AMPK regulation of Raptor and TSC2 mediate metformin effects on transcriptional control of anabolism and inflammation

Genes Dev. 2020 Oct 1;34(19-20):1330-1344. doi: 10.1101/gad.339895.120. Epub 2020 Sep 10.

Abstract

Despite being the frontline therapy for type 2 diabetes, the mechanisms of action of the biguanide drug metformin are still being discovered. In particular, the detailed molecular interplays between the AMPK and the mTORC1 pathway in the hepatic benefits of metformin are still ill defined. Metformin-dependent activation of AMPK classically inhibits mTORC1 via TSC/RHEB, but several lines of evidence suggest additional mechanisms at play in metformin inhibition of mTORC1. Here we investigated the role of direct AMPK-mediated serine phosphorylation of RAPTOR in a new RaptorAA mouse model, in which AMPK phospho-serine sites Ser722 and Ser792 of RAPTOR were mutated to alanine. Metformin treatment of primary hepatocytes and intact murine liver requires AMPK regulation of both RAPTOR and TSC2 to fully inhibit mTORC1, and this regulation is critical for both the translational and transcriptional response to metformin. Transcriptionally, AMPK and mTORC1 were both important for regulation of anabolic metabolism and inflammatory programs triggered by metformin treatment. The hepatic transcriptional response in mice on high-fat diet treated with metformin was largely ablated by AMPK deficiency under the conditions examined, indicating the essential role of this kinase and its targets in metformin action in vivo.

Keywords: AMPK; RAPTOR; STAT3; TSC2; mTOR; metformin.

Publication types

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

MeSH terms

  • AMP-Activated Protein Kinases / metabolism*
  • Animals
  • Diabetes Mellitus, Type 2 / drug therapy
  • Disease Models, Animal
  • Gene Expression Regulation / drug effects*
  • Gene Knock-In Techniques
  • Genotype
  • Hypoglycemic Agents / pharmacology
  • Inflammation
  • Mechanistic Target of Rapamycin Complex 1 / metabolism
  • Metabolism / drug effects
  • Metformin / pharmacology*
  • Metformin / therapeutic use
  • Mice
  • Phosphorylation / drug effects
  • Regulatory-Associated Protein of mTOR / genetics*
  • Regulatory-Associated Protein of mTOR / metabolism
  • Signal Transduction / drug effects*
  • TOR Serine-Threonine Kinases / metabolism
  • Tuberous Sclerosis Complex 2 Protein / genetics
  • Tuberous Sclerosis Complex 2 Protein / metabolism

Substances

  • Hypoglycemic Agents
  • Regulatory-Associated Protein of mTOR
  • Tsc2 protein, mouse
  • Tuberous Sclerosis Complex 2 Protein
  • Metformin
  • mTOR protein, mouse
  • Mechanistic Target of Rapamycin Complex 1
  • TOR Serine-Threonine Kinases
  • AMP-Activated Protein Kinases