Hydroxamic acid analogue histone deacetylase inhibitors attenuate estrogen receptor-α levels and transcriptional activity: A result of hyperacetylation and inhibition of chaperone function of heat shock protein 90

Clinical Cancer Research

Volumn 13, Issue 16, 2007, Pages 4882-4890

  Fiskus, Warren ^a   Ren, Yuan ^b   Mohapatra, Alex ^c   Bali, Purva ^a   Mandawat, Aditya ^a   Rao, Rekha ^a   Herger, Bryan ^a   Yang, Yonghua ^a   Atadja, Peter ^d   Wu, Jie ^b   Bhalla, Kapil ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^c YALE UNIVERSITY   (United States)

^d NOVARTIS PHARMA AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

4 [N (2 HYDROXYETHYL) N [2 (3 INDOLYL)ETHYL]AMINOMETHYL]CINNAMOHYDROXAMIC ACID; 4 HYDROXYTAMOXIFEN; BORTEZOMIB; CHAPERONE; ESTROGEN RECEPTOR ALPHA; HEAT SHOCK PROTEIN 90; HISTONE DEACETYLASE 6; HISTONE DEACETYLASE INHIBITOR; HYDROXAMIC ACID DERIVATIVE; LBH 589; LUCIFERASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROGESTERONE RECEPTOR B; PROTEIN KINASE B; RAF PROTEIN; TAMOXIFEN; UNCLASSIFIED DRUG; VALPROIC ACID; VORINOSTAT;

APOPTOSIS; ARTICLE; CELL STRAIN MCF 7; CELL SURVIVAL; CHEMICAL REACTION; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DRUG EFFECT; ESTROGEN RESPONSIVE ELEMENT; HUMAN; HUMAN CELL; HYPERACETYLATION; MONOTHERAPY; POLYUBIQUITYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BINDING; UBIQUITINATION;

ACETYLATION; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; ENZYME INHIBITORS; ESTROGEN RECEPTOR ALPHA; FEMALE; HISTONE DEACETYLASES; HSP90 HEAT-SHOCK PROTEINS; HUMANS; HYDROXAMIC ACIDS; POLY(ADP-RIBOSE) POLYMERASES; TAMOXIFEN; TRANSCRIPTION, GENETIC;

EID: 34548075217     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-06-3093     Document Type: Article

References (43)

