Systemic Reprogramming of Translation Efficiencies on Oxygen Stimulus

Cell Rep. 2016 Feb 16;14(6):1293-1300. doi: 10.1016/j.celrep.2016.01.036. Epub 2016 Feb 4.

Abstract

Protein concentrations evolve under greater evolutionary constraint than mRNA levels. Translation efficiency of mRNA represents the chief determinant of basal protein concentrations. This raises a fundamental question of how mRNA and protein levels are coordinated in dynamic systems responding to physiological stimuli. This report examines the contributions of mRNA abundance and translation efficiency to protein output in cells responding to oxygen stimulus. We show that changes in translation efficiencies, and not mRNA levels, represent the major mechanism governing cellular responses to [O2] perturbations. Two distinct cap-dependent protein synthesis machineries select mRNAs for translation: the normoxic eIF4F and the hypoxic eIF4F(H). O2-dependent remodeling of translation efficiencies enables cells to produce adaptive translatomes from preexisting mRNA pools. Differences in mRNA expression observed under different [O2] are likely neutral, given that they occur during evolution. We propose that mRNAs contain translation efficiency determinants for their triage by the translation apparatus on [O2] stimulus.

Keywords: HIF; RNA sequencing; SILAC; cancer; eIF4E; eIF4E2; eIF4F; hypoxia; oxygen; translation.

Publication types

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

MeSH terms

  • Cell Hypoxia
  • Cell Line, Tumor
  • Epithelial Cells / cytology
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • Eukaryotic Initiation Factor-4F / genetics*
  • Eukaryotic Initiation Factor-4F / metabolism
  • Evolution, Molecular
  • Humans
  • Neuroglia / cytology
  • Neuroglia / drug effects
  • Neuroglia / metabolism
  • Oxygen / pharmacology*
  • Protein Biosynthesis / drug effects*
  • RNA, Messenger / genetics*
  • RNA, Messenger / metabolism

Substances

  • Eukaryotic Initiation Factor-4F
  • RNA, Messenger
  • Oxygen