Impaired B Cell Apoptosis Results in Autoimmunity That Is Alleviated by Ablation of Btk

Front Immunol. 2021 Aug 26:12:705307. doi: 10.3389/fimmu.2021.705307. eCollection 2021.

Abstract

While apoptosis plays a role in B-cell self-tolerance, its significance in preventing autoimmunity remains unclear. Here, we report that dysregulated B cell apoptosis leads to delayed onset autoimmune phenotype in mice. Our longitudinal studies revealed that mice with B cell-specific deletion of pro-apoptotic Bim (BBimfl/fl ) have an expanded B cell compartment with a notable increase in transitional, antibody secreting and recently described double negative (DN) B cells. They develop greater hypergammaglobulinemia than mice lacking Bim in all cells and accumulate several autoantibodies characteristic of Systemic Lupus Erythematosus (SLE) and related Sjögren's Syndrome (SS) including anti-nuclear, anti-Ro/SSA and anti-La/SSB at a level comparable to NODH2h4 autoimmune mouse model. Furthermore, lymphocytes infiltrated the tissues including submandibular glands and formed follicle-like structures populated with B cells, plasma cells and T follicular helper cells indicative of ongoing immune reaction. This autoimmunity was ameliorated upon deletion of Bruton's tyrosine kinase (Btk) gene, which encodes a key B cell signaling protein. These studies suggest that Bim-mediated apoptosis suppresses and B cell tyrosine kinase signaling promotes B cell-mediated autoimmunity.

Keywords: B cell tolerance; Bcl-2-like 11 (Bim); Bruton’s tyrosine kinase (Bkt); Sjogren’s syndrome; apoptosis; autoantibodies; autoimmunity; systemic lupus - erythematosus.

Publication types

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

MeSH terms

  • Agammaglobulinaemia Tyrosine Kinase / antagonists & inhibitors*
  • Agammaglobulinaemia Tyrosine Kinase / deficiency
  • Agammaglobulinaemia Tyrosine Kinase / physiology
  • Animals
  • Antibody Specificity
  • Apoptosis / physiology*
  • Autoantibodies / blood
  • Autoimmune Diseases / immunology*
  • Autoimmunity / immunology*
  • B-Lymphocytes / enzymology
  • B-Lymphocytes / immunology*
  • B-Lymphocytes / pathology
  • Bcl-2-Like Protein 11 / deficiency
  • Bcl-2-Like Protein 11 / physiology*
  • Cell Division
  • Cells, Cultured
  • Hypergammaglobulinemia / immunology
  • Immune Tolerance / immunology
  • Lupus Erythematosus, Systemic / immunology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Receptors, Antigen / immunology
  • Sjogren's Syndrome / immunology
  • T-Lymphocytes / immunology

Substances

  • Autoantibodies
  • Bcl-2-Like Protein 11
  • Bcl2l11 protein, mouse
  • Receptors, Antigen
  • Agammaglobulinaemia Tyrosine Kinase
  • Btk protein, mouse