Disrupted BMP-9 Signaling Impairs Pulmonary Vascular Integrity in Hepatopulmonary Syndrome

Am J Respir Crit Care Med. 2024 Sep 1;210(5):648-661. doi: 10.1164/rccm.202307-1289OC.

Abstract

Rationale: Hepatopulmonary syndrome (HPS) is a severe complication of liver diseases characterized by abnormal dilation of pulmonary vessels, resulting in impaired oxygenation. Recent research highlights the pivotal role of liver-produced BMP-9 (bone morphogenetic protein-9) in maintaining pulmonary vascular integrity. Objectives: This study aimed to investigate the involvement of BMP-9 in human and experimental HPS. Methods: Circulating BMP-9 levels were measured in 63 healthy control subjects and 203 patients with cirrhosis with or without HPS. Two animal models of portal hypertension were employed: common bile duct ligation with cirrhosis and long-term partial portal vein ligation without cirrhosis. Additionally, the therapeutic effect of low-dose BMP activator FK506 was investigated, and the pulmonary vascular phenotype of BMP-9-knockout rats was analyzed. Measurements and Main Results: Patients with HPS related to compensated cirrhosis exhibited lower levels of circulating BMP-9 compared with patients without HPS. Patients with severe cirrhosis exhibited consistently low levels of BMP-9. HPS characteristics were observed in animal models, including intrapulmonary vascular dilations and an increase in the alveolar-arterial gradient. HPS development in both rat models correlated with reduced intrahepatic BMP-9 expression, decreased circulating BMP-9 level and activity, and impaired pulmonary BMP-9 endothelial pathway. Daily treatment with FK506 for 2 weeks restored the BMP pathway in the lungs, alleviating intrapulmonary vascular dilations and improving gas exchange impairment. Furthermore, BMP-9-knockout rats displayed a pulmonary HPS phenotype, supporting its role in disease progression. Conclusions: The study findings suggest that portal hypertension-induced loss of BMP-9 signaling contributes to HPS development.

Keywords: BMP-9; cirrhosis; hepatopulmonary syndrome; intrapulmonary vascular dilatations; portal hypertension.

MeSH terms

  • Adult
  • Aged
  • Animals
  • Case-Control Studies
  • Disease Models, Animal*
  • Female
  • Growth Differentiation Factor 2*
  • Hepatopulmonary Syndrome* / metabolism
  • Hepatopulmonary Syndrome* / physiopathology
  • Humans
  • Hypertension, Portal / physiopathology
  • Liver Cirrhosis / complications
  • Liver Cirrhosis / physiopathology
  • Lung / metabolism
  • Male
  • Middle Aged
  • Rats
  • Signal Transduction
  • Tacrolimus / pharmacology
  • Tacrolimus / therapeutic use

Substances

  • Growth Differentiation Factor 2
  • Tacrolimus
  • Bmp9 protein, rat