Simulations of the NK cell immune synapse reveal that activation thresholds can be established by inhibitory receptors acting locally

Journal of Immunology

Volumn 187, Issue 2, 2011, Pages 760-773

  Kaplan, Asya ^a   Kotzer, Shulamit ^a   Almeida, Catarina R ^b,d   Kohen, Refael ^a   Halpert, Gilad ^a   Salmon Divon, Mali ^a,e   Köhler, Karsten ^a,f,g   Höglund, Petter ^c   Davis, Daniel M ^b   Mehr, Ramit ^a  

^a BAR ILAN UNIVERSITY   (Israel)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c KAROLINSKA INSTITUTE   (Sweden)

^d UNIVERSITY OF PORTO   (Portugal)

^e SHEBA MEDICAL CENTER   (Israel)

^f ADDENBROOKE S HOSPITAL   (United Kingdom)

^g UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HLA ANTIGEN; HLA C ANTIGEN; INTERCELLULAR ADHESION MOLECULE 1; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL1; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NATURAL KILLER CELL RECEPTOR NKG2D; VAV PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN RECOGNITION; ARTICLE; CELL MATURATION; CELL MEMBRANE; COMPUTER SIMULATION; CONTROLLED STUDY; DISSOCIATION; IMMUNOLOGICAL SYNAPSE; LYMPHOCYTE ACTIVATION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; SIGNAL TRANSDUCTION; STEADY STATE;

ANIMALS; COMPUTER SIMULATION; H-2 ANTIGENS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNOLOGICAL SYNAPSES; INTERCELLULAR ADHESION MOLECULE-1; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; MEMBRANE MICRODOMAINS; MICE; MODELS, IMMUNOLOGICAL; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY A; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; RECEPTORS, KIR;

EID: 79960517468     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1002208     Document Type: Article

References (98)

