Ubiquitin-dependent endocytosis of NKG2D-DAP10 receptor complexes activates signaling and functions in human NK cells

Science Signaling

Volumn 8, Issue 400, 2015, Pages

  Quatrini, Linda ^a,c   Molfetta, Rosa ^a   Zitti, Beatrice ^a   Peruzzi, Giovanna ^b   Fionda, Cinzia ^a   Capuano, Cristina ^b   Galandrini, Ricciarda ^b   Cippitelli, Marco ^a   Santoni, Angela ^a,b   Paolini, Rossella ^a,b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; DNAX ACTIVATING PROTEIN 10; GAMMA INTERFERON; MITOGEN ACTIVATED PROTEIN KINASE; NATURAL KILLER CELL RECEPTOR NKG2D; UBIQUITIN; UNCLASSIFIED DRUG; HCST PROTEIN, HUMAN; IMMUNOGLOBULIN RECEPTOR; KLRK1 PROTEIN, HUMAN; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY K;

ARTICLE; BIOCHEMICAL ANALYSIS; CELL ACTIVATION; CELL FUNCTION; CELL LINE; CELL MEMBRANE; CELLULAR SECRETION; COMPLEX FORMATION; CONTROLLED STUDY; CYTOTOXIC LYMPHOCYTE; ENDOCYTOSIS; HUMAN; HUMAN CELL; INTERNALIZATION; MICROSCOPY; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION; UBIQUITINATION; CYTOLOGY; GENETICS; IMMUNOLOGY;

CELL LINE; ENDOCYTOSIS; HUMANS; KILLER CELLS, NATURAL; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; PROTEOLYSIS; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION; UBIQUITIN;

EID: 84945551002     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.aab2724     Document Type: Article

References (60)

