Activation and selection of NK cells via recognition of an allogeneic, non-classical MHC class I molecule, RT1-E

European Journal of Immunology

Volumn 29, Issue 11, 1999, Pages 3663-3673

  Petersson, Eva ^a   Holmdahl, Rikard ^a   Butcher, Geoffrey W ^b   Hedlund, Gunnar ^a,c  

^a LUND UNIVERSITY   (Sweden)

^b BABRAHAM INSTITUTE   (United Kingdom)

^c Active Biotech Research AB   (Sweden)

Author keywords

MHC class Ib; NK cell; Selective activation

Indexed keywords

COMPLEMENTARY DNA; LYMPHOCYTE RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN RECOGNITION; ARTICLE; CELL SELECTION; CONTROLLED STUDY; CYTOLYSIS; DNA TRANSFECTION; FIBROBLAST; HAPLOTYPE; IMMUNIZATION; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; RAT; T LYMPHOCYTE ACTIVATION; TARGET CELL;

EID: 0032723675     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1521-4141(199911)29:11<3663::AID-IMMU3663>3.0.CO;2-F     Document Type: Article

References (64)

1. Kiessling, R., Hochman, P. S., Haller, O., Shearer, G. M., Wigzell, H. and Cudkowicz, G., Evidence for a similar or common mechanism for natural killer cell activity and resistance to hemopoietic grafts. Eur. J. Immunol. 1977. 7: 655-663.
2. Rolstad, B., Fossum, S., Bazin, H., Kimber, I., Marshall, J., Sparshott, S. M. and Ford, W. L., The rapid rejection of allogeneic lymphocytes by a non-adaptive, cell-mediated mechanism (NK activity). Immunology 1985. 54: 127-138.
3. Trinchieri, G., Biology of natural killer cells. Adv. Immunol. 1989. 47: 187-376.
4. Karre, K., Ljunggren, H. G., Piontek, G. and Kiessling, R., Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 1986. 319: 675-678.
5. Ljunggren, H. G. and Karre, K., In search of the 'missing self: MHC molecules and NK cell recognition. Immunol. Today 1990. 11: 237-244.
6. Storkus, W. J., Salter, R. D., Alexander, J., Ward, F. E., Ruiz, R. E., Cresswell, P. and Dawson, J. R., Class I-induced resistance to natural killing: identification of nonpermissive residues in HLA-A2. Proc. Natl. Acad. Sci. USA 1991. 88: 5989-5992.
7. Karlhofer, F. M., Ribaudo, R. K. and Yokoyama, W. M., MHC class I alloantigen specificity of Ly-49+ IL-2-activated natural killer cells. Nature 1992. 358: 66-70.
8. Yokoyama, W. M. and Seaman, W. E., The Ly-49 and NKR-P1 gene families encoding lectin-like receptors on natural killer cells: the NK gene complex. Annu. Rev. Immunol. 1993. 11: 613-635.
9. Ryan, J. C. and Seaman, W. E., Divergent functions of lectin-like receptors on NK cells. Immunol. Rev. 1997, 155: 79-89.
10. Lanier, L. L., Natural killer cells: from no receptors to too many. Immunity 1997. 6: 371-378.
11. Lazetic, S., Chang, C., Houchins, J. P., Lanier, L. L. and Phillips, J. H., Human natural killer cell receptors involved in MHC class I recognition are disulfide-linked heterodimers of CD94 and NKG2 subunits. J. Immunol. 1996. 157: 4741-4745.
12. Brooks, A. G., Posch, P. E., Scorzelli, C. J., Borrego, F. and Coligan, J. E., NKG2A complexed with CD94 defines a novel inhibitory natural killer cell receptor. J. Exp. Med. 1997. 185: 795-800.
13. Carretero, M., Cantoni, C., Bellon, T., Bottino, C., Biassoni, R., Rodriguez, A., Perez-Villar, J. J., Moretta, L., Moretta, A. and Lopez-Botet, M., 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. 1997. 27: 563-567.
14. Colonna, M. and Samaridis, J., Cloning of immunoglobulin-superfamily members associated with HLA-C and HLA-B recognition by human natural killer cells. Science 1995. 268: 405-408.
