Complement C3 deficiency attenuates chronic hypoxia-induced pulmonary hypertension in mice

PLoS One. 2011;6(12):e28578. doi: 10.1371/journal.pone.0028578. Epub 2011 Dec 14.

Abstract

Background: Evidence suggests a role of both innate and adaptive immunity in the development of pulmonary arterial hypertension. The complement system is a key sentry of the innate immune system and bridges innate and adaptive immunity. To date there are no studies addressing a role for the complement system in pulmonary arterial hypertension.

Methodology/principal findings: Immunofluorescent staining revealed significant C3d deposition in lung sections from IPAH patients and C57Bl6/J wild-type mice exposed to three weeks of chronic hypoxia to induce pulmonary hypertension. Right ventricular systolic pressure and right ventricular hypertrophy were increased in hypoxic vs. normoxic wild-type mice, which were attenuated in C3-/- hypoxic mice. Likewise, pulmonary vascular remodeling was attenuated in the C3-/- mice compared to wild-type mice as determined by the number of muscularized peripheral arterioles and morphometric analysis of vessel wall thickness. The loss of C3 attenuated the increase in interleukin-6 and intracellular adhesion molecule-1 expression in response to chronic hypoxia, but not endothelin-1 levels. In wild-type mice, but not C3-/- mice, chronic hypoxia led to platelet activation as assessed by bleeding time, and flow cytometry of platelets to determine cell surface P-selectin expression. In addition, tissue factor expression and fibrin deposition were increased in the lungs of WT mice in response to chronic hypoxia. These pro-thrombotic effects of hypoxia were abrogated in C3-/- mice.

Conclusions: Herein, we provide compelling genetic evidence that the complement system plays a pathophysiologic role in the development of PAH in mice, promoting pulmonary vascular remodeling and a pro-thrombotic phenotype. In addition we demonstrate C3d deposition in IPAH patients suggesting that complement activation plays a role in the development of PAH in humans.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arterioles / metabolism
  • Arterioles / pathology
  • Biomarkers / metabolism
  • Cell Proliferation
  • Chronic Disease
  • Complement C3 / deficiency*
  • Complement C3 / metabolism
  • Complement C3a / metabolism
  • Complement C5a / metabolism
  • Endothelium, Vascular / pathology
  • Endothelium, Vascular / physiopathology
  • Fibrin / metabolism
  • Gene Deletion
  • Humans
  • Hypertension, Pulmonary / etiology*
  • Hypertension, Pulmonary / physiopathology
  • Hypertension, Pulmonary / prevention & control*
  • Hypoxia / complications*
  • Hypoxia / physiopathology
  • Mice
  • Mice, Inbred C57BL
  • Myocytes, Smooth Muscle / metabolism
  • Myocytes, Smooth Muscle / pathology
  • Platelet Activation
  • Pulmonary Artery / pathology
  • Pulmonary Artery / physiopathology
  • Thromboplastin / metabolism
  • Up-Regulation / genetics

Substances

  • Biomarkers
  • Complement C3
  • Complement C3a
  • Complement C5a
  • Fibrin
  • Thromboplastin