Molecular mechanism of the activation-induced cell death inhibition mediated by a p70 inhibitory killer cell Ig-like receptor in Jurkat T cells

Journal of Immunology

Volumn 169, Issue 7, 2002, Pages 3726-3735

  Chwae, Yong Joon ^a   Chang, Mi Jung ^a   Park, Sang Myun ^a   Yoon, Ho ^a   Park, Hyun Joo ^a   Kim, Se Jong ^a   Kim, Jongsun ^a  

^a Yonsei University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; CD8 ANTIGEN; FAS LIGAND; IONOMYCIN; PHYTOHEMAGGLUTININ; PROTEIN; PROTEIN KINASE C; PROTEIN KIR3DL1; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CELL DEATH; CONTROLLED STUDY; ENZYME INHIBITION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; KILLER CELL; LEUKEMIA CELL LINE; MOLECULAR INTERACTION; MOLECULAR MECHANICS; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION;

EID: 0036784655     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.169.7.3726     Document Type: Article

References (74)

1. Moretta, A., C. Bottino, M. Vitale, D. Pende, R. Biassoni, M. C. Mingari, and L. Moretta, 1996. Receptors for HLA class-I molecules in human natural killer cells. Annu. Rev. Immunol. 14:619.
2. Lanier, L. L. 1998. NK cell receptors. Annu. Rev. Immunol. 16:359.
3. Takei, F., J. Brennan, and D. L. Mager. 1997, The Ly-49 family: genes, proteins and recognition of class I MHC. Immunol. Rev. 155:67.
4. Brooks, A. G., P. E. Posch, C. J. Scorzelli, F. Borrego, and J. E. Coligan. 1997. NKG2A complexed with CD94 defines a novel inhibitory natural killer cell receptor. J. Exp. Med. 185:795.
5. Steffens, U., Y. Vyas, B. Dupont, and A. Selvakumar. 1998, Nucleotide and amino acid sequence alignment for human killer cell inhibitory receptors (KIR). Tissue Antigens 51:398.
6. Colonna, M., F. Navarro, T. Bellon, M. Llano, P. Garcia, J. Samaridis, L. Angman, M. Cella, and M. Lopez-Botet. 1997, A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and myelomonocytic cells. J. Exp. Med. 186:1809.
7. Cosman, D., N. Fanger, L. Borges, M. Kubin, W. Chin, L. Peterson, and M. L. Hsu. 1997. A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules. Immunity 7:273.
8. Ugolini, S., and E. Vivier. 2000. Regulation of T cell function by NK cell receptors for classical MHC class I molecules. Curr. Opin. Immunol. 12:295.
9. Binstadt, B. A., K. M. Brumbaugh, C. J. Dick, A. M. Scharenberg, B. L. Williams, M. Colonna, L. L. Lanier, J. P. Kinet, R. T. Abraham, and P. J. Leibson. 1996. Sequential involvement of Lck and SHP-1 with MHC-recognizing receptors on NK cells inhibits FcR-initiated tyrosine kinase activation. Immunity 5:629.
10. Marti, F., C. W. Xu, A. Selvakumar, R. Brent, B. Dupont, and P. D. King. 1998. LCK-phosphorylated human killer cell-inhibitory receptors recruit and activate phosphatidylinositol 3-kinase. Proc. Natl. Acad. Sci. USA 95:11810.
11. Uhrberg, M., N. M. Valiante, N. T. Young, L. L. Lanier, J. H. Phillips, and P. Parham. 2001. The repertoire of killer cell Ig-like receptor and CD94:NKG2A receptors in T cells: clones sharing identical αβ TCR rearrangement express highly diverse killer cell Ig-like receptor patterns. J. Immunol. 166:3923.
12. Phillips, J. H., J. E. Gumperz, P. Parham, and L. L. Lanier. 1995. Superantigen-dependent, cell-mediated cytotoxicity inhibited by MHC class I receptors on T lymphocytes. Science 268:403.
13. Mingari, M. C., C. Vitale, A. Cambiaggi, F. Schiavetti, G. Melioli, S. Ferrini, and A. Poggi. 1995. Cytolytic T lymphocytes displaying natural killer (NK)-like activity: expression of NK-related functional receptors for HLA class I molecules (p58 and CD94) and inhibitory effect on the TCR-mediated target cell lysis or lymphokine production. Int. Immunol. 7:697.
14. Ferrini, S., A. Cambiaggi, R. Meazza, S. Sforzini, S. Marciano, M. C. Mingari, and L. Moretta. 1994. T cell clones expressing the natural killer cell-related p58 receptor molecule display heterogeneity in phenotypic properties and p58 function. Eur. J. Immunol. 24:2294.
