BRCA1 and HSP90 cooperate in homologous and non-homologous DNA double-strand-break repair and G2/M checkpoint activation

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

Volumn 109, Issue 34, 2012, Pages 13650-13655

  Stecklein, Shane R ^a,b   Kumaraswamy, Easwari ^a,b   Behbod, Fariba ^a,b   Wang, Wenjia ^a,b   Chaguturu, Vamsee ^b   Harlan Williams, Lisa M ^b,c   Jensen, Roy A ^a,b,c  

^a Department of Pathology and Laboratory Medicine ^*  (United States)

^b UNIVERSITY OF KANSAS CANCER CENTER   (United States)

^c UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

Chemosensitivity; DNA repair

Indexed keywords

BRCA1 PROTEIN; DOUBLE STRANDED DNA; FANCONI ANEMIA GROUP A PROTEIN; HEAT SHOCK PROTEIN 90; TANESPIMYCIN;

ARTICLE; BREAST CANCER; CANCER PROGNOSIS; CANCER RESISTANCE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL SURVIVAL; CONTROLLED STUDY; DNA CROSS LINKING; DNA REPAIR; DRUG RESPONSE; DRUG SENSITIVITY; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; IN VITRO STUDY; IONIZING RADIATION; M PHASE CELL CYCLE CHECKPOINT; MITOSIS; OVARY CANCER; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; RECOMBINATION REPAIR; TUMOR SUPPRESSOR GENE; UBIQUITINATION;

ANTINEOPLASTIC AGENTS; BENZOQUINONES; BRCA1 PROTEIN; CELL DIVISION; CELL LINE, TUMOR; CROSS-LINKING REAGENTS; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DRUG DESIGN; DRUG SCREENING ASSAYS, ANTITUMOR; G2 PHASE; HELA CELLS; HOMOLOGOUS RECOMBINATION; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LACTAMS, MACROCYCLIC;

EID: 84865306252     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1203326109     Document Type: Article

References (50)

