A Tbc1d1 Ser231Ala-knockin mutation partially impairs AICAR- but not exercise-induced muscle glucose uptake in mice

Diabetologia. 2017 Feb;60(2):336-345. doi: 10.1007/s00125-016-4151-9. Epub 2016 Nov 8.

Abstract

Aims/hypothesis: TBC1D1 (tre-2/USP6, BUB2, cdc16 domain family member 1) is a Rab GTPase-activating protein (RabGAP) that has been implicated in regulating GLUT4 trafficking. TBC1D1 can be phosphorylated by the AMP-activated protein kinase (AMPK) on Ser231, which consequently interacts with 14-3-3 proteins. Given the key role for AMPK in regulating insulin-independent muscle glucose uptake, we hypothesised that TBC1D1-Ser231 phosphorylation and/or 14-3-3 binding may mediate AMPK-governed glucose homeostasis.

Methods: Whole-body glucose homeostasis and muscle glucose uptake were assayed in mice bearing a Tbc1d1 Ser231Ala-knockin mutation or harbouring skeletal muscle-specific Ampkα1/α2 (also known as Prkaa1/2) double-knockout mutations in response to an AMPK-activating agent, 5-aminoimidazole-4-carboxamide-1-β-D-ribofuranoside (AICAR). Exercise-induced muscle glucose uptake and exercise capacity were also determined in the Tbc1d1 Ser231Ala-knockin mice.

Results: Skeletal muscle-specific deletion of Ampkα1/a2 in mice prevented AICAR-induced hypoglycaemia and muscle glucose uptake. The Tbc1d1 Ser231Ala-knockin mutation also attenuated the glucose-lowering effect of AICAR in mice. Glucose uptake and cell surface GLUT4 content were significantly lower in muscle isolated from the Tbc1d1 Ser231Ala-knockin mice upon stimulation with a submaximal dose of AICAR. However, this Tbc1d1 Ser231Ala-knockin mutation neither impaired exercise-induced muscle glucose uptake nor affected exercise capacity in mice.

Conclusions/interpretation: TBC1D1-Ser231 phosphorylation and/or 14-3-3 binding partially mediates AMPK-governed glucose homeostasis and muscle glucose uptake in a context-dependent manner.

Keywords: 14-3-3; AMPK; Glucose uptake; Phosphorylation; TBC1D1.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 14-3-3 Proteins / genetics
  • 14-3-3 Proteins / metabolism
  • AMP-Activated Protein Kinases / genetics
  • AMP-Activated Protein Kinases / metabolism
  • Aminoimidazole Carboxamide / analogs & derivatives*
  • Aminoimidazole Carboxamide / metabolism
  • Animals
  • Biological Transport
  • Exercise / physiology*
  • GTPase-Activating Proteins / genetics*
  • Glucose / metabolism*
  • Glucose Transporter Type 4 / genetics
  • Glucose Transporter Type 4 / metabolism
  • Humans
  • Immunoblotting
  • Immunoprecipitation
  • Mice
  • Muscle, Skeletal / metabolism
  • Mutation / genetics
  • Phosphorylation
  • Ribonucleotides / genetics
  • Ribonucleotides / metabolism*
  • Signal Transduction / genetics
  • Signal Transduction / physiology

Substances

  • 14-3-3 Proteins
  • GTPase-Activating Proteins
  • Glucose Transporter Type 4
  • Ribonucleotides
  • TBC1D1 protein, human
  • Aminoimidazole Carboxamide
  • AMPK alpha1 subunit, mouse
  • AMPK alpha2 subunit, mouse
  • AMP-Activated Protein Kinases
  • AICA ribonucleotide
  • Glucose