Rad51 recombinase prevents Mre11 nuclease-dependent degradation and excessive PrimPol-mediated elongation of nascent DNA after UV irradiation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 48, 2015, Pages E6624-E6633

  Vallerga, María Belén ^a   Mansilla, Sabrina F ^a   Federico, María Belén ^a   Bertolin, Agustina P ^a   Gottifredi, Vanesa ^a  

^a FUNDACIÓN INSTITUTO LELOIR   (Argentina)

Author keywords

DNA damage tolerance; DNA replication; Pol ; Pol ; PrimPol

Indexed keywords

DNA; MRE11 PROTEIN; RAD51 PROTEIN; DNA BINDING PROTEIN; DNA DIRECTED DNA POLYMERASE; DNA DIRECTED DNA POLYMERASE ETA; DNA PRIMASE; MRE11A PROTEIN, HUMAN; MULTIFUNCTIONAL ENZYME; POLK PROTEIN, HUMAN; PRIMPOL PROTEIN, HUMAN; RAD51 PROTEIN, HUMAN; SMALL INTERFERING RNA;

CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL DEATH; CONFERENCE PAPER; CONTROLLED STUDY; DNA DEGRADATION; DNA REPAIR; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; ULTRAVIOLET IRRADIATION; CELL CYCLE; CELL SURVIVAL; DISEASE COURSE; HELA CELL LINE; METABOLISM; PHYSIOLOGY; RADIATION RESPONSE; TUMOR CELL LINE; ULTRAVIOLET RADIATION;

CELL CYCLE; CELL DEATH; CELL LINE, TUMOR; CELL SURVIVAL; DISEASE PROGRESSION; DNA; DNA BREAKS, DOUBLE-STRANDED; DNA PRIMASE; DNA REPAIR; DNA REPLICATION; DNA-BINDING PROTEINS; DNA-DIRECTED DNA POLYMERASE; DOSE-RESPONSE RELATIONSHIP, RADIATION; HELA CELLS; HUMANS; MULTIFUNCTIONAL ENZYMES; RAD51 RECOMBINASE; RNA, SMALL INTERFERING; ULTRAVIOLET RAYS;

EID: 84948666162     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1508543112     Document Type: Article

References (65)

