Murine natural killer immunoreceptors use distinct proximal signaling complexes to direct cell function

Blood. 2013 Apr 18;121(16):3135-46. doi: 10.1182/blood-2012-12-474361. Epub 2013 Feb 13.

Abstract

Signaling pathways leading to natural killer (NK)-cell effector function are complex and incompletely understood. Here, we investigated the proximal signaling pathways downstream of the immunotyrosine-based activation motif (ITAM) bearing activating receptors. We found that the adaptor molecule SH2 domain-containing leukocyte protein of 76 kD (SLP-76) is recruited to microclusters at the plasma membrane in activated NK cells and that this is required for initiation of downstream signaling and multiple NK-cell effector functions in vitro and in vivo. Surprisingly, we found that 2 types of proximal signaling complexes involving SLP-76 were formed. In addition to the canonical membrane complex formed between SLP-76 and linker for activation of T cells (LAT) family members, a novel LAT family-independent SLP-76-dependent signaling pathway was identified. The LAT family-independent pathway involved the SH2 domain of SLP-76 and adhesion and degranulation-promoting adaptor protein (ADAP). Both the LAT family-dependent and ADAP-dependent pathway contributed to interferon-gamma production and cytotoxicity; however, they were not essential for other SLP-76-dependent events, including phosphorylation of AKT and extracellular signal-related kinase and cellular proliferation. These results demonstrate that NK cells possess an unexpected bifurcation of proximal ITAM-mediated signaling, each involving SLP-76 and contributing to optimal NK-cell function.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / analysis
  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / immunology*
  • Adaptor Proteins, Signal Transducing / metabolism
  • Amino Acid Transport System y+ / immunology*
  • Amino Acid Transport System y+L
  • Animals
  • Cell Line, Tumor
  • Cell Proliferation
  • Cells, Cultured
  • Fusion Regulatory Protein 1, Light Chains / immunology*
  • Interferon-gamma / immunology
  • Killer Cells, Natural / cytology
  • Killer Cells, Natural / immunology*
  • Killer Cells, Natural / metabolism
  • MAP Kinase Signaling System
  • Mice
  • Mice, Inbred C57BL
  • Mice, Inbred NOD
  • Mice, Knockout
  • NK Cell Lectin-Like Receptor Subfamily A / immunology*
  • Neoplasms / genetics
  • Neoplasms / immunology
  • Neoplasms / pathology
  • Phosphoproteins / analysis
  • Phosphoproteins / genetics
  • Phosphoproteins / immunology*
  • Phosphoproteins / metabolism
  • Phosphorylation
  • Proto-Oncogene Proteins c-akt / immunology
  • Signal Transduction

Substances

  • Adaptor Proteins, Signal Transducing
  • Amino Acid Transport System y+
  • Amino Acid Transport System y+L
  • Fusion Regulatory Protein 1, Light Chains
  • Fyb protein, mouse
  • NK Cell Lectin-Like Receptor Subfamily A
  • Phosphoproteins
  • SLC7A8 protein, mouse
  • SLP-76 signal Transducing adaptor proteins
  • Slc7a7 protein, mouse
  • Interferon-gamma
  • Proto-Oncogene Proteins c-akt