Negative regulation of T cell receptor signaling by Siglec-7 (p70/AIRM) and Siglec-9

J Biol Chem. 2004 Oct 8;279(41):43117-25. doi: 10.1074/jbc.M403538200. Epub 2004 Aug 3.

Abstract

Siglec-7 (p70/AIRM) and Siglec-9 are "CD33"-related siglecs expressed on natural killer (NK) cells and subsets of peripheral T cells. Like other inhibitory NK cell receptors, they contain immunoglobulin receptor family tyrosine-based inhibitory motifs in their cytoplasmic domains, and Siglec-7 has been demonstrated to negatively regulate NK cell activation. Based on reports of the presence of these siglecs on T cells, we sought to determine if they are capable of modulating T cell receptor (TCR) signaling using Jurkat T cells stably and transiently transfected with Siglec-7 or Siglec-9. Following either pervanadate stimulation or TCR engagement, both Siglecs exhibited increased tyrosine phosphorylation and recruitment of SHP-1. Effects of Siglec-7 and -9 were also evident in downstream events in the signaling pathway. Both siglecs reduced phosphorylation of Tyr319 on ZAP-70, known to play a pivotal role in up-regulation of gene transcription following TCR stimulation. There was also a corresponding decreased transcriptional activity of nuclear factor of activated T cells (NFAT) as determined using a luciferase reporter gene. Like all siglecs, Siglec-7 and -9 recognize sialic acid-containing glycans of glycoproteins and glycolipids as ligands. Mutation of the conserved Arg in the ligand binding site of Siglec-7 (Arg124) or Siglec-9 (Arg120) resulted in reduced inhibitory function in the NFAT/luciferase transcription assay, suggesting that ligand binding is required for optimal inhibition of TCR signaling. The combined results demonstrate that both Siglec-7 and Siglec-9 are capable of negative regulation of TCR signaling and that ligand binding is required for optimal activity.

Publication types

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

MeSH terms

  • Amino Acid Motifs
  • Antigens, CD / chemistry
  • Antigens, CD / metabolism
  • Antigens, CD / physiology*
  • Antigens, Differentiation, Myelomonocytic / chemistry
  • Antigens, Differentiation, Myelomonocytic / metabolism
  • Antigens, Differentiation, Myelomonocytic / physiology*
  • Blotting, Western
  • Cell Separation
  • Cytoplasm / metabolism
  • Dose-Response Relationship, Drug
  • Enzyme Activation
  • Enzyme Inhibitors / pharmacology
  • Flow Cytometry
  • Genes, Reporter
  • Humans
  • Immunoprecipitation
  • Jurkat Cells
  • Lectins / metabolism
  • Lectins / physiology*
  • Ligands
  • Luciferases / metabolism
  • Microscopy, Fluorescence
  • Models, Biological
  • Phosphorylation
  • Protein Binding
  • Protein Structure, Tertiary
  • Protein-Tyrosine Kinases / chemistry
  • Sialic Acid Binding Ig-like Lectin 3
  • Sialic Acid Binding Immunoglobulin-like Lectins
  • Signal Transduction
  • T-Lymphocytes / metabolism
  • Time Factors
  • Transcription, Genetic
  • Transcriptional Activation
  • Transfection
  • Tyrosine / chemistry
  • Vanadates / chemistry
  • ZAP-70 Protein-Tyrosine Kinase

Substances

  • Antigens, CD
  • Antigens, Differentiation, Myelomonocytic
  • CD33 protein, human
  • Enzyme Inhibitors
  • Lectins
  • Ligands
  • SIGLEC7 protein, human
  • SIGLEC9 protein, human
  • Sialic Acid Binding Ig-like Lectin 3
  • Sialic Acid Binding Immunoglobulin-like Lectins
  • pervanadate
  • Vanadates
  • Tyrosine
  • Luciferases
  • Protein-Tyrosine Kinases
  • ZAP-70 Protein-Tyrosine Kinase
  • ZAP70 protein, human