CtIP Is Required to Initiate Replication-Dependent Interstrand Crosslink Repair

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DNA interstrand crosslinks (ICLs) are toxic lesions that block the progression of replication and transcription. CtIP is a conserved DNA repair protein that facilitates DNA end resection in the double-strand break (DSB) repair pathway. Here we show that CtIP plays a critical role during initiation of ICL processing in replicating human cells that is distinct from its role in DSB repair. CtIP depletion sensitizes human cells to ICL inducing agents and significantly impairs the accumulation of DNA damage response proteins RPA, ATR, FANCD2, γH2AX, and phosphorylated ATM at sites of laser generated ICLs. In contrast, the appearance of γH2AX and phosphorylated ATM at sites of laser generated double strand breaks (DSBs) is CtIP-independent. We present a model in which CtIP functions early in ICL repair in a BRCA1– and FANCM–dependent manner prior to generation of DSB repair intermediates.

Vyšlo v časopise: CtIP Is Required to Initiate Replication-Dependent Interstrand Crosslink Repair. PLoS Genet 8(11): e32767. doi:10.1371/journal.pgen.1003050
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003050

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1. D'AndreaAD (2010) Susceptibility pathways in Fanconi's anemia and breast cancer. N Engl J Med 362: 1909–1919.

2. AndreassenPR, RenK (2009) Fanconi anemia proteins, DNA interstrand crosslink repair pathways, and cancer therapy. Curr Cancer Drug Targets 9: 101–117.

3. McVeyM (2010) Strategies for DNA interstrand crosslink repair: insights from worms, flies, frogs, and slime molds. Environ Mol Mutagen 51: 646–658.

4. AkkariYM, BatemanRL, ReifsteckCA, OlsonSB, GrompeM (2000) DNA replication is required To elicit cellular responses to psoralen-induced DNA interstrand cross-links. Mol Cell Biol 20: 8283–8289.

5. RothfussA, GrompeM (2004) Repair kinetics of genomic interstrand DNA cross-links: evidence for DNA double-strand break-dependent activation of the Fanconi anemia/BRCA pathway. Mol Cell Biol 24: 123–134.

6. SobeckA, StoneS, CostanzoV, de GraafB, ReuterT, et al. (2006) Fanconi anemia proteins are required to prevent accumulation of replication-associated DNA double-strand breaks. Mol Cell Biol 26: 425–437.

7. MladenovaV, RussevG (2006) Enhanced repair of DNA interstrand crosslinks in S phase. FEBS Lett 580: 1631–1634.

8. McHughPJ, SarkarS (2006) DNA interstrand cross-link repair in the cell cycle: a critical role for polymerase zeta in G1 phase. Cell Cycle 5: 1044–1047.

9. MuniandyPA, ThapaD, ThazhathveetilAK, LiuST, SeidmanMM (2009) Repair of laser-localized DNA interstrand cross-links in G1 phase mammalian cells. J Biol Chem 284: 27908–27917.

10. Ben-YehoyadaM, WangLC, KozekovID, RizzoCJ, GottesmanME, et al. (2009) Checkpoint signaling from a single DNA interstrand crosslink. Mol Cell 35: 704–715.

11. RaschleM, KnipscheerP, EnoiuM, AngelovT, SunJ, et al. (2008) Mechanism of replication-coupled DNA interstrand crosslink repair. Cell 134: 969–980.

12. CicciaA, LingC, CoulthardR, YanZ, XueY, et al. (2007) Identification of FAAP24, a Fanconi anemia core complex protein that interacts with FANCM. Mol Cell 25: 331–343.

13. GariK, DecailletC, DelannoyM, WuL, ConstantinouA (2008) Remodeling of DNA replication structures by the branch point translocase FANCM. Proc Natl Acad Sci U S A 105: 16107–16112.

14. DeansAJ, WestSC (2009) FANCM connects the genome instability disorders Bloom's Syndrome and Fanconi Anemia. Mol Cell 36: 943–953.