1. Burgess, S. J., K. Maasho, M. Masilamani, S. Narayanan, F. Borrego, and J. E. Coligan. 2008. The NKG2D receptor: immunobiology and clinical implications. Immunol. Res. 40: 18-34.
2. González, S., A. López-Soto, B. Suarez-Alvarez, A. López-Vázquez, and C. López-Larrea. 2008. NKG2D ligands: key targets of the immune response. Trends Immunol. 29: 397-403.
3. Vyas, Y. M., H. Maniar, and B. Dupont. 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. (Pubitemid 34250373)
4. Long, E. O. 2008. Negative signaling by inhibitory receptors: the NK cell paradigm. Immunol. Rev. 224: 70-84.
5. Ljunggren, H. G., and K. Kärre. 1990. In search of the 'missing self': MHC molecules and NK cell recognition. Immunol. Today 11: 237-244.
6. Kane, K. P., E. T. Silver, and B. Hazes. 2001. Specificity and function of activating Ly-49 receptors. Immunol. Rev. 181: 104-114.
7. Lanier, L. L. 2008. Up on the tightrope: natural killer cell activation and inhibition. Nat. Immunol. 9: 495-502.
8. Radaev, S., and P. D. Sun. 2003. Structure and function of natural killer cell surface receptors. Annu. Rev. Biophys. Biomol. Struct. 32: 93-114.
9. Vivier, E., J. A. Nunès, and F. Vély. 2004. Natural killer cell signaling pathways. Science 306: 1517-1519. (Pubitemid 39564941)
10. Yokoyama, W. M., and B. F. Plougastel. 2003. Immune functions encoded by the natural killer gene complex. Nat. Rev. Immunol. 3: 304-316.
11. Stebbins, C. C., C. Watzl, D. D. Billadeau, P. J. Leibson, D. N. Burshtyn, and E. O. Long. 2003. Vav1 dephosphorylation by the tyrosine phosphatase SHP-1 as amechanism for inhibition of cellular cytotoxicity. Mol. Cell. Biol. 23: 6291-6299.
12. Bryceson, Y. T., and E. O. Long. 2008. Line of attack: NK cell specificity and integration of signals. Curr. Opin. Immunol. 20: 344-352.
13. McCann, F. E., K. Suhling, L. M. Carlin, K. Eleme, S. B. Taner, K. Yanagi, B. Vanherberghen, P. M. French, and D. M. Davis. 2002. Imaging immune surveillance by T cells and NK cells. Immunol. Rev. 189: 179-192.
14. Davis, D. M. 2002. Assembly of the immunological synapse for T cells and NK cells. Trends Immunol. 23: 356-363. (Pubitemid 34717913)
15. Vyas, Y. M., K. M. Mehta, M. Morgan, H. Maniar, L. Butros, S. Jung, J. K. Burkhardt, and B. Dupont. 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. (Pubitemid 32954312)
16. Vyas, Y. M., H. Maniar, C. E. Lyddane, M. Sadelain, and B. Dupont. 2004. Ligand binding to inhibitory killer cell Ig-like receptors induce colocalization with Src homology domain 2-containing protein tyrosine phosphatase 1 and interruption of ongoing activation signals. J. Immunol. 173: 1571-1578. (Pubitemid 38971586)
17. Orange, J. S. 2008. Formation and function of the lytic NK-cell immunological synapse. Nat. Rev. Immunol. 8: 713-725.
18. Eleme, K., S. B. Taner, B. Onfelt, L. M. Collinson, F. E. McCann, N. J. Chalupny, D. Cosman, C. Hopkins, A. I. Magee, and D. M. Davis. 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.
19. Cebo, C., S. Da Rocha, S. Wittnebel, A. G. Turhan, J. Abdelali, S. Caillat- Zucman, J. H. Bourhis, S. Chouaib, and A. Caignard. 2006. The decreased susceptibility of Bcr/Abl targets to NK cell-mediated lysis in response to imatinib mesylate involves modulation of NKG2D ligands, GM1 expression, and synapse formation. J. Immunol. 176: 864-872. (Pubitemid 43099683)
20. Burack, W. R., K. H. Lee, A. D. Holdorf, M. L. Dustin, and A. S. Shaw. 2002. Cutting edge: quantitative imaging of raft accumulation in the immunological synapse. J. Immunol. 169: 2837-2841.
21. Harder, T., and K. R. Engelhardt. 2004.Membrane domains in lymphocytes - from lipid rafts to protein scaffolds. Traffic 5: 265-275.
22. Laude, A. J., and I. A. Prior. 2004. Plasma membrane microdomains: organization, function and trafficking. Mol. Membr. Biol. 21: 193-205.
