FANCD2 Maintains Fork Stability in BRCA1/2-Deficient Tumors and Promotes Alternative End-Joining DNA Repair

Cell Reports

Volumn 15, Issue 11, 2016, Pages 2488-2499

  Kais, Zeina ^a   Rondinelli, Beatrice ^a   Holmes, Amie ^a   O'Leary, Colin ^a   Kozono, David ^a   D'Andrea, Alan D ^a,b   Ceccaldi, Raphael ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; BRCA2 PROTEIN; DNA POLYMERASE; DNA POLYMERASE THETA; FANCONI ANEMIA GROUP D2 PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; UNCLASSIFIED DRUG; CARRIER PROTEIN; DNA DIRECTED DNA POLYMERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NUCLEAR PROTEIN; RBBP8 PROTEIN, HUMAN;

ALTERNATIVE END JOINING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER RESISTANCE; CELL DEATH; CONTROLLED STUDY; DNA REPAIR; DNA REPLICATION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REPLICATION FORK; TUMOR CELL; TUMOR GROWTH; UBIQUITINATION; UPREGULATION; ANIMAL; CELL SURVIVAL; DEFICIENCY; DNA END JOINING REPAIR; GENETICS; GENOMIC INSTABILITY; METABOLISM; MUTATION; NEOPLASM; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; BRCA1 PROTEIN; BRCA2 PROTEIN; CARRIER PROTEINS; CELL LINE, TUMOR; CELL SURVIVAL; DNA END-JOINING REPAIR; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; FANCONI ANEMIA COMPLEMENTATION GROUP D2 PROTEIN; GENOMIC INSTABILITY; HUMANS; MICE, NUDE; MUTATION; NEOPLASMS; NUCLEAR PROTEINS; POLY(ADP-RIBOSE) POLYMERASES; UBIQUITINATION; UP-REGULATION;

EID: 84974662397     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.05.031     Document Type: Article

References (78)

