Neonatal rhinovirus induces mucous metaplasia and airways hyperresponsiveness through IL-25 and type 2 innate lymphoid cells

J Allergy Clin Immunol. 2014 Aug;134(2):429-39. doi: 10.1016/j.jaci.2014.04.020. Epub 2014 Jun 6.

Abstract

Background: Early-life human rhinovirus infection has been linked to asthma development in high-risk infants and children. Nevertheless, the role of rhinovirus infection in the initiation of asthma remains unclear.

Objective: We hypothesized that, in contrast to infection of mature BALB/c mice, neonatal infection with rhinovirus promotes an IL-25-driven type 2 response, which causes persistent mucous metaplasia and airways hyperresponsiveness.

Methods: Six-day-old and 8-week-old BALB/c mice were inoculated with sham HeLa cell lysate or rhinovirus. Airway responses from 1 to 28 days after infection were assessed by using quantitative PCR, ELISA, histology, immunofluorescence microscopy, flow cytometry, and methacholine responsiveness. Selected mice were treated with a neutralizing antibody to IL-25.

Results: Compared with mature mice, rhinovirus infection in neonatal mice increased lung IL-13 and IL-25 production, whereas IFN-γ, IL-12p40, and TNF-α expression was suppressed. In addition, the population of IL-13-secreting type 2 innate lymphoid cells (ILC2s) was expanded with rhinovirus infection in neonatal but not mature mice. ILC2s were the major cell type secreting IL-13 in neonates. Finally, anti-IL-25 neutralizing antibody attenuated ILC2 expansion, mucous hypersecretion, and airways responsiveness.

Conclusions: These findings suggest that early-life viral infection could contribute to asthma development by provoking age-dependent, IL-25-driven type 2 immune responses.

Keywords: Asthma; IL-25; mouse; neonatal; rhinovirus; type 2 innate lymphoid cells.

MeSH terms

  • Age Factors
  • Animals
  • Animals, Newborn
  • Antibodies, Neutralizing / pharmacology
  • Cell Proliferation
  • Child
  • Gene Expression Regulation
  • Humans
  • Interferon-gamma / genetics
  • Interferon-gamma / immunology
  • Interleukin-12 Subunit p40 / genetics
  • Interleukin-12 Subunit p40 / immunology
  • Interleukin-13 / genetics
  • Interleukin-13 / immunology
  • Interleukins / antagonists & inhibitors
  • Interleukins / genetics
  • Interleukins / immunology*
  • Lung / immunology*
  • Lung / pathology
  • Lymphocytes / immunology*
  • Lymphocytes / pathology
  • Mice
  • Mucus / immunology
  • Picornaviridae Infections / complications
  • Picornaviridae Infections / immunology*
  • Picornaviridae Infections / pathology
  • Respiratory Hypersensitivity / complications
  • Respiratory Hypersensitivity / immunology*
  • Respiratory Hypersensitivity / pathology
  • Rhinovirus / immunology*
  • Signal Transduction
  • Tumor Necrosis Factor-alpha / genetics
  • Tumor Necrosis Factor-alpha / immunology

Substances

  • Antibodies, Neutralizing
  • Interleukin-12 Subunit p40
  • Interleukin-13
  • Interleukins
  • Mydgf protein, mouse
  • Tumor Necrosis Factor-alpha
  • Interferon-gamma