Intercellular protein transfer at the NK cell immune synapse: Mechanisms and physiological significance

FASEB Journal

Volumn 21, Issue 8, 2007, Pages 1636-1646

  Roda Navarro, Pedro ^a,b,c   Reyburn, Hugh T ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b Max Planck Institute of Molecular Physiology ^*  (United Kingdom)

^c MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

Author keywords

Membrane connective structure nanotube

Indexed keywords

PROTEIN;

CELL COMMUNICATION; CYTOTOXICITY; HUMAN; IMMUNE SYSTEM; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SUPRAMOLECULAR CHEMISTRY; SYNAPSE;

ANIMALS; CELL COMMUNICATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNOLOGIC SURVEILLANCE; KILLER CELLS, NATURAL; PROTEINS; RECEPTORS, IMMUNOLOGIC; TUMOR ESCAPE;

EID: 34249787886     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-7488rev     Document Type: Review

References (92)

1. Monks, C. R., Freiberg, B. A., Kupfer, H., Sciaky, N., and Kupfer, A. (1998) Three-dimensional segregation of supramolecular activation clusters in T cells. Nature 395, 82-86
2. Batista, F. D., Iber, D., and Neuberger, M. S. (2001) B cells acquire antigen from target cells after synapse formation. Nature 411, 489-494
3. Carrasco, Y. R., Fleire, S. J., Cameron, T., Dustin, M. L., and Batista, F. D. (2004) LFA-1/ICAM-1 interaction lowers the threshold of B cell activation by facilitating B cell adhesion and synapse formation. Immunity 20, 589-599
4. Stinchcombe, J. C., Bossi, G., Booth, S., and Griffiths, G. M. (2001) The immunological synapse of CTL contains a secretory domain and membrane bridges. Immunity 15, 751-761
5. Barcia, C., Thomas, C. E., Curtin, J. F., King, G. D., Wawrowsky, K., Candolfi, M., Xiong, W. D., Liu, C., Kroeger, K., Boyer, O., et al. (2006) In vivo mature immunological synapses forming SMACs mediate clearance of virally infected astrocytes from the brain. J. Exp. Med. 203, 2095-2107
6. Moretta, L., and Moretta, A. (2004) Unravelling natural killer cell function: triggering and inhibitory human NK receptors. EMBO J. 23, 255-259
7. Biassoni, R., Cantoni, C., Pende, D., Sivori, S., Parolini, S., Vitale, M., Bottino, C., and Moretta, A. (2001) Human natural killer cell receptors and co-receptors. Immunol. Rev. 181, 203-214
8. Arnon, T. I., Achdout, H., Lieberman, N., Gazit, R., Gonen-Gross, T., Katz, G., Bar-Ilan, A., Bloushtain, N., Lev, M., Joseph, A., et al. (2004) The mechanisms controlling the recognition of tumor- and virus-infected cells by NKp46. Blood 103, 664-672
9. Upshaw, J. L., Arneson, L. N., Schoon, R. A., Dick, C. J., Billadeau, D. D., and Leibson, P. J. (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
10. Gonzalez, S., Groh, V., and Spies, T. (2006) Immunobiology of human NKG2D and its ligands. Curr. Top. Microbiol. Immunol. 298, 121-138
11. Brown, M. H., Boles, K., van der Merwe, P. A., Kumar, V., Mathew, P. A., and Barclay, A. N. (1998) 2B4, the natural killer and T cell immunoglobulin superfamily surface protein, is a ligand for CD48. J. Exp. Med. 188, 2083-2090
12. Tangye, S. G., Lazetic, S., Woollatt, E., Sutherland, G. R., Lanier, L. L., and Phillips, J. H. (1999) Cutting edge: human 2B4, an activating NK cell receptor, recruits the protein tyrosine phosphatase SHP-2 and the adaptor signaling protein SAP. J. Immunol. 162, 6981-6985
