Comprehensive analysis of NKG2D ligand expression and release in leukemia: Implications for NKG2D-mediated NK cell responses

Journal of Immunology

Volumn 189, Issue 3, 2012, Pages 1360-1371

  Hilpert, Julia ^a   Grosse Hovest, Ludger ^a   Grünebach, Frank ^a   Buechele, Corina ^a   Nuebling, Tina ^a   Raum, Tobias ^b   Steinle, Alexander ^c   Salih, Helmut Rainer ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b MICROMET AG   (Germany)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; HLA A ANTIGEN; HLA B ANTIGEN; LYMPHOCYTE ANTIGEN; NATURAL KILLER CELL RECEPTOR NKG2D; NKG2D LIGAND; UL16 BINDING PROTEIN 1; UL16 BINDING PROTEIN 2; UL16 BINDING PROTEIN 3; UNCLASSIFIED DRUG;

ADULT; ANTIGEN EXPRESSION; ANTIGEN FUNCTION; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOREACTIVITY; LEUKEMIA; LEUKEMIA CELL; MAJOR CLINICAL STUDY; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION;

ADULT; CELL LINE, TUMOR; CYTOTOXICITY, IMMUNOLOGIC; DOWN-REGULATION; GPI-LINKED PROTEINS; HUMANS; IMMUNOLOGIC MEMORY; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; KILLER CELLS, NATURAL; LEUKEMIA; MONITORING, IMMUNOLOGIC; T-LYMPHOCYTE SUBSETS;

EID: 84864131272     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200796     Document Type: Article

References (49)

