Type V collagen induced tolerance suppresses collagen deposition, TGF-β and associated transcripts in pulmonary fibrosis

PLoS One. 2013 Oct 21;8(10):e76451. doi: 10.1371/journal.pone.0076451. eCollection 2013.

Abstract

Rationale: Idiopathic pulmonary fibrosis (IPF) is a fatal interstitial lung disease characterized by progressive scarring and matrix deposition. Recent reports highlight an autoimmune component in IPF pathogenesis. We have reported anti-col(V) immunity in IPF patients. The objective of our study was to determine the specificity of col(V) expression profile and anti-col(V) immunity relative to col(I) in clinical IPF and the efficacy of nebulized col(V) in pre-clinical IPF models.

Methods: Col(V) and col(I) expression profile was analyzed in normal human and IPF tissues. C57-BL6 mice were intratracheally instilled with bleomycin (0.025 U) followed by col(V) nebulization at pre-/post-fibrotic stage and analyzed for systemic and local responses.

Results: Compared to normal lungs, IPF lungs had higher protein and transcript expression of the alpha 1 chain of col(V) and col(I). Systemic anti-col(V) antibody concentrations, but not of anti-col(I), were higher in IPF patients. Nebulized col(V), but not col(I), prevented bleomycin-induced fibrosis, collagen deposition, and myofibroblast differentiation. Col(V) treatment suppressed systemic levels of anti-col(V) antibodies, IL-6 and TNF-α; and local Il-17a transcripts. Compared to controls, nebulized col(V)-induced tolerance abrogated antigen-specific proliferation in mediastinal lymphocytes and production of IL-17A, IL-6, TNF-α and IFN-γ. In a clinically relevant established fibrosis model, nebulized col(V) decreased collagen deposition. mRNA array revealed downregulation of genes specific to fibrosis (Tgf-β, Il-1β, Pdgfb), matrix (Acta2, Col1a2, Col3a1, Lox, Itgb1/6, Itga2/3) and members of the TGF-β superfamily (Tgfbr1/2, Smad2/3, Ltbp1, Serpine1, Nfkb/Sp1/Cebpb).

Conclusions: Anti-col(V) immunity is pathogenic in IPF, and col(V)-induced tolerance abrogates bleomycin-induced fibrogenesis and down regulates TGF- β-related signaling pathways.

Publication types

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

MeSH terms

  • Animals
  • Autoantibodies / blood
  • Autoantibodies / immunology
  • Bleomycin / adverse effects
  • Collagen Type I / immunology
  • Collagen Type V / administration & dosage
  • Collagen Type V / genetics
  • Collagen Type V / immunology*
  • Collagen Type V / metabolism
  • Cytokines / biosynthesis
  • Cytokines / genetics
  • Disease Models, Animal
  • Female
  • Gene Expression
  • Gene Expression Regulation / drug effects
  • Humans
  • Idiopathic Pulmonary Fibrosis / drug therapy
  • Idiopathic Pulmonary Fibrosis / genetics
  • Idiopathic Pulmonary Fibrosis / immunology
  • Idiopathic Pulmonary Fibrosis / metabolism
  • Idiopathic Pulmonary Fibrosis / pathology
  • Immune Tolerance*
  • Inflammation Mediators / metabolism
  • Lymphocyte Activation / immunology
  • Mice
  • Nebulizers and Vaporizers
  • Pulmonary Fibrosis / drug therapy
  • Pulmonary Fibrosis / genetics*
  • Pulmonary Fibrosis / immunology*
  • Pulmonary Fibrosis / metabolism
  • Pulmonary Fibrosis / pathology
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocyte Subsets / metabolism
  • Transcription, Genetic* / drug effects
  • Transforming Growth Factor beta / biosynthesis
  • Transforming Growth Factor beta / genetics*

Substances

  • Autoantibodies
  • Collagen Type I
  • Collagen Type V
  • Cytokines
  • Inflammation Mediators
  • RNA, Messenger
  • Transforming Growth Factor beta
  • Bleomycin