15. Wagtmann, N., Biassoni, R., Cantoni, C., Verdiani, S., Malnati, M. S., Vitale, M., Bottino, C., Moretta, L., Moretta, A. and Long, E. O., Molecular clones of the p58 NK cell receptor reveal immunoglobulin-related molecules with diversity in both the extra- and intracellular domains. Immunity 1995. 2: 439-449.
16. Moretta, A., Bottino, C., Vitale, M., Pende, D., Biassoni, R., Mingari, M. C. and Moretta, L., Receptors for HLA class-I molecules in human natural killer cells. Annu. Rev. Immunol. 1996. 14: 619-648.
17. Dissen, E., Berg, S. F., Westgaard, I. H. and Fossum, S., Molecular characterization of a gene in the rat homologous to human CD94. Eur. J. Immunol. 1997. 27: 2080-2086.
18. Berg, S. F., Dissen, E., Westgaard, I. H. and Fossum, S., Two genes in the rat homologous to human NKG2. Eur. J. Immunol. 1998. 28: 444-450.
19. Naper, C., Ryan, J. C., Nakamura, M. C., Lambracht, D., Rolstad, B. and Vaage, J. T., Identification of an inhibitory MHC receptor on alloreactive rat natural killer cells. J. Immunol. 1998. 160: 219-224.
20. Houchins, J. P., Lanier, L. L., Niemi, E. C., Phillips, J. H. and Ryan, J. C., Natural killer cell cytolytic activity is inhibited by NKG2-A and activated by NKG2-C. J. Immunol. 1997. 158: 3603-3609.
21. Cantoni, C., Biassoni, R., Pende, D., Sivori, S., Accame, L., Pareti, L., Semenzato, G., Moretta, L., Moretta, A. and Bottino, C., The activating form of CD94 receptor complex: CD94 covalently associates with the Kp39 protein that represents the product of the NKG2-C gene. Eur. J. Immunol. 1998. 28: 327-338.
22. Mason, L. H., Anderson, S. K., Yokoyama, M. W., Smith, H. R., Winkler-Pickett, R. and Ortaldo, J. R., The Ly-49D receptor activates murine natural killer cells. J. Exp. Med. 1996. 184: 2119-2128.
23. Moretta, A., Sivori, S., Vitale, M., Pende, D., Morelli, L., Augugliaro, R., Bottino, C. and Moretta, L., Existence of both inhibitory (p58) and activatory (p50) receptors for HLA-C molecules in human natural killer cells. J. Exp. Med. 1995. 182: 875-884.
24. Biassoni, R., Cantoni, C., Falco, M., Verdiani, S., Bottino, C., Vitale, M., Conte, R., Poggi, A., Moretta, A. and Moretta, L., The human leukocyte antigen (HLA)-C-specific "activatory" and "inhibitory" natural killer cell receptors display highly homologous extracellular domains but differ in their transmembrane and intracytoplasmic portions. J. Exp. Med. 1996. 183: 645-650.
25. Nakamura, M. C., Linnemeyer, P. A., Niemi, E. C., Mason, L. H., Ortaldo, J. R., Ryan, J. C. and Seaman, W. E., Mouse Ly-49D recognizes H-2Dd and activates natural killer cell cytotoxicity. J. Exp. Med. 1999. 189: 493-500.
26. Vaage, J. T., Dissen, E., Ager, A., Fossum, S. and Rolstad, B., Allospecific recognition of hemic cells in vitro by natural killer cells from athymic rats: evidence that allodeterminants coded for by single major histocompatibility complex haplotypes are recognized. Eur. J. Immunol. 1991. 21: 2167-2175.
27. Rolstad, B., Vaage, J. T., Naper, C., Lambracht, D., Wonigeit, K., Joly, E. and Butcher, G. W., Positive and negative MHC class I recognition by rat NK cells. Immunol.Rev. 1997. 155: 91-104.
28. Gunther, E., Current status of the molecular genetic analysis of the rat major histocompatibility complex. Folia Biol. (Praha) 1996. 42: 129-145.
29. Gunther, E. and Wurst, W., Cytotoxic T lymphocytes of the rat are predominantly restricted by RT1.A and not RT1.C-determined major histocompatibility class I antigens. Immunogenetics 1984. 20: 1-12.