23. Lou, Z., D. Jevremovic, D. D. Billadeau, and P. J. Leibson. 2000. A balance between positive and negative signals in cytotoxic lymphocytes regulates the polarization of lipid rafts during the development of cell-mediated killing. J. Exp. Med. 191: 347-354.
24. Pike, L. J. 2003. Lipid rafts: bringing order to chaos. J. Lipid Res. 44: 655-667. (Pubitemid 37279667)
25. Pizzo, P., and A. Viola. 2003. Lymphocyte lipid rafts: structure and function. Curr. Opin. Immunol. 15: 255-260.
26. Rodgers, W., D. Farris, and S. Mishra. 2005. Merging complexes: properties of membrane raft assembly during lymphocyte signaling. Trends Immunol. 26: 97-103.
27. Schmitz, G., and M. Grandl. 2008. Update on lipid membrane microdomains. Curr. Opin. Clin. Nutr. Metab. Care 11: 106-112.
28. Wright, M. D., G. W. Moseley, and A. B. van Spriel. 2004. Tetraspanin microdomains in immune cell signalling and malignant disease. Tissue Antigens 64: 533-542. (Pubitemid 39472918)
29. Vogt, A. B., S. Spindeldreher, and H. Kropshofer. 2002. Clustering of MHCpeptide complexes prior to their engagement in the immunological synapse: lipid raft and tetraspan microdomains. Immunol. Rev. 189: 136-151.
30. Lee, S. J. E., Y. Hori, J. T. Groves, M. L. Dustin, and A. K. Chakraborty. 2002. Correlation of a dynamic model for immunological synapse formation with effector functions: two pathways to synapse formation. Trends Immunol. 23: 492-499.
31. Giagulli, C., E. Scarpini, L. Ottoboni, S. Narumiya, E. C. Butcher, G. Constantin, and C. Laudanna. 2004. RhoA and zeta PKC control distinct modalities of LFA-1 activation by chemokines: critical role of LFA-1 affinity triggering in lymphocyte in vivo homing. Immunity 20: 25-35. (Pubitemid 38134291)
32. 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.
33. Weikl, T. R., and R. Lipowsky. 2004. Pattern formation during T-cell adhesion. Biophys. J. 87: 3665-3678. (Pubitemid 39602878)
34. Kotzer, S., M. Salmon-Divon, A. Kaplan, C. R. Almeida, P. Hoglund, D. M. Davis, and R. Mehr. 2007. Modeling the influence of molecule and cell surface micro-domain distribution on the formation of T cell immunological synapses. Life Science Systems and Applications Workshop, 2007. LISA 2007. IEEE/NIH. 8-9 November. Available at: http://ieeexplore.ieee.org/xpl/freeabs-all.jsp?arnumber= 4400878.
35. Culley, F. J., M. Johnson, J. H. Evans, S. Kumar, R. Crilly, J. Casasbuenas, T. Schnyder, M. Mehrabi, M. P. Deonarain, D. S. Ushakov, et al. 2009. Natural killer cell signal integration balances synapse symmetry and migration. PLoS Biol. 7: e1000159.
36. Treanor, B., P. M. P. Lanigan, S. Kumar, C. Dunsby, I. Munro, E. Auksorius, F. J. Culley, M. A. Purbhoo, D. Phillips, M. A. A. Neil, et al. 2006. Microclusters of inhibitory killer immunoglobulin-like receptor signaling at natural killer cell immunological synapses. J. Cell Biol. 174: 153-161.
37. Back, J., A. Chalifour, L. Scarpellino, and W. Held. 2007. Stable masking by H-2Dd cis ligand limits Ly49A relocalization to the site of NK cell/target cell contact. Proc. Natl. Acad. Sci. USA 104: 3978-3983.
38. Back, J., L. Scarpellino, and W. Held. 2010. Probing the interactions of NK cell receptors with ligand expressed in trans and cis. MethodsMol. Biol. 612: 313-323.
39. Chalifour, A., L. Scarpellino, J. Back, P. Brodin, E. Devèvre, F. Gros, F. Lévy, G. Leclercq, P. Höglund, F. Beermann, and W. Held. 2009. A role for cis interaction between the inhibitory Ly49A receptor and MHC class I for natural killer cell education. Immunity 30: 337-347.
40. Doucey, M. A., L. Scarpellino, J. Zimmer, P. Guillaume, I. F. Luescher, C. Bron, and W. Held. 2004. Cis association of Ly49A with MHC class I restricts natural killer cell inhibition. Nat. Immunol. 5: 328-336.
41. Held, W., and R. A. Mariuzza. 2008. Cis interactions of immunoreceptors with MHC and non-MHC ligands. Nat. Rev. Immunol. 8: 269-278.
