Association of DAP12 with activating CD94/NKG2C NK cell receptors.

While the inhibitory NK cell receptors for MHC class I express immunoreceptor tyrosine-based inhibitory motifs that recruit intracellular tyrosine phosphatases and prevent NK cell effector function, the activating NK cell receptors lack intrinsic sequences required for cellular stimulation. CD94/NKG2C, an activating NK cell receptor of the C-type lectin superfamily that binds to HLA-E, noncovalently associates with DAP12, a membrane receptor containing an immunoreceptor tyrosine-based activating motif. Efficient expression of CD94/NKG2C on the cell surface requires the presence of DAP12, and charged residues in the transmembrane domains of DAP12 and NKG2C are necessary for this interaction. These results provide a molecular basis for the assembly of NK cell receptors for MHC class I involved in cellular activation and inhibition.

[1]  L. Lanier,et al.  Multicolor immunofluorescence and flow cytometry , 1991 .

[2]  C. Geisler,et al.  CD3 gamma contains a phosphoserine‐dependent di‐leucine motif involved in down‐regulation of the T cell receptor. , 1994, The EMBO journal.

[3]  Eric O Long,et al.  Killer cell inhibitory receptors specific for HLA-C and HLA-B identified by direct binding and by functional transfer. , 1995, Immunity.

[4]  J. Bonifacino,et al.  Membrane protein association by potential intrarnembrane charge pairs , 1991, Nature.

[5]  E. Dissen,et al.  Molecular characterization of a gene in the rat homologous to human CD94 , 1997, European journal of immunology.

[6]  J. Trowsdale,et al.  Cloning of NKG2‐F, a new member of the NKG2 family of human natural killer cell receptor genes , 1997, European journal of immunology.

[7]  J. Bell,et al.  HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C , 1998, Nature.

[8]  Eric O Long,et al.  Recruitment of tyrosine phosphatase HCP by the killer cell inhibitor receptor. , 1996, Immunity.

[9]  L. Lanier,et al.  Co-association of CD3ζ with a receptor (CD16) for IgG Fc on human natural killer cells , 1989, Nature.

[10]  A. Weiss,et al.  The lysine residue in the membrane-spanning domain of the beta chain is necessary for cell surface expression of the T cell antigen receptor , 1988, The Journal of experimental medicine.

[11]  Eric O Long,et al.  The Direct Binding of a p58 Killer Cell Inhibitory Receptor to Human Histocompatibility Leukocyte Antigen (HLA)-Cw4 Exhibits Peptide Selectivity , 1997, The Journal of experimental medicine.

[12]  M. Colonna,et al.  Tyrosine phosphorylation of a human killer inhibitory receptor recruits protein tyrosine phosphatase 1C , 1996, The Journal of experimental medicine.

[13]  E. Dissen,et al.  Two genes in the rat homologous to human NKG2 , 1998, European journal of immunology.

[14]  Jennifer L. Merolla,et al.  The Politics of Major Policy Reform in Postwar America: Follow the Leader , 2014 .

[15]  T. Takai,et al.  Molecular Cloning of a Novel Murine Cell-surface Glycoprotein Homologous to Killer Cell Inhibitory Receptors* , 1997, The Journal of Biological Chemistry.

[16]  T. Mcclanahan,et al.  Molecular cloning of NKB1. A natural killer cell receptor for HLA-B allotypes. , 1995, Journal of immunology.

[17]  C. Geisler,et al.  Regulation and Function of the CD3γ DxxxLL Motif: A Binding Site for Adaptor Protein-1 and Adaptor Protein-2 in Vitro , 1997, The Journal of cell biology.

[18]  P Parham,et al.  Functionally and structurally distinct NK cell receptor repertoires in the peripheral blood of two human donors. , 1997, Immunity.

[19]  G. Trinchieri,et al.  The role of natural killer cells in host-parasite interactions. , 1995, Current opinion in immunology.

[20]  L. Lanier,et al.  Natural killer cell cytolytic activity is inhibited by NKG2-A and activated by NKG2-C. , 1997, Journal of immunology.

