Combined histone deacetylase inhibition and tamoxifen induces apoptosis in tamoxifen-resistant breast cancer models, by reversing Bcl-2 overexpression

Breast Cancer Research

Volumn 17, Issue 1, 2015, Pages

  Raha, Paromita ^a   Thomas, Scott ^a   Thurn, K Ted ^a   Park, Jeenah ^a   Munster, Pamela N ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENTINOSTAT; ESTROGEN RECEPTOR; HISTONE DEACETYLASE; MYC PROTEIN; PANOBINOSTAT; PROGESTERONE RECEPTOR; PROTEIN BCL 2; PROTEIN P21; TAMOXIFEN; TAMOXIFEN CITRATE; VALPROIC ACID; VORINOSTAT; AFIMOXIFENE; ANTINEOPLASTIC AGENT; ESTRADIOL; FULVESTRANT; HISTONE DEACETYLASE INHIBITOR; LIGAND; PROTEIN BINDING; TRANSCRIPTOME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER COMBINATION CHEMOTHERAPY; CANCER RESISTANCE; CELL CYCLE ARREST; CELL PROLIFERATION; CELL SURVIVAL; CHEMOSENSITIVITY; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; ENZYME INHIBITION; EPIGENETICS; FEMALE; GENE EXPRESSION; GENETIC MANIPULATION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION; ANALOGS AND DERIVATIVES; ANIMAL; BREAST NEOPLASMS; DISEASE MODEL; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GENETICS; HUMAN; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, NEOPLASM; ESTRADIOL; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; LIGANDS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-BCL-2; PROTO-ONCOGENE PROTEINS C-MYC; PROTO-ONCOGENE PROTEINS P21(RAS); RECEPTORS, ESTROGEN; TAMOXIFEN; TRANSCRIPTION, GENETIC; TRANSCRIPTOME; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84928248328     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/s13058-015-0533-z     Document Type: Article

References (52)

