DAP12 impacts trafficking and surface stability of killer immunoglobulin-like receptors on natural killer cells

Journal of Leukocyte Biology

Volumn 94, Issue 2, 2013, Pages 301-313

  Mulrooney, Tiernan J ^a   Posch, Phillip E ^a   Hurley, Carolyn Katovich ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Innate immunity; Receptor internalization; Receptor maturation

Indexed keywords

ISOPROTEIN; KILLER CELL ACTIVATING RECEPTOR ASSOCIATED PROTEIN; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; SMALL INTERFERING RNA;

ARTICLE; CELL SURFACE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FLOW CYTOMETRY; GENE REPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; INTERNALIZATION; LYSOSOME; MOLECULAR RECOGNITION; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SIGNAL TRANSDUCTION;

INNATE IMMUNITY; RECEPTOR INTERNALIZATION; RECEPTOR MATURATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL LINE; CELL MEMBRANE; ENDOPLASMIC RETICULUM; HEK293 CELLS; HUMANS; JURKAT CELLS; KILLER CELLS, NATURAL; LYSOSOMES; MEMBRANE PROTEINS; MUTAGENESIS, SITE-DIRECTED; PROTEIN INTERACTION MAPPING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STABILITY; PROTEIN TRANSPORT; RECEPTORS, KIR; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSFECTION;

EID: 84880999675     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.0213093     Document Type: Article

References (44)

