Obesity-Induced Cellular Senescence Drives Anxiety and Impairs Neurogenesis

Cell Metab. 2019 May 7;29(5):1061-1077.e8. doi: 10.1016/j.cmet.2018.12.008. Epub 2019 Jan 3.

Abstract

Cellular senescence entails a stable cell-cycle arrest and a pro-inflammatory secretory phenotype, which contributes to aging and age-related diseases. Obesity is associated with increased senescent cell burden and neuropsychiatric disorders, including anxiety and depression. To investigate the role of senescence in obesity-related neuropsychiatric dysfunction, we used the INK-ATTAC mouse model, from which p16Ink4a-expressing senescent cells can be eliminated, and senolytic drugs dasatinib and quercetin. We found that obesity results in the accumulation of senescent glial cells in proximity to the lateral ventricle, a region in which adult neurogenesis occurs. Furthermore, senescent glial cells exhibit excessive fat deposits, a phenotype we termed "accumulation of lipids in senescence." Clearing senescent cells from high fat-fed or leptin receptor-deficient obese mice restored neurogenesis and alleviated anxiety-related behavior. Our study provides proof-of-concept evidence that senescent cells are major contributors to obesity-induced anxiety and that senolytics are a potential new therapeutic avenue for treating neuropsychiatric disorders.

Keywords: aging; anxiety; anxiety-like behavior; brain; high-fat diet; lipid droplets; neurogenesis; obesity; senescence; stem cells.

Publication types

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

MeSH terms

  • Animals
  • Anxiety / drug therapy
  • Anxiety / etiology*
  • Astrocytes / metabolism
  • Behavior, Animal / drug effects
  • Brain / cytology
  • Brain / embryology
  • Cells, Cultured
  • Cellular Senescence / drug effects*
  • Cyclin-Dependent Kinase Inhibitor p16 / genetics
  • Dasatinib / pharmacology
  • Diet, High-Fat / adverse effects
  • Disease Models, Animal
  • Female
  • Fibroblasts / metabolism
  • Lipid Droplets
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Neurogenesis*
  • Obesity / complications*
  • Obesity / etiology
  • Quercetin / pharmacology
  • Tacrolimus / analogs & derivatives
  • Tacrolimus / pharmacology
  • Tacrolimus / therapeutic use

Substances

  • AP20187
  • Cdkn2a protein, mouse
  • Cyclin-Dependent Kinase Inhibitor p16
  • Quercetin
  • Dasatinib
  • Tacrolimus