Pulmonary suppressor of cytokine signaling-1 induced by IL-13 regulates allergic asthma phenotype

Am J Respir Crit Care Med. 2009 Jun 1;179(11):992-8. doi: 10.1164/rccm.200806-992OC. Epub 2009 Mar 19.

Abstract

Rationale: Th2 cytokines play an important role in allergic diseases. These cytokines activate signal transduction pathways, including Janus kinase/signal transducer and activator of transcription (STAT) signaling. Although the suppressor of cytokine signaling (SOCS) family protein, a negative regulator of the Janus kinase/STAT signaling pathway, contributes to helper T cell differentiation during immune responses, the role of SOCS proteins within the structural cells of a target organ has not been clarified in allergy.

Objectives: To study the local function of SOCS in the development of asthma.

Methods: We used mouse models of IL-13- and ovalbumin (OVA)-induced allergic airway disease. Airway smooth muscle cells were cultured from patients with asthma.

Measurements and main results: The administration of IL-13 induced not only airway responses but also SOCS1 expression at the local inflammatory site. The up-regulated SOCS1 markedly suppressed IL-13-dependent STAT6 activation and eotaxin expression and subsequently down-regulated IL-13-induced airway inflammatory responses. The inactivation of SOCS1 induced airway hyperresponsiveness after IL-13 treatment even in hyporesponsive C57BL/6 background mice. In an OVA-induced model of allergic airway disease, allergen exposure up-regulated local SOCS1 expression, and the induction of SOCS1 in the airways attenuated allergen-induced airway responses. Inactivation of IL-13 inhibited SOCS1 induction in a model of allergic airway disease. Interestingly, airway smooth muscle cells from individuals with asthma had impaired up-regulation of SOCS1 after IL-13 stimulation.

Conclusions: SOCS1 induction by IL-13 in airway structural cells is critical to negatively control allergic airway disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Asthma / immunology*
  • Cells, Cultured
  • Disease Models, Animal
  • Humans
  • Interleukin-13 / immunology*
  • Mice
  • Myocytes, Smooth Muscle / immunology*
  • STAT6 Transcription Factor / metabolism
  • Suppressor of Cytokine Signaling 1 Protein
  • Suppressor of Cytokine Signaling Proteins / immunology*
  • Suppressor of Cytokine Signaling Proteins / metabolism*
  • Th2 Cells / immunology
  • Up-Regulation

Substances

  • Interleukin-13
  • SOCS1 protein, human
  • STAT6 Transcription Factor
  • STAT6 protein, human
  • Socs1 protein, mouse
  • Stat6 protein, mouse
  • Suppressor of Cytokine Signaling 1 Protein
  • Suppressor of Cytokine Signaling Proteins