[21]  J. Bonifacino,et al.  Role of potentially charged transmembrane residues in targeting proteins for retention and degradation within the endoplasmic reticulum. , 1991, The EMBO journal.

[22]  P. Parham,et al.  CD94 and a novel associated protein (94AP) form a NK cell receptor involved in the recognition of HLA-A, HLA-B, and HLA-C allotypes. , 1996, Immunity.

[23]  D. Goodlett,et al.  HLA-E surface expression depends on binding of TAP-dependent peptides derived from certain HLA class I signal sequences. , 1998, Journal of immunology.

[24]  C. Geisler,et al.  Role of CD3 gamma in T cell receptor assembly , 1996, The Journal of cell biology.

[25]  L. Lanier,et al.  Follow the Leader: NK Cell Receptors for Classical and Nonclassical MHC Class I , 1998, Cell.

[26]  I. Melero,et al.  Functional ambivalence of the Kp43 (CD94) NK cell-associated surface antigen. , 1995, Journal of immunology.

[27]  D. Marguet,et al.  Human and mouse killer-cell inhibitory receptors recruit PTP1C and PTP1D protein tyrosine phosphatases. , 1996, Journal of immunology.

[28]  M. Llano,et al.  HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[29]  A. Trautmann,et al.  Reconstituted Killer Cell Inhibitory Receptors for Major Histocompatibility Complex Class I Molecules Control Mast Cell Activation Induced via Immunoreceptor Tyrosine-based Activation Motifs* , 1997, The Journal of Biological Chemistry.

[30]  L. Lanier,et al.  Phosphotyrosines in the killer cell inhibitory receptor motif of NKB1 are required for negative signaling and for association with protein tyrosine phosphatase 1C , 1996, The Journal of experimental medicine.

[31]  J. Johnson,et al.  The HLA-E gene encodes two differentially regulated transcripts and a cell surface protein. , 1992, Journal of immunology.

[32]  P. Taillon-Miller,et al.  Cloning and physical mapping of the HLA class I region spanning the HLA-E-to-HLA-F interval by using yeast artificial chromosomes. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[33]  T. Hanke,et al.  Cloning of a mouse homolog of CD94 extends the family of C‐type lectins on murine natural killer cells , 1997, European journal of immunology.

[34]  P Parham,et al.  Human diversity in killer cell inhibitory receptor genes. , 1997, Immunity.

[35]  L. Lanier.  NK cell receptors. , 1998, Annual review of immunology.

[36]  M. Colonna,et al.  Signaling through human killer cell activating receptors triggers tyrosine phosphorylation of an associated protein complex , 1998, European journal of immunology.

[37]  L. Lanier,et al.  Human natural killer cell receptors involved in MHC class I recognition are disulfide-linked heterodimers of CD94 and NKG2 subunits. , 1996, Journal of immunology.

[38]  Eric O Long,et al.  Direct binding of a soluble natural killer cell inhibitory receptor to a soluble human leukocyte antigen-Cw4 class I major histocompatibility complex molecule. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[39]  W. Yokoyama,et al.  Ly-49 multigene family expressed by IL-2-activated NK cells. , 1994, Journal of immunology.

[40]  Eric O Long,et al.  Binding of a soluble p70 killer cell inhibitory receptor to HLA‐B*5101: Requirement for all three p70 immunoglobulin domains , 1997, European journal of immunology.

[41]  M. Colonna,et al.  Cloning of immunoglobulin-superfamily members associated with HLA-C and HLA-B recognition by human natural killer cells. , 1995, Science.

[42]  Jun Wu,et al.  Immunoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells , 1998, Nature.

[43]  Eric O Long,et al.  Molecular clones of the p58 NK cell receptor reveal immunoglobulin-related molecules with diversity in both the extra- and intracellular domains. , 1995, Immunity.

[44]  R. Biassoni,et al.  The human leukocyte antigen (HLA)-C-specific "activatory" or "inhibitory" natural killer cell receptors display highly homologous extracellular domains but differ in their transmembrane and intracytoplasmic portions , 1996, The Journal of experimental medicine.