1. Raha P, Thomas S, Munster PN. Epigenetic modulation: a novel therapeutic target for overcoming hormonal therapy resistance. Epigenomics. 2011;3:451-70.
2. Osborne CK, SchiffR. Mechanisms of endocrine resistance in breast cancer. Annu Rev Med. 2011;62:233-47.
3. Miller TW, Balko JM, Ghazoui Z, Dunbier A, Anderson H, Dowsett M, et al. A gene expression signature from human breast cancer cells with acquired hormone independence identifies MYC as a mediator of antiestrogen resistance. Clin Cancer Res. 2011;17:2024-34.
4. Pathiraja TN, Stearns V, Oesterreich S. Epigenetic regulation in estrogen receptor positive breast cancer-role in treatment response. J Mammary Gland Biol Neoplasia. 2010;15:35-47.
5. Kurebayashi J. Endocrine-resistant breast cancer: underlying mechanisms and strategies for overcoming resistance. Breast Cancer. 2003;10:112-9.
6. West AC, Johnstone RW. New and emerging HDAC inhibitors for cancer treatment. J Clin Invest. 2014;124:30-9.
7. Thurn KT, Thomas S, Moore A, Munster PN. Rational therapeutic combinations with histone deacetylase inhibitors for the treatment of cancer. Future Oncol. 2011;7:263-83.
8. Hirokawa Y, Arnold M, Nakajima H, Zalcberg J, Maruta H. Signal therapy of breast cancers by the HDAC inhibitor FK228 that blocks the activation of PAK1 and abrogates the tamoxifen-resistance. Cancer Biol Ther. 2005;4:956-60.
9. Jang ER, Lim SJ, Lee ES, Jeong G, Kim TY, Bang YJ, et al. The histone deacetylase inhibitor trichostatin A sensitizes estrogen receptor alpha-negative breast cancer cells to tamoxifen. Oncogene. 2004;23:1724-36.
10. 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.
11. Munster PN, Thurn KT, Thomas S, Raha P, Lacevic M, Miller A, et al. A phase II study of the histone deacetylase inhibitor vorinostat combined with tamoxifen for the treatment of patients with hormone therapy-resistant breast cancer. Br J Cancer. 2011;104:1828-35.
12. Yardley DA, Ismail-Khan RR, Melichar B, Lichinitser M, Munster PN, Klein PM, et al. Randomized phase II, double-blind, placebo-controlled study of exemestane with or without entinostat in postmenopausal women with locally recurrent or metastatic estrogen receptor-positive breast cancer progressing on treatment with a nonsteroidal aromatase inhibitor. J Clin Oncol. 2013;31:2128-35.
13. Thomas S, Thurn KT, Raha P, Chen S, Munster PN. Efficacy of histone deacetylase and estrogen receptor inhibition in breast cancer cells due to concerted down regulation of Akt. PLoS One. 2013;8:e68973.
14. Nawata H, Bronzert D, Lippman ME. Isolation and characterization of a tamoxifen-resistant cell line derived from MCF-7 human breast cancer cells. J Biol Chem. 1981;256:5016-21.
15. Nawata H, Chong MT, Bronzert D, Lippman ME. Estradiol-independent growth of a subline of MCF-7 human breast cancer cells in culture. J Biol Chem. 1981;256:6895-902.
16. Massarweh S, Osborne CK, Creighton CJ, Qin L, Tsimelzon A, Huang S, et al. Tamoxifen resistance in breast tumors is driven by growth factor receptor signaling with repression of classic estrogen receptor genomic function. Cancer Res. 2008;68:826-33.
17. Stone A, Valdes-Mora F, Gee JM, Farrow L, McClelland RA, Fiegl H, et al. Tamoxifen-induced epigenetic silencing of oestrogen-regulated genes in anti-hormone resistant breast cancer. PLoS One. 2012;7:e40466.
18. Thrane S, Lykkesfeldt AE, Larsen MS, Sorensen BS, Yde CW. Estrogen receptor alpha is the major driving factor for growth in tamoxifen-resistant breast cancer and supported by HER/ERK signaling. Breast Cancer Res Treat. 2013;139:71-80.
19. Adamo V, Iorfida M, Montalto E, Festa V, Garipoli C, Scimone A, et al. Overview and new strategies in metastatic breast cancer (MBC) for treatment of tamoxifen-resistant patients. Ann Oncol. 2007; 18:vi53-7.
20. Osborne CK, Wakeling A, Nicholson RI. Fulvestrant: an oestrogen receptor antagonist with a novel mechanism of action. Br J Cancer. 2004;90:S2-6.
21. Osborne CK. Tamoxifen in the treatment of breast cancer. N Engl J Med. 1998;339:1609-18.
22. Johnston SR, Saccani-Jotti G, Smith IE, Salter J, Newby J, Coppen M, et al. Changes in estrogen receptor, progesterone receptor, and pS2 expression in tamoxifen-resistant human breast cancer. Cancer Res. 1995;55:3331-8.
23. Dong L, Wang W, Wang F, Stoner M, Reed JC, Harigai M, et al. Mechanisms of transcriptional activation of bcl-2 gene expression by 17beta-estradiol in breast cancer cells. J Biol Chem. 1999;274:32099-107.
24. Dubik D, Shiu RP. Transcriptional regulation of c-myc oncogene expression by estrogen in hormone-responsive human breast cancer cells. J Biol Chem. 1988;263:12705-8.
25. Mandal S, Davie JR. Estrogen regulated expression of the p21 Waf1/Cip1 gene in estrogen receptor positive human breast cancer cells. J Cell Physiol. 2010;224:28-32.
26. Bicaku E, Marchion DC, Schmitt M, Munster PN. Selective inhibition of histone deacetylase 2 silences progesterone receptor mediated signaling. Cancer Res. 2008;68:1513-9.
27. Thomas S, Thurn KT, Bicaku E, Marchion DC, Munster PN. Addition of a histone deacetylase inhibitor redirects tamoxifen-treated breast cancer cells into apoptosis, which is opposed by the induction of autophagy. Breast Cancer Res Treat. 2011;130:437-47.
