Cell-intrinsic expression of TLR9 in autoreactive B cells constrains BCR/TLR7-dependent responses

J Immunol. 2015 Mar 15;194(6):2504-12. doi: 10.4049/jimmunol.1402425. Epub 2015 Feb 13.

Abstract

Endosomal TLRs play an important role in systemic autoimmune diseases, such as systemic erythematosus lupus, in which DNA- and RNA-associated autoantigens activate autoreactive B cells through TLR9- and TLR7-dependent pathways. Nevertheless, TLR9-deficient autoimmune-prone mice develop more severe clinical disease, whereas TLR7-deficient and TLR7/9-double deficient autoimmune-prone mice develop less severe disease. To determine whether the regulatory activity of TLR9 is B cell intrinsic, we directly compared the functional properties of autoantigen-activated wild-type, TLR9-deficient, and TLR7-deficient B cells in an experimental system in which proliferation depends on BCR/TLR coengagement. In vitro, TLR9-deficient cells are less dependent on survival factors for a sustained proliferative response than are either wild-type or TLR7-deficient cells. The TLR9-deficient cells also preferentially differentiate toward the plasma cell lineage, as indicated by expression of CD138, sustained expression of IRF4, and other molecular markers of plasma cells. In vivo, autoantigen-activated TLR9-deficient cells give rise to greater numbers of autoantibody-producing cells. Our results identify distinct roles for TLR7 and TLR9 in the differentiation of autoreactive B cells that explain the capacity of TLR9 to limit, as well as TLR7 to promote, the clinical features of systemic erythematosus lupus.

Publication types

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

MeSH terms

  • Animals
  • Autoantibodies / immunology
  • Autoantibodies / metabolism
  • Autoantigens / immunology
  • Autoimmunity / genetics
  • Autoimmunity / immunology
  • B-Lymphocytes / immunology*
  • B-Lymphocytes / metabolism
  • Cell Differentiation / genetics
  • Cell Differentiation / immunology
  • Cell Proliferation / genetics
  • Cells, Cultured
  • Flow Cytometry
  • Interferon Regulatory Factors / immunology
  • Interferon Regulatory Factors / metabolism
  • Lymphocyte Activation / genetics
  • Lymphocyte Activation / immunology
  • Mice, Inbred BALB C
  • Mice, Knockout
  • Mice, Transgenic
  • Oligonucleotide Array Sequence Analysis
  • Plasma Cells / immunology
  • Plasma Cells / metabolism
  • Receptors, Antigen, B-Cell / immunology*
  • Receptors, Antigen, B-Cell / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Rheumatoid Factor / immunology
  • Syndecan-1 / immunology
  • Syndecan-1 / metabolism
  • Toll-Like Receptor 7 / deficiency
  • Toll-Like Receptor 7 / genetics
  • Toll-Like Receptor 7 / immunology*
  • Toll-Like Receptor 9 / deficiency
  • Toll-Like Receptor 9 / genetics
  • Toll-Like Receptor 9 / immunology*
  • Transcriptome / immunology

Substances

  • Autoantibodies
  • Autoantigens
  • Interferon Regulatory Factors
  • Receptors, Antigen, B-Cell
  • Syndecan-1
  • Toll-Like Receptor 7
  • Toll-Like Receptor 9
  • interferon regulatory factor-4
  • Rheumatoid Factor

Associated data

  • GEO/GSE58756