TGF-β-induced IL-6 prevents development of acute lung injury in influenza A virus-infected F508del CFTR-heterozygous mice

Am J Physiol Lung Cell Mol Physiol. 2015 Jun 1;308(11):L1136-44. doi: 10.1152/ajplung.00078.2015. Epub 2015 Apr 3.

Abstract

As the eighth leading cause of annual mortality in the USA, influenza A viruses are a major public health concern. In 20% of patients, severe influenza progresses to acute lung injury (ALI). However, pathophysiological mechanisms underlying ALI development are poorly defined. We reported that, unlike wild-type (WT) C57BL/6 controls, influenza A virus-infected mice that are heterozygous for the F508del mutation in the cystic fibrosis transmembrane conductance regulator (HETs) did not develop ALI. This effect was associated with higher IL-6 and alveolar macrophages (AMs) at 6 days postinfection (d.p.i.) in HET bronchoalveolar lavage fluid (BALF). In the present study, we found that HET AMs were an important source of IL-6 at 6 d.p.i. Infection also induced TGF-β production by HET but not WT mice at 2 d.p.i. TGF-β neutralization at 2 d.p.i. (TGF-N) significantly reduced BALF IL-6 in HETs at 6 d.p.i. Neither TGF-N nor IL-6 neutralization at 4 d.p.i. (IL-6-N) altered postinfection weight loss or viral replication in either mouse strain. However, both treatments increased influenza A virus-induced hypoxemia, pulmonary edema, and lung dysfunction in HETs to WT levels at 6 d.p.i. TGF-N and IL-6-N did not affect BALF AM and neutrophil numbers but attenuated the CXCL-1/keratinocyte chemokine response in both strains and reduced IFN-γ production in WT mice. Finally, bone marrow transfer experiments showed that HET stromal and myeloid cells are both required for protection from ALI in HETs. These findings indicate that TGF-β-dependent production of IL-6 by AMs later in infection prevents ALI development in influenza A virus-infected HET mice.

Keywords: acute lung injury; cystic fibrosis transmembrane conductance regulator; influenza; interleukin-6; transforming growth factor-β.

Publication types

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

MeSH terms

  • Acute Lung Injury / immunology
  • Acute Lung Injury / virology*
  • Animals
  • Bronchoalveolar Lavage Fluid
  • Cystic Fibrosis Transmembrane Conductance Regulator / genetics
  • Immunity, Innate
  • Influenza A virus / immunology*
  • Interleukin-6 / physiology*
  • Macrophages, Alveolar / metabolism
  • Macrophages, Alveolar / virology
  • Mice, 129 Strain
  • Mice, Inbred C57BL
  • Mice, Inbred CFTR
  • Orthomyxoviridae Infections / immunology*
  • Sequence Deletion
  • Transforming Growth Factor beta / physiology*

Substances

  • Interleukin-6
  • Transforming Growth Factor beta
  • Cystic Fibrosis Transmembrane Conductance Regulator