Riluzole induces AR degradation via endoplasmic reticulum stress pathway in androgen-dependent and castration-resistant prostate cancer cells

Prostate. 2019 Feb;79(2):140-150. doi: 10.1002/pros.23719. Epub 2018 Oct 2.

Abstract

Background: Prostate cancer (PCa) is diagnosed at the highest rate of all non-cutaneous male cancers in the United States. The androgen-dependent (AD) transcription factor, androgen receptor (AR), drives PCa-but inhibiting AR or androgen biosynthesis induces remission for only a short time. At which point, patients acquire more aggressive castration-resistant (CR) disease with re-activated AR-dependent signaling. To combat treatment resistance, down-regulating AR protein expression has been considered as a potential treatment strategy for CR-PCa.

Methods: AD- and CR-PCa cell lines were treated with the well-tolerated FDA-approved oral medicine, riluzole. Expression of full-length or wild-type AR (AR-FL) and constitutively active AR-splice variant 7 (AR-V7) was assessed by immunoblotting. AR-FL/AR-V7 activity was measured using qRT-PCR of AR-target genes. Cytoplasmic [Ca2+ ] levels were measured using a fluorescent Ca2+ indicator microplate assay. Markers of the endoplasmic reticulum stress (ERS) pathway and autophagy were assessed by immunoblotting. Direct interaction between AR and selective autophagy receptor p62 was demonstrated by co-immunoprecipitation.

Results: We demonstrate that riluzole downregulates AR-FL, mutant ARs, and AR-V7 proteins expression by protein degradation through ERS pathway and selective autophagy. Riluzole also significantly inhibited AR transcription activity by decreasing its target genes expression (PSA, TMPRSS2, and KLK2).

Conclusions: We provide key mechanistic insights by which riluzole exerts its anti-tumorigenic effects and induces AR protein degradation via ERS pathways. Our findings support the potential utility of riluzole for treatment of PCa.

Keywords: AR-V7; ER stress; androgen receptor; autophagy; riluzole.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Activating Transcription Factor 6 / metabolism
  • Androgens / metabolism*
  • Autophagy / drug effects
  • Cell Line, Tumor
  • Drug Interactions
  • Endoplasmic Reticulum Stress / drug effects*
  • Endoribonucleases / antagonists & inhibitors
  • Endoribonucleases / metabolism
  • Humans
  • Male
  • Prostatic Neoplasms / drug therapy*
  • Prostatic Neoplasms / metabolism
  • Prostatic Neoplasms, Castration-Resistant / drug therapy*
  • Prostatic Neoplasms, Castration-Resistant / metabolism
  • Protein Serine-Threonine Kinases / antagonists & inhibitors
  • Protein Serine-Threonine Kinases / metabolism
  • Receptors, Androgen / biosynthesis
  • Receptors, Androgen / metabolism*
  • Riluzole / pharmacology*
  • Sequestosome-1 Protein / metabolism
  • Signal Transduction / drug effects
  • Sulfonamides / pharmacology
  • Thiophenes / pharmacology

Substances

  • AR protein, human
  • ATF6 protein, human
  • Activating Transcription Factor 6
  • Androgens
  • Receptors, Androgen
  • SQSTM1 protein, human
  • STF 083010
  • Sequestosome-1 Protein
  • Sulfonamides
  • Thiophenes
  • Riluzole
  • ERN1 protein, human
  • Protein Serine-Threonine Kinases
  • Endoribonucleases