Poly-ADP-ribose polymerase inhibition enhances ischemic and diabetic wound healing by promoting angiogenesis

J Vasc Surg. 2017 Apr;65(4):1161-1169. doi: 10.1016/j.jvs.2016.03.407. Epub 2016 Jun 8.

Abstract

Objective: Chronic nonhealing wounds are a major health problem for patients in the United States and worldwide. Diabetes and ischemia are two major risk factors behind impaired healing of chronic lower extremity wounds. Poly-ADP-ribose polymerase (PARP) is found to be overactivated with both ischemic and diabetic conditions. This study seeks a better understanding of the role of PARP in ischemic and diabetic wound healing, with a specific focus on angiogenesis and vasculogenesis.

Methods: Ischemic and diabetic wounds were created in FVB/NJ mice and an in vitro scratch wound model. PARP inhibitor PJ34 was delivered to the animals at 10 mg/kg/d through implanted osmotic pumps or added to the culture medium, respectively. Animal wound healing was assessed by daily digital photographs. Animal wound tissues, peripheral blood, and bone marrow cells were collected at different time points for further analysis with Western blot and flow cytometry. Scratch wound migration and invasion angiogenesis assays were performed using human umbilical vein endothelial cells (HUVECs). Measurements were reported as mean ± standard deviation. Continuous measurements were compared by t-test. P < .05 was considered statistically significant.

Results: A significant increase in PARP activity was observed under ischemic and diabetic conditions that correlated with delayed wound healing and slower HUVEC migration. The beneficial effect of PARP inhibition with PJ34 on ischemic and diabetic wound healing was observed in both animal and in vitro models. In the animal model, the percentage of wound healing was significantly enhanced from 43% ± 6% to 71% ± 9% (P < .05) by day 7 with the addition of PJ34. PARP inhibition promoted angiogenesis at the ischemic and diabetic wound beds as evidenced by significantly higher levels of endothelial cell markers (vascular endothelial growth factor receptor 2 [VEGFR2] and endothelial nitric oxide synthase) in mice treated with PJ34 compared with controls. Flow cytometry analysis of peripheral blood mononuclear cells showed that PARP inhibition increased mobilization of endothelial progenitor cells (VEGFR2+/CD133+ and VEGFR2+/CD34+) into the systemic circulation. Furthermore, under in vitro hyperglycemia and hypoxia conditions, PARP inhibition enhanced HUVEC migration and invasion in Boyden chamber assays by 80% and 180% (P < .05), respectively.

Conclusions: Delayed healing in ischemic and diabetic wounds is caused by PARP hyperactivity, and PARP inhibition significantly enhanced ischemic and diabetic wound healing by promoting angiogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • AC133 Antigen / metabolism
  • Angiogenesis Inducing Agents / pharmacology*
  • Animals
  • Antigens, CD34 / metabolism
  • Cell Hypoxia
  • Cell Movement / drug effects
  • Cells, Cultured
  • Diabetes Mellitus, Experimental / complications*
  • Diabetes Mellitus, Experimental / enzymology
  • Diabetes Mellitus, Experimental / pathology
  • Diabetes Mellitus, Experimental / physiopathology
  • Diabetic Angiopathies / drug therapy*
  • Diabetic Angiopathies / enzymology
  • Diabetic Angiopathies / etiology
  • Diabetic Angiopathies / pathology
  • Endothelial Progenitor Cells / drug effects
  • Endothelial Progenitor Cells / enzymology
  • Glucose / metabolism
  • Human Umbilical Vein Endothelial Cells / drug effects
  • Human Umbilical Vein Endothelial Cells / enzymology
  • Humans
  • Ischemia / complications*
  • Ischemia / enzymology
  • Ischemia / pathology
  • Male
  • Mice, Knockout
  • Neovascularization, Physiologic / drug effects*
  • Nitric Oxide Synthase Type III / metabolism
  • Phenanthrenes / pharmacology*
  • Poly (ADP-Ribose) Polymerase-1 / antagonists & inhibitors*
  • Poly (ADP-Ribose) Polymerase-1 / deficiency
  • Poly (ADP-Ribose) Polymerase-1 / genetics
  • Poly (ADP-Ribose) Polymerase-1 / metabolism
  • Poly(ADP-ribose) Polymerase Inhibitors / pharmacology*
  • Skin Ulcer / drug therapy*
  • Skin Ulcer / enzymology
  • Skin Ulcer / etiology
  • Skin Ulcer / pathology
  • Time Factors
  • Vascular Endothelial Growth Factor Receptor-2 / metabolism
  • Wound Healing / drug effects*

Substances

  • AC133 Antigen
  • Angiogenesis Inducing Agents
  • Antigens, CD34
  • N-(oxo-5,6-dihydrophenanthridin-2-yl)-N,N-dimethylacetamide hydrochloride
  • Phenanthrenes
  • Poly(ADP-ribose) Polymerase Inhibitors
  • Prom1 protein, mouse
  • Nitric Oxide Synthase Type III
  • Nos3 protein, mouse
  • Parp1 protein, mouse
  • Poly (ADP-Ribose) Polymerase-1
  • Kdr protein, mouse
  • Vascular Endothelial Growth Factor Receptor-2
  • Glucose