Tolbutamide controls glucagon release from mouse islets differently than glucose: involvement of K(ATP) channels from both α-cells and δ-cells

Diabetes. 2013 May;62(5):1612-22. doi: 10.2337/db12-0347. Epub 2013 Feb 4.

Abstract

We evaluated the role of ATP-sensitive K⁺ (K(ATP)) channels, somatostatin, and Zn²⁺ in the control of glucagon secretion from mouse islets. Switching from 1 to 7 mmol/L glucose inhibited glucagon release. Diazoxide did not reverse the glucagonostatic effect of glucose. Tolbutamide decreased glucagon secretion at 1 mmol/L glucose (G1) but stimulated it at 7 mmol/L glucose (G7). The reduced glucagon secretion produced by high concentrations of tolbutamide or diazoxide, or disruption of K(ATP) channels (Sur1(-/-) mice) at G1 could be inhibited further by G7. Removal of the somatostatin paracrine influence (Sst(-/-) mice or pretreatement with pertussis toxin) strongly increased glucagon release, did not prevent the glucagonostatic effect of G7, and unmasked a marked glucagonotropic effect of tolbutamide. Glucose inhibited glucagon release in the absence of functional K(ATP) channels and somatostatin signaling. Knockout of the Zn²⁺ transporter ZnT8 (ZnT8(-/-) mice) did not prevent the glucagonostatic effect of glucose. In conclusion, glucose can inhibit glucagon release independently of Zn²⁺, K(ATP) channels, and somatostatin. Closure of K(ATP) channels controls glucagon secretion by two mechanisms, a direct stimulation of α-cells and an indirect inhibition via somatostatin released from δ-cells. The net effect on glucagon release results from a balance between both effects.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP-Binding Cassette Transporters / genetics
  • ATP-Binding Cassette Transporters / metabolism
  • Animals
  • Cation Transport Proteins / genetics
  • Cation Transport Proteins / metabolism
  • Crosses, Genetic
  • Diazoxide / pharmacology
  • Glucagon / metabolism*
  • Glucose / metabolism
  • Hypoglycemic Agents / pharmacology*
  • Insulin-Secreting Cells / drug effects*
  • Insulin-Secreting Cells / metabolism
  • Islets of Langerhans / drug effects*
  • Islets of Langerhans / metabolism
  • KATP Channels / agonists
  • KATP Channels / antagonists & inhibitors
  • KATP Channels / metabolism*
  • Membrane Transport Modulators / pharmacology
  • Mice
  • Mice, Knockout
  • Osmolar Concentration
  • Potassium Channel Blockers / pharmacology
  • Potassium Channels, Inwardly Rectifying / genetics
  • Potassium Channels, Inwardly Rectifying / metabolism
  • Receptors, Drug / genetics
  • Receptors, Drug / metabolism
  • Somatostatin / genetics
  • Somatostatin / metabolism
  • Somatostatin-Secreting Cells / drug effects*
  • Somatostatin-Secreting Cells / metabolism
  • Sulfonylurea Receptors
  • Tissue Culture Techniques
  • Tolbutamide / pharmacology*
  • Zinc Transporter 8

Substances

  • ATP-Binding Cassette Transporters
  • Abcc8 protein, mouse
  • Cation Transport Proteins
  • Hypoglycemic Agents
  • KATP Channels
  • Membrane Transport Modulators
  • Potassium Channel Blockers
  • Potassium Channels, Inwardly Rectifying
  • Receptors, Drug
  • Slc30a8 protein, mouse
  • Sulfonylurea Receptors
  • Zinc Transporter 8
  • Somatostatin
  • Glucagon
  • Tolbutamide
  • Glucose
  • Diazoxide