mTOR Modulation of IKr through hERG1b-Dependent Mechanisms in Lipotoxic Heart

Int J Mol Sci. 2022 Jul 22;23(15):8061. doi: 10.3390/ijms23158061.

Abstract

In the atria, the rapid delayed rectifier channel (IKr) is a critical contributor to repolarization. In lipotoxic atria, increased activity of the serine/threonine mammalian target of rapamycin (mTOR) may remodel IKr and predispose patients to arrhythmias. To investigate whether mTOR produced defects in IKr channel function (protein expression and gating mechanisms), electrophysiology and biochemical assays in HEK293 cells stably expressing hERG1a/1b, and adult guinea pig atrial myocytes were used. Feeding with the saturated fatty acid palmitic acid high-fat diet (HFD) was used to induce lipotoxicity. Lipotoxicity-challenged HEK293 cells displayed an increased density of hERG1a/1b currents due to a targeted and significant increase in hERG1b protein expression. Furthermore, lipotoxicity significantly slowed the hERG1a/1b inactivation kinetics, while the activation and deactivation remained essentially unchanged. mTOR complex 1 (mTORC1) inhibition with rapamycin (RAP) reversed the increase in hERG1a/1b density and inactivation. Compared to lipotoxic myocytes, RAP-treated cells displayed action potential durations (APDs) and IKr densities similar to those of controls. HFD feeding triggered arrhythmogenic changes (increased the IKr density and shortened the APD) in the atria, but this was not observed in low-fat-fed controls. The data are the first to show the modulation of IKr by mTORC1, possibly through the remodeling of hERG1b, in lipotoxic atrial myocytes. These results offer mechanistic insights with implications for targeted therapeutic options for the therapy of acquired supraventricular arrhythmias in obesity and associated pathologies.

Keywords: IKr; atrial myocytes; guinea pig; hERG1a/1b; lipotoxicity; mTOR.

MeSH terms

  • Action Potentials
  • Animals
  • Arrhythmias, Cardiac* / metabolism
  • Guinea Pigs
  • HEK293 Cells
  • Humans
  • Mechanistic Target of Rapamycin Complex 1 / metabolism
  • Myocytes, Cardiac* / metabolism
  • TOR Serine-Threonine Kinases / metabolism

Substances

  • MTOR protein, human
  • Mechanistic Target of Rapamycin Complex 1
  • TOR Serine-Threonine Kinases