1. Alabert C., Bukowski-Wills J.C., Lee S.B., Kustatscher G., Nakamura K., de Lima Alves F., Menard P., Mejlvang J., Rappsilber J., Groth A. Nascent chromatin capture proteomics determines chromatin dynamics during DNA replication and identifies unknown fork components. Nat. Cell Biol. 2014, 16:281-293.
2. Aparicio T., Baer R., Gautier J. DNA double-strand break repair pathway choice and cancer. DNA Repair (Amst.) 2014, 19:169-175.
3. Audebert M., Salles B., Calsou P. Involvement of poly(ADP-ribose) polymerase-1 and XRCC1/DNA ligase III in an alternative route for DNA double-strand breaks rejoining. J. Biol. Chem. 2004, 279:55117-55126.
4. Badie S., Carlos A.R., Folio C., Okamoto K., Bouwman P., Jonkers J., Tarsounas M. BRCA1 and CtIP promote alternative non-homologous end-joining at uncapped telomeres. EMBO J. 2015, 34:828.
5. Bartkova J., Horejsí Z., Koed K., Krämer A., Tort F., Zieger K., Guldberg P., Sehested M., Nesland J.M., Lukas C., et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 2005, 434:864-870.
6. Bennardo N., Cheng A., Huang N., Stark J.M. Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet. 2008, 4:e1000110.
7. Bouwman P., Jonkers J. Molecular pathways: how can BRCA-mutated tumors become resistant to PARP inhibitors?. Clin. Cancer Res. 2014, 20:540-547.
8. Branzei D., Foiani M. Interplay of replication checkpoints and repair proteins at stalled replication forks. DNA Repair (Amst.) 2007, 6:994-1003.
9. Branzei D., Foiani M. Maintaining genome stability at the replication fork. Nat. Rev. Mol. Cell Biol. 2010, 11:208-219.
10. Bryant H.E., Schultz N., Thomas H.D., Parker K.M., Flower D., Lopez E., Kyle S., Meuth M., Curtin N.J., Helleday T. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 2005, 434:913-917.
11. Bryant H.E., Petermann E., Schultz N., Jemth A.S., Loseva O., Issaeva N., Johansson F., Fernandez S., McGlynn P., Helleday T. PARP is activated at stalled forks to mediate Mre11-dependent replication restart and recombination. EMBO J. 2009, 28:2601-2615.
12. Bunting S.F., Nussenzweig A. End-joining, translocations and cancer. Nat. Rev. Cancer 2013, 13:443-454.
13. Bunting S.F., Callén E., Kozak M.L., Kim J.M., Wong N., López-Contreras A.J., Ludwig T., Baer R., Faryabi R.B., Malhowski A., et al. BRCA1 functions independently of homologous recombination in DNA interstrand crosslink repair. Mol. Cell 2012, 46:125-135.
14. Comprehensive molecular portraits of human breast tumours. Nature 2012, 490:61-70. Cancer Genome Atlas Network.
15. Integrated genomic analyses of ovarian carcinoma. Nature 2011, 474:609-615. Cancer Genome Atlas Research Network.
16. Ceccaldi R., Liu J.C., Amunugama R., Hajdu I., Primack B., Petalcorin M.I., O'Connor K.W., Konstantinopoulos P.A., Elledge S.J., Boulton S.J., et al. Homologous-recombination-deficient tumours are dependent on Polθ-mediated repair. Nature 2015, 518:258-262.
17. Ceccaldi R., Rondinelli B., D'Andrea A.D. Repair pathway choices and consequences at the double-strand break. Trends Cell Biol. 2016, 1:52-64.
18. Chan K.L., Palmai-Pallag T., Ying S., Hickson I.D. Replication stress induces sister-chromatid bridging at fragile site loci in mitosis. Nat. Cell Biol. 2009, 11:753-760.
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, 41:6444-6459.
20. Chaudhury I., Stroik D.R., Sobeck A. FANCD2-controlled chromatin access of the Fanconi-associated nuclease FAN1 is crucial for the recovery of stalled replication forks. Mol. Cell. Biol. 2014, 34:3939-3954.
21. Chen Y.H., Jones M.J., Yin Y., Crist S.B., Colnaghi L., Sims R.J., Rothenberg E., Jallepalli P.V., Huang T.T. ATR-mediated phosphorylation of FANCI regulates dormant origin firing in response to replication stress. Mol. Cell 2015, 58:323-338.
22. Couch F.B., Bansbach C.E., Driscoll R., Luzwick J.W., Glick G.G., Bétous R., Carroll C.M., Jung S.Y., Qin J., Cimprich K.A., Cortez D. ATR phosphorylates SMARCAL1 to prevent replication fork collapse. Genes Dev. 2013, 27:1610-1623.
23. Cox M.M., Goodman M.F., Kreuzer K.N., Sherratt D.J., Sandler S.J., Marians K.J. The importance of repairing stalled replication forks. Nature 2000, 404:37-41.
24. Deans A.J., West S.C. DNA interstrand crosslink repair and cancer. Nature Rev. Cancer 2011, 11:467-480.
25. Deriano L., Roth D.B. Modernizing the nonhomologous end-joining repertoire: alternative and classical NHEJ share the stage. Annu. Rev. Genet. 2013, 47:433-455.
26. Duquette M.L., Zhu Q., Taylor E.R., Tsay A.J., Shi L.Z., Berns M.W., McGowan C.H. CtIP is required to initiate replication-dependent interstrand crosslink repair. PLoS Genet. 2012, 8:e1003050.
27. Edwards S.L., Brough R., Lord C.J., Natrajan R., Vatcheva R., Levine D.A., Boyd J., Reis-Filho J.S., Ashworth A. Resistance to therapy caused by intragenic deletion in BRCA2. Nature 2008, 451:1111-1115.
