Intracellular sequestration of the NKG2D ligand ULBP3 by human cytomegalovirus

Journal of Immunology

Volumn 185, Issue 2, 2010, Pages 1093-1102

  Bennett, Neil J ^a   Ashiru, Omodele ^b   Morgan, Fiona J E ^a   Pang, Yin ^a   Okecha, Georgina ^a   Eagle, Rob A ^c   Trowsdale, John ^c   Sissons, J G Patrick ^a   Wills, Mark R ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; NATURAL KILLER CELL RECEPTOR NKG2D; ULBP3 LIGAND; UNCLASSIFIED DRUG; VIRUS GENE PRODUCT UL142; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; MEMBRANE PROTEIN; SIGNAL PEPTIDE; UL142 PROTEIN, HUMAN HERPESVIRUS 5; ULBP3 PROTEIN, HUMAN; VIRUS PROTEIN;

ARTICLE; CELL SURFACE; CYTOMEGALOVIRUS INFECTION; CYTOTOXICITY; DOWN REGULATION; GOLGI COMPLEX; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; VIRUS GENE; CELL CULTURE; CELL LINE; CELL MEMBRANE; CYTOLOGY; CYTOMEGALOVIRUS; FIBROBLAST; FLUORESCENCE MICROSCOPY; GENETIC TRANSFECTION; GENETICS; HELA CELL; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INTRACELLULAR SPACE; MALE; METABOLISM; NATURAL KILLER CELL; PROTEIN TRANSPORT; TUMOR CELL LINE; VIROLOGY; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL LINE; CELL LINE, TUMOR; CELL MEMBRANE; CELLS, CULTURED; CYTOMEGALOVIRUS; CYTOTOXICITY, IMMUNOLOGIC; FIBROBLASTS; GOLGI APPARATUS; GREEN FLUORESCENT PROTEINS; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTRACELLULAR SPACE; KILLER CELLS, NATURAL; MALE; MEMBRANE GLYCOPROTEINS; MICROSCOPY, FLUORESCENCE; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; TRANSFECTION; VIRAL PROTEINS;

EID: 77955483375     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1000789     Document Type: Article

References (70)

1. Lin, A., H. Xu, and W. Yan. 2007. Modulation of HLA expression in human cytomegalovirus immune evasion. Cell. Mol. Immunol. 4: 91-98.
2. Ljunggren, H. G., and K. Kärre. 1990. In search of the 'missing self': MHC molecules and NK cell recognition. Immunol. Today 11: 237-244.
3. Pinto, A. K., M. W. Munks, U. H. Koszinowski, and A. B. Hill. 2006. Coordinated function of murine cytomegalovirus genes completely inhibits CTL lysis. J. Immunol. 177: 3225-3234.
4. Brier, A. M., L. Chess, and S. F. Schlossman. 1975. Human antibody-dependent cellular cytotoxicity. Isolation and identification of a subpopulation of peripheral blood lymphocytes which kill antibody-coated autologous target cells. J. Clin. Invest. 56: 1580-1586.
5. Domzig, W., B. M. Stadler, and R. B. Herberman. 1983. Interleukin 2 dependence of human natural killer (NK) cell activity. J. Immunol. 130: 1970-1973.
6. Moretta, L., C. Bottino, C. Cantoni, M. C. Mingari, and A. Moretta. 2001. Human natural killer cell function and receptors. Curr. Opin. Pharmacol. 1: 387-391.
7. Biassoni, R. 2008. Natural killer cell receptors. Adv. Exp. Med. Biol. 640: 35-52.
8. Gleimer, M., and P. Parham. 2003. Stress management: MHC class I and class I-ike molecules as reporters of cellular stress. Immunity 19: 469-477. (Pubitemid 37311429)
9. Groh, V., R. Rhinehart, H. Secrist, S. Bauer, K. H. Grabstein, and T. Spies. 1999. Broad tumor-associated expression and recognition by tumor-derived gamma delta T cells of MICA and MICB. Proc. Natl. Acad. Sci. USA 96: 6879-6884.