30. Lambracht, D. and Wonigeit, K., Sequence analysis of the promoter regions of the classical class I gene RT1.A1 and two other class I genes of the rat MHC. Immunogenetics 1995. 41: 375-379.
31. Wang, C. R., Livongstone, A., Butcher, G. W., Hermel, E., Howard J. C. and Fischer Lindahl, K., Antigen presentation by neoclassical MHC class I gene products in murine rodents. In Klein, J. and Klein, D. (Eds.) Molecular evolution of the major histocompatibility complex. NATO ASI Series, Vol. H59. Springer, Berlin 1991, pp 441-462.
32. Jameson, S. C., Tope, W. D., Tredgett, E. M., Windle, J. M., Diamond, A. G. and Howard, J. C., Cloning and expression of class I major histocompatibility complex genes of the rat. J. Exp. Med. 1992. 175: 1749-1757.
33. Ericsson, P. O., Hansson, J., Dohlsten, M., Sjogren, H. O., Hiserodt, J. C. and Hedlund, G., In vivo induced allo-reactive natural killer cells. J. Immunol. 1992. 149: 1504-1509.
34. Petersson, E., Qi, Z., Ekberg, H., Ostraat, O., Dohlsten, M. and Hedlund, G., Activation of alloreactive natural killer cells is resistant to cyclosporine. Transplantation 1997. 63: 1138-1144.
35. Lovik, G., Vaage, J. T., Naper, C., Benestad, H. B. and Rolstad, B., Recruitment of alloreactive natural killer cells to the rat peritoneum by a transfected cell line secreting rat recombinant interleukin-2. J. Immunol. Methods 1995. 179: 59-69.
36. Ciccone, E., Viale, O., Pende, D., Malnati, M., Biassoni, R., Melioli, G., Moretta, A., Long, E. O. and Moretta, L., Specific lysis of allogeneic cells after activation of CD3- lymphocytes in mixed lymphocyte culture. J. Exp. Med. 1988. 168: 2403-2408.
37. Cudkowicz, G. and Bennett, M., Peculiar immunobiology of bone marrow allografts. II. Rejection of parental grafts by resistant F 1 hybrid mice. J. Exp. Med. 1971. 134: 1513-1528.
38. Murphy, W. J., Reynolds, C. W., Tiberghien, P. and Longo, D. L., Natural killer cells and bone marrow transplantation. J. Natl. Cancer Inst. 1993. 85: 1475-1482.
39. Lanier, L. L., Follow the leader: NK cell receptors for classical and nonclassical MHC class I. Cell 1998. 92: 705-707.
40. Long, E. O., Signal sequences stop killer cells. Nature 1998. 391: 740-743.
41. Vaage, J. T., Naper, C., Lovik, G., Lambracht, D., Rehm, A., Hedrich, H. J., Wonigeit, K. and Rolstad, B., Control of rat natural killer cell-mediated allorecognition by a major histocompatibility complex region encoding nonclassical class I antigens. J. Exp. Med. 1994. 180: 641-651.
42. Lopez-Botet, M. and Bellon, T., Natural killer cell activation and inhibition by receptors for MHC class I. Curr. Opin. Immunol. 1999. 11: 301-307.
43. Raziuddin, A., Longi, D. L., Mason, L., Ortaldo, J. R., Bennett, M. and Murphy, W. J., Differential effects of the rejection of bone marrow allografts by the depletion of activating versus inhibiting Ly-49 natural killer cell subsets. J. Immunol. 1998. 160: 87-94.
44. Misra, D. N., Kunz, H. W. and Gill, T. J. D., Analysis of class I MHC antigens in the rat by monoclonal antibodies. J. Immunol. 1985. 134: 2520-2528.
45. Dissen, E., Ryan, J. C., Seaman, W. E. and Fossum, S., An autosomal dominant locus, Nka, mapping to the Ly-49 region of a rat natural killer (NK) gene complex, controls NK cell lysis of allogeneic lymphocytes. J. Exp. Med. 1996. 183: 2197-2207.
46. Smith, K. M., Wu, J., Bakker, A. B., Phillips, J. H. and Lanier, L. L., Cutting edge: Ly-49D and Ly-49H associate with mouse DAP12 and form activating receptors. J. Immunol. 1998. 161: 7-10.
