Histone deacetylase inhibitor treatment induces 'BRCAness' and synergistic lethality with PARP inhibitor and cisplatin against human triple negative breast cancer cells

Oncotarget

Volumn 5, Issue 14, 2014, Pages 5637-5650

  Ha, Kyungsoo ^a   Fiskus, Warren ^b   Choi, Dong Soon ^b   Bhaskara, Srividya ^c   Cerchietti, Leandro ^d   Devaraj, Santhana G T ^b   Shah, Bhavin ^b   Sharma, Sunil ^c   Chang, Jenny C ^b   Melnick, Ari M ^d   Hiebert, Scott ^e   Bhalla, Kapil N ^b  

^a AUGUSTA UNIVERSITY   (United States)

^b HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF UTAH   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

^e VANDERBILT UNIVERSITY   (United States)

Author keywords

BRCAness; HDAC inhibitor; PARP inhibitor; Triple Negative Breast Cancer

Indexed keywords

ATR PROTEIN; BRCA1 PROTEIN; CHECKPOINT KINASE 1; CISPLATIN; HEAT SHOCK PROTEIN 90; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE INHIBITOR; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; PANOBINOSTAT; RAD52 PROTEIN; REACTIVE OXYGEN METABOLITE; VELIPARIB; VORINOSTAT; ANTINEOPLASTIC AGENT; ATM PROTEIN; ATR PROTEIN, HUMAN; BRCA1 PROTEIN, HUMAN; ENZYME INHIBITOR; HYDROXAMIC ACID; INDOLE DERIVATIVE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN KINASE;

ACETYLATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER CELL LINE; CANCER CELL DESTRUCTION; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CANCER SURVIVAL; CONTROLLED STUDY; DNA STRAND BREAKAGE; DRUG EFFECT; DRUG MECHANISM; DRUG POTENTIATION; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MONOTHERAPY; MOUSE; NONHUMAN; PROTEIN DEPLETION; PROTEIN EXPRESSION; TRIPLE NEGATIVE BREAST CANCER; TUMOR XENOGRAFT; ANIMAL; ANTAGONISTS AND INHIBITORS; DNA DAMAGE; DRUG EFFECTS; DRUG SCREENING; GENE SILENCING; GENETICS; HELA CELL LINE; MCF 7 CELL LINE; METABOLISM; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; BRCA1 PROTEIN; CELL LINE, TUMOR; CISPLATIN; DNA DAMAGE; DRUG SYNERGISM; ENZYME INHIBITORS; FEMALE; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HISTONE DEACETYLASE INHIBITORS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; HYDROXAMIC ACIDS; INDOLES; MCF-7 CELLS; MICE; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN KINASES; REACTIVE OXYGEN SPECIES; TRIPLE NEGATIVE BREAST NEOPLASMS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84906217436     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2154     Document Type: Article

References (51)