1. S. González, V. Groh, T. Spies, Immunobiology of human NKG2D and its ligands. Curr. Top. Microbiol. Immunol. 298, 121-138 (2006).
2. E. Ullrich, J. Koch, A. Cerwenka, A. Steinle, New prospects on the NKG2D/NKG2DL system for oncology. Oncoimmunology 2, e26097 (2013).
3. D. H. Raulet, S. Gasser, B. G. Gowen, W. Deng, H. Jung, Regulation of ligands for the NKG2D activating receptor. Annu. Rev. Immunol. 31, 413-441 (2013).
4. M. Champsaur, L. L. Lanier, Effect of NKG2D ligand expression on host immune responses. Immunol. Rev. 235, 267-285 (2010).
5. M. J. Smyth, J. Swann, E. Cretney, N. Zerafa, W. M. Yokoyama, Y. Hayakawa, NKG2D function protects the host from tumor initiation. J. Exp. Med. 202, 583-588 (2005).
6. N. Guerra, Y. X. Tan, N. T. Joncker, A. Choy, F. Gallardo, N. Xiong, S. Knoblaugh, D. Cado, N. M. Greenberg, N. R. Greenberg, D. H. Raulet, NKG2D-deficient mice are defective in tumor surveillance in models of spontaneous malignancy. Immunity 28, 571-580 (2008).
7. D. Garrity, M. E. Call, J. Feng, K. W. Wucherpfennig, The activating NKG2D receptor assembles in the membrane with two signaling dimers into a hexameric structure. Proc. Natl. Acad. Sci. U.S.A. 102, 7641-7646 (2005).
8. S. Bauer, V. Groh, J. Wu, A. Steinle, J. H. Phillips, L. L. Lanier, T. Spies, Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 285, 727-729 (1999).
9. D. D. Billadeau, J. L. Upshaw, R. A. Schoon, C. J. Dick, P. J. Leibson, NKG2D-DAP10 triggers human NK cell-mediated killing via a Syk-independent regulatory pathway. Nat. Immunol. 4, 557-564 (2003).
10. J. L. Upshaw, L. N. Arneson, R. A. Schoon, C. J. Dick, D. D. Billadeau, P. J. Leibson, NKG2D-mediated signaling requires a DAP10-bound Grb2-Vav1 intermediate and phosphatidylinositol-3-kinase in human natural killer cells. Nat. Immunol. 7, 524-532 (2006).
11. J. Wu, Y. Song, A. B. H. Bakker, S. Bauer, T. Spies, L. L. Lanier, J. H. Phillips, An activating immunoreceptor complex formed by NKG2D and DAP10. Science 285, 730-732 (1999).
12. C. Chang, J. Dietrich, A. G. Harpur, J. A. Lindquist, A. Haude, Y.W. Loke, A. King, M. Colonna, J. Trowsdale, M. J. Wilson, Cutting edge: KAP10, a novel transmembrane adapter protein genetically linked to DAP12 but with unique signaling properties. J. Immunol. 163, 4651-4654 (1999).
13. L. L. Lanier, NK cell recognition. Annu. Rev. Immunol. 23, 225-274 (2005).
14. E. O. Long, H. S. Kim, D. Liu, M. E. Peterson, S. Rajagopalan, Controlling natural killer cell responses: Integration of signals for activation and inhibition. Annu. Rev. Immunol. 31, 227-258 (2013).
15. A. M. Jamieson, A. Diefenbach, C. W. McMahon, N. Xiong, J. R. Carlyle, D. H. Raulet, The role of the NKG2D immunoreceptor in immune cell activation and natural killing. Immunity 17, 19-29 (2002).
16. E. Vivier, E. Tomasello, M. Baratin, T. Walzer, S. Ugolini, Functions of natural killer cells. Nat. Immunol. 9, 503-510 (2008).
17. V. Groh, J. Wu, C. Yee, T. Spies, Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 419, 734-738 (2002).
18. E. S. Doubrovina, M. M. Doubrovin, E. Vider, R. B. Sisson, R. J. OReilly, B. Dupont, Y. M. Vyas, Evasion from NK cell immunity by MHC class I chain-related molecules expressing colon adenocarcinoma. J. Immunol. 171, 6891-6899 (2003).
19. H. Song, J. Kim, D. Cosman, I. Choi, Soluble ULBP suppresses natural killer cell activity via down-regulating NKG2D expression. Cell. Immunol. 239, 22-30 (2006).
20. I. Waldhauer, A. Steinle, Proteolytic release of soluble UL16-binding protein 2 from tumor cells. Cancer Res. 66, 2520-2526 (2006).
21. O. Ashiru, P. Boutet, L. Fernández-Messina, S. Agöera-González, J. N. Skepper, M. Valés-Gómez, H. T. Reyburn, Natural killer cell cytotoxicity is suppressed by exposure to the human NKG2D ligand MICA 008 that is shed by tumor cells in exosomes. Cancer Res. 70, 481-489 (2010).
22. C. Cenciarelli, D. Hou, K. C. Hsu, B. L. Rellahan, D. L. Wiest, H. T. Smith, V. A. Fried, A. M. Weissman, Activation-induced ubiquitination of the T cell antigen receptor. Science 257, 795-797 (1992).
