The NKG2D ligand ULBP2 is specifically regulated through an invariant chain-dependent endosomal pathway

Journal of Immunology

Volumn 193, Issue 4, 2014, Pages 1654-1665

  Uhlenbrock, Franziska ^a   Hagemann Jensen, Michael ^a   Kehlet, Stephanie ^a   Andresen, Lars ^a   Pastorekova, Silvia ^b   Skov, Søren ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b INSTITUTE OF VIROLOGY   (Slovakia)

Author keywords

[No Author keywords available]

Indexed keywords

INORGANIC ACID; MEMBRANE PROTEIN; MESSENGER RNA; METHYLSELENIC ACID; NATURAL KILLER CELL RECEPTOR NKG2D; PROTEIN KINASE C; PROTEIN MICA; PROTEIN MICB; PROTEIN ULBP2; UNCLASSIFIED DRUG;

ARTICLE; CELL SURFACE; CONTROLLED STUDY; ENDOSOME; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IMMUNE SYSTEM; LYSOSOME; MELANOMA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROTEIN TARGETING; PROTEIN TRANSPORT; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANTIGENS, DIFFERENTIATION, B-LYMPHOCYTE; ANTIGENS, SURFACE; BIOLOGICAL TRANSPORT; CARBAZOLES; CD4-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; DEPSIPEPTIDES; ENDOSOMES; ENZYME INHIBITORS; GPI-LINKED PROTEINS; HEK293 CELLS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HISTOCOMPATIBILITY ANTIGENS CLASS II; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; JURKAT CELLS; LYMPHOCYTE ACTIVATION; MELANOMA; NEOPLASMS; ORGANOSELENIUM COMPOUNDS; PROTEIN KINASE C; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING; TRANSCRIPTION, GENETIC;

EID: 84905964469     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1303275     Document Type: Article

References (54)

