DNA helicases FANCM and DDX11 are determinants of PARP inhibitor sensitivity

DNA Repair

Volumn 26, Issue , 2015, Pages 54-64

  Stoepker, Chantal ^a   Faramarz, Atiq ^a   Rooimans, Martin A ^a   van Mil, Saskia E ^a   Balk, Jesper A ^a   Velleuer, Eunike ^b   Ameziane, Najim ^a   te Riele, Hein ^a   de Winter, Johan P ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

Author keywords

DDX11; FANCM; Fanconi anemia; PARP inhibitor; Sister chromatid cohesion; Warsaw breakage syndrome

Indexed keywords

BRCA2 PROTEIN; CAMPTOTHECIN; CISPLATIN; DEAD BOX PROTEIN 20; DNA HELICASE; FANCONI ANEMIA PROTEIN; KU 0058948; MITOMYCIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; UNCLASSIFIED DRUG; BRCA2 PROTEIN, HUMAN; DDX11 PROTEIN, HUMAN; DEAD BOX PROTEIN; ENZYME INHIBITOR; FANCM PROTEIN, HUMAN; FLUOROBENZENE; KU0058948; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PHTHALAZINE DERIVATIVE;

ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CHROMOSOME BREAKAGE; CONTROLLED STUDY; GENE MUTATION; HUMAN; HUMAN CELL; LYMPHOBLASTOID CELL LINE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TREATMENT RESPONSE; ANTAGONISTS AND INHIBITORS; FANCONI ANEMIA; FEMALE; GENE SILENCING; GENETICS; MALE; TRANSFORMED CELL LINE;

BRCA2 PROTEIN; CELL LINE, TRANSFORMED; DEAD-BOX RNA HELICASES; DNA HELICASES; ENZYME INHIBITORS; FANCONI ANEMIA; FEMALE; FLUOROBENZENES; GENE KNOCKDOWN TECHNIQUES; HUMANS; MALE; PHTHALAZINES; POLY(ADP-RIBOSE) POLYMERASES;

EID: 84921475346     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2014.12.003     Document Type: Article

References (66)

