An epitranscriptomic mechanism underlies selective mRNA translation remodelling in melanoma persister cells

Nat Commun. 2019 Dec 16;10(1):5713. doi: 10.1038/s41467-019-13360-6.

Abstract

Cancer persister cells tolerate anticancer drugs and serve as the founders of acquired resistance and cancer relapse. Here we show that a subpopulation of BRAFV600 mutant melanoma cells that tolerates exposure to BRAF and MEK inhibitors undergoes a reversible remodelling of mRNA translation that evolves in parallel with drug sensitivity. Although this process is associated with a global reduction in protein synthesis, a subset of mRNAs undergoes an increased efficiency in translation. Inhibiting the eIF4A RNA helicase, a component of the eIF4F translation initiation complex, abrogates this selectively increased translation and is lethal to persister cells. Translation remodelling in persister cells coincides with an increased N6-methyladenosine modification in the 5'-untranslated region of some highly translated mRNAs. Combination of eIF4A inhibitor with BRAF and MEK inhibitors effectively inhibits the emergence of persister cells and may represent a new therapeutic strategy to prevent acquired drug resistance.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 5' Untranslated Regions / genetics
  • Adenosine / analogs & derivatives
  • Adenosine / metabolism
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology*
  • Antineoplastic Combined Chemotherapy Protocols / therapeutic use
  • Cell Line, Tumor
  • DNA Methylation / drug effects
  • DNA Methylation / genetics
  • Drug Resistance, Neoplasm / drug effects
  • Drug Resistance, Neoplasm / genetics*
  • Epigenesis, Genetic / drug effects
  • Eukaryotic Initiation Factor-4A / antagonists & inhibitors
  • Gene Expression Regulation, Neoplastic / drug effects
  • Gene Expression Regulation, Neoplastic / genetics*
  • Humans
  • MAP Kinase Kinase Kinases / antagonists & inhibitors
  • Melanoma / drug therapy*
  • Melanoma / genetics
  • Melanoma / pathology
  • Mutation
  • Protein Kinase Inhibitors / pharmacology*
  • Protein Kinase Inhibitors / therapeutic use
  • Proto-Oncogene Proteins B-raf / antagonists & inhibitors
  • Proto-Oncogene Proteins B-raf / genetics
  • RNA Helicases / antagonists & inhibitors
  • RNA, Messenger / metabolism*
  • Skin Neoplasms / drug therapy*
  • Skin Neoplasms / genetics
  • Skin Neoplasms / pathology
  • Transcription, Genetic / drug effects

Substances

  • 5' Untranslated Regions
  • Protein Kinase Inhibitors
  • RNA, Messenger
  • N-methyladenosine
  • BRAF protein, human
  • Proto-Oncogene Proteins B-raf
  • MAP Kinase Kinase Kinases
  • Eukaryotic Initiation Factor-4A
  • RNA Helicases
  • Adenosine