15. HuangM, KimJM, ShiotaniB, YangK, ZouL, et al. (2010) The FANCM/FAAP24 complex is required for the DNA interstrand crosslink-induced checkpoint response. Mol Cell 39: 259–268.

16. SchwabRA, BlackfordAN, NiedzwiedzW (2010) ATR activation and replication fork restart are defective in FANCM-deficient cells. EMBO J 29: 806–818.

17. SinghTR, SaroD, AliAM, ZhengXF, DuCH, et al. (2010) MHF1-MHF2, a histone-fold-containing protein complex, participates in the Fanconi anemia pathway via FANCM. Mol Cell 37: 879–886.

18. KnipscheerP, RaschleM, SmogorzewskaA, EnoiuM, HoTV, et al. (2009) The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair. Science 326: 1698–1701.

19. ZouL, ElledgeSJ (2003) Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300: 1542–1548.

20. AndreassenPR, D'AndreaAD, TaniguchiT (2004) ATR couples FANCD2 monoubiquitination to the DNA-damage response. Genes Dev 18: 1958–1963.

21. PichierriP, RosselliF (2004) The DNA crosslink-induced S-phase checkpoint depends on ATR-CHK1 and ATR-NBS1-FANCD2 pathways. EMBO J 23: 1178–1187.

22. ByunTS, PacekM, YeeMC, WalterJC, CimprichKA (2005) Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev 19: 1040–1052.

23. LongDT, RaschleM, JoukovV, WalterJC (2011) Mechanism of RAD51-dependent DNA interstrand cross-link repair. Science 333: 84–87.

24. HoGP, MargossianS, TaniguchiT, D'AndreaAD (2006) Phosphorylation of FANCD2 on two novel sites is required for mitomycin C resistance. Mol Cell Biol 26: 7005–7015.

25. IshiaiM, KitaoH, SmogorzewskaA, TomidaJ, KinomuraA, et al. (2008) FANCI phosphorylation functions as a molecular switch to turn on the Fanconi anemia pathway. Nat Struct Mol Biol 15: 1138–1146.

26. Garcia-HigueraI, TaniguchiT, GanesanS, MeynMS, TimmersC, et al. (2001) Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol Cell 7: 249–262.

27. SmogorzewskaA, MatsuokaS, VinciguerraP, McDonaldER3rd, HurovKE, et al. (2007) Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell 129: 289–301.

28. AlpiAF, PacePE, BabuMM, PatelKJ (2008) Mechanistic insight into site-restricted monoubiquitination of FANCD2 by Ube2t, FANCL, and FANCI. Mol Cell 32: 767–777.

29. NiedernhoferLJ, OdijkH, BudzowskaM, van DrunenE, MaasA, et al. (2004) The structure-specific endonuclease Ercc1-Xpf is required to resolve DNA interstrand cross-link-induced double-strand breaks. Mol Cell Biol 24: 5776–5787.

30. Al-MinawiAZ, LeeYF, HakanssonD, JohanssonF, LundinC, et al. (2009) The ERCC1/XPF endonuclease is required for completion of homologous recombination at DNA replication forks stalled by inter-strand cross-links. Nucleic Acids Res 37: 6400–6413.

31. BhagwatN, OlsenAL, WangAT, HanadaK, StuckertP, et al. (2009) XPF-ERCC1 participates in the Fanconi anemia pathway of cross-link repair. Mol Cell Biol 29: 6427–6437.

32. FekairiS, ScaglioneS, ChahwanC, TaylorER, TissierA, et al. (2009) Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell 138: 78–89.

33. CrossanGP, van der WeydenL, RosadoIV, LangevinF, GaillardPH, et al. (2011) Disruption of mouse Slx4, a regulator of structure-specific nucleases, phenocopies Fanconi anemia. Nat Genet

34. KimY, LachFP, DesettyR, HanenbergH, AuerbachAD, et al. (2011) Mutations of the SLX4 gene in Fanconi anemia. Nat Genet

35. StoepkerC, HainK, SchusterB, Hilhorst-HofsteeY, RooimansMA, et al. (2011) SLX4, a coordinator of structure-specific endonucleases, is mutated in a new Fanconi anemia subtype. Nat Genet

36. YamamotoKN, KobayashiS, TsudaM, KurumizakaH, TakataM, et al. (2011) Involvement of SLX4 in interstrand cross-link repair is regulated by the Fanconi anemia pathway. Proc Natl Acad Sci U S A 108: 6492–6496.

