Preventing over-resection by DNA2 helicase/nuclease suppresses repair defects in Fanconi anemia cells

Cell Cycle

Volumn 13, Issue 10, 2014, Pages 1540-1550

  Karanja, KennethK ^a   Lee, Eu Han ^b   Hendrickson, EricA ^b   Campbell, Judith L ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Dna recombination; Dna replication; DNA2; FANCD2; Fanconi anemia; Formaldehyde dna damage; Interstrand crosslinks

Indexed keywords

CISPLATIN; DNA HELICASE; DNA2 HELICASE; FANCONI ANEMIA GROUP D2 PROTEIN; FORMALDEHYDE; NUCLEASE; OKAZAKI FRAGMENT; UNCLASSIFIED DRUG; DNA2 PROTEIN, HUMAN; PSORALEN;

ARTICLE; CONTROLLED STUDY; CROSS LINKING; DNA REPLICATION; FANCONI ANEMIA; GENOMIC INSTABILITY; PHENOTYPE; PROTEIN DNA INTERACTION; CHEMISTRY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; DRUG EFFECTS; GENETICS; HUMAN; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

CELL LINE, TUMOR; CISPLATIN; DNA BREAKS, DOUBLE-STRANDED; DNA HELICASES; DNA REPAIR; FANCONI ANEMIA; FANCONI ANEMIA COMPLEMENTATION GROUP D2 PROTEIN; FICUSIN; FORMALDEHYDE; GENOMIC INSTABILITY; HUMANS;

EID: 84900559537     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.28476     Document Type: Article

References (68)