13. Nakajima, H., and Colonna, M. (2000) 2B4: an NK cell activating receptor with unique specificity and signal transduction mechanism. Hum. Immunol. 61, 39-43
14. Carretero, M., Cantoni, C., Bellon, T., Bottino, C., Biassoni, R., Rodriguez, A., Perez-Villar, J. J., Moretta, L., Moretta, A., and Lopez-Botet, M. (1997) The CD94 and NKG2-A C-type lectins covalently assemble to form a natural killer cell inhibitory receptor for HLA class I molecules. Eur. J. Immunol. 27, 563-567
15. Lopez-Botet, M., Angulo, A., and Guma, M. (2004) Natural killer cell receptors for major histocompatibility complex class I and related molecules in cytomegalovirus infection. Tissue Antigens 63, 195-203
16. Long, E. O., Barber, D. F., Burshtyn, D. N., Faure, M., Peterson, M., Rajagopalan, S., Renard, V., Sandusky, M., Stebbins, C. C., Wagtmann, N., and Watzl, C. (2001) Inhibition of natural killer cell activation signals by killer cell immunoglobulin-like receptors (CD158). Immunol. Rev. 181, 223-233
17. Eriksson, M., Leitz, G., Fallman, E., Axner, O., Ryan, J. C., Nakamura, M. C., and Sentman, C. L. (1999) Inhibitory receptors alter natural killer cell interactions with target cells yet allow simultaneous killing of susceptible targets. J. Exp. Med. 190, 1005-1012
18. Vyas, Y. M., Mehta, K. M., Morgan, M., Maniar, H., Butros, L., Jung, S., Burkhardt, J. K., and Dupont, B. (2001) Spatial organization of signal transduction molecules in the NK cell immune synapses during MHC class I-regulated noncytolytic and cytolytic interactions. J. Immunol. 167, 4358-4367
19. Roda-Navarro, P., Vales-Gomez, M., Chisholm, S. E., and Reyburn, H. T. (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. U. S. A. 103, 11258-11263
20. Sancho, D., Nieto, M., Llano, M., Rodriguez-Fernandez, J. L., Tejedor, R., Avraham, S., Cabanas, C., Lopez-Botet, M., and Sanchez-Madrid, F. (2000) The tyrosine kinase PYK-2/RAFTK regulates natural killer (NK) cell cytotoxic response, and is translocated and activated upon specific target cell recognition and killing. J. Cell Biol. 149, 1249-1262
21. Kopcow, H. D., Allan, D. S., Chen, X., Rybalov, B., Andzelm, M. M., Ge, B., and Strominger, J. L. (2005) Human decidual NK cells form immature activating synapses and are not cytotoxic. Proc. Natl. Acad. Sci. U. S. A. 102, 15563-15568
22. Vyas, Y. M., Maniar, H., and Dupont, B. (2002) Visualization of signaling pathways and cortical cytoskeleton in cytolytic and noncytolytic natural killer cell immune synapses. Immunol. Rev. 189, 161-178
23. Vyas, Y. M., Maniar, H., and Dupont, B. (2002) Cutting edge: differential segregation of the SRC homology 2-containing protein tyrosine phosphatase-1 within the early NK cell immune synapse distinguishes noncytolytic from cytolytic interactions. J. Immunol. 168, 3150-3154
24. Binstadt, B. A., Brumbaugh, K. M., Dick, C. J., Scharenberg, A. M., Williams, B. L., Colonna, M., Lanier, L. L., Kinet, J. P., Abraham, R. T., and Leibson, P. J. (1996) Sequential involvement of Lck and SHP-1 with MHC-recognizing receptors on NK cells inhibits FcR-initiated tyrosine kinase activation. Immunity 5, 629-638
25. Davis, D. M., Chiu, I., Fassett, M., Cohen, G. B., Mandelboim, O., and Strominger, J. L. (1999) The human natural killer cell immune synapse. Proc. Natl. Acad. Sci. U. S. A. 96, 15062-15067