10. Daniels, K. A., G. Devora, W. C. Lai, C. L. O'Donnell, M. Bennett, and R. M. Welsh. 2001. Murine cytomegalovirus is regulated by a discrete subset of natural killer cells reactive with monoclonal antibody to Ly49H. J. Exp. Med. 194: 29-44.
11. Lee, S. H., S. Girard, D. Macina, M. Busà, A. Zafer, A. Belouchi, P. Gros, and S. M. Vidal. 2001. Susceptibility to mouse cytomegalovirus is associated with deletion of an activating natural killer cell receptor of the C-type lectin superfamily. Nat. Genet. 28: 42-45.
12. 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: 619-648.
13. Posch, P. E., F. Borrego, A. G. Brooks, and J. E. Coligan. 1998. HLA-E is the ligand for the natural killer cell CD94/NKG2 receptors. J. Biomed. Sci. 5: 321-331.
14. Braud, V. M., D. S. Allan, C. A. O'Callaghan, K. Söderström, A. D'Andrea, G. S. Ogg, S. Lazetic, N. T. Young, J. I. Bell, J. H. Phillips, et al. 1998. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391: 795-799.
15. Tomasec, P., V. M. Braud, C. Rickards, M. B. Powell, B. P. McSharry, S. Gadola, V. Cerundolo, L. K. Borysiewicz, A. J. McMichael, and G. W. Wilkinson. 2000. Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 287: 1031.
16. Ulbrecht, M., S. Martinozzi, M. Grzeschik, H. Hengel, J. W. Ellwart, M. Pla, and E. H. Weiss. 2000. Cutting edge: the human cytomegalovirus UL40 gene product contains a ligand for HLA-E and prevents NK cell-mediated lysis. J. Immunol. 164: 5019-5022.
17. Beck, S., and B. G. Barrell. 1988. Human cytomegalovirus encodes a glycoprotein homologous to MHC class-I antigens. Nature 331: 269-272.
18. Maffei, M., F. Ghiotto, M. Occhino, M. Bono, A. De Santanna, L. Battini, G. L. Gusella, F. Fais, S. Bruno, and E. Ciccone. 2008. Human cytomegalovirus regulates surface expression of the viral protein UL18 by means of two motifs present in the cytoplasmic tail. J. Immunol. 180: 969-979.
19. 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: 273-282.
20. Chapman, T. L., A. P. Heikeman, and P. J. Bjorkman. 1999. The inhibitory receptor LIR-1 uses a common binding interaction to recognize class I MHC molecules and the viral homolog UL18. Immunity 11: 603-613.
21. Prod'homme, V., C. Griffin, R. J. Aicheler, E. C. Wang, B. P. McSharry, C. R. Rickards, R. J. Stanton, L. K. Borysiewicz, M. López-Botet, G.W.Wilkinson, and P. Tomasec. 2007. The human cytomegalovirus MHC class I homolog UL18 inhibits LIR-1+ but activates LIR-1- NK cells. J. Immunol. 178: 4473-4481.
22. Arnon, T. I., H. Achdout, O. Levi, G. Markel, N. Saleh, G. Katz, R. Gazit, T. Gonen-Gross, J. Hanna, E. Nahari, et al. 2005. Inhibition of the NKp30 activating receptor by pp65 of human cytomegalovirus. Nat. Immunol. 6: 515-523.
23. Tomasec, P., E. C. Wang, A. J. Davison, B. Vojtesek, M. Armstrong, C. Griffin, B. P. McSharry, R. J. Morris, S. Llewellyn-Lacey, C. Rickards, et al. 2005. Downregulation of natural killer cell-activating ligand CD155 by human cytomegalovirus UL141. Nat. Immunol. 6: 181-188.
24. 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.
25. Eagle, R. A., I. Jafferji, and A. D. Barrow. 2009. Beyond Stressed Self: Evidence for NKG2D Ligand Expression on Healthy Cells. Curr. Immunol. Rev. 5: 22-34.