1. 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 stressinducible MICA. Science 285: 727-729.
2. Groh, V., A. Bruhl, H. El-Gabalawy, J. L. Nelson, and T. Spies. 2003. Stimulation of T cell autoreactivity by anomalous expression of NKG2D and its MIC ligands in rheumatoid arthritis. Proc. Natl. Acad. Sci. USA 100: 9452-9457.
3. Groh, V., K. Smythe, Z. Dai, and T. Spies. 2006. Fas-ligand-mediated paracrine T cell regulation by the receptor NKG2D in tumor immunity. Nat. Immunol. 7: 755-762.
4. Vivier, E., E. Tomasello, and P. Paul. 2002. Lymphocyte activation via NKG2D: towards a new paradigm in immune recognition? Curr. Opin. Immunol. 14: 306-311.
5. Champsaur, M., and L. L. Lanier. 2010. Effect of NKG2D ligand expression on host immune responses. Immunol. Rev. 235: 267-285.
6. Groh, V., R. Rhinehart, J. Randolph-Habecker, M. S. Topp, S. R. Riddell, and T. Spies. 2001. Costimulation of CD8ab T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nat. Immunol. 2: 255-260.
7. 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.
8. Raffaghello, L., I. Prigione, I. Airoldi, M. Camoriano, I. Levreri, C. Gambini, D. Pende, A. Steinle, S. Ferrone, and V. Pistoia. 2004. Downregulation and/or release of NKG2D ligands as immune evasion strategy of human neuroblastoma. Neoplasia 6: 558-568.
9. Routes, J. M., S. Ryan, K. Morris, R. Takaki, A. Cerwenka, and L. L. Lanier. 2005. Adenovirus serotype 5 E1A sensitizes tumor cells to NKG2D-dependent NK cell lysis and tumor rejection. J. Exp. Med. 202: 1477-1482.
10. Andresen, L., H. Jensen, M. T. Pedersen, K. A. Hansen, and S. Skov. 2007. Molecular regulation of MHC class I chain-related protein A expression after HDAC-inhibitor treatment of Jurkat T cells. J. Immunol. 179: 8235-8242.
11. Bauman, Y., D. Nachmani, A. Vitenshtein, P. Tsukerman, N. Drayman, N. Stern-Ginossar, D. Lankry, R. Gruda, and O. Mandelboim. 2011. An identical miRNA of the human JC and BK polyoma viruses targets the stress-induced ligand ULBP3 to escape immune elimination. Cell Host Microbe 9: 93-102.
12. Nachmani, D., D. Lankry, D. G. Wolf, and O. Mandelboim. 2010. The human cytomegalovirus microRNA miR-UL112 acts synergistically with a cellular microRNA to escape immune elimination. Nat. Immunol. 11: 806-813.
13. Textor, S., N. Fiegler, A. Arnold, A. Porgador, T. G. Hofmann, and A. Cerwenka. 2011. Human NK cells are alerted to induction of p53 in cancer cells by upregulation of the NKG2D ligands ULBP1 and ULBP2. Cancer Res. 71: 5998-6009.
14. Andresen, L., S. L. Skovbakke, G. Persson, M. Hagemann-Jensen, K. A. Hansen, H. Jensen, and S. Skov. 2012. 2-deoxy D-glucose prevents cell surface expression of NKG2D ligands through inhibition of N-linked glycosylation. J. Immunol. 188: 1847-1855.
15. Fuertes, M. B., M. V. Girart, L. L. Molinero, C. I. Domaica, L. E. Rossi, M. M. Barrio, J. Mordoh, G. A. Rabinovich, and N. W. Zwirner. 2008. Intracellular retention of the NKG2D ligand MHC class I chain-related gene A in human melanomas confers immune privilege and prevents NK cell-mediated cytotoxicity. J. Immunol. 180: 4606-4614.
16. Nice, T. J., W. Deng, L. Coscoy, and D. H. Raulet. 2010. Stress-regulated targeting of the NKG2D ligand Mult1 by a membrane-Associated RING-CH family E3 ligase. J. Immunol. 185: 5369-5376.
17. Renszel, K. M., R. S. Traister, and W. P. Lynch. 2013. Unique N-linked glycosylation of CasBrE Env influences its stability, processing, and viral infectivity but not its neurotoxicity. J. Virol. 87: 8372-8387.
18. Welte, S. A., C. Sinzger, S. Z. Lutz, H. Singh-Jasuja, K. L. Sampaio, U. Eknigk, H. G. Rammensee, and A. Steinle. 2003. Selective intracellular retention of virally induced NKG2D ligands by the human cytomegalovirus UL16 glycoprotein. Eur. J. Immunol. 33: 194-203.
19. Paschen, A., A. Sucker, B. Hill, I. Moll, M. Zapatka, X. D. Nguyen, G. C. Sim, I. Gutmann, J. Hassel, J. C. Becker, et al. 2009. Differential clinical significance of individual NKG2D ligands in melanoma: soluble ULBP2 as an indicator of poor prognosis superior to S100B. Clin. Cancer Res. 15: 5208-5215.
