Defective negative regulation of antigen receptor signaling in Lyn-deficient B lymphocytes

Curr Biol. 1998 May 7;8(10):545-53. doi: 10.1016/s0960-9822(98)70223-4.

Abstract

Background: To elucidate the role of the Src family kinase Lyn in B cell receptor (BCR) signaling, we and others previously generated lyn-/- mice and analyzed their B cell responses. Although the initiation of BCR signaling in lyn-/- B cells is delayed, BCR-induced ERK2 activation and proliferation are enhanced. As the co-receptors Fc gamma RIIb1 and CD22 have been shown to be negative regulators of BCR signaling, we have now examined their functional roles in lyn-/- B cells.

Results: B cells from lyn-/- mice have increased expression of the protein product of the early response gene egr-1, enhanced activation of Jun N-terminal kinase (JNK), and elevated calcium responses upon BCR cross-linking. Tyrosine phosphorylation of Fc gamma RIIb1 in lyn-/- B cells was reduced but negative regulation of the BCR signal by Fc gamma RIIb1 was only modestly impaired. In contrast, tyrosine phosphorylation of CD22 was greatly decreased in lyn-/- B cells, correlating with the inability of CD22 to downregulate the BCR-induced calcium response in these cells. Surprisingly, CD22 remains capable of regulating the ERK2 and JNK pathways in lyn-/- B cells, which may relate to the small residual increase in BCR-induced CD22 phosphorylation.

Conclusions: BCR signal initiation and negative regulation by Fc gamma RIIb1 is not critically dependent on Lyn. In contrast, Lyn plays a particularly important role in the tyrosine phosphorylation of CD22 and in the consequent inhibition of BCR-induced calcium influx. The net result of the Lyn deficiency in B cells is hyperresponsiveness to antigen stimulation, which may explain the autoimmunity observed in lyn-/- mice.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Antigens, CD / biosynthesis
  • Antigens, CD / metabolism*
  • Antigens, Differentiation, B-Lymphocyte / metabolism*
  • B-Lymphocytes / metabolism*
  • Calcium / metabolism
  • Calcium-Calmodulin-Dependent Protein Kinases / metabolism
  • Cell Adhesion Molecules*
  • Cells, Cultured
  • Enzyme Activation
  • Gene Deletion
  • JNK Mitogen-Activated Protein Kinases
  • Lectins*
  • Mice
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 9
  • Mitogen-Activated Protein Kinases*
  • Protein Kinases / metabolism
  • Rabbits
  • Receptors, Antigen, B-Cell / genetics
  • Receptors, Antigen, B-Cell / physiology*
  • Receptors, IgG / biosynthesis
  • Sialic Acid Binding Ig-like Lectin 2
  • Signal Transduction*
  • Tyrosine / metabolism
  • src-Family Kinases / genetics
  • src-Family Kinases / physiology*

Substances

  • Antigens, CD
  • Antigens, Differentiation, B-Lymphocyte
  • Cd22 protein, mouse
  • Cell Adhesion Molecules
  • Fc gamma receptor IIB
  • Lectins
  • Receptors, Antigen, B-Cell
  • Receptors, IgG
  • Sialic Acid Binding Ig-like Lectin 2
  • Tyrosine
  • Protein Kinases
  • Mitogen-Activated Protein Kinase 9
  • src-Family Kinases
  • Calcium-Calmodulin-Dependent Protein Kinases
  • JNK Mitogen-Activated Protein Kinases
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinases
  • Calcium