Translation in amino-acid-poor environments is limited by tRNAGln charging

Elife. 2020 Dec 8:9:e62307. doi: 10.7554/eLife.62307.

Abstract

An inadequate supply of amino acids leads to accumulation of uncharged tRNAs, which can bind and activate GCN2 kinase to reduce translation. Here, we show that glutamine-specific tRNAs selectively become uncharged when extracellular amino acid availability is compromised. In contrast, all other tRNAs retain charging of their cognate amino acids in a manner that is dependent upon intact lysosomal function. In addition to GCN2 activation and reduced total translation, the reduced charging of tRNAGln in amino-acid-deprived cells also leads to specific depletion of proteins containing polyglutamine tracts including core-binding factor α1, mediator subunit 12, transcriptional coactivator CBP and TATA-box binding protein. Treating amino-acid-deprived cells with exogenous glutamine or glutaminase inhibitors restores tRNAGln charging and the levels of polyglutamine-containing proteins. Together, these results demonstrate that the activation of GCN2 and the translation of polyglutamine-encoding transcripts serve as key sensors of glutamine availability in mammalian cells.

Keywords: cell biology; glutamine; human; mouse; nutrient depletion; polyglutamine; tRNA; translation.

Publication types

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

MeSH terms

  • Amino Acids / deficiency*
  • Animals
  • Cell Line, Tumor
  • Glutaminase / antagonists & inhibitors
  • Glutaminase / metabolism
  • Glutamine / metabolism
  • Humans
  • Mice
  • Peptides / metabolism
  • Protein Biosynthesis*
  • RNA, Transfer, Gln / metabolism*
  • Transfer RNA Aminoacylation*

Substances

  • Amino Acids
  • Peptides
  • RNA, Transfer, Gln
  • Glutamine
  • polyglutamine
  • Glutaminase

Associated data

  • GEO/GSE157276