Reduction of plasma membrane glutamate transport potentiates insulin but not glucagon secretion in pancreatic islet cells

Mol Cell Endocrinol. 2011 May 16;338(1-2):46-57. doi: 10.1016/j.mce.2011.02.019. Epub 2011 Mar 1.

Abstract

Glutamate is generated during nutrient stimulation of pancreatic islets and has been proposed to act both as an intra- and extra-cellular messenger molecule. We demonstrate that glutamate is not co-secreted with the hormones from intact islets or purified α- and β-cells. Fractional glutamate release was 5-50 times higher than hormone secretion. Furthermore, various hormone secretagogues did not elicit glutamate efflux. Interestingly, epinephrine even decreased glutamate release while increasing glucagon secretion. Rather than being co-secreted with hormones, we show that glutamate is mainly released via plasma membrane excitatory amino acid transporters (EAAT) by uptake reversal. Transcripts for EAAT1, 2 and 3 were present in both rat α- and β-cells. Inhibition of EAATs by L-trans-pyrrolidine-2,4-dicarboxylate augmented intra-cellular glutamate and α-ketoglutarate contents and potentiated glucose-stimulated insulin secretion from islets and purified β-cells without affecting glucagon secretion from α-cells. In conclusion, intra-cellular glutamate-derived metabolite pools are linked to glucose-stimulated insulin but not glucagon secretion.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alanine / metabolism
  • Animals
  • Aspartic Acid / metabolism
  • Cell Membrane / metabolism
  • Cells, Cultured
  • Dicarboxylic Acids / pharmacology
  • Epinephrine / pharmacology
  • Glucagon / metabolism*
  • Glucagon-Secreting Cells / metabolism*
  • Glucose / metabolism
  • Glucose / pharmacology
  • Glutamate Plasma Membrane Transport Proteins / antagonists & inhibitors*
  • Glutamate Plasma Membrane Transport Proteins / genetics
  • Glutamate Plasma Membrane Transport Proteins / metabolism
  • Glutamic Acid / metabolism*
  • Glutamine / metabolism
  • Insulin / metabolism*
  • Insulin Secretion
  • Insulin-Secreting Cells / metabolism*
  • Ketoglutaric Acids / metabolism
  • Malates / metabolism
  • Male
  • Pyrrolidines / pharmacology
  • Rats
  • Rats, Wistar
  • Transcription, Genetic
  • gamma-Aminobutyric Acid / metabolism

Substances

  • Dicarboxylic Acids
  • Glutamate Plasma Membrane Transport Proteins
  • Insulin
  • Ketoglutaric Acids
  • Malates
  • Pyrrolidines
  • Glutamine
  • Aspartic Acid
  • Glutamic Acid
  • gamma-Aminobutyric Acid
  • malic acid
  • Glucagon
  • pyrrolidine-2,4-dicarboxylic acid
  • Glucose
  • Alanine
  • Epinephrine