Acute exposure of beta-cells to troglitazone decreases insulin hypersecretion via activating AMPK

Biochim Biophys Acta. 2014 Jan;1840(1):577-85. doi: 10.1016/j.bbagen.2013.10.021. Epub 2013 Oct 18.

Abstract

Background: It has been recognized that insulin hypersecretion can lead to the development of insulin resistance and type 2 diabetes mellitus. There is substantial evidence demonstrating that thiazolidinediones are able to delay and prevent the progression of pancreatic β-cell dysfunction. However, the mechanism underlying the protective effect of thiazolidinediones on β-cell function remains elusive.

Methods: We synchronously detected the effects of troglitazone on insulin secretion and AMP-activated protein kinase (AMPK) activity under various conditions in isolated rat islets and MIN6 cells.

Results: Long-term exposure to high glucose stimulated insulin hypersecretion and inhibited AMPK activity in rat islets. Troglitazone-suppressed insulin hypersecretion was closely related to the activation of AMPK. This action was most prominent at the moderate concentration of glucose. Glucose-stimulated insulin secretion was decreased by long-term troglitazone treatment, but significantly increased after the drug withdrawal. Compound C, an AMPK inhibitor, reversed troglitazone-suppressed insulin secretion in MIN6 cells and rat islets. Knockdown of AMPKα2 showed a similar result. In MIN6 cells, troglitazone blocked high glucose-closed ATP-sensitive K(+) (KATP) channel and decreased membrane potential, along with increased voltage-dependent potassium channel currents. Troglitazone suppressed intracellular Ca(2+) response to high glucose, which was abolished by treatment with compound C.

Conclusion: Our results suggest that troglitazone provides β-cell "a rest" through activating AMPK and inhibiting insulin hypersecretion, and thus restores its response to glucose.

General significance: These data support that AMPK activation may be an important mechanism for thiazolidinediones preserving β-cell function.

Keywords: ACC; AMP-activated protein kinase; AMPK; ATP-sensitive K(+) channel; Beta-cell; GSIS; IFG; IGT; Insulin hyperscretion; K(ATP); Kv; PPARγ; TZD; Troglitazone; acetyl-CoA carboxylase; glucose-stimulated insulin secretion; impaired fasting glucose; impaired glucose tolerance; peroxisome proliferator-activated receptor γ; shRNA; short hairpin RNA; thiazolidinediones; voltage-dependent potassium channel.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • AMP-Activated Protein Kinase Kinases
  • Animals
  • Calcium / metabolism*
  • Cells, Cultured
  • Chromans / pharmacology*
  • Electrophysiology
  • Glucose / metabolism
  • Hypoglycemic Agents / pharmacology*
  • Insulin / metabolism*
  • Insulin Secretion
  • Insulin-Secreting Cells / drug effects
  • Insulin-Secreting Cells / metabolism*
  • Male
  • Protein Kinases / chemistry
  • Protein Kinases / genetics
  • Protein Kinases / metabolism*
  • RNA, Small Interfering / genetics
  • Rats
  • Rats, Sprague-Dawley
  • Thiazolidinediones / pharmacology*
  • Troglitazone

Substances

  • Chromans
  • Hypoglycemic Agents
  • Insulin
  • RNA, Small Interfering
  • Thiazolidinediones
  • Protein Kinases
  • AMP-Activated Protein Kinase Kinases
  • Troglitazone
  • Glucose
  • Calcium