37. WangAT, SengerovaB, CattellE, InagawaT, HartleyJM, et al. (2011) Human SNM1A and XPF-ERCC1 collaborate to initiate DNA interstrand cross-link repair. Genes Dev 25: 1859–1870.

38. HazratiA, Ramis-CastelltortM, SarkarS, BarberLJ, SchofieldCJ, et al. (2008) Human SNM1A suppresses the DNA repair defects of yeast pso2 mutants. DNA Repair (Amst) 7: 230–238.

39. BaeJB, MukhopadhyaySS, LiuL, ZhangN, TanJ, et al. (2008) Snm1B/Apollo mediates replication fork collapse and S Phase checkpoint activation in response to DNA interstrand cross-links. Oncogene 27: 5045–5056.

40. HanadaK, BudzowskaM, ModestiM, MaasA, WymanC, et al. (2006) The structure-specific endonuclease Mus81-Eme1 promotes conversion of interstrand DNA crosslinks into double-strands breaks. EMBO J 25: 4921–4932.

41. CicciaA, McDonaldN, WestSC (2008) Structural and functional relationships of the XPF/MUS81 family of proteins. Annu Rev Biochem 77: 259–287.

42. DendougaN, GaoH, MoecharsD, JanicotM, VialardJ, et al. (2005) Disruption of murine Mus81 increases genomic instability and DNA damage sensitivity but does not promote tumorigenesis. Mol Cell Biol 25: 7569–7579.

43. TaylorER, McGowanCH (2008) Cleavage mechanism of human Mus81-Eme1 acting on Holliday-junction structures. Proc Natl Acad Sci U S A 105: 3757–3762.

44. KratzK, SchopfB, KadenS, SendoelA, EberhardR, et al. (2010) Deficiency of FANCD2-associated nuclease KIAA1018/FAN1 sensitizes cells to interstrand crosslinking agents. Cell 142: 77–88.

45. MacKayC, DeclaisAC, LundinC, AgostinhoA, DeansAJ, et al. (2010) Identification of KIAA1018/FAN1, a DNA repair nuclease recruited to DNA damage by monoubiquitinated FANCD2. Cell 142: 65–76.

46. SmogorzewskaA, DesettyR, SaitoTT, SchlabachM, LachFP, et al. (2010) A genetic screen identifies FAN1, a Fanconi anemia-associated nuclease necessary for DNA interstrand crosslink repair. Mol Cell 39: 36–47.

47. NiedzwiedzW, MosedaleG, JohnsonM, OngCY, PaceP, et al. (2004) The Fanconi anaemia gene FANCC promotes homologous recombination and error-prone DNA repair. Mol Cell 15: 607–620.

48. EdmundsCE, SimpsonLJ, SaleJE (2008) PCNA ubiquitination and REV1 define temporally distinct mechanisms for controlling translesion synthesis in the avian cell line DT40. Mol Cell 30: 519–529.

49. ZietlowL, SmithLA, BesshoM, BesshoT (2009) Evidence for the involvement of human DNA polymerase N in the repair of DNA interstrand cross-links. Biochemistry 48: 11817–11824.

50. BienkoM, GreenCM, SabbionedaS, CrosettoN, MaticI, et al. (2010) Regulation of translesion synthesis DNA polymerase eta by monoubiquitination. Mol Cell 37: 396–407.

51. CuiX, BrennemanM, MeyneJ, OshimuraM, GoodwinEH, et al. (1999) The XRCC2 and XRCC3 repair genes are required for chromosome stability in mammalian cells. Mutat Res 434: 75–88.

52. HowlettNG, TaniguchiT, OlsonS, CoxB, WaisfiszQ, et al. (2002) Biallelic inactivation of BRCA2 in Fanconi anemia. Science 297: 606–609.

