SLC1A5 glutamine transporter is a target of MYC and mediates reduced mTORC1 signaling and increased fatty acid oxidation in long-lived Myc hypomorphic mice

Aging Cell. 2019 Jun;18(3):e12947. doi: 10.1111/acel.12947. Epub 2019 Mar 25.

Abstract

Mice that express reduced levels of the c-Myc gene (Myc+/- heterozygotes) are long-lived. Myc hypomorphic mice display reduced rates of protein translation and decreased activity of the mammalian target of rapamycin (mTOR) complex 1 (mTORC1). Given the prominent effect of mTOR on aging, lower mTORC1 activity could contribute to the exceptional longevity and enhanced healthspan of Myc+/- animals. However, given the downstream position of MYC in these signaling cascades, the mechanism through which mTORC1 activity is downregulated in Myc+/- mice is not understood. We report that the high-affinity glutamine transporter SLC1A5, which is critical for activation of mTORC1 activity by amino acids, is a transcriptional target of MYC. Myc+/- cells display decreased Slc1a5 gene expression that leads to lower glutamine uptake and consequently reduced mTORC1 activity. Decreased mTORC1 activity in turn mediates an elevation of fatty acid oxidation (FAO) by indirectly upregulating the expression of carnitine palmitoyltransferase 1a (Cpt1a) that mediates the rate-limiting step of β-oxidation. Increased FAO has been noted in a number of long-lived mouse models. Taken together, our results show that transcriptional feedback loops regulated by MYC modulate upstream signaling pathways such as mTOR and impact FAO on an organismal level.

Keywords: MYC gene; fatty acid oxidation; genetic models; mTOR signaling; metabolic regulation; mouse longevity.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amino Acid Transport System ASC / genetics
  • Amino Acid Transport System ASC / metabolism*
  • Animals
  • Carnitine O-Palmitoyltransferase / genetics
  • Carnitine O-Palmitoyltransferase / metabolism
  • Cell Line
  • Fatty Acids / metabolism
  • Glutamine / metabolism*
  • Hepatocytes / enzymology
  • Hepatocytes / metabolism
  • Longevity / genetics*
  • Mechanistic Target of Rapamycin Complex 1 / metabolism*
  • Mice
  • Minor Histocompatibility Antigens / genetics
  • Minor Histocompatibility Antigens / metabolism*
  • Oxidation-Reduction
  • Protein Biosynthesis / genetics
  • Proto-Oncogene Proteins c-myc / genetics
  • Proto-Oncogene Proteins c-myc / metabolism*
  • Signal Transduction / genetics
  • TOR Serine-Threonine Kinases / antagonists & inhibitors
  • TOR Serine-Threonine Kinases / genetics
  • TOR Serine-Threonine Kinases / metabolism*

Substances

  • Amino Acid Transport System ASC
  • Fatty Acids
  • Minor Histocompatibility Antigens
  • Myc protein, mouse
  • Proto-Oncogene Proteins c-myc
  • Slc1a5 protein, mouse
  • Glutamine
  • Carnitine O-Palmitoyltransferase
  • Mechanistic Target of Rapamycin Complex 1
  • TOR Serine-Threonine Kinases