PGRN induces impaired insulin sensitivity and defective autophagy in hepatic insulin resistance

Mol Endocrinol. 2015 Apr;29(4):528-41. doi: 10.1210/me.2014-1266. Epub 2015 Feb 9.

Abstract

Progranulin (PGRN) has recently emerged as an important regulator for glucose metabolism and insulin sensitivity. However, the underlying mechanisms of PGRN in the regulation of insulin sensitivity and autophagy remain elusive. In this study, we aimed to address the direct effects of PGRN in vivo and to evaluate the potential interaction of impaired insulin sensitivity and autophagic disorders in hepatic insulin resistance. We found that mice treated with PGRN for 21 days exhibited the impaired glucose tolerance and insulin tolerance and hepatic autophagy imbalance as well as defective insulin signaling. Furthermore, treatment of mice with TNF receptor (TNFR)-1 blocking peptide-Fc, a TNFR1 blocking peptide-Fc fusion protein to competitively block the interaction of PGRN and TNFR1, resulted in the restoration of systemic insulin sensitivity and the recovery of autophagy and insulin signaling in liver. Consistent with these findings in vivo, we also observed that PGRN treatment induced defective autophagy and impaired insulin signaling in hepatocytes, with such effects being drastically nullified by the addition of TNFR1 blocking peptide -Fc or TNFR1-small interference RNA via the TNFR1-nuclear factor-κB-dependent manner, indicating the causative role of PGRN in hepatic insulin resistance. In conclusion, our findings supported the notion that PGRN is a key regulator of hepatic insulin resistance and that PGRN may mediate its effects, at least in part, by inducing defective autophagy via TNFR1/nuclear factor-κB.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Autophagy / drug effects*
  • Blood Glucose / metabolism
  • Cells, Cultured
  • Etanercept / pharmacology
  • Female
  • Granulins
  • Hepatocytes / drug effects
  • Hepatocytes / metabolism
  • Insulin / blood
  • Insulin Resistance / physiology*
  • Intercellular Signaling Peptides and Proteins / blood
  • Intercellular Signaling Peptides and Proteins / pharmacology*
  • Lipogenesis / drug effects
  • Liver / drug effects*
  • Liver / metabolism
  • Mice
  • NF-kappa B / metabolism
  • Phosphorylation / drug effects
  • Progranulins
  • RNA, Small Interfering
  • Signal Transduction / drug effects
  • Tumor Necrosis Factor-alpha / antagonists & inhibitors
  • Tumor Necrosis Factor-alpha / genetics

Substances

  • Blood Glucose
  • Granulins
  • Grn protein, mouse
  • Insulin
  • Intercellular Signaling Peptides and Proteins
  • NF-kappa B
  • Progranulins
  • RNA, Small Interfering
  • Tumor Necrosis Factor-alpha
  • Etanercept

Grants and funding

This work was supported by the National Natural Science Foundation of China (Programs 81370899, 81170741, 81472038), National Excellent Young Scientist Program 81222026, and the New Century Excellent Talents in University from the Ministry of Education, China.