NK cell CD94/NKG2A inhibitory receptors are internalized and recycle independently of inhibitory signaling processes

Journal of Immunology

Volumn 169, Issue 11, 2002, Pages 6102-6111

  Borrego, Francisco ^a   Kabat, Juraj ^a   Sanni, Tolib B ^a   Coligan, John E ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD71 ANTIGEN; CD94 ANTIGEN; HLA E ANTIGEN; INHIBITOR PROTEIN; NKG2A INHIBITORY RECEPTOR; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG; HLA ANTIGEN; HLA ANTIGEN CLASS 1; HLA-E ANTIGEN; IMMUNOGLOBULIN RECEPTOR; KLRD1 PROTEIN, HUMAN; KLRD1 PROTEIN, MOUSE; KLRD1 PROTEIN, RAT; LECTIN; LEUKOCYTE ANTIGEN; LIGAND; MONOCLONAL ANTIBODY; NATURAL KILLER CELL ACTIVATING RECEPTORS; RECOMBINANT PROTEIN;

ANIMAL CELL; ANTIGEN RECOGNITION; ARTICLE; BASOPHIL; BIOCHEMISTRY; CELL COMPARTMENTALIZATION; CELL SURFACE; CONFOCAL MICROSCOPY; CYTOSKELETON; FLOW CYTOMETRY; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSFECTION; HLA SYSTEM; HOMEOSTASIS; HUMAN; HUMAN CELL; INHIBITION KINETICS; INTERNALIZATION; INTRACELLULAR TRANSPORT; LIGAND BINDING; NATURAL KILLER CELL; NONHUMAN; PERIPHERAL CIRCULATION; PRIORITY JOURNAL; PROCESS MODEL; PROTEIN CROSS LINKING; PROTEIN MOTIF; RAT; RECEPTOR BINDING; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION; WILD TYPE; ANIMAL; CELL LINE; CELL MEMBRANE; ENERGY METABOLISM; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE; MUTATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD; ANTIGENS, CD94; CELL COMPARTMENTATION; CELL LINE; CELL MEMBRANE; CYTOSKELETON; ENERGY METABOLISM; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA ANTIGENS; HUMANS; KILLER CELLS, NATURAL; LECTINS, C-TYPE; LIGANDS; MICE; MUTATION; RATS; RECEPTORS, IMMUNOLOGIC; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 0036884904     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.169.11.6102     Document Type: Article

References (43)