1. Yager JD, Davidson NE. Estrogen carcinogenesis in breast cancer. N Engl J Med 2006;354:270-82.
2. Dahlman-Wright K, Cavailles V, Fuqua Suzanne A, et al. International Union of Pharmacology: LXIV. Estrogen receptors. Pharmacol Rev 2006;58:773-81.
3. Klinge CM. Estrogen receptor interaction with co-activators and co-repressors. Steroids 2000;65:227-51.
4. McKenna NJ, O'Malley BW. Combinational control of gene expression by nuclear receptors and coregulators. Cell 2002;108:465-74.
5. Fliss AE, Benzeno S, Rao J, Caplan AJ. Control of estrogen receptor ligand binding by hsp90. J Steroid Biochem Mol Biol 2000;72:223-30.
6. Saji S, Kawakami M, Hayashi S, et al. Significance of HDAC6 regulation via estrogen signaling for cell-motility and prognosis in estrogen receptor-positive breast cancer. Oncogene 2005;24:4531-9.
7. McDonnell DP, Norris JD. Connections and regulation of the human estrogen receptor. Science 2002;296:1642-4.
8. Levin ER. Cellular functions of plasma membrane estrogen receptors. Steroids 2002;67:471-5.
9. Lannigan D. Estrogen receptor phosphorylation. Steroids 2003;68:1-9.
10. Martin MB, Franke TF, Stoica GE, et al. A role for Akt in mediating the estrogenic functions of epidermal growth factor and insulin-like growth factor I. Endocrinology 2000;141:4503-11.
11. Levin ER. Bidirectional signaling between the estrogen receptor and the epidermal growth factor receptor. Mol Endocrinol 2003;17:309-17.
12. Stoica GE, Franke TF, Moroni M, et al. Effect of estradiol on estrogen receptor-α gene expression and activity can be modulated by the ErbB2/PI 3-K/Akt pathway. Oncogene 2003;22:7998-8011.
13. Liu M, Albanese C, Anderson CM, et al. Opposing action of estrogen receptors α and β on cyclin D1 gene expression. J Biol Chem 2002;277:24353-60.
14. Alao JP, Lam EW-F, Ali S, et al. Histone deacetylase inhibitor trichostatin A represses estrogen receptor α-dependent transcription and promotes proteasomal degradation of cyclin D1 in human breast carcinoma cell lines. Clin Cancer Res 2004;10:8094-104.
15. Whitesell L, Lindquist SL. Hsp90 and the chaperoning of cancer. Nat Rev Cancer 2005;5:761-72.
16. Oxelmark E, Knoblauch R, Arnal S, et al. Genetic dissection of p23, an hsp90 cochaperon, reveals a distinct surface involved in estrogen receptor signaling. J Biol Chem 2003;278:36547-55.
17. Gougelet A, Bouclier C, Marsaud V, et al. Estrogen receptor α and β subtype expression and transactivation capacity are differentially affected by receptor-, hsp90- and immunophilin-ligands in human breast cancer cells. J Steroid Biochem Mol Biol 2005;94:71-81.
18. Beliakoff J, Whitesell L. Hsp90: an emerging target for breast cancer therapy. Anticancer Drugs 2004;15:651-62.
19. Neckers L. Heat shock protein 90 is a rational molecular target in breast cancer. Breast Disease 2002;15:53-60.
20. Verdin E, Dequiedt F, Kasler HG. Class II histone deacetylases: versatile regulators. Trends Genet 2003;19:286-93.
21. Hubbert C, Guardiola A, Shao R, et al. HDAC6 is a microtubule-associated deacetylase. Nature 2002;417:455-8.
22. Haggarty SJ, Koeller KM, Wong JC, Grozinger CM, Schreiber SL. Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc Natl Acad Sci U S A 2003;100:4389-94.
23. Bali P, Pranpat M, Bradner J, et al. Inhibition of histone deacetylase 6 acetylates and disrupts the chaperone function of heat shock protein 90: a novel basis for antileukemia activity of histone deacetylase inhibitors. J Biol Chem 2005;280:26729-34.
24. Kovacs JJ, Murphy PJ, Gaillard S, et al. HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol Cell 2005;18:601-7.
25. Bali P, Pranpat M, Swaby R, et al. Activity of suberoylanilide hydroxamic Acid against human breast cancer cells with amplification of her-2. Clin Cancer Res 2005;11:6382-9.
26. George P, Bali P, Annavarapu S, et al. Combination of the histone deacetylase inhibitor LBH589 and the hsp90 inhibitor 17-AAG is highly active against human CML-BC cells and AML cells with activating mutation of FLT-3. Blood 2005;105:1768-76.
27. Murphy PJ, Morishima Y, Kovacs JJ, Yao TP, Pratt WB. Regulation of the dynamics of hsp90 action on the glucocorticoid receptor by acetylation/ deacetylation of the chaperone. J Biol Chem 2005;280:33792-9.
28. Fuino L, Bali P, Wittmann S, et al. Histone deacetylase inhibitor LAQ824 down-regulates Her-2 and sensitizes human breast cancer cells to trastuzumab, Taxotere, gemcitabine, and epothilone B. Mol Cancer Ther 2003;2:971-84.
29. Guo F, Rocha K, Bali P, et al. Abrogation of hsp70 induction as a strategy to increase anti-leukemia activity of hsp90 inhibitor 17-allylamino-demethoxy geldanamycin. Cancer Res 2005;65:10536-44.
30. Munster PN, Marchion D, Bicaku E, et al. Feasibility and efficacy of valproic acid as a histone deacetylase inhibitor to potentiate anthracyclines: a phase 1 and pilot study in locally advanced/metastatic breast cancer. American Association for cancer Research Annual Proceedings, Apr 14-18 2007, Los Angeles, California. Philadelphia (PA): AACR; 2007. Supplement: Abstract LB-353.
31. Bagatell R, Khan O, Paine-Murrieta G, et al. Destabilization of steroid receptors by heat shock protein 90-binding drugs: a ligand-independent approach to hormonal therapy of breast cancer. Clin Cancer Res 2001;7:2076-84.
32. Lee M, Kim E, Kwon HJ, et al. Radicicol represses the transcriptional function of the estrogen receptor by suppressing the stabilization of the receptor by heat shock protein 90. Mol Cell Endocrinol 2002;188:47-54.
33. Ottaviano YL, Issa J-P, Parl FF, et al. Methylation of the estrogen receptor gene CpG island marks loss of estrogen receptor expression in human breast cancer cells. Cancer Res 1994;54:2552-5.
34. Yang X, Phillips D, Ferguson AT, et al. Synergistic activation of functional estrogen receptor (ER)-α by DNA methyl-transferase and histone deacetylase inhibition in human ER-α negative breast cancer cells. Cancer Res 2001;61:7025-9.
35. Sharma D, Saxena NK, Davidson NE, Vertino PM. Restoration of tamoxifen sensitivity in estrogen receptor-negative breast cancer cells: tamoxifen-bound reactivated ER recruits distinctive corepressor complexes. Cancer Res 2006;66:6370-8.
36. Margueron R, Duong V, Bonnet S, et al. Histone deacetylase inhibition and estrogen receptor α levels modulate the transcriptional activity of partial antiestrogens. J Mol Endocrinol 2004;32:583-94.
37. Hayashi S, Yamaguchi Y. Basic research for hormone-sensitivity of breast cancer. Breast Cancer 2006;13:123-8.
38. Moy B, Goss PE. Estrogen receptor pathway: resistance to endocrine therapy and new therapeutic approaches. Clin Cancer Res 2006;12:4790-3.
39. Creighton CJ, Hilger AM, Murthy S, et al. Activation of mitogen-activated protein kinase in estrogen receptor α-positive breast cancer cells in vitro induces an in vivo molecular phenotype of estrogen receptor α-negative human breast tumors. Cancer Res 2006;66:3903-11.
40. Shou J, Massarweh S, Osborne CK, et al. Mechanisms of tamoxifen resistance: increased estrogen receptor-HER2/neu cross-talk in ER/HER2-positive breast cancer. J Natl Cancer Inst 2004;96:926-35.
41. Lewis JS, Osipo C, Meeke K, et al. Estrogen-induced apoptosis in a breast cancer model resistant to long-term estrogen withdrawal. J Steroid Biochem Mol Biol 2005;94:131-41.
42. Ariazi EA, Lewis-Wambi JS, Gill SD, et al. Emerging principles for the development of resistance to anti-hormonal therapy: implications for the clinical utility of fulvestrant. J Steroid Biochem Mol Biol 2006;102:128-38.
43. Martin LA, Farmer I, Johnston SR, et al. Enhanced estrogen receptor (ER) α, ERBB2, and MAPK signal transduction pathways operate duringt he adaptation of MCF-7 cells to long term estrogen deprivation. J Biol Chem 2003;278:30458-68.