1. Hellman S., Vokes E.E. Advancing current treatments for cancer. Sci. Am. 1996, 275:118-123.
2. Hartwell L.H., Szankasi P., Roberts C.J., Murray A.W., Friend S.H. Integrating genetic approaches into the discovery of anticancer drugs. Science 1997, 278:1064-1068.
3. Kaelin W.G. The concept of synthetic lethality in the context of anticancer therapy. Nat. Rev. Cancer 2005, 5:689-698.
4. Chan D.A., Giaccia A.J. Harnessing synthetic lethal interactions in anticancer drug discovery. Nat. Rev. Drug Discov. 2011, 10:351-364.
5. Menissier-de M.J., Molinete M., Gradwohl G., Simonin F., de Murcia G. Zinc-binding domain of poly(ADP-ribose)polymerase participates in the recognition of single strand breaks on DNA. J. Mol. Biol. 1989, 210:229-233.
6. Schreiber V., Dantzer F., Ame J.C., de Murcia G. Poly(ADP-ribose): novel functions for an old molecule. Nat. Rev. Mol. Cell Biol. 2006, 7:517-528.
7. 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.
8. 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., Martin N.M., Jackson S.P., Smith G.C., Ashworth A. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005, 434:917-921.
9. Moynahan M.E., Chiu J.W., Koller B.H., Jasin M. Brca1 controls homology-directed DNA repair. Mol. Cell 1999, 4:511-518.
10. Moynahan M.E., Pierce A.J., Jasin M. BRCA2 is required for homology-directed repair of chromosomal breaks. Mol. Cell 2001, 7:263-272.
11. Strom C.E., Johansson F., Uhlen M., Szigyarto C.A., Erixon K., Helleday T. Poly (ADP-ribose) polymerase (PARP) is not involved in base excision repair but PARP inhibition traps a single-strand intermediate. Nucleic Acids Res. 2011, 39:3166-3175.
12. Helleday T. The underlying mechanism for the PARP and BRCA synthetic lethality: clearing up the misunderstandings. Mol. Oncol. 2011, 5:387-393.
13. Murai J., Huang S.Y., Das B.B., Renaud A., Zhang Y., Doroshow J.H., Ji J., Takeda S., Pommier Y. Trapping of PARP1 and PARP2 by clinical PARP inhibitors. Cancer Res. 2012, 72:5588-5599.
14. 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.
15. Yang Y.G., Cortes U., Patnaik S., Jasin M., Wang Z.Q. Ablation of PARP-1 does not interfere with the repair of DNA double-strand breaks, but compromises the reactivation of stalled replication forks. Oncogene 2004, 23:3872-3882.
16. Fong P.C., Boss D.S., Yap T.A., Tutt A., Wu P., Mergui-Roelvink M., Mortimer P., Swaisland H., Lau A., O'Connor M.J., Ashworth A., Carmichael J., Kaye S.B., Schellens J.H., Bono J.S.de Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N. Engl. J. Med. 2009, 361:123-134.
17. Buisson R., Dion-Cote A.M., Coulombe Y., Launay H., Cai H., Stasiak A.Z., Stasiak A., Xia B., Masson J.Y. Cooperation of breast cancer proteins PALB2 and piccolo BRCA2 in stimulating homologous recombination. Nat. Struct. Mol. Biol. 2010, 17:1247-1254.
18. Min A., Im S.A., Yoon Y.K., Song S.H., Nam H.J., Hur H.S., Kim H.P., Lee K.H., Han S.W., Oh D.Y., Kim T.Y., O'Connor M.J., Kim W.H., Bang Y.J. RAD51C-deficient cancer cells are highly sensitive to the PARP inhibitor olaparib. Mol. Cancer Ther. 2013, 12:865-877.
19. Kim Y., Spitz G.S., Veturi U., Lach F.P., Auerbach A.D., Smogorzewska A. Regulation of multiple DNA repair pathways by the Fanconi anemia protein SLX4. Blood 2013, 121:54-63.
20. Howlett N.G., Taniguchi T., Olson S., Cox B., Waisfisz Q., De Die-Smulders C., Persky N., Grompe M., Joenje H., Pals G., Ikeda H., Fox E.A., D'Andrea A.D. Biallelic inactivation of BRCA2 in Fanconi anemia. Science 2002, 297:606-609.
21. Xia B., Dorsman J.C., Ameziane N., de V.Y., Rooimans M.A., Sheng Q., Pals G., Errami A., Gluckman E., Llera J., Wang W., Livingston D.M., Joenje H., de Winter J.P. Fanconi anemia is associated with a defect in the BRCA2 partner PALB2. Nat. Genet. 2007, 39:159-161.
