Identification of an immunodominant peptide from citrullinated tenascin-C as a major target for autoantibodies in rheumatoid arthritis

Ann Rheum Dis. 2016 Oct;75(10):1876-83. doi: 10.1136/annrheumdis-2015-208495. Epub 2015 Dec 9.

Abstract

Objectives: We investigated whether citrullinated tenascin-C (cTNC), an extracellular matrix protein expressed at high levels in the joints of patients with rheumatoid arthritis (RA), is a target for the autoantibodies in RA.

Methods: Citrullinated sites were mapped by mass spectrometry in the fibrinogen-like globe (FBG) domain of tenascin-C treated with peptidylarginine deiminases (PAD) 2 and 4. Antibodies to cyclic peptides containing citrullinated sites were screened in sera from patients with RA by ELISA. Potential cross-reactivity with well-established anticitrullinated protein antibody (ACPA) epitopes was tested by inhibition assays. The autoantibody response to one immunodominant cTNC peptide was then analysed in 101 pre-RA sera (median 7 years before onset) and two large independent RA cohorts.

Results: Nine arginine residues within FBG were citrullinated by PAD2 and PAD4. Two immunodominant peptides cTNC1 (VFLRRKNG-cit-ENFYQNW) and cTNC5 (EHSIQFAEMKL-cit-PSNF-cit-NLEG-cit-cit-KR) were identified. Antibodies to both showed limited cross-reactivity with ACPA epitopes from α-enolase, vimentin and fibrinogen, and no reactivity with citrullinated fibrinogen peptides sharing sequence homology with FBG. cTNC5 antibodies were detected in 18% of pre-RA sera, and in 47% of 1985 Swedish patients with RA and 51% of 287 North American patients with RA. The specificity was 98% compared with 160 healthy controls and 330 patients with osteoarthritis.

Conclusions: There are multiple citrullination sites in the FBG domain of tenascin-C. Among these, one epitope is recognised by autoantibodies that are detected years before disease onset, and which may serve as a useful biomarker to identify ACPA-positive patients with high sensitivity and specificity in established disease.

Keywords: Ant-CCP; Autoantibodies; Rheumatoid Arthritis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Arthritis, Rheumatoid / blood*
  • Arthritis, Rheumatoid / immunology
  • Autoantibodies / blood*
  • Case-Control Studies
  • Disease Progression
  • Enzyme-Linked Immunosorbent Assay
  • Epitopes / immunology
  • Female
  • Fibrinogen / immunology
  • Fibrinogen / metabolism
  • Humans
  • Joints / immunology
  • Joints / metabolism
  • Male
  • Middle Aged
  • North America
  • Peptides, Cyclic / blood*
  • Peptides, Cyclic / immunology
  • Sweden
  • Tenascin / blood*
  • Tenascin / immunology
  • United Kingdom

Substances

  • Autoantibodies
  • Epitopes
  • Peptides, Cyclic
  • Tenascin
  • cyclic citrullinated peptide
  • Fibrinogen