15. D'Andrea, A., and L. L. Lanier. 1998. Killer cell inhibitory receptor expression by T cells. Curr. Top. Microbiol. Immunol. 230:25.
16. Battistini, L., G. Borsellino, G. Sawicki, F. Poccia, M. Salvetti, G. Ristori, and C. F. Brosnan. 1997. Phenotypic and cytokine analysis of human peripheral blood γδ T cells expressing NK cell receptors. J. Immunol. 159:3723.
17. Nakajima, H., H. Tomiyama, and M. Takiguchi. 1995. Inhibition of γδ T cell recognition by receptors for MHC class I molecules. J. Immunol. 155:4139.
18. D'Andrea, A., C. Chang, J. H. Phillips, and L. L. Lanier. 1996. Regulation of T cell lymphokine production by killer cell inhibitory receptor recognition of self HLA class I alleles. J. Exp. Med. 184:789.
19. De Maria, A., A. Ferraris, M. Guastella, S. Pilia, C. Cantoni, L. Polero, M. C. Mingari, D. Bassetti, A. S. Fauci, and L. Moretta. 1997. Expression of HLA class I-specific inhibitory natural killer cell receptors in HIV-specific cytolytic T lymphocytes: impairment of specific cytolytic functions. Proc. Natl. Acad. Sci. USA 94:10285.
20. Halary, F., M. A. Peyrat, E. Champagne, M. Lopez-Botet, A. Moretta, L. Moretta, H. Vie, J. J. Fournie, and M. Bonneville. 1997. Control of self-reactive cytotoxic T lymphocytes expressing γδ T cell receptors by natural killer inhibitory receptors. Eur. J. Immunol. 27:2812.
21. Ikeda, H., B. Lethe, F. Lehmann, N. van Baren, J. F. Baurain, C. de Smet, H. Chambost, M. Vitale, A. Moretta, T. Boon, et al. 1997. Characterization of an antigen that is recognized on a melanoma showing partial HLA loss by CTL expressing an NK inhibitory receptor. Immunity 6:199.
22. Bakker, A. B., J. H. Phillips, C. G. Figdor, and L. L. Lanier. 1998. Killer cell inhibitory receptors for MHC class I molecules regulate lysis of melanoma cells mediated by NK cells, γδ T cells, and antigen-specific CTL. J. Immunol. 160:5239.
23. Speiser, D. E., M. J. Pittet, D. Valmori, R. Dunbar, D. Rimoldi, D. Lienard, H. R. MacDonald, J. C. Cerottini, V. Cerundolo, and P. Romero. 1999. In vivo expression of natural killer cell inhibitory receptors by human melanoma-specific cytolytic T lymphocytes. J. Exp. Med. 190:775.
24. + T lymphocyte subsets that express HLA class I-specific inhibitory receptors represent oligoclonally or monoclonally expanded cell populations. Proc. Natl. Acad. Sci. USA 93:12433.
25. Sallusto, F., D. Lenig, R. Forster, M. Lipp, and A. Lanzavecchia. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401:708.
26. + T cells. Nat. Immunol. 2:430.
27. Young, N. T., M. Uhrberg, J. H. Phillips, L. L. Lanier, and P. Parham. 2001. Differential expression of leukocyte receptor complex-encoded Ig-like receptors correlates with the transition from effector to memory CTL. J. Immunol. 166: 3933.
28. Roger, J., A. Chalifour, S. Lemieux, and P. Duplay. 2001. Cutting edge: Ly49A inhibits TCR/CD3-induced apoptosis and IL-2 secretion. J. Immunol. 167:6.
29. Weiss, A., and D. R. Littman. 1994. Signal transduction by lymphocyte antigen receptors. Cell 76:263.
30. Weiss, A., M. Iwashima, B. Irving, N. S. van Oers, T. A. Kadlecek, D. Straus, and A. Chan. 1994. Molecular and genetic insights into T cell antigen receptor signal transduction. Adv. Exp. Med. Biol. 365:53.
31. Hug, H., and T. F. Sarre. 1993. Protein kinase C isoenzymes: divergence in signal transduction? Biochem. J. 291:329.
32. Dekker, L. V., R. H. Palmer, and P. J. Parker. 1995. The protein kinase C and protein kinase C related gene families. Curr. Opin. Struct. Biol. 5:396.
33. Dekker, L. V., and P. J. Parker. 1994. Protein kinase C: a question of specificity. Trends Biochem. Sci. 19:73.
34. Nishizuka, Y. 1992. Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science 258:607.