28. Escribano-Díaz C., Orthwein A., Fradet-Turcotte A., Xing M., Young J.T., Tkáč J., Cook M.A., Rosebrock A.P., Munro M., Canny M.D., et al. A cell cycle-dependent regulatory circuit composed of 53BP1-RIF1 and BRCA1-CtIP controls DNA repair pathway choice. Mol. Cell 2013, 49:872-883.
29. Farmer H., McCabe N., Lord C.J., Tutt A.N., Johnson D.A., Richardson T.B., Santarosa M., Dillon K.J., Hickson I., Knights C., et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005, 434:917-921.
30. Garcia-Higuera I., Taniguchi T., Ganesan S., Meyn M.S., Timmers C., Hejna J., Grompe M., D'Andrea A.D. Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol. Cell 2001, 7:249-262.
31. Gari K., Décaillet C., Stasiak A.Z., Stasiak A., Constantinou A. The Fanconi anemia protein FANCM can promote branch migration of Holliday junctions and replication forks. Mol. Cell 2008, 29:141-148.
32. Gorgoulis V.G., Vassiliou L.V., Karakaidos P., Zacharatos P., Kotsinas A., Liloglou T., Venere M., Ditullio R.A., Kastrinakis N.G., Levy B., et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 2005, 434:907-913.
33. Hastings P.J., Ira G., Lupski J.R. A microhomology-mediated break-induced replication model for the origin of human copy number variation. PLoS Genet. 2009, 5:e1000327.
34. Howard S.M., Yanez D.A., Stark J.M. DNA damage response factors from diverse pathways, including DNA crosslink repair, mediate alternative end joining. PLoS Genet. 2015, 11:e1004943.
35. Howlett N.G., Taniguchi T., Durkin S.G., D'Andrea A.D., Glover T.W. The Fanconi anemia pathway is required for the DNA replication stress response and for the regulation of common fragile site stability. Hum. Mol. Genet. 2005, 14:693-701.
36. Howlett N.G., Harney J.A., Rego M.A., Kolling F.W., Glover T.W. Functional interaction between the Fanconi Anemia D2 protein and proliferating cell nuclear antigen (PCNA) via a conserved putative PCNA interaction motif. J. Biol. Chem. 2009, 284:28935-28942.
37. Jackson D.A., Pombo A. 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. 1998, 140:1285-1295.
38. Kent T., Chandramouly G., McDevitt S.M., Ozdemir A.Y., Pomerantz R.T. Mechanism of microhomology-mediated end-joining promoted by human DNA polymerase θ. Nat. Struct. Mol. Biol. 2015, 22:230-237.
39. Kim H., D'Andrea A.D. Regulation of DNA cross-link repair by the Fanconi anemia/BRCA pathway. Genes Dev. 2012, 26:1393-1408.
40. Konstantinopoulos P.A., Ceccaldi R., Shapiro G.I., D'Andrea A.D. Homologous recombination deficiency: exploiting the fundamental vulnerability of ovarian cancer. Cancer Discov. 2015, 5:1137-1154.
41. Lachaud C., Moreno A., Marchesi F., Toth R., Blow J.J., Rouse J. Ubiquitinated Fancd2 recruits Fan1 to stalled replication forks to prevent genome instability. Science 2016, 351:846-849.
42. Lee-Theilen M., Matthews A.J., Kelly D., Zheng S., Chaudhuri J. CtIP promotes microhomology-mediated alternative end joining during class-switch recombination. Nat. Struct. Mol. Biol. 2011, 18:75-79.
43. Lomonosov M., Anand S., Sangrithi M., Davies R., Venkitaraman A.R. Stabilization of stalled DNA replication forks by the BRCA2 breast cancer susceptibility protein. Genes Dev. 2003, 17:3017-3022.
44. Long D.T., Joukov V., Budzowska M., Walter J.C. BRCA1 promotes unloading of the CMG helicase from a stalled DNA replication fork. Mol. Cell 2014, 56:174-185.
45. Lord C.J., Ashworth A. Mechanisms of resistance to therapies targeting BRCA-mutant cancers. Nat. Med. 2013, 19:1381-1388.
46. 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, 51:678-690.
47. Mateos-Gomez P.A., Gong F., Nair N., Miller K.M., Lazzerini-Denchi E., Sfeir A. Mammalian polymerase θ promotes alternative NHEJ and suppresses recombination. Nature 2015, 518:254-257.
48. Michel B., Grompone G., Florès M.J., Bidnenko V. Multiple pathways process stalled replication forks. Proc. Natl. Acad. Sci. USA 2004, 101:12783-12788.
49. Moynahan M.E., Chiu J.W., Koller B.H., Jasin M. Brca1 controls homology-directed DNA repair. Mol. Cell 1999, 4:511-518.
50. Moynahan M.E., Pierce A.J., Jasin M. BRCA2 is required for homology-directed repair of chromosomal breaks. Mol. Cell 2001, 7:263-272.
51. Murina O., von Aesch C., Karakus U., Ferretti L.P., Bolck H.A., Hänggi K., Sartori A.A. FANCD2 and CtIP cooperate to repair DNA interstrand crosslinks. Cell Rep. 2014, 7:1030-1038.
52. Naim V., Rosselli F. The FANC pathway and BLM collaborate during mitosis to prevent micro-nucleation and chromosome abnormalities. Nat. Cell Biol. 2009, 11:761-768.
53. Nakanishi K., Yang Y.G., Pierce A.J., Taniguchi T., Digweed M., D'Andrea A.D., Wang Z.Q., Jasin M. Human Fanconi anemia monoubiquitination pathway promotes homologous DNA repair. Proc. Natl. Acad. Sci. USA 2005, 102:1110-1115.