26. Treanor, B., Lanigan, P. M., Kumar, S., Dunsby, C., Munro, I., Auksorius, E., Culley, F. J., Purbhoo, M. A., Phillips, D., Neil, M. A., et al. (2006) Microclusters of inhibitory killer immunoglobulin-like receptor signaling at natural killer cell immunological synapses. J. Cell Biol. 174, 153-161
27. Fassett, M. S., Davis, D. M., Valter, M. M., Cohen, G. B., and Strominger, J. L. (2001) Signaling at the inhibitory natural killer cell immune synapse regulates lipid raft polarization but not class I MHC clustering. Proc. Natl. Acad. Sci. U. S. A. 98, 14547-14552
28. Sanni, T. B., Masilamani, M., Kabat, J., Coligan, J. E., and Borrego, F. (2004) Exclusion of lipid rafts and decreased mobility of CD94/NKG2A receptors at the inhibitory NK cell synapse. Mol. Biol. Cell 15, 3210-3223
29. Roda-Navarro, P., Mittelbrunn, M., Ortega, M., Howie, D., Terhorst, C., Sanchez-Madrid, F., and Fernandez-Ruiz, E. (2004) Dynamic redistribution of the activating 2B4/SAP complex at the cytotoxic NK cell immune synapse. J. Immunol. 173, 3640-3646
30. Orange, J. S., Harris, K. E., Andzelm, M. M., Valter, M. M., Geha, R. S., and Strominger, J. L. (2003) The mature activating natural killer cell immunologic synapse is formed in distinct stages. Proc. Natl. Acad. Sci. U. S. A. 100, 14151-14156
31. Ferlazzo, G., Tsang, M. L., Moretta, L., Melioli, G., Steinman, R. M., and Munz, C. (2002) Human dendritic cells activate resting natural killer (NK) cells and are recognized via the NKp30 receptor by activated NK cells. J. Exp. Med. 195, 343-351
32. Moretta, A. (2002) Natural killer cells and dendritic cells: rendezvous in abused tissues. Nat. Rev. Immunol. 2, 957-964
33. Moretta, A. (2005) The dialogue between human natural killer cells and dendritic cells. Curr. Opin. Immunol. 17, 306-311
34. O'Keefe, J. P., Blaine, K., Alegre, M. L., and Gajewski, T. F. (2004) Formation of a central supramolecular activation cluster is not required for activation of naive CD8+ T cells. Proc. Natl. Acad. Sci. U. S. A. 101, 9351-9356
35. Joly, E., and Hudrisier, D. (2003) What is trogocytosis and what is its purpose? Nat. Immunol. 4, 815
36. Hudrisier, D., and Bongrand, P. (2002) Intercellular transfer of antigen-presenting cell determinants onto T cells: molecular mechanisms and biological significance. FASEB J. 16, 477-486
37. Hudrisier, D., Riond, J., Mazarguil, H., Gairin, J. E., and Joly, E. (2001) Cutting edge: CTLs rapidly capture membrane fragments from target cells in a TCR signaling-dependent manner. J. Immunol. 166, 3645-3649
38. Huang, J. F., Yang, Y., Sepulveda, H., Shi, W., Hwang, I., Peterson, P. A., Jackson, M. R., Sprent, J., and Cai, Z. (1999) TCR-Mediated internalization of peptide-MHC complexes acquired by T cells. Science 286, 952-954
39. Mostbock, S., Catalfamo, M., Tagaya, Y., Schlom, J., and Sabzevari, H. (2006) Acquisition of antigen presentasomes (APS), an MHC/costimulatory complex, is a check-point of memory T cell homeostasis. Blood, E-pub ahead of print
40. Hudrisier, D., Riond, J., Garidou, L., Duthoit, C., and Joly, E. (2005) T cell activation correlates with an increased proportion of antigen among the materials acquired from target cells. Eur. J. Immunol. 35, 2284-2294
41. Carlin, L. M., Eleme, K., McCann, F. E., and Davis, D. M. (2001) Intercellular transfer and supramolecular organization of human leukocyte antigen C at inhibitory natural killer cell immune synapses. J. Exp. Med. 194, 1507-1517
