Immunization with pentraxin 3 (PTX3) leads to anti-PTX3 antibody production and delayed lupus-like nephritis in NZB/NZW F1 mice

J Autoimmun. 2016 Nov:74:208-216. doi: 10.1016/j.jaut.2016.07.002. Epub 2016 Jul 9.

Abstract

Background: Anti-pentraxin 3 (PTX3) antibodies were associated with the absence of lupus glomerulonephritis in humans.

Aim: To explore the effects of anti-PTX3 antibodies in New Zealand Black/White (NZB/NZW F1) mice and their inherent mechanisms of action.

Materials and methods: 30 NZB/NZW F1 mice were subdivided into 3 groups of 10 mice each and subcutaneously injected with PTX3, alum and PBS (group 1), alum and PBS (group 2) or PBS alone (group 3), 3 times 3 weeks apart, before development of renal disease. Mice were followed until natural death. Histological analysis and immunohistochemistry were performed on harvested kidneys. Effects of anti-PTX3 antibodies on C1q binding to immobilized PTX3-anti-PTX3 immune complexes were evaluated in vitro using human SLE sera. Qualitative characterization of human IgG anti-PTX3 was performed.

Results: Only group 1 mice developed anti-PTX3 antibodies. Anti-dsDNA and anti-C1q antibodies appeared significantly later and at lower levels in group 1 mice vs. controls (p < 0.0001). Proteinuria-free and overall survival were significantly increased in group 1 mice vs. controls (p < 0.05 and p = 0.03, respectively). Histopathological analysis showed that glomerular and tubular PTX3 staining and renal lesions were increased in controls compared with immunized mice. Addition of human SLE sera positive for anti-PTX3 antibodies to C1q and fixed PTX3 interfered with C1q binding to PTX3-anti-PTX3 immune complexes. Qualitative characterization of human IgG anti-PTX3 showed an increased proportion of IgG4.

Conclusions: Anti-PTX3 antibodies delay lupus-like nephritis and prolong survival of NZB/NZW F1 mice. In vitro observations suggest anti-PTX3 antibodies may dampen complement activation via their Fc fragment, likely hindering renal inflammation.

Keywords: Anti-pentraxin 3 antibodies; Complement activation; Lupus glomerulonephritis; Nephritogenic antibodies; Survival.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Inflammatory Agents / immunology
  • Anti-Inflammatory Agents / pharmacology
  • Autoantibodies / blood
  • Autoantibodies / immunology*
  • Autoantibodies / pharmacology
  • Biomarkers
  • Biopsy
  • C-Reactive Protein / genetics
  • C-Reactive Protein / immunology*
  • C-Reactive Protein / metabolism
  • Complement Activation / immunology
  • Complement C1q / immunology
  • Disease Models, Animal
  • Female
  • Humans
  • Immunization
  • Immunoglobulin G / blood
  • Immunoglobulin G / immunology
  • Immunohistochemistry
  • Kidney Function Tests
  • Lupus Nephritis / diagnosis
  • Lupus Nephritis / immunology*
  • Lupus Nephritis / metabolism
  • Lupus Nephritis / mortality
  • Mice
  • Mice, Inbred NZB
  • Protective Agents
  • Serum Amyloid P-Component / genetics
  • Serum Amyloid P-Component / immunology*
  • Serum Amyloid P-Component / metabolism
  • Time Factors

Substances

  • Anti-Inflammatory Agents
  • Autoantibodies
  • Biomarkers
  • Immunoglobulin G
  • Protective Agents
  • Serum Amyloid P-Component
  • PTX3 protein
  • Complement C1q
  • C-Reactive Protein