Phosphatidylinositol 3-Kinase Activation Is Required To Form the NKG2D Immunological Synapse

REFERENCES

• Bauer, S., V. Groh, J. Wu, A. Steinle, J. H. Phillips, L. L. Lanier, and T. Spies. 1999. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 285:727–729.
   PubMed Web of Science ®Google Scholar
• Billadeau, D. D., J. L. Upshaw, R. A. Schoon, C. J. Dick, and P. J. Leibson. 2003. NKG2D-DAP10 triggers human NK cell-mediated killing via a Syk-independent regulatory pathway. Nat. Immunol. 4:557–564.
   PubMed Web of Science ®Google Scholar
• Bossi, G., C. Trambas, S. Booth, R. Clark, J. Stinchcombe, and G. M. Griffiths. 2002. The secretory synapse: the secrets of a serial killer. Immunol. Rev. 189:152–160.
   PubMed Web of Science ®Google Scholar
• Bromley, S. K., W. R. Burack, K. G. Johnson, K. Somersalo, T. N. Sims, C. Sumen, M. M. Davis, A. S. Shaw, P. M. Allen, and M. L. Dustin. 2001. The immunological synapse. Annu. Rev. Immunol. 19:375–396.
   PubMed Web of Science ®Google Scholar
• Bryceson, Y. T., M. E. March, H. G. Ljunggren, and E. O. Long. 2006. Activation, coactivation, and costimulation of resting human natural killer cells. Immunol. Rev. 214:73–91.
   PubMed Web of Science ®Google Scholar
• Campbell, R. E., O. Tour, A. E. Palmer, P. A. Steinbach, G. S. Baird, D. A. Zacharias, and R. Y. Tsien. 2002. A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. USA 99:7877–7882.
   PubMed Web of Science ®Google Scholar
• Cella, M., K. Fujikawa, I. Tassi, S. Kim, K. Latinis, S. Nishi, W. Yokoyama, M. Colonna, and W. Swat. 2004. Differential requirements for Vav proteins in DAP10- and ITAM-mediated NK cell cytotoxicity. J. Exp. Med. 200:817–823.
   PubMedGoogle Scholar
• Chang, C., J. Dietrich, A. G. Harpur, J. A. Lindquist, A. Haude, Y. W. Loke, A. King, M. Colonna, J. Trowsdale, and M. J. Wilson. 1999. Cutting edge: KAP10, a novel transmembrane adapter protein genetically linked to DAP12 but with unique signaling properties. J. Immunol. 163:4651–4654.
   PubMed Web of Science ®Google Scholar
• Chardin, P., J. H. Camonis, N. W. Gale, L. van Aelst, J. Schlessinger, M. H. Wigler, and D. Bar-Sagi. 1993. Human Sos1: a guanine nucleotide exchange factor for Ras that binds to GRB2. Science 260:1338–1343.
   PubMed Web of Science ®Google Scholar
• Chen, X., P. P. Trivedi, B. Ge, K. Krzewski, and J. L. Strominger. 2007. Many NK cell receptors activate ERK2 and JNK1 to trigger microtubule organizing center and granule polarization and cytotoxicity. Proc. Natl. Acad. Sci. USA 104:6329–6334.
   PubMed Web of Science ®Google Scholar
• Cosman, D., J. Mullberg, C. L. Sutherland, W. Chin, R. Armitage, W. Fanslow, M. Kubin, and N. J. Chalupny. 2001. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 14:123–133.
   PubMed Web of Science ®Google Scholar
• Das, B., X. Shu, G. J. Day, J. Han, U. M. Krishna, J. R. Falck, and D. Broek. 2000. Control of intramolecular interactions between the pleckstrin homology and Dbl homology domains of Vav and Sos1 regulates Rac binding. J. Biol. Chem. 275:15074–15081.
   PubMedGoogle Scholar
• Davis, D. M. 2002. Assembly of the immunological synapse for T cells and NK cells. Trends Immunol. 23:356–363.
