T cell Ig and mucin domain-containing protein 3 is recruited to the immune synapse, disrupts stable synapse formation, and associates with receptor phosphatases

J Immunol. 2014 Jan 15;192(2):782-91. doi: 10.4049/jimmunol.1302663. Epub 2013 Dec 13.

Abstract

CD8(+) CTLs are adept at killing virally infected cells and cancer cells and releasing cytokines (e.g., IFN-γ) to aid this response. However, during cancer and chronic viral infections, such as with HIV, this CTL response is progressively impaired due to a process called T cell exhaustion. Previous work has shown that the glycoprotein T cell Ig and mucin domain-containing protein 3 (Tim-3) plays a functional role in establishing T cell exhaustion. Tim-3 is highly upregulated on virus and tumor Ag-specific CD8(+) T cells, and antagonizing Tim-3 helps restore function of CD8(+) T cells. However, very little is known of how Tim-3 signals in CTLs. In this study, we assessed the role of Tim-3 at the immunological synapse as well as its interaction with proximal TCR signaling molecules in primary human CD8(+) T cells. Tim-3 was found within CD8(+) T cell lipid rafts at the immunological synapse. Blocking Tim-3 resulted in a significantly greater number of stable synapses being formed between Tim-3(hi)CD8(+) T cells and target cells, suggesting that Tim-3 plays a functional role in synapse formation. Further, we confirmed that Tim-3 interacts with Lck, but not the phospho-active form of Lck. Finally, Tim-3 colocalizes with receptor phosphatases CD45 and CD148, an interaction that is enhanced in the presence of the Tim-3 ligand, galectin-9. Thus, Tim-3 interacts with multiple signaling molecules at the immunological synapse, and characterizing these interactions could aid in the development of therapeutics to restore Tim-3-mediated immune dysfunction.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • CD8-Positive T-Lymphocytes / metabolism
  • Galectins / metabolism
  • HIV Infections / metabolism
  • Hepatitis A Virus Cellular Receptor 2
  • Humans
  • Leukocyte Common Antigens / metabolism
  • Lymphocyte Specific Protein Tyrosine Kinase p56(lck) / metabolism
  • Membrane Proteins / metabolism*
  • Phosphoric Monoester Hydrolases / metabolism*
  • Receptor-Like Protein Tyrosine Phosphatases, Class 3 / metabolism
  • Signal Transduction / physiology
  • Synapses / metabolism*

Substances

  • Galectins
  • HAVCR2 protein, human
  • Hepatitis A Virus Cellular Receptor 2
  • Membrane Proteins
  • Lymphocyte Specific Protein Tyrosine Kinase p56(lck)
  • Phosphoric Monoester Hydrolases
  • Leukocyte Common Antigens
  • PTPRC protein, human
  • PTPRJ protein, human
  • Receptor-Like Protein Tyrosine Phosphatases, Class 3