Anti-inflammatory and immunomodulatory properties of α1-antitrypsin without inhibition of elastase

Proc Natl Acad Sci U S A. 2013 Sep 10;110(37):15007-12. doi: 10.1073/pnas.1309648110. Epub 2013 Aug 23.

Abstract

The rationale of α1-antitrypsin (AAT) augmentation therapy to treat progressive emphysema in AAT-deficient patients is based on inhibition of neutrophil elastase; however, the benefit of this treatment remains unclear. Here we show that clinical grade AAT (with elastase inhibitory activity) and a recombinant form of AAT (rAAT) without anti-elastase activity reduces lung inflammatory responses to LPS in elastase-deficient mice. WT and elastase-deficient mice treated with either native AAT or rAAT exhibited significant reductions in infiltrating neutrophils (23% and 68%), lavage fluid levels of TNF-α (70% and 80%), and the neutrophil chemokine KC (CXCL1) (64% and 90%), respectively. Lung parenchyma TNF-α, DNA damage-inducible transcript 3 and X-box binding protein-1 mRNA levels were reduced in both mouse strains treated with AAT; significantly lower levels of these genes, as well as IL-1β gene expression, were observed in lungs of AAT-deficient patients treated with AAT therapy compared with untreated patients. In vitro, LPS-induced cytokines from WT and elastase-deficient mouse neutrophils, as well as neutrophils of healthy humans, were similarly reduced by AAT or rAAT; human neutrophils adhering to endothelial cells were decreased by 60-80% (P < 0.001) with either AAT or rAAT. In mouse pancreatic islet macrophages, LPS-induced surface expression of MHC II, Toll-like receptor-2 and -4 were markedly lower (80%, P < 0.001) when exposed to either AAT or rAAT. Consistently, in vivo and in vitro, rAAT reduced inflammatory responses at concentrations 40- to 100-fold lower than native plasma-derived AAT. These data provide evidence that the anti-inflammatory and immunomodulatory properties of AAT can be independent of elastase inhibition.

Keywords: alpha 1-antitrypsin; immunomodulation; inflammation.

Publication types

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

MeSH terms

  • Acute Lung Injury / drug therapy
  • Acute Lung Injury / genetics
  • Acute Lung Injury / immunology
  • Adult
  • Animals
  • Anti-Inflammatory Agents / pharmacology*
  • Cytokines / metabolism
  • Disease Models, Animal
  • Female
  • Gene Expression / drug effects
  • Humans
  • Immunologic Factors / pharmacology*
  • Leukocyte Elastase / antagonists & inhibitors
  • Leukocyte Elastase / deficiency
  • Leukocyte Elastase / metabolism*
  • Lipopolysaccharides / toxicity
  • Lung / drug effects
  • Lung / pathology
  • Lung / physiopathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Middle Aged
  • Neutrophils / drug effects
  • Neutrophils / immunology
  • Pulmonary Emphysema / drug therapy*
  • Pulmonary Emphysema / genetics
  • Pulmonary Emphysema / immunology
  • Recombinant Proteins / pharmacology
  • alpha 1-Antitrypsin / pharmacology*
  • alpha 1-Antitrypsin Deficiency / drug therapy
  • alpha 1-Antitrypsin Deficiency / genetics
  • alpha 1-Antitrypsin Deficiency / immunology

Substances

  • Anti-Inflammatory Agents
  • Cytokines
  • Immunologic Factors
  • Lipopolysaccharides
  • Recombinant Proteins
  • alpha 1-Antitrypsin
  • Leukocyte Elastase