High insulin-induced down-regulation of Erk-1/IGF-1R/FGFR-1 signaling is required for oxidative stress-mediated apoptosis of adipose-derived stem cells

J Cell Physiol. 2014 Dec;229(12):2077-87. doi: 10.1002/jcp.24667.

Abstract

Homeostasis of adipose tissue requires highly coordinated response between circulating factors and cell population. Human adult adipose-derived stem cells (ASCs) display multiple differentiation properties and are sensitive to insulin stimulation. Insulin resistance and high level of circulating insulin characterize patients with type 2 diabetes and obesity. At physiological concentration, insulin promoted proliferation and survival of ASCs in vitro, whereas high insulin level induced their dose-dependent proliferative arrest and apoptosis. Insulin-induced apoptotic commitment depended on the down-regulation of Erk-1, insulin growth factor-1 receptor (IGF-1R), and fibroblast growth factor receptor-1 (FGFR-1)-mediated signaling. Specific inhibition of Erk-1/2, IGF-1R, and FGFR activity promoted ASC apoptosis but did not increase insulin effects, whereas EGFR and ErbB2 inhibition potentiated insulin-induced apoptosis. FGFRs and EGFR inhibition reduced ASC adipogenic differentiation, whereas Erk-1/2 and IGF-1R inhibition was ineffective. Insulin-induced apoptosis associated to reactive oxygen species (ROS) accumulation and inhibition of NADPH oxidase 4 (Nox4) activity prevented ASC apoptosis. Moreover, specific inhibition of Erk-1/2, IGF-1R, and FGFR-1 activity promoted ROS generation and this effect was not cumulative with that of insulin alone. Our data indicate that insulin concentration is a critical regulatory switch between proliferation and survival of ASCs. High insulin level-induced apoptotic machinery involves Nox4-generated oxidative stress and the down-regulation of a complex receptor signaling, partially distinct from that influencing adipogenic differentiation of ASCs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adipose Tissue / growth & development
  • Adipose Tissue / metabolism
  • Apoptosis / drug effects
  • Gene Expression Regulation, Developmental / drug effects
  • Humans
  • Insulin / administration & dosage*
  • Mitogen-Activated Protein Kinase 3 / biosynthesis*
  • NADPH Oxidase 4
  • NADPH Oxidases / metabolism
  • Oxidative Stress / drug effects
  • Receptor, Fibroblast Growth Factor, Type 1 / biosynthesis*
  • Receptor, IGF Type 1 / biosynthesis*
  • Signal Transduction
  • Stem Cells / cytology
  • Stem Cells / metabolism

Substances

  • Insulin
  • NADPH Oxidase 4
  • NADPH Oxidases
  • NOX4 protein, human
  • FGFR1 protein, human
  • Receptor, Fibroblast Growth Factor, Type 1
  • Receptor, IGF Type 1
  • Mitogen-Activated Protein Kinase 3