22. Reid S., Schindler D., Hanenberg H., Barker K., Hanks S., Kalb R., Neveling K., Kelly P., Seal S., Freund M., Wurm M., Batish S.D., Lach F.P., Yetgin S., Neitzel H., Ariffin H., Tischkowitz M., Mathew C.G., Auerbach A.D., Rahman N. Biallelic mutations in PALB2 cause Fanconi anemia subtype FA-N and predispose to childhood cancer. Nat. Genet. 2007, 39:162-164.
23. Kim Y., Lach F.P., Desetty R., Hanenberg H., Auerbach A.D., Smogorzewska A. Mutations of the SLX4 gene in Fanconi anemia. Nat. Genet. 2011, 43:142-146.
24. Stoepker C., Hain K., Schuster B., Hilhorst-Hofstee Y., Rooimans M.A., Steltenpool J., Oostra A.B., Eirich K., Korthof E.T., Nieuwint A.W., Jaspers N.G., Bettecken T., Joenje H., Schindler D., Rouse J., de Winter J.P. SLX4, a coordinator of structure-specific endonucleases, is mutated in a new Fanconi anemia subtype. Nat. Genet. 2011, 43:138-141.
25. Vaz F., Hanenberg H., Schuster B., Barker K., Wiek C., Erven V., Neveling K., Endt D., Kesterton I., Autore F., Fraternali F., Freund M., Hartmann L., Grimwade D., Roberts R.G., Schaal H., Mohammed S., Rahman N., Schindler D., Mathew C.G. Mutation of the RAD51C gene in a Fanconi anemia-like disorder. Nat. Genet. 2010, 42:406-409.
26. Kottemann M.C., Smogorzewska A. Fanconi anaemia and the repair of Watson and Crick DNA crosslinks. Nature 2013, 493:356-363.
27. Bogliolo M., Schuster B., Stoepker C., Derkunt B., Su Y., Raams A., Trujillo J.P., Minguillon J., Ramirez M.J., Pujol R., Casado J.A., Banos R., Rio P., Knies K., Zuniga S., Benitez J., Bueren J.A., Jaspers N.G., Scharer O.D., de Winter J.P., Schindler D., Surralles J. Mutations in ERCC4, encoding the DNA-repair endonuclease XPF, cause Fanconi anemia. Am. J. Hum. Genet. 2013, 92:800-806.
28. Schwab R.A., Blackford A.N., Niedzwiedz W. ATR activation and replication fork restart are defective in FANCM-deficient cells. EMBO J. 2010, 29:806-818.
29. Singh T.R., Bakker S.T., Agarwal S., Jansen M., Grassman E., Godthelp B.C., Ali A.M., Du C.H., Rooimans M.A., Fan Q., Wahengbam K., Steltenpool J., Andreassen P.R., Williams D.A., Joenje H., de Winter J.P., Meetei A.R. Impaired FANCD2 monoubiquitination and hypersensitivity to camptothecin uniquely characterize Fanconi anemia complementation group M. Blood 2009, 114:174-180.
30. van der Lelij P., Chrzanowska K.H., Godthelp B.C., Rooimans M.A., Oostra A.B., Stumm M., Zdzienicka M.Z., Joenje H., de Winter J.P. Warsaw breakage syndrome, a cohesinopathy associated with mutations in the XPD helicase family member DDX11/ChlR1. Am. J. Hum. Genet. 2010, 86:262-266.
31. Joenje H., Lo ten Foe J.R., Oostra A.B., van Berkel C.G., Rooimans M.A., Schroeder-Kurth T., Wegner R.D., Gille J.J., Buchwald M., Arwert F. Classification of Fanconi anemia patients by complementation analysis: evidence for a fifth genetic subtype. Blood 1995, 86:2156-2160.
32. Wijker M., Morgan N.V., Herterich S., van Berkel C.G., Tipping A.J., Gross H.J., Gille J.J., Pals G., Savino M., Altay C., Mohan S., Dokal I., Cavenagh J., Marsh J., van W.M., Ortega J.J., Schuler D., Samochatova E., Karwacki M., Bekassy A.N., Abecasis M., Ebell W., Kwee M.L., de R.T., Mathew C.G. Heterogeneous spectrum of mutations in the Fanconi anaemia group A gene. Eur. J. Hum. Genet. 1999, 7:52-59.
33. Joenje H., Levitus M., Waisfisz Q., D'Andrea A., Garcia-Higuera I., Pearson T., van Berkel C.G., Rooimans M.A., Morgan N., Mathew C.G., Arwert F. Complementation analysis in Fanconi anemia: assignment of the reference FA-H patient to group A. Am. J. Hum. Genet. 2000, 67:759-762.
34. Meetei A.R., Levitus M., Xue Y., Medhurst A.L., Zwaan M., Ling C., Rooimans M.A., Bier P., Hoatlin M., Pals G., de Winter J.P., Wang W., Joenje H. X-linked inheritance of Fanconi anemia complementation group B. Nat. Genet. 2004, 36:1219-1224.
