Impact of loss of NF-κB1, NF-κB2 or c-REL on SLE-like autoimmune disease and lymphadenopathy in Fas(lpr/lpr) mutant mice

Immunol Cell Biol. 2016 Jan;94(1):66-78. doi: 10.1038/icb.2015.66. Epub 2015 Jun 18.

Abstract

Defects in apoptosis can cause autoimmune disease. Loss-of-function mutations in the 'death receptor' FAS impair the deletion of autoreactive lymphocytes in the periphery, leading to progressive lymphadenopathy and systemic lupus erythematosus-like autoimmune disease in mice (Fas(lpr/lpr) (mice homozygous for the lymphoproliferation inducing spontaneous mutation)) and humans. The REL/nuclear factor-κB (NF-κB) transcription factors regulate a broad range of immune effector functions and are also implicated in various autoimmune diseases. We generated compound mutant mice to investigate the individual functions of the NF-κB family members NF-κB1, NF-κB2 and c-REL in the various autoimmune pathologies of Fas(lpr/lpr) mutant mice. We show that loss of each of these transcription factors resulted in amelioration of many classical features of autoimmune disease, including hypergammaglobulinaemia, anti-nuclear autoantibodies and autoantibodies against tissue-specific antigens. Remarkably, only c-REL deficiency substantially reduced immune complex-mediated glomerulonephritis and extended the lifespan of Fas(lpr/lpr) mice. Interestingly, compared with the Fas(lpr/lpr) animals, Fas(lpr/lpr)nfkb2(-/-) mice presented with a dramatic acceleration and augmentation of lymphadenopathy that was accompanied by severe lung pathology due to extensive lymphocytic infiltration. The Fas(lpr/lpr)nfkb1(-/-) mice exhibited the combined pathologies caused by defects in FAS-mediated apoptosis and premature ageing due to loss of NF-κB1. These findings demonstrate that different NF-κB family members exert distinct roles in the development of the diverse autoimmune and lymphoproliferative pathologies that arise in Fas(lpr/lpr) mice, and suggest that pharmacological targeting of c-REL should be considered as a strategy for therapeutic intervention in autoimmune diseases.

Publication types

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

MeSH terms

  • AIRE Protein
  • Animals
  • Autoantibodies / blood
  • Chemokines / blood
  • Chemokines / metabolism
  • Dermatitis / blood
  • Dermatitis / complications
  • Dermatitis / immunology
  • Forkhead Transcription Factors / metabolism
  • Genotype
  • Hypergammaglobulinemia / blood
  • Hypergammaglobulinemia / complications
  • Immune Tolerance / immunology
  • Leukocytes / pathology
  • Longevity
  • Lupus Erythematosus, Systemic / blood
  • Lupus Erythematosus, Systemic / complications*
  • Lymphatic Diseases / blood
  • Lymphatic Diseases / complications*
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Mutant Strains
  • NF-kappa B p50 Subunit / deficiency*
  • NF-kappa B p50 Subunit / metabolism
  • NF-kappa B p52 Subunit / deficiency*
  • NF-kappa B p52 Subunit / metabolism
  • Organ Specificity
  • Proto-Oncogene Proteins c-rel / metabolism*
  • Splenomegaly / blood
  • Transcription Factors / metabolism
  • fas Receptor / metabolism*

Substances

  • Autoantibodies
  • Chemokines
  • Fas protein, mouse
  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • NF-kappa B p50 Subunit
  • NF-kappa B p52 Subunit
  • Nfkb2 protein, mouse
  • Proto-Oncogene Proteins c-rel
  • Transcription Factors
  • fas Receptor
  • Nfkb1 protein, mouse