A glutaminase isoform switch drives therapeutic resistance and disease progression of prostate cancer

Proc Natl Acad Sci U S A. 2021 Mar 30;118(13):e2012748118. doi: 10.1073/pnas.2012748118.

Abstract

Cellular metabolism in cancer is significantly altered to support the uncontrolled tumor growth. How metabolic alterations contribute to hormonal therapy resistance and disease progression in prostate cancer (PCa) remains poorly understood. Here we report a glutaminase isoform switch mechanism that mediates the initial therapeutic effect but eventual failure of hormonal therapy of PCa. Androgen deprivation therapy inhibits the expression of kidney-type glutaminase (KGA), a splicing isoform of glutaminase 1 (GLS1) up-regulated by androgen receptor (AR), to achieve therapeutic effect by suppressing glutaminolysis. Eventually the tumor cells switch to the expression of glutaminase C (GAC), an androgen-independent GLS1 isoform with more potent enzymatic activity, under the androgen-deprived condition. This switch leads to increased glutamine utilization, hyperproliferation, and aggressive behavior of tumor cells. Pharmacological inhibition or RNA interference of GAC shows better treatment effect for castration-resistant PCa than for hormone-sensitive PCa in vitro and in vivo. In summary, we have identified a metabolic function of AR action in PCa and discovered that the GLS1 isoform switch is one of the key mechanisms in therapeutic resistance and disease progression.

Keywords: GAC; glutaminase; prostate cancer; therapeutic resistance.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Androgen Antagonists / pharmacology*
  • Androgen Antagonists / therapeutic use
  • Animals
  • Cell Line, Tumor
  • Computational Biology
  • Disease Progression
  • Drug Resistance, Neoplasm / drug effects
  • Drug Resistance, Neoplasm / genetics*
  • Gene Expression Profiling
  • Gene Expression Regulation, Neoplastic / drug effects
  • Glutaminase / genetics*
  • Glutaminase / metabolism
  • Glutamine / metabolism
  • Humans
  • Isoenzymes / genetics
  • Isoenzymes / metabolism
  • Male
  • Mice
  • Prostate / pathology
  • Prostatic Neoplasms / drug therapy*
  • Prostatic Neoplasms / genetics
  • Prostatic Neoplasms / pathology
  • Receptors, Androgen / metabolism*
  • Tissue Array Analysis
  • Xenograft Model Antitumor Assays

Substances

  • AR protein, human
  • Androgen Antagonists
  • Isoenzymes
  • Receptors, Androgen
  • Glutamine
  • GLS protein, human
  • Glutaminase