53. LitmanR, PengM, JinZ, ZhangF, ZhangJ, et al. (2005) BACH1 is critical for homologous recombination and appears to be the Fanconi anemia gene product FANCJ. Cancer Cell 8: 255–265.

54. WuHI, BrownJA, DorieMJ, LazzeroniL, BrownJM (2004) Genome-wide identification of genes conferring resistance to the anticancer agents cisplatin, oxaliplatin, and mitomycin C. Cancer Res 64: 3940–3948.

55. UanschouC, SiwiecT, Pedrosa-HarandA, KerzendorferC, Sanchez-MoranE, et al. (2007) A novel plant gene essential for meiosis is related to the human CtIP and the yeast COM1/SAE2 gene. EMBO J 26: 5061–5070.

56. YuX, ChenJ (2004) DNA damage-induced cell cycle checkpoint control requires CtIP, a phosphorylation-dependent binding partner of BRCA1 C-terminal domains. Mol Cell Biol 24: 9478–9486.

57. LiuF, LeeWH (2006) CtIP activates its own and cyclin D1 promoters via the E2F/RB pathway during G1/S progression. Mol Cell Biol 26: 3124–3134.

58. LimboO, ChahwanC, YamadaY, de BruinRA, WittenbergC, et al. (2007) Ctp1 is a cell-cycle-regulated protein that functions with Mre11 complex to control double-strand break repair by homologous recombination. Mol Cell 28: 134–146.

59. SartoriAA, LukasC, CoatesJ, MistrikM, FuS, et al. (2007) Human CtIP promotes DNA end resection. Nature 450: 509–514.

60. ChenL, NieveraCJ, LeeAY, WuX (2008) Cell cycle-dependent complex formation of BRCA1.CtIP.MRN is important for DNA double-strand break repair. J Biol Chem 283: 7713–7720.

61. WilliamsRS, DodsonGE, LimboO, YamadaY, WilliamsJS, et al. (2009) Nbs1 flexibly tethers Ctp1 and Mre11-Rad50 to coordinate DNA double-strand break processing and repair. Cell 139: 87–99.

62. YouZ, ShiLZ, ZhuQ, WuP, ZhangYW, et al. (2009) CtIP links DNA double-strand break sensing to resection. Mol Cell 36: 954–969.

63. HuertasP, JacksonSP (2009) Human CtIP mediates cell cycle control of DNA end resection and double strand break repair. J Biol Chem 284: 9558–9565.

64. HearstJE (1981) Psoralen photochemistry and nucleic acid structure. J Invest Dermatol 77: 39–44.

65. KanneD, StraubK, RapoportH, HearstJE (1982) Psoralen-deoxyribonucleic acid photoreaction. Characterization of the monoaddition products from 8-methoxypsoralen and 4,5′8-trimethylpsoralen. Biochemistry 21: 861–871.

66. CleaverJE, GruenertDC (1984) Repair of psoralen adducts in human DNA: differences among xeroderma pigmentosum complementation groups. J Invest Dermatol 82: 311–315.

67. YanZ, DelannoyM, LingC, DaeeD, OsmanF, et al. (2010) A histone-fold complex and FANCM form a conserved DNA-remodeling complex to maintain genome stability. Mol Cell 37: 865–878.

68. KongX, MohantySK, StephensJ, HealeJT, Gomez-GodinezV, et al. (2009) Comparative analysis of different laser systems to study cellular responses to DNA damage in mammalian cells. Nucleic Acids Res 37: e68.

69. BostockCJ, PrescottDM, KirkpatrickJB (1971) An evaluation of the double thymidine block for synchronizing mammalian cells at the G1-S border. Exp Cell Res 68: 163–168.

70. ChenPL, LiuF, CaiS, LinX, LiA, et al. (2005) Inactivation of CtIP leads to early embryonic lethality mediated by G1 restraint and to tumorigenesis by haploid insufficiency. Mol Cell Biol 25: 3535–3542.