1. Kim H, D'Andrea AD. Regulation of DNA cross-link repair by the Fanconi anemia/BRCA pathway. Genes Dev 2012; 26:1393-408; PMID:22751496; http://dx.doi.org/10.1101/gad.195248.112
2. Kee Y, D'Andrea AD. Expanded roles of the Fanconi anemia pathway in preserving genomic stability. Genes Dev 2010; 24:1680-94; PMID:20713514; http://dx.doi.org/10.1101/gad.1955310
3. Constantinou A. Rescue of replication failure by Fanconi anaemia proteins. Chromosoma 2012; 121:21-36; PMID:22057367; http://dx.doi.org/10.1007/ s00412-011-0349-2
4. Kottemann MC, Smogorzewska A. Fanconi anaemia and the repair of Watson and Crick DNA crosslinks. Nature 2013; 493:356-63; PMID:23325218; http://dx.doi.org/10.1038/nature11863
5. Deans AJ, West SC. DNA interstrand crosslink repair and cancer. Nat Rev Cancer 2011; 11:467-80; PMID:21701511; http://dx.doi.org/10.1038/nrc3088
6. Schlacher K, Wu H, Jasin M. A distinct replication fork protection pathway connects Fanconi anemia tumor suppressors to RAD51-BRCA1/2. Cancer Cell 2012; 22:106-16; PMID:22789542; http://dx.doi.org/10.1016/j.ccr.2012.05.015
7. Lossaint G, Larroque M, Ribeyre C, Bec N, Larroque C, Décaillet C, Gari K, Constantinou A. FANCD2 binds MCM proteins and controls replisome function upon activation of s phase checkpoint signaling. Mol Cell 2013; 51:678-90; PMID:23993743; http://dx.doi.org/10.1016/j.molcel.2013.07.023
8. Schwab RA, Blackford AN, Niedzwiedz W. ATR activation and replication fork restart are defective in FANCM-deficient cells. EMBO J 2010; 29:806-18; PMID:20057355; http://dx.doi.org/10.1038/emboj.2009.385
9. Collis SJ, Ciccia A, Deans AJ, Horejsí Z, Martin JS, Maslen SL, Skehel JM, Elledge SJ, West SC, Boulton SJ. FANCM and FAAP24 function in ATR-mediated checkpoint signaling independently of the Fanconi anemia core complex. Mol Cell 2008; 32:313-24; PMID:18995830; http://dx.doi.org/10.1016/j. molcel.2008.10.014
10. Ciccia A, Ling C, Coulthard R, Yan Z, Xue Y, Meetei AR, Laghmani H, Joenje H, McDonald N, de Winter JP, et al. Identification of FAAP24, a Fanconi anemia core complex protein that interacts with FANCM. Mol Cell 2007; 25:331-43; PMID:17289582; http://dx.doi.org/10.1016/j.molcel.2007.01.003
11. Deans AJ, West SC. FANCM connects the genome instability disorders Bloom's Syndrome and Fanconi Anemia. Mol Cell 2009; 36:943-53; PMID:20064461; http://dx.doi.org/10.1016/j.molcel.2009.12.006
12. Kim JM, Kee Y, Gurtan A, D'Andrea AD. Cell cycle-dependent chromatin loading of the Fanconi anemia core complex by FANCM/FAAP24. Blood 2008; 111:5215-22; PMID:18174376; http://dx.doi.org/10.1182/blood-2007-09-113092
13. Huang J, Liu S, Bellani MA, Thazhathveetil AK, Ling C, de Winter JP, Wang Y, Wang W, Seidman MM. The DNA translocase FANCM/MHF promotes replication traverse of DNA interstrand crosslinks. Mol Cell 2013; 52:434-46; PMID:24207054; http://dx.doi.org/10.1016/j.molcel.2013.09.021
14. Pace P, Mosedale G, Hodskinson MR, Rosado IV, Sivasubramaniam M, Patel KJ. Ku70 corrupts DNA repair in the absence of the Fanconi anemia pathway. Science 2010; 329:219-23; PMID:20538911; http://dx.doi.org/10.1126/science. 1192277
15. Adamo A, Collis SJ, Adelman CA, Silva N, Horejsi Z, Ward JD, Martinez-Perez E, Boulton SJ, La Volpe A. Preventing nonhomologous end joining suppresses DNA repair defects of Fanconi anemia. Mol Cell 2010; 39:25-35; PMID:20598602; http://dx.doi.org/10.1016/j.molcel.2010.06.026
16. Bunting SF, Callén E, Kozak ML, Kim JM, Wong N, López-Contreras AJ, Ludwig T, Baer R, Faryabi RB, Malhowski A, et al. BRCA1 functions independently of homologous recombination in DNA interstrand crosslink repair. Mol Cell 2012; 46:125-35; PMID:22445484; http://dx.doi.org/10. 1016/j.molcel.2012.02.015
17. Chan KL, Palmai-Pallag T, Ying S, Hickson ID. Replication stress induces sister-chromatid bridging at fragile site loci in mitosis. Nat Cell Biol 2009; 11:753-60; PMID:19465922; http://dx.doi.org/10.1038/ncb1882
18. Naim V, Rosselli F. The FANC pathway and mitosis: a replication legacy. Cell Cycle 2009; 8:2907-11; PMID:19729998; http://dx.doi.org/10.4161/cc.8.18. 9538