   PubMed Web of Science ®Google Scholar
• Davis, D. M., I. Chiu, M. Fassett, G. B. Cohen, O. Mandelboim, and J. L. Strominger. 1999. The human natural killer cell immune synapse. Proc. Natl. Acad. Sci. USA 96:15062–15067.
   PubMed Web of Science ®Google Scholar
• Davis, D. M., and M. L. Dustin. 2004. What is the importance of the immunological synapse? Trends Immunol. 25:323–327.
   PubMed Web of Science ®Google Scholar
• Diefenbach, A., E. Tomasello, M. Lucas, A. M. Jamieson, J. K. Hsia, E. Vivier, and D. H. Raulet. 2002. Selective associations with signaling proteins determine stimulatory versus costimulatory activity of NKG2D. Nat. Immunol. 3:1142–1149.
   PubMed Web of Science ®Google Scholar
• Doubrovina, E. S., M. M. Doubrovin, E. Vider, R. B. Sisson, R. J. O'Reilly, B. Dupont, and Y. M. Vyas. 2003. Evasion from NK cell immunity by MHC class I chain-related molecules expressing colon adenocarcinoma. J. Immunol. 171:6891–6899.
   PubMed Web of Science ®Google Scholar
• Dustin, M. L., M. W. Olszowy, A. D. Holdorf, J. Li, S. Bromley, N. Desai, P. Widder, F. Rosenberger, P. A. van der Merwe, P. M. Allen, and A. S. Shaw. 1998. A novel adaptor protein orchestrates receptor patterning and cytoskeletal polarity in T-cell contacts. Cell 94:667–677.
   PubMed Web of Science ®Google Scholar
• Endt, J., F. E. McCann, C. R. Almeida, D. Urlaub, R. Leung, D. Pende, D. M. Davis, and C. Watzl. 2007. Inhibitory receptor signals suppress ligation-induced recruitment of NKG2D to GM1-rich membrane domains at the human NK cell immune synapse. J. Immunol. 178:5606–5611.
   PubMed Web of Science ®Google Scholar
• Falasca, M., S. K. Logan, V. P. Lehto, G. Baccante, M. A. Lemmon, and J. Schlessinger. 1998. Activation of phospholipase C gamma by PI 3-kinase-induced PH domain-mediated membrane targeting. EMBO J. 17:414–422.
   PubMed Web of Science ®Google Scholar
• Garrity, D., M. E. Call, J. Feng, and K. W. Wucherpfennig. 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.
   PubMed Web of Science ®Google Scholar
• Gasser, S., S. Orsulic, E. J. Brown, and D. H. Raulet. 2005. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 436:1186–1190.
   PubMed Web of Science ®Google Scholar
• Gilfillan, S., E. L. Ho, M. Cella, W. M. Yokoyama, and M. Colonna. 2002. NKG2D recruits two distinct adapters to trigger NK cell activation and costimulation. Nat. Immunol. 3:1150–1155.
   PubMed Web of Science ®Google Scholar
• Graham, D. B., M. Cella, E. Giurisato, K. Fujikawa, A. V. Miletic, T. Kloeppel, K. Brim, T. Takai, A. S. Shaw, M. Colonna, and W. Swat. 2006. Vav1 controls DAP10-mediated natural cytotoxicity by regulating actin and microtubule dynamics. J. Immunol. 177:2349–2355.
   PubMed Web of Science ®Google Scholar
• Grakoui, A., S. K. Bromley, C. Sumen, M. M. Davis, A. S. Shaw, P. M. Allen, and M. L. Dustin. 1999. The immunological synapse: a molecular machine controlling T cell activation. Science 285:221–227.
   PubMed Web of Science ®Google Scholar
• Han, J., K. Luby-Phelps, B. Das, X. Shu, Y. Xia, R. D. Mosteller, U. M. Krishna, J. R. Falck, M. A. White, and D. Broek. 1998. Role of substrates and products of PI 3-kinase in regulating activation of Rac-related guanosine triphosphatases by Vav. Science 279:558–560.
   PubMedGoogle Scholar
• Harada, Y., D. Ohgai, R. Watanabe, K. Okano, O. Koiwai, K. Tanabe, H. Toma, A. Altman, and R. Abe. 2003. A single amino acid alteration in cytoplasmic domain determines IL-2 promoter activation by ligation of CD28 but not inducible costimulator (ICOS). J. Exp. Med. 197:257–262.
