Critical role of serpinB1 in regulating inflammatory responses in pulmonary influenza infection

J Infect Dis. 2011 Aug 15;204(4):592-600. doi: 10.1093/infdis/jir352.

Abstract

Background: Excessive inflammatory host response increases morbidity and mortality associated with seasonal respiratory influenza, and highly pathogenic virus strains are characterized by massive infiltration of monocytes and/or macrophages that produce a storm of injurious cytokines.

Methods: Here, we examined the role in respiratory influenza of serpinB1, an endogenous inhibitor of the serine proteases elastase, cathepsin G, and proteinase-3, increasingly recognized as regulators of inflammation.

Results: After challenge with high-dose surfactant protein-D (SP-D)-sensitive influenza A/Philadelphia/82 (H3N2), serpinB1(-/-) mice died earlier and in greater numbers than did wild-type mice. Sublethally infected animals suffered increased morbidity, delayed resolution of epithelial injury, and increased immune cell death. Viral clearance and SP-D/SP-A upregulation were unimpaired and so were early virus-induced cytokine and chemokine burst and influx of large numbers of neutrophils and monocytes. Whereas initial cytokines and chemokines rapidly cleared in wild-type mice, TNF-α, IL-6, KC/CXCL1, G-CSF, IL-17A, and MCP-1/CCL2 remained elevated in serpinB1(-/-) mice. Monocyte-derived cells were the dominant immune cells in influenza-infected lungs, and those from serpinB1(-/-) mice produced excessive IL-6 and TNF-α when tested ex vivo. Pulmonary γδ T-cells that produced IL-17A were also increased.

Conclusions: Because viral clearance was unimpaired, the study highlights the critical role of serpinB1 in mitigating inflammation and restricting pro-inflammatory cytokine production in influenza infection.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Cell Death
  • Cytokines / genetics
  • Cytokines / metabolism
  • Gene Expression Regulation / physiology
  • Inflammation / metabolism*
  • Inflammation / pathology
  • Influenza A Virus, H3N2 Subtype
  • Lung / pathology*
  • Lung Diseases / pathology
  • Lung Diseases / virology*
  • Mice
  • Mice, Knockout
  • Orthomyxoviridae Infections / immunology
  • Orthomyxoviridae Infections / pathology*
  • Serpins / genetics
  • Serpins / metabolism*
  • Time Factors

Substances

  • Cytokines
  • Serpinb1a protein, mouse
  • Serpins