42. Vanherberghen, B., Andersson, K., Carlin, L. M., Nolte-'t Hoen, E. N., Williams, G. S., Hoglund, P., and Davis, D. M. (2004) Human and murine inhibitory natural killer cell receptors transfer from natural killer cells to target cells. Proc. Natl. Acad. Sci. U. S. A. 101, 16873-16878
43. Sjostrom, A., Eriksson, M., Cerboni, C., Johansson, M. H., Sentman, C. L., Karre, K., and Hoglund, P. (2001) Acquisition of external major histocompatibility complex class I molecules by natural killer cells expressing inhibitory Ly49 receptors. J. Exp. Med. 194, 1519-1530
44. Zimmer, J., Ioannidis, V., and Held, W. (2001) H-2D ligand expression by Ly49A+ natural killer (NK) cells precludes ligand uptake from environmental cells: implications for NK cell function. J. Exp. Med. 194, 1531-1539
45. Lanier, L. L. (1998) NK cell receptors. Annu. Rev. Immunol. 16, 359-393
46. Doucey, M. A., Scarpellino, L., Zimmer, J., Guillaume, P., Luescher, I. F., Bron, C., and Held, W. (2004) Cis association of Ly49A with MHC class I restricts natural killer cell inhibition. Nat. Immunol. 5, 328-336
47. Tabiasco, J., Espinosa, E., Hudrisier, D., Joly, E., Fournie, J. J., and Vercellone, A. (2002) Active trans-synaptic capture of membrane fragments by natural killer cells. Eur. J. Immunol. 32, 1502-1508
48. Onfelt, B., Nedvetzki, S., Yanagi, K., and Davis, D. M. (2004) Cutting edge: membrane nanotubes connect immune cells. J. Immunol. 173, 1511-1513
49. Tabiasco, J., Vercellone, A., Meggetto, F., Hudrisier, D., Brousset, P., and Fournie, J. J. (2003) Acquisition of viral receptor by NK cells through immunological synapse. J. Immunol. 170, 5993-5998
50. Fuchs, A., Cella, M., Giurisato, E., Shaw, A. S., and Colonna, M. (2004) Cutting edge: CD96 (tactile) promotes NK cell-target cell adhesion by interacting with the poliovirus receptor (CD155). J. Immunol. 172, 3994-3998
51. Black, P. H. (1980) Shedding from the cell surface of normal and cancer cells. Adv. Cancer Res. 32, 75-199
52. Becker, J. C., Dummer, R., Hartmann, A. A., Burg, G., and Schmidt, R. E. (1991) Shedding of ICAM-1 from human melanoma cell lines induced by IFN-gamma and tumor necrosis factor-alpha. Functional consequences on cell-mediated cytotoxicity. J. Immunol. 147, 4398-4401
53. Matala, E., Alexander, S. R., Kishimoto, T. K., and Walcheck, B. (2001) The cytoplasmic domain of L-selectin participates in regulating L-selectin endoproteolysis. J. Immunol. 167, 1617-1623
54. Shi, M., Dennis, K., Peschon, J. J., Chandrasekaran, R., and Mikecz, K. (2001) Antibody-induced shedding of CD44 from adherent cells is linked to the assembly of the cytoskeleton. J. Immunol. 167, 123-131
55. Zavazava, N., and Kronke, M. (1996) Soluble HLA class I molecules induce apoptosis in alloreactive cytotoxic T lymphocytes. Nat. Med. 2, 1005-1010
56. Wu, J. D., Higgins, L. M., Steinle, A., Cosman, D., Haugk, K., and Plymate, S. R. (2004) Prevalent expression of the immunostimulatory MHC class I chain-related molecule is counteracted by shedding in prostate cancer. J. Clin. Invest. 114, 560-568
57. Salih, H. R., Antropius, H., Gieseke, F., Lutz, S. Z., Kanz, L., Rammensee, H. G., and Steinle, A. (2003) Functional expression and release of ligands for the activating immunoreceptor NKG2D in leukemia. Blood 102, 1389-1396
58. Eisele, G., Wischhusen, J., Mittelbronn, M., Meyermann, R., Waldhauer, I., Steinle, A., Weller, M., and Friese, M. A. (2006) TGF-beta and metalloproteinases differentially suppress NKG2D ligand surface expression on malignant glioma cells. Brain. 129, 2416-2425