   PubMed Web of Science ®Google Scholar
• Hemmings, B. A. 1997. PH domains—a universal membrane adapter. Science 275:1899.
   PubMedGoogle Scholar
• Huang, F., and A. Sorkin. 2005. Growth factor receptor binding protein 2-mediated recruitment of the RING domain of Cbl to the epidermal growth factor receptor is essential and sufficient to support receptor endocytosis. Mol. Biol. Cell 16:1268–1281.
   PubMedGoogle Scholar
• Isakoff, S. J., T. Cardozo, J. Andreev, Z. Li, K. M. Ferguson, R. Abagyan, M. A. Lemmon, A. Aronheim, and E. Y. Skolnik. 1998. Identification and analysis of PH domain-containing targets of phosphatidylinositol 3-kinase using a novel in vivo assay in yeast. EMBO J. 17:5374–5387.
   PubMed Web of Science ®Google Scholar
• Kaifu, T., J. Nakahara, M. Inui, K. Mishima, T. Momiyama, M. Kaji, A. Sugahara, H. Koito, A. Ujike-Asai, A. Nakamura, K. Kanazawa, K. Tan-Takeuchi, K. Iwasaki, W. M. Yokoyama, A. Kudo, M. Fujiwara, H. Asou, and T. Takai. 2003. Osteopetrosis and thalamic hypomyelinosis with synaptic degeneration in DAP12-deficient mice. J. Clin. Investig. 111:323–332.
   PubMed Web of Science ®Google Scholar
• Khurana, D., L. N. Arneson, R. A. Schoon, C. J. Dick, and P. J. Leibson. 2007. Differential regulation of human NK cell-mediated cytotoxicity by the tyrosine kinase itk. J. Immunol. 178:3575–3582.
   PubMed Web of Science ®Google Scholar
• Kim, H. H., M. Tharayil, and C. E. Rudd. 1998. Growth factor receptor-bound protein 2 SH2/SH3 domain binding to CD28 and its role in co-signaling. J. Biol. Chem. 273:296–301.
   PubMedGoogle Scholar
• Lanier, L. L. 2003. Natural killer cell receptor signaling. Curr. Opin. Immunol. 15:308–314.
   PubMed Web of Science ®Google Scholar
• Lanier, L. L., B. C. Corliss, J. Wu, C. Leong, and J. H. Phillips. 1998. Immunoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells. Nature 391:703–707.
   PubMed Web of Science ®Google Scholar
• Long, E. O. 2002. Tumor cell recognition by natural killer cells. Semin. Cancer Biol. 12:57–61.
   PubMedGoogle Scholar
• Markiewicz, M. A., L. N. Carayannopoulos, O. V. Naidenko, K. Matsui, W. R. Burack, E. L. Wise, D. H. Fremont, P. M. Allen, W. M. Yokoyama, M. Colonna, and A. S. Shaw. 2005. Costimulation through NKG2D enhances murine CD8+ CTL function: similarities and differences between NKG2D and CD28 costimulation. J. Immunol. 175:2825–2833.
   PubMed Web of Science ®Google Scholar
• Masilamani, M., C. Nguyen, J. Kabat, F. Borrego, and J. E. Coligan. 2006. CD94/NKG2A inhibits NK cell activation by disrupting the actin network at the immunological synapse. J. Immunol. 177:3590–3596.
   PubMed Web of Science ®Google Scholar
• Meresse, B., Z. Chen, C. Ciszewski, M. Tretiakova, G. Bhagat, T. N. Krausz, D. H. Raulet, L. L. Lanier, V. Groh, T. Spies, E. C. Ebert, P. H. Green, and B. Jabri. 2004. Coordinated induction by IL15 of a TCR-independent NKG2D signaling pathway converts CTL into lymphokine-activated killer cells in celiac disease. Immunity 21:357–366.
