T Cells Promote Bronchial Epithelial Cell Secretion of Matrix Metalloproteinase-9 via a C-C Chemokine Receptor Type 2 Pathway: Implications for Chronic Lung Allograft Dysfunction

Am J Transplant. 2017 Jun;17(6):1502-1514. doi: 10.1111/ajt.14166. Epub 2017 Jan 23.

Abstract

Chronic lung allograft dysfunction (CLAD) is the major limitation of long-term survival after lung transplantation. CLAD manifests as bronchiolitis obliterans syndrome (BOS) or restrictive allograft syndrome (RAS). Alloimmune reactions and epithelial-to-mesenchymal transition have been suggested in BOS. However, little is known regarding the role of allogenicity in epithelial cell differentiation. Primary human bronchial epithelial cells (BECs) were treated with activated T cells in the presence or absence of transforming growth factor (TGF)-β. The expression of epithelial and mesenchymal markers was investigated. The secretion of inflammatory cytokines and matrix metalloproteinase (MMP)-9 was measured in culture supernatants and in plasma from lung transplant recipients (LTRs): 49 stable, 29 with BOS, and 16 with RAS. We demonstrated that C-C motif chemokine 2 secreted by T cells supports TGF-β-induced MMP-9 production by BECs after binding to C-C chemokine receptor type 2. Longitudinal investigation in LTRs revealed a rise in plasma MMP-9 before CLAD onset. Multivariate analysis showed that plasma MMP-9 was independently associated with BOS (odds ratio [OR] = 6.19, p = 0.002) or RAS (OR = 3.9, p = 0.024) and predicted the occurrence of CLAD 12 months before the functional diagnosis. Thus, immune cells support airway remodeling through the production of MMP-9. Plasma MMP-9 is a potential predictive biomarker of CLAD.

Keywords: bronchiolitis obliterans (BOS); lung (allograft) function/dysfunction; lung transplantation/pulmonology; rejection: chronic; translational research/science.

MeSH terms

  • Adult
  • Allografts
  • Biomarkers / blood*
  • Bronchi / immunology
  • Bronchi / metabolism
  • Bronchi / pathology
  • Chronic Disease
  • Cytokines / metabolism
  • Epithelial Cells / immunology*
  • Epithelial Cells / metabolism
  • Epithelial Cells / pathology
  • Female
  • Follow-Up Studies
  • Graft Rejection / blood
  • Graft Rejection / diagnosis*
  • Graft Rejection / etiology
  • Graft Survival / immunology
  • Humans
  • Longitudinal Studies
  • Lung Diseases / complications*
  • Lung Diseases / surgery
  • Lung Transplantation / adverse effects*
  • Male
  • Matrix Metalloproteinase 9 / blood*
  • Middle Aged
  • Postoperative Complications
  • Prognosis
  • Receptors, CCR2 / metabolism*
  • Risk Factors
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / metabolism
  • Transforming Growth Factor beta / metabolism

Substances

  • Biomarkers
  • CCR2 protein, human
  • Cytokines
  • Receptors, CCR2
  • Transforming Growth Factor beta
  • MMP9 protein, human
  • Matrix Metalloproteinase 9