1. Winter, C. C., Gumperz, J. E., Parham, P., Long, E. O., Wagtmann, N. (1998) Direct binding and functional transfer of NK cell inhibitory receptors reveal novel patterns of HLA-C allotype recognition. J. Immunol. 161, 571-577.
2. Litwin, V., Gumperz, J., Parham, P., Phillips, J. H., Lanier, L. L. (1994) NKB1: a natural killer cell receptor involved in the recognition of polymorphic HLA-B molecules. J. Exp. Med. 180, 537-543.
3. Burshtyn, D. N., Scharenberg, A. M., Wagtmann, N., Rajagopalan, S., Berrada, K., Yi, T., Kinet, J. P., Long, E. O. (1996) Recruitment of ty-rosine phosphatase HCP by the killer cell inhibitor receptor. Immunity 4, 77-85.
4. Olcese, L., Lang, P., Vély, F., Cambiaggi, A., Marguet, D., Blery, M., Hip-pen, K. L., Biassoni, R., Moretta, A., Moretta, L., Cambier, J. C., Vivier, E. (1996) Human and mouse killer-cell inhibitory receptors recruit PTP1C and PTP1D protein tyrosine phosphatases. J. Immunol. 156, 4531-4534.
5. Anfossi, N., Guia, S., Falk, C. S., Roetnyck, S., Stewart, C.A., Breso, V., Frassati, C., Reviron, D., Middleton, D., Romagne, F., Ugolini, S., Vivier, E. (2006) Human NK cell education by inhibitory receptors for MHC class I. Immunity 25, 331-342.
6. Ljunggren, H. G., Kärre, K. (1990) In search of the 'missing self': MHC molecules and NK cell recognition. Immunol. Today 11, 237-244.
7. Biassoni, R., Pessino, A., Malaspina, A., Cantoni, C., Bottino, C., Sivori, S., Moretta, L., Moretta, A. (1997) Role of amino acid position 70 in the binding affinity of p50.1 and p58.1 receptors for HLA-Cw4 molecules. Eur. J. Immunol. 27, 3095-3099.
8. Chewning, J. H., Gudme, C. N., Hsu, K. C., Selvakumar, A., Dupont, B. (2007) KIR2DS1-positive NK cells mediate alloresponse against the C2 HLA-KIR ligand group in vitro. J. Immunol. 179, 854-868.
9. Stewart, C. A., Laugier-Anfossi, F., Vély, F., Saulquin, X., Riedmuller, J., Tisserant, A., Gauthier, L., Romagne, F., Ferraci, G., Arosa, F. A, Moretta, A, Sun, P. D., Ugolini, S., Vivier, E. (2005) Recognition of peptide-MHC class I complexes by activating killer immunoglobulin-like receptors. Proc. Natl. Acad. Sci. USA 102, 13224-13229.
10. Graef, T., Moesta, A. K, Norman, P. J., Abi-Rached, L., Vago, L., Older Aguilar, A. M., Gleimer, M., Hammond, J. A, Guethlein, L. A, Bush-nell, D. A, Robinson, P. J., Parham, P. (2009) KIR2DS4 is a product of gene conversion with KIR3DL2 that introduced specificity for HLA-A*11 while diminishing avidity for HLA-C. J. Exp. Med. 206, 2557-2572.
11. Katz, G., Markel, G., Mizrahi, S., Arnon, T. I., Mandelboim, O. (2001) Recognition of HLA-Cw4 but not HLA-Cw6 by the NK cell receptor killer cell Ig-like receptor two-domain short tail number 4. J. Immunol 166, 7260-7267.
12. Katz, G., Gazit, R, Arnon, T. I., Gonen-Gross, T., Tarcic, G., Markel, G., Gruda, R, Achdout, H., Drize, O., Merim, S., Mandelboim, O. (2004) MHC class I-independent recognition of NK-activating receptor KIR2DS4. J. Immunol. 173, 1819-1825.
13. Lanier, L. L., Corliss, B. C, Wu, J., Leong, C, Phillips, J. H. (1998) Im-munoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells. Nature 391, 703-707.
14. Snyder, M. R, Lucas, M., Vivier, E., Weyand, C. M., Goronzy, J. J. (2003) Selective activation of the c-Jun NH2-terminal protein kinase signaling pathway by stimulatory KIR in the absence of KARAP/DAP12 in CD4 + T cells. J. Exp. Med. 197, 437-449.
15. Snyder, M. R, Nakajima, T., Leibson, P. J., Weyand, C. M., Goronzy, J. J. (2004) Stimulatory killer Ig-like receptors modulate T cell activation through DAP12-dependent and DAP12-independent mechanisms. J. Immunol. 173, 3725-3731.
16. Burgess, S. J., Marusina, A. I., Pathmanathan, I., Borrego, F., Coligan, J. E. (2006) IL-21 down-regulates NKG2D/DAP10 expression on human NK and CD8+ T cells. J. Immunol. 176, 1490-1497.
17. Park, Y. P., Choi, S. C, Kiesler, P., Gil-Krzewska, A, Borrego, F., Weck, J., Krzeski, K, Coligan, J. E. (2011) Complex regulation of human NKG2D-DAP10 cell surface expression: opposing roles of the 7c cytokines and TGF-/31. Blood 118, 3019-3027.
18. De Rham, C, Ferrari-Lacraz, S., Jendly, S., Schneiter, G., Dayer, J. M., Villard, J. (2007) The proinflammatory cytokines IL-2, IL-15 and IL-21 modulate the repertoire of mature human natural killer cell receptors. Arthritis Res. Ther. 9, R125.
19. Carr, W. H., Rosen, D. B., Arase, H., Nixon, D. F., Michaelsson, J., Lanier, L. L. (2007) Cutting edge: KIR3DS1, a gene implicated in resistance to progression to AIDS, encodes a DAP12-associated receptor expressed on NK cells that triggers NK cell activation. J. Immunol. 178, 647-651.
20. Hou, L., Chen, M., Jiang, B., Kariyawasam, K, Ng, J., Hurley, C. K (2009) In contrast to other stimulatory natural killer cell immunoglobulin-like receptor loci, several KIR2DS5 alleles predominate in African Americans. Hum. Immunol. 70, 733-737.
21. Steiner, N. K, Dakshanamurthy, S., VandenBussche, C. J., Hurley, C. K (2008) Extracellular domain alterations impact surface expression of stimulatory natural killer cell receptor KIR2DS5. Immunogenetics 60, 655-667.
