CD226 protein is involved in immune synapse formation and triggers natural killer (NK) cell activation via its first extracellular domain

Journal of Biological Chemistry

Volumn 289, Issue 10, 2014, Pages 6969-6977

  Hou, Shengke ^a   Ge, Kuikui ^a   Zheng, Xiaodong ^a   Wei, Haiming ^a,b   Sun, Rui ^a,b   Tian, Zhigang ^a,b  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CHEMICAL ACTIVATION; PROTEINS;

EXTRACELLULAR DOMAINS; IMMUNE SYNAPSE; NATURAL KILLER CELLS; NK CELLS; TARGET CELLS;

CYTOLOGY;

2E6 ANTIBODY; 3B9 ANTIBODY; CD155 ANTIGEN; CD226 ANTIGEN; CD69 ANTIGEN; GRANZYME B; INTERLEUKIN 2; LYMPHOCYTE ANTIGEN; LYMPHOCYTE RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; MONOCLONAL ANTIBODY; MUTANT PROTEIN; NECTIN 2; UNCLASSIFIED DRUG;

ANTIGEN BINDING; ARTICLE; CELL ADHESION; CELL STRAIN K 562; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOTOXICITY; DELETION MUTANT; ENZYME PHOSPHORYLATION; FLOW CYTOMETRY; GENETIC RECOMBINATION; HELA CELL; IMMUNOLOGICAL SYNAPSE; LYMPHOCYTE ACTIVATION; MOLECULAR RECOGNITION; NATURAL KILLER CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; SURFACE PLASMON RESONANCE;

CELL BIOLOGY; CELL JUNCTIONS; ERK; NATURAL KILLER (NK) CELL; PHOSPHORYLATION;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD55; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; CHO CELLS; CRICETULUS; CYTOTOXICITY, IMMUNOLOGIC; HELA CELLS; HUMANS; IMMUNOLOGICAL SYNAPSES; K562 CELLS; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SURFACE PLASMON RESONANCE;

EID: 84896790446     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.498253     Document Type: Article

References (39)

