The CD94/NKG2C killer lectin-like receptor constitutes an alternative activation pathway for a subset of CD8+ T cells

European Journal of Immunology

Volumn 35, Issue 7, 2005, Pages 2071-2080

  Gumá, Mónica ^a   Busch, Lisa K ^a   Salazar Fontana, Laura I ^a   Bellosillo, Beatriz ^a   Morte, Carles ^a   García, Pilar ^a   López Botet, Miguel ^a  

^a UNIVERSITAT POMPEU FABRA   (Spain)

Author keywords

CD94 NKG2; Cytotoxicity; HLA E; NK cell 7 T lymphocyte

Indexed keywords

ADAPTOR PROTEIN; CD4 ANTIGEN; CD8 ANTIGEN; CD94 ANTIGEN; CELL RECEPTOR; HLA ANTIGEN CLASS 1; HLA E ANTIGEN; INTERLEUKIN 2 RECEPTOR ALPHA; KILLER CELL ACTIVATING RECEPTOR ASSOCIATED PROTEIN; LYMPHOCYTE ANTIGEN RECEPTOR; LYMPHOCYTE RECEPTOR; MONOCLONAL ANTIBODY; NATURAL KILLER CELL RECEPTOR NKG2C; NATURAL KILLER CELL RECEPTOR NKG2C KILLER LECTIN LIKE RECEPTOR; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; T LYMPHOCYTE RECEPTOR DELTA CHAIN; T LYMPHOCYTE RECEPTOR GAMMA CHAIN; UNCLASSIFIED DRUG;

ANTIBODY SPECIFICITY; ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; ARTICLE; CELL CLONING; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY; EFFECTOR CELL; HUMAN; HUMAN CELL; LYMPHOCYTE PROLIFERATION; LYMPHOMA CELL; NATURAL KILLER CELL; PRECIPITATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION;

ANTIGENS, CD; ANTIGENS, CD94; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; COCULTURE TECHNIQUES; FLOW CYTOMETRY; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA ANTIGENS; HUMANS; KILLER CELLS, NATURAL; LECTINS, C-TYPE; LYMPHOCYTE ACTIVATION; RECEPTORS, IMMUNOLOGIC; RECEPTORS, INTERLEUKIN-2; T-LYMPHOCYTE SUBSETS; TRANSFECTION;

EID: 22544466982     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200425843     Document Type: Article

References (52)