35. Nakanishi, H., K. A. Brewer, and J. H. Exton. 1993. Activation of the zeta isozyme of protein kinase C by phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 268:13.
36. Toker, A., M. Meyer, K. K. Reddy, J. R. Falck, R. Aneja, S. Aneja, A. Parra, D. J. Burns, L. M. Ballas, and L. C. Cantley. 1994. Activation of protein kinase C family members by the novel polyphosphoinositides PtdIns-3,4-P2 and PtdIns-3,4,5-P3. J. Biol. Chem. 269:32358.
37. Russell, J. H. 1995. Activation-induced death of mature T cells in the regulation of immune responses. Curr. Opin. Immunol. 7:382.
38. Brunner, T., R. J. Mogil, D. LaFace, N. J. Yoo, A. Mahboubi, F. Echeverri, S. J. Martin, W. R. Force, D. H. Lynch, and C. F. Ware. 1995. Cell-autonomous Fas (CD95)/Fas-ligand interaction mediates activation-induced apoptosis in T-cell hybridomas. Nature 373:441.
39. Dhein, J., H. Walczak, C. Baumler, K. M. Debatin, and P. H. Krammer. 1995. Autocrine T-cell suicide mediated by APO-1/(Fas/CD95). Nature 373:438.
40. Ju, S. T., D. J. Panka, H. Cui, R. Ettinger, M. el-Khatib, D. H. Sherr, B. Z. Stanger, and A. Marshak-Rothstein. 1995. Fas(CD95)/FasL interactions required for programmed cell death after T-cell activation. Nature 373:444.
41. Nagata, S. 1997. Apoptosis by death factor. Cell 88:355.
42. Ashkenazi, A., and V. M. Dixit. 1998. Death receptors: signaling and modulation. Science 281:1305.
43. Norian, L. A., K. M. Latinis, and G. A. Koretzky. 1998. A newly identified response element in the CD95 ligand promoter contributes to optimal inducibility in activated T lymphocytes. J. Immunol. 161:1078.
44. Latinis, K. M., L. L. Carr, E. J. Peterson, L. A. Norian, S. L. Eliason, and G. A. Koretzky. 1997. Regulation of CD95 (Fas) ligand expression by TCR-mediated signaling events. J. Immunol. 158:4602.
45. Rodriguez-Tarduchy, G., A. G. Sahuquillo, B. Alarcon, and R. Bragado. 1996. Apoptosis but not other activation events is inhibited by a mutation in the transmembrane domain of T cell receptor β that impairs CD3 zeta association. J. Biol. Chem. 271:30417.
46. Yahata, T., N. Abe, C. Yahata, Y. Ohmi, A. Ohta, K. lwakabe, S. Habu, H. Yagita, H. Kitamura, N. Matsuki, et al. 1999. The essential role of phorbol ester-sensitive protein kinase C isoforms in activation-induced cell death of Th1 cells. Eur. J. Immunol. 29:727.
47. Villalba, M., S. Kasibhatla, L. Genestier, A. Mahboubi, D. R. Green, and A. Altman. 1999. Protein kinase CO cooperates with calcineurin to induce Fas ligand expression during activation-induced T cell death. J. Immunol. 163:5813.
48. Villunger, A., N. Ghaffari-Tabrizi, I. Tinhofer, N. Krumbock, B. Bauer, T. Schneider, S. Kasibhatla, R. Greil, G. Baier-Bitterlich, F. Uberall, et al. 1999. Synergistic action of protein kinase CO and calcineurin is sufficient for Fas ligand expression and induction of a crmA-sensitive apoptosis pathway in Jurkat T cells. Eur. J. Immunol. 29:3549.
49. Cho, H. I., C. G. Park, and J. Kim. 1999. Reconstitution of killer cell inhibitory receptor-mediated signal transduction machinery in a cell-free model system. Arch. Biochem. Biophys. 368:221.
50. Cho, H. I., C. G. Park, and J. Kim. 1999. The cytoplasmic tail of killer inhibitory receptor (KIR) associates with TCRζ in a phosphorylation-dependent manner. Immunol. Lett. 68:339.
51. D'Andrea, A., C. Chang, K. Franz-Bacon, T. McClanahan, J. H. Phillips, and L. L. Lanier. 1995. Molecular cloning of NKB1: a natural killer cell receptor for HLA-B allotypes. J. Immunol. 155:2306.
52. Irving, B. A., A. C. Chan, and A. Weiss. 1993. Functional characterization of a signal transducing motif present in the T cell antigen receptor @ chain. J. Exp. Med. 177:1093.
53. Shin, E. C., J. S. Shin, J. H. Park, H. Kim, and S. J. Kim. 1999. Expression of Fas ligand in human hepatoma cell lines: role of hepatitis-B virus X (HBX) in induction of Fas ligand. Int. J. Cancer 82:587.
54. - human T cells. J. Immunol. 165:1910.
