Expression and function of NKG2D in CD4+ T cells specific for human cytomegalovirus

European Journal of Immunology

Volumn 36, Issue 12, 2006, Pages 3198-3206

  Sáez Borderías, Andrea ^a   Gumá, Mónica ^a   Angulo, Ana ^b   Bellosillo, Beatriz ^a   Pende, Daniela ^c   López Botet, Miguel ^a  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^c UNIVERSITY OF GENOA   (Italy)

Author keywords

Cytomegalovirus; GD85j; KIR; NKG2D; T cell

Indexed keywords

CD28 ANTIGEN; CD4 ANTIGEN; CD94 ANTIGEN; GAMMA INTERFERON; HLA ANTIGEN CLASS 2; MONOCLONAL ANTIBODY; NATURAL KILLER CELL RECEPTOR; NATURAL KILLER CELL RECEPTOR NKG2D; PERFORIN; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOMEGALOVIRUS; HUMAN; HUMAN CELL; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; VIRUS IMMUNITY;

ADULT; CD4-POSITIVE T-LYMPHOCYTES; CELL LINE; CELLS, CULTURED; CYTOMEGALOVIRUS; EPITOPES, T-LYMPHOCYTE; HUMANS; RECEPTORS, IMMUNOLOGIC; T-LYMPHOCYTE SUBSETS;

EID: 33845593312     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200636682     Document Type: Article

References (60)