19. Chaudhury I, Sareen A, Raghunandan M, Sobeck A. FANCD2 regulates BLM complex functions independently of FANCI to promote replication fork recovery. Nucleic Acids Res 2013; 41:6444-59; PMID:23658231; http://dx.doi.org/10.1093/ nar/gkt348
20. Pichierri P, Franchitto A, Rosselli F. BLM and the FANC proteins collaborate in a common pathway in response to stalled replication forks. EMBO J 2004; 23:3154-63; PMID:15257300; http://dx.doi.org/10.1038/sj.emboj.7600277
21. Kang YH, Lee CH, Seo YS. Dna2 on the road to Okazaki fragment processing and genome stability in eukaryotes. Crit Rev Biochem Mol Biol 2010; 45:71-96; PMID:20131965; http://dx.doi.org/10.3109/10409230903578593
22. Meetei AR, Sechi S, Wallisch M, Yang D, Young MK, Joenje H, Hoatlin ME, Wang W. A multiprotein nuclear complex connects Fanconi anemia and Bloom syndrome. Mol Cell Biol 2003; 23:3417-26; PMID:12724401; http://dx.doi.org/10. 1128/MCB.23.10.3417-3426.2003
23. Roques C, Coulombe Y, Delannoy M, Vignard J, Grossi S, Brodeur I, Rodrigue A, Gautier J, Stasiak AZ, Stasiak A, et al. MRE11-RAD50-NBS1 is a critical regulator of FANCD2 stability and function during DNA double-strand break repair. EMBO J 2009; 28:2400-13; PMID:19609304; http://dx.doi.org/10.1038/ emboj.2009.193
24. Karanja KK, Cox SW, Duxin JP, Stewart SA, Campbell JL. DNA2 and EXO1 in replication-coupled, homology-directed repair and in the interplay between HDR and the FA/BRCA network. Cell Cycle 2012; 11:3983-96; PMID:22987153; http://dx.doi.org/10.4161/cc.22215
25. Duxin JP, Dao B, Martinsson P, Rajala N, Guittat L, Campbell JL, Spelbrink JN, Stewart SA. Human Dna2 is a nuclear and mitochondrial DNA maintenance protein. Mol Cell Biol 2009; 29:4274-82; PMID:19487465; http://dx.doi.org/10.1128/MCB.01834-08
26. Duxin JP, Moore HR, Sidorova J, Karanja K, Honaker Y, Dao B, Piwnica-Worms H, Campbell JL, Monnat RJ Jr., Stewart SA. Okazaki fragment processing-independent role for human Dna2 enzyme during DNA replication. J Biol Chem 2012; 287:21980-91; PMID:22570476; http://dx.doi.org/10.1074/jbc.M112. 359018
27. Budd ME. Cox Ls, Campbell JL. Coordination of Nucleases and Helicases during DNA Replication and Double-strand Break Repair. In: Cox LS, ed. Molecular Themes in DNA Replication. London: RSC Publishing, 2009.
28. Budd ME, Campbell JL. Interplay of Mre11 nuclease with Dna2 plus Sgs1 in Rad51-dependent recombinational repair. PLoS One 2009; 4:e4267; PMID:19165339; http://dx.doi.org/10.1371/journal.pone.0004267
29. Zhu Z, Chung WH, Shim EY, Lee SE, Ira G. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 2008; 134:981-94; PMID:18805091; http://dx.doi.org/10.1016/j.cell.2008.08.037
30. Mimitou EP, Symington LS. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 2008; 455:770-4; PMID:18806779; http://dx.doi.org/10.1038/nature07312
31. Nimonkar AV, Genschel J, Kinoshita E, Polaczek P, Campbell JL, Wyman C, Modrich P, Kowalczykowski SC. BLM-DNA2-RPA-MRN and EXO1-BLM-RPAMRN constitute two DNA end resection machineries for human DNA break repair. Genes Dev 2011; 25:350-62; PMID:21325134; http://dx.doi.org/10.1101/gad.2003811
32. Cejka P, Cannavo E, Polaczek P, Masuda-Sasa T, Pokharel S, Campbell JL, Kowalczykowski SC. DNA end resection by Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2. Nature 2010; 467:112-6; PMID:20811461; http://dx.doi.org/10.1038/nature09355
33. Hu J, Sun L, Shen F, Chen Y, Hua Y, Liu Y, Zhang M, Hu Y, Wang Q, Xu W, et al. The intra-S phase checkpoint targets Dna2 to prevent stalled replication forks from reversing. Cell 2012; 149:1221-32; PMID:22682245; http://dx.doi.org/10.1016/j.cell.2012.04.030
34. Imamura O, Campbell JL. The human Bloom syndrome gene suppresses the DNA replication and repair defects of yeast dna2 mutants. Proc Natl Acad Sci U S A 2003; 100:8193-8; PMID:12826610; http://dx.doi.org/10.1073/pnas.1431624100
35. Kang YH, Kang MJ, Kim JH, Lee CH, Cho IT, Hurwitz J, Seo YS. The MPH1 gene of Saccharomyces cerevisiae functions in Okazaki fragment processing. J Biol Chem 2009; 284:10376-86; PMID:19181670; http://dx.doi.org/10.1074/jbc. M808894200
