Matrix metalloproteinase-19 deficiency promotes tenascin-C accumulation and allergen-induced airway inflammation

Am J Respir Cell Mol Biol. 2010 Sep;43(3):286-95. doi: 10.1165/rcmb.2008-0426OC. Epub 2009 Oct 20.

Abstract

Matrix metalloproteinases (MMPs) recently appeared as key regulators of inflammation, allowing the recruitment and clearance of inflammatory cells and modifying the biological activity of many peptide mediators by cleavage. MMP-19 is newly described, and it preferentially cleaves matrix proteins such as collagens and tenascin-C. The role of MMP-19 in asthma has not been described to date. The present study sought to assess the expression of MMP-19 in a murine asthma model, and to address the biological effects of MMP-19 deficiency in mice. Allergen-exposed, wild-type mice displayed increased expression of MMP-19 mRNA and an increased number of MMP-19-positive cells in the lungs, as detected by immunohistochemistry. After an allergen challenge of MMP-19 knockout (MMP-19(-/-)) mice, exacerbated eosinophilic inflammation was detected in bronchoalveolar lavage fluid and bronchial tissue, along with increased airway responsiveness to methacholine. A shift toward increased T helper-2 lymphocyte (Th2)-driven inflammation in MMP-19(-/-) mice was demonstrated by (1) increased numbers of cells expressing the IL-33 receptor T(1)/ST(2) in lung parenchyma, (2) increased IgG(1) levels in serum, and (3) higher levels of IL-13 and eotaxin-1 in lung extracts. Tenascin-C was found to accumulate in peribronchial areas of MMP-19(-/-) after allergen challenges, as assessed by Western blot and immunohistochemistry analyses. We conclude that MMP-19 is a new mediator in asthma, preventing tenascin-C accumulation and directly or indirectly controlling Th2-driven airway eosinophilia and airway hyperreactivity. Our data suggest that MMP-19 may act on Th2 inflammation homeostasis by preventing the accumulation of tenascin protein.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Allergens / pharmacology*
  • Animals
  • Asthma / metabolism*
  • Asthma / pathology
  • Blotting, Western
  • Bone Marrow / metabolism
  • Bronchial Hyperreactivity / immunology
  • Bronchial Hyperreactivity / metabolism
  • Bronchoalveolar Lavage Fluid
  • Cells, Cultured
  • Eosinophils / immunology
  • Eosinophils / metabolism*
  • Eosinophils / pathology
  • Female
  • Flow Cytometry
  • Humans
  • Immunoenzyme Techniques
  • Interleukin-13 / pharmacology
  • Lung / metabolism*
  • Lung / pathology
  • Male
  • Matrix Metalloproteinases, Secreted / deficiency*
  • Mice
  • Mice, Knockout
  • Myocytes, Smooth Muscle / metabolism
  • RNA, Messenger / genetics
  • Respiratory System / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • T-Lymphocytes / metabolism
  • Tenascin / genetics
  • Tenascin / metabolism*
  • Th2 Cells / metabolism

Substances

  • Allergens
  • Interleukin-13
  • RNA, Messenger
  • Tenascin
  • Matrix Metalloproteinases, Secreted
  • matrix metalloproteinase 19