23. R. Paolini, A. Serra, R. Molfetta, M. Piccoli, L. Frati, A. Santoni, Tyrosine kinasedependent ubiquitination of CD16 z subunit in human NK cells following receptor engagement. Eur. J. Immunol. 29, 3179-3187 (1999).
24. G. M. Di Guglielmo, C. Le Roy, A. F. Goodfellow, J. L. Wrana, Distinct endocytic pathways regulate TGF-b receptor signalling and turnover. Nat. Cell Biol. 5, 410-421 (2003).
25. R. Molfetta, F. Gasparrini, G. Peruzzi, L. Vian, M. Piccoli, L. Frati, A. Santoni, R. Paolini, Lipid raft-dependent FceRI ubiquitination regulates receptor endocytosis through the action of ubiquitin binding adaptors. PLOS One 4, e5604 (2009).
26. R. Molfetta, L. Quatrini, C. Capuano, F. Gasparrini, B. Zitti, A. Zingoni, R. Galandrini, A. Santoni, R. Paolini, c-Cbl regulates MICA-but not ULBP2-induced NKG2D downmodulation in human NK cells. Eur. J. Immunol. 44, 2761-2770 (2014).
27. S. Polo, P. P. Di Fiore, Endocytosis conducts the cell signaling orchestra. Cell 124, 897-900 (2006).
28. A. Sorkin, M. von Zastrow, Endocytosis and signalling: Intertwining molecular networks. Nat. Rev. Mol. Cell Biol. 10, 609-622 (2009).
29. A. V. Vieira, C. Lamaze, S. L. Schmid, Control of EGF receptor signaling by clathrinmediated endocytosis. Science 274, 2086-2089 (1996).
30. K. A. DeFea, J. Zalevsky, M. S. Thoma, O. Déry, R. D. Mullins, N.W. Bunnett, b-Arrestin-dependent endocytosis of proteinase-Activated receptor 2 is required for intracellular targeting of activated ERK1/2. J. Cell Biol. 148, 1267-1281 (2000).
31. C. L. Howe, J. S. Valletta, A. S. Rusnak, W. C. Mobley, NGF signaling from clathrincoated vesicles: Evidence that signaling endosomes serve as a platform for the Ras-MAPK pathway. Neuron 32, 801-814 (2001).
32. L.M. Luttrell, F. L. Roudabush, E.W. Choy, W. E. Miller, M. E. Field, K. L. Pierce, R. J. Lefkowitz, Activation and targeting of extracellular signal-regulated kinases by b-Arrestin scaffolds. Proc. Natl. Acad. Sci. U.S.A. 98, 2449-2454 (2001).
33. D. Teis, W. Wunderlich, L. A. Huber, Localization of the MP1-MAPK scaffold complex to endosomes is mediated by p14 and required for signal transduction. Dev. Cell 3, 803-814 (2002).
34. E. Galperin, A. Sorkin, Endosomal targeting of MEK2 requires RAF, MEK kinase activity and clathrin-dependent endocytosis. Traffic 9, 1776-1790 (2008).
35. A. Chaturvedi, R. Martz, D. Dorward, M. Waisberg, S. K. Pierce, Endocytosed BCRs sequentially regulate MAPK and Akt signaling pathways from intracellular compartments. Nat. Immunol. 12, 1119-1126 (2011).
36. N. Parameswaran, G. Enyindah-Asonye, N. Bagheri, N. B. Shah, N. Gupta, Spatial coupling of JNK activation to the B cell antigen receptor by tyrosine-phosphorylated ezrin. J. Immunol. 190, 2017-2026 (2013).
37. I. A. Yudushkin, R. D. Vale, Imaging T-cell receptor activation reveals accumulation of tyrosine-phosphorylated CD3z in the endosomal compartment. Proc. Natl. Acad. Sci. U.S.A. 107, 22128-22133 (2010).
38. D. D. Billadeau, T cell activation at the immunological synapse: Vesicles emerge for LATer signaling. Sci. Signal. 3, pe16 (2010).
39. T. Willinger, M. Staron, S. M. Ferguson, P. De Camilli, R. A. Flavell, Dynamin 2-dependent endocytosis sustains T-cell receptor signaling and drives metabolic reprogramming in T lymphocytes. Proc. Natl. Acad. Sci. U.S.A. 112, 4423-4428 (2015).
40. R. Paolini, R. Molfetta, M. Piccoli, L. Frati, A. Santoni, Ubiquitination and degradation of Syk and ZAP-70 protein tyrosine kinases in human NK cells upon CD16 engagement. Proc. Natl. Acad. Sci. U.S.A. 98, 9611-9616 (2001).
41. Y. T. Bryceson, M. E. March, H.-G. Ljunggren, E. O. Long, Synergy among receptors on resting NK cells for the activation of natural cytotoxicity and cytokine secretion. Blood 107, 159-166 (2006).
42. M. Milella, A. Gismondi, P. Roncaioli, L. Bisogno, G. Palmieri, L. Frati, M. G. Cifone, A. Santoni, CD16 cross-linking induces both secretory and extracellular signal-regulated kinase (ERK)-dependent cytosolic phospholipase A2 (PLA2) activity in human natural killer cells: Involvement of ERK, but not PLA2, in CD16-Triggered granule exocytosis. J. Immunol. 158, 3148-3154 (1997).
