Leucine modulates contraction- and insulin-stimulated glucose transport and upstream signaling events in rat skeletal muscle

J Appl Physiol (1985). 2010 Feb;108(2):274-82. doi: 10.1152/japplphysiol.00420.2009. Epub 2009 Nov 25.

Abstract

Leucine has profound effects on glucose metabolism in muscle; however, the effects of leucine on glucose transport in muscle have not been well documented. We investigated the effects of leucine on contraction- and insulin-stimulated glucose transport in isolated rat epitrochlearis muscle in vitro. In the absence of insulin, tetanic contraction increased 3-O-methyl-D-glucose (3-MG) transport and Thr(172) phosphorylation of the catalytic alpha-subunit of 5'-AMP-activated protein kinase (AMPK), a signaling intermediary leading to insulin-independent glucose transport. Leucine (2 mM, 30 min) significantly enhanced contraction-stimulated 3-MG transport and AMPK phosphorylation, accompanied by increased phosphorylation of p70 S6 kinase (p70S6K) Thr(389). The stimulatory effects of leucine on 3-MG transport and AMPK phosphorylation were canceled by STO-609 blockade of Ca(2+)/calmodulin-dependent protein kinase kinase (CaMKK) or rapamycin blockade of p70S6K. On the other hand, leucine blunted insulin-stimulated 3-MG transport and reduced insulin-stimulated Akt Thr(473) phosphorylation. Leucine increased insulin-stimulated p70S6K Thr(389) phosphorylation and enhanced the inhibitory phosphorylation of the insulin receptor substrate 1 (IRS1) Ser(636/639). Furthermore, the effects of leucine on insulin-stimulated 3-MG transport and IRS phosphorylation were abolished by rapamycin. These results indicate that leucine activates contraction-stimulated glucose transport and inhibits insulin-stimulated glucose transport in skeletal muscle by activating mammalian target of rapamycin (mTOR)/p70S6K signaling. Enhanced increases in contraction-stimulated AMPK Thr(172) phosphorylation and insulin-stimulated IRS1 Ser(636/639) phosphorylation might be responsible for these opposing effects of leucine, respectively.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3-O-Methylglucose / metabolism
  • AMP-Activated Protein Kinase Kinases
  • Adenosine Triphosphate / metabolism
  • Animals
  • Biological Transport, Active / drug effects
  • Energy Metabolism / drug effects
  • Glucose / metabolism*
  • Glucose / physiology*
  • Glycogen / metabolism
  • Hypoglycemic Agents / pharmacology*
  • Insulin / pharmacology*
  • Insulin Receptor Substrate Proteins / metabolism
  • Leucine / pharmacology*
  • Male
  • Muscle Contraction / drug effects
  • Muscle, Skeletal / drug effects*
  • Muscle, Skeletal / metabolism*
  • Oncogene Protein v-akt / metabolism
  • Phosphocreatine / metabolism
  • Protein Kinases / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Ribosomal Protein S6 Kinases, 70-kDa / metabolism
  • Signal Transduction / drug effects*

Substances

  • Hypoglycemic Agents
  • Insulin
  • Insulin Receptor Substrate Proteins
  • Irs1 protein, rat
  • Phosphocreatine
  • 3-O-Methylglucose
  • Adenosine Triphosphate
  • Glycogen
  • Protein Kinases
  • Oncogene Protein v-akt
  • Ribosomal Protein S6 Kinases, 70-kDa
  • AMP-Activated Protein Kinase Kinases
  • Leucine
  • Glucose