Structural immunology and crystallography help immunologists see the immune system in action: How T and NK cells touch their ligands

IUBMB Life

Volumn 61, Issue 6, 2009, Pages 579-590

  Chen, Yong ^a,b   Shi, Yi ^a,b   Cheng, Hao ^a,b   An, Yun Qing ^c   Gao, George F ^a,b,c  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

Crystallography; HLA; Immune system; Interaction; KIR; Ligand; LILR; MHC; NK cell; Receptor; Structural immunology; T cell

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; CD94 ANTIGEN; HLA ANTIGEN; IMMUNOGLOBULIN; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; LEUKOCYTE IMMUNOGLOBULIN LIKE RECEPTORS; LYSINE; NATURAL KILLER CELL RECEPTOR; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; IMMUNOGLOBULIN RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR;

CELL FUNCTION; CELL INTERACTION; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; MAJOR HISTOCOMPATIBILITY COMPLEX; NATURAL KILLER CELL; NONHUMAN; PROTEIN BINDING; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; ANIMAL; IMMUNOLOGY; PHYSIOLOGY;

ANIMALS; ANTIGENS, CD4; ANTIGENS, CD8; CRYSTALLOGRAPHY; HLA ANTIGENS; HUMANS; KILLER CELLS, NATURAL; MAJOR HISTOCOMPATIBILITY COMPLEX; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; RECEPTORS, IMMUNOLOGIC; RECEPTORS, KIR; RECEPTORS, NATURAL KILLER CELL; T-LYMPHOCYTES;

EID: 69449084042     PISSN: 15216543     EISSN: 15216551     Source Type: Journal    
DOI: 10.1002/iub.208     Document Type: Review

References (88)

1. Zinkernagel, R. M. and Doherty, P. C. (1974) Restriction of in vitro T cell-mediated cytotoxicity in lymphocytic choriomeningitis within a syngeneic or semiallogeneic system. Nature 248, 701-702.
2. Sawicki, M. W., Dimasi, N., Natarajan, K., Wang, J., Margulies, D. H., and Mariuzza, R. A. (2001) Structural basis of MHC class I recognition by natural killer cell receptors. Immunol. Rev. 181, 52-65.
3. Rudolph, M. G., Stanfield, R. L., and Wilson, I. A. (2006) How TCRs bind MHCs, peptides, and coreceptors. Annu. Rev. Immunol. 24, 419-466.
4. Lanier, L. L. (2005) NK cell recognition. Annu. Rev. Immunol. 23, 225-274.
5. Arden, B., Clark, S. P., Kabelitz, D., and Mak, T. W. (1995) Human T-cell receptor variable gene segment families. Immunogenetics 42, 455-500. (Pubitemid 26025063)
6. Rowen, L., Koop, B. F., and Hood, L. (1996) The complete 685-kilo-base DNA sequence of the human beta T cell receptor locus. Science 272, 1755-1762.
7. Jerne, N. K. (1971) The somatic generation of immune recognition. Eur. J. Immunol. 1, 1-9.
8. Davis, M. M. and Bjorkman, P. J. (1988) T-cell antigen receptor genes and T-cell recognition. Nature 334, 395-402.
9. Garboczi, D. N., Ghosh, P., Utz, U., Fan, Q. R., Biddison, W. E., and Wiley, D. C. (1996) Structure of the complex between human T-cell receptor, viral peptide and HLA-A2. Nature 384, 134-141.
10. Garcia, K. C., Degano, M., Stanfield, R. L., Brunmark, A., Jackson, M. R., Peterson, P. A., Teyton, L., and Wilson, I. A. (1996) An alphabeta T cell receptor structure at 2.5 A and its orientation in the TCR-MHC complex. Science 274, 209-219.
11. Zerrahn, J., Held, W., and Raulet, D. H. (1997) The MHC reactivity of the T cell repertoire prior to positive and negative selection. Cell 88, 627-636. (Pubitemid 27152405)
12. Feng, D., Bond, C. J., Ely, L. K., Maynard, J., and Garcia, K. C. (2007) Structural evidence for a germline-encoded T cell receptor-major histocompatibility complex interaction 'codon'. Nat. Immunol. 8, 975-983.