1. Jasin M, Rothstein R (2013) Repair of strand breaks by homologous recombination. Cold Spring Harb Perspect Biol 5(11):a012740.
2. Jones RM, Kotsantis P, Stewart GS, Groth P, Petermann E (2014) BRCA2 and RAD51 promote double-strand break formation and cell death in response to gemcitabine. Mol Cancer Ther 13(10):2412-2421.
3. Alabert C, et al. (2014) Nascent chromatin capture proteomics determines chromatin dynamics during DNA replication and identifies unknown fork components. Nat Cell Biol 16(3):281-293.
4. Hashimoto Y, Ray Chaudhuri A, Lopes M, Costanzo V (2010) Rad51 protects nascent DNA from Mre11-dependent degradation and promotes continuous DNA synthesis. Nat Struct Mol Biol 17(11):1305-1311.
5. Petermann E, Orta ML, Issaeva N, Schultz N, Helleday T (2010) Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51- mediated pathways for restart and repair. Mol Cell 37(4):492-502.
6. Schlacher K, et al. (2011) Double-strand break repair-independent role for BRCA2 in blocking stalled replication fork degradation by MRE11. Cell 145(4):529-542.
7. Schlacher K, Wu H, Jasin M (2012) A distinct replication fork protection pathway connects Fanconi anemia tumor suppressors to RAD51-BRCA1/2. Cancer Cell 22(1): 106-116.
8. Ying S, Hamdy FC, Helleday T (2012) Mre11-dependent degradation of stalled DNA replication forks is prevented by BRCA2 and PARP1. Cancer Res 72(11): 2814-2821.
9. Chaudhury I, Sareen A, Raghunandan M, Sobeck A (2013) FANCD2 regulates BLM complex functions independently of FANCI to promote replication fork recovery. Nucleic Acids Res 41(13):6444-6459.
10. Chaudhury I, Stroik DR, Sobeck A (2014) FANCD2-controlled chromatin access of the Fanconi-associated nuclease FAN1 is crucial for the recovery of stalled replication forks. Mol Cell Biol 34(21):3939-3954.
11. Raghunandan M, Chaudhury I, Kelich SL, Hanenberg H, Sobeck A (2015) FANCD2, FANCJ and BRCA2 cooperate to promote replication fork recovery independently of the Fanconi Anemia core complex. Cell Cycle 14(3):342-353.
12. Yeo JE, Lee EH, Hendrickson EA, Sobeck A (2014) CtIP mediates replication fork recovery in a FANCD2-regulated manner. Hum Mol Genet 23(14):3695-3705.
13. Su F, et al. (2014) Nonenzymatic role for WRN in preserving nascent DNA strands after replication stress. Cell Reports 9(4):1387-1401.
14. Pathania S, et al. (2014) BRCA1 haploinsufficiency for replication stress suppression in primary cells. Nat Commun 5:5496.
15. Thangavel S, et al. (2015) DNA2 drives processing and restart of reversed replication forks in human cells. J Cell Biol 208(5):545-562.
16. Bryant HE, et al. (2009) PARP is activated at stalled forks to mediate Mre11-dependent replication restart and recombination. EMBO J 28(17):2601-2615.
17. Ciccia A, et al. (2009) The SIOD disorder protein SMARCAL1 is an RPA-interacting protein involved in replication fork restart. Genes Dev 23(20):2415-2425.
18. Hanada K, et al. (2007) The structure-specific endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nat Struct Mol Biol 14(11):1096-1104.
19. Yang YG, Cortes U, Patnaik S, Jasin M, Wang ZQ (2004) Ablation of PARP-1 does not interfere with the repair of DNA double-strand breaks, but compromises the reactivation of stalled replication forks. Oncogene 23(21):3872-3882.
20. Davies SL, North PS, Hickson ID (2007) Role for BLM in replication-fork restart and suppression of origin firing after replicative stress. Nat Struct Mol Biol 14(7): 677-679.
21. Zellweger R, et al. (2015) Rad51-mediated replication fork reversal is a global response to genotoxic treatments in human cells. J Cell Biol 208(5):563-579.
22. Elvers I, Johansson F, Groth P, Erixon K, Helleday T (2011) UV stalled replication forks restart by re-priming in human fibroblasts. Nucleic Acids Res 39(16):7049-7057.
23. Rastogi RP, Richa, Kumar A, Tyagi MB, Sinha RP (2010) Molecular mechanisms of ultraviolet radiation-induced DNA damage and repair. J Nucleic Acids 2010:592980.
24. Jansen JG, Tsaalbi-Shtylik A, de Wind N (2015) Roles of mutagenic translesion synthesis in mammalian genome stability, health and disease. DNA Repair (Amst) 29: 56-64.
25. Scully R, et al. (1997) Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell 90(3):425-435.
26. Eppink B, et al. (2011) The response of mammalian cells to UV-light reveals Rad54- dependent and independent pathways of homologous recombination. DNA Repair (Amst) 10(11):1095-1105.
27. Jackson DA, Pombo A (1998) Replicon clusters are stable units of chromosome structure: Evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells. J Cell Biol 140(6):1285-1295.
28. Yoon SW, Kim DK, Kim KP, Park KS (2014) Rad51 regulates cell cycle progression by preserving G2/M transition in mouse embryonic stem cells. Stem Cells Dev 23(22): 2700-2711.
29. Hashimoto Y, Puddu F, Costanzo V (2012) RAD51- and MRE11-dependent reassembly of uncoupled CMG helicase complex at collapsed replication forks. Nat Struct Mol Biol 19(1):17-24.
30. Daboussi F, et al. (2008) A homologous recombination defect affects replication-fork progression in mammalian cells. J Cell Sci 121(Pt 2):162-166.
31. Wilhelm T, et al. (2014) Spontaneous slow replication fork progression elicits mitosis alterations in homologous recombination-deficient mammalian cells. Proc Natl Acad Sci USA 111(2):763-768.
32. Courbet S, et al. (2008) Replication fork movement sets chromatin loop size and origin choice in mammalian cells. Nature 455(7212):557-560.