59. Salih, H. R., Rammensee, H. G., and Steinle, A. (2002) Cutting edge: down-regulation of MICA on human tumors by proteolytic shedding. J. Immunol. 169, 4098-4102
60. Waldhauer, I., and Steinle, A. (2006) Proteolytic release of soluble UL16-binding protein 2 from tumor cells. Cancer Res. 66, 2520-2526
61. Clayton, A., and Tabi, Z. (2005) Exosomes and the MICA-NKG2D system in cancer. Blood. Cells. Mol. Dis. 34, 206-213
62. Sheetz, M. P. (2001) Cell control by membrane-cytoskeleton adhesion. Nat. Rev. Mol. Cell. Biol. 2, 392-396
63. Dwir, O., Kansas, G. S., and Alon, R. (2001) Cytoplasmic anchorage of L-selectin controls leukocyte capture and rolling by increasing the mechanical stability of the selectin tether. J. Cell Biol. 155, 145-156
64. Raposo, G., Nijman, H. W., Stoorvogel, W., Liejendekker, R., Harding, C. V., Melief, C. J., and Geuze, H. J. (1996) B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med. 183, 1161-1172
65. Hwang, I., Shen, X., and Sprent, J. (2003) Direct stimulation of naive T cells by membrane vesicles from antigen-presenting cells: distinct roles for CD54 and B7 molecules. Proc. Natl. Acad. Sci. U. S. A. 100, 6670-6675
66. Kovar, M., Boyman, O., Shen, X., Hwang, I., Kohler, R., and Sprent, J. (2006) Direct stimulation of T cells by membrane vesicles from antigen-presenting cells. Proc. Natl. Acad. Sci. U. S. A. 103, 11671-11676
67. Togo, T., Krasieva, T. B., and Steinhardt, R. A. (2000) A decrease in membrane tension precedes successful cell-membrane repair. Mol. Biol. Cell 11, 4339-4346
68. Coleman, M. L., Sahai, E. A., Yeo, M., Bosch, M., Dewar, A., and Olson, M. F. (2001) Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I. Nat. Cell Biol. 3, 339-345
69. Arnold, P. Y., and Mannie, M. D. (1999) Vesicles bearing MHC class II molecules mediate transfer of antigen from antigen-presenting cells to CD4+ T cells. Eur. J. Immunol. 29, 1363-1373
70. Hwang, I., Huang, J. F., Kishimoto, H., Brunmark, A., Peterson, P. A., Jackson, M. R., Surh, C. D., Cai, Z., and Sprent, J. (2000) T cells can use either T cell receptor or CD28 receptors to absorb and internalize cell surface molecules derived from antigen-presenting cells. J. Exp. Med. 191, 1137-1148
71. Peters, P. J., Geuze, H. J., Van der Donk, H. A., Slot, J. W., Griffith, J. M., Stam, N. J., Clevers, H. C., and Borst, J. (1989) Molecules relevant for T cell-target cell interaction are present in cytolytic granules of human T lymphocytes. Eur. J. Immunol. 19, 1469-1475
72. Peters, P. J., Geuze, H. J., van der Donk, H. A., and Borst, J. (1990) A new model for lethal hit delivery by cytotoxic T lymphocytes. Immunol. Today 11, 28-32
73. Rustom, A., Saffrich, R., Markovic, I., Walther, P., and Gerdes, H. H. (2004) Nanotubular highways for intercellular organelle transport. Science 303, 1007-1010
74. Dai, J., and Sheetz, M. P. (1995) Mechanical properties of neuronal growth cone membranes studied by tether formation with laser optical tweezers. Biophys. J. 68, 988-996
75. Raucher, D., and Sheetz, M. P. (2000) Cell spreading and lamellipodial extension rate is regulated by membrane tension. J. Cell Biol. 148, 127-136
76. Bi, G. Q., Alderton, J. M., and Steinhardt, R. A. (1995) Calcium-regulated exocytosis is required for cell membrane resealing. J. Cell Biol. 131, 1747-1758