13. Dai, S., Huseby, E. S., Rubtsova, K., Scott-Browne, J., Crawford, F., Macdonald, W. A., Marrack, P., and Kappler, J. W. (2008) Crossreactive T Cells spotlight the germline rules for alphabeta T cell-receptor interactions with MHC molecules. Immunity 28, 324-334.
14. Wucherpfennig, K. W., Allen, P. M., Celada, F., Cohen, I. R., De Boer, R., Garcia, K. C., Goldstein, B., Greenspan, R., Hafler, D., Hodgkin, P., Huseby, E. S., Krakauer, D. C., Nemazee, D., Perelson, A. S., Pinilla, C., Strong, R. K., and Sercarz, E. E. (2007) Polyspecificity of T cell and B cell receptor recognition. Semin. Immunol. 19, 216-224.
15. Gao, G. F., Tormo, J., Gerth, U. C., Wyer, J. R., McMichael, A. J., Stuart, D. I., Bell, J. I., Jones, E. Y., and Jakobsen, B. K. (1997) Crystal structure of the complex between human CD8alpha(alpha) and HLA-A2. Nature 387, 630-634. (Pubitemid 27248771)
16. Garcia, K. C., Scott, C. A., Brunmark, A., Carbone, F. R., Peterson, P. A., Wilson, I. A., and Teyton, L. (1996) CD8 enhances formation of stable T-cell receptor/MHC class I molecule complexes. Nature 384, 577-581. (Pubitemid 26415937)
17. Kern, P. S., Teng, M. K., Smolyar, A., Liu, J. H., Liu, J., Hussey, R. E., Spoerl, R., Chang, H. C., Reinherz, E. L., and Wang, J. H. (1998) Structural basis of CD8 coreceptor function revealed by crystallographic analysis of a murine CD8alphaalpha ectodomain fragment in complex with H-2Kb. Immunity 9, 519-530. (Pubitemid 28499203)
18. Wang, J. H., Meijers, R., Xiong, Y., Liu, J. H., Sakihama, T., Zhang, R., Joachimiak, A., and Reinherz, E. L. (2001) Crystal structure of the human CD4 N-terminal two-domain fragment complexed to a class II MHC molecule. Proc. Natl. Acad. Sci. USA 98, 10799-10804.
19. Wyer, J. R., Willcox, B. E., Gao, G. F., Gerth, U. C., Davis, S. J., Bell, J. I., van der Merwe, P. A., and Jakobsen, B. K. (1999) T cell receptor and coreceptor CD8 alphaalpha bind peptide-MHC independently and with distinct kinetics. Immunity 10, 219-225.
20. Xiong, Y., Kern, P., Chang, H., and Reinherz, E. (2001) T Cell Receptor Binding to a pMHCII Ligand Is Kinetically Distinct from and Independent of CD4. J. Biol. Chem. 276, 5659-5667.
21. Arcaro, A., Gregoire, C., Bakker, T. R., Baldi, L., Jordan, M., Goffin, L., Boucheron, N., Wurm, F., van der Merwe, P. A., Malissen, B., and Luescher, I. F. (2001) CD8beta endows CD8 with efficient coreceptor function by coupling T cell receptor/CD3 to raft-associated CD8/p56(lck) complexes. J. Exp. Med. 194, 1485-1495.
22. Janeway, C. A., Jr. (1992) The T cell receptor as a multicomponent signalling machine: CD4/CD8 coreceptors and CD45 in T cell activation. Annu. Rev. Immunol. 10, 645-674.