   PubMed Web of Science ®Google Scholar
• Micucci, F., A. Zingoni, M. Piccoli, L. Frati, A. Santoni, and R. Galandrini. 2006. High-efficient lentiviral vector-mediated gene transfer into primary human NK cells. Exp. Hematol. 34:1344–1352.
   PubMed Web of Science ®Google Scholar
• 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. 19:197–223.
   PubMed Web of Science ®Google Scholar
• Nedvetzki, S., S. Sowinski, R. A. Eagle, J. Harris, F. Vely, D. Pende, J. Trowsdale, E. Vivier, S. Gordon, and D. M. Davis. 2007. Reciprocal regulation of natural killer cells and macrophages associated with distinct immune synapses. Blood 109:3776–3785.
   PubMed Web of Science ®Google Scholar
• Nimnual, A., and D. Bar-Sagi. 2002. The two hats of SOS. Sci. STKE 2002:PE36.
   PubMedGoogle Scholar
• Nishida, M., K. Nagata, Y. Hachimori, M. Horiuchi, K. Ogura, V. Mandiyan, J. Schlessinger, and F. Inagaki. 2001. Novel recognition mode between Vav and Grb2 SH3 domains. EMBO J. 20:2995–3007.
   PubMed Web of Science ®Google Scholar
• Nosaka, T., T. Kawashima, K. Misawa, K. Ikuta, A. L. Mui, and T. Kitamura. 1999. STAT5 as a molecular regulator of proliferation, differentiation and apoptosis in hematopoietic cells. EMBO J. 18:4754–4765.
   PubMed Web of Science ®Google Scholar
• Ogura, K., K. Nagata, M. Horiuchi, E. Ebisui, T. Hasuda, S. Yuzawa, M. Nishida, H. Hatanaka, and F. Inagaki. 2002. Solution structure of N-terminal SH3 domain of Vav and the recognition site for Grb2 C-terminal SH3 domain. J. Biomol. NMR 22:37–46.
   PubMedGoogle Scholar
• Orange, J. S., K. E. Harris, M. M. Andzelm, M. M. Valter, R. S. Geha, and J. L. Strominger. 2003. The mature activating natural killer cell immunologic synapse is formed in distinct stages. Proc. Natl. Acad. Sci. USA 100:14151–14156.
   PubMed Web of Science ®Google Scholar
• Pende, D., P. Rivera, S. Marcenaro, C. C. Chang, R. Biassoni, R. Conte, M. Kubin, D. Cosman, S. Ferrone, L. Moretta, and A. Moretta. 2002. Major histocompatibility complex class I-related chain A and UL16-binding protein expression on tumor cell lines of different histotypes: analysis of tumor susceptibility to NKG2D-dependent natural killer cell cytotoxicity. Cancer Res. 62:6178–6186.
   PubMed Web of Science ®Google Scholar
• Prasad, K. V., Y. C. Cai, M. Raab, B. Duckworth, L. Cantley, S. E. Shoelson, and C. E. Rudd. 1994. T-cell antigen CD28 interacts with the lipid kinase phosphatidylinositol 3-kinase by a cytoplasmic Tyr(P)-Met-Xaa-Met motif. Proc. Natl. Acad. Sci. USA 91:2834–2838.
   PubMed Web of Science ®Google Scholar
• Raulet, D. H. 2003. Roles of the NKG2D immunoreceptor and its ligands. Nat. Rev. Immunol. 3:781–790.
   PubMed Web of Science ®Google Scholar
• Richie, L. I., P. J. Ebert, L. C. Wu, M. F. Krummel, J. J. Owen, and M. M. Davis. 2002. Imaging synapse formation during thymocyte selection: inability of CD3zeta to form a stable central accumulation during negative selection. Immunity 16:595–606.
   PubMed Web of Science ®Google Scholar
• Roda-Navarro, P., M. Vales-Gomez, S. E. Chisholm, and H. T. Reyburn. 2006. Transfer of NKG2D and MICB at the cytotoxic NK cell immune synapse correlates with a reduction in NK cell cytotoxic function. Proc. Natl. Acad. Sci. USA 103:11258–11263.
