Innate and humoral recognition of the products of cell death: differential antigenicity and immunogenicity in lupus

Clin Exp Immunol. 2017 Mar;187(3):353-368. doi: 10.1111/cei.12889. Epub 2016 Dec 5.

Abstract

While apoptotic debris is believed to constitute the original antigenic insult in lupus (which is characterized by a time-dependent diversification of autoreactivity), whether such debris and autoantibodies specifically recognizing its constituents mediate differential effects on innate and humoral responses in lupus-prone mice is currently unknown. Apoptotic blebs (as opposed to cellular lysate) enhanced preferentially the maturation of dendritic cells (DCs) from bone marrow precursors drawn from lupus-prone mice. Murine, somatically mutated, apoptotic cell-reactive immunoglobulin (Ig)G monoclonal antibodies demonstrated enhanced recognition of DCs and also displayed a prominent lupus strain-specific bias in mediating DC maturation. Further, immunization of such antibodies specifically in lupus-prone mice resulted in widespread humoral autoreactivity; hypergammaglobulinaemia (a hallmark of systemic autoimmunity) was observed, accompanied by enhanced antibody titres to cellular moieties. Induced antibodies recognized antigens distinct from those recognized by the antibodies employed for immunization; in particular, nephritis-associated anti-double stranded (ds) DNA antibodies and neonatal lupus-associated anti-Ro60 antibodies were elicited by a non-dsDNA, non-Ro60 reactive antibody, and Sm was a favoured target. Further, only in lupus-prone mice did such immunization enhance the kinetics of humoral anti-self responses, resulting in the advanced onset of glomerulosclerosis. These studies reveal that preferential innate and humoral recognition of the products of cell death in a lupus milieu influence the indices associated with autoimmune pathology.

Keywords: aberrant apoptosis; antigen spreading; apoptosis; immune pathology; systemic autoreactivity; systemic lupus erthythematosus.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Antinuclear / immunology
  • Antibody Formation / immunology*
  • Antibody Specificity / immunology
  • Antigens / immunology*
  • Apoptosis / immunology
  • Autoantibodies / immunology
  • Autoimmunity / immunology
  • Cell Death / immunology*
  • DNA / immunology
  • Dendritic Cells / immunology
  • Humans
  • Immunity, Humoral / immunology*
  • Immunity, Innate / immunology*
  • Immunization / methods
  • Immunoglobulin G / immunology
  • Lupus Erythematosus, Systemic / immunology*
  • Lupus Nephritis / immunology
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred NZB

Substances

  • Antibodies, Antinuclear
  • Antigens
  • Autoantibodies
  • Immunoglobulin G
  • DNA