47. Lanier, L. L., Corliss, B. C., Wu, J., Leong, C. and Phillips, J. H., Immunoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells. Nature 1998. 391: 703-707.
48. Parker, K. E., Carter, C. A., Murphy, G. and Fabre, J. W., The rat RT.BM1 MHC class I cDNA shows a high level of sequence similarity to the mouse H-2T23d gene. Immunogenetics 1991. 34: 211-213.
49. 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., HLA-E binds to natural killer cell receptors CD49/NKG2A, B and C. Nature 1998. 391: 795-799.
50. O'Callaghan, C. A., Tormo, J., Willcox, B. E., Braud, V. M., Jakobsen, B. K., Stuart, D. I., McMichael, A. J., Bell, J. I. and Jones, E. Y., Structural features impose tight peptide binding specificity in the nonclassical MHC molecule HLA-E. Mol. Cell 1998. 1: 531-541.
51. Lee, N., Llano, M., Carretero, M., Ishitani, A., Navarro, F., Lopez Botet, M. and Geraghty, D. E., HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc. Natl. Acad. Sci. USA 1998. 95: 5199-5204.
52. Lanier, L. L., Corliss, B., Wu, J. and Phillips, J. H., Association of DAP12 with activating CD94/NKG2C NK cell receptors. Immunity 1998. 8: 693-701.
53. Schulze, F., Winkler, M., Schwinzer, R. and Winogeit, K., Expression of RT1.C antigens on lymphoid cells: analysis by monoclonal antibodies. Transplant. Proc. 1990. 22: 2514-2516.
54. Biron, C. A., Su, H. C. and Orange, J. S., Function and Regulation of Natural Killer (NK) Cells during Viral Infections: Characterization of Responses in vivo. Methods 1996. 9: 379-393.
55. Biron, C. A., Activation and function of natural killer cell responses during viral infections. Curr. Opin. Immunol. 1997. 9: 24-34.
56. Cosman, D., Fanger, N., Borges, L., Kubin, M., Chin, W., Petersson, L. and Hsu, M. L., A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules. Immunity 1997. 7: 273-282.
57. Vitale, M., Castriconi, R., Parolini, S., Pende, D., Hsu, M. L., Moretta, L., Cosman, D. and Moretta, A., The leukocyte Ig-like receptor (LIR)-1 for the cytomegalovirus UL18 protein displays a broad specificity for different HLA class I alleles: analysis for LIR-1 + NK cells clones. Int. Immunol. 1999. 11: 29-35.
58. Joly, E. and Oldstone, M. B., Neuronal cells are deficient in loading peptides onto MHC class I molecules. Neuron 1992. 8: 1185-1190.
59. Joly, E., Clarkson, C., Howard, J. C. and Butcher, G. W., Isolation of a functional cDNA encoding the RT1. Au MHC class I heavy chain by a novel PCR-based method. Immunogenetics 1995. 41: 326-328.
60. Powis, S. J., Young, L. L., Joly, E., Barker, P. J., Richardson, L., Brandt, R. P., Melief, C. J., Howard, J. C. and Butcher, G. W., The rat cim effect: TAP allele-dependent changes in a class I MHC anchor motif and evidence against C-terminal trimming of peptides in the ER. Immunity 1996. 4: 159-165.
61. Salgar, S. K., Kunz, H. W. and Gill III, T. J., Nucleotide sequence and structural analysis of the rat RT1.Eu and RT1.Aw31 genes, and of genes related to RT1.0 and RT1.C. Immunogenetics 1995. 42: 244-253.
62. Hedlund, G., Brodin, T. and Sjogren, H. O., Selective induction of OX19+ (CD5+) or OX19-(CD5-) alloreactive cytolytic lymphocytes in the rat. Cell. Immunol. 1987. 105: 366-373.
63. McKinney, M. M. and Parkinson, A., A simple, non-chromatographic procedure to purify immunoglobulins from serum and ascites fluid. J. Immunol. Methods 1987. 96: 271-278.
64. Augener, W. H. and Grey, M., Studies on the mechanism of heat aggregation of human Ig. J. Immunol. 1970. 105: 1024-1030.