1. Ciccia A, Elledge SJ. The DNA damage response: making it safe to play with knives. Mol Cell. 2010;40:179-204.
2. Lord CJ, Ashworth A. The DNA damage response and cancer therapy. Nature. 2012;481:287-94.
3. Furgason JM, Bahassi el M. Targeting DNA repair mechanisms in cancer. Pharmacol Ther. 2013;137:298-308.
4. Smith J, Tho LM, Xu N, Gillespie DA. The ATM-Chk2 and ATR-Chk1 pathways in DNA damage signaling and cancer. Adv Cancer Res. 2010;108:73-112.
5. Nam EA, Cortez D. ATR signalling: more than meeting at the fork. Biochem J. 2011;436:527-36.
6. Ha K, Fiskus W, Rao R, Balusu R, Venkannagari S, Nalabothula NR, and Bhalla KN. Hsp90 inhibitor-mediated disruption of chaperone association of ATR with hsp90 sensitizes cancer cells to DNA damage. Mol Cancer Ther. 2011;10:1194-206.
7. Stecklein SR, Kumaraswamy E, Behbod F, Wang W, Chaguturu V, Harlan-Williams LM, and Jensen RA. BRCA1 and HSP90 cooperate in homologous and non-homologous DNA double-strand-break repair and G2/M checkpoint activation. Proc Natl Acad Sci. 2012;109:13650-5.
8. Bouwman P, Jonkers J. The effects of deregulated DNA damage signalling on cancer chemotherapy response and resistance. Nat Rev Cancer. 2012;12:587-98.
9. Huntoon CJ, Flatten KS, Wahner Hendrickson AE, Huehls AM, Sutor SL, Kaufmann SH, and Karnitz LM. ATR inhibition broadly sensitizes ovarian cancer cells to chemotherapy independent of BRCA status. Cancer Res. 2013;73:3683-91.
10. Gibson BA, Kraus WL. New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat Rev Mol Cell Biol. 2012;13:411-24.
11. Rouleau M, Patel A, Hendzel MJ, Kaufmann SH, Poirier GG. PARP inhibition: PARP1 and beyond. Nat Rev Cancer. 2010;10:293-301.
12. Horton JK, Wilson SH. Predicting enhanced cell killing through PARP inhibition. Mol Cancer Res. 2013;11:13-8.
13. Murai J, Huang SY, Das BB, Renaud A, Zhang Y, Doroshow JH, Ji J, Takeda S and Pommier Y. Trapping of PARP1 and PARP2 by Clinical PARP Inhibitors. Cancer Res. 2012;72:5588-99.
14. Patel AG, Sarkaria JN, Kaufmann SH. Nonhomologous end joining drives poly(ADP-ribose) polymerase (PARP) inhibitor lethality in homologous recombination-deficient cells. Proc Natl Acad Sci 2011;108:3046-11.
15. Turner NC, Reis-Filho JS. Tackling the diversity of triple-negative breast Cancer. Clin Cancer Res. 2013;19:6380-88.
16. Stevens KN, Vachon CM, Couch FJ. Genetic Susceptibility to triple-negative breast cancer. Cancer Res. 2013;73:2025-30.
17. Tutt A, Robson M, Garber JE, Domchek SM, Audeh MW, Weitzel JN, Friedlander M, Arun B, Loman N, Schmutzler RK, Wardley A, Mitchell G, Earl H, Wickens M and Carmichael J. Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and advanced breast cancer: a proof-of-concept trial. Lancet. 2010;376:235-44.
18. Clark CC, Weitzel JN, O'Connor TR. Enhancement of synthetic lethality via combinations of ABT-888, a PARP inhibitor, and carboplatin in vitro and in vivo using BRCA1 and BRCA2 isogenic models. Mol Cancer Ther. 2012;11:1948-58.
19. Turner N, Tutt A, Ashworth A. Hallmarks of 'BRCAness' in sporadic cancers. Nat Rev Cancer. 2004;4:814-819.
20. Hastak K, Alli E, Ford JM. Synergistic chemosensitivity of triple-negative breast cancer cell lines to poly(ADP-Ribose) polymerase inhibition, gemcitabine, and cisplatin. Cancer Res. 2010;70:7970-80
21. Stefansson OA, Villanueva A, Vidal A, Martí L, Esteller M. BRCA1 epigenetic inactivation predicts sensitivity to platinum-based chemotherapy in breast and ovarian cancer. Epigenetics. 2012;7:1225-9.
