Melanoma Persister Cells Are Tolerant to BRAF/MEK Inhibitors via ACOX1-Mediated Fatty Acid Oxidation

Cell Rep. 2020 Nov 24;33(8):108421. doi: 10.1016/j.celrep.2020.108421.

Abstract

Emerging evidence indicates that non-mutational drug tolerance mechanisms underlie the survival of residual cancer "persister" cells. Here, we find that BRAF(V600E) mutant melanoma persister cells tolerant to BRAF/MEK inhibitors switch their metabolism from glycolysis to oxidative respiration supported by peroxisomal fatty acid β-oxidation (FAO) that is transcriptionally regulated by peroxisome proliferator-activated receptor alpha (PPARα). Knockdown of the key peroxisomal FAO enzyme, acyl-CoA oxidase 1 (ACOX1), as well as treatment with the peroxisomal FAO inhibitor thioridazine, specifically suppresses the oxidative respiration of persister cells and significantly decreases their emergence. Consistently, a combination treatment of BRAF/MEK inhibitors with thioridazine in human-melanoma-bearing mice results in a durable anti-tumor response. In BRAF(V600E) melanoma samples from patients treated with BRAF/MEK inhibitors, higher baseline expression of FAO-related genes and PPARα correlates with patients' outcomes. These results pave the way for a metabolic strategy to overcome drug resistance.

Keywords: fatty acid oxidation; melanoma; peroxisome; persistent cancer cell; targeted therapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3-Hydroxyacyl CoA Dehydrogenases / metabolism*
  • Acetyl-CoA C-Acyltransferase / metabolism*
  • Acyl-CoA Oxidase / metabolism*
  • Animals
  • Carbon-Carbon Double Bond Isomerases / metabolism*
  • Enoyl-CoA Hydratase / metabolism*
  • Humans
  • Melanoma / genetics*
  • Melanoma / pathology
  • Mice
  • Protein Kinase Inhibitors / pharmacology
  • Protein Kinase Inhibitors / therapeutic use*
  • Proto-Oncogene Proteins B-raf / antagonists & inhibitors*
  • Racemases and Epimerases / metabolism*

Substances

  • Protein Kinase Inhibitors
  • fatty acid oxidation complex
  • 3-Hydroxyacyl CoA Dehydrogenases
  • ACOX1 protein, mouse
  • Acyl-CoA Oxidase
  • Acetyl-CoA C-Acyltransferase
  • Proto-Oncogene Proteins B-raf
  • Enoyl-CoA Hydratase
  • Racemases and Epimerases
  • Carbon-Carbon Double Bond Isomerases