Distinct spatiotemporal patterns and PARP dependence of XRCC1 recruitment to single-strand break and base excision repair

Nucleic Acids Research

Volumn 41, Issue 5, 2013, Pages 3115-3129

  Campalans, Anna ^a   Kortulewski, Thierry ^a   Amouroux, Rachel ^a   Menoni, Hervé ^b   Vermeulen, Wim ^b   Radicella, J Pablo ^a  

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

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; SINGLE STRANDED DNA; XRCC1 PROTEIN;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELLULAR DISTRIBUTION; DNA DAMAGE; EMBRYO; ENZYME ACTIVITY; ENZYME KINETICS; EUCHROMATIN; EXCISION REPAIR; HETEROCHROMATIN; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN INDUCTION; PROTEIN LOCALIZATION; SINGLE STRANDED DNA BREAK;

ANIMALS; CELL LINE; CELL NUCLEUS; DNA BREAKS, SINGLE-STRANDED; DNA GLYCOSYLASES; DNA REPAIR; DNA-BINDING PROTEINS; EUCHROMATIN; HETEROCHROMATIN; HUMANS; MICE; OXIDATION-REDUCTION; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SINGLE-CELL ANALYSIS;

EID: 84876393023     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt025     Document Type: Article

References (56)

1. El-Khamisy, S.F., Masutani, M., Suzuki, H. and Caldecott, K.W. (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.
2. Okano, S., Lan, L., Caldecott, K.W., Mori, T. and Yasui, A. (2003) Spatial and temporal cellular responses to single-strand breaks in human cells. Mol. Cell. Biol., 23, 3974-3981.
3. Caldecott, K.W. (2003) XRCC1 and DNA strand break repair. DNA Repair, 2, 955-969.
4. Marsin, S., Vidal, A.E., Sossou, M., Menissier-de Murcia, J., Le Page, F., Boiteux, S., de Murcia, G. and Radicella, J.P. (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.
5. Tebbs, R.S., Flannery, M.L., Meneses, J.J., Hartmann, A., Tucker, J.D., Thompson, L.H., Cleaver, J.E. and Pedersen, R.A. (1999) Requirement for the Xrcc1 DNA base excision repair gene during early mouse development. Dev. Biol., 208, 513-529.
6. Wilson, S.H. and Kunkel, T.A. (2000) Passing the baton in base excision repair. Nat. Struct. Biol., 7, 176-178.
7. Caldecott, K.W. (2007) Mammalian single-strand break repair: mechanisms and links with chromatin. DNA Repair, 6, 443-453.
8. Campalans, A., Marsin, S., Nakabeppu, Y., O'Connor, T.R., Boiteux, S. and Radicella, J.P. (2005) XRCC1 interactions with multiple DNA glycosylases: a model for its recruitment to base excision repair. DNA Repair, 4, 826-835.
9. Vidal, A.E., Boiteux, S., Hickson, I.D. and Radicella, J.P. (2001) XRCC1 coordinates the initial and late stages of DNA abasic site repair through protein-protein interactions. EMBO J., 20, 6530-6539.
10. Bekker-Jensen, S. and Mailand, N. (2010) Assembly and function of DNA double-strand break repair foci in mammalian cells. DNA Repair, 9, 1219-1228.
11. Polo, S.E. and Jackson, S.P. (2011) Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev., 25, 409-433.
12. Vermeulen, W. (2011) Dynamics of mammalian NER proteins. DNA Repair, 10, 760-771.
13. Costes, S.V., Ponomarev, A., Chen, J.L., Nguyen, D., Cucinotta, F.A. and Barcellos-Hoff, M.H. (2007) Image-based modeling reveals dynamic redistribution of DNA damage into nuclear sub-domains. PLoS Comput. Biol., 3, e155.
14. Cowell, I.G., Sunter, N.J., Singh, P.B., Austin, C.A., Durkacz, B.W. and Tilby, M.J. (2007) gammaH2AX foci form preferentially in euchromatin after ionising-radiation. PLoS One, 2, e1057.
15. Goodarzi, A.A., Noon, A.T., Deckbar, D., Ziv, Y., Shiloh, Y., Lobrich, M. and Jeggo, P.A. (2008) ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol. Cell, 31, 167-177.
16. Goodarzi, A.A., Jeggo, P. and Lobrich, M. (2010) The influence of heterochromatin on DNA double strand break repair: Getting the strong, silent type to relax. DNA Repair, 9, 1273-1282.