71. FisherLA, BesshoM, BesshoT (2008) Processing of a psoralen DNA interstrand cross-link by XPF-ERCC1 complex in vitro. J Biol Chem 283: 1275–1281.

72. BakkenistCJ, KastanMB (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421: 499–506.

73. LeeJH, PaullTT (2007) Activation and regulation of ATM kinase activity in response to DNA double-strand breaks. Oncogene 26: 7741–7748.

74. RogakouEP, PilchDR, OrrAH, IvanovaVS, BonnerWM (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273: 5858–5868.

75. WardIM, ChenJ (2001) Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J Biol Chem 276: 47759–47762.

76. WardIM, MinnK, ChenJ (2004) UV-induced ataxia-telangiectasia-mutated and Rad3-related (ATR) activation requires replication stress. J Biol Chem 279: 9677–9680.

77. StiffT, WalkerSA, CerosalettiK, GoodarziAA, PetermannE, et al. (2006) ATR-dependent phosphorylation and activation of ATM in response to UV treatment or replication fork stalling. EMBO J 25: 5775–5782.

78. HuertasP, Cortes-LedesmaF, SartoriAA, AguileraA, JacksonSP (2008) CDK targets Sae2 to control DNA-end resection and homologous recombination. Nature 455: 689–692.

79. YuX, WuLC, BowcockAM, AronheimA, BaerR (1998) The C-terminal (BRCT) domains of BRCA1 interact in vivo with CtIP, a protein implicated in the CtBP pathway of transcriptional repression. J Biol Chem 273: 25388–25392.

80. YuX, FuS, LaiM, BaerR, ChenJ (2006) BRCA1 ubiquitinates its phosphorylation-dependent binding partner CtIP. Genes Dev 20: 1721–1726.

81. BruunD, FoliasA, AkkariY, CoxY, OlsonS, et al. (2003) siRNA depletion of BRCA1, but not BRCA2, causes increased genome instability in Fanconi anemia cells. DNA Repair (Amst) 2: 1007–1013.

82. XiongJ, FanS, MengQ, SchrammL, WangC, et al. (2003) BRCA1 inhibition of telomerase activity in cultured cells. Mol Cell Biol 23: 8668–8690.

83. CollisSJ, CicciaA, DeansAJ, HorejsiZ, MartinJS, et al. (2008) FANCM and FAAP24 function in ATR-mediated checkpoint signaling independently of the Fanconi anemia core complex. Mol Cell 32: 313–324.

84. XueY, LiY, GuoR, LingC, WangW (2008) FANCM of the Fanconi anemia core complex is required for both monoubiquitination and DNA repair. Hum Mol Genet 17: 1641–1652.

85. BakkerST, van de VrugtHJ, RooimansMA, OostraAB, SteltenpoolJ, et al. (2009) Fancm-deficient mice reveal unique features of Fanconi anemia complementation group M. Hum Mol Genet 18: 3484–3495.

86. BotvinickEL, BernsMW (2005) Internet-based robotic laser scissors and tweezers microscopy. Microsc Res Tech 68: 65–74.

87. OhDH, StanleyRJ, LinM, HoefflerWK, BoxerSG, et al. (1997) Two-photon excitation of 4′-hydroxymethyl-4,5′,8-trimethylpsoralen. Photochem Photobiol 65: 91–95.

88. VianaNB, RochaMS, MesquitaON, MazolliA, NetoPAM (2006) Characterization of objective transmittance for optical tweezers. Applied Optics 45: 4263–4269.

89. MirzoevaOK, PetriniJH (2003) DNA replication-dependent nuclear dynamics of the Mre11 complex. Mol Cancer Res 1: 207–218.

90. YuX, BaerR (2000) Nuclear localization and cell cycle-specific expression of CtIP, a protein that associates with the BRCA1 tumor suppressor. J Biol Chem 275: 18541–18549.

91. WangH, ShaoZ, ShiLZ, HwangPY, TruongLN, et al. (2012) CtIP Protein Dimerization Is Critical for Its Recruitment to Chromosomal DNA Double-stranded Breaks. J Biol Chem 287: 21471–21480.