22. VandenBussche, C. J., Mulrooney, T. J., Frazier, W. R, Dakshanamurthy, S., Hurley, C. K. (2009) Dramatically reduced surface expression of NK cell receptor KIR2DS3 is attributed to multiple residues throughout the molecule. Genes Immun. 10, 162-173.
23. Hou, P., Araujo, E., Zhao, T., Zhang, M., Massenburg, D., Veselits, M., Doyle, C, Dinner, A. R, Clark, M. R. (2006) B cell antigen receptor signaling and internalization are mutually exclusive events. PLoS Biol. 4, e200.
24. Feng, J., Call, M. E., Wucherpfenning, K. W. (2006) The assembly of diverse immune receptors is focused on a polar membrane-embedded interaction site. PLoS Biol. 4, e142.
25. Rajagopalan, S., Bryceson, Y. T., Kuppusamy, S. P., Geraghty, D. E., van der Meer, A., Joosten, I., Long, E. O. (2006) Activation of NK cells by an endocytosed receptor for soluble HLA-G. PLoS Biol. 4, e9.
26. Rajagopalan, S., Moyle, M. W., Joosten, I., Long, E. O. (2010) DNA-PKcs controls an endosomal signaling pathway for a proinflammoatory response by natural killer cells. Sci. Signal. 3, ra14.
27. Fauriat, C, Ivarsson, M. A, Ljunggren, H. G., Malmberg, K. J., Michaëlsson, J. (2010) Education of human natural killer cells by activating killer cell immunoglobulin-like receptors. Blood 115, 1166-1174.
28. Hiby, S. E., Apps, R, Sharkey, A, Farrel, L., Gardner, L., Mulder, A, Claas, F. H., Walker, J., Redman, C, Morgan, L., Tower, C, Regan, L., Moore, G., Carrington, M., Moffet, A. (2010) Maternal activating KIRs protect against human reproductive failure mediated by fetal HLA-C2. J. Clin. Invest. 120, 4102-4110.
29. Sivori, S., Carlomagno, S., Falco, M., Romeo, E., Moretta, L., Moretta, A. (2011) Natural killer cells expressing the KIR2DS1-activating receptor efficiently kill T-cell blasts and dendritic cells: implications in haploiden-tical HSCT. Blood 117, 4284-4292.
30. Venstrom, J. M., Pittari, G., Gooley, T. A, Chewning, J. H., Spellman, S., Haagenson, M., Gallagher, M. M., Malkki, M., Petersdorf, E., Dupont, B., Hsu, K. C. (2012) HLA-C-dependent prevention of leukemia relapse by donor activating KIR2DS1. N. Engl. J. Med. 367, 805-816.
31. Orr, M. T., Sun, J. C., Hesslein, D. G., Arase, H., Phillips, J. H., Takari, T., Lanier, L. L. (2009) Ly49H signaling through DAP10 is essential for optimal natural killer cell responses to mouse cytomegalovirus infection. J. Exp. Med. 206, 807-817.
32. Sivori, S., Parolini, S., Falco, M., Biassoni, R., Bottino, C., Morreta, L., Morreta, A. (2000) 2B4 functions as a co-receptor in human NK cell activation. Eur. J. Immunol. 30, 787-793.
33. Garrity, D., Call, M. E., Feng, J., Wucherpfenning, K. W. (2005) The activating NKG2D receptor assembles in the membrane with two signaling dimers into a hexameric structure. Proc. Natl. Acad. Sci. USA 102, 7641-7646.
34. Irvine, D. J., Purboo, M. A., Krogsgaard, M., Davis, M. M. (2002) Direct observation of ligand recognition by T cells. Nature 419, 845-849.
35. Sykulev, Y., Joo, M., Vturina, I., Tsomides, T. J., Eisen, H. N. (1996) Evidence that a single peptide-MHC complex on a target cell can elicit a cytolytic T cell response. Immunity 4, 565-571.
36. Fan, Q. R., Long, E. O., Wiley, D. C. (2000) A disulfide-linked natural killer cell receptor dimer has higher affinity for HLA-C than wild-type monomer. Eur. J. Immunol. 30, 2692-2697.
37. Fan, Q. R., Long, E. O., Wiley, D. C. (2000) Cobalt-mediated dimeriza-tion of the human natural killer cell inhibitory receptor. J. Biol. Chem. 275, 23700-23706.
38. Alarcon, B., Berkhout, B., Breitmeyer, J., Terhorst, C. (1988) Assembly of the human T cell receptor-CD3 complex takes place in the endoplas-mic reticulum and involves intermediary complexes between the CD3- y.S.e core and single T cell receptor a /3 chains. J. Biol. Chem. 263, 2953-2961.
39. Dong, C, Filipeanu, C. M., Duvernay, M. T., Wu, G. (2007) Regulation of G protein-coupled receptor export trafficking. Biochim. Biophys. Acta 1768, 853-870.
40. Dietrich, J., Bäckström, T., Lauritsen, J. P., Kastrup, J., Christensen, M. D., von Bulow, F., Palmer, E., Geisler, C. (1998) The phosphorylation state of CD37 influences T cell responsiveness and controls T cell receptor cycling. J. Biol. Chem. 273, 24232-24238.
41. Von Essen, M., Nielsen, M. W., Bonefeld, C. M., Boding, L., Larsen, J. M., Leitges, M., Baier, G., Odum, N., Geisler, C. (2006) Protein kinase C (PKC) a and PKC 0 are the major PKC isotypes involved in TCR down-regulation. J. Immunol. 176, 7502-7510.
42. Alvarez-Arias, D. A., Campbell, K. S. (2007) Protein kinase C regulates expression and function of inhibitory killer cell Ig-like receptors in NK cells. J. Immunol. 179, 5281-5290.
43. Valitutti, S., Muller, S., Salio, M., Lanzavecchia, A. (1997) Degradation of T cell receptor (TCR)-CD3-£ complexes after antigenic stimulation. J. Exp. Med. 185, 1859-1864.
44. Paloneva, J., Kestilä, M., Wu, J., Salminen, A., Böhling, T., Ruotsalainen, V., Hakola, P., Bakker, A. B., Phillips, J. H., Pekkarinen, P., Lanier, L. L., Timonen, T., Peltonen, L. (2000) Loss-of-function mutations in TYROBP (DAP12) result in a presenile dementia with bone cysts. Nat. Genet. 25, 357-361.