1. Scharton-Kersten, T. M., and Sher, A. (1997) Role of natural killer cells in innate resistance to protozoan infections. Curr. Opin. Immunol. 9, 44-51
2. Talmadge, J. E., Meyers, K. M., Prieur, D. J., and Starkey, J. R. (1980) Role of natural killer cells in tumor growth and metastasis: C57BL/6 normal and beige mice. J. Natl. Cancer Inst. 65, 929-935
3. Trinchieri, G. (1989) Biology of natural killer cells. Adv. Immunol. 47, 187-376
4. Cerwenka, A., and Lanier, L. L. (2001) Ligands for natural killer cell receptors: redundancy or specificity. Immunol. Rev. 181, 158-169
5. Diefenbach, A., and Raulet, D. H. (2001) Strategies for target cell recognition by natural killer cells. Immunol. Rev. 181, 170-184
6. Barber, D. F., and Long, E. O. (2003) Coexpression of CD58 or CD48 with intercellular adhesion molecule 1 on target cells enhances adhesion of resting NK cells. J. Immunol. 170, 294-299
7. McVicar, D. W., and Burshtyn, D. N. (2001) Intracellular signaling by the killer immunoglobulin-like receptors and Ly49. Sci. STKE 2001, re1
8. Carlsten, M., Björkström, N. K., Norell, H., Bryceson, Y., van Hall, T., Baumann, B. C., Hanson, M., Schedvins, K., Kiessling, R., Ljunggren, H. G., and Malmberg, K. J. (2007) DNAX accessory molecule-1 mediated recognition of freshly isolated ovarian carcinoma by resting natural killer cells. Cancer Res. 67, 1317-1325
9. Castriconi, R., Dondero, A., Corrias, M. V., Lanino, E., Pende, D., Moretta, L., Bottino, C., and Moretta, A. (2004) Natural killer cell-mediated killing of freshly isolated neuroblastoma cells: critical role of DNAX accessory molecule-1-poliovirus receptor interaction. Cancer Res. 64, 9180-9184
10. El-Sherbiny, Y. M., Meade, J. L., Holmes, T. D., McGonagle, D., Mackie, S. L., Morgan, A. W., Cook, G., Feyler, S., Richards, S. J., Davies, F. E., Morgan, G. J., and Cook, G. P. (2007) The requirement for DNAM-1, NKG2D, and NKp46 in the natural killer cell-mediated killing of myeloma cells. Cancer Res. 67, 8444-8449
11. Moretta, L., Bottino, C., Pende, D., Castriconi, R., Mingari, M. C., and Moretta, A. (2006) Surface NK receptors and their ligands on tumor cells. Semin. Immunol. 18, 151-158
12. Pende, D., Bottino, C., Castriconi, R., Cantoni, C., Marcenaro, S., Rivera, P., Spaggiari, G. M., Dondero, A., Carnemolla, B., Reymond, N., Mingari, M. C., Lopez, M., Moretta, L., and Moretta, A. (2005) PVR (CD155) and Nectin-2 (CD112) as ligands of the human DNAM-1 (CD226) activating receptor: involvement in tumor cell lysis. Mol. Immunol. 42, 463-469
13. Pende, D., Spaggiari, G. M., Marcenaro, S., Martini, S., Rivera, P., Capobianco, A., Falco, M., Lanino, E., Pierri, I., Zambello, R., Bacigalupo, A., Mingari, M. C., Moretta, A., and Moretta, L. (2005) Analysis of the receptor-ligand interactions in the natural killer-mediated lysis of freshly isolated myeloid or lymphoblastic leukemias: evidence for the involvement of the Poliovirus receptor (CD155) and Nectin-2 (CD112). Blood 105, 2066-2073
14. Elishmereni, M., Bachelet, I., and Levi-Schaffer, F. (2008) DNAM-1: an amplifier of immune responses as a therapeutic target in various disorders. Curr. Opin. Investig. Drugs 9, 491-496
15. Kojima, H., Kanada, H., Shimizu, S., Kasama, E., Shibuya, K., Nakauchi, H., Nagasawa, T., and Shibuya, A. (2003) CD226 mediates platelet and megakaryocytic cell adhesion to vascular endothelial cells. J. Biol. Chem. 278, 36748-36753
16. Castriconi, R., Dondero, A., Cantoni, C., Della Chiesa, M., Prato, C., Nanni, M., Fiorini, M., Notarangelo, L., Parolini, S., Moretta, L., Notarangelo, L., Moretta, A., and Bottino, C. (2007) Functional characterization of natural killer cells in type I leukocyte adhesion deficiency. Blood 109, 4873-4881
17. Shibuya, K., Shirakawa, J., Kameyama, T., Honda, S., Tahara-Hanaoka, S., Miyamoto, A., Onodera, M., Sumida, T., Nakauchi, H., Miyoshi, H., and Shibuya, A. (2003) CD226 (DNAM-1) is involved in lymphocyte functionassociated antigen 1 costimulatory signal for naive T cell differentiation and proliferation. J. Exp. Med. 198, 1829-1839
18. Bottino, C., Castriconi, R., Pende, D., Rivera, P., Nanni, M., Carnemolla, B., Cantoni, C., Grassi, J., Marcenaro, S., Reymond, N., Vitale, M., Moretta, L., Lopez, M., and Moretta, A. (2003) Identification of PVR (CD155) and Nectin-2 (CD112) as cell surface ligands for the human DNAM-1 (CD226) activating molecule. J. Exp. Med. 198, 557-567
19. Aricescu, A. R., and Jones, E. Y. (2007) Immunoglobulin superfamily cell adhesion molecules: zippers and signals. Curr. Opin. Cell Biol. 19, 543-550
