Serological and Genetic Evidence for Altered Complement System Functionality in Systemic Lupus Erythematosus: Findings of the GAPAID Consortium

PLoS One. 2016 Mar 7;11(3):e0150685. doi: 10.1371/journal.pone.0150685. eCollection 2016.

Abstract

Systemic lupus erythematosus is a chronic autoimmune disease with multifactorial ethiopathogenesis. The complement system is involved in both the early and late stages of disease development and organ damage. To better understand autoantibody mediated complement consumption we examined ex vivo immune complex formation on autoantigen arrays. We recruited patients with SLE (n = 211), with other systemic autoimmune diseases (n = 65) and non-autoimmune control subjects (n = 149). Standard clinical and laboratory data were collected and serum complement levels were determined. The genotype of SNP rs1143679 in the ITGAM gene was also determined. Ex vivo formation of immune complexes, with respect to IgM, IgG, complement C4 and C3 binding, was examined using a functional immunoassay on autoantigen microarray comprising nucleic acids, proteins and lipids. Complement consumption of nucleic acids increased upon binding of IgM and IgG even when serum complement levels were decreased due to consumption in SLE patients. A negative correlation between serum complement levels and ex vivo complement deposition on nucleic acid autoantigens is demonstrated. On the contrary, complement deposition on tested protein and lipid autoantigens showed positive correlation with C4 levels. Genetic analysis revealed that the non-synonymous variant rs1143679 in complement receptor type 3 is associated with an increased production of anti-dsDNA IgG antibodies. Notwithstanding, homozygous carriers of the previously reported susceptible allele (AA) had lower levels of dsDNA specific IgM among SLE patients. Both the non-synonymous variant rs1143679 and the high ratio of nucleic acid specific IgG/IgM were associated with multiple organ involvement. In summary, secondary complement deficiency in SLE does not impair opsonization of nucleic-acid-containing autoantigens but does affect other antigens and potentially other complement dependent processes. Dysfunction of the receptor recognizing complement opsonized immune complexes promotes the development of class-switched autoantibodies targeting nucleic acids.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Autoantibodies / immunology
  • Autoantigens / immunology
  • CD11b Antigen / genetics
  • Complement System Proteins / metabolism*
  • Female
  • Humans
  • Lupus Erythematosus, Systemic / blood
  • Lupus Erythematosus, Systemic / genetics*
  • Lupus Erythematosus, Systemic / immunology*
  • Lupus Erythematosus, Systemic / metabolism
  • Male
  • Middle Aged
  • Polymorphism, Single Nucleotide
  • Serologic Tests*

Substances

  • Autoantibodies
  • Autoantigens
  • CD11b Antigen
  • ITGAM protein, human
  • Complement System Proteins

Grants and funding

This work was funded by European Union grant FP7/2007–2013 grant agreement n° 314971 (GAPAID-314971, FP7-SME2012, http://cordis.europa.eu/project/rcn/105440_en.html). Support from the National Research, Development and Innovation Office - NKFIH to JP, grant number K109683 is acknowledged. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Diagnosticum Zrt, Toscana Biomarkers and Progenika provided support in the form of salaries for authors JP, ZH, HP, IP, MCA, JDA and MU, but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section.