Decoration of T-independent antigen with ligands for CD22 and Siglec-G can suppress immunity and induce B cell tolerance in vivo

J Exp Med. 2010 Jan 18;207(1):173-87. doi: 10.1084/jem.20091873. Epub 2009 Dec 28.

Abstract

Autoreactive B lymphocytes first encountering self-antigens in peripheral tissues are normally regulated by induction of anergy or apoptosis. According to the "two-signal" model, antigen recognition alone should render B cells tolerant unless T cell help or inflammatory signals such as lipopolysaccharide are provided. However, no such signals seem necessary for responses to T-independent type 2 (TI-2) antigens, which are multimeric antigens lacking T cell epitopes and Toll-like receptor ligands. How then do mature B cells avoid making a TI-2-like response to multimeric self-antigens? We present evidence that TI-2 antigens decorated with ligands of inhibitory sialic acid-binding Ig-like lectins (siglecs) are poorly immunogenic and can induce tolerance to subsequent challenge with immunogenic antigen. Two siglecs, CD22 and Siglec-G, contributed to tolerance induction, preventing plasma cell differentiation or survival. Although mutations in CD22 and its signaling machinery have been associated with dysregulated B cell development and autoantibody production, previous analyses failed to identify a tolerance defect in antigen-specific mutant B cells. Our results support a role for siglecs in B cell self-/nonself-discrimination, namely suppressing responses to self-associated antigens while permitting rapid "missing self"-responses to unsialylated multimeric antigens. The results suggest use of siglec ligand antigen constructs as an approach for inducing tolerance.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Antibody Formation / physiology
  • Autoantibodies / genetics
  • Autoantibodies / immunology
  • Autoantigens / genetics
  • Autoantigens / immunology*
  • Cell Differentiation / genetics
  • Cell Differentiation / immunology
  • Cell Survival / genetics
  • Cell Survival / immunology
  • Immune Tolerance / physiology*
  • Inflammation / genetics
  • Inflammation / immunology
  • Lectins / genetics
  • Lectins / immunology*
  • Ligands
  • Mice
  • Mice, Knockout
  • Plasma Cells / cytology
  • Plasma Cells / immunology*
  • Receptors, Antigen, B-Cell / genetics
  • Receptors, Antigen, B-Cell / immunology*
  • Sialic Acid Binding Ig-like Lectin 2 / genetics
  • Sialic Acid Binding Ig-like Lectin 2 / immunology*
  • Sialic Acid Binding Immunoglobulin-like Lectins
  • Signal Transduction / immunology*
  • T-Lymphocytes, Helper-Inducer / cytology
  • T-Lymphocytes, Helper-Inducer / immunology

Substances

  • Autoantibodies
  • Autoantigens
  • Cd22 protein, mouse
  • Lectins
  • Ligands
  • Receptors, Antigen, B-Cell
  • Sialic Acid Binding Ig-like Lectin 2
  • Sialic Acid Binding Immunoglobulin-like Lectins
  • Siglecg protein, mouse