DsbA-L prevents obesity-induced inflammation and insulin resistance by suppressing the mtDNA release-activated cGAS-cGAMP-STING pathway

Proc Natl Acad Sci U S A. 2017 Nov 14;114(46):12196-12201. doi: 10.1073/pnas.1708744114. Epub 2017 Oct 30.

Abstract

Chronic inflammation in adipose tissue plays a key role in obesity-induced insulin resistance. However, the mechanisms underlying obesity-induced inflammation remain elusive. Here we show that obesity promotes mtDNA release into the cytosol, where it triggers inflammatory responses by activating the DNA-sensing cGAS-cGAMP-STING pathway. Fat-specific knockout of disulfide-bond A oxidoreductase-like protein (DsbA-L), a chaperone-like protein originally identified in the mitochondrial matrix, impaired mitochondrial function and promoted mtDNA release, leading to activation of the cGAS-cGAMP-STING pathway and inflammatory responses. Conversely, fat-specific overexpression of DsbA-L protected mice against high-fat diet-induced activation of the cGAS-cGAMP-STING pathway and inflammation. Taken together, we identify DsbA-L as a key molecule that maintains mitochondrial integrity. DsbA-L deficiency promotes inflammation and insulin resistance by activating the cGAS-cGAMP-STING pathway. Our study also reveals that, in addition to its well-characterized roles in innate immune surveillance, the cGAS-cGAMP-STING pathway plays an important role in mediating obesity-induced metabolic dysfunction.

Keywords: DsbA-L; cGAS; inflammation; insulin resistance; obesity.

Publication types

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

MeSH terms

  • 3T3-L1 Cells
  • Adipocytes / metabolism
  • Adipocytes / pathology
  • Animals
  • DNA, Mitochondrial / metabolism*
  • Diet, High-Fat / adverse effects
  • Gene Expression Regulation
  • Glutathione Transferase / deficiency
  • Glutathione Transferase / genetics*
  • Humans
  • Inflammation
  • Insulin Resistance*
  • Male
  • Membrane Proteins / genetics*
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mitochondria / metabolism
  • Mitochondria / pathology
  • Nucleotidyltransferases / genetics*
  • Nucleotidyltransferases / metabolism
  • Obesity / etiology
  • Obesity / genetics*
  • Obesity / metabolism
  • Obesity / pathology
  • Primary Cell Culture
  • Protein Isoforms / genetics
  • Protein Isoforms / metabolism
  • Signal Transduction

Substances

  • DNA, Mitochondrial
  • Membrane Proteins
  • Protein Isoforms
  • Sting1 protein, mouse
  • Glutathione Transferase
  • disulfide-bond A oxidoreductase-like protein DsbA-L, mouse
  • Nucleotidyltransferases
  • cGAS protein, mouse