42. Scarpellino, L., F. Oeschger, P. Guillaume, J. D. Coudert, F. Lévy, G. Leclercq, and W. Held. 2007. Interactions of Ly49 family receptors with MHC class I ligands in trans and cis. J. Immunol. 178: 1277-1284. (Pubitemid 46154597)
43. Saffman, P. G., and M. Delbrück. 1975. Brownian motion in biological membranes. Proc. Natl. Acad. Sci. USA 72: 3111-3113.
44. Raychaudhuri, S., A. K. Chakraborty, and M. Kardar. 2003. Effective membrane model of the immunological synapse. Phys. Rev. Lett. 91: 208101.
45. Burroughs, N. J., and C. Wülfing. 2002. Differential segregation in a cell-cell contact interface: the dynamics of the immunological synapse. Biophys. J. 83: 1784-1796.
46. Coombs, D., and B. Goldstein. 2004. Effects of the geometry of the immunological synapse on the delivery of effector molecules. Biophys. J. 87: 2215-2220. (Pubitemid 41071324)
47. Köhler, K., S. Xiong, J. Brzostek, M. Mehrabi, P. Eissmann, A. Harrison, S. P. Cordoba, S. Oddos, V. Miloserdov, K. Gould, et al. 2010. Matched sizes of activating and inhibitory receptor/ligand pairs are required for optimal signal integration by human natural killer cells. PLoS ONE 5: e15374.
48. Dykstra, M., A. Cherukuri, H. W. Sohn, S. J. Tzeng, and S. K. Pierce. 2003. Location is everything: lipid rafts and immune cell signaling. Annu. Rev. Immunol. 21: 457-481.
49. Horejsí, V. 2003. The roles of membrane microdomains (rafts) in T cell activation. Immunol. Rev. 191: 148-164.
50. Fujiwara, T., K. Ritchie, H. Murakoshi, K. Jacobson, and A. Kusumi. 2002. Phospholipids undergo hop diffusion in compartmentalized cell membrane. J. Cell Biol. 157: 1071-1081. (Pubitemid 34839781)
51. Giurisato, E., D. P. McIntosh, M. Tassi, A. Gamberucci, and A. Benedetti. 2003. T cell receptor can be recruited to a subset of plasma membrane rafts, independently of cell signaling and attendantly to raft clustering. J. Biol. Chem. 278: 6771-6778.
52. Kusumi, A., I. Koyama-Honda, and K. Suzuki. 2004. Molecular dynamics and interactions for creation of stimulation-induced stabilized rafts from small unstable steady-state rafts. Traffic 5: 213-230. (Pubitemid 38455745)
53. Marwali, M. R., M. A. MacLeod, D. N. Muzia, and F. Takei. 2004. Lipid rafts mediate association of LFA-1 and CD3 and formation of the immunological synapse of CTL. J. Immunol. 173: 2960-2967. (Pubitemid 39142000)
54. Montixi, C., C. Langlet, A. M. Bernard, J. Thimonier, C. Dubois, M. A. Wurbel, J. P. Chauvin, M. Pierres, and H. T. He. 1998. Engagement of T cell receptor triggers its recruitment to low-density detergent-insoluble membrane domains. EMBO J. 17: 5334-5348.
55. Munro, S. 2003. Lipid rafts: elusive or illusive? Cell 115: 377-388.
56. Pizzo, P., E. Giurisato, A. Bigsten, M. Tassi, R. Tavano, A. Shaw, and A. Viola. 2004. Physiological T cell activation starts and propagates in lipid rafts. Immunol. Lett. 91: 3-9.
57. Xavier, R., T. Brennan, Q. Li, C. McCormack, and B. Seed. 1998. Membrane compartmentation is required for efficient T cell activation. Immunity 8: 723-732.
58. Filipp, D., and M. Julius. 2004. Lipid rafts: resolution of the "fyn problem"? Mol. Immunol. 41: 645-656.
59. Schade, A. E., and A. D. Levine. 2002. Lipid raft heterogeneity in human peripheral blood T lymphoblasts: a mechanism for regulating the initiation of TCR signal transduction. J. Immunol. 168: 2233-2239.
60. Janes, P. W., S. C. Ley, and A. I. Magee. 1999. Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J. Cell Biol. 147: 447-461.
61. Hiltbold, E. M., N. J. Poloso, and P. A. Roche. 2003. MHC class II-peptide complexes and APC lipid rafts accumulate at the immunological synapse. J. Immunol. 170: 1329-1338.