77. 2+-dependent vesicle-vesicle fusion events. J. Cell Biol. 139, 63-74
78. Colonna, M., Borsellino, G., Falco, M., Ferrara, G. B., and Strominger, J. L. (1993) HLA-C is the inhibitory ligand that determines dominant resistance to lysis by NK1- and NK2-specific natural killer cells. Proc. Natl. Acad. Sci. U. S. A. 90, 12000-12004
79. Sentman, C. L., Olsson, M. Y., and Karre, K. (1995) Missing self recognition by natural killer cells in MHC class I transgenic mice. A 'receptor calibration' model for how effector cells adapt to self. Semin. Immunol. 7, 109-119
80. Groh, V., Wu, J., Yee, C., and Spies, T. (2002) Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 419, 734-738
81. Salih, H. R., Goehlsdorf, D., and Steinle, A. (2006) Release of MICB molecules by tumor cells: mechanism and soluble MICB in sera of cancer patients. Hum. Immunol. 67, 188-195
82. Haugh, J. M., Huang, A. C., Wiley, H. S., Wells, A., and Lauffenburger, D. A. (1999) Internalized epidermal growth factor receptors participate in the activation of p21(ras) in fibroblasts. J. Biol. Chem. 274, 34350-34360
83. Eleme, K., Taner, S. B., Onfelt, B., Collinson, L. M., McCann, F. E., Chalupny, N. J., Cosman, D., Hopkins, C., Magee, A. I., and Davis, D. M. (2004) Cell surface organization of stress-inducible proteins ULBP and MICA that stimulate human NK cells and T cells via NKG2D. J. Exp. Med. 199, 1005-1010
84. Simons, K., and Ikonen, E. (1997) Functional rafts in cell membranes. Nature 387, 569-572
85. Hanna, J., Gonen-Gross, T., Fitchett, J., Rowe, T., Daniels, M., Arnon, T. I., Gazit, R., Joseph, A., Schjetne, K. W., Steinle, A., et al. (2004) Novel APC-like properties of human NK cells directly regulate T cell activation. J. Clin. Invest. 114, 1612-1623
86. Jones, S. A., and Rose-John, S. (2002) The role of soluble receptors in cytokine biology: the agonistic properties of the sIL-6R/IL-6 complex. Biochim. Biophys. Acta 1592, 251-263
87. Suzuki, T., Kiyokawa, N., Taguchi, T., Sekino, T., Katagiri, Y. U., and Fujimoto, J. (2001) CD24 induces apoptosis in human B cells via the glycolipid-enriched membrane domains/rafts-mediated signaling system. J. Immunol. 166, 5567-5577
88. Coudert, J. D., Zimmer, J., Tomasello, E., Cebecauer, M., Colonna, M., Vivier, E., and Held, W. (2005) Altered NKG2D function in NK cells induced by chronic exposure to NKG2D ligand-expressing tumor cells. Blood 106, 1711-1717
89. Oppenheim, D. E., Roberts, S. J., Clarke, S. L., Filler, R., Lewis, J. M., Tigelaar, R. E., Girardi, M., and Hayday, A. C. (2005) Sustained localized expression of ligand for the activating NKG2D receptor impairs natural cytotoxicity in vivo and reduces tumor immunosurveillance. Nat. Immunol. 6, 928-937
90. San Jose, E., and Alarcon, B. (1999) Receptor engagement transiently diverts the T cell receptor heterodimer from a constitutive degradation pathway. J. Biol. Chem. 274, 33740-33746
91. Vilen, B. J., Nakamura, T., and Cambier, J. C. (1999) Antigen-stimulated dissociation of BCR mIg from Ig-alpha/Ig-beta: implications for receptor desensitization. Immunity 10, 239-248
92. Igakura, T., Stinchcombe, J. C., Goon, P. K., Taylor, G. P., Weber, J. N., Griffiths, G. M., Tanaka, Y., Osame, M., and Bangham, C. R. (2003) Spread of HTLV-I between lymphocytes by virus-induced polarization of the cytoskeleton. Science 299, 1713-1716