Sildenafil attenuates hypoxic pulmonary remodelling by inhibiting bone marrow progenitor cells

J Cell Mol Med. 2017 May;21(5):871-880. doi: 10.1111/jcmm.13026. Epub 2016 Nov 18.

Abstract

The recruitment of bone marrow (BM)-derived progenitor cells to the lung is related to pulmonary remodelling and the pathogenesis of pulmonary hypertension (PH). Although sildenafil is a known target in PH treatment, the underlying molecular mechanism is still elusive. To test the hypothesis that the therapeutic effect of sildenafil is linked to the reduced recruitment of BM-derived progenitor cells, we induced pulmonary remodelling in rats by two-week exposure to chronic hypoxia (CH, 10% oxygen), a trigger of BM-derived progenitor cells. Rats were treated with either placebo (saline) or sildenafil (1.4 mg/kg/day ip) during CH. Control rats were kept in room air (21% oxygen) with no treatment. As expected, sildenafil attenuated the CH-induced increase in right ventricular systolic pressure and right ventricular hypertrophy. However, sildenafil suppressed the CH-induced increase in c-kit+ cells in the adventitia of pulmonary arteries. Moreover, sildenafil reduced the number of c-kit+ cells that colocalize with tyrosine kinase receptor 2 (VEGF-R2) and CD68 (a marker for macrophages), indicating a positive effect on moderating hypoxia-induced smooth muscle cell proliferation and inflammation without affecting the pulmonary levels of hypoxia-inducible factor (HIF)-1α. Furthermore, sildenafil depressed the number of CXCR4+ cells. Collectively, these findings indicate that the improvement in pulmonary haemodynamic by sildenafil is linked to decreased recruitment of BM-derived c-kit+ cells in the pulmonary tissue. The attenuation of the recruitment of BM-derived c-kit+ cells by sildenafil may provide novel therapeutic insights into the control of pulmonary remodelling.

Keywords: CXCR4 receptor; bone marrow progenitor cells; c-kit cells; chronic hypoxia; pulmonary hypertension; sildenafil.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blood Gas Analysis
  • Bone Marrow Cells / drug effects
  • Bone Marrow Cells / metabolism
  • Bone Marrow Cells / pathology*
  • Cell Hypoxia / drug effects
  • Cyclic GMP / metabolism
  • Inflammation / pathology
  • Lung / pathology*
  • Male
  • Muscles / drug effects
  • Muscles / pathology
  • Proto-Oncogene Proteins c-kit / metabolism
  • Rats, Sprague-Dawley
  • Receptors, CXCR4 / metabolism
  • Sildenafil Citrate / pharmacology*
  • Stem Cells / drug effects
  • Stem Cells / metabolism
  • Stem Cells / pathology*
  • Vascular Endothelial Growth Factor Receptor-2 / metabolism

Substances

  • Receptors, CXCR4
  • Sildenafil Citrate
  • Proto-Oncogene Proteins c-kit
  • Vascular Endothelial Growth Factor Receptor-2
  • Cyclic GMP