17. Chiolo, I., Minoda, A., Colmenares, S.U., Polyzos, A., Costes, S.V. and Karpen, G.H. (2011) Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair. Cell, 144, 732-744.
18. Jakob, B., Splinter, J., Conrad, S., Voss, K.O., Zink, D., Durante, M., Lobrich, M. and Taucher-Scholz, G. (2011) DNA double-strand breaks in heterochromatin elicit fast repair protein recruitment, histone H2AX phosphorylation and relocation to euchromatin. Nucleic Acids Res., 39, 6489-6499.
19. Menoni, H., Gasparutto, D., Hamiche, A., Cadet, J., Dimitrov, S., Bouvet, P. and Angelov, D. (2007) ATP-dependent chromatin remodeling is required for base excision repair in conventional but not in variant H2A.Bbd nucleosomes. Mol. Cell. Biol., 27, 5949-5956.
20. Menoni, H., Shukla, M.S., Gerson, V., Dimitrov, S. and Angelov, D. (2012) Base excision repair of 8-oxoG in dinucleosomes. Nucleic Acids Res., 40, 692-700.
21. Amouroux, R., Campalans, A., Epe, B. and Radicella, J.P. (2010) Oxidative stress triggers the preferential assembly of base excision repair complexes on open chromatin regions. Nucleic Acids Res., 38, 2878-2890.
22. Bolte, S. and Cordelieres, F.P. (2006) A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc., 224, 213-232.
23. Costes, S.V., Daelemans, D., Cho, E.H., Dobbin, Z., Pavlakis, G. and Lockett, S. (2004) Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys. J., 86, 3993-4003.
24. Godon, C., Cordelieres, F.P., Biard, D., Giocanti, N., Megnin-Chanet, F., Hall, J. and 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.
25. Lan, L., Nakajima, S., Oohata, Y., Takao, M., Okano, S., Masutani, M., Wilson, S.H. and Yasui, A. (2004) In situ analysis of repair processes for oxidative DNA damage in mammalian cells. Proc. Natl Acad. Sci. USA, 101, 13738-13743.
26. Mortusewicz, O., Ame, J.C., Schreiber, V. and 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.
27. Hanssen-Bauer, A., Solvang-Garten, K., Sundheim, O., Pena-Diaz, J., Andersen, S., Slupphaug, G., Krokan, H.E., Wilson, D.M. 3rd, Akbari, M. and 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.
28. Lan, L., Nakajima, S., Komatsu, K., Nussenzweig, A., Shimamoto, A., Oshima, J. and Yasui, A. (2005) Accumulation of Werner protein at DNA double-strand breaks in human cells. J. Cell Sci., 118, 4153-4162.
29. Will, O., Gocke, E., Eckert, I., Schulz, I., Pflaum, M., Mahler, H.C. and Epe, B. (1999) Oxidative DNA damage and mutations induced by a polar photosensitizer, Ro19-8022. Mutat. Res., 435, 89-101.
30. Soriano, F.G., Virag, L. and Szabo, C. (2001) Diabetic endothelial dysfunction: role of reactive oxygen and nitrogen species production and poly(ADP-ribose) polymerase activation. J. Mol. Med., 79, 437-448.
31. Schreiber, V., Dantzer, F., Ame, J.C. and de Murcia, G. (2006) Poly(ADP-ribose): novel functions for an old molecule. Nat. Rev. Mol. Cell. Biol., 7, 517-528.
32. Yelamos, J., Farres, J., Llacuna, L., Ampurdanes, C. and Martin-Caballero, J. (2012) PARP-1 and PARP-2: new players in tumour development. Am. J. Cancer Res., 1, 328-346.
33. Strom, C.E., Johansson, F., Uhlen, M., Szigyarto, C.A., Erixon, K. and 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.
34. Masson, M., Niedergang, C., Schreiber, V., Muller, S., Menissier-de Murcia, J. and 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.
35. Ballmaier, D. and Epe, B. (2006) DNA damage by bromate: mechanism and consequences. Toxicology, 221, 166-171.
36. Houtsmuller, A.B. and Vermeulen, W. (2001) Macromolecular dynamics in living cell nuclei revealed by fluorescence redistribution after photobleaching. Histochem. Cell Biol., 115, 13-21.
37. Hollenbach, S., Dhenaut, A., Eckert, I., Radicella, J.P. and Epe, B. (1999) Overexpression of Ogg1 in mammalian cells: effects on induced and spontaneous oxidative DNA damage and mutagenesis. Carcinogenesis, 20, 1863-1868.