1. Vivier, E., D. H. Raulet, A. Moretta, M. A. Caligiuri, L. Zitvogel, L. L. Lanier, W. M. Yokoyama, and S. Ugolini. 2011. Innate or adaptive immunity? The example of natural killer cells. Science 331: 44-49.
2. Tajima, F., T. Kawatani, A. Endo, and H. Kawasaki. 1996. Natural killer cell activity and cytokine production as prognostic factors in adult acute leukemia. Leukemia 10: 478-482. (Pubitemid 26128788)
3. Pierson, B. A., and J. S. Miller. 1996. CD56+bright and CD56+dim natural killer cells in patients with chronic myelogenous leukemia progressively decrease in number, respond less to stimuli that recruit clonogenic natural killer cells, and exhibit decreased proliferation on a per cell basis. Blood 88: 2279-2287. (Pubitemid 26307932)
4. Lowdell, M. W., R. Craston, D. Samuel, M. E. Wood, E. O'Neill, V. Saha, and H. G. Prentice. 2002. Evidence that continued remission in patients treated for acute leukaemia is dependent upon autologous natural killer cells. Br. J. Haematol. 117: 821-827. (Pubitemid 34639242)
5. Ruggeri, L., M. Capanni, E. Urbani, K. Perruccio, W. D. Shlomchik, A. Tosti, S. Posati, D. Rogaia, F. Frassoni, F. Aversa, et al. 2002. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 295: 2097-2100. (Pubitemid 34229476)
6. Moretta, L., F. Locatelli, D. Pende, S. Sivori, M. Falco, C. Bottino, M. C. Mingari, and A. Moretta. 2011. Human NK receptors: from the molecules to the therapy of high risk leukemias. FEBS Lett. 585: 1563-1567.
7. Gasser, S., and D. H. Raulet. 2006. Activation and self-tolerance of natural killer cells. Immunol. Rev. 214: 130-142. (Pubitemid 44707907)
8. Caligiuri, M. A. 2008. Human natural killer cells. Blood 112: 461-469.
9. Orr, M. T., and L. L. Lanier. 2010. Natural killer cell education and tolerance. Cell 142: 847-856.
10. Lanier, L. L. 2005. NK cell recognition. Annu. Rev. Immunol. 23: 225-274. (Pubitemid 40563170)
11. Bauer, S., V. Groh, J. Wu, A. Steinle, J. H. Phillips, L. L. Lanier, and T. Spies. 1999. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 285: 727-729.
12. Raulet, D. H. 2003. Roles of the NKG2D immunoreceptor and its ligands. Nat. Rev. Immunol. 3: 781-790. (Pubitemid 37328656)
13. Li, P. W., D. L. Morris, B. E. Willcox, A. Steinle, T. Spies, and R. K. Strong. 2001. Complex structure of the activating immunoreceptor NKG2D and its MHC class I-like ligand MICA. Nat. Immunol. 2: 443-451. (Pubitemid 33706143)
14. Steinle, A., P. W. Li, D. L. Morris, V. Groh, L. L. Lanier, R. K. Strong, and T. Spies. 2001. Interactions of human NKG2D with its ligands MICA, MICB, and homologs of the mouse RAE-1 protein family. Immunogenetics 53: 279-287. (Pubitemid 32678762)
15. Champsaur, M., and L. L. Lanier. 2010. Effect of NKG2D ligand expression on host immune responses. Immunol. Rev. 235: 267-285.
16. Eagle, R. A., and J. Trowsdale. 2007. Promiscuity and the single receptor: NKG2D. Nat. Rev. Immunol. 7: 737-744. (Pubitemid 47327391)
17. Cerwenka, A., J. L. Baron, and L. L. Lanier. 2001. Ectopic expression of retinoic acid early inducible-1 gene (RAE-1) permits natural killer cell-mediated rejection of a MHC class I-bearing tumor in vivo. Proc. Natl. Acad. Sci. USA 98: 11521-11526. (Pubitemid 32928761)
18. Diefenbach, A., E. R. Jensen, A. M. Jamieson, and D. H. Raulet. 2001. Rae1 and H60 ligands of the NKG2D receptor stimulate tumour immunity. Nature 413: 165-171. (Pubitemid 32867877)
19. Salih, H. R., H. G. Rammensee, and A. Steinle. 2002. Cutting edge: downregulation of MICA on human tumors by proteolytic shedding. J. Immunol. 169: 4098-4102. (Pubitemid 35178177)
20. Groh, V., J.Wu, C. Yee, and T. Spies. 2002. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 419: 734-738. (Pubitemid 35177960)
21. Salih, H. R., S. Holdenrieder, and A. Steinle. 2008. Soluble NKG2D ligands: prevalence, release, and functional impact. Front. Biosci. 13: 3448-3456. (Pubitemid 351594695)