20. Song, H., J. Kim, D. Cosman, and I. Choi. 2006. Soluble ULBP suppresses natural killer cell activity via down-regulating NKG2D expression. Cell. Immunol. 239: 22-30.
21. 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.
22. Nuckel, H., M. Switala, L. Sellmann, P. A. Horn, J. Durig, U. Duhrsen, R. Kuppers, H. Grosse-Wilde, and V. Rebmann. 2010. The prognostic significance of soluble NKG2D ligands in B-cell chronic lymphocytic leukemia. Leukemia 24: 1152-1159.
23. Wu, J. D., L. M. Higgins, A. Steinle, D. Cosman, K. Haugk, and S. R. Plymate. 2004. Prevalent expression of the immunostimulatory MHC class I chain-related molecule is counteracted by shedding in prostate cancer. J. Clin. Invest. 114: 560-568.
24. Li, K., M. Mandai, J. Hamanishi, N. Matsumura, A. Suzuki, H. Yagi, K. Yamaguchi, T. Baba, S. Fujii, and I. Konishi. 2009. Clinical significance of the NKG2D ligands, MICA/B and ULBP2 in ovarian cancer: high expression of ULBP2 is an indicator of poor prognosis. Cancer Immunol. Immunother. 58: 641-652.
25. Blum, J. S., P. A. Wearsch, and P. Cresswell. 2013. Pathways of antigen processing. Annu. Rev. Immunol. 31: 443-473.
26. Grybko, M. J., A. T. Pores-Fernando, G. A. Wurth, and A. Zweifach. 2007. Protein kinase C activity is required for cytotoxic T cell lytic granule exocytosis, but the theta isoform does not play a preferential role. J. Leukoc. Biol. 81: 509-519.
27. De Marinis, Y. Z., E. Zhang, S. Amisten, J. Taneera, E. Renström, P. Rorsman, and L. Eliasson. 2010. Enhancement of glucagon secretion in mouse and human pancreatic alpha cells by protein kinase C (PKC) involves intracellular trafficking of PKCa and PKCd. Diabetologia 53: 717-729.
28. Zhao, D., S. Amria, A. Hossain, K. Sundaram, P. Komlosi, M. Nagarkatti, and A. Haque. 2011. Enhancement of HLA class II-restricted CD4+ T cell recognition of human melanoma cells following treatment with bryostatin-1. Cell. Immunol. 271: 392-400.
29. Nikodemova, M., J. J.Watters, S. J. Jackson, S. K. Yang, and I. D. Duncan. 2007. Minocycline down-regulates MHC II expression in microglia and macrophages through inhibition of IRF-1 and protein kinase C (PKC)a/bII. J. Biol. Chem. 282: 15208-15216.
30. Majewski, M., T. O. Bose, F. C. Sillé, A. M. Pollington, E. Fiebiger, and M. Boes. 2007. Protein kinase C d stimulates antigen presentation by class II MHC in murine dendritic cells. Int. Immunol. 19: 719-732.
31. Bikoff, E. K., R. N. Germain, and E. J. Robertson. 1995. Allelic differences affecting invariant chain dependency of MHC class II subunit assembly. Immunity 2: 301-310.
32. Huang, S., S. Gilfillan, S. Kim, B. Thompson, X. Wang, A. J. Sant, D. H. Fremont, O. Lantz, and T. H. Hansen. 2008. MR1 uses an endocytic pathway to activate mucosal-Associated invariant T cells. J. Exp. Med. 205: 1201-1211.
33. Sloma, I., M. T. Zilber, T. Vasselon, N. Setterblad, M. Cavallari, L. Mori, G. De Libero, D. Charron, N. Mooney, and C. Gelin. 2008. Regulation of CD1a surface expression and antigen presentation by invariant chain and lipid rafts. J. Immunol. 180: 980-987.
34. Sillé, F. C., C. Martin, P. Jayaraman, A. Rothchild, G. S. Besra, S. M. Behar, and M. Boes. 2011. Critical role for invariant chain in CD1d-mediated selection and maturation of Va14-invariant NKT cells. Immunol. Lett. 139: 33-41.
35. Brutkiewicz, R. R., C. A. Willard, K. K. Gillett-Heacock, M. R. Pawlak, J. C. Bailey, M. A. Khan, M. Nagala, W. Du, J. Gervay-Hague, and G. J. Renukaradhya. 2007. Protein kinase C d is a critical regulator of CD1dmediated antigen presentation. Eur. J. Immunol. 37: 2390-2395.
36. Neumann, J., and N. Koch. 2006. A novel domain on HLA-DRb chain regulates the chaperone role of the invariant chain. J. Cell Sci. 119: 4207-4214.