36. Zheng P, Fay DS, Burton J, Xiao H, Pinkham JL, Stern DF. SPK1 is an essential S-phase-specific gene of Saccharomyces cerevisiae that encodes a nuclear serine/threonine/tyrosine kinase. Mol Cell Biol 1993; 13:5829-42; PMID:8355715
37. Roberts SA, Sterling J, Thompson C, Harris S, Mav D, Shah R, Klimczak LJ, Kryukov GV, Malc E, Mieczkowski PA, et al. Clustered mutations in yeast and in human cancers can arise from damaged long single-strand DNA regions. Mol Cell 2012; 46:424-35; PMID:22607975; http://dx.doi.org/10.1016/j.molcel.2012.03.030
38. Setlur SR, Lee C. Tumor archaeology reveals that mutations love company. Cell 2012; 149:959-61; PMID:22632962; http://dx.doi.org/10.1016/j.cell.2012.05. 010
39. Hastings PJ, Ira G, Lupski JR. A microhomology-mediated break-induced replication model for the origin of human copy number variation. PLoS Genet 2009; 5:e1000327; PMID:19180184; http://dx.doi.org/10.1371/journal.pgen.1000327
40. Stephens PJ, Greenman CD, Fu B, Yang F, Bignell GR, Mudie LJ, Pleasance ED, Lau KW, Beare D, Stebbings LA, et al. Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell 2011; 144:27-40; PMID:21215367; http://dx.doi.org/10.1016/j.cell.2010.11.055
41. Rosado IV, Langevin F, Crossan GP, Takata M, Patel KJ. Formaldehyde catabolism is essential in cells deficient for the Fanconi anemia DNA-repair pathway. Nat Struct Mol Biol 2011; 18:1432-4; PMID:22081012; http://dx.doi.org/10.1038/nsmb.2173
42. Ridpath JR, Nakamura A, Tano K, Luke AM, Sonoda E, Arakawa H, Buerstedde JM, Gillespie DA, Sale JE, Yamazoe M, et al. Cells deficient in the FANC/BRCA pathway are hypersensitive to plasma levels of formaldehyde. Cancer Res 2007; 67:11117-22; PMID:18056434; http://dx.doi.org/10.1158/0008-5472.CAN-07-3028
43. Heck Hd, Casanova M. The implausibility of leukemia induction by formaldehyde: a critical review of the biological evidence on distant-site toxicity. Regul Toxicol Pharmacol 2004; 40:92-106; PMID:15450713; http://dx.doi.org/10.1016/j.yrtph.2004.05.001
44. Fattah FJ, Lichter NF, Fattah KR, Oh S, Hendrickson EA. Ku70, an essential gene, modulates the frequency of rAAV-mediated gene targeting in human somatic cells. Proc Natl Acad Sci U S A 2008; 105:8703-8; PMID:18562296; http://dx.doi.org/10.1073/pnas.0712060105
45. Russell DW, Hirata RK. Human gene targeting by viral vectors. Nat Genet 1998; 18:325-30; PMID:9537413; http://dx.doi.org/10.1038/ng0498-325
46. Nakanishi K, Cavallo F, Perrouault L, Giovannangeli C, Moynahan ME, Barchi M, Brunet E, Jasin M. Homology-directed Fanconi anemia pathway crosslink repair is dependent on DNA replication. Nat Struct Mol Biol 2011; 18:500-3; PMID:21423196; http://dx.doi.org/10.1038/nsmb.2029
47. Nakanishi K, Cavallo F, Brunet E, Jasin M. Homologous recombination assay for interstrand cross-link repair. Methods Mol Biol 2011; 745:283-91; PMID:21660700; http://dx.doi.org/10.1007/978-1-61779-129-1-16
48. Gunn A, Bennardo N, Cheng A, Stark JM. Correct end use during end joining of multiple chromosomal double strand breaks is influenced by repair protein RAD50, DNA-dependent protein kinase DNA-PKcs, and transcription context. J Biol Chem 2011; 286:42470-82; PMID:22027841; http://dx.doi.org/10.1074/jbc.M111. 309252
49. Bennardo N, Cheng A, Huang N, Stark JM. Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet 2008; 4:e1000110; PMID:18584027; http://dx.doi.org/10.1371/journal.pgen. 1000110
50. Wang X, Andreassen PR, D'Andrea AD. Functional interaction of monoubiquitinated FANCD2 and BRCA2/FANCD1 in chromatin. Mol Cell Biol 2004; 24:5850-62; PMID:15199141; http://dx.doi.org/10.1128/MCB.24.13.5850-5862.2004
51. Yang SH, Zhou R, Campbell J, Chen J, Ha T, Paull TT. The SOSS1 single-stranded DNA binding complex promotes DNA end resection in concert with Exo1. EMBO J 2013; 32:126-39; PMID:23178594; http://dx.doi.org/10.1038/emboj. 2012.314
52. Moldovan GL, Dejsuphong D, Petalcorin MI, Hofmann K, Takeda S, Boulton SJ, D'Andrea AD. Inhibition of homologous recombination by the PCNA-interacting protein PARI. Mol Cell 2012; 45:75-86; PMID:22153967; http://dx.doi.org/10.1016/ j.molcel.2011.11.010