54. Negrini S., Gorgoulis V.G., Halazonetis T.D. Genomic instability--an evolving hallmark of cancer. Nat. Rev. Mol. Cell Biol. 2010, 11:220-228.
55. Newman J.A., Cooper C.D., Aitkenhead H., Gileadi O. Structure of the Helicase Domain of DNA Polymerase Theta Reveals a Possible Role in the Microhomology-Mediated End-Joining Pathway. Structure 2015, 23:2319-2330.
56. Nguyen T.V., Riou L., Aoufouchi S., Rosselli F. Fanca deficiency reduces A/T transitions in somatic hypermutation and alters class switch recombination junctions in mouse B cells. J. Exp. Med. 2014, 211:1011-1018.
57. Nijman S.M., Huang T.T., Dirac A.M., Brummelkamp T.R., Kerkhoven R.M., D'Andrea A.D., Bernards R. The deubiquitinating enzyme USP1 regulates the Fanconi anemia pathway. Mol. Cell 2005, 17:331-339.
58. Pathania S., Bade S., Le Guillou M., Burke K., Reed R., Bowman-Colin C., Su Y., Ting D.T., Polyak K., Richardson A.L., et al. BRCA1 haploinsufficiency for replication stress suppression in primary cells. Nat. Commun. 2014, 5:5496.
59. Prakash R., Zhang Y., Feng W., Jasin M. Homologous recombination and human health: the roles of BRCA1, BRCA2, and associated proteins. Cold Spring Harb. Perspect. Biol. 2015, 7:a016600.
60. Sakai W., Swisher E.M., Karlan B.Y., Agarwal M.K., Higgins J., Friedman C., Villegas E., Jacquemont C., Farrugia D.J., Couch F.J., et al. Secondary mutations as a mechanism of cisplatin resistance in BRCA2-mutated cancers. Nature 2008, 451:1116-1120.
61. Sartori A.A., Lukas C., Coates J., Mistrik M., Fu S., Bartek J., Baer R., Lukas J., Jackson S.P. Human CtIP promotes DNA end resection. Nature 2007, 450:509-514.
62. 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, 145:529-542.
63. Schlacher K., Wu H., Jasin M. A distinct replication fork protection pathway connects Fanconi anemia tumor suppressors to RAD51-BRCA1/2. Cancer Cell 2012, 22:106-116.
64. Schwab R.A., Nieminuszczy J., Shah F., Langton J., Lopez Martinez D., Liang C.C., Cohn M.A., Gibbons R.J., Deans A.J., Niedzwiedz W. The Fanconi Anemia Pathway Maintains Genome Stability by Coordinating Replication and Transcription. Mol. Cell 2015, 60:351-361.
65. Simsek D., Jasin M. Alternative end-joining is suppressed by the canonical NHEJ component Xrcc4-ligase IV during chromosomal translocation formation. Nat. Struct. Mol. Biol. 2010, 17:410-416.
66. Sirbu B.M., McDonald W.H., Dungrawala H., Badu-Nkansah A., Kavanaugh G.M., Chen Y., Tabb D.L., 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, 288:31458-31467.
67. Smogorzewska A., Matsuoka S., Vinciguerra P., McDonald E.R., Hurov K.E., Luo J., Ballif B.A., Gygi S.P., Hofmann K., D'Andrea A.D., Elledge S.J. Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell 2007, 129:289-301.
68. Unno J., Itaya A., Taoka M., Sato K., Tomida J., Sakai W., Sugasawa K., Ishiai M., Ikura T., Isobe T., et al. FANCD2 binds CtIP and regulates DNA-end resection during DNA interstrand crosslink repair. Cell Rep. 2014, 7:1039-1047.
69. Wang X., Andreassen P.R., D'Andrea A.D. Functional interaction of monoubiquitinated FANCD2 and BRCA2/FANCD1 in chromatin. Mol. Cell. Biol. 2004, 24:5850-5862.
70. Wang M., Wu W., Wu W., Rosidi B., Zhang L., Wang H., Iliakis G. PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res. 2006, 34:6170-6182.
71. Willis N.A., Chandramouly G., Huang B., Kwok A., Follonier C., Deng C., Scully R. BRCA1 controls homologous recombination at Tus/Ter-stalled mammalian replication forks. Nature 2014, 510:556-559.
72. Yan S., Michael W.M. TopBP1 and DNA polymerase-alpha directly recruit the 9-1-1 complex to stalled DNA replication forks. J. Cell Biol. 2009, 184:793-804.
73. Yeo J.E., Lee E.H., Hendrickson E.A., Sobeck A. CtIP mediates replication fork recovery in a FANCD2-regulated manner. Hum. Mol. Genet. 2014, 23:3695-3705.
74. Ying S., Hamdy F.C., Helleday T. Mre11-dependent degradation of stalled DNA replication forks is prevented by BRCA2 and PARP1. Cancer Res. 2012, 72:2814-2821.
75. Ying S., Chen Z., Medhurst A.L., Neal J.A., Bao Z., Mortusewicz O., McGouran J., Song X., Shen H., Hamdy F.C., et al. DNA-PKcs and PARP1 bind to unresected stalled DNA replication forks where they recruit XRCC1 to mediate repair. Cancer Res. 2016, 76:1078-1088.
76. Yousefzadeh M.J., Wood R.D. DNA polymerase POLQ and cellular defense against DNA damage. DNA Repair (Amst.) 2013, 12:1-9.
77. Zeman M.K., Cimprich K.A. Causes and consequences of replication stress. Nat. Cell Biol. 2014, 16:2-9.
78. Zhang Y., Jasin M. An essential role for CtIP in chromosomal translocation formation through an alternative end-joining pathway. Nat. Struct. Mol. Biol. 2011, 18:80-84.