Relationships between early inflammatory response to bleomycin and sensitivity to lung fibrosis: a role for dipeptidyl-peptidase I and tissue inhibitor of metalloproteinase-3?

Am J Respir Crit Care Med. 2007 Dec 1;176(11):1098-107. doi: 10.1164/rccm.200607-1051OC. Epub 2007 Aug 2.

Abstract

Rationale: Different sensitivities to profibrotic compounds such as bleomycin are observed among mouse strains.

Objectives: To identify genetic factors contributing to the outcome of lung injury.

Methods: Physiological comparison of C57BL/6 (sensitive) and BALB/c (resistant) mice challenged by intratracheal bleomycin instillation revealed several early differences: global gene expression profiles were thus established from lungs derived from the two strains, in the absence of any bleomycin administration.

Measurements and main results: Expression of 25 genes differed between the two strains. Among them, two molecules, not previously associated with pulmonary fibrosis, were identified. The first corresponded to dipeptidyl-peptidase I (DPPI), a cysteine peptidase (also known as cathepsin C) essential for the activation of serine proteinases produced by immune/inflammatory cells. The second corresponded to tissue inhibitor of matrix metalloproteinase-3, which also inhibits members of the ADAM (a disintegrin and metalloproteinase) family, such as the tumor necrosis factor-converting enzyme. In functional studies performed in the bleomycin-induced lung fibrosis model, the level of expression of these two genes was closely correlated with specific early events associated with lung fibrosis, namely activation of polymorphonuclear neutrophil-derived serine proteases and tumor necrosis factor-alpha-dependent inflammatory syndrome. Surprisingly, genetic deletion of DPPI in the context of a C57BL/6 genetic background did not protect against bleomycin-mediated fibrosis, suggesting additional function(s) for this key enzyme.

Conclusions: This study highlights the importance of the early inflammatory events that follow bleomycin instillation in the development of lung fibrosis, and describes for the first time the roles that DPPI and tissue inhibitor of matrix metalloproteinase-3 may play in this process.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • ADAM Proteins / metabolism
  • ADAM17 Protein
  • Animals
  • Apoptosis
  • Bleomycin* / administration & dosage
  • Bronchoalveolar Lavage Fluid / chemistry
  • Cathepsin C / deficiency
  • Cathepsin C / metabolism*
  • Eosinophilia / chemically induced
  • Eosinophilia / etiology
  • Gene Expression Profiling
  • Genetic Predisposition to Disease
  • Instillation, Drug
  • Interleukin-5 / metabolism
  • Lung / metabolism
  • Male
  • Matrix Metalloproteinases / metabolism
  • Mice
  • Mice, Inbred BALB C / genetics
  • Mice, Inbred BALB C / metabolism
  • Mice, Inbred C57BL / genetics
  • Mice, Inbred C57BL / metabolism
  • Mice, Knockout
  • Neutrophils / enzymology
  • Oligonucleotide Array Sequence Analysis
  • Pneumonia / chemically induced*
  • Pneumonia / metabolism*
  • Pneumonia / physiopathology
  • Pulmonary Fibrosis / chemically induced*
  • Pulmonary Fibrosis / genetics*
  • Serine Endopeptidases / metabolism
  • Species Specificity
  • Tissue Inhibitor of Metalloproteinase-3 / metabolism*
  • Trachea
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Interleukin-5
  • Tissue Inhibitor of Metalloproteinase-3
  • Tumor Necrosis Factor-alpha
  • Bleomycin
  • Cathepsin C
  • Serine Endopeptidases
  • ADAM Proteins
  • Matrix Metalloproteinases
  • ADAM17 Protein