1. Vilches, C. and Parham, P., KIR: diverse, rapidly evolving receptors of innate and adaptive immunity. Annu. Rev. Immunol. 2002. 20: 217-251.
2. Moretta, A., Bottino, C., Vitale, M., Pende, D., Cantoni, C., Mingari, M. C., Biassoni, R. and Moretta, L., Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu. Rev. Immunol. 2001. 19: 197-223.
3. 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
4. Lanier, L. L., Natural killer cell receptor signaling. Curr. Opin. Immunol. 2003. 15: 308-314.
5. Raulet, D. H., Interplay of natural killer cells and their receptors with the adaptive immune response. Nat. Immunol. 2004. 5: 996-1002.
6. 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.
7. Mingari M. C., Moretta, A. and Moretta, I., Regulation of KIR expression in human T cells: a safety mechanism that may impair protective T-cell responses. Immunol. Today 1998. 19: 153-157.
8. 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.
9. Antrobus, R. D., Khan, N., Hislop, A. D., Montamat-Sicotte, D., Garner, L. I., Rickinson, A. B., Moss, P. A. and Willcox, B. E., Virus-specific cytotoxic T lymphocytes differentially express cell-surface leukocyte immunoglobulin-like receptor-1, an inhibitory receptor for class I major histocompatibility complex molecules. J. Infect. Dis. 2005. 191: 1842-1853.
10. Ince, M. N., Harnisch, B., Xu, Z., Lee, S. K., Lange, C., Moretta, L., Lederman, M. and Lieberman, J., Increased expression of the natural killer cell inhibitory receptor CD85j/ILT2 on antigen-specific effector CD8 T cells and its impact on CD8 T-cell function. Immunology 2004. 112: 531-542.
11. + T cells is controlled by T-cell receptor engagement. Nature 2000. 403: 325-328.
12. + T cells. Curr. Opin. Immunol. 2001. 13: 465-470.
13. + T cells. Eur. J. Immunol. 2005. 35: 2071-2080.
14. Mandelboim, C., Kent, S., Davis, D. M., Wilson, S. B., Okazaki, T., Jackson, R., Hafter, 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.
15. Snyder, M. R., Weyand, C. M. and Goronzy, J. J., The double life of NK receptors: stimulation or co-stimulation? Rends Immunol. 2004. 25: 25-32.
16. Bauer, S., Groh, V., Wu, J., Steinle, A., Phillips, J. H., Lanier, L. L., and Spies, T., Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 1999. 285: 727-729.
17. Wu, J., Song, Y., Bakker, A. B., Bauer, S., Spies, T., Lanier, L. L., and Phillips, J. H., An activating immunoreceptor complex formed by NKG2D and DAP10. Science 1999. 285: 730-732.
18. Groh, 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.
19. Raulet, D. H., Roles of the NKG2D immunoreceptor and its ligands. Nat Rev. Immunol. 2003. 3: 781-790.
20. Billadeau, D. D., Upshaw, J. L., Schoon, R. A., Dick, C. J. and Leibson, P. J., NKG2D-DAP10 triggers human NK cell-mediated killing via a Syk-independent regulatory pathway. Nat. Immunol. 2003. 4: 557-564.
21. Meresse, B., Chen, Z., Ciszewski, C., Tretiakova, M., Bhagat, G., Krausz, T. N., Raulet, D. H. et al., Coordinated induction by EL15 of a TCR-independent NKG2D signaling pathway converts CTL into lymphokine-activated killer cells in celiac disease. Immunity 2004. 21: 357-366.
22. Cosman, D., Mullberg, J., Sutherland, C. L., Chin, W., Armitage, R., Fanslow, W., Kubin, M. and Chalupny, N. J., ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 2001. 14: 123-133.
23. Pende, D., Cantoni, C., Rivera, P., Vitale, M., Castriconi R., Marcenaro, S., Nanni, M. et al., Role of NKG2D in tumor cell lysis mediated by human NK cells: cooperation with natural cytotoxicity receptors and capability of recognizing tumors of nonepithelial origin. Eur. J. Immunol. 2001. 31: 1076-1086.
24. Bacon, L, Eagle, R. A., Meyer, M., Easom, N., Young, N. T. and Trowsdale, J., Two human ULBP/RAET1 molecules with transmembrane regions are ligands for NKG2D. J. Immunol. 2004. 173: 1078-1084.
25. Chalupny, N. J., Sutherland, C. L., Lawrence, W. A., Rein-Weston, A. and Cosman, D., ULBP4 is a novel ligand for human NKG2D. Biochem. Biophys. Res. Commun. 2003. 305: 129-135.
26. González, S., Groh, V. and Spies, T., Immunobiology of human NKG2D and its ligands. Curr. Top. Microbiol. Immunol. 2006. 298: 121-138.
27. Valés-Gómez, M., Browne, H. and Reyburn, H. T., Expression of the UL16 glycoprotein of Human Cytomegalovirus protects the Virus-infected cell from attack by natural killer cells. BMC Immunol. 2003. 4: 4.
28. Welte, S. A., Sinzger, C., Lutz, S. Z., Singh-Jasuja, H., Sampaio, K. L., Eknigk, U., Rammensee, H. G. and Steinle, A., Selective intracellular retention of virally induced NKG2D ligands by the human cytomegalovirus UL16 glycoprotein. Eur. J. Immunol. 2003. 33: 194-203.
29. Rolle, A., Mousavi-Jazi M., Eriksson, M., Odeberg, J., Soderberg-Naucler, C., Cosman, D., Karre, K. and Cerboni, C., Effects of human cytomegalovirus infection on ligands for the activating NKG2D receptor of NK cells: up-regulation of UL16-binding protein (U1BP)1 and ULBP2 is counteracted by the viral UL16 protein. J. Immunol. 2003. 171: 902-908.
