Identification of new citrulline-specific autoantibodies, which bind to human arthritic cartilage, by mass spectrometric analysis of citrullinated type II collagen

Arthritis Rheumatol. 2014 Jun;66(6):1440-9. doi: 10.1002/art.38383.

Abstract

Objective: To investigate type II collagen (CII) as a joint-specific target of the anti-citrullinated protein antibody (ACPA) response in rheumatoid arthritis (RA).

Methods: Potential citrullinated neoepitopes were identified by high-resolution tandem mass spectrometry (MS/MS) of in vitro peptidylarginine deiminase 2 (PAD-2)-treated CII, and the relationship between citrullination and CII conformation was investigated by circular dichroism and conformation-dependent antibodies. Based on the MS analyses, synthetic peptides were designed and analyzed for serum IgG reactivity in the Epidemiological Investigation of RA (EIRA) case-control cohort of 1,949 RA patients and 278 healthy controls. Peptide-specific antibodies were purified from RA patient serum and used to stain RA cartilage specimens.

Results: We described the conformation-dependent citrullination pattern of CII after PAD-2 treatment at room temperature and 37°C and showed that CII could be citrullinated in its native triple-helical conformation. Screening of Arg and Cit pairs of synthetic peptides revealed new citrullinated B cell epitopes on CII. Antibodies directed to 2 proximal epitopes close to the C-terminus of the CII triple helix were recognized by autoantibodies in 21% and 17% of RA patients, respectively. Affinity-purified antibodies from RA sera directed to these 2 epitopes, but not antibodies directed to citrullinated α-enolase peptide 1, bound to RA cartilage.

Conclusion: These findings suggest that cartilage-directed anticitrulline immunity contributes to the induction of joint inflammation in RA.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arthritis, Rheumatoid / metabolism*
  • Autoantibodies / metabolism*
  • Cartilage, Articular / metabolism*
  • Case-Control Studies
  • Citrulline / immunology*
  • Collagen Type II / drug effects
  • Collagen Type II / metabolism*
  • Epitopes / immunology
  • Humans
  • Hydrolases / pharmacology
  • Immunoglobulin G / metabolism
  • In Vitro Techniques
  • Protein-Arginine Deiminases
  • Rats
  • Tandem Mass Spectrometry

Substances

  • Autoantibodies
  • Collagen Type II
  • Epitopes
  • Immunoglobulin G
  • Citrulline
  • Hydrolases
  • Protein-Arginine Deiminases