Endothelial HIF-2α as a Key Endogenous Mediator Preventing Emphysema

Am J Respir Crit Care Med. 2020 Oct 1;202(7):983-995. doi: 10.1164/rccm.202001-0078OC.

Abstract

Rationale: Endothelial injury may provoke emphysema, but molecular pathways of disease development require further discernment. Emphysematous lungs exhibit decreased expression of HIF-2α (hypoxia-inducible factor-2α)-regulated genes, and tobacco smoke decreases pulmonary HIF-2α concentrations. These findings suggest that decreased HIF-2α expression is important in the development of emphysema.Objectives: The objective of this study was to evaluate the roles of endothelial-cell (EC) HIF-2α in the pathogenesis of emphysema in mice.Methods: Mouse lungs were examined for emphysema after either the loss or the overexpression of EC Hif-2α. In addition, SU5416, a VEGFR2 inhibitor, was used to induce emphysema. Lungs were evaluated for HGF (hepatocyte growth factor), a protein involved in alveolar development and homeostasis. Lungs from patients with emphysema were measured for endothelial HIF-2α expression.Measurements and Main Results: EC Hif-2α deletion resulted in emphysema in association with fewer ECs and pericytes. After SU5416 exposure, EC Hif-2α-knockout mice developed more severe emphysema, whereas EC Hif-2α-overexpressing mice were protected. EC Hif-2α-knockout mice demonstrated lower levels of HGF. Human emphysema lung samples exhibited reduced EC HIF-2α expression.Conclusions: Here, we demonstrate a unique protective role for pulmonary endothelial HIF-2α and how decreased expression of this endogenous factor causes emphysema; its pivotal protective function is suggested by its ability to overcome VEGF antagonism. HIF-2α may maintain alveolar architecture by promoting vascular survival and associated HGF production. In summary, HIF-2α may be a key endogenous factor that prevents the development of emphysema, and its upregulation has the potential to foster lung health in at-risk patients.

Keywords: emphysema; hepatocyte growth factor; hypoxia-inducible factor-2α.

Publication types

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

MeSH terms

  • Angiogenesis Inhibitors / toxicity
  • Animals
  • Basic Helix-Loop-Helix Transcription Factors / genetics*
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Deferoxamine / pharmacology
  • Disease Models, Animal
  • Endothelial Cells / metabolism*
  • Endothelial Cells / pathology
  • Hepatocyte Growth Factor / genetics
  • Hepatocyte Growth Factor / metabolism
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / genetics*
  • Indoles / toxicity
  • Iron Chelating Agents / pharmacology
  • Lung / blood supply
  • Lung / cytology
  • Lung / drug effects
  • Lung / metabolism*
  • Mice
  • Mice, Knockout
  • Microvessels
  • Pericytes / metabolism
  • Pulmonary Circulation
  • Pulmonary Disease, Chronic Obstructive / metabolism
  • Pulmonary Emphysema / chemically induced
  • Pulmonary Emphysema / genetics*
  • Pulmonary Emphysema / metabolism
  • Pulmonary Emphysema / pathology
  • Pyrroles / toxicity
  • Smoke / adverse effects

Substances

  • Angiogenesis Inhibitors
  • Basic Helix-Loop-Helix Transcription Factors
  • Hif1a protein, mouse
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Indoles
  • Iron Chelating Agents
  • Pyrroles
  • Smoke
  • endothelial PAS domain-containing protein 1
  • Hepatocyte Growth Factor
  • Semaxinib
  • Deferoxamine