23. Chang, H. C., Tan, K., Ouyang, J., Parisini, E., Liu, J. H., Le, Y., Wang, X., Reinherz, E. L., and Wang, J. H. (2005) Structural and mutational analyses of a CD8alphabeta heterodimer and comparison with the CD8alphaalpha homodimer. Immunity 23, 661-671. (Pubitemid 41779487)
24. Liu, Y., Xiong, Y., Naidenko, O. V., Liu, J. H., Zhang, R., Joachimiak, A., Kronenberg, M., Cheroutre, H., Reinherz, E. L., and Wang, J. H. (2003) The crystal structure of a TL/CD8alphaalpha complex at 2.1 A resolution: implications for modulation of T cell activation and memory. Immunity 18, 205-215. (Pubitemid 36262996)
25. Gao, G. F. and Jakobsen, B. K. (2000) Molecular interactions of coreceptor CD8 and MHC class I: the molecular basis for functional coordination with the T-cell receptor. Immunol. Today. 21, 630-636.
26. Gao, G. F., Rao, Z., and Bell, J. I. (2002) Molecular coordination of alphabeta T-cell receptors and coreceptors CD8 and CD4 in their recognition of peptide-MHC ligands. Trends. Immunol. 23, 408-413.
27. Allen, T. M., Sidney, J., del Guercio, M. F., Glickman, R. L., Lensmeyer, G. L., Wiebe, D. A., DeMars, R., Pauza, C. D., Johnson, R. P., Sette, A., and Watkins, D. I. (1998) Characterization of the peptide binding motif of a rhesus MHC class I molecule (Mamu-A*01) that binds an immunodominant CTL epitope from simian immunodeficiency virus. J. Immunol. 160, 6062-6071. (Pubitemid 28298070)
28. Matano, T., Shibata, R., Siemon, C., Connors, M., Lane, H. C., and Martin, M. A. (1998) Administration of an anti-CD8 monoclonal antibody interferes with the clearance of chimeric simian/human immunodeficiency virus during primary infections of rhesus macaques. J. Virol. 72, 164-169. (Pubitemid 28048825)
29. Schmitz, J. E., Kuroda, M. J., Santra, S., Sasseville, V. G., Simon, M. A., Lifton, M. A., Racz, P., Tenner-Racz, K., Dalesandro, M., Scallon, B. J., Ghrayeb, J., Forman, M. A., Montefiori, D. C., Rieber, E. P., Letvin, N. L., and Reimann, K. A. (1999) Control of viremia in simian immunodeficiency virus infection by CD81 lymphocytes. Science, 283, 857-860. (Pubitemid 129501128)
30. Chu, F., Lou, Z., Chen, Y. W., Liu, Y., Gao, B., Zong, L., Khan, A. H., Bell, J. I., Rao, Z., and Gao, G. F. (2007) First glimpse of the peptide presentation by rhesus macaque MHC class I: crystal structures of Mamu-A*01 complexed with two immunogenic SIV epitopes and insights into CTL escape. J. Immunol. 178, 944-952. (Pubitemid 46095167)
31. Zong, L., Chen, Y., Peng, H., Gao, F., Iwamoto, A., and Gao, G. F. (2009) Rhesus macaque: a tight homodimeric CD8alphaalpha. Proteins 75, 241-244.
32. Bretscher, P. and Cohn, M. (1970) A theory of self-nonself discrimination. Science 169, 1042-1049.
33. Gross, J. A., Callas, E., and Allison, J. P. (1992) Identification and distribution of the costimulatory receptor CD28 in the mouse. J. Immunol. 149, 380-388.
34. Hathcock, K. S., Laszlo, G., Pucillo, C., Linsley, P., and Hodes, R. J. (1994) Comparative analysis of B7-1 and B7-2 costimulatory ligands: expression and function. J. Exp. Med. 180, 631-640.
35. Coyle, A. J., Lehar, S., Lloyd, C., Tian, J., Delaney, T., Manning, S., Nguyen, T., Burwell, T., Schneider, H., Gonzalo, J. A., Gosselin, M., Owen, L. R., Rudd, C. E., and Gutierrez-Ramos, J. C. (2000) The CD28-related molecule ICOS is required for effective T cell-dependent immune responses. Immunity 13, 95-105.
36. Dong, C., Juedes, A. E., Temann, U. A., Shresta, S., Allison, J. P., Ruddle, N. H., and Flavell, R. A. (2001) ICOS co-stimulatory receptor is essential for T-cell activation and function. Nature 409, 97-101. (Pubitemid 32098632)
37. Brunet, J. F., Denizot, F., Luciani, M. F., Roux-Dosseto, M., Suzan, M., Mattei, M. G., and Golstein, P. (1987) A new member of the immunoglobulin superfamily--CTLA-4. Nature 328, 267-270.
