Metabolic remodeling precedes mTORC1-mediated cardiac hypertrophy

J Mol Cell Cardiol. 2021 Sep:158:115-127. doi: 10.1016/j.yjmcc.2021.05.016. Epub 2021 Jun 1.

Abstract

Rationale: The nutrient sensing mechanistic target of rapamycin complex 1 (mTORC1) and its primary inhibitor, tuberin (TSC2), are cues for the development of cardiac hypertrophy. The phenotype of mTORC1 induced hypertrophy is unknown.

Objective: To examine the impact of sustained mTORC1 activation on metabolism, function, and structure of the adult heart.

Methods and results: We developed a mouse model of inducible, cardiac-specific sustained mTORC1 activation (mTORC1iSA) through deletion of Tsc2. Prior to hypertrophy, rates of glucose uptake and oxidation, as well as protein and enzymatic activity of glucose 6-phosphate isomerase (GPI) were decreased, while intracellular levels of glucose 6-phosphate (G6P) were increased. Subsequently, hypertrophy developed. Transcript levels of the fetal gene program and pathways of exercise-induced hypertrophy increased, while hypertrophy did not progress to heart failure. We therefore examined the hearts of wild-type mice subjected to voluntary physical activity and observed early changes in GPI, followed by hypertrophy. Rapamycin prevented these changes in both models.

Conclusion: Activation of mTORC1 in the adult heart triggers the development of a non-specific form of hypertrophy which is preceded by changes in cardiac glucose metabolism.

Keywords: Exercise; Glycolysis; Hypertrophy; Metabolism; mTORC1.

Publication types

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

MeSH terms

  • Animals
  • Cardiomegaly / diet therapy
  • Cardiomegaly / genetics
  • Cardiomegaly / metabolism*
  • Cardiomegaly / prevention & control
  • Cells, Cultured
  • Diet / methods
  • Disease Models, Animal
  • Enzyme Activation / genetics
  • Gene Knockdown Techniques / methods*
  • Glucose / metabolism*
  • Glucose-6-Phosphatase / metabolism
  • Isomerases / metabolism
  • Male
  • Mechanistic Target of Rapamycin Complex 1 / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Myocytes, Cardiac / metabolism
  • Oxidation-Reduction
  • Phosphorylation / genetics
  • Signal Transduction / genetics*
  • Sirolimus / administration & dosage
  • Tuberous Sclerosis Complex 2 Protein / genetics
  • Tuberous Sclerosis Complex 2 Protein / metabolism

Substances

  • Tsc2 protein, mouse
  • Tuberous Sclerosis Complex 2 Protein
  • Mechanistic Target of Rapamycin Complex 1
  • Glucose-6-Phosphatase
  • Isomerases
  • Glucose
  • Sirolimus