22. Steigerwald, J., T. Raum, S. Pflanz, R. Cierpka, S. Mangold, D. Rau, P. Hoffmann, M. Kvesic, C. Zube, S. Linnerbauer, et al. 2009. Human IgG1 antibodies antagonizing activating receptor NKG2D on natural killer cells. MAbs 1: 115-127.
23. Armour, K. L., M. R. Clark, A. G. Hadley, and L. M. Williamson. 1999. Recombinant human IgG molecules lacking Fcgamma receptor I binding and monocyte triggering activities. Eur. J. Immunol. 29: 2613-2624. (Pubitemid 29378132)
24. Salih, H. R., H. Antropius, F. Gieseke, S. Z. Lutz, L. Kanz, H. G. Rammensee, and A. Steinle. 2003. Functional expression and release of ligands for the activating immunoreceptor NKG2D in leukemia. Blood 102: 1389-1396. (Pubitemid 36988048)
25. Baltz, K. M., M. Krusch, A. Bringmann, P. Brossart, F. Mayer, M. Kloss, T. Baessler, I. Kumbier, A. Peterfi, S. Kupka, et al. 2007. Cancer immunoediting by GITR (glucocorticoid-induced TNF-related protein) ligand in humans: NK cell/tumor cell interactions. FASEB J. 21: 2442-2454. (Pubitemid 47230674)
26. Baessler, T., M. Krusch, B. J. Schmiedel, M. Kloss, K. M. Baltz, A. Wacker, H. M. Schmetzer, and H. R. Salih. 2009. Glucocorticoid-induced tumor necrosis factor receptor-related protein ligand subverts immunosurveillance of acute myeloid leukemia in humans. Cancer Res. 69: 1037-1045.
27. Waldhauer, I., and A. Steinle. 2006. Proteolytic release of soluble UL16-binding protein 2 from tumor cells. Cancer Res. 66: 2520-2526.
28. Diermayr, S., H. Himmelreich, B. Durovic, A. Mathys-Schneeberger, U. Siegler, U. Langenkamp, J. Hofsteenge, A. Gratwohl, A. Tichelli, M. Paluszewska, et al. 2008. NKG2D ligand expression in AML increases in response to HDAC inhibitor valproic acid and contributes to allorecognition by NK-cell lines with single KIR-HLA class I specificities. Blood 111: 1428-1436. (Pubitemid 351213430)
29. Poggi, A., S. Catellani, A. Garuti, I. Pierri, M. Gobbi, and M. R. Zocchi. 2009. Effective in vivo induction of NKG2D ligands in acute myeloid leukaemias by all-trans-retinoic acid or sodium valproate. Leukemia 23: 641-648.
30. Sanchez-Correa, B., S. Morgado, I. Gayoso, J. M. Bergua, J. G. Casado, M. J. Arcos, M. L. Bengochea, E. Duran, R. Solana, and R. Tarazona. 2011. Human NK cells in acute myeloid leukaemia patients: analysis of NK cell-activating receptors and their ligands. Cancer Immunol. Immunother. 60: 1195-1205.
31. Kato, N., J. Tanaka, J. Sugita, T. Toubai, Y. Miura, M. Ibata, Y. Syono, S. Ota, T. Kondo, M. Asaka, and M. Imamura. 2007. Regulation of the expression of MHC class I-related chain A, B (MICA, MICB) via chromatin remodeling and its impact on the susceptibility of leukemic cells to the cytotoxicity of NKG2D-expressing cells. Leukemia 21: 2103-2108. (Pubitemid 47423800)
32. Pende, D., G. M. Spaggiari, S. Marcenaro, S. Martini, P. Rivera, A. Capobianco, M. Falco, E. Lanino, I. Pierri, R. Zambello, et al. 2005. Analysis of the receptorligand interactions in the natural killer-mediated lysis of freshly isolated myeloid or lymphoblastic leukemias: evidence for the involvement of the Poliovirus receptor (CD155) and Nectin-2 (CD112). Blood 105: 2066-2073. (Pubitemid 40731793)
33. Nückel, H., M. Switala, L. Sellmann, P. A. Horn, J. Dürig, U. Dührsen, R. Küppers, H. Grosse-Wilde, and V. Rebmann. 2010. The prognostic significance of soluble NKG2D ligands in B-cell chronic lymphocytic leukemia. Leukemia 24: 1152-1159.
34. Sconocchia, G., M. Lau, M. Provenzano, K. Rezvani, W. Wongsena, H. Fujiwara, N. Hensel, J. Melenhorst, J. M. Li, S. Ferrone, and A. J. Barrett. 2005. The antileukemia effect of HLA-matched NK and NK-T cells in chronic myelogenous leukemia involves NKG2D-target-cell interactions. Blood 106: 3666-3672. (Pubitemid 41609209)