26. Eagle, R. A., J. A. Traherne, O. Ashiru, M. R. Wills, and J. Trowsdale. 2006. Regulation of NKG2D ligand gene expression. Hum. Immunol. 67: 159-169.
27. Cosman, D., J. Müllberg, C. L. Sutherland, W. Chin, R. Armitage, W. Fanslow, M. Kubin, and N. J. Chalupny. 2001. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 14: 123-133.
28. Eagle, R. A., J. A. Traherne, J. R. Hair, I. Jafferji, and J. Trowsdale. 2009. ULBP6/RAET1L is an additional human NKG2D ligand. Eur. J. Immunol. 39: 3207-3216.
29. Rölle, A., M. Mousavi-Jazi, M. Eriksson, J. Odeberg, C. Söderberg-Nauclér, D. Cosman, K. Kärre, and C. Cerboni. 2003. Effects of human cytomegalovirus infection on ligands for the activating NKG2D receptor of NK cells: up-regulation of UL16-binding protein (ULBP)1 and ULBP2 is counteracted by the viral UL16 protein. J. Immunol. 171: 902-908. (Pubitemid 36871403)
30. Dunn, C., N. J. Chalupny, C. L. Sutherland, S. Dosch, P. V. Sivakumar, D. C. Johnson, and D. Cosman. 2003. Human cytomegalovirus glycoprotein UL16 causes intracellular sequestration of NKG2D ligands, protecting against natural killer cell cytotoxicity. J. Exp. Med. 197: 1427-1439.
31. 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.
32. Nachmani, D., N. Stern-Ginossar, R. Sarid, and O. Mandelboim. 2009. Diverse herpesvirus microRNAs target the stress-induced immune ligand MICB to escape recognition by natural killer cells. Cell Host Microbe 5: 376-385.
33. Chalupny, N. J., A. Rein-Weston, S. Dosch, and D. Cosman. 2006. Downregulation of the NKG2D ligand MICA by the human cytomegalovirus glycoprotein UL142. Biochem. Biophys. Res. Commun. 346: 175-181.
34. Zou, Y., W. Bresnahan, R. T. Taylor, and P. Stastny. 2005. Effect of human cytomegalovirus on expression of MHC class I-related chains A. J. Immunol. 174: 3098-3104. (Pubitemid 40279732)
35. Bradley, A. J., N. S. Lurain, P. Ghazal, U. Trivedi, C. Cunningham, K. Baluchova, D. Gatherer, G. W. Wilkinson, D. J. Dargan, and A. J. Davison. 2009. High-throughput sequence analysis of variants of human cytomegalovirus strains Towne and AD169. J. Gen. Virol. 90: 2375-2380.
36. Dolan, A., C. Cunningham, R. D. Hector, A. F. Hassan-Walker, L. Lee, C. Addison, D. J. Dargan, D. J. McGeoch, D. Gatherer, V. C. Emery, et al. 2004. Genetic content of wild-type human cytomegalovirus. J. Gen. Virol. 85: 1301-1312.
37. Wills, M. R., O. Ashiru, M. B. Reeves, G. Okecha, J. Trowsdale, P. Tomasec, G. W. Wilkinson, J. Sinclair, and J. G. Sissons. 2005. Human cytomegalovirus encodes an MHC class I-like molecule (UL142) that functions to inhibit NK cell lysis. J. Immunol. 175: 7457-7465.
38. Ashiru, O., N. J. Bennett, L. H. Boyle, M. Thomas, J. Trowsdale, and M. R. Wills. 2009. NKG2D ligand MICA is retained in the cis-Golgi apparatus by human cytomegalovirus protein UL142. J. Virol. 83: 12345-12354.
39. Petersdorf, E. W., K. B. Shuler, G. M. Longton, T. Spies, and J. A. Hansen. 1999. Population study of allelic diversity in the human MHC class I-related MIC-A gene. Immunogenetics 49: 605-612.
