Spatiotemporal dynamics of regulatory protein recruitment at DNA damage sites

Journal of Cellular Biochemistry

Volumn 104, Issue 5, 2008, Pages 1562-1569

  Mortusewicz, Oliver ^a,b   Leonhardt, Heinrich ^a,b   Cardoso, M Cristina ^c  

^a Munich Center for Integrated Protein Science   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

DNA damage; DNA repair; Loading platforms; Microirradiation; PCNA; XRCC1

Indexed keywords

CYCLINE; DNA METHYLTRANSFERASE 1; XRCC1 PROTEIN;

CELL DEATH; CELL METABOLISM; CELL TRANSFORMATION; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; EXCISION REPAIR; HUMAN; IRRADIATION; MAMMAL CELL; MOLECULAR SENSOR; PRIORITY JOURNAL; REGULATORY SEQUENCE; REVIEW;

ANIMALS; CELL SURVIVAL; DNA DAMAGE; DNA REPAIR; NUCLEAR PROTEINS; TIME FACTORS;

MAMMALIA;

EID: 50249173882     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21751     Document Type: Review

References (51)

1. Aten JA, Stap J, Krawczyk PM, van Oven CH, Hoebe RA, Essers J, Kanaar R. 2004. Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science 303:92-95.
2. Bakkenist CJ, Kastan MB. 2003. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421:499-506.
3. Bennett EJ, Harper JW. 2008. DNA damage: Ubiquitin marks the spot. Nat Struct Mol Biol 15:20-22.
4. Caldecott KW. 2003. XRCC1 and DNA strand break repair. DNA Repair (Amst) 2:955-969.
5. 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.
6. Chuang LS, Ian HI, Koh TW, Ng HH, Xu G, Li BF. 1997. Human DNA-(cytosine-5) methyltransferase-PCNA complex as a target for p21W AF1. Science 277:1996-2000.
7. Dorazi R, Parker JL, White MF. 2006. PCNA activates the Holliday junction endonuclease Hjc. J Mol Biol 364:243-247.
8. Essers J, Houtsmuller AB, van Veelen L, Paulusma C, Nigg AL, Pastink A, Vermeulen W, Hoeijmakers JH, Kanaar R. 2002. Nuclear dynamics of RAD52 group homologous recombination proteins in response to DNA damage. EMBO J 21:2030-2037.
9. Essers J, Theil AF, Baldeyron C, van Cappellen WA, Houtsmuller AB, Kanaar R, Vermeulen W. 2005. Nuclear dynamics of PCNA in DNA replication and repair. Mol Cell Biol 25:9350-9359.
10. Fan J, Otterlei M, Wong HK, Tomkinson AE, Wilson DM III. 2004. XRCC1 co-localizes and physically interacts with PCNA. Nucleic Acids Res 32:2193-2201.
11. Friedberg EC. 2003. DNA damage and repair. Nature 421: 436-440.
12. Gary R, Kim K, Cornelius HL, Park MS, Matsumoto Y. 1999. Proliferating cell nuclear antigen facilitates excision in long-patch base excision repair. J Biol Chem 274: 4354-4363.
13. Harper JW, Elledge SJ. 2007. The DNA damage response: Ten years after. Mol Cell 28:739-745.
14. Hashiguchi K, Matsumoto Y, Yasui A. 2007. Recruitment of DNA repair synthesis machinery to sites of DNA damage/ repair in living human cells. Nucleic Acids Res 35:2913-2923.
15. Hauptner A, Krucken R, Greubel C, Hable V, Dollinger G, Drexler GA, Deutsch M, Lowe R, Friedl AA, Dietzel S, Strickfaden H, Cremer T. 2006. DNA-repair protein distribution along the tracks of energetic ions. Radiat Prot Dosim 122:147-149.
16. Hoege C, Pfander B, Moldovan GL, Pyrowolakis G, Jentsch S. 2002. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419:135-141.
17. Hoeijmakers JH. 2001. Genome maintenance mechanisms for preventing cancer. Nature 411:366-374.
18. Holmes AM, Haber JE. 1999. Double-strand break repair in yeast requires both leading and lagging strand DNA polymerases. Cell 96:415-424.
19. Houtsmuller AB, Rademakers S, Nigg AL, Hoogstraten D, Hoeijmakers JH, Vermeulen W. 1999. Action of DNA repair endonuclease ERCC1/XPF in living cells. Science 284:958-961.
20. Jakob B, Scholz M, Taucher-Scholz G. 2003. Biological imaging of heavy charged-particle tracks. Radiat Res 159:676-684.
21. Jasin M. 1996. Genetic manipulation of genomes with rare-cutting endonucleases. Trends Genet 12:224-228.
22. Jiricny J. 2006. The multifaceted mismatch-repair system. Nat Rev Mol Cell Biol 7:335-346.
23. Johnson RE, Kovvali GK, Guzder SN, Amin NS, Holm C, Habraken Y, Sung P, Prakash L, Prakash S. 1996. Evidence for involvement of yeast proliferating cell nuclear antigen in DNA mismatch repair. J Biol Chem 271:27987-27990.
24. Kim JS, Krasieva TB, LaMorte V, Taylor AM, Yokomori K. 2002. Specific recruitment of human cohesin to laser-induced DNA damage. J Biol Chem 277:45149-45153.
