Functional cloning of Src-like adapter protein-2 (SLAP-2), a novel inhibitor of antigen receptor signaling

J Exp Med. 2001 Nov 5;194(9):1263-76. doi: 10.1084/jem.194.9.1263.

Abstract

In an effort to identify novel therapeutic targets for autoimmunity and transplant rejection, we developed and performed a large-scale retroviral-based functional screen to select for proteins that inhibit antigen receptor-mediated activation of lymphocytes. In addition to known regulators of antigen receptor signaling, we identified a novel adaptor protein, SLAP-2 which shares 36% sequence similarity with the known Src-like adaptor protein, SLAP. Similar to SLAP, SLAP-2 is predominantly expressed in hematopoietic cells. Overexpression of SLAP-2 in B and T cell lines specifically impaired antigen receptor-mediated signaling events, including CD69 surface marker upregulation, nuclear factor of activated T cells (NFAT) promoter activation and calcium influx. Signaling induced by phorbol myristate acetate (PMA) and ionomycin was not significantly reduced, suggesting SLAP-2 functions proximally in the antigen receptor signaling cascade. The SLAP-2 protein contains an NH2-terminal myristoylation consensus sequence and SH3 and SH2 Src homology domains, but lacks a tyrosine kinase domain. In antigen receptor-stimulated cells, SLAP-2 associated with several tyrosine phosphorylated proteins, including the ubiquitin ligase Cbl. Deletion of the COOH terminus of SLAP-2 blocked function and abrogated its association with Cbl. Mutation of the putative myristoylation site of SLAP-2 compromised its inhibitory activity and impaired its localization to the membrane compartment. Our identification of the negative regulator SLAP-2 demonstrates that a retroviral-based screening strategy may be an efficient way to identify and characterize the function of key components of many signal transduction systems.

MeSH terms

  • Adaptor Proteins, Signal Transducing*
  • Amino Acid Sequence
  • Antigens, CD / biosynthesis
  • Antigens, CD / genetics
  • Antigens, CD / immunology
  • Antigens, Differentiation, T-Lymphocyte / biosynthesis
  • Antigens, Differentiation, T-Lymphocyte / genetics
  • Antigens, Differentiation, T-Lymphocyte / immunology
  • B-Lymphocytes / cytology
  • B-Lymphocytes / immunology
  • Base Sequence
  • Calcium / metabolism
  • Cell Line
  • Cloning, Molecular
  • DNA, Complementary
  • DNA-Binding Proteins / genetics
  • Humans
  • Jurkat Cells
  • Lectins, C-Type
  • Molecular Sequence Data
  • Myristic Acid / metabolism
  • NFATC Transcription Factors
  • Nuclear Proteins*
  • Phosphorylation
  • Promoter Regions, Genetic
  • Proto-Oncogene Proteins pp60(c-src) / genetics*
  • Proto-Oncogene Proteins pp60(c-src) / immunology*
  • Receptor Protein-Tyrosine Kinases / biosynthesis
  • Receptor Protein-Tyrosine Kinases / immunology
  • Receptors, Antigen, B-Cell / immunology*
  • Receptors, Antigen, T-Cell / immunology*
  • Sequence Homology, Amino Acid
  • Signal Transduction / immunology*
  • Tetracycline / pharmacology
  • Trans-Activators
  • Transcription Factors / genetics
  • Transcriptional Activation
  • Tyrosine / metabolism
  • src Homology Domains*

Substances

  • Adaptor Proteins, Signal Transducing
  • Antigens, CD
  • Antigens, Differentiation, T-Lymphocyte
  • CD69 antigen
  • DNA, Complementary
  • DNA-Binding Proteins
  • Lectins, C-Type
  • NFATC Transcription Factors
  • Nuclear Proteins
  • Receptors, Antigen, B-Cell
  • Receptors, Antigen, T-Cell
  • SLA protein, human
  • SLA2 protein, human
  • Sla2 protein, mouse
  • Trans-Activators
  • Transcription Factors
  • Myristic Acid
  • Tyrosine
  • Receptor Protein-Tyrosine Kinases
  • TYRO3 protein, human
  • Proto-Oncogene Proteins pp60(c-src)
  • Tetracycline
  • Calcium