Dysregulation of the IL-13 receptor system: a novel pathomechanism in pulmonary arterial hypertension

Am J Respir Crit Care Med. 2010 Sep 15;182(6):805-18. doi: 10.1164/rccm.200909-1367OC. Epub 2010 Jun 3.

Abstract

Rationale: Idiopathic pulmonary arterial hypertension (IPAH) is characterized by medial hypertrophy due to pulmonary artery smooth muscle cell (paSMC) hyperplasia. Inflammation is proposed to play a role in vessel remodeling associated with IPAH. IL-13 is emerging as a regulator of tissue remodeling; however, the contribution of the IL-13 system to IPAH has not been assessed.

Objectives: The objective of this study was to assess the possible contribution of the IL-13 system to IPAH.

Methods: Expression and localization of IL-13, and IL-13 receptors IL-4R, IL-13Rα1, and IL-13Rα2 were assessed by real-time reverse transcription-polymerase chain reaction, immunohistochemistry, and flow cytometry in lung tissue, paSMC, and microdissected vascular lesions from patients with IPAH, and in lung tissue from rodents with hypoxia- or monocrotaline-induced pulmonary hypertension. A whole-genome microarray analysis was used to study IL-13-regulated genes in paSMC.

Measurements and main results: Pulmonary expression of the IL-13 decoy receptor IL-13Rα2 was up-regulated relative to that of the IL-13 signaling receptors IL-4R and IL-13Rα1 in patients with IPAH and in two animal models of IPAH. IL-13, signaling via STAT3 and STAT6, suppressed proliferation of paSMC by promoting G(0)/G(1) arrest. Whole-genome microarrays revealed that IL-13 suppressed endothelin-1 production by paSMC, suggesting that IL-13 controlled paSMC growth by regulating endothelin production. Ectopic expression of the il13ra2 gene resulted in partial loss of paSMC growth control by IL-13 and blunted IL-13 suppression of endothelin-1 production by paSMC, whereas small-interfering RNA knockdown of il13ra2 gene expression had the opposite effects.

Conclusions: The IL-13 system is a novel regulator of paSMC growth. Dysregulation of IL-13 receptor expression in IPAH may partially underlie smooth muscle hypertrophy associated with pathological vascular remodeling in IPAH.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Animals
  • Disease Models, Animal
  • Female
  • Flow Cytometry
  • Humans
  • Hypertension, Pulmonary / etiology*
  • Immunohistochemistry
  • Interleukin-13 / metabolism*
  • Interleukin-13 Receptor alpha1 Subunit / metabolism
  • Interleukin-13 Receptor alpha2 Subunit / metabolism
  • Lung / metabolism
  • Male
  • Mice
  • Middle Aged
  • Muscle, Smooth, Vascular / metabolism
  • Myocytes, Smooth Muscle / metabolism
  • Pulmonary Artery / metabolism
  • Rats
  • Receptors, Interleukin-13 / physiology*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Up-Regulation / physiology*
  • Young Adult

Substances

  • Interleukin-13
  • Interleukin-13 Receptor alpha1 Subunit
  • Interleukin-13 Receptor alpha2 Subunit
  • Receptors, Interleukin-13

Associated data

  • GEO/GSE15739