Pancreastatin-dependent inflammatory signaling mediates obesity-induced insulin resistance

Diabetes. 2015 Jan;64(1):104-16. doi: 10.2337/db13-1747. Epub 2014 Jul 21.

Abstract

Chromogranin A knockout (Chga-KO) mice exhibit enhanced insulin sensitivity despite obesity. Here, we probed the role of the chromogranin A-derived peptide pancreastatin (PST: CHGA(273-301)) by investigating the effect of diet-induced obesity (DIO) on insulin sensitivity of these mice. We found that on a high-fat diet (HFD), Chga-KO mice (KO-DIO) remain more insulin sensitive than wild-type DIO (WT-DIO) mice. Concomitant with this phenotype is enhanced Akt and AMPK signaling in muscle and white adipose tissue (WAT) as well as increased FoxO1 phosphorylation and expression of mature Srebp-1c in liver and downregulation of the hepatic gluconeogenic genes, Pepck and G6pase. KO-DIO mice also exhibited downregulation of cytokines and proinflammatory genes and upregulation of anti-inflammatory genes in WAT, and peritoneal macrophages from KO mice displayed similarly reduced proinflammatory gene expression. The insulin-sensitive, anti-inflammatory phenotype of KO-DIO mice is masked by supplementing PST. Conversely, a PST variant peptide PSTv1 (PST-NΔ3: CHGA(276-301)), lacking PST activity, simulated the KO phenotype by sensitizing WT-DIO mice to insulin. In summary, the reduced inflammation due to PST deficiency prevented the development of insulin resistance in KO-DIO mice. Thus, obesity manifests insulin resistance only in the presence of PST, and in its absence obesity is dissociated from insulin resistance.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adipose Tissue / immunology
  • Adipose Tissue / metabolism
  • Animals
  • Cells, Cultured
  • Chemotaxis / immunology
  • Chromogranin A / genetics
  • Chromogranin A / immunology*
  • Chromogranin A / metabolism
  • Forkhead Box Protein O1
  • Forkhead Transcription Factors / immunology
  • Forkhead Transcription Factors / metabolism
  • Glucose Intolerance / drug therapy
  • Glucose Intolerance / immunology
  • Glucose Intolerance / metabolism
  • Insulin Resistance / immunology
  • Macrophages, Peritoneal / cytology
  • Macrophages, Peritoneal / immunology
  • Macrophages, Peritoneal / metabolism
  • Male
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Obesity / drug therapy
  • Obesity / immunology*
  • Obesity / metabolism*
  • Pancreatic Hormones / immunology
  • Pancreatic Hormones / metabolism
  • Pancreatic Hormones / pharmacology*
  • Panniculitis / drug therapy
  • Panniculitis / immunology*
  • Panniculitis / metabolism
  • Signal Transduction / drug effects
  • Signal Transduction / immunology*
  • Sterol Regulatory Element Binding Protein 1 / immunology
  • Sterol Regulatory Element Binding Protein 1 / metabolism

Substances

  • Chromogranin A
  • Forkhead Box Protein O1
  • Forkhead Transcription Factors
  • Foxo1 protein, mouse
  • Pancreatic Hormones
  • Srebf1 protein, mouse
  • Sterol Regulatory Element Binding Protein 1
  • chromogranin A, mouse
  • pancreastatin-52