38. Freeman, G. J., Long, A. J., Iwai, Y., Bourque, K., Chernova, T., Nishimura, H., Fitz, L. J., Malenkovich, N., Okazaki, T., Byrne, M. C., Horton, H. F., Fouser, L., Carter, L., Ling, V., Bowman, M. R., Carreno, B. M., Collins, M., Wood, C. R., and Honjo, T. (2000) Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J. Exp. Med. 192, 1027-1034.
39. Latchman, Y., Wood, C. R., Chernova, T., Chaudhary, D., Borde, M., Chernova, I., Iwai, Y., Long, A. J., Brown, J. A., Nunes, R., Greenfield, E. A., Bourque, K., Boussiotis, V. A., Carter, L. L., Carreno, B. M., Malenkovich, N., Nishimura, H., Okazaki, T., Honjo, T., Sharpe, A. H. and Freeman, G. J. (2001) PD-L2 is a second ligand for PD-1 and inhibits T cell activation. Nat. Immunol. 2, 261-268.
40. Stamper, C. C., Zhang, Y., Tobin, J. F., Erbe, D. V., Ikemizu, S., Davis, S. J., Stahl, M. L., Seehra, J., Somers, W. S., and Mosyak, L. (2001) Crystal structure of the B7-1/CTLA-4 complex that inhibits human immune responses. Nature 410, 608-611. (Pubitemid 32267208)
41. Schwartz, J. C., Zhang, X., Fedorov, A. A., Nathenson, S. G., and Almo, S. C. (2001) Structural basis for co-stimulation by the human CTLA-4/B7-2 complex. Nature 410, 604-608. (Pubitemid 32267207)
42. Evans, E. J., Esnouf, R. M., Manso-Sancho, R., Gilbert, R. J., James, J. R., Yu, C., Fennelly, J. A., Vowles, C., Hanke, T., Walse, B., Hunig, T., Sorensen, P., Stuart, D. I., and Davis, S. J. (2005) Crystal structure of a soluble CD28-Fab complex. Nat. Immunol. 6, 271-279.
43. Zhang, X., Schwartz, J. C., Guo, X., Bhatia, S., Cao, E., Lorenz, M., Cammer, M., Chen, L., Zhang, Z. Y., Edidin, M. A., Nathenson, S. G. and Almo, S. C. (2004) Structural and functional analysis of the costimulatory receptor programmed death-1. Immunity 20, 337-347. (Pubitemid 38388235)
44. Lin, D. Y., Tanaka, Y., Iwasaki, M., Gittis, A. G., Su, H. P., Mikami, B., Okazaki, T., Honjo, T., Minato, N., and Garboczi, D. N. (2008) The PD-1/PD-L1 complex resembles the antigen-binding Fv domains of anti-bodies and T cell receptors. Proc. Natl. Acad. Sci. USA 105, 3011-3016.
45. Lazar-Molnar, E., Yan, Q., Cao, E., Ramagopal, U., Nathenson, S. G., and Almo, S. C. (2008) Crystal structure of the complex between programmed death-1 (PD-1) and its ligand PD-L2. Proc. Natl. Acad. Sci. USA 105, 10483-10488.
46. Hayday, A. C. (2000) cd cells: a right time and a right place for a conserved third way of protection. Annu. Rev. Immunol. 18, 975-1026.
47. Rock, E. P., Sibbald, P. R., Davis, M. M., and Chien, Y. H. (1994) CDR3 length in antigen-specific immune receptors. J. Exp. Med. 179, 323-328.
48. Morita, C. T., Mariuzza, R. A., and Brenner, M. B. (2000) Antigen recognition by human gamma delta T cells: pattern recognition by the adaptive immune system. Springer Semin. Immunopathol. 22, 191-217.
49. Adams, E. J., Chien, Y. H., and Garcia, K. C. (2005) Structure of a gammadelta T cell receptor in complex with the nonclassical MHC T22. Science 308, 227-231.