40. Wilkinson, G. W., P. Tomasec, R. J. Stanton, M. Armstrong, V. Prod'homme, R. Aicheler, B. P. McSharry, C. R. Rickards, D. Cochrane, S. Llewellyn-Lacey, et al. 2008. Modulation of natural killer cells by human cytomegalovirus. J. Clin. Virol. 41: 206-212.
41. Krmpotic, A., M. Hasan, A. Loewendorf, T. Saulig, A. Halenius, T. Lenac, B. Polic, I. Bubic, A. Kriegeskorte, E. Pernjak-Pugel, et al. 2005. NK cell activation through the NKG2D ligand MULT-1 is selectively prevented by the glycoprotein encoded by mouse cytomegalovirus gene m145. J. Exp. Med. 201: 211-220.
42. Lodoen, M., K. Ogasawara, J. A. Hamerman, H. Arase, J. P. Houchins, E. S. Mocarski, and L. L. Lanier. 2003. NKG2D-mediated natural killer cell protection against cytomegalovirus is impaired by viral gp40 modulation of retinoic acid early inducible 1 gene molecules. J. Exp. Med. 197: 1245-1253.
43. Hasan, M., A. Krmpotic, Z. Ruzsics, I. Bubic, T. Lenac, A. Halenius, A. Loewendorf, M. Messerle, H. Hengel, S. Jonjic, and U. H. Koszinowski. 2005. Selective down-regulation of the NKG2D ligand H60 by mouse cytomegalovirus m155 glycoprotein. J. Virol. 79: 2920-2930.
44. Lodoen, M. B., G. Abenes, S. Umamoto, J. P. Houchins, F. Liu, and L. L. Lanier. 2004. The cytomegalovirus m155 gene product subverts natural killer cell antiviral protection by disruption of H60-NKG2D interactions. J. Exp. Med. 200: 1075-1081.
45. Thäle, R., P. Lucin, K. Schneider, M. Eggers, and U. H. Koszinowski. 1994. Identification and expression of a murine cytomegalovirus early gene coding for an Fc receptor. J. Virol. 68: 7757-7765.
46. Lenac, T., M. Budt, J. Arapovic, M. Hasan, A. Zimmermann, H. Simic, A. Krmpotic, M. Messerle, Z. Ruzsics, U. H. Koszinowski, et al. 2006. The herpesviral Fc receptor fcr-1 down-regulates the NKG2D ligands MULT-1 and H60. J. Exp. Med. 203: 1843-1850.
47. Arapovic, J., T. Lenac, R. Antulov, B. Polic, Z. Ruzsics, L. N. Carayannopoulos, U. H. Koszinowski, A. Krmpotic, and S. Jonjic. 2009. Differential susceptibility of RAE-1 isoforms to mouse cytomegalovirus. J. Virol. 83: 8198-8207.
48. Wittenbrink, M., J. Spreu, and A. Steinle. 2009. Differential NKG2D binding to highly related human NKG2D ligands ULBP2 and RAET1G is determined by a single amino acid in the alpha2 domain. Eur. J. Immunol. 39: 1642-1651.
49. Apps, R., L. Gardner, J. Traherne, V. Male, and A. Moffett. 2008. Natural-killer cell ligands at the maternal-fetal interface: UL-16 binding proteins, MHC class-I chain related molecules, HLA-F and CD48. Hum. Reprod. 23: 2535-2548.
50. Bacon, L., R. A. Eagle, M. Meyer, N. Easom, N. T. Young, and J. Trowsdale. 2004. Two human ULBP/RAET1 molecules with transmembrane regions are ligands for NKG2D. J. Immunol. 173: 1078-1084. (Pubitemid 38924282)
51. Boyle, L. H., A. K. Gillingham, S. Munro, and J. Trowsdale. 2006. Selective export of HLA-F by its cytoplasmic tail. J. Immunol. 176: 6464-6472.
52. 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.
53. Cha, T. A., E. Tom, G. W. Kemble, G. M. Duke, E. S. Mocarski, and R. R. Spaete. 1996. Human cytomegalovirus clinical isolates carry at least 19 genes not found in laboratory strains. J. Virol. 70: 78-83.
