Human neutrophil elastase degrades SPLUNC1 and impairs airway epithelial defense against bacteria

PLoS One. 2013 May 31;8(5):e64689. doi: 10.1371/journal.pone.0064689. Print 2013.

Abstract

Background: Acute exacerbations of chronic obstructive pulmonary disease (AECOPD) are a significant cause of mortality of COPD patients, and pose a huge burden on healthcare. One of the major causes of AECOPD is airway bacterial (e.g. nontypeable Haemophilus influenzae [NTHi]) infection. However, the mechanisms underlying bacterial infections during AECOPD remain poorly understood. As neutrophilic inflammation including increased release of human neutrophil elastase (HNE) is a salient feature of AECOPD, we hypothesized that HNE impairs airway epithelial defense against NTHi by degrading airway epithelial host defense proteins such as short palate, lung, and nasal epithelium clone 1 (SPLUNC1).

Methodology/main results: Recombinant human SPLUNC1 protein was incubated with HNE to confirm SPLUNC1 degradation by HNE. To determine if HNE-mediated impairment of host defense against NTHi was SPLUNC1-dependent, SPLUNC1 protein was added to HNE-treated primary normal human airway epithelial cells. The in vivo function of SPLUNC1 in NTHi defense was investigated by infecting SPLUNC1 knockout and wild-type mice intranasally with NTHi. We found that: (1) HNE directly increased NTHi load in human airway epithelial cells; (2) HNE degraded human SPLUNC1 protein; (3) Recombinant SPLUNC1 protein reduced NTHi levels in HNE-treated human airway epithelial cells; (4) NTHi levels in lungs of SPLUNC1 knockout mice were increased compared to wild-type mice; and (5) SPLUNC1 was reduced in lungs of COPD patients.

Conclusions: Our findings suggest that SPLUNC1 degradation by neutrophil elastase may increase airway susceptibility to bacterial infections. SPLUNC1 therapy likely attenuates bacterial infections during AECOPD.

Publication types

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

MeSH terms

  • Animals
  • Cells, Cultured
  • Epithelial Cells / drug effects
  • Epithelial Cells / immunology
  • Epithelial Cells / microbiology
  • Glycoproteins / immunology
  • Glycoproteins / metabolism*
  • Glycoproteins / pharmacology
  • Haemophilus Infections / immunology*
  • Haemophilus Infections / metabolism
  • Haemophilus Infections / microbiology
  • Haemophilus Infections / pathology
  • Haemophilus influenzae / drug effects
  • Haemophilus influenzae / growth & development
  • Humans
  • Leukocyte Elastase / metabolism*
  • Lung / immunology*
  • Lung / microbiology
  • Lung / pathology
  • Mice
  • Mice, Knockout
  • Neutrophil Infiltration / immunology*
  • Phosphoproteins / immunology
  • Phosphoproteins / metabolism*
  • Phosphoproteins / pharmacology
  • Proteolysis
  • Pulmonary Disease, Chronic Obstructive / immunology*
  • Pulmonary Disease, Chronic Obstructive / metabolism
  • Pulmonary Disease, Chronic Obstructive / microbiology
  • Pulmonary Disease, Chronic Obstructive / pathology
  • Recombinant Proteins / immunology
  • Recombinant Proteins / metabolism
  • Recombinant Proteins / pharmacology
  • Respiratory Mucosa / immunology
  • Respiratory Mucosa / microbiology
  • Respiratory Mucosa / pathology

Substances

  • BPIFA1 protein, human
  • Glycoproteins
  • Phosphoproteins
  • Recombinant Proteins
  • Leukocyte Elastase