Distinct Roles for Bruton's Tyrosine Kinase in B Cell Immune Synapse Formation

Front Immunol. 2018 Sep 6:9:2027. doi: 10.3389/fimmu.2018.02027. eCollection 2018.

Abstract

Bruton's tyrosine kinase (Btk) has a key role in the signaling pathways of receptors essential for the B lymphocyte response. Given its implication in B cell-related immunodeficiencies, leukemias/lymphomas and autoimmunity, Btk is studied intensely and is a target for therapy. Here, using primary B cells from distinct mouse models and the pharmacological inhibitors ibrutinib and acalabrutinib, we report distinct roles for Btk in antigen-triggered immune synapse (IS) formation. Btk recruitment to the plasma membrane regulates the B cell ability to trigger IS formation as well as its appropriate molecular assembly; Btk shuttling/scaffold activities seem more relevant than the kinase function on that. Btk-kinase activity controls antigen accumulation at the IS through the PLCγ2/Ca2+ axis. Impaired Btk membrane-recruitment or kinase function likewise alters antigen-triggered microtubule-organizing center (MTOC) polarization to the IS, B cell activation and proliferation. Data also show that, for B cell function, IS architecture is as important as the quantity of antigen that accumulates at the synapse.

Keywords: B cells; Btk; actin cytoskeleton; cell activation; immune synapse; kinase; shuttling/scaffold.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenine / analogs & derivatives
  • Agammaglobulinaemia Tyrosine Kinase / antagonists & inhibitors
  • Agammaglobulinaemia Tyrosine Kinase / genetics
  • Agammaglobulinaemia Tyrosine Kinase / metabolism*
  • Animals
  • Antigens / metabolism
  • B-Lymphocytes / immunology*
  • Benzamides / pharmacology
  • Calcium Signaling
  • Cell Membrane / metabolism*
  • Cell Polarity
  • Cell Proliferation
  • Cells, Cultured
  • Immunological Synapses / metabolism*
  • Lymphocyte Activation
  • Mice
  • Mice, Inbred C57BL
  • Mice, Inbred CBA
  • Mice, Knockout
  • Microtubule-Organizing Center
  • Mutation / genetics
  • Phospholipase C gamma / metabolism
  • Piperidines
  • Protein Transport
  • Pyrazines / pharmacology
  • Pyrazoles / pharmacology
  • Pyrimidines / pharmacology
  • Receptors, Antigen, B-Cell / metabolism

Substances

  • Antigens
  • Benzamides
  • Piperidines
  • Pyrazines
  • Pyrazoles
  • Pyrimidines
  • Receptors, Antigen, B-Cell
  • ibrutinib
  • Agammaglobulinaemia Tyrosine Kinase
  • Phospholipase C gamma
  • acalabrutinib
  • Adenine