53. Nik-Zainal S, Van Loo P, Wedge DC, Alexandrov LB, Greenman CD, Lau KW, Raine K, Jones D, Marshall J, Ramakrishna M, et al.; Breast Cancer Working Group of the International Cancer Genome Consortium. The life history of 21 breast cancers. Cell 2012; 149:994-1007; PMID:22608083; http://dx.doi.org/10.1016/j. cell.2012.04.023
54. Chan K, Sterling JF, Roberts SA, Bhagwat AS, Resnick MA, Gordenin DA. Base damage within single-strand DNA underlies in vivo hypermutability induced by a ubiquitous environmental agent. PLoS Genet 2012; 8:e1003149; PMID:23271983; http://dx.doi.org/10.1371/journal.pgen.1003149
55. Liu P, Erez A, Nagamani SC, Dhar SU, Kołodziejska KE, Dharmadhikari AV, Cooper ML, Wiszniewska J, Zhang F, Withers MA, et al. Chromosome catastrophes involve replication mechanisms generating complex genomic rearrangements. Cell 2011; 146:889-903; PMID:21925314; http://dx.doi.org/10.1016/j.cell.2011.07.042
56. Branzei D, Foiani M. Maintaining genome stability at the replication fork. Nat Rev Mol Cell Biol 2010; 11:208-19; PMID:20177396; http://dx.doi.org/ 10.1038/nrm2852
57. Schlacher K, Christ N, Siaud N, Egashira A, Wu H, Jasin M. Double-strand break repair-independent role for BRCA2 in blocking stalled replication fork degradation by MRE11. Cell 2011; 145:529-42; PMID:21565612; http://dx.doi.org/ 10.1016/j.cell.2011.03.041
58. Sirbu BM, McDonald WH, Dungrawala H, Badu-Nkansah A, Kavanaugh GM, Chen Y, Tabb DL, Cortez D. Identification of proteins at active, stalled, and collapsed replication forks using isolation of proteins on nascent DNA (iPOND) coupled with mass spectrometry. J Biol Chem 2013; 288:31458-67; PMID:24047897; http://dx.doi.org/10.1074/jbc.M113.511337
59. Hashimoto Y, Ray Chaudhuri A, Lopes M, Costanzo V. Rad51 protects nascent DNA from Mre11-dependent degradation and promotes continuous DNA synthesis. Nat Struct Mol Biol 2010; 17:1305-11; PMID:20935632; http://dx.doi.org/10.1038/ nsmb.1927
60. Symington LS, Gautier J. Double-strand break end resection and repair pathway choice. Annu Rev Genet 2011; 45:247-71; PMID:21910633; http://dx.doi.org/10.1146/annurev-genet-110410-132435
61. Shibata A, Moiani D, Arvai AS, Perry J, Harding SM, Genois MM, Maity R, van Rossum-Fikkert S, Kertokalio A, Romoli F, et al. DNA double-strand break repair pathway choice is directed by distinct MRE11 nuclease activities. Mol Cell 2014; 53:7-18; PMID:24316220
62. Peng G, Dai H, Zhang W, Hsieh HJ, Pan MR, Park YY, Tsai RY, Bedrosian I, Lee JS, Ira G, et al. Human nuclease/helicase DNA2 alleviates replication stress by promoting DNA end resection. Cancer Res 2012; 72:2802-13; PMID:22491672; http://dx.doi.org/10.1158/0008-5472.CAN-11-3152
63. Duquette ML, Zhu Q, Taylor ER, Tsay AJ, Shi LZ, Berns MW, McGowan CH. CtIP is required to initiate replication-dependent interstrand crosslink repair. PLoS Genet 2012; 8:e1003050; PMID:23144634; http://dx.doi.org/10.1371/journal. pgen.1003050
64. Petermann E, Orta ML, Issaeva N, Schultz N, Helleday T. Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol Cell 2010; 37:492-502; PMID:20188668; http://dx.doi.org/10.1016/j.molcel.2010.01.021
65. Langevin F, Crossan GP, Rosado IV, Arends MJ, Patel KJ. Fancd2 counteracts the toxic effects of naturally produced aldehydes in mice. Nature 2011; 475:53-8; PMID:21734703; http://dx.doi.org/10.1038/nature10192
66. Pierce AJ, Johnson RD, Thompson LH, Jasin M. XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev 1999; 13:2633-8; PMID:10541549; http://dx.doi.org/10.1101/gad.13.20.2633
67. Saharia A, Guittat L, Crocker S, Lim A, Steffen M, Kulkarni S, Stewart SA. Flap endonuclease 1 contributes to telomere stability. Curr Biol 2008; 18:496-500; PMID:18394896; http://dx.doi.org/10.1016/j.cub.2008.02.071
68. Lin W, Sampathi S, Dai H, Liu C, Zhou M, Hu J, Huang Q, Campbell J, Shin-Ya K, Zheng L, et al. Mammalian DNA2 helicase/nuclease cleaves G-quadruplex DNA and is required for telomere integrity. EMBO J 2013; 32:1425-39; PMID:23604072; http://dx.doi.org/10.1038/emboj.2013.88