Npr2 inhibits TORC1 to prevent inappropriate utilization of glutamine for biosynthesis of nitrogen-containing metabolites

Sci Signal. 2014 Dec 16;7(356):ra120. doi: 10.1126/scisignal.2005948.

Abstract

Cells must be capable of switching between growth and autophagy in unpredictable nutrient environments. The conserved Npr2 protein complex (comprising Iml1, Npr2, and Npr3; also called SEACIT) inhibits target of rapamycin complex 1 (TORC1) kinase signaling, which inhibits autophagy in nutrient-rich conditions. In yeast cultured in media with nutrient limitations that promote autophagy and inhibit growth, loss of Npr2 enables cells to bypass autophagy and proliferate. We determined that Npr2-deficient yeast had a metabolic state distinct from that of wild-type yeast when grown in minimal media containing ammonium as a nitrogen source and a nonfermentable carbon source (lactate). Unlike wild-type yeast, which accumulated glutamine, Npr2-deficient yeast metabolized glutamine into nitrogen-containing metabolites and maintained a high concentration of S-adenosyl methionine (SAM). Moreover, in wild-type yeast grown in these nutrient-limited conditions, supplementation with methionine stimulated glutamine consumption for synthesis of nitrogenous metabolites, demonstrating integration of a sulfur-containing amino acid cue and nitrogen utilization. These data revealed the metabolic basis by which the Npr2 complex regulates cellular homeostasis and demonstrated a key function for TORC1 in regulating the synthesis and utilization of glutamine as a nitrogen source.

Publication types

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

MeSH terms

  • Ammonium Compounds / metabolism
  • Glutamine / genetics
  • Glutamine / metabolism*
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • S-Adenosylmethionine / genetics
  • S-Adenosylmethionine / metabolism
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / metabolism*
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*

Substances

  • Ammonium Compounds
  • Intracellular Signaling Peptides and Proteins
  • NPR2 protein, S cerevisiae
  • Saccharomyces cerevisiae Proteins
  • TORC1 protein complex, S cerevisiae
  • Transcription Factors
  • Glutamine
  • S-Adenosylmethionine