43. S. Wei, A. M. Gamero, J. H. Liu, A. A. Daulton, N. I. Valkov, J. A. Trapani, A. C. Larner, M. J. Weber, J. Y. Djeu, Control of lytic function by mitogen-Activated protein kinase/extracellular regulatory kinase 2 (ERK2) in a human natural killer cell line: Identification of perforin and granzyme B mobilization by functional ERK2. J. Exp. Med. 187, 1753-1765 (1998).
44. F. Mainiero, A. Gismondi, A. Soriani, M. Cippitelli, G. Palmieri, J. Jacobelli, M. Piccoli, L. Frati, A. Santoni, Integrin-mediated Ras-extracellular regulated kinase (ERK) signaling regulates interferon g production in human natural killer cells. J. Exp. Med. 188, 1267-1275 (1998).
45. R. Trotta, K. A. Puorro, M. Paroli, L. Azzoni, B. Abebe, L. C. Eisenlohr, B. Perussia, Dependence of both spontaneous and antibody-dependent, granule exocytosis-mediated NK cell cytotoxicity on extracellular signal-regulated kinases. J. Immunol. 161, 6648-6656 (1998).
46. X. Chen, D. S. Allan, K. Krzewski, B. Ge, H. Kopcow, J. L. Strominger, CD28-stimulated ERK2 phosphorylation is required for polarization of the microtubule organizing center and granules in YTS NK cells. Proc. Natl. Acad. Sci. U.S.A. 103, 10346-10351 (2006).
47. E. Macia, M. Ehrlich, R. Massol, E. Boucrot, C. Brunner, T. Kirchhausen, Dynasore, a cell-permeable inhibitor of dynamin. Dev. Cell 10, 839-850 (2006).
48. P. Roda-Navarro, H. T. Reyburn, The traffic of the NKG2D/Dap10 receptor complex during natural killer (NK) cell activation. J. Biol. Chem. 284, 16463-16472 (2009).
49. K. Ogasawara, J. A. Hamerman, H. Hsin, S. Chikuma, H. Bour-Jordan, T. Chen, T. Pertel, C. Carnaud, J. A. Bluestone, L. L. Lanier, Impairment of NK cell function by NKG2D modulation in NOD mice. Immunity 18, 41-51 (2003).
50. T. Horng, J. S. Bezbradica, R. Medzhitov, NKG2D signaling is coupled to the interleukin 15 receptor signaling pathway. Nat. Immunol. 8, 1345-1352 (2007).
51. J. C. Kagan, T. Su, T. Horng, A. Chow, S. Akira, R.Medzhitov, TRAMcouples endocytosis of Toll-like receptor 4 to the induction of interferon-b. Nat. Immunol. 9, 361-368 (2008).
52. S. Rajagopalan, Y. T. Bryceson, S. P. Kuppusamy, D. E. Geraghty, A. van der Meer, I. Joosten, E. O. Long, Activation of NK cells by an endocytosed receptor for soluble HLA-G. PLOS Biol. 4, e9 (2006).
53. S. M. S.Miah, A. K. Purdy, N. B. Rodin, A.W.MacFarlane IV, J. Oshinsky, D. A. Alvarez-Arias, K. S. Campbell, Ubiquitylation of an internalized killer cell Ig-like receptor by Triad3A disrupts sustained NF-kB signaling. J. Immunol. 186, 2959-2969 (2011).
54. L. Ge, Y. Ly, M. Hollenberg, K. DeFea, A b-Arrestin-dependent scaffold is associated with prolonged MAPK activation in pseudopodia during protease-Activated receptor-2-induced chemotaxis. J. Biol. Chem. 278, 34418-34426 (2003).
55. K. Honda, Y. Ohba, H. Yanai, H. Negishi, T. Mizutani, A. Takaoka, C. Taya, T. Taniguchi, Spatiotemporal regulation of MyD88-IRF-7 signalling for robust type-I interferon induction. Nature 434, 1035-1040 (2005).
56. S. Hisata, T. Sakisaka, T. Baba, T. Yamada, K. Aoki, M. Matsuda, Y. Takai, Rap1-PDZGEF1 interacts with a neurotrophin receptor at late endosomes, leading to sustained activation of Rap1 and ERK and neurite outgrowth. J. Cell Biol. 178, 843-860 (2007).
57. J. Huynh, M. Q. Kwa, A. D. Cook, J. A. Hamilton, G. M. Scholz, CSF-1 receptor signalling from endosomes mediates the sustained activation of Erk1/2 and Akt in macrophages. Cell. Signal. 24, 1753-1761 (2012).
58. C. Fionda, M. P. Abruzzese, A. Zingoni, A. Soriani, B. Ricci, R. Molfetta, R. Paolini, A. Santoni, M. Cippitelli, Nitric oxide donors increase PVR/CD155 DNAM-1 ligand expression in multiple myeloma cells: Role of DNA damage response activation. BMC Cancer 15, 17 (2015).
59. F. Gasparrini, R. Molfetta, L. Quatrini, L. Frati, A. Santoni, R. Paolini, Syk-dependent regulation of Hrs phosphorylation and ubiquitination upon FceRI engagement: Impact on Hrs membrane/cytosol localization. Eur. J. Immunol. 42, 2744-2753 (2012).
60. C. Capuano, R. Paolini, R. Molfetta, L. Frati, A. Santoni, R. Galandrini, PIP2-dependent regulation of Munc13-4 endocytic recycling: Impact on the cytolytic secretory pathway. Blood 119, 2252-2262 (2012).