Phosphorylation of the multifunctional signal transducer B-cell adaptor protein (BCAP) promotes recruitment of multiple SH2/SH3 proteins including GRB2

J Biol Chem. 2019 Dec 27;294(52):19852-19861. doi: 10.1074/jbc.RA119.009931. Epub 2019 Sep 16.

Abstract

B-cell adaptor protein (BCAP) is a multimodular, multifunctional signal transducer that regulates signal transduction pathways in leukocytes, including macrophages, B-cells, and T-cells. In particular, BCAP suppresses inflammatory signaling by Toll-like receptors (TLRs). However, how BCAP itself is regulated and what its interaction partners are is unclear. Here, using human immune cell lines, including THP-1 cells, we characterized the complex phosphorylation patterns of BCAP and used a novel protein complex trapping strategy, called virotrap, to identify its interaction partners. This analysis identified known interactions of BCAP with phosphoinositide 3-kinase (PI3K) p85 subunit and NCK adaptor protein (NCK), together with previously unknown interactions of BCAP with Src homology 2 (SH2) and SH3 domain-containing adaptor proteins, notably growth factor receptor-bound protein 2 (GRB2) and CRK-like proto-oncogene, adaptor protein (CRKL). We show that the SH3 domain of GRB2 can bind to BCAP independently of BCAP phosphorylation status, suggesting that the SH2 domains mediate interactions with activated receptor tyrosine kinase complexes including the CD19 subunit of the B-cell receptor. Our results also suggested that the PI3K p85 subunit binds to BCAP via SH3 domains forming an inactive complex that is then activated by sequential binding with the SH2 domains. Taken together, our results indicate that BCAP is a complex hub that processes signals from multiple pathways in diverse cell types of the immune system.

Keywords: B-cell adaptor protein; Src homology 2 domain (SH2 domain); Src homology 3 domain (SH3 domain); Toll-like receptor (TLR); immunity; kinase signaling; phosphoinositide 3-kinase; phosphorylation; signal transduction; virotrap.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism*
  • Agammaglobulinaemia Tyrosine Kinase / metabolism
  • Amino Acid Motifs
  • Binding Sites
  • Cell Line, Tumor
  • GRB2 Adaptor Protein / metabolism*
  • Genes, Reporter
  • HEK293 Cells
  • Humans
  • Mass Spectrometry
  • Oncogene Proteins / metabolism
  • Peptides / analysis
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphorylation
  • Protein Binding
  • Proto-Oncogene Mas
  • src Homology Domains

Substances

  • Adaptor Proteins, Signal Transducing
  • CRKL protein
  • GRB2 Adaptor Protein
  • GRB2 protein, human
  • MAS1 protein, human
  • Nck protein
  • Oncogene Proteins
  • PIK3AP1 protein, human
  • Peptides
  • Proto-Oncogene Mas
  • phosphoinositol-3 kinase regulatory subunit 2, human
  • Agammaglobulinaemia Tyrosine Kinase
  • BTK protein, human