50. Adams, E. J., Strop, P., Shin, S., Chien, Y. H., and Garcia, K. C. (2008) An autonomous CDR3delta is sufficient for recognition of the nonclassical MHC class I molecules T10 and T22 by gammadelta T cells. Nat. Immunol. 9, 777-784.
51. Fan, Q. R., Long, E. O., and Wiley, D. C. (2001) Crystal structure of the human natural killer cell inhibitory receptor KIR2DL1-HLA-Cw4 complex. Nat. Immunol. 2, 452-460.
52. Snyder, G. A., Brooks, A. G., and Sun, P. D. (1999) Crystal structure of the HLA-Cw3 allotype-specific killer cell inhibitory receptor KIR2DL2. Proc. Natl. Acad. Sci. USA 96, 3864-3869.
53. Petrie, E. J., Clements, C. S., Lin, J., Sullivan, L. C., Johnson, D., Huyton, T., Heroux, A., Hoare, H. L., Beddoe, T., Reid, H. H., Wilce, M. C., Brooks, A. G., and Rossjohn, J. (2008) CD94-NKG2A recognition of human leukocyte antigen (HLA)-E bound to an HLA class I leader sequence. J. Exp. Med. 205, 725-735.
54. Deng, L., Cho, S., Malchiodi, E. L., Kerzic, M. C., Dam, J., and Mariuzza, R. A. (2008) Molecular architecture of the major histocompatibility complex class I-binding site of Ly49 natural killer cell receptors. J. Biol. Chem. 283, 16840-16849.
55. Shiroishi, M., Kuroki, K., Rasubala, L., Tsumoto, K., Kumagai, I., Kurimoto, E., Kato, K., Kohda, D., and Maenaka, K. (2006) Structural basis for recognition of the nonclassical MHC molecule HLA-G by the leukocyte Ig-like receptor B2 (LILRB2/LIR2/ILT4/CD85d). Proc. Natl. Acad. Sci. USA 103, 16412-16417.
56. Willcox, B. E., Thomas, L. M., and Bjorkman, P. J. (2003) Crystal structure of HLA-A2 bound to LIR-1, a host and viral major histocompatibility complex receptor. Nat. Immunol. 4, 913-919.
57. Tormo, J., Natarajan, K., Margulies, D. H., and Mariuzza, R. A. (1999) Crystal structure of a lectin-like natural killer cell receptor bound to its MHC class I ligand. Nature 402, 623-631. (Pubitemid 129516325)
58. Deng, L. and Mariuzza, R. A. (2006) Structural basis for recognition of MHC and MHC-like ligands by natural killer cell receptors. Semin. Immunol. 18, 159-166.
59. Rajagopalan, S. and Long, E. O. (1997) The direct binding of a p58 killer cell inhibitory receptor to human histocompatibility leukocyte antigen (HLA)-Cw4 exhibits peptide selectivity. J. Exp. Med. 185, 1523-1528.
60. Boyington, J. C., Motyka, S. A., Schuck, P., Brooks, A. G., and Sun, P. D. (2000) Crystal structure of an NK cell immunoglobulin-like receptor in complex with its class I MHC ligand. Nature 405, 537-543.
61. Rudolph, M. G., Luz, J. G., and Wilson, I. A. (2002) Structural and thermodynamic correlates of T cell signaling. Annu. Rev. Biophys. Biomol. Struct. 31, 121-149.
62. Colonna, M., Navarro, F., Bellon, T., Llano, M., Garcia, P., Samaridis, J., Angman, L., Cella, M., and Lopez-Botet, M. (1997) A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and myelomonocytic cells. J. Exp. Med. 186, 1809-1818.