1. Ford D, Easton DF, Bishop DT, Narod SA, Goldgar DE; Breast Cancer Linkage Consortium (1994) Risks of cancer in BRCA1-mutation carriers. Lancet 343:692-695.
2. King MC, Marks JH, Mandell JB; New York Breast Cancer Study Group (2003) Breast and ovarian cancer risks due to inherited mutations in BRCA1 and BRCA2. Science 302:643-646.
3. Thompson ME, Jensen RA, Obermiller PS, Page DL, Holt JT (1995) Decreased expression of BRCA1 accelerates growth and is often present during sporadic breast cancer progression. Nat Genet 9:444-450.
4. Hall JM, et al. (1990) Linkage of early-onset familial breast cancer to chromosome 17q21. Science 250:1684-1689.
5. Friedman LS, et al. (1994) Confirmation of BRCA1 by analysis of germline mutations linked to breast and ovarian cancer in ten families. Nat Genet 8:399-404.
6. Huen MS, Sy SM, Chen J (2010) BRCA1 and its toolbox for the maintenance of genome integrity. Nat Rev Mol Cell Biol 11:138-148.
7. Cortez D, Wang Y, Qin J, Elledge SJ (1999) Requirement of ATM-dependent phosphorylation of brca1 in the DNA damage response to double-strand breaks. Science 286:1162-1166.
8. Yarden RI, Pardo-Reoyo S, Sgagias M, Cowan KH, Brody LC (2002) BRCA1 regulates the G2/M checkpoint by activating Chk1 kinase upon DNA damage. Nat Genet 30:285-289.
9. Abbott DW, et al. (1999) BRCA1 expression restores radiation resistance in BRCA1-defective cancer cells through enhancement of transcription-coupled DNA repair. J Biol Chem 274:18808-18812.
10. Scata KA, El-Deiry WS (2007) p53, BRCA1 and breast Cancer chemoresistance. Adv Exp Med Biol 608:70-86.
11. Bhattacharyya A, Ear US, Koller BH, Weichselbaum RR, Bishop DK (2000) The breast cancer susceptibility gene BRCA1 is required for subnuclear assembly of Rad51 and survival following treatment with the DNA cross-linking agent cisplatin. J Biol Chem 275:23899-23903.
12. Husain A, He G, Venkatraman ES, Spriggs DR (1998) BRCA1 up-regulation is associated with repair-mediated resistance to cis-diamminedichloroplatinum(II). Cancer Res 58:1120-1123.
13. Silver DP, et al. (2010) Efficacy of neoadjuvant Cisplatin in triple-negative breast cancer. J Clin Oncol 28:1145-1153.
14. Adhikari S, et al. (2008) Targeting base excision repair for chemosensitization. Anticancer Agents Med Chem 8:351-357.
15. Fong PC, et al. (2010) Poly(adp)-ribose polymerase inhibition: Frequent durable responses in BRCA carrier ovarian cancer correlating with platinum-free interval. J Clin Oncol 28:2512-2519.
16. Turner NC, et al. (2007) BRCA1 dysfunction in sporadic basal-like breast cancer. Oncogene 26:2126-2132.
17. Swisher EM, et al. (2008) Secondary BRCA1 mutations in BRCA1-mutated ovarian carcinomas with platinum resistance. Cancer Res 68:2581-2586.
18. Ashworth A (2008) Drug resistance caused by reversion mutation. Cancer Res 68:10021-10023.
19. Chen X, Arciero CA, Godwin AK (2006) BRCA1-associated complexes: New targets to overcome breast cancer radiation resistance. Expert Rev Anticancer Ther 6:187-196.
20. Whitesell L, Lindquist SL (2005) HSP90 and the chaperoning of cancer. Nat Rev Cancer 5:761-772.
21. Blagg BS, Kerr TD (2006) Hsp90 inhibitors: Small molecules that transform the Hsp90 protein folding machinery into a catalyst for protein degradation. Med Res Rev 26:310-338.
22. Kim YS, et al. (2009) Update on Hsp90 inhibitors in clinical trial. Curr Top Med Chem 9:1479-1492.
23. Camphausen K, Tofilon PJ (2007) Inhibition of Hsp90: A multitarget approach to radiosensitization. Clin Cancer Res 13:4326-4330.
24. Dungey FA, Caldecott KW, Chalmers AJ (2009) Enhanced radiosensitization of human glioma cells by combining inhibition of poly(ADP-ribose) polymerase with inhibition of heat shock protein 90. Mol Cancer Ther 8:2243-2254.
25. Arlander SJ, et al. (2003) Hsp90 inhibition depletes Chk1 and sensitizes tumor cells to replication stress. J Biol Chem 278:52572-52577.
26. Dote H, Burgan WE, Camphausen K, Tofilon PJ (2006) Inhibition of hsp90 compromises the DNA damage response to radiation. Cancer Res 66:9211-9220.
27. Oda T, Hayano T, Miyaso H, Takahashi N, Yamashita T (2007) Hsp90 regulates the Fanconi anemia DNA damage response pathway. Blood 109:5016-5026.
28. Chen L, Nievera CJ, Lee AY, Wu X (2008) Cell cycle-dependent complex formation of BRCA1.CtIP.MRN is important for DNA double-strand break repair. J Biol Chem 283:7713-7720.
29. D'Andrea AD, Grompe M (2003) The Fanconi anaemia/BRCA pathway. Nat Rev Cancer 3:23-34.
30. Folias A, et al. (2002) BRCA1 interacts directly with the Fanconi anemia protein FANCA. Hum Mol Genet 11:2591-2597.
31. Zhang F, Fan Q, Ren K, Andreassen PR (2009) PALB2 functionally connects the breast cancer susceptibility proteins BRCA1 and BRCA2. Mol Cancer Res 7:1110-1118.
32. Zhong Q, et al. (1999) Association of BRCA1 with the hRad50-hMre11-p95 complex and the DNA damage response. Science 285:747-750.
33. McCollum AK, et al. (2008) Cisplatin abrogates the geldanamycin-induced heat shock response. Mol Cancer Ther 7:3256-3264.
34. Joukov V, Chen J, Fox EA, Green JB, Livingston DM (2001) Functional communication between endogenous BRCA1 and its partner, BARD1, during Xenopus laevis development. Proc Natl Acad Sci USA 98:12078-12083.
35. McCarthy EE, Celebi JT, Baer R, Ludwig T (2003) Loss of Bard1, the heterodimeric partner of the Brca1 tumor suppressor, results in early embryonic lethality and chromosomal instability. Mol Cell Biol 23:5056-5063.
36. Choudhury AD, Xu H, Baer R (2004) Ubiquitination and proteasomal degradation of the BRCA1 tumor suppressor is regulated during cell cycle progression. J Biol Chem 279:33909-33918.
37. Shrivastav M, De Haro LP, Nickoloff JA (2008) Regulation of DNA double-strand break repair pathway choice. Cell Res 18:134-147.
38. Nakanishi K, et al. (2005) Human Fanconi anemia monoubiquitination pathway promotes homologous DNA repair. Proc Natl Acad Sci USA 102:1110-1115.
39. Kachhap SK, Vetale SP, Dange P, Ghosh SN (2001) Reduced expression of the BRCA1 gene and increased chromosomal instability in MCF-7 cell line. Cell Biol Int 25:547-551.
40. Ransburgh DJ, Chiba N, Ishioka C, Toland AE, Parvin JD (2010) Identification of breast tumor mutations in BRCA1 that abolish its function in homologous DNA recombination. Cancer Res 70:988-995.
41. Noguchi M, et al. (2006) Inhibition of homologous recombination repair in irradiated tumor cells pretreated with Hsp90 inhibitor 17-allylamino-17- demethoxygeldanamycin. Biochem Biophys Res Commun 351:658-663.
42. Chou TC, Talalay P (1983) Analysis of combined drug effects: A new look at a very old problem. Trends Pharmacol Sci 4:450-454.
43. Chou TC, Talalay P (1984) Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 22:27-55.
44. Xian Ma Y, et al. (2003) Role of BRCA1 in heat shock response. Oncogene 22:10-27.
45. Guervilly JH, Macé-Aimé G, Rosselli F (2008) Loss of CHK1 function impedes DNA damage-induced FANCD2 monoubiquitination but normalizes the abnormal G2 arrest in Fanconi anemia. Hum Mol Genet 17:679-689.
46. Zhuang J, et al. (2006) Checkpoint kinase 2-mediated phosphorylation of BRCA1 regulates the fidelity of nonhomologous end-joining. Cancer Res 66:1401-1408.
47. Wei L, et al. (2008) Rapid recruitment of BRCA1 to DNA double-strand breaks is dependent on its association with Ku80. Mol Cell Biol 28:7380-7393.
48. Bau DT, et al. (2004) Breast cancer risk and the DNA double-strand break end-joining capacity of nonhomologous end-joining genes are affected by BRCA1. Cancer Res 64:5013-5019.
49. Mérel P, Prieur A, Pfeiffer P, Delattre O (2002) Absence of major defects in non-homologous DNA end joining in human breast cancer cell lines. Oncogene 21:5654-5659.
50. Chiba N, Parvin JD (2002) The BRCA1 and BARD1 association with the RNA polymerase II holoenzyme. Cancer Res 62:4222-4228.