The tRNA-GCN2-FBXO22-axis-mediated mTOR ubiquitination senses amino acid insufficiency

Cell Metab. 2023 Dec 5;35(12):2216-2230.e8. doi: 10.1016/j.cmet.2023.10.016. Epub 2023 Nov 17.

Abstract

Mammalian target of rapamycin complex 1 (mTORC1) monitors cellular amino acid changes for function, but the molecular mediators of this process remain to be fully defined. Here, we report that depletion of cellular amino acids, either alone or in combination, leads to the ubiquitination of mTOR, which inhibits mTORC1 kinase activity by preventing substrate recruitment. Mechanistically, amino acid depletion causes accumulation of uncharged tRNAs, thereby stimulating GCN2 to phosphorylate FBXO22, which in turn accrues in the cytoplasm and ubiquitinates mTOR at Lys2066 in a K27-linked manner. Accordingly, mutation of mTOR Lys2066 abolished mTOR ubiquitination in response to amino acid depletion, rendering mTOR insensitive to amino acid starvation both in vitro and in vivo. Collectively, these data reveal a novel mechanism of amino acid sensing by mTORC1 via a previously unknown GCN2-FBXO22-mTOR pathway that is uniquely controlled by uncharged tRNAs.

Keywords: FBXO22; GCN2; amino acids; mTOR; mTORC1; ubiquitination; uncharged tRNA.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acids / metabolism
  • Mechanistic Target of Rapamycin Complex 1 / metabolism
  • Protein Serine-Threonine Kinases* / genetics
  • Protein Serine-Threonine Kinases* / metabolism
  • RNA, Transfer / genetics
  • RNA, Transfer / metabolism
  • TOR Serine-Threonine Kinases*

Substances

  • Protein Serine-Threonine Kinases
  • TOR Serine-Threonine Kinases
  • Amino Acids
  • RNA, Transfer
  • Mechanistic Target of Rapamycin Complex 1