30. Chalupny, N. J., Rein-Weston, A., Dosch, S. and Cosman D., Down-regulation of the NKG2D ligand MICA by the human cytomegalovirus glycoprotein UL142. Biochem. Biophys. Res. Commun. 2006. 346: 175-181.
31. Groh, V., Bruhl, A., El Gabalawy, H., Nelson, J. L. and Spies, T., Stimulation of T cell autoreactivity by anomalous expression of NKG2D and its MIC ligands in rheumatoid arthritis. Proc. Natl. Acad. ScL USA 2003. 100: 9452-9457.
32. Groh, V., Smythe, FL, Dai, Z. and Spies, T., Fas ligand-mediated paracrine T cell regulation by the receptor NKG2D in tumor immunity. Nat. Immunol. 2006. 7: 755-762.
33. Goronzy, J. J. and Weyand, C. K, Rheumatoid arthritis. Immunol. Rev. 2005. 204: 55-73.
34. Azimi N., Jacobson, S., Tanaka, Y., Corey, L, Groh, V. and Spies, T., Immunostimulation by induced expression of NKG2D and its MIC ligands in HTLV-1-associated neurologic disease. Immunogenetics 2006. 58: 252-258.
35. + memory T cell response to cytomegalovirus. J. Immunol. 2001. 167: 1151-1163.
36. Gumá, M., Angulo, &, 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.
37. Roberts, A. L, Lee, L, Schwarz E., Groh, V., Spies, T., Ebert, E. C. and Jabri, B., NKG2D receptors induced by IL-15 costimulate CD28-negative effector CTL in the tissue microenviromnent. J. Immunol. 2001. 167: 5527-5530.
38. De Maria, A. and Moretta, L, HLA class I-specific inhibitory receptors in HIV-1 infection. Hum. Immunol. 2000. 61: 74-81.
39. Berg L, Riise, G. C., Cosman D., Bergstrom, T., Olofsson, S., Karre, V. and Carbone, E.. LIR-1 expression on lymphocytes, and cytomegalovirus disease in lung-transplant recipients. Lancet 2003. 361: 1099-1101.
40. + T-cell clones specific for Mycobacterium tuberculosis. Infect. Immun. 2001. 69: 6022-6029.
41. Cosman, D., Fanger, N., Borges, L, Kubin, M., Chin, W., Peterson, L and Hsu, M. L., A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules. Immunity 1997. 7: 273-282.
42. Colonna, M., Navarro, F., Bellón, T., Llano, M., García, P., Samaridis, J., Angman L. et al., A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and myelomonocytic cells. J. Exp. Med 1997. 186: 1809-1818.
43. +, cytomegalovirus-specific T cell subset after recovery of primary cytomegalovirus infection. J. Immunol. 2004. 173: 1834-1841.
44. Rentenaar, R. J., Gamadia, L. E., van DerHoek, N., van Diepen, F. N., Boom, R., Weel, J. F., Wertheim-van Dillen, P. M. et al., Development of virus-specific CD4(+) T cells during primary cytomegalovirus infection. J. Clin. Invest. 2000, 105: 541-548.
45. Gamadia, L. E., Rentenaar, R. J., van Lier, R. A. and ten Berge, I. J., Properties of CD4(+) T cells in human cytomegalovirus infection. Hum. Immunal. 2004. 65: 486-492.
46. + T cells in healthy carriers are continuously driven to replicative exhaustion. J. Immunol. 2005. 175: 8218-8225.
47. Gumá, M., Angulo, A. and López-Botet, M., NK cell receptors involved in the response to human cytomegalovirus infection. Curr. Top. Microbiol. Immunol. 2006. 298: 207-223.
48. Moss, P. and Khan, N., CD8(+) T-cell immunity to cytomegalovirus. Hum. Immunol. 2004. 65: 456-464.
49. + T-cell clones specifically activated by IE1 peptides in vitro. J. Virol. 1996. 70: 2162-2169.
50. Kern, F., Bunde, T., Faulhaber, N., Kiecker, F., Khatamzas, E., Rudawski, I. M., Pruss, A. et al., Cytomegalovirus (CMV) phosphoprotein 65 makes a large contribution to shaping the T cell repertoire in CMV-exposed individuals. J. Infect. Dis. 2002. 185: 1709-1716.
51. Li, P. G., Bottone, L, Ivaldi, F., Tagliamacco, A., Fiordoro, S., Ricciardi, A., Barbano, G. and Manca, F., Generation of cytomegalovirus (CMV)- specific CD4 T cell lines devoid of alloreactivity, by use of a mixture of CMV- phosphoprotein 65 peptides for reconstitution of the T helper repertoire. J. Infect. Dis. 2005. 191: 215-226.
52. + CTL. J. Exp. Med. 2005. 202: 1109-1119.
53. Hegde N. R., Chevalier, M. S. and Johnson, D. C., Viral inhibition of MHC class II antigen presentation. Trends Immunol. 2003. 24: 278-285.
54. Koch, S., Solana, R., Dela, R. O. and Pawelec, G., Human cytomegalovirus infection and T cell immunosenescence: a mini review. Mech. Ageing Dev. 2006. 127: 538-543.
55. Eagle, R. A., Traherne, J. A., Ashiru, O., Wills, M. R. and Trowsdale J., Regulation of NKG2D ligand gene expression. Hum. Immunol. 2006. 67: 159-169.
56. Gasser, S., Orsulic, S., Brown, E. J. and Raulet, D. H., The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 2005. 436: 1186-1190.
57. Cerwenka, A. and Lanier, L. L., Natural killer cells, viruses and cancer. Nat. Rev. Immunol. 2001. 1: 41-49.
58. Ogasawara, YL, Hamerman, J. A., Ehrlich, L. R., Bour-Jordan, H., Santamaria, P., Bluestone, J. A. and Lanier, L. L., NKG2D blockade prevents autoimmune diabetes in NOD mice. Immunity 2004. 20: 757-767.
59. + NK cells in response to human cytomegalovirus-infected fibroblasts. Blood 2006. 107: 3624-3631.
60. Ríncón, M., Tugores, A. and López-Botet, M., Cyclic AMP and calcium regulate at a transcriptional level the expression of the CD7 leukocyte differentiation antigen. J. Biol. Chem. 1992. 267: 18026-18031.