Nuclear autoantigen translocation and autoantibody opsonization lead to increased dendritic cell phagocytosis and presentation of nuclear antigens: a novel pathogenic pathway for autoimmunity?

J Immunol. 2005 Aug 15;175(4):2692-701. doi: 10.4049/jimmunol.175.4.2692.

Abstract

Autoreactivity in lupus requires the delivery of autoantigens to APCs in a proinflammatory context. It has been proposed that apoptotic cells are a source of lupus autoantigens and targets for autoantibodies. Using a histone H2B-GFP fusion protein as traceable Ag, we show here that lupus autoantibodies, directed against nuclear autoantigens, can opsonize apoptotic cells, enhance their uptake through induction of proinflammatory Fc gammaR-mediated phagocytosis, and augment Ag-specific T cell proliferation by increasing Ag loading. Apoptotic blebs and bodies seemed to be a preferred target of DC phagocytosis, via both "eat-me signals" and Fc gammaR-mediated mechanisms; furthermore, inhibition of nuclear Ag redistribution, by blockade of chromatin fragmentation, could stop binding and opsonization of apoptotic cells by autoantibodies, and inhibited Fc gamma-R-mediated enhancement of phagocytosis. Our results suggest that DC uptake of opsonized histones and other nuclear Ags from apoptotic cells is a novel pathway for the presentation of nuclear Ags in a highly inflammatory context. Blockade of chromatin fragmentation in lupus is a potential therapeutic approach, which could theoretically limit DC access to autoantigens delivered in proinflammatory context, while leaving available for tolerization those delivered in a noninflammatory context.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Active Transport, Cell Nucleus / immunology
  • Animals
  • Antibodies, Antinuclear / metabolism*
  • Antibodies, Antinuclear / physiology
  • Antigen Presentation / immunology*
  • Apoptosis / immunology
  • Apoptosis / radiation effects
  • Autoantigens / immunology
  • Autoantigens / metabolism*
  • Binding Sites, Antibody
  • Cell Line, Tumor
  • Chromatin / metabolism
  • DNA Fragmentation / immunology
  • Dendritic Cells / immunology*
  • Dendritic Cells / metabolism
  • Green Fluorescent Proteins / genetics
  • Histones / genetics
  • Histones / immunology
  • Histones / metabolism
  • Humans
  • Lupus Erythematosus, Systemic / immunology*
  • Lupus Erythematosus, Systemic / metabolism
  • Lupus Erythematosus, Systemic / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nuclear Proteins / immunology
  • Nuclear Proteins / metabolism*
  • Opsonin Proteins / metabolism*
  • Phagocytosis / immunology*
  • Receptors, IgG / metabolism
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / immunology
  • Recombinant Fusion Proteins / metabolism

Substances

  • Antibodies, Antinuclear
  • Autoantigens
  • Chromatin
  • Histones
  • Nuclear Proteins
  • Opsonin Proteins
  • Receptors, IgG
  • Recombinant Fusion Proteins
  • Green Fluorescent Proteins