63. Cosman, D., Fanger, N., Borges, L., Kubin, M., Chin, W., Peterson, L., and Hsu, M. L. (1997) A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules. Immunity 7, 273-282. (Pubitemid 27392018)
64. Saverino, D., Fabbi, M., Ghiotto, F., Merlo, A., Bruno, S., Zarcone, D., Tenca, C., Tiso, M., Santoro, G., Anastasi, G., Cosman, D., Grossi, C. E., and Ciccone, E. (2000) The CD85/LIR-1/ILT2 inhibitory receptor is expressed by all human T lymphocytes and down-regulates their functions. J. Immunol. 165, 3742-3755. (Pubitemid 32057280)
65. Cella, M., Dohring, C., Samaridis, J., Dessing, M., Brockhaus, M., Lanzavecchia, A., and Colonna, M. (1997) A novel inhibitory receptor (ILT3) expressed on monocytes, macrophages, and dendritic cells involved in antigen processing. J. Exp. Med. 185, 1743-1751.
66. Shiroishi, M., Kajikawa, M., Kuroki, K., Ose, T., Kohda, D., and Maenaka, K. (2006) Crystal structure of the human monocyte-activating receptor, "Group 2" leukocyte Ig-like receptor A5 (LILRA5/LIR9/ILT11). J. Biol. Chem. 281, 19536-19544.
67. Willcox, B. E., Thomas, L. M., Chapman, T. L., Heikema, A. P., West, A. P., Jr., and Bjorkman, P. J. (2002) Crystal structure of LIR-2 (ILT4) at 1.8 A: differences from LIR-1 (ILT2) in regions implicated in the binding of the Human Cytomegalovirus class I MHC homolog UL18. BMC. Struct. Biol., 2, 6-15.
68. Chapman, T. L., Heikema, A. P., West, A. P., Jr., and Bjorkman, P. J. (2000) Crystal structure and ligand binding properties of the D1D2 region of the inhibitory receptor LIR-1 (ILT2). Immunity 13, 727-736.
69. Yang, Z. and Bjorkman, P. J. (2008) Structure of UL18, a peptide-binding viral MHC mimic, bound to a host inhibitory receptor. Proc. Natl. Acad. Sci. USA 105, 10095-10100.
70. Garner, L. I., Salim, M., Mohammed, F., and Willcox, B. E. (2006) Expression, purification, and refolding of the myeloid inhibitory receptor leukocyte immunoglobulin-like receptor-5 for structural and ligand identification studies. Protein Expr. Purif. 47, 490-497.
71. Chen, Y., Chu, F., Gao, F., Zhou, B., and Gao, G. F. (2007) Stability engineering, biophysical, and biological characterization of the myeloid activating receptor immunoglobulin-like transcript 1 (ILT1/LIR-7/LILRA2). Protein Expr. Purif. 56, 253-260. (Pubitemid 47633226)
72. Shiroishi, M., Tsumoto, K., Amano, K., Shirakihara, Y., Colonna, M., Braud, V. M., Allan, D. S., Makadzange, A., Rowland-Jones, S., Willcox, B., Jones, E. Y., van der Merwe, P. A., Kumagai, I., and Maenaka, K. (2003) Human inhibitory receptors Ig-like transcript 2 (ILT2) and ILT4 compete with CD8 for MHC class I binding and bind preferentially to HLA-G. Proc. Natl. Acad. Sci. USA, 100, 8856-8861.
73. Young, N. T., Waller, E. C., Patel, R., Roghanian, A., Austyn, J. M., and Trowsdale, J. (2008) The inhibitory receptor LILRB1 modulates the differentiation and regulatory potential of human dendritic cells. Blood 111, 3090-3096.
74. Lichterfeld, M., Kavanagh, D. G., Williams, K. L., Moza, B., Mui, S. K., Miura, T., Sivamurthy, R., Allgaier, R., Pereyra, F., Trocha, A., Feeney, M., Gandhi, R. T., Rosenberg, E. S., Altfeld, M., Allen, T. M., Allen, R., Walker, B. D., Sundberg, E. J., and Yu, X. G. (2007) A viral CTL escape mutation leading to immunoglobulin-like transcript 4-mediated functional inhibition of myelomonocytic cells. J. Exp. Med. 204, 2813-2824.
75. Tedla, N., Bandeira-Melo, C., Tassinari, P., Sloane, D. E., Samplaski, M., Cosman, D., Borges, L., Weller, P. F., and Arm, J. P. (2003) Activation of human eosinophils through leukocyte immunoglobulin-like receptor 7. Proc. Natl. Acad. Sci. USA 100, 1174-1179.