35. de Winter J.P., van der Weel L., de G.J., Stone S., Waisfisz Q., Arwert F., Scheper R.J., Kruyt F.A., Hoatlin M.E., Joenje H. The Fanconi anemia protein FANCF forms a nuclear complex with FANCA, FANCC and FANCG. Hum. Mol. Genet. 2000, 9:2665-2674.
36. Kalb R., Neveling K., Hoehn H., Schneider H., Linka Y., Batish S.D., Hunt C., Berwick M., Callen E., Surralles J., Casado J.A., Bueren J., Dasi A., Soulier J., Gluckman E., Zwaan C.M., van S.R., Pals G., de Winter J.P., Joenje H., Grompe M., Auerbach A.D., Hanenberg H., Schindler D. Hypomorphic mutations in the gene encoding a key Fanconi anemia protein, FANCD2, sustain a significant group of FA-D2 patients with severe phenotype. Am. J. Hum. Genet. 2007, 80:895-910.
37. Dorsman J.C., Levitus M., Rockx D., Rooimans M.A., Oostra A.B., Haitjema A., Bakker S.T., Steltenpool J., Schuler D., Mohan S., Schindler D., Arwert F., Pals G., Mathew C.G., Waisfisz Q., de Winter J.P., Joenje H. Identification of the Fanconi anemia complementation group I gene, FANCI. Cell. Oncol. 2007, 29:211-218.
38. Meetei A.R., de Winter J.P., Medhurst A.L., Wallisch M., Waisfisz Q., van de Vrugt H.J., Oostra A.B., Yan Z., Ling C., Bishop C.E., Hoatlin M.E., Joenje H., Wang W. A novel ubiquitin ligase is deficient in Fanconi anemia. Nat. Genet. 2003, 35:165-170.
39. Meetei A.R., Medhurst A.L., Ling C., Xue Y., Singh T.R., Bier P., Steltenpool J., Stone S., Dokal I., Mathew C.G., Hoatlin M., Joenje H., de Winter J.P., Wang W. A human ortholog of archaeal DNA repair protein Hef is defective in Fanconi anemia complementation group M. Nat. Genet. 2005, 37:958-963.
40. Levitus M., Waisfisz Q., Godthelp B.C., de V.Y., Hussain S., Wiegant W.W., Elghalbzouri-Maghrani E., Steltenpool J., Rooimans M.A., Pals G., Arwert F., Mathew C.G., Zdzienicka M.Z., Hiom K., de Winter J.P., Joenje H. The DNA helicase BRIP1 is defective in Fanconi anemia complementation group J. Nat. Genet. 2005, 37:934-935.
41. Vega H., Waisfisz Q., Gordillo M., Sakai N., Yanagihara I., Yamada M., van G.D., Kayserili H., Xu C., Ozono K., Jabs E.W., Inui K., Joenje H. Roberts syndrome is caused by mutations in ESCO2, a human homolog of yeast ECO1 that is essential for the establishment of sister chromatid cohesion. Nat. Genet. 2005, 37:468-470.
42. Vrouwe M.G., Elghalbzouri-Maghrani E., Meijers M., Schouten P., Godthelp B.C., Bhuiyan Z.A., Redeker E.J., Mannens M.M., Mullenders L.H., Pastink A., Darroudi F. Increased DNA damage sensitivity of Cornelia de Lange syndrome cells: evidence for impaired recombinational repair. Hum. Mol. Genet. 2007, 16:1478-1487.
43. van Zeeburg H.J., Snijders P.J., Pals G., Hermsen M.A., Rooimans M.A., Bagby G., Soulier J., Gluckman E., Wennerberg J., Leemans C.R., Joenje H., Brakenhoff R.H. Generation and molecular characterization of head and neck squamous cell lines of fanconi anemia patients. Cancer Res. 2005, 65:1271-1276.
44. Marston N.J., Richards W.J., Hughes D., Bertwistle D., Marshall C.J., Ashworth A. Interaction between the product of the breast cancer susceptibility gene BRCA2 and DSS1, a protein functionally conserved from yeast to mammals. Mol. Cell. Biol. 1999, 19:4633-4642.
45. Yang H., Jeffrey P.D., Miller J., Kinnucan E., Sun Y., Thoma N.H., Zheng N., Chen P.L., Lee W.H., Pavletich N.P. BRCA2 function in DNA binding and recombination from a BRCA2-DSS1-ssDNA structure. Science 2002, 297:1837-1848.
46. Gudmundsdottir K., Lord C.J., Witt E., Tutt A.N., Ashworth A. DSS1 is required for RAD51 focus formation and genomic stability in mammalian cells. EMBO Rep. 2004, 5:989-993.
47. Siaud N., Barbera M.A., Egashira A., Lam I., Christ N., Schlacher K., Xia B., Jasin M. Plasticity of BRCA2 function in homologous recombination: genetic interactions of the PALB2 and DNA binding domains. PLoS Genet. 2011, 7:e1002409.
48. Wong A.K., Pero R., Ormonde P.A., Tavtigian S.V., Bartel P.L. RAD51 interacts with the evolutionarily conserved BRC motifs in the human breast cancer susceptibility gene brca2. J. Biol. Chem. 1997, 272:31941-31944.
