Low copy numbers of complement C4 and C4A deficiency are risk factors for myositis, its subgroups and autoantibodies

Ann Rheum Dis. 2023 Feb;82(2):235-245. doi: 10.1136/ard-2022-222935. Epub 2022 Sep 28.

Abstract

Background: Idiopathic inflammatory myopathies (IIM) are a group of autoimmune diseases characterised by myositis-related autoantibodies plus infiltration of leucocytes into muscles and/or the skin, leading to the destruction of blood vessels and muscle fibres, chronic weakness and fatigue. While complement-mediated destruction of capillary endothelia is implicated in paediatric and adult dermatomyositis, the complex diversity of complement C4 in IIM pathology was unknown.

Methods: We elucidated the gene copy number (GCN) variations of total C4, C4A and C4B, long and short genes in 1644 Caucasian patients with IIM, plus 3526 matched healthy controls using real-time PCR or Southern blot analyses. Plasma complement levels were determined by single radial immunodiffusion.

Results: The large study populations helped establish the distribution patterns of various C4 GCN groups. Low GCNs of C4T (C4T=2+3) and C4A deficiency (C4A=0+1) were strongly correlated with increased risk of IIM with OR equalled to 2.58 (2.28-2.91), p=5.0×10-53 for C4T, and 2.82 (2.48-3.21), p=7.0×10-57 for C4A deficiency. Contingency and regression analyses showed that among patients with C4A deficiency, the presence of HLA-DR3 became insignificant as a risk factor in IIM except for inclusion body myositis (IBM), by which 98.2% had HLA-DR3 with an OR of 11.02 (1.44-84.4). Intragroup analyses of patients with IIM for C4 protein levels and IIM-related autoantibodies showed that those with anti-Jo-1 or with anti-PM/Scl had significantly lower C4 plasma concentrations than those without these autoantibodies.

Conclusions: C4A deficiency is relevant in dermatomyositis, HLA-DRB1*03 is important in IBM and both C4A deficiency and HLA-DRB1*03 contribute interactively to risk of polymyositis.

Keywords: autoantibodies; dermatomyositis; polymyositis.

MeSH terms

  • Adult
  • Autoantibodies / genetics
  • Child
  • Complement C4
  • Complement C4a / genetics
  • DNA Copy Number Variations
  • Dermatomyositis*
  • Genetic Predisposition to Disease
  • HLA-DR3 Antigen / genetics
  • HLA-DRB1 Chains / genetics
  • Humans
  • Myositis*
  • Risk Factors

Substances

  • Complement C4
  • HLA-DRB1 Chains
  • Autoantibodies
  • HLA-DR3 Antigen
  • Complement C4a

Supplementary concepts

  • Complement Component 4a Deficiency