25. 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.
26. 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.
27. Levin DS, McKenna AE, Motycka TA, Matsumoto Y, Tomkinson AE. 2000. Interaction between PCNA and DNA ligase I is critical for joining of Okazaki fragments and long-patch base-excision repair. Curr Biol 10:919-922.
28. Lisby M, Mortensen UH, Rothstein R. 2003. Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat Cell Biol 5:572-577.
29. Lukas C, Bartek J, Lukas J. 2005. Imaging of protein movement induced by chromosomal breakage: Tiny 'local' lesions pose great 'global' challenges. Chromosoma 114: 146-154.
30. Maga G, Hubscher U. 2003. Proliferating cell nuclear antigen (PCNA): A dancer with many partners. J Cell Sci 116:3051-3060.
31. 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.
32. Matsuoka S, Ballif BA, Smogorzewska A, McDonald ER III, Hurov KE, Luo J, Bakalarski CE, Zhao Z, Solimini N, Lerenthal Y, Shiloh Y, Gygi SP, Elledge SJ. 2007. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316:1160-1166.
33. Matunis MJ. 2002. On the road to repair: PCNA encounters SUMO and ubiquitin modifications. Mol Cell 10:441-442.
34. Melo JA, Cohen J, Toczyski DP. 2001. Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. Genes Dev 15:2809-2821.
35. Moggs JG, Grandi P, Quivy JP, Jonsson ZO, Hubscher U, Becker PB, Almouzni G. 2000. A CAF-1-PCNA-mediated chromatin assembly pathway triggered by sensing DNA damage. Mol Cell Biol 20:1206-1218.
36. Moldovan GL, Pfander B, Jentsch S. 2007. PCNA, the maestro of the replication fork. Cell 129:665-679.
37. 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.
38. Mortusewicz O, Schermelleh L, Walter J, Cardoso MC, Leonhardt H. 2005. Recruitment of DNA methyltransfer-ase I to DNA repair sites. Proc Natl Acad Sci USA 102: 8905-8909.
39. Mortusewicz O, Rothbauer U, Cardoso MC, Leonhardt H. 2006. Differential recruitment of DNA Ligase I and III to DNA repair sites. Nucleic Acids Res 34:3523-3532.
40. Pfander B, Moldovan GL, Sacher M, Hoege C, Jentsch S. 2005. SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 436:428-433.
41. Politi A, Mone MJ, Houtsmuller AB, Hoogstraten D, Vermeulen W, Heinrich R, van Driel R. 2005. Mathematical modeling of nucleotide excision repair reveals efficiency of sequential assembly strategies. Mol Cell 19: 679-690.
42. 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 XR CC1. J Biol Chem 277:23028-23036.
43. Shivji KK, Kenny MK, Wood RD. 1992. Proliferating cell nuclear antigen is required for DNA excision repair. Cell 69:367-374.
44. Solomon DA, Cardoso MC, Knudsen ES. 2004. Dynamic targeting of the replication machinery to sites of DNA damage. J Cell Biol 166:455-463.
45. Soutoglou E, Dorn JF, Sengupta K, Jasin M, Nussenzweig A, Ried T, Danuser G, Misteli T. 2007. Positional stability of single double-strand breaks in mammalian cells. Nat Cell Biol 9:675-682.
46. Sporbert A, Gahl A, Ankerhold R, Leonhardt H, Cardoso MC. 2002. DNA polymerase clamp shows little turnover at established replication sites but sequential de novo assembly at adjacent origin clusters. Mol Cell 10:1355-1365.
47. Sporbert A, Domaing P, Leonhardt H, Cardoso MC. 2005. PCNA acts as a stationary loading platform for transiently interacting Okazaki fragment maturation proteins. Nucleic Acids Res 33:3521-3528.
48. Thompson LH, Brookman KW, Dillehay LE, Carrano AV, Mazrimas JA, Mooney CL, Minkler JL. 1982. A CHO-cell strain having hypersensitivity to mutagens, a defect in DNA strand-break repair, and an extraordinary baseline frequency of sister-chromatid exchange. Mutat Res 95: 427-440.
49. Umar A, Buermeyer AB, Simon JA, Thomas DC, Clark AB, Liskay RM, Kunkel TA. 1996. Requirement for PCNA in DNA mismatch repair at a step preceding DNA resyn-thesis. Cell 87:65-73.
50. Warbrick E. 2000. The puzzle of PCNA's many partners. Bioessays 22:997-1006.
51. Wei YF, Robins P, Carter K, Caldecott K, Pappin DJ, Yu GL, Wang RP, Shell BK, Nash RA, Schar P., et al. 1995. Molecular cloning and expression of human cDNAs encoding a novel DNA ligase IV and DNA ligase III, an enzyme active in DNA repair and recombination. Mol Cell Biol 15:3206-3216.