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 Aug 15;13(16):4882-90. doi: 10.1158/1078-0432.CCR-06-3093.

Abstract

Purpose: The molecular chaperone heat shock protein (hsp)-90 maintains estrogen receptor (ER)-alpha in an active conformation, allowing it to bind 17beta-estradiol (E2) and transactivate genes, including progesterone receptor (PR)-beta and the class IIB histone deacetylase HDAC6. By inhibiting HDAC6, the hydroxamic acid analogue pan-HDAC inhibitors (HA-HDI; e.g., LAQ824, LBH589, and vorinostat) induce hyperacetylation of the HDAC6 substrates alpha-tubulin and hsp90. Hyperacetylation of hsp90 inhibits its chaperone function, thereby depleting hsp90 client proteins. Here, we determined the effect of HA-HDIs on the levels and activity of ERalpha, as well as on the survival of ERalpha-expressing, estrogen-responsive human breast cancer MCF-7 and BT-474 cells.

Experimental design: Following exposure to HA-HDIs, hsp90 binding, polyubiquitylation levels, and transcriptional activity of ERalpha, as well as apoptosis and loss of survival, were determined in MCF-7 and BT-474 cells.

Results: Treatment with HA-HDI induced hsp90 hyperacetylation, decreased its binding to ERalpha, and increased polyubiquitylation and depletion of ERalpha levels. HA-HDI treatment abrogated E2-induced estrogen response element-luciferase expression and attenuated PRbeta and HDAC6 levels. Exposure to HA-HDI also depleted p-Akt, Akt, c-Raf, and phospho-extracellular signal-regulated kinase-1/2 levels, inhibited growth, and sensitized ERalpha-positive breast cancer cells to tamoxifen.

Conclusions: These findings show that treatment with HA-HDI abrogates ERalpha levels and activity and could sensitize ERalpha-positive breast cancers to E2 depletion or ERalpha antagonists.

MeSH terms

  • Acetylation
  • Antineoplastic Agents / pharmacology*
  • Breast Neoplasms / drug therapy
  • Breast Neoplasms / metabolism
  • Breast Neoplasms / pathology
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Enzyme Inhibitors / pharmacology*
  • Estrogen Receptor alpha / analysis*
  • Estrogen Receptor alpha / antagonists & inhibitors
  • Female
  • HSP90 Heat-Shock Proteins / antagonists & inhibitors*
  • Histone Deacetylase 6
  • Histone Deacetylase Inhibitors*
  • Histone Deacetylases / analysis
  • Humans
  • Hydroxamic Acids / pharmacology*
  • Poly(ADP-ribose) Polymerases / metabolism
  • Tamoxifen / analogs & derivatives
  • Tamoxifen / pharmacology
  • Transcription, Genetic / drug effects*

Substances

  • Antineoplastic Agents
  • Enzyme Inhibitors
  • Estrogen Receptor alpha
  • HSP90 Heat-Shock Proteins
  • Histone Deacetylase Inhibitors
  • Hydroxamic Acids
  • Tamoxifen
  • afimoxifene
  • Poly(ADP-ribose) Polymerases
  • HDAC6 protein, human
  • Histone Deacetylase 6
  • Histone Deacetylases