1. Soloski, M. J. 2001. Recognition of tumor cells by the innate immune system. Curr. Opin. Immunol. 13:154.
2. Biron, C. A., and L. Brossay. 2001. NK cells and NKT cells in innate defense against viral infections. Curr. Opin. Immunol. 13:458.
3. Lanier, L. L. 1998. NK cell receptors. Annu. Rev. Immunol. 16:359.
4. Borrego, F., J. Kabat, D. K. Kim, L. Lieto, K. Maasho, J. Pena, R. Solana, and J. E. Coligan. 2002. Structure and function of major histocompatibility complex (MHC) class I specific receptors expressed on human natural killer (NK) cells. Mol. Immunol. 38:637.
5. Ljunggren, H. G., and K. Karre. 1990. In search of the "missing self": MHC molecules and NK cell recognition. Immunol. Today 11:237.
6. Lazetic, S., C. Chang, J. P. Houchins, L. L. Lanier, and J. H. Phillips. 1996. Human natural killer cell receptors involved in MHC class I recognition are disulfide-linked heterodimers of CD94 and NKG2 subunits. J. Immunol. 157:4741.
7. Brooks, A. G., P. E. Posch, C. J. Scorzelli, F. Borrego, and J. E. Coligan. 1997. NKG2A complexed with CD94 defines a novel inhibitory natural killer cell receptor. J. Exp. Med. 185:795.
8. Braud, V. M., D. S. Allan, C. A. O'Callaghan, K. Soderstrom, A. D'Andrea, G. S. Ogg, S. Lazetic, N. T. Young, J. I. Bell, J. H. Phillips, et al. 1998. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391:795.
9. Borrego, F., M. Ulbrecht, E. H. Weiss, J. E. Coligan, and A. G. Brooks. 1998. 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. J. Exp. Med. 187:813.
10. Lee, N., M. Llano, M. Carretero, A. Ishitani, F. Navarro, M. Lopez-Botet, and D. E. Geraghty. 1998. HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc. Natl. Acad. Sci. USA 95:5199.
11. Carretero, M., G. Palmieri, M. Llano, V. Tullio, A. Santoni, D. E. Geraghty, and M. Lopez-Botet. 1998. Specific engagement of the CD94/NKG2-A killer inhibitory receptor by the HLA-E class Ib molecule induces SHP-1 phosphatase recruitment to tyrosine-phosphorylated NKG2-A: evidence for receptor function in heterologous transfectants. Eur. J. Immunol. 28:1280.
12. Kabat, J., F. Borrego, A. G. Brooks, and J. E. Coligan. 2002. Role that each NKG2A immunoreceptor tyrosine based inhibitory motif plays in mediating the human CD94/NKG2A inhibitory signal. J. Immunol. 169:1948.
13. Moretta, A., C. Bottino, M. Vitale, D. Pende, C. Cantoni, M. C. Mingari, R. Biassoni, and L. Moretta. 2001. Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu. Rev. Immunol. 19:197.
14. Valiante, N. M., M. Uhrberg, H. G. Shilling, K. Lienert-Weidenbach, K. L. Arnett, A. D'Andrea, J. H. Phillips, L. L. Lanier, and P. Parham. 1997. Functionally and structurally distinct NK cell receptor repertoires in the peripheral blood of two human donors. Immunity 7:739.
15. Moretta, A., C. Bottino, M. C. Mingari, R. Biassoni, and L. Moretta. 2002. What is a natural killer cell? Nat. Immunol. 3:6.
16. Mellman, I. 1996. Endocytosis and molecular sorting. Annu Rev. Cell. Dev. Biol. 12:575.
17. Klausner, R. D., J. Van Renswoude, G. Ashwell, C. Kempf, A. N. Schechter, A. Dean, and K. R. Bridges. 1983. Receptor-mediated endocytosis of transferrin in K562 cells. J. Biol. Chem. 258:4715.
18. Krangel, M. S. 1987. Endocytosis and recycling of the T3-T cell receptor complex: the role of T3 phosphorylation. J. Exp. Med. 165:1141.
19. Liu, H., M. Rhodes, D. L. Wiest, and D. A. A. Vignali. 2000. On the dynamics of TCR:CD3 complex cell surface expression and downmodulation. Immunity 13:665.
20. Dietrich, J., C. Menne, J. P. Lauritsen, M. von Essen, A. B. Rasmussen, N. Odum, and C. Geisler. 2002. Ligand-induced TCR down-regulation is not dependent on constitutive TCR cycling. J. Immunol. 168:5434.
21. Valitutti, S., S. Muller, M. Cella, E. Padovan, and A. Lanzavecchia. 1995. Serial triggering of many T-cell receptors by a few peptide-MHC complexes. Nature 375:148.
22. Cassard, S., J. Salamero, D. Hanau, D. Spehner, J. Davoust, W. H. Fridman, and C. Bonnerot. 1998. A tyrosine-based signal present in Igα mediates B cell receptor constitutive internalization. J. Immunol. 160:1767.