38. Parsons, J.L., Tait, P.S., Finch, D., Dianova, I.I., Allinson, S.L. and Dianov, G.L. (2008) CHIP-mediated degradation and DNA damage-dependent stabilization regulate base excision repair proteins. Mol. Cell, 29, 477-487.
39. Fan, J., Otterlei, M., Wong, H.K., Tomkinson, A.E. and Wilson, D.M. 3rd (2004) XRCC1 co-localizes and physically interacts with PCNA. Nucleic Acids Res., 32, 2193-2201.
40. Ohno, M., Miura, T., Furuichi, M., Tominaga, Y., Tsuchimoto, D., Sakumi, K. and Nakabeppu, Y. (2006) A genome-wide distribution of 8-oxoguanine correlates with the preferred regions for recombination and single nucleotide polymorphism in the human genome. Genome Res., 16, 567-575.
41. Caldecott, K.W. (2008) Single-strand break repair and genetic disease. Nat. Rev. Genet., 9, 619-631.
42. Noren Hooten, N., Kompaniez, K., Barnes, J., Lohani, A. and Evans, M.K. (2011) Poly(ADP-ribose) polymerase 1 (PARP-1) binds to 8-oxoguanine-DNA glycosylase (OGG1). J. Biol. Chem., 286, 44679-44690.
43. Vodenicharov, M.D., Sallmann, F.R., Satoh, M.S. and Poirier, G.G. (2000) Base excision repair is efficient in cells lacking poly(ADP-ribose) polymerase 1. Nucleic Acids Res., 28, 3887-3896.
44. Helleday, T. (2011) The underlying mechanism for the PARP and BRCA synthetic lethality: clearing up the misunderstandings. Mol. Oncol., 5, 387-393.
45. Chou, W.C., Wang, H.C., Wong, F.H., Ding, S.L., Wu, P.E., Shieh, S.Y. and Shen, C.Y. (2008) Chk2-dependent phosphorylation of XRCC1 in the DNA damage response promotes base excision repair. EMBO J., 27, 3140-3150.
46. Whitehouse, C.J., Taylor, R.M., Thistlethwaite, A., Zhang, H., Karimi-Busheri, F., Lasko, D.D., Weinfeld, M. and Caldecott, K.W. (2001) XRCC1 stimulates human polynucleotide kinase activity at damaged DNA termini and accelerates DNA single-strand break repair. Cell, 104, 107-117.
47. Kruhlak, M.J., Celeste, A., Dellaire, G., Fernandez-Capetillo, O., Muller, W.G., McNally, J.G., Bazett-Jones, D.P. and Nussenzweig, A. (2006) Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks. J. Cell Biol., 172, 823-834.
48. Kim, J.S., Krasieva, T.B., Kurumizaka, H., Chen, D.J., Taylor, A.M. and Yokomori, K. (2005) Independent and sequential recruitment of NHEJ and HR factors to DNA damage sites in mammalian cells. J. Cell Biol., 170, 341-347.
49. Nagy, Z. and Soutoglou, E. (2009) DNA repair: easy to visualize, difficult to elucidate. Trends Cell Biol., 19, 617-629.
50. Volker, M., Mone, M.J., Karmakar, P., van Hoffen, A., Schul, W., Vermeulen, W., Hoeijmakers, J.H., van Driel, R., van Zeeland, A.A. and Mullenders, L.H. (2001) Sequential assembly of the nucleotide excision repair factors in vivo. Mol. Cell, 8, 213-224.
51. Cappelli, E., Degan, P. and 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.
52. Dunn, A.R., Kad, N.M., Nelson, S.R., Warshaw, D.M. and Wallace, S.S. (2011) Single Qdot-labeled glycosylase molecules use a wedge amino acid to probe for lesions while scanning along DNA. Nucleic Acids Res., 39, 7487-7498.
53. Chen, L., Haushalter, K.A., Lieber, C.M. and Verdine, G.L. (2002) Direct visualization of a DNA glycosylase searching for damage. Chem. Biol., 9, 345-350.
54. Ljungman, M. and Hanawalt, P.C. (1992) Efficient protection against oxidative DNA damage in chromatin. Mol. Carcinog., 5, 264-269.
55. Neumaier, T., Swenson, J., Pham, C., Polyzos, A., Lo, A.T., Yang, P., Dyball, J., Asaithamby, A., Chen, D.J., Bissell, M.J. et al. (2012) Evidence for formation of DNA repair centers and dose-response nonlinearity in human cells. Proc. Natl Acad. Sci. USA, 109, 443-448.
56. Schuster-Bockler, B. and Lehner, B. (2012) Chromatin organization is a major influence on regional mutation rates in human cancer cells. Nature, 488, 504-507.