Palmitate-induced insulin resistance causes actin filament stiffness and GLUT4 mis-sorting without altered Akt signalling

J Cell Sci. 2023 Nov 1;136(21):jcs261300. doi: 10.1242/jcs.261300. Epub 2023 Nov 8.

Abstract

Skeletal muscle insulin resistance, a major contributor to type 2 diabetes, is linked to the consumption of saturated fats. This insulin resistance arises from failure of insulin-induced translocation of glucose transporter type 4 (GLUT4; also known as SLC2A4) to the plasma membrane to facilitate glucose uptake into muscle. The mechanisms of defective GLUT4 translocation are poorly understood, limiting development of insulin-sensitizing therapies targeting muscle glucose uptake. Although many studies have identified early insulin signalling defects and suggest that they are responsible for insulin resistance, their cause-effect has been debated. Here, we find that the saturated fat palmitate (PA) causes insulin resistance owing to failure of GLUT4 translocation in skeletal muscle myoblasts and myotubes without impairing signalling to Akt2 or AS160 (also known as TBC1D4). Instead, PA altered two basal-state events: (1) the intracellular localization of GLUT4 and its sorting towards a perinuclear storage compartment, and (2) actin filament stiffness, which prevents Rac1-dependent actin remodelling. These defects were triggered by distinct mechanisms, respectively protein palmitoylation and endoplasmic reticulum (ER) stress. Our findings highlight that saturated fats elicit muscle cell-autonomous dysregulation of the basal-state machinery required for GLUT4 translocation, which 'primes' cells for insulin resistance.

Keywords: Actin cytoskeleton; GLUT4; Insulin resistance; Palmitate.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actin Cytoskeleton / metabolism
  • Diabetes Mellitus, Type 2* / metabolism
  • Glucose / metabolism
  • Glucose Transporter Type 4
  • Humans
  • Insulin / metabolism
  • Insulin Resistance* / physiology
  • Muscle, Skeletal / metabolism
  • Palmitates / metabolism
  • Palmitates / pharmacology
  • Protein Transport
  • Proto-Oncogene Proteins c-akt / metabolism

Substances

  • Palmitates
  • Proto-Oncogene Proteins c-akt
  • Glucose Transporter Type 4
  • Insulin
  • Glucose

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