22. Chalasani P, Livingston R. Differential chemotherapeutic sensitivity for breast tumors with "BRCAness": a review. Oncologist. 2013;18:909-16.
23. Park SR, Chen A. Poly(Adenosine diphosphate-ribose) polymerase inhibitors in cancer treatment. Hematol Oncol Clin North Am. 2012 26:649-70.
24. Yang Y, Rao R, Shen J, Tang Y, Fiskus W, Nechtman J, Atadja P and Bhalla K. Role of acetylation and extracellular location of heat shock protein 90alpha in tumor cell invasion. Cancer Res. 2008;68:4833-42.
25. Minucci S, Pelicci PG. Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat. Rev. Cancer. 2006; 6:38-51.
26. Matthews GM, Newbold A, Johnstone RW. Intrinsic and extrinsic apoptotic pathway signaling as determinants of histone deacetylase inhibitor antitumor activity. Adv Cancer Res. 2012;116:165-97.
27. Hu Y, Lu W, Chen G, Zhang H, Jia Y, Wei Y, Yang H, Zhang W, Fiskus W, Bhalla K, Keating M, Huang P and Garcia-Manero G. Overcoming resistance to histone deacetylase inhibitors in human leukemia with the redox modulating compound beta-phenylethyl isothiocyanate. Blood. 2010;116:2732-41.
28. Fiskus W, Hembruff SL, Rao R, Sharma P, Balusu R, Venkannagari S, Smith JE, Peth K, Peiper SC and Bhalla KN. Co-treatment with vorinostat synergistically enhances activity of Aurora kinase inhibitor against human breast cancer cells. Breast Cancer Res Treat. 2012;135:433-44.
29. Bhaskara S, Chyla BJ, Amann JM, Knutson SK, Cortez D, Sun ZW, and Hiebert SW. Deletion of histone deacetylase 3 reveals critical roles in S phase progression and DNA damage control. Mol Cell. 2008;30:61-72.
30. Bhaskara S, Knutson SK, Jiang G, Chandrasekharan MB, Wilson AJ, Zheng S, Yenamandra A, Locke K, Yuan JL, Bonine-Summers AR, Wells CE, Kaiser JF, Washington MK, Zhao Z, Wagner FF, Sun ZW, et al. Hdac3 is essential for the maintenance of chromatin structure and genome stability. Cancer Cell. 2010;18:436-47.
31. Galluzzi L, Senovilla L, Vitale I, Michels J, Martins I, Kepp O, Castedo M and Kroemer G. Molecular mechanisms of cisplatin resistance. Oncogene. 2012;31:1869-83.
32. Bradner JE, West N, Grachan ML, Greenberg EF, Haggarty SJ, Warnow T, and Mazitschek R. Chemical phylogenetics of histone deacetylases. Nature Chem Biol. 2010;6:238-43.
33. Lee JH, Choy ML, Ngo L, Foster SS, Marks PA. Histone deacetylase inhibitor induces DNA damage, which normal but not transformed cells can repair. Proc Natnl Acad Sci. 2010;107:14639-44.
34. Kao GD, McKenna WG, Guenther MG, Muschel RJ, Lazar MA, Yen TJ. Histone deacetylase 4 interacts with 53BP1 to mediate the DNA damage response. J Cell Biol. 2003;160:1017-27.
35. Miller KM, Tjeertes JV, Coates J, Legube G, Polo SE, Britton S and Jackson SP. Human HDAC1 and HDAC2 function in the DNA-damage response to promote DNA nonhomologous end-joining. Nat Struct Mol Biol. 2010;17:1144-51.
36. Sun Z, Feng D, Fang B, Mullican SE, You SH, Lim HW, Everett LJ, Nabel CS, Li Y, Selvakumaran V, Won KJ, Lazar MA. Deacetylase-Independent Function of HDAC3 in Transcription and Metabolism Requires Nuclear Receptor Corepressor. Mol Cell. 2013;52:769-82.
37. Taniguchi T, Tischkowitz M, Ameziane N, Hodgson SV, Mathew CG, Joenje H, Mok SC and D'Andrea AD. Disruption of the Fanconi anemia-BRCA pathway in cisplatin-sensitive ovarian tumors. Nat Med. 2003;9:568-74.
38. Johnson N, Li YC, Walton ZE, Cheng KA, Li D, Rodig SJ, Moreau LA, Unitt C, Bronson RT, Thomas HD, Newell DR, D'Andrea AD, Curtin NJ, Wong KK and Shapiro GI. Compromised CDK1 activity sensitizes BRCA-proficient cancers to PARP inhibition. Nat Med. 2011;17:875-82.
