Disruption of cortical actin in skeletal muscle demonstrates an essential role of the cytoskeleton in glucose transporter 4 translocation in insulin-sensitive tissues

J Biol Chem. 2004 Sep 24;279(39):40699-706. doi: 10.1074/jbc.M402697200. Epub 2004 Jul 6.

Abstract

Cell culture work suggests that signaling to polymerize cortical filamentous actin (F-actin) represents a required pathway for the optimal redistribution of the insulin-responsive glucose transporter, GLUT4, to the plasma membrane. Recent in vitro study further suggests that the actin-regulatory neural Wiskott-Aldrich syndrome protein (N-WASP) mediates the effect of insulin on the actin filament network. Here we tested whether similar cytoskeletal mechanics are essential for insulin-regulated glucose transport in isolated rat epitrochlearis skeletal muscle. Microscopic analysis revealed that cortical F-actin is markedly diminished in muscle exposed to latrunculin B. Depolymerization of cortical F-actin with latrunculin B caused a time- and concentration-dependent decline in 2-deoxyglucose transport. The loss of cortical F-actin and glucose transport was paralleled by a decline in insulin-stimulated GLUT4 translocation, as assessed by photolabeling of cell surface GLUT4 with Bio-LC-ATB-BMPA. Although latrunculin B impaired insulin-stimulated GLUT4 translocation and glucose transport, activation of phosphatidylinositol 3-kinase and Akt by insulin was not rendered ineffective. In contrast, the ability of insulin to elicit the cortical F-actin localization of N-WASP was abrogated. These data provide the first evidence that actin cytoskeletal mechanics are an essential feature of the glucose transport process in intact skeletal muscle. Furthermore, these findings support a distal actin-based role for N-WASP in insulin action in vivo.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / metabolism*
  • Animals
  • Biological Transport
  • Bridged Bicyclo Compounds, Heterocyclic / chemistry*
  • Cytoskeleton / metabolism*
  • Deoxyglucose / chemistry
  • Deoxyglucose / metabolism
  • Dose-Response Relationship, Drug
  • Glucose / metabolism
  • Glucose Transporter Type 4
  • Insulin / metabolism*
  • Insulin Receptor Substrate Proteins
  • Light
  • Male
  • Microscopy, Confocal
  • Monosaccharide Transport Proteins / metabolism
  • Monosaccharide Transport Proteins / physiology*
  • Muscle Proteins / metabolism
  • Muscle Proteins / physiology*
  • Muscle, Skeletal / metabolism*
  • Muscles / metabolism
  • Nerve Tissue Proteins / metabolism*
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphoproteins / metabolism
  • Protein Serine-Threonine Kinases / metabolism
  • Protein Transport
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins c-akt
  • Rats
  • Rats, Wistar
  • Thiazoles / chemistry*
  • Thiazolidines
  • Time Factors
  • Wiskott-Aldrich Syndrome Protein, Neuronal

Substances

  • Actins
  • Bridged Bicyclo Compounds, Heterocyclic
  • Glucose Transporter Type 4
  • Insulin
  • Insulin Receptor Substrate Proteins
  • Irs1 protein, rat
  • Monosaccharide Transport Proteins
  • Muscle Proteins
  • Nerve Tissue Proteins
  • Phosphoproteins
  • Proto-Oncogene Proteins
  • Slc2a4 protein, rat
  • Thiazoles
  • Thiazolidines
  • Wasl protein, rat
  • Wiskott-Aldrich Syndrome Protein, Neuronal
  • Deoxyglucose
  • Akt1 protein, rat
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt
  • Glucose
  • latrunculin B