[45]  Andrew G. Brooks,et al.  NKG2A Complexed with CD94 Defines a Novel Inhibitory Natural Killer Cell Receptor , 1997, The Journal of experimental medicine.

[46]  M. López-Botet,et al.  Clonotypic differences in signaling from CD94 (kp43) on NK cells lead to divergent cellular responses. , 1996, Journal of immunology.

[47]  J. Coligan,et al.  Recognition of Human Histocompatibility Leukocyte Antigen (HLA)-E Complexed with HLA Class I Signal Sequence–derived Peptides by CD94/NKG2 Confers Protection from Natural Killer Cell–mediated Lysis , 1998, The Journal of experimental medicine.

[48]  I. Melero,et al.  Biochemical and serologic evidence for the existence of functionally distinct forms of the CD94 NK cell receptor. , 1996, Journal of immunology.

[49]  Eric Vivier,et al.  Inhibition of antigen‐induced T cell response and antibody‐induced NK cell cytotoxicity by NKG2A: association of NKG2A with SHP‐1 and SHP‐2 protein‐tyrosine phosphatases , 1998, European journal of immunology.

[50]  G. Nolan,et al.  Applications of retrovirus-mediated expression cloning. , 1996, Experimental hematology.

[51]  R. Klausner,et al.  A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal targeting and endocytosis of CD3 chains , 1992, Cell.

[52]  M. Colonna,et al.  Cloning of novel immunoglobulin superfamily receptors expressed on human myeloid and lymphoid cells: Structural evidence for new stimulatory and inhibitory pathways , 1997, European journal of immunology.

[53]  J. Bonifacino,et al.  Colocalized transmembrane determinants for ER degradation and subunit assembly explain the intracellular fate of TCR chains , 1990, Cell.

[54]  P. Parham,et al.  NKB1: a natural killer cell receptor involved in the recognition of polymorphic HLA-B molecules , 1994, The Journal of experimental medicine.

[55]  L. Lanier,et al.  The human natural killer gene complex is located on chromosome 12p12-p13 , 1997, Immunogenetics.

[56]  L. Lanier,et al.  Human NKR-P1A. A disulfide-linked homodimer of the C-type lectin superfamily expressed by a subset of NK and T lymphocytes. , 1994, Journal of immunology.

[57]  W. V. van Blitterswijk,et al.  Serum-free medium for generation and propagation of functional human cytotoxic and helper T cell clones. , 1984, Journal of immunological methods.

[58]  É. Vivier,et al.  Human killer cell activatory receptors for MHC class I molecules are included in a multimeric complex expressed by natural killer cells. , 1997, Journal of immunology.

[59]  F. Bach,et al.  DNA sequence analysis of NKG2, a family of related cDNA clones encoding type II integral membrane proteins on human natural killer cells , 1991, The Journal of experimental medicine.

[60]  L. Lanier,et al.  Molecular characterization of human CD94: A type II membrane glycoprotein related to the C‐type lectin superfamily , 1995, European journal of immunology.

[61]  M. Kubin,et al.  A family of human lymphoid and myeloid Ig-like receptors, some of which bind to MHC class I molecules. , 1997, Journal of immunology.

[62]  R. Biassoni,et al.  The activating form of CD94 receptor complex: CD94 covalently associated with the Kp39 protein that represents the product of the NKG2‐C gene , 1998, European journal of immunology.

[63]  M. Carretero,et al.  The CD94 and NKG2‐A C‐type lectins covalently assemble to form a natural killer cell inhibitory receptor for HLA class I molecules , 1997, European journal of immunology.

[64]  M. Colonna,et al.  Human natural killer cell inhibitory receptors bind to HLA class I molecules , 1996, European journal of immunology.

[65]  G. Trinchieri,et al.  Biology of Natural Killer Cells , 1989, Advances in Immunology.

[66]  M. Cooper,et al.  A novel pair of immunoglobulin-like receptors expressed by B cells and myeloid cells. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[67]  A. McMichael,et al.  The human major histocompatibility complex class Ib molecule HLA‐E binds signal sequence‐derived peptides with primary anchor residues at positions 2 and 9 , 1997, European journal of immunology.