Bmal1 and β-cell clock are required for adaptation to circadian disruption, and their loss of function leads to oxidative stress-induced β-cell failure in mice

Mol Cell Biol. 2013 Jun;33(11):2327-38. doi: 10.1128/MCB.01421-12. Epub 2013 Apr 1.

Abstract

Circadian disruption has deleterious effects on metabolism. Global deletion of Bmal1, a core clock gene, results in β-cell dysfunction and diabetes. However, it is unknown if this is due to loss of cell-autonomous function of Bmal1 in β cells. To address this, we generated mice with β-cell clock disruption by deleting Bmal1 in β cells (β-Bmal1(-/-)). β-Bmal1(-/-) mice develop diabetes due to loss of glucose-stimulated insulin secretion (GSIS). This loss of GSIS is due to the accumulation of reactive oxygen species (ROS) and consequent mitochondrial uncoupling, as it is fully rescued by scavenging of the ROS or by inhibition of uncoupling protein 2. The expression of the master antioxidant regulatory factor Nrf2 (nuclear factor erythroid 2-related factor 2) and its targets, Sesn2, Prdx3, Gclc, and Gclm, was decreased in β-Bmal1(-/-) islets, which may contribute to the observed increase in ROS accumulation. In addition, by chromatin immunoprecipitation experiments, we show that Nrf2 is a direct transcriptional target of Bmal1. Interestingly, simulation of shift work-induced circadian misalignment in mice recapitulates many of the defects seen in Bmal1-deficient islets. Thus, the cell-autonomous function of Bmal1 is required for normal β-cell function by mitigating oxidative stress and serves to preserve β-cell function in the face of circadian misalignment.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • ARNTL Transcription Factors / genetics
  • ARNTL Transcription Factors / metabolism*
  • Adaptation, Physiological / physiology*
  • Animals
  • Antioxidants / metabolism
  • Circadian Rhythm / physiology*
  • Diabetes Mellitus, Experimental / genetics
  • Gene Expression Regulation
  • Glucose / metabolism
  • Hyperglycemia / genetics
  • Insulin / metabolism
  • Insulin Secretion
  • Insulin-Secreting Cells / pathology
  • Insulin-Secreting Cells / physiology*
  • Ion Channels / genetics
  • Ion Channels / metabolism
  • Male
  • Mice
  • Mice, Transgenic
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism
  • Oxidative Stress / physiology*
  • Reactive Oxygen Species / metabolism
  • Uncoupling Protein 2

Substances

  • ARNTL Transcription Factors
  • Antioxidants
  • Bmal1 protein, mouse
  • Insulin
  • Ion Channels
  • Mitochondrial Proteins
  • Reactive Oxygen Species
  • Ucp2 protein, mouse
  • Uncoupling Protein 2
  • Glucose