Glutamate is an essential mediator in glutamine-amplified insulin secretion

J Diabetes Investig. 2021 Jun;12(6):920-930. doi: 10.1111/jdi.13497. Epub 2021 Feb 17.

Abstract

Aims/introduction: Glutamine is the most abundant amino acid in the circulation. In this study, we investigated cell signaling in the amplification of insulin secretion by glutamine.

Materials and methods: Clonal pancreatic β-cells MIN6-K8, wild-type B6 mouse islets, glutamate dehydrogenase (GDH) knockout clonal β-cells (Glud1KOβCL), and glutamate-oxaloacetate transaminase 1 (GOT1) knockout clonal β-cells (Got1KOβCL) were studied. Insulin secretion from these cells and islets was examined under various conditions, and intracellular glutamine metabolism was assessed by metabolic flux analysis. Intracellular Ca2+ concentration ([Ca2+ ]i ) was also measured.

Results: Glutamine dose-dependently amplified insulin secretion in the presence of high glucose in both MIN6-K8 cells and Glud1KOβCL. Inhibition of glutaminases, the enzymes that convert glutamine to glutamate, dramatically reduced the glutamine-amplifying effect on insulin secretion. A substantial amount of glutamate was produced from glutamine through direct conversion by glutaminases. Glutamine also increased [Ca2+ ]i at high glucose, which was abolished by inhibition of glutaminases. Glutamic acid dimethylester (dm-Glu), a membrane permeable glutamate precursor that is converted to glutamate in cells, increased [Ca2+ ]i as well as induced insulin secretion at high glucose. These effects of glutamine and dm-Glu were dependent on calcium influx. Glutamine also induced insulin secretion in clonal β-cells MIN6-m14, which otherwise exhibit no insulin secretory response to glucose.

Conclusions: Glutamate converted from glutamine is an essential mediator that enhances calcium signaling in the glutamine-amplifying effect on insulin secretion. Our data also suggest that glutamine exerts a permissive effect on glucose-induced insulin secretion.

Keywords: Glutamate; Glutamine; Insulin secretion.

MeSH terms

  • Animals
  • Aspartate Aminotransferase, Cytoplasmic
  • Cells, Cultured
  • Glucose / metabolism
  • Glutamate Dehydrogenase
  • Glutamic Acid / metabolism*
  • Glutamine / metabolism*
  • Insulin / metabolism
  • Insulin Secretion / physiology*
  • Insulin-Secreting Cells / metabolism*
  • Islets of Langerhans / cytology
  • Mice
  • Signal Transduction

Substances

  • Insulin
  • Glutamine
  • Glutamic Acid
  • Glutamate Dehydrogenase
  • Aspartate Aminotransferase, Cytoplasmic
  • Glucose