1. Raulet, D. H., Interplay of natural killer cells and their receptors with the adaptive immune response. Nat. Immunol. 2004. 5: 996-1002.
2. Vilches, C. and Parham, P., KIR: diverse, rapidly evolving receptors of innate and adaptive immunity. Annu. Rev. Immunol. 2002. 20: 217-251.
3. Moretta, L., Biassoni, R., Bottino, C., Mingari, M. C. and Moretta, A., Human NK-cell receptors. Immunol. Today 2000. 21: 420-422.
4. López-Botet, M., Bellón, T., Llano, M., Navarro, F., García, P. and de Miguel, M., Paired inhibitory and triggering NK cell receptors for HLA class I molecules. Hum. Immunol. 2000. 61: 7-17.
5. Lanier, L. L., Natural killer cell receptor signaling. Curr. Opin. Immunol. 2003. 15: 308-314.
6. Lee, N., Llano, M., Carretero, M., Ishitani, A., Navarro, F., López-Botet, M. and Geraghty, D., HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc. Natl. Acad. Sci. USA 1998. 95: 5199-5204.
7. 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 CD94/NKG2A, B and C. Nature 1998. 391: 795-799.
8. Borrego, F., Ulbrecht, M., Weiss, E. H., Coligan, J. E. and Brooks, A. G., Recognition of human histocompatibility leukocyte antigen (HLA)-E complexed with HLA class I signal sequence-derived peptides by CD94/NKG2 confers protection from natural killer cell-mediated lysis. J. Exp. Med. 1998. 187: 813-818.
9. Moretta, A., Bottino, C., Vitale, M., Pende, D., Cantoni, C., Mingari, M. C., Blassoni, R. and Moretta, L., Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu. Rev. Immunol. 2001. 19: 197-223.
10. Vivier, E. and Anfossi, N., Inhibitory NK-cell receptors on T cells: witness of the past, actors of the future. Nat. Rev. Immunol. 2004. 4: 190-198.
11. Mingari, M. C., Moretta, A. and Moretta, L., Regulation of KIR expression in human T cells: a safety mechanism that may impair protective T-cell responses. Immunol. Today 1998. 19: 153-157.
12. Young, N. T., Uhrberg, M., Phillips, J. H., Lanier, L. L. and Parham, P., Differential expression of leukocyte receptor complex-encoded Ig-like receptors correlates with the transition from effector to memory CTL. J. Immunol. 2001. 166: 3933-3941.
13. Uhrberg, M., Valiante, N. M., Young, N. T., Lanier, L. L., Phillips, J. H. and Parham, P., The repertoire of killer cell Ig-like receptor and CD94:NKG2A receptors in T cells: clones sharing identical alpha beta TCR rearrangement express highly diverse killer cell Ig-like receptor patterns. J. Immunol. 2001. 166: 3923-3932.
14. Noppen, C., Schaefer, C., Zajac, P., Schutz, A., Kocher, T., Kloth, J., Heberer, M., Colonna, M., De Libero, G. and Spagnoli, G. C., C-type lectin-like receptors in peptide-specific HLA class I-restricted cytotoxic T lymphocytes: differential expression and modulation of effector functions in clones sharing identical TCR structure and epitope specificity. Eur. J. Immunol. 1998. 28: 1134-1142.
15. Poccia, F., Cipriani, B., Vendetti, S., Colizzi, V., Poquet, Y., Battistini, L., Lopez-Botet, M., Fournie, J. J. and Gougeon, M. L., CD94/NKG2 inhibitory receptor complex modulates both anti-viral and anti-tumoral responses of polyclonal phosphoantigen-reactive V gamma 9V delta 2 T lymphocytes. J. Immunol. 1997. 159: 6009-6017.
16. Jabri, B., Selby, J. M., Negulescu, FL, Lee, L., Roberts, A. I., Beavis, A., Lopez-Botet, M., Ebert, E. C. and Winchester, R. J., TCR specificity dictates CD94/NKG2A expression by human CTL. Immunity 2002. 17: 487-499.
17. +) T cells. J. Immunol. 2002. 169: 1444-1452.
18. + T cells expressing NK cell receptors in influenza A virus-infected mice. J. Immunol. 2000. 165: 4964-4969.
19. +) T cell responses. Nat. Immunol. 2002. 3: 189-195.
20. De Maria, A. and Moretta, L., HLA-class I-specific inhibitory receptors in HIV-1 infection. Hum. Immunol. 2000. 61: 74-81.
21. + T cells. Curr. Opin. Immunol. 2001. 13: 465-470.
22. Gröh, V., Rhinehart, R., Randolph-Habecker, J., Topp, M. S., Riddell, S. R. and Spies, T., Costimulation of CD8alphabeta T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nat. Immunol. 2001. 2: 255-260.
23. Raulet, D. H., Roles of the NKG2D immunoreceptor and its ligands. Nat. Rev. Immunol. 2003. 3: 781-790.
24. Meresse, B., Chen, Z., Ciszewski, C., Tretiakova, M., Bhagat, G., Krausz, T. N., Raulet, D. H., Lanier, L. L., Gröh, V., Spies, T. et al., Coordinated induction by IL15 of a TCR-independent NKG2D signaling pathway converts CTL into lymphokine-activated killer cells in celiac disease. Immunity 2004. 21: 357-366.
25. + T cells specific for melanocyte differentiation antigens expresses killer inhibitory receptors (KIR) in healthy donors: evidence for a role of KIR in the control of peripheral tolerance. Eur. J. Immunol. 2000. 30: 1665-1675.
26. Mandelboim, O., Kent, S., Davis, D. M., Wilson, S. B., Okazaki, T., Jackson, R., Hafler, D. and Strominger, J. L., Natural killer activating receptors trigger interferon gamma secretion from T cells and natural killer cells. Proc. Natl. Acad. Sci. USA 1998. 95: 3798-3803.
27. null T cells clonally expanded in rheumatoid arthritis. J. Immunol. 2000. 165: 1138-1145.
