PBX transcription factors drive pulmonary vascular adaptation to birth

J Clin Invest. 2018 Feb 1;128(2):655-667. doi: 10.1172/JCI93395. Epub 2017 Dec 18.

Abstract

A critical event in the adaptation to extrauterine life is relaxation of the pulmonary vasculature at birth, allowing for a rapid increase in pulmonary blood flow that is essential for efficient gas exchange. Failure of this transition leads to pulmonary hypertension (PH), a major cause of newborn mortality associated with preterm birth, infection, hypoxia, and malformations including congenital diaphragmatic hernia (CDH). While individual vasoconstrictor and dilator genes have been identified, the coordination of their expression is not well understood. Here, we found that lung mesenchyme-specific deletion of CDH-implicated genes encoding pre-B cell leukemia transcription factors (Pbx) led to lethal PH in mice shortly after birth. Loss of Pbx genes resulted in the misexpression of both vasoconstrictors and vasodilators in multiple pathways that converge to increase phosphorylation of myosin in vascular smooth muscle (VSM) cells, causing persistent constriction. While targeting endothelin and angiotensin, which are upstream regulators that promote VSM contraction, was not effective, treatment with the Rho-kinase inhibitor Y-27632 reduced vessel constriction and PH in Pbx-mutant mice. These results demonstrate a lung-intrinsic, herniation-independent cause of PH in CDH. More broadly, our findings indicate that neonatal PH can result from perturbation of multiple pathways and suggest that targeting the downstream common effectors may be a more effective treatment for neonatal PH.

Keywords: Cardiovascular disease; Development; Genetics; Mouse models; Respiration.

Publication types

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

MeSH terms

  • Alleles
  • Animals
  • Apoptosis
  • Cell Proliferation
  • Disease Models, Animal
  • Echocardiography
  • Elastin / metabolism
  • Female
  • Gene Deletion
  • Hernias, Diaphragmatic, Congenital / etiology*
  • Homeodomain Proteins / metabolism*
  • Hypertension, Pulmonary / etiology
  • Lung / blood supply
  • Lung / embryology*
  • Mice
  • Mice, Knockout
  • Muscle, Smooth, Vascular / metabolism
  • Myocytes, Smooth Muscle / metabolism
  • Myosins / metabolism
  • Parturition
  • Phosphorylation
  • Pre-B-Cell Leukemia Transcription Factor 1 / metabolism*
  • Proto-Oncogene Proteins / metabolism*
  • Pulmonary Artery / metabolism
  • Respiration
  • Vasoconstriction / physiology

Substances

  • Homeodomain Proteins
  • Pbx1 protein, mouse
  • Pbx2 protein, mouse
  • Pre-B-Cell Leukemia Transcription Factor 1
  • Proto-Oncogene Proteins
  • Elastin
  • Myosins