62. Wülfing, C., I. Tskvitaria-Fuller, N. Burroughs, M. D. Sjaastad, J. Klem, and J. D. Schatzle. 2002. Interface accumulation of receptor/ligand couples in lymphocyte activation: methods, mechanisms, and significance. Immunol. Rev. 189: 64-83.
63. Poloso, N. J., and P. A. Roche. 2004. Association of MHC class II-peptide complexes with plasma membrane lipid microdomains. Curr. Opin. Immunol. 16: 103-107.
64. Anderson, H. A., E. M. Hiltbold, and P. A. Roche. 2000. Concentration of MHC class II molecules in lipid rafts facilitates antigen presentation. Nat. Immunol. 1: 156-162.
65. Meyer zum Bueschenfelde, C. O., J. Unternaehrer, I. Mellman, and K. Bottomly. 2004. Regulated recruitment of MHC class II and costimulatory molecules to lipid rafts in dendritic cells. J. Immunol. 173: 6119-6124.
66. Szöllósi, J., V. Horejsí, L. Bene, P. Angelisová, and S. Damjanovich. 1996. Supramolecular complexes of MHC class I, MHC class II, CD20, and tetraspan molecules (CD53, CD81, and CD82) at the surface of a B cell line JY. J. Immunol. 157: 2939-2946. (Pubitemid 126450050)
67. Leitinger, B., and N. Hogg. 2002. The involvement of lipid rafts in the regulation of integrin function. J. Cell Sci. 115: 963-972. (Pubitemid 34257381)
68. Cherukuri, A., P. C. Cheng, and S. K. Pierce. 2001. The role of the CD19/CD21 complex in B cell processing and presentation of complement-tagged antigens. J. Immunol. 167: 163-172.
69. Sheets, E. D., D. Holowka, and B. Baird. 1999. Critical role for cholesterol in Lyn-mediated tyrosine phosphorylation of FcepsilonRI and their association with detergent-resistant membranes. J. Cell Biol. 145: 877-887. (Pubitemid 29240862)
70. Jordan, S., and W. Rodgers. 2003. T cell glycolipid-enriched membrane domains are constitutively assembled as membrane patches that translocate to immune synapses. J. Immunol. 171: 78-87. (Pubitemid 36745275)
71. Kaizuka, Y., A. D. Douglass, S. Vardhana, M. L. Dustin, and R. D. Vale. 2009. The coreceptor CD2 uses plasma membrane microdomains to transduce signals in T cells. J. Cell Biol. 185: 521-534.
72. Dustin, M. L. 2002. Membrane domains and the immunological synapse: keeping T cells resting and ready. J. Clin. Invest. 109: 155-160.
73. Almeida, C. R., and D. M. Davis. 2006. Segregation of HLA-C from ICAM-1 at NK cell immune synapses is controlled by its cell surface density. J. Immunol. 177: 6904-6910.
74. Delon, J. 2000. The immunological synapse. Curr. Biol. 10: R214.
75. Anton van der Merwe, P., S. J. Davis, A. S. Shaw, and M. L. Dustin. 2000. Cytoskeletal polarization and redistribution of cell-surface molecules during T cell antigen recognition. Semin. Immunol. 12: 5-21.
76. 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.
77. 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. (Pubitemid 46674356)
78. Gasser, S., and D. H. Raulet. 2006. Activation and self-tolerance of natural killer cells. Immunol. Rev. 214: 130-142.
79. Rubio, G., X. Férez, M. Sánchez-Campillo, J. Gálvez, S. Martí, R. Verdú, T. Hernández-Caselles, and P. García-Peñarrubia. 2004. Cross-linking of MHC class I molecules on human NK cells inhibits NK cell function, segregates MHC I from the NK cell synapse, and induces intracellular phosphotyrosines. J. Leukoc. Biol. 76: 116-124.
80. Kaizuka, Y., A. D. Douglass, R. Varma, M. L. Dustin, and R. D. Vale. 2007. Mechanisms for segregating T cell receptor and adhesion molecules during immunological synapse formation in Jurkat T cells. Proc. Natl. Acad. Sci. USA 104: 20296-20301.
81. Brodin, P., T. Lakshmikanth, R. Mehr, M. H. Johansson, A. D. Duru, A. Achour, M. Salmon-Divon, K. Kärre, P. Höglund, and S. Johansson. 2010. Natural killer cell tolerance persists despite significant reduction of self MHC class I on normal target cells in mice. PLoS ONE 5: e1317.