20. Peggs, K. S., and Allison, J. P. (2005) Co-stimulatory pathways in lymphocyte regulation: the immunoglobulin superfamily. Br. J. Haematol. 130, 809-824
21. Zhang, P., Mueller, S., Morais, M. C., Bator, C. M., Bowman, V. D., Hafenstein, S., Wimmer, E., and Rossmann, M. G. (2008) Crystal structure of CD155 and electron microscopic studies of its complexes with polioviruses. Proc. Natl. Acad. Sci. U.S.A. 105, 18284-18289
22. Xu, Z., and Jin, B. (2010) A novel interface consisting of homologous immunoglobulin superfamily members with multiple functions. Cell. Mol. Immunol. 7, 11-19
23. Liu, J., Qian, X., Chen, Z., Xu, X., Gao, F., Zhang, S., Zhang, R., Qi, J., Gao, G. F., and Yan, J. (2012) Crystal structure of cell adhesion molecule nectin-2/CD112 and its binding to immune receptor DNAM-1/CD226. J. Immunol. 188, 5511-5520
24. Friberg, D. D., Bryant, J. L., and Whiteside, T. L. (1996) Measurements of natural killer (NK) activity and NK-cell quantification. Methods 9, 316-326
25. Ziegler, S. F., Ramsdell, F., and Alderson, M. R. (1994) The activation antigen CD69. Stem Cells 12, 456-465
26. Krzewski, K., and Coligan, J. E. (2012) Human NK cell lytic granules and regulation of their exocytosis. Front. Immunol. 3, 335
27. Pala, P., Hussell, T., and Openshaw, P. J. (2000) Flow cytometric measurement of intracellular cytokines. J. Immunol. Methods 243, 107-124
28. Djeu, J. Y., Jiang, K., and Wei, S. (2002) A view to a kill: signals triggering cytotoxicity. Clin. Cancer Res. 8, 636-640
29. Lanier, L. L. (2005)NKcell recognition. Annu. Rev. Immunol. 23, 225-274
30. Bachelet, I., Munitz, A., Mankutad, D., and Levi-Schaffer, F. (2006) Mast cell costimulation by CD226/CD112 (DNAM-1/Nectin-2): a novel interface in the allergic process. J. Biol. Chem. 281, 27190-27196
31. Chen, L., Xie, X., Zhang, X., Jia, W., Jian, J., Song, C., and Jin, B. (2003) The expression, regulation and adhesion function of a novel CD molecule, CD226, on human endothelial cells. Life Sci. 73, 2373-2382
32. Ma, D., Sun, Y., Lin, D., Wang, H., Dai, B., Zhang, X., Ouyang, W., Jian, J., Jia, W., Xu, X., and Jin, B. (2005) CD226 is expressed on the megakaryocytic lineage from hematopoietic stem cells/progenitor cells and involved in its polyploidization. Eur. J. Haematol. 74, 228-240
33. Ye, X., Zhang, Z., Jiang, Y., Han, X., Wang, Y., Zhang, M., Liu, J., Geng, W., Dai, D., Shi, W., and Shang, H. (2006) Expression of human CD226 on T cells and natural killer cells and of soluble CD226 in plasma of HIV-1-infected Chinese patients. Viral Immunol. 19, 576-581
34. Shibuya, A., Campbell, D., Hannum, C., Yssel, H., Franz-Bacon, K., Mc-Clanahan, T., Kitamura, T., Nicholl, J., Sutherland, G. R., Lanier, L. L., and Phillips, J. H. (1996) DNAM-1, a novel adhesion molecule involved in the cytolytic function of T lymphocytes. Immunity 4, 573-581
35. Meyer, D., Seth, S., Albrecht, J., Maier, M. K., du Pasquier, L., Ravens, I., Dreyer, L., Burger, R., Gramatzki, M., Schwinzer, R., Kremmer, E., Foerster, R., and Bernhardt, G. (2009) CD96 interaction with CD155 via its first Ig-like domain is modulated by alternative splicing or mutations in distal Ig-like domains. J. Biol. Chem. 284, 2235-2244
36. Seth, S., Georgoudaki, A. M., Chambers, B. J., Qiu, Q., Kremmer, E., Maier, M. K., Czeloth, N., Ravens, I., Foerster, R., and Bernhardt, G. (2009) Heterogeneous expression of the adhesion receptor CD226 on murine NK and T cells and its function in NK-mediated killing of immature dendritic cells. J. Leukoc. Biol. 86, 91-101
37. Stanietsky, N., Simic, H., Arapovic, J., Toporik, A., Levy, O., Novik, A., Levine, Z., Beiman, M., Dassa, L., Achdout, H., Stern-Ginossar, N., Tsukerman, P., Jonjic, S., and Mandelboim, O. (2009) The interaction of TIGIT with PVR and PVRL2 inhibits human NK cell cytotoxicity. Proc. Natl. Acad. Sci. U.S.A. 106, 17858-17863
38. Stengel, K. F., Harden-Bowles, K., Yu, X., Rouge, L., Yin, J., Comps-Agrar, L., Wiesmann, C., Bazan, J. F., Eaton, D. L., and Grogan, J. L. (2012) Structure of TIGIT immunoreceptor bound to poliovirus receptor reveals a cell-cell adhesion and signaling mechanism that requires cis-trans receptor clustering. Proc. Natl. Acad. Sci. U.S.A. 109, 5399-5404
39. Burns, G. F., Triglia, T., Werkmeister, J. A., Begley, C. G., and Boyd, A. W. (1985) TLiSA, a human T lineage-specific activation antigen involved in the differentiation of cytotoxic T lymphocytes and anomalous killer cells from their precursors. J. Exp. Med. 161, 1063-1078