23. Song, W., H. Cho, P. Cheng, and S. K. Pierce. 1995. Entry of B cell antigen receptor and antigen into class II peptide-loading compartment is independent of receptor cross-linking. J. Immunol. 155:4255.
24. Braud, V. M., D. S. Allan, and A. J. McMichael. 1999. Functions of nonclassical MHC and non-MHC-encoded class I molecules. Curr. Opin. Immunol. 11:100.
25. Lanier, L. L., B. Corliss, J. Wu, and J. H. Phillips. 1998. Association of DAP12 with activating CD94/NKG2C NK cell receptors. Immunity 8:693.
26. Houchins, J. P., L. L. Lanier, E. C. Niemi, J. H. Phillips, and J. C. Ryan. 1997. Natural killer cell cytolytic activity is inhibited by NKG2-A and activated by NKG2-C. J. Immunol. 158:3603.
27. Lippincott-Schwartz, J., L. Yuan, C. Tipper, M. Amherdt, L. Orci, and R. D. Klausner. 1991. Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic. Cell 67:601.
28. Wood, S. A., J. E Park, and W. J. Brown. 1991. Brefeldin A causes a microtubule-mediated fusion of the trans-Golgi network and early endosomes. Cell 67:591.
29. Houchins, J. P., T. Yabe, C. McSherry, and F. H. Bach. 1991. DNA sequence analysis of NKG2, a family of related cDNA clones encoding type II integral membrane proteins on human natural killer cells. J. Exp. Med. 173:1017.
30. Braud, V. M., D. S. Allan, D. Wilson, and A. J. McMichael. 1998. TAP- and tapasin-dependent HLA-E surface expression correlates with the binding of an MHC class I leader peptide. Curr. Biol. 8:1.
31. Alcover, A., and B. Alarcon. 2000. Internalization and intracellular fate of TCR-CD3 complexes. Crit. Rev. Immunol. 20:325.
32. Carlin, L. M., K. Eleme, F. E. McCann, and D. M. Davis. 2001. Intercellular transfer and supramolecular organization of human leukocyte antigen C at inhibitory natural killer cell immune synapses. J. Exp. Med. 194:1507.
33. Ayscough, K. R., J. Stryker, N. Pokala, M. Sanders, P. Crews, and D. G. Drubin. 1997. High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin-A. J. Cell Biol. 137:399.
34. Minskoff, S. A., K. Matter, and I. Mellman. 1998. FcγRII-B1 regulates the presentation of B cell receptor-bound antigens. J. Immunol. 161:2079.
35. Turner, N. A., S. G. Ball, and A. J. Balmforth. 2001. The mechanism of angiotensin II-induced extracellular signal-regulated kinase-1/2 activation is independent of angiotensin AT(1A) receptor internalization. Cell. Signal. 13:269.
36. Letourneur, F., and R. D. Klausner. 1992. A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal targeting and endocytosis of CD3 chains. Cell 69:1143.
37. Vales-Gomez, M., H. T. Reyburn, R. A. Erskine, M. Lopez-Botet, and J. L. Strominger. 1999. Kinetics and peptide dependency of the binding of the inhibitory NK receptor CD94/NKG2-A and the activating receptor CD94/ NKG2-C to HLA-E. EMBO J. 18:4250.
38. Huard, B., L. Karlsson, and F. Triebel. 2001. KIR down-regulation on NK cells is associated with down-regulation of activating receptors and NK cell inactivation. Eur. J. Immunol. 31:1728.
39. Palacios, S., V. Lalioti, S. Martinez-Arca, S. Chattopadhyay, and I. V. Sandoval. 2001. Recycling of the insulin-sensitive glucose transporter GLUT4: access of surface internalized GLUT4 molecules to the perinuclear storage compartment is mediated by the Phe5-Gln6-Gln7-Ile8 motif. J. Biol. Chem. 276:3371.
40. Martin, S. 2000. Biogenesis of insulin-responsive GLUT4 vesicles is independent of brefeldin A-sensitive trafficking. Traffic 1:652.
41. Lamaze, C., L. M. Fujimoto, H. L. Yin, and S. L. Schmid. 1997. The actin cytoskeleton is required for receptor-mediated endocytosis in mammalian cells. J. Biol. Chem. 272:20332.
42. McGavin, M. K., K. Badour, L. A. Hardy, T. J. Kubiseski, J. Zhang, and K. A. Siminovitch. 2001. The intersectin 2 adaptor links Wiskott Aldrich Syndrome protein (WASp)-mediated actin polymerization to T cell antigen receptor endocytosis. J. Exp. Med. 194:1777.
43. Brown, B. K., and W. Song. 2001. The actin cytoskeleton is required for the trafficking of the B cell antigen receptor to the late endosomes. Traffic 2:414.