Z α1-antitrypsin confers a proinflammatory phenotype that contributes to chronic obstructive pulmonary disease

Am J Respir Crit Care Med. 2014 Apr 15;189(8):909-31. doi: 10.1164/rccm.201308-1458OC.

Abstract

Rationale: Severe α1-antitrypsin deficiency caused by the Z variant (Glu342Lys; ZZ-AT) is a well-known genetic cause for emphysema. Although severe lack of antiproteinase protection is the critical etiologic factor for ZZ-AT-associated chronic obstructive pulmonary disease (COPD), some reports have suggested enhanced lung inflammation as a factor in ZZ-AT homozygotes.

Objectives: To provide molecular characterization of inflammation in ZZ-AT.

Methods: Inflammatory cell and cytokine profile (nuclear factor-κB, IL-6, tumor necrosis factor-α), intracellular polymerization of Z-AT, and endoplasmic reticulum (ER) stress markers (protein kinase RNA-like ER kinase, activator transcription factor 4) were assessed in transgenic mice and transfected cells in response to cigarette smoke, and in explanted lungs from ZZ and MM individuals with severe COPD.

Measurements and main results: Compared with M-AT, transgenic Z-AT mice lungs exposed to cigarette smoke had higher levels of pulmonary cytokines, neutrophils, and macrophages and an exaggerated ER stress. Similarly, the ER overload response was greater in lungs from ZZ-AT homozygotes with COPD, and was particularly found in pulmonary epithelial cells. Cigarette smoke increased intracellular Z-AT polymers, ER overload response, and proinflammatory cytokine release in Z-AT-expressing pulmonary epithelial cells, which could be prevented with an inhibitor of polymerization, an antioxidant, and an inhibitor of protein kinase RNA-like ER kinase.

Conclusions: We show here that aggregation of intracellular mutant Z-AT invokes a specific deleterious cellular inflammatory phenotype in COPD. Oxidant-induced intracellular polymerization of Z-AT in epithelial cells causes ER stress, and promotes excess cytokine and cellular inflammation. This pathway is likely to contribute to the development of COPD in ZZ-AT homozygotes, and therefore merits further investigation.

Publication types

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

MeSH terms

  • Animals
  • Biomarkers / metabolism
  • Disease Models, Animal
  • Endoplasmic Reticulum / metabolism
  • Glutamic Acid
  • Humans
  • Interleukin-6 / genetics
  • Lysine
  • Macrophages / metabolism
  • Macrophages / pathology
  • Mice
  • Mice, Transgenic
  • Mutation*
  • NF-kappa B / genetics
  • Neutrophils / metabolism
  • Neutrophils / pathology
  • Oxidative Stress
  • Phenotype
  • Pulmonary Disease, Chronic Obstructive / genetics*
  • Pulmonary Disease, Chronic Obstructive / metabolism
  • Tobacco Smoke Pollution / adverse effects
  • Trypsin Inhibitors / genetics*
  • Trypsin Inhibitors / metabolism
  • Tumor Necrosis Factor-alpha / genetics
  • alpha 1-Antitrypsin / genetics*
  • alpha 1-Antitrypsin / metabolism

Substances

  • Biomarkers
  • Interleukin-6
  • NF-kappa B
  • Tobacco Smoke Pollution
  • Trypsin Inhibitors
  • Tumor Necrosis Factor-alpha
  • alpha 1-Antitrypsin
  • Glutamic Acid
  • Lysine