1093/emboj/20.22.6530.
23. Hanssen-Bauer A, Solvang-Garten K, Sundheim O, Pena-Diaz J, Andersen S, Slupphaug G, Krokan HE, Wilson DM, III, Akbari M, Otterlei M. 2011. XRCC1 coordinates disparate responses and multiprotein repair complexes depending on the nature and context of the DNA damage. Environ Mol Mutagen 52:623-635. http://dx.doi.org/10.1002/em.20663.
24. Strom CE, Johansson F, Uhlen M, Szigyarto CA, 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. http://dx.doi.org/10.1093/nar/gkq1241.
25. Goode EL, Ulrich CM, Potter JD. 2002. Polymorphisms in DNA repair genes and associations with cancer risk. Cancer Epidemiol Biomarkers Prev 11:1513-1530.
26. Ladiges W, Wiley J, MacAuley A. 2003. Polymorphisms in the DNA repair gene XRCC1 and age-related disease. Mech Ageing Dev 124:27-32. http://dx.doi.org/10.1016/S0047-6374(02)00166-5.
27. Berquist BR, Singh DK, Fan J, Kim D, Gillenwater E, Kulkarni A, Bohr VA, Ackerman EJ, Tomkinson AE, Wilson DM, III. 2010. Functional capacity of XRCC1 protein variants identified in DNA repair-deficient Chinese hamster ovary cell lines and the human population. Nucleic Acids Res 38:5023-5035. http://dx.doi.org/10.1093/nar/gkq193.
28. Amouroux R, Campalans A, Epe B, Radicella JP. 2010. Oxidative stress triggers the preferential assembly of base excision repair complexes on open chromatin regions. Nucleic Acids Res 38:2878-2890. http://dx.doi.org/10.1093/nar/gkp1247.
29. Campalans A, Amouroux R, Bravard A, Epe B, Radicella JP. 2007. UVA irradiation induces relocalisation of the DNA repair protein hOGG1 to nuclear speckles. J Cell Sci 120:23-32. http://dx.doi.org/10.1242/jcs.03312.
30. Biard DS, Despras E, Sarasin A, Angulo JF. 2005. Development of new EBV-based vectors for stable expression of small interfering RNA to mimick human syndromes: application to NER gene silencing. Mol Cancer Res 3:519-529. http://dx.doi.org/10.1158/1541-7786.MCR-05-0044.
31. Bolte S, Cordelieres FP. 2006. A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224:213-232. http://dx.doi.org/10.1111/j.1365-2818.2006.01706.x.
32. Pflaum M, Will O, Epe B. 1997. Determination of steady-state levels of oxidative DNA base modifications in mammalian cells by means of repair endonucleases. Carcinogenesis 18:2225-2231. http://dx.doi.org/10.1093/carcin/18.11.2225.
33. Kohn KW, Erickson LC, Ewig RA, Friedman CA. 1976. Fractionation of DNA from mammalian cells by alkaline elution. Biochemistry 15:4629-4637. http://dx.doi.org/10.1021/bi00666a013.
34. Sossou M, Flohr-Beckhaus C, Schulz I, Daboussi F, Epe B, Radicella JP. 2005. APE1 overexpression in XRCC1-deficient cells complements the defective repair of oxidative single strand breaks but increases genomic instability. Nucleic Acids Res 33:298-306. http://dx.doi.org/10.1093/nar/gki173.
35. Kowalczykowski SC. 2000. Some assembly required. Nat Struct Biol 7:1087-1089. http://dx.doi.org/10.1038/81923.
36. Volker M, Mone MJ, Karmakar P, van Hoffen A, Schul W, Vermeulen W, Hoeijmakers JH, van Driel R, van Zeeland AA, Mullenders LH. 2001. Sequential assembly of the nucleotide excision repair factors in vivo. Mol Cell 8:213-224. http://dx.doi.org/10.1016/S1097-2765(01)00281-7.
37. Thompson LH, West MG. 2000. XRCC1 keeps DNA from getting stranded. Mutat Res 459:1-18. http://dx.doi.org/10.1016/S0921-8777 (99)00058-0.
38. Takanami T, Nakamura J, Kubota Y, Horiuchi S. 2005. The Arg280His polymorphism in X-ray repair cross-complementing gene 1 impairs DNA repair ability. Mutat Res 582:135-145. http://dx.doi.org/10.1016/j.mrgentox.2005.01.007.
39. Iarmarcovai G, Bonassi S, Botta A, Baan RA, Orsiere T. 2008. Genetic polymorphisms and micronucleus formation: a review of the literature. Mutat Res 658:215-233. http://dx.doi.org/10.1016/j.mrrev.2007.10.001.
40. Brem R, Hall J. 2005. XRCC1 is required for DNA single-strand break repair in human cells. Nucleic Acids Res 33:2512-2520. http://dx.doi.org/10.1093/nar/gki543.
