Glucagon-like Peptide 1 Receptor Activation Inhibits Microglial Pyroptosis via Promoting Mitophagy to Alleviate Depression-like Behaviors in Diabetic Mice

Nutrients. 2022 Dec 21;15(1):38. doi: 10.3390/nu15010038.

Abstract

Depression is a frequent and serious comorbidity associated with diabetes which adversely affects prognosis and quality of life. Glucagon-like peptide-1 receptor (GLP-1R) agonists, widely used in the treatment of diabetes, are reported to exert neuroprotective effects in the central nervous system. Thus, we aim to evaluate whether GLP-1R agonist exendin-4 (EX-4) could alleviate depression-like behaviors in diabetic mice and to explore its underlying mechanism. The antidepressant effects of EX-4 were evaluated using behavioral tests in db/db mice. The effects of EX-4 on microglial pyroptosis and neuroinflammation were assessed in N9 microglial cells. EX-4 administration alleviated depression-like behaviors in diabetic db/db mice. GLP-1R activation by EX-4 significantly suppressed microglial pyroptosis and neuroinflammation by downregulation of gasdermin D (GSDMD) and interleukin (IL)-1β in diabetic mice and lipopolysaccharide (LPS)-primed N9 microglia. Mechanistically, GLP-1R activation improved mitochondrial function and promoted mitophagy by decreasing the accumulation of mitochondrial reactive oxygen species (mtROS) and intracellular ROS production. EX-4 exhibits antidepressant effects in depression associated with diabetes in diabetic mice, which may be mediated by inhibiting microglial pyroptisis via promoting mitophagy. It is supposed that GLP-1R agonists may be a promising therapy in depression associated with diabetes.

Keywords: GLP-1 receptor; depression; diabetes; microglia; mitophagy; pyroptosis.

MeSH terms

  • Animals
  • Antidepressive Agents / pharmacology
  • Antidepressive Agents / therapeutic use
  • Depression / drug therapy
  • Depression / etiology
  • Diabetes Mellitus, Experimental* / complications
  • Exenatide / pharmacology
  • Glucagon-Like Peptide 1
  • Glucagon-Like Peptide-1 Receptor
  • Mice
  • Microglia*
  • Mitophagy
  • Neuroinflammatory Diseases
  • Pyroptosis
  • Quality of Life

Substances

  • Glucagon-Like Peptide-1 Receptor
  • Exenatide
  • Glucagon-Like Peptide 1
  • Antidepressive Agents

Grants and funding

This research was funded by grants from National Natural Science Foundation of China (No. 81571278; No. 82003734; No. 82071474; No. 81771420), the Shanxi Key Research and Development Program (No. 2020SF088), Natural Science Basic Research Program of Shaanxi Province (No. 2022JQ869), and China Postdoctoral Science Foundation (No. 70 General Fund).