28. +) T cells. J. Exp. Med. 2003. 197: 437-449.
29. Snyder, M. R., Nakajima, T., Leibson, P. J., Weyand, C. M. and Goronzy, J., Stimulatory killer Ig-like receptors modulate T cell activation through DAP12-dependent and DAP12-independent mechanisms. J. Immunol. 2004. 173: 3725-3731.
30. Snyder, M. R., Weyand, C. M. and Goronzy, J. J., The double life of NK receptors: stimulation or co-stimulation? Trends Immunol. 2004. 25: 25-32.
31. Gumá, M., Angulo, A., Vilches, C., Gómez-Lozano, N., Malats, N. and López-Botet, M., Imprint of human cytomegalovirus infection on the NK cell receptor repertoire. Blood 2004. 104:3664-3671.
32. 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.
33. Llano, M., Lee, N., Navarro, F., Garcia, P., Albar, J. P., Geraghty, D. E. and López-Botet, M., HLA-E-bound peptides influence recognition by inhibitory and triggering CD94/NKG2 receptors: preferential response to an HLA-G-derived nonamer. Eur. J. Immunol. 1998. 28: 2854-2863.
34. García, P., Llano, M., de Heredia, A. B., Willberg, C. B., Caparrós, E., Aparicio, P., Brand, V. M. and López-Botet, M., Human T cell receptor-mediated recognition of HLA-E. Eur. J. Immunol. 2002. 32: 936-944.
35. Mingari, M. C., Ponte, M., Cantoni, C., Vitale, C., Schiavetti, F., Bertone, S., Bellomo, R., Cappai, A. T. and Biassoni, R., HLA-class I-specific inhibitory receptors in human cytolytic T lymphocytes: molecular characterization, distribution in lymphoid tissues and co-expression by individual T cells. Int. Immunol. 1997. 9: 485-491.
36. + TCR alphabeta lymphocytes. Eur. J. Immunol. 2004. 34: 3456-3464.
37. + T cell clone upon the aggregation of an activatory CD94/kp39 heterodimer. J. Immunol. 1999. 162: 3996-4002.
38. Pietra, G., Romagnani, C., Falco, M., Vitale, M., Castriconi, R., Pende, D., Millo, E., Anfossi, S., Biassoni, R., Moretta, L. and Mingari, M. C., The analysis of the natural killer-like activity of human cytolytic T lymphocytes revealed HLA-E as a novel target for TCR alpha/beta-mediated recognition. Eur. J. Immunol. 2001. 31: 3687-3693.
39. Moretta, L., Romagnani, C., Pietra, G., Moretta, A. and Mingari, M. C., NK-CTLs, a novel HLA-E-restricted T-cell subset. Trends Immunol. 2003. 24: 136-143.
40. André, P., Castriconi, R., Espeli, M., Anfossi, N., Juarez, T., Hue, S., Conway, H., Romagné, F., Dondero, A., Nanni, M. et al., Comparative analysis of human NK cell activation induced by NKG2D and natural cytotoxicity receptors. Eur. J. Immunol. 2004. 34: 961-971.
41. +) T cells in healthy and immunosuppressed virus carriers. Blood 2001. 98: 754-761.
42. López-Botet, M., Angulo, A. and Gumá, M., Natural killer cell receptors for major histocompatibility complex class I and related molecules in cytomegalovirus infection. Tissue Antigens 2004. 63: 195-203.
43. Llano, M., Gumá, M., Ortega, M., Angulo, A. and López-Botet, M., Differential effects of US2, US6 and US11 human cytomegalovirus proteins on HLA class Ia and HLA-E expression: impact on target susceptibility to NK cell subsets. Eur. J. Immunol. 2003. 33: 2744-2754.
44. Tomasec, P., Braud, V. M., Rickards, C., Powell, M. B., McSharry, B. P., Gadola, S., Cerundolo, V., Borysiewicz, L. K., McMichael, A. J. and Wilkinson, G. W., Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 2000. 287: 1031-1033.
45. Wang, E. C., McSharry, B., Retiere, C., Tomasec, P., Williams, S., Borysiewicz, L. K., Brand, V. M. and Wilkinson, G. W., UL40-mediated NK evasion during productive infection with human cytomegalovirus. Proc. Natl. Acad. Sci. USA 2002. 99: 7570-7575.
46. Ulbrecht, M., Martinozzi, S., Grzeschik, M., Hengel, H., Ellwart, J. W., Pla, M. and Weiss, E. H., Cutting edge: the human cytomegalovirus UL40 gene product contains a ligand for HLA-E and prevents NK cell-mediated lysis. J. Immunol. 2000. 164: 5019-5022.
47. Navarro, F., Llano, M., Bellón, T., Colonna, M., Geraghty, D. E. and López-Botet, M., The ILT2(LIR1) and CD94 /NKG2A NK cell receptors, respectively recognize HLA-G1 and HLA-E molecules co-expressed on target cells. Eur. J. Immunol. 1999. 29: 277-283.
48. de Miguel, M. and Lopez-Botet, M., Characterization of monoclonal antibodies specific for receptors of the KIR family. Immunología 2002. 21: 187-193.
49. + T lymphocytes. I. Inhibition of the IL-2-dependent proliferation by anti-Kp43 monoclonal antibody. J. Immunol. 1990. 144: 3238-3247.
50. Lee, N., Goodlett, D. R., Ishitani, A., Marquardt, H. and Geraghty, D. E., HLA-E surface expression depends on binding of TAP-dependent peptides derived from certain HLA class I signal sequences. J. Immunol. 1998. 160: 4951-4960.
51. Pérez-Villar, J. J., Melero, I., Rodríguez, A., Carretero, M., Aramburu, J., Sivori, S., Orengo, A. M., Moretta, A. and López-Botet, M., Functional ambivalence of the Kp43 (CD94) NK cell-associated surface antigen. J. Immunol. 1995. 154: 5779-5788.
52. Bellón, T., Kitzig, F., Sayós, J. and López-Botet, M., Mutational analysis of immunoreceptor tyrosine-based inhibition motifs of the Ig-like transcript 2 (CD85j) leukocyte receptor. J. Immunol. 2002. 168: 3351-3359.