41. Fan J, Wilson PF, Wong HK, Urbin SS, Thompson LH, Wilson DM, III. 2007. XRCC1 down-regulation in human cells leads to DNA-damaging agent hypersensitivity, elevated sister chromatid exchange, and reduced survival of BRCA2 mutant cells. Environ Mol Mutagen 48:491-500. http://dx.doi.org/10.1002/em.20312.
42. Caldecott KW, Tucker JD, Stanker LH, Thompson LH. 1995. Characterization of the XRCC1-DNA ligase III complex in vitro and its absence from mutant hamster cells. Nucleic Acids Res 23:4836-4843. http://dx.doi.org/10.1093/nar/23.23.4836.
43. Taylor RM, Moore DJ, Whitehouse J, Johnson P, Caldecott KW. 2000. A cell cycle-specific requirement for the XRCC1 BRCT II domain during mammalianDNAstrand break repair. Mol Cell Biol 20:735-740. http://dx.doi.org/10.1128/MCB.20.2.735-740.2000.
44. Kim JS, Krasieva TB, Kurumizaka H, Chen DJ, Taylor AM, Yokomori K. 2005. Independent and sequential recruitment of NHEJ andHRfactors to DNA damage sites in mammalian cells. J Cell Biol 170:341-347. http://dx.doi.org/10.1083/jcb.200411083.
45. Nagy Z, Soutoglou E. 2009. DNA repair: easy to visualize, difficult to elucidate. Trends Cell Biol 19:617-629. http://dx.doi.org/10.1016/j.tcb.2009.08.010.
46. 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. http://dx.doi.org/10.1186/1471-2199-8-81.
47. Cappelli E, Degan P, Frosina G. 2000. Comparative repair of the endogenous lesions 8-oxo-7,8-dihydroguanine (8-oxoG), uracil and abasic site by mammalian cell extracts: 8-oxoG is poorly repaired by human cell extracts. Carcinogenesis 21:1135-1141. http://dx.doi.org/10.1093/carcin/21.6.1135.
48. Chou WC, Wang HC, Wong FH, Ding SL, Wu PE, Shieh SY, Shen CY. 2008. Chk2-dependent phosphorylation of XRCC1 in the DNA damage response promotes base excision repair. EMBO J 27:3140-3150. http://dx.doi.org/10.1038/emboj.2008.229.
49. Ensminger M, Iloff L, Ebel C, Nikolova T, Kaina B, Löbrich M. 2014. DNA breaks and chromosomal aberrations arise when replication meets base excision repair. J Cell Biol 206:29-43. http://dx.doi.org/10.1083/jcb.201312078.
50. Okano S, Kanno S, Nakajima S, Yasui A. 2000. Cellular responses and repair of single-strand breaks introduced by UV damage endonuclease in mammalian cells. J Biol Chem 275:32635-32641. http://dx.doi.org/10.1074/jbc. M004085200.
51. Cappelli E, Taylor R, Cevasco M, Abbondandolo A, Caldecott K, Frosina G. 1997. Involvement of XRCC1 and DNA ligase III gene products inDNAbase excision repair. J Biol Chem 272:23970-23975. http://dx.doi.org/10.1074/jbc.272.38.23970.
52. Caldecott KW, McKeown CK, Tucker JD, Ljungquist S, Thompson LH. 1994. An interaction between the mammalianDNArepair proteinXRCC1 and DNA ligase III. Mol Cell Biol 14:68-76.
53. Feng YZ, Liu YL, He XF, Wei W, Shen XL, Xie DL. 2014. Association between the XRCC1 Arg194Trp polymorphism and risk of cancer: evidence from 201 case-control studies. Tumour Biol 35:10677-10697. http://dx.doi.org/10.1007/s13277-014-2326-x.
54. Zhou X, Gu L, Zeng Y, Wei L, Ying M, Wang N, Su C, Wang Y, Liu C. 2014. The XRCC1 Arg194Trp and Arg280His polymorphisms in head and neck cancer susceptibility: a meta-analysis. Tumour Biol 35:10665-10676. http://dx.doi.org/10.1007/s13277-014-2247-8.
55. Jaruga P, Zastawny TH, Skokowski J, Dizdaroglu M, Olinski R. 1994. Oxidative DNA base damage and antioxidant enzyme activities in human lung cancer. FEBS Lett 341:59-64. http://dx.doi.org/10.1016/0014-5793(94)80240-8.
56. Olinski R, Zastawny T, Budzbon J, Skokowski J, Zegarski W, Dizdaroglu M. 1992. DNA base modifications in chromatin of human cancerous tissues. FEBS Lett 309:193-198. http://dx.doi.org/10.1016/0014-5793(92)81093-2.
57. Toyokuni S, Okamoto K, Yodoi J, Hiai H. 1995. Persistent oxidative stress in cancer. FEBS Lett 358:1-3. http://dx.doi.org/10.1016/0014-5793 (94)01368-B.