28. Kim YH, Park JW, Lee JY, Surh YJ, Kwon TK. Bcl-2 overexpression prevents daunorubicin-induced apoptosis through inhibition of XIAP and Akt degradation. Biochem Pharmacol. 2003;66:1779-86.
29. Raisova M, Goltz G, Bektas M, Bielawska A, Riebeling C, Hossini AM, et al. Bcl-2 overexpression prevents apoptosis induced by ceramidase inhibitors in malignant melanoma and HaCaT keratinocytes. FEBS Lett. 2002;516:47-52.
30. Wang Y, Wang X, Zhao H, Liang B, Du Q. Clusterin confers resistance to TNF-alpha-induced apoptosis in breast cancer cells through NF-kappaB activation and Bcl-2 overexpression. J Chemother. 2012;24:348-57.
31. Vaillant F, Merino D, Lee L, Breslin K, Pal B, Ritchie ME, et al. Targeting BCL-2 with the BH3 mimetic ABT-199 in estrogen receptor-positive breast cancer. Cancer Cell. 2013;24:120-9.
32. Trump DL, Smith DC, Ellis PG, Rogers MP, Schold SC, Winer EP, et al. High-dose oral tamoxifen, a potential multidrug-resistance-reversal agent: phase I trial in combination with vinblastine. J Natl Cancer Inst. 1992;84:1811-6.
33. Bergan RC, Reed E, Myers CE, Headlee D, Brawley O, Cho HK, et al. A Phase II study of high-dose tamoxifen in patients with hormone-refractory prostate cancer. Clin Cancer Res. 1999;5:2366-73.
34. Badia E, Duchesne MJ, Fournier-Bidoz S, Simar-Blanchet AE, Terouanne B, Nicolas JC, et al. Hydroxytamoxifen induces a rapid and irreversible inactivation of an estrogenic response in an MCF-7-derived cell line. Cancer Res. 1994;54:5860-6.
35. Brunner N, Frandsen TL, Holst-Hansen C, Bei M, Thompson EW, Wakeling AE, et al. MCF7/LCC2: a 4-hydroxytamoxifen resistant human breast cancer variant that retains sensitivity to the steroidal antiestrogen ICI 182,780. Cancer Res. 1993;53:3229-32.
36. de Leeuw R, Flach K, Bentin Toaldo C, Alexi X, Canisius S, Neefjes J, et al. PKA phosphorylation redirects ERalpha to promoters of a unique gene set to induce tamoxifen resistance. Oncogene. 2013;32:3543-51.
37. Wang C, Mayer JA, Mazumdar A, Fertuck K, Kim H, Brown M, et al. Estrogen induces c-myc gene expression via an upstream enhancer activated by the estrogen receptor and the AP-1 transcription factor. Mol Endocrinol. 2011;25:1527-38.
38. Toy W, Shen Y, Won H, Green B, Sakr RA, Will M, et al. ESR1 ligand-binding domain mutations in hormone-resistant breast cancer. Nat Genet. 2013;45:1439-45.
39. deFazio A, Chiew YE, Donoghue C, Lee CS, Sutherland RL. Effect of sodium butyrate on estrogen receptor and epidermal growth factor receptor gene expression in human breast cancer cell lines. J Biol Chem. 1992; 267:18008-12.
40. Fiskus W, Ren Y, Mohapatra A, Bali P, Mandawat A, Rao R, et al. Hydroxamic acid analogue histone deacetylase inhibitors attenuate estrogen receptor-alpha levels and transcriptional activity: a result of hyperacetylation and inhibition of chaperone function of heat shock protein 90. Clin Cancer Res. 2007;13:4882-90.
41. Oie S, Matsuzaki K, Yokoyama W, Murayama A, Yanagisawa J. HDAC3 regulates stability of estrogen receptor alpha mRNA. Biochem Biophys Res Commun. 2013;432:236-41.
42. Reid G, Metivier R, Lin CY, Denger S, Ibberson D, Ivacevic T, et al. Multiple mechanisms induce transcriptional silencing of a subset of genes, including oestrogen receptor alpha, in response to deacetylase inhibition by valproic acid and trichostatin A. Oncogene. 2005;24:4894-907.
43. Sharma D, Blum J, Yang X, Beaulieu N, Macleod AR, Davidson NE. Release of methyl CpG binding proteins and histone deacetylase 1 from the Estrogen receptor alpha (ER) promoter upon reactivation in ER-negative human breast cancer cells. Mol Endocrinol. 2005;19:1740-51.
44. Plotkin A, Volmar CH, Wahlestedt C, Ayad N, El-Ashry D. Transcriptional repression of ER through hMAPK dependent histone deacetylation by class I HDACs. Breast Cancer Res Treat. 2014;147:249-63.
45. Ocker M, Schneider-Stock R. Histone deacetylase inhibitors: signalling towards p21cip1/waf1. Int J Biochem Cell Biol. 2007;39:1367-74.
46. Duong V, Bret C, Altucci L, Mai A, Duraffourd C, Loubersac J, et al. Specific activity of class II histone deacetylases in human breast cancer cells. Mol Cancer Res. 2008;6:1908-19.
47. Strasser A, Cory S, Adams JM. Deciphering the rules of programmed cell death to improve therapy of cancer and other diseases. EMBO J. 2011;30:3667-83.
48. Silvestrini R, Benini E, Veneroni S, Daidone MG, Tomasic G, Squicciarini P, et al. p53 and bcl-2 expression correlates with clinical outcome in a series of node-positive breast cancer patients. J Clin Oncol. 1996;14:1604-10.
49. Hellemans P, van Dam PA, Weyler J, van Oosterom AT, Buytaert P, Van Marck E. Prognostic value of bcl-2 expression in invasive breast cancer. Br J Cancer. 1995;72:354-60.
50. Johnston SR, MacLennan KA, Sacks NP, Salter J, Smith IE, Dowsett M. Modulation of Bcl-2 and Ki-67 expression in oestrogen receptor-positive human breast cancer by tamoxifen. Eur J Cancer. 1994;30A:1663-9.
51. Planas-Silva MD, Bruggeman RD, Grenko RT, Smith JS. Overexpression of c-Myc and Bcl-2 during progression and distant metastasis of hormone-treated breast cancer. Exp Mol Pathol. 2007;82:85-90.
52. Gutierrez MC, Detre S, Johnston S, Mohsin SK, Shou J, Allred DC, et al. Molecular changes in tamoxifen-resistant breast cancer: relationship between estrogen receptor, HER-2, and p38 mitogen-activated protein kinase. J Clin Oncol. 2005;23:2469-76.