37. Marienhagen, J., A. Dennig, and U. Schwaneberg. 2012. Phosphorothioate-based DNA recombination: an enzyme-free method for the combinatorial assembly of multiple DNA fragments. Biotechniques 0: 1-6.
38. Jensen, H., M. Hagemann-Jensen, F. Lauridsen, and S. Skov. 2013. Regulation of NKG2D-ligand cell surface expression by intracellular calcium after HDACinhibitor treatment. Mol. Immunol. 53: 255-264.
39. Skov, S., M. T. Pedersen, L. Andresen, P. T. Straten, A. Woetmann, and N. Odum. 2005. Cancer cells become susceptible to natural killer cell killing after exposure to histone deacetylase inhibitors due to glycogen synthase kinase-3-dependent expression of MHC class I-related chain A and B. Cancer Res. 65: 11136-11145.
40. Chen, Y. C., K. S. Prabhu, A. Das, and A. M. Mastro. 2013. Dietary selenium supplementation modifies breast tumor growth and metastasis. Int. J. Cancer 133: 2054-2064.
41. Yan, L., and L. C. DeMars. 2012. Dietary supplementation with methylseleninic acid, but not selenomethionine, reduces spontaneous metastasis of Lewis lung carcinoma in mice. Int. J. Cancer 131: 1260-1266.
42. Rock, K. L., S. Gamble, and L. Rothstein. 1990. Presentation of exogenous antigen with class I major histocompatibility complex molecules. Science 249: 918-921.
43. Gundimeda, U., J. E. Schiffman, D. Chhabra, J. Wong, A. Wu, and R. Gopalakrishna. 2008. Locally generated methylseleninic acid induces specific inactivation of protein kinase C isoenzymes: relevance to selenium-induced apoptosis in prostate cancer cells. J. Biol. Chem. 283: 34519-34531.
44. Kedei, N., D. J. Lundberg, A. Toth, P. Welburn, S. H. Garfield, and P. M. Blumberg. 2004. Characterization of the interaction of ingenol 3-Angelate with protein kinase C. Cancer Res. 64: 3243-3255.
45. Marinari, U. M., M. Nitti, M. A. Pronzato, and C. Domenicotti. 2003. Role of PKC-dependent pathways in HNE-induced cell protein transport and secretion. Mol. Aspects Med. 24: 205-211.
46. Anderson, H. A., D. T. Bergstralh, T. Kawamura, A. Blauvelt, and P. A. Roche. 1999. Phosphorylation of the invariant chain by protein kinase C regulates MHC class II trafficking to antigen-processing compartments. J. Immunol. 163: 5435-5443.
47. Robinson, J. W., X. Lou, and L. R. Potter. 2011. The indolocarbazole, Gö6976, inhibits guanylyl cyclase-A and-B. Br. J. Pharmacol. 164(2b): 499-506.
48. Gould, C. M., C. E. Antal, G. Reyes, M. T. Kunkel, R. A. Adams, A. Ziyar, T. Riveros, and A. C. Newton. 2011. Active site inhibitors protect protein kinase C from dephosphorylation and stabilize its mature form. J. Biol. Chem. 286: 28922-28930.
49. Goodwin, B. J., J. O. Moore, and J. B. Weinberg. 1984. Specific receptors for phorbol diesters on freshly isolated human myeloid and lymphoid leukemia cells: comparable binding characteristics despite different cellular responses. Blood 63: 298-304.
50. Zeng, L., S. V. Webster, and P. M. Newton. 2012. The biology of protein kinase C. Adv. Exp. Med. Biol. 740: 639-661.
51. Burton, J. D., S. Ely, P. K. Reddy, R. Stein, D. V. Gold, T. M. Cardillo, and D. M. Goldenberg. 2004. CD74 is expressed by multiple myeloma and is a promising target for therapy. Clin. Cancer Res. 10: 6606-6611.
52. Suzuki, K. T., Y. Tsuji, Y. Ohta, and N. Suzuki. 2008. Preferential organ distribution of methylselenol source Se-methylselenocysteine relative to methylseleninic acid. Toxicol. Appl. Pharmacol. 227: 76-83.
53. Fernández-Messina, L., O. Ashiru, S. Agüera-González, H. T. Reyburn, and M. Valés-Gómez. 2011. The human NKG2D ligand ULBP2 can be expressed at the cell surface with or without a GPI anchor and both forms can activate NK cells. J. Cell Sci. 124: 321-327.
54. Qatsha, K. A., C. Rudolph, D. Marmé, C. Schächtele, and W. S. May. 1993. Gö6976, a selective inhibitor of protein kinase C, is a potent antagonist of human immunodeficiency virus 1 induction from latent/low-level- producing reservoir cells in vitro. Proc. Natl. Acad. Sci. USA 90: 4674-4678.