Divergent effects of sulforaphane on basal and glucose-stimulated insulin secretion in β-cells: role of reactive oxygen species and induction of endogenous antioxidants

Pharm Res. 2013 Sep;30(9):2248-59. doi: 10.1007/s11095-013-1013-8. Epub 2013 Mar 7.

Abstract

Purpose: Oxidative stress is implicated in pancreatic β-cell dysfunction, yet clinical outcomes of antioxidant therapies on diabetes are inconclusive. Since reactive oxygen species (ROS) can function as signaling intermediates for glucose-stimulated insulin secretion (GSIS), we hypothesize that exogenously boosting cellular antioxidant capacity dampens signaling ROS and GSIS.

Methods: To test the hypothesis, we formulated a mathematical model of redox homeostatic control circuit comprising known feedback and feedforward loops and validated model predictions with plant-derived antioxidant sulforaphane (SFN).

Results: SFN acutely (30-min treatment) stimulated basal insulin secretion in INS-1(832/13) cells and cultured mouse islets, which could be attributed to SFN-elicited ROS as N-acetylcysteine or glutathione ethyl ester suppressed SFN-stimulated insulin secretion. The mathematical model predicted an adapted redox state characteristic of strong induction of endogenous antioxidants but marginally increased ROS under prolonged SFN exposure, a state that attenuates rather than facilitates glucose-stimulated ROS and GSIS. We validated the prediction by demonstrating that although 24-h treatment of INS-1(832/13) cells with low, non-cytotoxic concentrations of SFN (2-10 μM) protected the cells from cytotoxicity by oxidative insult, it markedly suppressed insulin secretion stimulated by 20 mM glucose.

Conclusions: Our study indicates that adaptive induction of endogenous antioxidants by exogenous antioxidants, albeit cytoprotective, inhibits GSIS in β-cells.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Antioxidants / pharmacology*
  • Cell Line
  • Cells, Cultured
  • Glucose / metabolism*
  • Humans
  • Insulin / metabolism*
  • Insulin-Secreting Cells / drug effects*
  • Insulin-Secreting Cells / metabolism
  • Isothiocyanates / pharmacology*
  • Mice
  • Mice, Inbred C57BL
  • Models, Biological
  • Oxidative Stress / drug effects
  • Reactive Oxygen Species / metabolism*
  • Sulfoxides

Substances

  • Antioxidants
  • Insulin
  • Isothiocyanates
  • Reactive Oxygen Species
  • Sulfoxides
  • sulforaphane
  • Glucose