Incomplete activation of CD4 T cells by antigen-presenting transitional immature B cells: implications for peripheral B and T cell responsiveness

J Immunol. 2003 Aug 15;171(4):1758-67. doi: 10.4049/jimmunol.171.4.1758.

Abstract

B cells leave the bone marrow as transitional B cells. Transitional B cells represent a target of negative selection and peripheral tolerance, both of which are abrogated in vitro by mediators of T cell help. In vitro, transitional and mature B cells differ in their responses to B cell receptor ligation. Whereas mature B cells up-regulate the T cell costimulatory molecule CD86 (B7.2) and are activated, transitional B cells do not and undergo apoptosis. The ability of transitional B cells to process and present Ag to CD4 T cells and to elicit protective signals in the absence of CD86 up-regulation was investigated. We report that transitional B cells can process and present Ag as peptide:MHC class II complexes. However, their ability to activate T cells and elicit help signals from CD4-expressing Th cells was compromised compared with mature B cells, unless exogenous T cell costimulation was provided. A stringent requirement for CD28 costimulation was not evident in interactions between transitional B cells and preactivated CD4-expressing T cells, indicating that T cells involved in vivo in an ongoing immune response might rescue Ag-specific transitional B cells from negative selection. These data suggest that during an immune response, immature B cells may be able to sustain the responses of preactivated CD4(+) T cells, while being unable to initiate activation of naive T cells. Furthermore, the ability of preactivated, but not naive T cells to provide survival signals to B cell receptor-engaged transitional immature B cells argues that these B cells may be directed toward activation rather than negative selection when encountering Ag in the context of a pre-existing immune response.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Antigen Presentation
  • Antigen-Presenting Cells / immunology*
  • Antigen-Presenting Cells / metabolism
  • Antigens, CD / biosynthesis
  • Apoptosis / immunology
  • B-Lymphocyte Subsets / cytology*
  • B-Lymphocyte Subsets / immunology*
  • B-Lymphocyte Subsets / metabolism
  • B7-2 Antigen
  • Bystander Effect / immunology*
  • CD28 Antigens / pharmacology
  • CD4-Positive T-Lymphocytes / immunology*
  • Cell Differentiation / immunology
  • Cell Membrane / immunology
  • Cell Membrane / metabolism
  • Cells, Cultured
  • Clonal Anergy
  • Coculture Techniques
  • Endocytosis / immunology
  • Epitopes, T-Lymphocyte / metabolism
  • Female
  • Histocompatibility Antigens Class II / metabolism
  • Immune Tolerance
  • Lymphocyte Activation / immunology*
  • Macromolecular Substances
  • Membrane Glycoproteins / biosynthesis
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred CBA
  • Mice, Transgenic
  • Ovalbumin / immunology
  • Ovalbumin / metabolism
  • Peptide Fragments / immunology
  • Peptide Fragments / metabolism
  • Protein Processing, Post-Translational / immunology
  • Receptors, Antigen, B-Cell / physiology
  • Signal Transduction / immunology
  • Up-Regulation / immunology

Substances

  • Antigens, CD
  • B7-2 Antigen
  • CD28 Antigens
  • Cd86 protein, mouse
  • Epitopes, T-Lymphocyte
  • Histocompatibility Antigens Class II
  • Macromolecular Substances
  • Membrane Glycoproteins
  • OVA 323-339
  • Peptide Fragments
  • Receptors, Antigen, B-Cell
  • Ovalbumin