33. Quinet A, et al. (2014) Gap-filling and bypass at the replication fork are both active mechanisms for tolerance of low-dose ultraviolet-induced DNA damage in the human genome. DNA Repair (Amst) 14:27-38.
34. Edmunds CE, Simpson LJ, Sale JE (2008) PCNA ubiquitination and REV1 define temporally distinct mechanisms for controlling translesion synthesis in the avian cell line DT40. Mol Cell 30(4):519-529.
35. Hendel A, Ziv O, Gueranger Q, Geacintov N, Livneh Z (2008) Reduced efficiency and increased mutagenicity of translesion DNA synthesis across a TT cyclobutane pyrimidine dimer, but not a TT 6-4 photoproduct, in human cells lacking DNA polymerase eta. DNA Repair (Amst) 7(10):1636-1646.
36. Adar S, Izhar L, Hendel A, Geacintov N, Livneh Z (2009) Repair of gaps opposite lesions by homologous recombination in mammalian cells. Nucleic Acids Res 37(17):5737-5748.
37. González-Prieto R, Muñoz-Cabello AM, Cabello-Lobato MJ, Prado F (2013) Rad51 replication fork recruitment is required for DNA damage tolerance. EMBO J 32(9): 1307-1321.
38. Sturzenegger A, et al. (2014) DNA2 cooperates with the WRN and BLM RecQ helicases to mediate long-range DNA end resection in human cells. J Biol Chem 289(39): 27314-27326.
39. Shibata A, et al. (2014) DNA double-strand break repair pathway choice is directed by distinct MRE11 nuclease activities. Mol Cell 53(1):7-18.
40. Lafrance-Vanasse J, Williams GJ, Tainer JA (2015) Envisioning the dynamics and flexibility of Mre11-Rad50-Nbs1 complex to decipher its roles in DNA replication and repair. Prog Biophys Mol Biol 117(2-3):182-193.
41. Bétous R, et al. (2013) DNA polymerase κ-dependent DNA synthesis at stalled replication forks is important for CHK1 activation. EMBO J 32(15):2172-2185.
42. Bianchi J, et al. (2013) PrimPol bypasses UV photoproducts during eukaryotic chromosomal DNA replication. Mol Cell 52(4):566-573.
43. García-Gómez S, et al. (2013) PrimPol, an archaic primase/polymerase operating in human cells. Mol Cell 52(4):541-553.
44. Mourón S, et al. (2013) Repriming of DNA synthesis at stalled replication forks by human PrimPol. Nat Struct Mol Biol 20(12):1383-1389.
45. Sonoda E, et al. (1998) Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J 17(2):598-608.
46. Lopes M, Foiani M, Sogo JM (2006) Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions. Mol Cell 21(1):15-27.
47. Courcelle J, Hanawalt PC (2001) Participation of recombination proteins in rescue of arrested replication forks in UV-irradiated Escherichia coli need not involve recombination. Proc Natl Acad Sci USA 98(15):8196-8202.
48. Courcelle J, Hanawalt PC (2003) RecA-dependent recovery of arrested DNA replication forks. Annu Rev Genet 37:611-646.
49. Costanzo V (2011) Brca2, Rad51 and Mre11: Performing balancing acts on replication forks. DNA Repair (Amst) 10(10):1060-1065.
50. Bentsen IB, et al. (2013) MRX protects fork integrity at protein-DNA barriers, and its absence causes checkpoint activation dependent on chromatin context. Nucleic Acids Res 41(5):3173-3189.
51. Martinez-Jimenez MI, et al. (2015) Alternative solutions and new scenarios for translesion DNA synthesis by human PrimPol. DNA Repair (Amst) 29:127-138.
52. Longerich S, San Filippo J, Liu D, Sung P (2009) FANCI binds branched DNA and is monoubiquitinated by UBE2T-FANCL. J Biol Chem 284(35):23182-23186.
53. Leonhardt H, et al. (2000) Dynamics of DNA replication factories in living cells. J Cell Biol 149(2):271-280.
54. Kannouche P, et al. (2001) Domain structure, localization, and function of DNA polymerase eta, defective in xeroderma pigmentosum variant cells. Genes Dev 15(2): 158-172.
55. Guo C, et al. (2003) Mouse Rev1 protein interacts with multiple DNA polymerases involved in translesion DNA synthesis. EMBO J 22(24):6621-6630.
56. Mansilla SF, et al. (2013) UV-triggered p21 degradation facilitates damaged-DNA replication and preserves genomic stability. Nucleic Acids Res 41(14):6942-6951.
57. Speroni J, Federico MB, Mansilla SF, Soria G, Gottifredi V (2012) Kinase-independent function of checkpoint kinase 1 (Chk1) in the replication of damaged DNA. Proc Natl Acad Sci USA 109(19):7344-7349.
58. Ribeyre C, et al. (2009) The yeast Pif1 helicase prevents genomic instability caused by G-quadruplex-forming CEB1 sequences in vivo. PLoS Genet 5(5):e1000475.
59. Hicks JK, et al. (2010) Differential roles for DNA polymerases eta, zeta, and REV1 in lesion bypass of intrastrand versus interstrand DNA cross-links. Mol Cell Biol 30(5): 1217-1230.
60. Ito M, et al. (2005) Rad51 siRNA delivered by HVJ envelope vector enhances the anticancer effect of cisplatin. J Gene Med 7(8):1044-1052.
61. Rass E, et al. (2009) Role of Mre11 in chromosomal nonhomologous end joining in mammalian cells. Nat Struct Mol Biol 16(8):819-824.
62. Jones MJ, Colnaghi L, Huang TT (2012) Dysregulation of DNA polymerase κ recruitment to replication forks results in genomic instability. EMBO J 31(4):908-918.
63. Green CM, Almouzni G (2003) Local action of the chromatin assembly factor CAF-1 at sites of nucleotide excision repair in vivo. EMBO J 22(19):5163-5174.
64. Gueranger Q, et al. (2008) Role of DNA polymerases eta, iota and zeta in UV resistance and UV-induced mutagenesis in a human cell line. DNA Repair (Amst) 7(9): 1551-1562.
65. Neelsen KJ, Zanini IM, Herrador R, Lopes M (2013) Oncogenes induce genotoxic stress by mitotic processing of unusual replication intermediates. J Cell Biol 200(6):699-708.