   PubMed Web of Science ®Google Scholar
• Somersalo, K., N. Anikeeva, T. N. Sims, V. K. Thomas, R. K. Strong, T. Spies, T. Lebedeva, Y. Sykulev, and M. L. Dustin. 2004. Cytotoxic T lymphocytes form an antigen-independent ring junction. J. Clin. Investig. 113:49–57.
   PubMedGoogle Scholar
• Songyang, Z., S. E. Shoelson, M. Chaudhuri, G. Gish, T. Pawson, W. G. Haser, F. King, T. Roberts, S. Ratnofsky, R. J. Lechleider, et al. 1993. SH2 domains recognize specific phosphopeptide sequences. Cell 72:767–778.
   PubMed Web of Science ®Google Scholar
• Sutherland, C. L., N. J. Chalupny, K. Schooley, T. VandenBos, M. Kubin, and D. Cosman. 2002. UL16-binding proteins, novel MHC class I-related proteins, bind to NKG2D and activate multiple signaling pathways in primary NK cells. J. Immunol. 168:671–679.
   PubMed Web of Science ®Google Scholar
• Taylor, L. S., S. P. Paul, and D. W. McVicar. 2000. Paired inhibitory and activating receptor signals. Rev. Immunogenet. 2:204–219.
   PubMedGoogle Scholar
• Tomasello, E., and E. Vivier. 2005. KARAP/DAP12/TYROBP: three names and a multiplicity of biological functions. Eur. J. Immunol. 35:1670–1677.
   PubMed Web of Science ®Google Scholar
• Treanor, B., P. M. Lanigan, S. Kumar, C. Dunsby, I. Munro, E. Auksorius, F. J. Culley, M. A. Purbhoo, D. Phillips, M. A. Neil, D. N. Burshtyn, P. M. French, and D. M. Davis. 2006. Microclusters of inhibitory killer immunoglobulin-like receptor signaling at natural killer cell immunological synapses. J. Cell Biol. 174:153–161.
   PubMedGoogle Scholar
• Upshaw, J. L., L. N. Arneson, R. A. Schoon, C. J. Dick, D. D. Billadeau, and P. J. Leibson. 2006. NKG2D-mediated signaling requires a DAP10-bound Grb2-Vav1 intermediate and phosphatidylinositol-3-kinase in human natural killer cells. Nat. Immunol. 7:524–532.
   PubMedGoogle Scholar
• Vyas, Y. M., H. Maniar, and B. Dupont. 2002. Visualization of signaling pathways and cortical cytoskeleton in cytolytic and noncytolytic natural killer cell immune synapses. Immunol. Rev. 189:161–178.
   PubMed Web of Science ®Google Scholar
• Wu, J., H. Cherwinski, T. Spies, J. H. Phillips, and L. L. Lanier. 2000. DAP10 and DAP12 form distinct, but functionally cooperative, receptor complexes in natural killer cells. J. Exp. Med. 192:1059–1068.
   PubMedGoogle Scholar
• Wu, J., Y. Song, A. B. Bakker, S. Bauer, T. Spies, L. L. Lanier, and J. H. Phillips. 1999. An activating immunoreceptor complex formed by NKG2D and DAP10. Science 285:730–732.
   PubMed Web of Science ®Google Scholar
• Wulfing, C., B. Purtic, J. Klem, and J. D. Schatzle. 2003. Stepwise cytoskeletal polarization as a series of checkpoints in innate but not adaptive cytolytic killing. Proc. Natl. Acad. Sci. USA 100:7767–7772.
   PubMed Web of Science ®Google Scholar
• Yokoyama, W. M., and B. F. Plougastel. 2003. Immune functions encoded by the natural killer gene complex. Nat. Rev. Immunol. 3:304–316.
   PubMed Web of Science ®Google Scholar
• Zompi, S., J. A. Hamerman, K. Ogasawara, E. Schweighoffer, V. L. Tybulewicz, J. P. Di Santo, L. L. Lanier, and F. Colucci. 2003. NKG2D triggers cytotoxicity in mouse NK cells lacking DAP12 or Syk family kinases. Nat. Immunol. 4:565–572.
   PubMed Web of Science ®Google Scholar