CCL20 stimulates proinflammatory mediator synthesis in human fibroblast-like synoviocytes through a MAP kinase-dependent process with transcriptional and posttranscriptional control

J Rheumatol. 2011 Sep;38(9):1858-65. doi: 10.3899/jrheum.110049. Epub 2011 Jul 1.

Abstract

Objective: To compare levels of the chemokine CCL20 and its receptor CCR6 in donor, osteoarthritic (OA), and rheumatoid arthritis (RA) synovium; and to determine the molecular mechanism of cellular activation induced by chemokine/receptor ligation in human fibroblast-like synoviocytes (FLS).

Methods: Synovia and isolated FLS from donor, OA, and RA joints were analyzed for CCL20 and CCR6 expression by RT-PCR and immunohistochemistry. The effect of CCL20 on cytokines and mediators of cartilage degradation was examined by PCR for mRNA expression levels and ELISA, and Western blotting for protein. CCL20-dependent transcriptional and posttranscriptional activation of target genes was monitored using reporter constructs and luciferase assays in transfected donor FLS.

Results: CCL20 and CCR6 proteins were abundantly expressed in RA synovial lining cells compared to donor or OA synovia as judged by immunohistochemistry. RT-PCR of synovial extracts confirmed the predominance of CCL20/CCR6 mRNA expression in RA synovium. CCL20 mRNA expression was low in donor FLS, but increased dramatically after stimulation with recombinant human (rh) interleukin 1ß (IL-1ß). rhCCL20 increased mRNA and protein expression of COX-2, IL-1ß, tumor necrosis factor-α, IL-6, and the matrix-destructive metalloprotease MMP-3 in donor FLS cultures. High constitutive levels of IL-6 were released from RA synovia; CCL20-induced expression of IL-6 occurred through an NSAID/COXIB-sensitive process. CCL20-induced expression of COX-2 was mediated by a PLCP1/PKCα/MEK1/2/ERK1/2-dependent pathway involving both transcriptional and posttranscriptional mechanisms.

Conclusion: CCL20/CCR6 may play an important role in the pathogenesis of RA by assembling the molecular and cellular components orchestrating synovitis.

Publication types

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

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Arthritis, Rheumatoid / metabolism*
  • Arthritis, Rheumatoid / pathology
  • Cells, Cultured
  • Chemokine CCL20 / genetics
  • Chemokine CCL20 / physiology*
  • Fibroblasts / metabolism*
  • Fibroblasts / pathology
  • Humans
  • Inflammation Mediators / metabolism*
  • Inflammation Mediators / physiology
  • MAP Kinase Signaling System / genetics*
  • Middle Aged
  • Osteoarthritis / metabolism*
  • Osteoarthritis / pathology
  • Protein Biosynthesis / physiology
  • Receptors, CCR6 / physiology
  • Synovitis / metabolism*
  • Synovitis / pathology
  • Transcription, Genetic / physiology
  • Young Adult

Substances

  • CCL20 protein, human
  • CCR6 protein, human
  • Chemokine CCL20
  • Inflammation Mediators
  • Receptors, CCR6