Caveolin-1/PTRF upregulation constitutes a mechanism for mediating p53-induced cellular senescence: implications for evidence-based therapy of delayed wound healing in diabetes

Am J Physiol Endocrinol Metab. 2013 Oct 15;305(8):E951-63. doi: 10.1152/ajpendo.00189.2013. Epub 2013 Aug 13.

Abstract

A heightened state of oxidative stress and senescence of fibroblasts constitute potential therapeutic targets in nonhealing diabetic wounds. Here, we studied the underlying mechanism mediating diabetes-induced cellular senescence using in vitro cultured dermal fibroblasts and in vivo circular wounds. Our results demonstrated that the total antioxidant capacity and mRNA levels of thioredoxinreductase and glucose-6-phosphate dehydrogenase as well as the ratio of NADPH/NADP were decreased markedly in fibroblasts from patients with type 2 diabetes (DFs). Consistent with this shift in favor of excessive reactive oxygen species, DFs also displayed a significant increase in senescence-associated β-galactosidase activity and phospho-γ-histone H2AX (pH2AX) level. Moreover, the ability of PDGF to promote cell proliferation/migration and regulate the phosphorylation-dependent activation of Akt and ERK1/2 appears to be attenuated as a function of diabetes. Mechanistically, we found that diabetes-induced oxidative stress upregulated caveolin-1 (Cav-1) and PTRF expression, which in turn sequestered Mdm2 away from p53. This process resulted in the activation of a p53/p21-dependent pathway and the induction of premature senescence in DFs. Most of the aforementioned oxidative stress and senescence-based features observed in DFs were recapitulated in a 10-day-old diabetic wound. Intriguingly, we confirmed that the targeted depletion of Cav-1 or PTRF using siRNA- or Vivo-Morpholino antisense-based gene therapy markedly inhibited diabetes/oxidative stress-induced premature senescence and also accelerated tissue repair in this disease state. Overall, our data illuminate Cav-1/PTRF-1 as a key player of a novel signaling pathway that may link a heightened state of oxidative stress to cellular senescence and impaired wound healing in diabetes.

Keywords: polymerase I and transcript release factor.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Caveolin 1 / antagonists & inhibitors
  • Caveolin 1 / genetics
  • Caveolin 1 / metabolism*
  • Cells, Cultured
  • Cellular Senescence*
  • Diabetes Mellitus, Type 2 / complications
  • Diabetes Mellitus, Type 2 / metabolism*
  • Down-Regulation
  • Female
  • Gene Silencing
  • Glucosephosphate Dehydrogenase / genetics
  • Glucosephosphate Dehydrogenase / metabolism
  • Membrane Proteins / antagonists & inhibitors
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Molecular Targeted Therapy
  • Oxidative Stress
  • RNA, Messenger / metabolism
  • RNA-Binding Proteins
  • Rats
  • Rats, Inbred Strains
  • Rats, Wistar
  • Signal Transduction
  • Skin / drug effects
  • Skin / metabolism*
  • Skin / pathology
  • Thioredoxin-Disulfide Reductase / genetics
  • Thioredoxin-Disulfide Reductase / metabolism
  • Tumor Suppressor Protein p53 / metabolism
  • Up-Regulation*
  • Wound Healing* / drug effects

Substances

  • Cav1 protein, rat
  • Caveolin 1
  • Cavin1 protein, rat
  • Membrane Proteins
  • RNA, Messenger
  • RNA-Binding Proteins
  • Tumor Suppressor Protein p53
  • Glucosephosphate Dehydrogenase
  • Thioredoxin-Disulfide Reductase