35. Boissel, N., D. Rea, V. Tieng, N. Dulphy, M. Brun, J. M. Cayuela, P. Rousselot, R. Tamouza, P. Le Bouteiller, F. X. Mahon, et al. 2006. BCR/ABL oncogene directly controls MHC class I chain-related molecule A expression in chronic myelogenous leukemia. J. Immunol. 176: 5108-5116.
36. Salih, J., J. Hilpert, T. Placke, F. Grünebach, A. Steinle, H. R. Salih, and M. Krusch. 2010. The BCR/ABL-inhibitors imatinib, nilotinib and dasatinib differentially affect NK cell reactivity. Int. J. Cancer 127: 2119-2128.
37. Nowbakht, P., M. C. S. Ionescu, A. Rohner, C. P. Kalberer, E. Rossy, L. Mori, D. Cosman, G. De Libero, and A. Wodnar-Filipowicz. 2005. Ligands for natural killer cell-activating receptors are expressed upon the maturation of normal myelomonocytic cells but at low levels in acute myeloid leukemias. Blood 105: 3615-3622. (Pubitemid 40628208)
38. Sutherland, C. L., N. J. Chalupny, and D. Cosman. 2001. The UL16-binding proteins, a novel family of MHC class I-related ligands for NKG2D, activate natural killer cell functions. Immunol. Rev. 181: 185-192. (Pubitemid 32703406)
39. Sutherland, C. L., N. J. Chalupny, K. Schooley, T. VandenBos, M. Kubin, and D. Cosman. 2002. UL16-binding proteins, novel MHC class I-related proteins, bind to NKG2D and activate multiple signaling pathways in primary NK cells. J. Immunol. 168: 671-679. (Pubitemid 34049567)
40. Guerra, N., Y. X. Tan, N. T. Joncker, A. Choy, F. Gallardo, N. Xiong, S. Knoblaugh, D. Cado, N. M. Greenberg, and D. H. Raulet. 2008. NKG2D-deficient mice are defective in tumor surveillance in models of spontaneous malignancy. Immunity 28: 723. (Pubitemid 351636244)
41. Lu, X. Z., K. Ohata, Y. Kondo, J. L. Espinoza, Z. R. Qi, and S. Nakao. 2010. Hydroxyurea upregulates NKG2D ligand expression in myeloid leukemia cells synergistically with valproic acid and potentially enhances susceptibility of leukemic cells to natural killer cell-mediated cytolysis. Cancer Sci. 101: 609-615.
42. Stern-Ginossar, N., C. Gur, M. Biton, E. Horwitz, M. Elboim, N. Stanietsky, M. Mandelboim, and O. Mandelboim. 2008. Human microRNAs regulate stress-induced immune responses mediated by the receptor NKG2D. Nat. Immunol. 9: 1065-1073.
43. Salih, H. R., D. Goehlsdorf, and A. Steinle. 2006. Release of MICB molecules by tumor cells: mechanism and soluble MICB in sera of cancer patients. Hum. Immunol. 67: 188-195. (Pubitemid 43673929)
44. Waldhauer, I., D. Goehlsdorf, F. Gieseke, T. Weinschenk, M. Wittenbrink, A. Ludwig, S. Stevanovic, H. G. Rammensee, and A. Steinle. 2008. Tumor-associated MICA is shed by ADAM proteases. Cancer Res. 68: 6368-6376.
45. Fernández-Messina, L., O. Ashiru, P. Boutet, S. Agüera-González, J. N. Skepper, H. T. Reyburn, and M. Valés-Gómez. 2010. Differential mechanisms of shedding of the glycosylphosphatidylinositol (GPI)-anchored NKG2D ligands. J. Biol. Chem. 285: 8543-8551.
46. Ashiru, O., P. Boutet, L. Fernández-Messina, S. Agüera-González, J. N. Skepper, M. Valés-Gómez, and H. T. Reyburn. 2010. Natural killer cell cytotoxicity is suppressed by exposure to the human NKG2D ligand MICA*008 that is shed by tumor cells in exosomes. Cancer Res. 70: 481-489.
47. Crane, C. A., S. J. Han, J. J. Barry, B. J. Ahn, L. L. Lanier, and A. T. Parsa. 2010. TGF-beta downregulates the activating receptor NKG2D on NK cells and CD8+ T cells in glioma patients. Neuro-oncol. 12: 7-13.
48. Della Chiesa, M., S. Carlomagno, G. Frumento, M. Balsamo, C. Cantoni, R. Conte, L. Moretta, A. Moretta, and M. Vitale. 2006. The tryptophan catabolite L-kynurenine inhibits the surface expression of NKp46- and NKG2D-activating receptors and regulates NK-cell function. Blood 108: 4118-4125. (Pubitemid 44913283)
49. Siegler, U., C. P. Kalberer, P. Nowbakht, S. Sendelov, S. Meyer-Monard, and A. Wodnar-Filipowicz. 2005. Activated natural killer cells from patients with acute myeloid leukemia are cytotoxic against autologous leukemic blasts in NOD/SCID mice. Leukemia 19: 2215-2222. (Pubitemid 41741617)