49. Yuan S.S., Lee S.Y., Chen G., Song M., Tomlinson G.E., Lee E.Y. BRCA2 is required for ionizing radiation-induced assembly of Rad51 complex in vivo. Cancer Res. 1999, 59:3547-3551.
50. Hirsch B., Shimamura A., Moreau L., Baldinger S., Hag-alshiekh M., Bostrom B., Sencer S., D'Andrea A.D. Association of biallelic BRCA2/FANCD1 mutations with spontaneous chromosomal instability and solid tumors of childhood. Blood 2004, 103:2554-2559.
51. Wagner J.E., Tolar J., Levran O., Scholl T., Deffenbaugh A., Satagopan J., Ben-Porat L., Mah K., Batish S.D., Kutler D.I., MacMillan M.L., Hanenberg H., Auerbach A.D. Germline mutations in BRCA2: shared genetic susceptibility to breast cancer, early onset leukemia, and Fanconi anemia. Blood 2004, 103:3226-3229.
52. Mazoyer S., Dunning A.M., Serova O., Dearden J., Puget N., Healey C.S., Gayther S.A., Mangion J., Stratton M.R., Lynch H.T., Goldgar D.E., Ponder B.A., Lenoir G.M. A polymorphic stop codon in BRCA2. Nat. Genet. 1996, 14:253-254.
53. van der Lelij P., Oostra A.B., Rooimans M.A., Joenje H., de Winter J.P. Diagnostic overlap between Fanconi anemia and the cohesinopathies: Roberts syndrome and Warsaw breakage syndrome. Anemia 2010, 2010:565268.
54. Liu J., Krantz I.D. Cohesin and human disease. Annu. Rev. Genomics Hum. Genet. 2008, 9:303-320.
55. Xia B., Sheng Q., Nakanishi K., Ohashi A., Wu J., Christ N., Liu X., Jasin M., Couch F.J., Livingston D.M. Control of BRCA2 cellular and clinical functions by a nuclear partner, PALB2. Mol. Cell 2006, 22:719-729.
56. McCabe N., Turner N.C., Lord C.J., Kluzek K., Bialkowska A., Swift S., Giavara S., O'Connor M.J., Tutt A.N., Zdzienicka M.Z., Smith G.C., Ashworth A. Deficiency in the repair of DNA damage by homologous recombination and sensitivity to poly(ADP-ribose) polymerase inhibition. Cancer Res. 2006, 66:8109-8115.
57. Hsiang Y.H., Lihou M.G., Liu L.F. Arrest of replication forks by drug-stabilized topoisomerase I-DNA cleavable complexes as a mechanism of cell killing by camptothecin. Cancer Res. 1989, 49:5077-5082.
58. Pommier Y. Topoisomerase I inhibitors: camptothecins and beyond. Nat. Rev. Cancer 2006, 6:789-802.
59. Blackford A.N., Schwab R.A., Nieminuszczy J., Deans A.J., West S.C., Niedzwiedz W. The DNA translocase activity of FANCM protects stalled replication forks. Hum. Mol. Genet. 2012, 21:2005-2016.
60. Deans A.J., West S.C. FANCM connects the genome instability disorders Bloom's syndrome and Fanconi anemia. Mol. Cell 2009, 36:943-953.
61. Collis S.J., Ciccia A., Deans A.J., Horejsi Z., Martin J.S., Maslen S.L., Skehel J.M., Elledge S.J., West S.C., Boulton S.J. FANCM and FAAP24 function in ATR-mediated checkpoint signaling independently of the Fanconi anemia core complex. Mol. Cell 2008, 32:313-324.
62. Luke-Glaser S., Luke B., Grossi S., Constantinou A. FANCM regulates DNA chain elongation and is stabilized by S-phase checkpoint signalling. EMBO J. 2010, 29:795-805.
63. Turner N.C., Lord C.J., Iorns E., Brough R., Swift S., Elliott R., Rayter S., Tutt A.N., Ashworth A. A synthetic lethal siRNA screen identifying genes mediating sensitivity to a PARP inhibitor. EMBO J. 2008, 27:1368-1377.
64. Lengronne A., McIntyre J., Katou Y., Kanoh Y., Hopfner K.P., Shirahige K., Uhlmann F. Establishment of sister chromatid cohesion at the S. cerevisiae replication fork. Mol. Cell 2006, 23:787-799.
65. Leman A.R., Noguchi C., Lee C.Y., Noguchi E. Human timeless and tipin stabilize replication forks and facilitate sister-chromatid cohesion. J. Cell Sci. 2010, 123:660-670.
66. Farina A., Shin J.H., Kim D.H., Bermudez V.P., Kelman Z., Seo Y.S., Hurwitz J. Studies with the human cohesin establishment factor, ChlR1. Association of ChlR1 with Ctf18-RFC and Fen1. J. Biol. Chem. 2008, 283:20925-20936.