82. Carlin, L. M., K. Eleme, F. E. McCann, and D. M. Davis. 2001. Intercellular transfer and supramolecular organization of human leukocyte antigen C at inhibitory natural killer cell immune synapses. J. Exp. Med. 194: 1507-1517.
83. Fassett, M. S., D. M. Davis, M. M. Valter, G. B. Cohen, and J. L. Strominger. 2001. Signaling at the inhibitory natural killer cell immune synapse regulates lipid raft polarization but not class I MHC clustering. Proc. Natl. Acad. Sci. USA 98: 14547-14552.
84. Faure, M., D. F. Barber, S. M. Takahashi, T. Jin, and E. O. Long. 2003. Spontaneous clustering and tyrosine phosphorylation of NK cell inhibitory receptor induced by ligand binding. J. Immunol. 170: 6107-6114.
85. Standeven, L. J., L. M. Carlin, P. Borszcz, D. M. Davis, and D. N. Burshtyn. 2004. The actin cytoskeleton controls the efficiency of killer Ig-like receptor accumulation at inhibitory NK cell immune synapses. J. Immunol. 173: 5617-5625.
86. Abeyweera, T. P., E. Merino, and M. Huse. 2011. Inhibitory signaling blocks activating receptor clustering and induces cytoskeletal retraction in natural killer cells. J. Cell Biol. 192: 675-690.
87. Labadia, M. E., D. D. Jeanfavre, G. O. Caviness, and M. M. Morelock. 1998. Molecular regulation of the interaction between leukocyte function-associated antigen-1 and soluble ICAM-1 by divalent metal cations. J. Immunol. 161: 836-842.
88. Tominaga, Y., Y. Kita, A. Satoh, S. Asai, K. Kato, K. Ishikawa, T. Horiuchi, and T. Takashi. 1998. Affinity and kinetic analysis of the molecular interaction of ICAM-1 and leukocyte function-associated antigen-1. J. Immunol. 161: 4016-4022. (Pubitemid 28468979)
89. Maenaka, K., P. A. van der Merwe, D. I. Stuart, E. Y. Jones, and P. Sondermann. 2001. The human low affinity Fcgamma receptors IIa, IIb, and III bind IgG with fast kinetics and distinct thermodynamic properties. J. Biol. Chem. 276: 44898-44904.
90. Dustin, M. L., L. M. Ferguson, P. Y. Chan, T. A. Springer, and D. E. Golan. 1996. Visualization of CD2 interaction with LFA-3 and determination of the twodimensional dissociation constant for adhesion receptors in a contact area. J. Cell Biol. 132: 465-474.
91. Sloan-Lancaster, J., J. Presley, J. Ellenberg, T. Yamazaki, J. Lippincott-Schwartz, and L. E. Samelson. 1998. ZAP-70 association with T cell receptor zeta (TCRzeta): fluorescence imaging of dynamic changes upon cellular stimulation. J. Cell Biol. 143: 613-624.
92. von Essen, M., C. M. Bonefeld, V. Siersma, A. B. Rasmussen, J. P. Lauritsen, B. L. Nielsen, and C. Geisler. 2004. Constitutive and ligand-induced TCR degradation. J. Immunol. 173: 384-393. (Pubitemid 38797364)
93. Groves, J. T., C. Wulfing, and S. G. Boxer. 1996. Electrical manipulation of glycan-phosphatidyl inositol-tethered proteins in planar supported bilayers. Biophys. J. 71: 2716-2723.
94. Krogsgaard, M., Q. J. Li, C. Sumen, J. B. Huppa, M. Huse, and M. M. Davis. 2005. Agonist/endogenous peptide-MHC heterodimers drive T cell activation and sensitivity. Nature 434: 238-243.
95. Dimasi, N., M. W. Sawicki, L. A. Reineck, Y. Li, K. Natarajan, D. H. Margulies, and R. A. Mariuzza. 2002. Crystal structure of the Ly49I natural killer cell receptor reveals variability in dimerization mode within the Ly49 family. J. Mol. Biol. 320: 573-585.
96. Natarajan, K., L. F. Boyd, P. Schuck, W. M. Yokoyama, D. Eliat, and D. H. Margulies. 1999. Interaction of the NK cell inhibitory receptor Ly49A with H-2Dd: identification of a site distinct from the TCR site. Immunity 11: 591-601.
97. O'Callaghan, C. A., A. Cerwenka, B. E. Willcox, L. L. Lanier, and P. J. Bjorkman. 2001. Molecular competition for NKG2D: H60 and RAE1 compete unequally for NKG2D with dominance of H60. Immunity 15: 201-211.
98. Borrego, F., M. Masilamani, A. I. Marusina, X. Tang, and J. E. Coligan. 2006. The CD94/NKG2 family of receptors: from molecules and cells to clinical relevance. Immunol. Res. 35: 263-278.