B cell receptor basal signaling regulates antigen-induced Ig light chain rearrangements

J Immunol. 2008 Apr 1;180(7):4728-41. doi: 10.4049/jimmunol.180.7.4728.

Abstract

BCR editing in the bone marrow contributes to B cell tolerance by orchestrating secondary Ig rearrangements in self-reactive B cells. We have recently shown that loss of the BCR or a pharmacologic blockade of BCR proximal signaling pathways results in a global "back-differentiation" response in which immature B cells down-regulate genes important for the mature B cell program and up-regulate genes characteristic of earlier stages of B cell development. These observations led us to test the hypothesis that self-Ag-induced down-regulation of the BCR, and not self-Ag-induced positive signals, lead to Rag induction and hence receptor editing. Supporting this hypothesis, we found that immature B cells from xid (x-linked immunodeficiency) mice induce re-expression of a Rag2-GFP bacterial artificial chromosome reporter as well as wild-type immature B cells following Ag incubation. Incubation of immature B cells with self-Ag leads to a striking reversal in differentiation to the pro-/pre-B stage of development, consistent with the idea that back-differentiation results in the reinduction of genes required for L chain rearrangement and receptor editing. Importantly, Rag induction, the back-differentiation response to Ag, and editing in immature and pre-B cells are inhibited by a combination of phorbol ester and calcium ionophore, agents that bypass proximal signaling pathways and mimic BCR signaling. Thus, mimicking positive BCR signals actually inhibits receptor editing. These findings support a model whereby Ag-induced receptor editing is inhibited by BCR basal signaling on developing B cells; BCR down-regulation removes this basal signal, thereby initiating receptor editing.

Publication types

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

MeSH terms

  • Animals
  • Antigens / immunology*
  • B-Lymphocytes / cytology
  • B-Lymphocytes / drug effects
  • B-Lymphocytes / immunology
  • Cell Differentiation / drug effects
  • Cell Differentiation / immunology
  • Cells, Cultured
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Down-Regulation / immunology
  • Female
  • Genes, Reporter / genetics
  • Humans
  • Immunoglobulin Light Chains / immunology*
  • Ionophores / pharmacology
  • Kinetics
  • Male
  • Mice
  • Mice, Transgenic
  • Oligonucleotide Array Sequence Analysis
  • Phorbol Esters / pharmacology
  • Receptors, Antigen, B-Cell / immunology*
  • Receptors, Fc / immunology
  • Signal Transduction / immunology*
  • src-Family Kinases / genetics
  • src-Family Kinases / metabolism

Substances

  • Antigens
  • DNA-Binding Proteins
  • Immunoglobulin Light Chains
  • Ionophores
  • Phorbol Esters
  • Rag2 protein, mouse
  • Receptors, Antigen, B-Cell
  • Receptors, Fc
  • immunoglobulin M receptor
  • lyn protein-tyrosine kinase
  • src-Family Kinases