39. Mendes-Pereira AM, Martin SA, Brough R, McCarthy A, Taylor JR, Kim JS, Waldman T, Lord CJ and Ashworth A. Synthetic lethal targeting of PTEN mutant cells with PARP inhibitors. EMBO Mol Med. 2009;1:315-22.
40. Juvekar A, Burga LN, Hu H, Lunsford EP, Ibrahim YH, Balmana J, Rajendran A, Papa A, Spencer K, Lyssiotis CA, Nardella C, Pandolfi PP, Baselga J, Scully R, Asara JM, Cantley LC, et al. Combining a PI3K inhibitor with a PARP inhibitor provides an effective therapy for BRCA1-related breast cancer. Cancer Discov. 2012;2:1048-63.
41. Rao R, Balusu R, Fiskus W, Mudunuru U, Venkannagari S, Chauhan L, Smith JE, Hembruff SL, Ha K, Atadja P and Bhalla KN. Combination of pan-histone deacetylase inhibitor and autophagy inhibitor exerts superior efficacy against triple-negative human breast cancer cells. Mol Cancer Ther. 2012;11:973-83.
42. Bunting SF, Callen E, Wong N, Chen HT, Polato F, Gunn A, Bothmer A, Feldhahn N, Fernandez-Capetillo O, Cao L, Xu X, Deng CX, Finkel T, Nussenzweig M, Stark JM and Nussenzweig A. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell. 2010;141:243-54.
43. Jaspers JE, Kersbergen A, Boon U, Sol W, van Deemter L, Zander SA, Drost R, Wientjens E, Ji J, Aly A, Doroshow JH, Cranston A, Martin NM, Lau A, O'Connor MJ, Ganesan S, et al. Loss of 53BP1 causes PARP inhibitor resistance in Brca1-mutated mouse mammary tumors. Cancer Discov. 2013;3:68-81.
44. Barber LJ, Sandhu S, Chen L, Campbell J, Kozarewa I, Fenwick K, Assiotis I, Rodrigues DN, Reis Filho JS, Moreno V, Mateo J, Molife LR, De Bono J, Kaye S, Lord CJ and Ashworth A. Secondary mutations in BRCA2 associated with clinical resistance to a PARP inhibitor. J Pathol. 2013;229:422-9.
45. Liu S, Ginestier C, Charafe-Jauffret E, Foco H, Kleer CG, Merajver SD, Dontu G, Wicha MS. BRCA1 regulates human mammary stem/progenitor cell fate. Proc Natl Acad Sci. 2008;105:1680-85.
46. Puppe J, Drost R, Liu X, Joosse SA, Evers B, Cornelissen-Steijger P, Nederlof P, Yu Q, Jonkers J, van Lohuizen M, Pietersen AM. BRCA1-deficient mammary tumor cells are dependent on EZH2 expression and sensitive to Polycomb Repressive Complex 2-inhibitor 3-deazaneplanocin A. Breast Cancer Res. 2009;R63
47. Summers AR, Fischer MA, Stengel KR, Zhao Y, Kaiser JF, Wells CE, Hunt A, Bhaskara S, Luzwick JW, Sampathi S, Chen X, Thompson MA, Cortez D, Hiebert SW. HDAC3 is essential for DNA replication in hematopoietic progenitor cells. J Clin Invest. 2013;123:3112-23
48. Fiskus W, Pranpat M, Balasis M, Herger B, Rao R, Chinnaiyan A, Atadja P, Bhalla K. Histone deacetylase inhibitors deplete enhancer of zeste 2 and associated polycomb repressive complex 2 proteins in human acute leukemia cells. Mol Cancer Ther. 2006; 5: 3096-104.
49. Balusu R, Fiskus W, Rao R, Chong DG, Nalluri S, Mudunuru U, Ma H, Chen L, Venkannagari S, Ha K, Abhyankar S, Williams C, McGuirk J, Khoury HJ, Ustun C and Bhalla KN. Targeting levels or oligomerization of nucleophosmin 1 induces differentiation and loss of survival of human AML cells with mutant NPM1. Blood. 2011;118:3096-106.
50. Venkannagari S, Fiskus W, Peth K, Atadja P, Hidalgo M, Maitra A, Bhalla KN. Superior efficacy of co-treatment with dual PI3K/mTOR inhibitor NVP-BEZ235 and pan-histone deacetylase inhibitor against human pancreatic cancer. Oncotarget. 2012; 3:1416-27.
51. Fiskus W, Verstovsek S, Manshouri T, Smith JE, Peth K, Abhyankar S, McGuirk J and Bhalla KN. Dual PI3K/AKT/mTOR inhibitor BEZ235 synergistically enhances the activity of JAK2 inhibitor against cultured and primary human myeloproliferative neoplasm cells. Mol Cancer Ther. 2013;12:577-88.