mTORC1-CTLH E3 ligase regulates the degradation of HMG-CoA synthase 1 through the Pro/N-degron pathway

Mol Cell. 2024 Jun 6;84(11):2166-2184.e9. doi: 10.1016/j.molcel.2024.04.026. Epub 2024 May 23.

Abstract

Mammalian target of rapamycin (mTOR) senses changes in nutrient status and stimulates the autophagic process to recycle amino acids. However, the impact of nutrient stress on protein degradation beyond autophagic turnover is incompletely understood. We report that several metabolic enzymes are proteasomal targets regulated by mTOR activity based on comparative proteome degradation analysis. In particular, 3-hydroxy-3-methylglutaryl (HMG)-coenzyme A (CoA) synthase 1 (HMGCS1), the initial enzyme in the mevalonate pathway, exhibits the most significant half-life adaptation. Degradation of HMGCS1 is regulated by the C-terminal to LisH (CTLH) E3 ligase through the Pro/N-degron motif. HMGCS1 is ubiquitylated on two C-terminal lysines during mTORC1 inhibition, and efficient degradation of HMGCS1 in cells requires a muskelin adaptor. Importantly, modulating HMGCS1 abundance has a dose-dependent impact on cell proliferation, which is restored by adding a mevalonate intermediate. Overall, our unbiased degradomics study provides new insights into mTORC1 function in cellular metabolism: mTORC1 regulates the stability of limiting metabolic enzymes through the ubiquitin system.

Keywords: CTLH; GID; HMGCS1; degradomics; mTOR; mTORC1; mevalonate pathway; sterol; ubiquitin; ubiquitin-proteasome system.

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Cell Proliferation*
  • Degrons
  • HEK293 Cells
  • Humans
  • Hydroxymethylglutaryl-CoA Synthase* / genetics
  • Hydroxymethylglutaryl-CoA Synthase* / metabolism
  • Mechanistic Target of Rapamycin Complex 1* / genetics
  • Mechanistic Target of Rapamycin Complex 1* / metabolism
  • Mevalonic Acid / metabolism
  • Multiprotein Complexes / genetics
  • Multiprotein Complexes / metabolism
  • Proteasome Endopeptidase Complex / genetics
  • Proteasome Endopeptidase Complex / metabolism
  • Proteolysis*
  • Signal Transduction
  • TOR Serine-Threonine Kinases / genetics
  • TOR Serine-Threonine Kinases / metabolism
  • Ubiquitin-Protein Ligases* / genetics
  • Ubiquitin-Protein Ligases* / metabolism
  • Ubiquitination*

Substances

  • Mechanistic Target of Rapamycin Complex 1
  • Ubiquitin-Protein Ligases
  • Hydroxymethylglutaryl-CoA Synthase
  • Proteasome Endopeptidase Complex
  • TOR Serine-Threonine Kinases
  • Mevalonic Acid
  • Multiprotein Complexes
  • LAMTOR5 protein, human
  • Adaptor Proteins, Signal Transducing