55. Shi, Y. F., B. M. Sahai, and D. R. Green. 1989. Cyclosporin A inhibits activation-induced cell death in T-cell hybridomas and thymocytes. Nature 339:625.
56. Smith, C. A., G. T. Williams, R. Kingston, E. J. Jenkinson, and J. J. Owen. 1989. Antibodies to CD3/T-cell receptor complex induce death by apoptosis in immature T cells in thymic cultures. Nature 337:181.
57. Wyllie, A. H., R. G. Morris, A. L. Smith, and D. Dunlop. 1984. Chromatin cleavage in apoptosis: association with condensed chromatin morphology and dependence on macromolecular synthesis. J. Pathol. 142:67.
58. Muller. C., A. Ziegler, G. Muller, F. Schunter, and P. Wernet, 1982. Monoclonal antibody (Tu48) defining alloantigenic class I determinants specific for HLA-Bw4 and HLA-Aw23, -Aw24 as well as -Aw32. Hunt. Immunol. 5:269.
59. Radka, S. F., D. D. Kostyu, and D. B. Amos. 1982. A monoclonal antibody directed against the HLA-Bw6 epitope. J. Immunol. 128:2804.
60. Wong, B., and Y. Choi. 1997. Pathways leading to cell death in T cells. Curr. Opin. Immunol. 9:358.
61. Anel, A., M. Bufeme, C. Boyer, A. M. Schmitt-Verhulst, and P. Golstein. 1994. T cell receptor-induced Fas ligand expression in cytotoxic T lymphocyte clones is blocked by protein tyrosine kinase inhibitors and cyclosporin A. Eur. J. Immunol. 24:2469.
62. Littlebury, P., J. Watson, T. Williams, G. Beale, and M. Rumsby. 1997. Protein expression of the epsilon subspecies of protein kinase C ceases as Swiss 3T6 fibroblasts increase in cell density even though message for the protein is still present. FEBS Lett. 400:304.
63. 0 by contact inhibition in the presence of serum. Biochem. Soc. Trans. 23:446.
64. Nakaseko, C., S. Miyatake, T. Iida, S. Hara, R. Abe, H. Ohno, Y. Saito, and T. Saito. 1999. Cytotoxic T lymphocyte antigen 4 (CTLA-4) engagement delivers an inhibitory signal through the membrane-proximal region in the absence of the tyrosine motif in the cytoplasmic tail. J Exp. Med. 190:765.
65. Ward, N. E., K. R. Gravitt, and C. A. O'Brian. 1995. Irreversible inactivation of protein kinase C by a peptide-substrate analog. J. Biol. Chem. 270:8056.
66. Khoshnan, A., D. Bae, C. A. Tindell, and A. E. Nel. 2000. The physical association of protein kinase Cθ with a lipid raft-associated inhibitor of kappa B factor kinase (IKK) complex plays a role in the activation of the NF-κB cascade by TCR and CD28. J. Immunol. 165:6933.
67. Ghaffari-Tabrizi, N., B, Bauer, A, Villunger, G. Baier-Bittertich, A. Altman, G. Utermanm F. Uberall, and G. Baier, 1999. Protein kinase CO. a selective upstream regulator of JNK/SAPK and IL-2 promoter activation in Jurkat T cells. Eur. J. Immunol. 29:132.
68. Baier-Bitterlich, G., F. Uberall, B. Bauer, F. Fresser, H. Wachter, H. Grunicke, G. Utermann, A. Altman, and G. Baier. 1996. Protein kinase C-θ isoenzyme selective stimulation of the transcription factor complex AP-1 in T lymphocytes. Mol. Cell. Biol. 16:1842.
69. Izquierdo, M., S. J. Leevers, D. H. Williams, C. J. Marshall, A. Weiss, and D. Cantrell. 1994. The role of protein kinase C in the regulation of extracellular signal-regulated kinase by the T cell antigen receptor. Eur. J. Immunol. 24:2462.
70. Bertolotto, C., L. Maulon, N. Filippa, G. Baier, and P. Auberger. 2000. Protein kinase CO and epsilon promote T-cell survival by a rsk-dependent phosphorylation and inactivation of BAD. J. Biol. Chem. 275:37246.
71. Villalba, M., P. Bushway, and A. Altman. 2001. Protein kinase C-θ mediates a selective T cell survival signal via phosphorylation of BAD. J. Immunol. 166:5955.
72. + and cell shrinkage: a role for PKC upstream of caspases. J. Biol. Chem. 275:19609.
73. + T cells is controlled by T-cell receptor engagement. Nature 403:325.
74. Cambiaggi, A., S. Darche, S. Guia, P. Kourilsky, J. P. Abastado, and E. Vivier. 1999. Modulation of T-cell functions in KIR2DL3 (CD158b) transgenic mice. Blood 94:2396.