76. Sloane, D. E., Tedla, N., Awoniyi, M., Macglashan, D. W., Jr., Borges, L., Austen, K. F., and Arm, J. P. (2004) Leukocyte immunoglobulinlike receptors: novel innate receptors for human basophil activation and inhibition. Blood 104, 2832-2839. (Pubitemid 39434969)
77. Nakajima, H., Samaridis, J., Angman, L., and Colonna, M. (1999) Human myeloid cells express an activating ILT receptor (ILT1) that associates with Fc receptor gamma-chain. J. Immunol. 162, 5-8. (Pubitemid 29018897)
78. Chen, Y., Gao, F., Chu, F., Peng, H., Zong, L., Liu, Y., Tien, P., and Gao, G. F. (2009) Crystal structure of myeloid cell activating receptor leukocyte Ig-like receptor A2 (LILRA2/ILT1/LIR-7) domain swapped dimer: molecular basis for its non-binding to MHC complexes. J. Mol. Biol. 386, 841-853.
79. Braud, V. M., Allan, D. S., O'Callaghan, C. A., Soderstrom, K., D'Andrea, A., Ogg, G. S., Lazetic, S., Young, N. T., Bell, J. I., Phillips, J. H., Lanier, L. L., and McMichael, A. J. (1998) HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391, 795-799. (Pubitemid 28099678)
80. Gasser, S. and Raulet, D. H. (2006) Activation and self-tolerance of natural killer cells. Immunol. Rev. 214, 130-142.
81. Nakamura, M. C. and Seaman, W. E. (2001) Ligand interactions by activating and inhibitory Ly-49 receptors. Immunol. Rev. 181, 138-148.
82. Matsumoto, N., Mitsuki, M., Tajima, K., Yokoyama, W. M., and Yamamoto, K. (2001) The functional binding site for the C-type lectin-like natural killer cell receptor Ly49A spans three domains of its major histocompatibility complex class I ligand. J. Exp. Med. 193, 147-158.
83. Moretta, A., Bottino, C., Vitale, M., Pende, D., Cantoni, C., Mingari, M. C., Biassoni, R., and Moretta, L. (2001) Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu. Rev. Immunol. 19, 197-223.
84. Ho, J. W., Hershkovitz, O., Peiris, M., Zilka, A., Bar-Ilan, A., Nal, B., Chu, K., Kudelko, M., Kam, Y. W., Achdout, H., Mandelboim, M., Altmeyer, R., Mandelboim, O., Bruzzone, R., and Porgador, A. (2008) H5-type influenza virus hemagglutinin is functionally recognized by the natural killer-activating receptor NKp44. J. Virol. 82, 2028-2032. (Pubitemid 351206948)
85. Mandelboim, O., Lieberman, N., Lev, M., Paul, L., Arnon, T. I., Bushkin, Y., Davis, D. M., Strominger, J. L., Yewdell, J. W., and Porgador, A. (2001) Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature 409, 1055-1060. (Pubitemid 32204059)
86. Hahn, M., Nicholson, M. J., Pyrdol, J., and Wucherpfennig, K. W. (2005) Unconventional topology of self peptide-major histocompatibility complex binding by a human autoimmune T cell receptor. Nat. Immunol. 6, 490-496.
87. Tynan, F. E., Burrows, S. R., Buckle, A. M., Clements, C. S., Borg, N. A., Miles, J. J., Beddoe, T., Whisstock, J. C., Wilce, M. C., Silins, S. L., Burrows, J. M., Kjer-Nielsen, L., Kostenko, L., Purcell, A. W., McCluskey, J., and Rossjohn, J. (2005) T cell receptor recognition of a 'super-bulged' major histocompatibility complex class I-bound peptide. Nat. Immunol. 6, 1114-1122.
88. Arnett, K. L., Harrison, S. C., and Wiley, D. C. (2004) Crystal structure of a human CD3-epsilon/delta dimer in complex with a UCHT1 single-chain antibody fragment. Proc. Natl. Acad. Sci. USA 101, 16268-16273.