54. Lanier, L. L. 2008. Evolutionary struggles between NK cells and viruses. Nat. Rev. Immunol. 8: 259-268.
55. Eagle, R. A., and J. Trowsdale. 2007. Promiscuity and the single receptor: NKG2D. Nat. Rev. Immunol. 7: 737-744.
56. Müller, S., G. Zocher, A. Steinle, and T. Stehle. 2010. Structure of the HCMV UL16-MICB complex elucidates select binding of a viral immunoevasin to diverse NKG2D ligands. PLoS Pathog. 6: e1000723.
57. Zhang, Y., A. M. Lazaro, B. Lavingia, and P. Stastny. 2001. Typing for all known MICA alleles by group-specific PCR and SSOP. Hum. Immunol. 62: 620-631.
58. Reddehase, M. J. 2002. Antigens and immunoevasins: opponents in cytomegalovirus immune surveillance. Nat. Rev. Immunol. 2: 831-844.
59. McFarland, B. J., and R. K. Strong. 2003. Thermodynamic analysis of degenerate recognition by the NKG2D immunoreceptor: not induced fit but rigid adaptation. Immunity 19: 803-812.
60. O'Callaghan, C. A., A. Cerwenka, B. E. Willcox, L. L. Lanier, and P. J. Bjorkman. 2001. Molecular competition for NKG2D: H60 and RAE1 compete unequally for NKG2D with dominance of H60. Immunity 15: 201-211.
61. 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.
62. Ward, J., M. Bonaparte, J. Sacks, J. Guterman, M. Fogli, D. Mavilio, and E. Barker. 2007. HIV modulates the expression of ligands important in triggering natural killer cell cytotoxic responses on infected primary T-cell blasts. Blood 110: 1207-1214. (Pubitemid 47281418)
63. Cerboni, C., F. Neri, N. Casartelli, A. Zingoni, D. Cosman, P. Rossi, A. Santoni, and M. Doria. 2007. Human immunodeficiency virus 1 Nef protein downmodulates the ligands of the activating receptor NKG2D and inhibits natural killer cell-mediated cytotoxicity. J. Gen. Virol. 88: 242-250.
64. Wen, C., X. He, H. Ma, N. Hou, C. Wei, T. Song, Y. Zhang, L. Sun, Q. Ma, and H. Zhong. 2008. Hepatitis C virus infection downregulates the ligands of the activating receptor NKG2D. Cell. Mol. Immunol. 5: 475-478.
65. Schepis, D., M. D'Amato, M. Studahl, T. Bergström, K. Kärre, and L. Berg. 2009. Herpes simplex virus infection downmodulates NKG2D ligand expression. Scand. J. Immunol. 69: 429-436.
66. Thomas, M., J. M. Boname, S. Field, S. Nejentsev, M. Salio, V. Cerundolo, M. Wills, and P. J. Lehner. 2008. Down-regulation of NKG2D and NKp80 ligands by Kaposi's sarcoma-associated herpesvirus K5 protects against NK cell cytotoxicity. Proc. Natl. Acad. Sci. USA 105: 1656-1661.
67. Groh, V., R. Rhinehart, J. Randolph-Habecker, M. S. Topp, S. R. Riddell, and T. Spies. 2001. Costimulation of CD8alphabeta T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nat. Immunol. 2: 255-260.
68. Verneris, M. R., M. Karami, J. Baker, A. Jayaswal, and R. S. Negrin. 2004. Role of NKG2D signaling in the cytotoxicity of activated and expanded CD8+ T cells. Blood 103: 3065-3072.
69. Larmonier, N., J. Fraszczak, D. Lakomy, B. Bonnotte, and E. Katsanis. 2010. Killer dendritic cells and their potential for cancer immunotherapy. Cancer Immunol. Immunother. 59: 1-11.
70. Süss, G., and K. Shortman. 1996. A subclass of dendritic cells kills CD4 T cells via Fas/Fas-ligand-induced apoptosis. J. Exp. Med. 183: 1789-1796.