Human cytomegalovirus regulates surface expression of the viral protein UL18 by means of two motifs present in the cytoplasmic tail

Journal of Immunology

Volumn 180, Issue 2, 2008, Pages 969-979

  Maffei, Massimo ^a   Ghiotto, Fabio ^a   Occhino, Marzia ^a   Bono, Maria ^a   De Santanna, Amleto ^a   Battini, Lorenzo ^b   Gusella, G Luca ^b   Fais, Franco ^a   Bruno, Silvia ^a   Ciccone, Ermanno ^a  

^a UNIVERSITY OF GENOA   (Italy)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC PROTEIN; LIGAND; PROTEIN UL18; UNCLASSIFIED DRUG; VIRUS PROTEIN; CAPSID PROTEIN; HLA A2 ANTIGEN; HYBRID PROTEIN; VP23 PROTEIN, HUMAN HERPESVIRUS 1;

ARTICLE; CELL INTERACTION; CELL SURFACE; CONSENSUS SEQUENCE; CYTOMEGALOVIRUS INFECTION; CYTOPLASM; EMBRYO; FEMALE; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; MUTANT; NATURAL KILLER CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; REGULATORY MECHANISM; SEQUENCE HOMOLOGY; T LYMPHOCYTE; VIRUS GENOME; VIRUS STRAIN; AMINO ACID SEQUENCE; ANIMAL; CELL LINE; CELL MEMBRANE; CHEMISTRY; CYTOMEGALOVIRUS; ENDOPLASMIC RETICULUM; GENETICS; GOLGI COMPLEX; METABOLISM; MOLECULAR GENETICS; MUTATION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CAPSID PROTEINS; CELL LINE; CELL MEMBRANE; CONSENSUS SEQUENCE; CYTOMEGALOVIRUS; ENDOPLASMIC RETICULUM; FIBROBLASTS; GENOME, VIRAL; GOLGI APPARATUS; HLA-A2 ANTIGEN; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; RECOMBINANT FUSION PROTEINS;

EID: 40449087414     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.2.969     Document Type: Article

References (51)

1. Ho, M. 1990. Epidemiology of cytomegalovirus infections. Rev. Infect. Dis. 12(Suppl. 7): S701-S710.
2. Fruh, K., A. Gruhler, R. M. Krishna, and G. J. Schoenhals. 1999. A comparison of viral immune escape strategies targeting the MHC class I assembly pathway. Immunol. Rev. 168: 157-166.
3. Xu, X. N., G. R. Screaton, and A. J. McMichael. 2001. Virus infections: escape, resistance, and counterattack. Immunity 15: 867-870.
4. Farrell, H. E., H. Vally, D. M. Lynch, P. Fleming, G. R. Shellam, A. A. Scalzo, and N. J. Davis-Poynter. 1997. Inhibition of natural killer cells by a cytomegalovirus MHC class I homologue in vivo. Nature 386: 510-514.
5. 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: 1031-1033.
6. 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.
7. Stern-Ginossar, N., N. Elefant, A. Zimmermann, D. G. Wolf, N. Saleh, M. Biton, E. Horwitz, Z. Prokocimer, M. Prichard, G. Hahn, et al. 2007. Host immune system gene targeting by a viral miRNA. Science 317: 376-381.
8. Polic, B., H. Hengel, A. Krmpotic, J. Trgovcich, I. Pavic, P. Luccaronin, S. Jonjic, and U. H. Koszinowski. 1998. Hierarchical and redundant lymphocyte subset control precludes cytomegalovirus replication during latent infection. J. Exp. Med. 188: 1047-1054.
9. Arase, H., E. S. Mocarski, A. E. Campbell, A. B. Hill, and L. L. Lanier. 2002. Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 296: 1323-1326.
10. Gutierrez, A., I. Munoz, C. Solano, I. Benet, C. Gimeno, I. Marugan, M. D. Gea, J. Garcia-Conde, and D. Navarro. 2003. Reconstitution of lymphocyte populations and cytomegalovirus viremia or disease after allogeneic peripheral blood stem cell transplantation. J. Med. Virol. 70: 399-403.
11. Beck, S., and B. G. Barrell. 1988. Human cytomegalovirus encodes a glycoprotein homologous to MHC class-I antigens. Nature 331: 269-272.
12. 2 microglobulin. Nature 347: 770-772.
13. Fahnestock, M. L., J. L. Johnson, R. M. Feldman, J. M. Neveu, W. S. Lane, and P. J. Bjorkman. 1995. The MHC class I homolog encoded by human cytomegalovirus binds endogenous peptides. Immunity 3: 583-590.
14. Hassan-Walker, A. F., A. V. Cope, P. D. Griffiths, and V. C. Emery. 1998. Transcription of the human cytomegalovirus natural killer decoy gene, UL18, in vitro and in vivo. J. Gen. Virol. 79: 2113-2116.
15. Browne, H., M. Churcher, and T. Minson. 1992. Construction and characterization of a human cytomegalovirus mutant with the UL18 (class I homolog) gene deleted. J. Virol. 66: 6784-6787.
16. 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.
17. Bellon, T., F. Kitzig, J. Sayos, and M. Lopez-Botet. 2002. Mutational analysis of immunoreceptor tyrosine-based inhibition motifs of the Ig-like transcript 2 (CD85j) leukocyte receptor. J. Immunol. 168: 3351-3359.
18. 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: 1809-1818.
19. Saverino, D., M. Fabbi, F. Ghiotto, A. Merlo, S. Bruno, D. Zarcone, C. Tenca, M. Tiso, G. Santoro, G. Anastasi, et al. 2000. The CD85/LIR-1/ILT2 inhibitory receptor is expressed by all human T lymphocytes and down-regulates their functions. J. Immunol. 165: 3742-3755.
20. 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: 3933-3941.
21. Fanger, N. A., D. Cosman, L. Peterson, S. C. Braddy, C. R. Maliszewski, and L. Borges. 1998. The MHC class I binding proteins LIR-1 and LIR-2 inhibit Fc receptor-mediated signaling in monocytes. Eur. J. Immunol. 28: 3423-3434.
22. Dietrich, J., M. Cella, and M. Colonna. 2001. Ig-like transcript 2 (ILT2)/leukocyte Ig-like receptor 1 (LIR1) inhibits TCR signaling and actin cytoskeleton reorganization. J. Immunol. 166: 2514-2521.
23. + T-cell clones specific for Mycobacterium tuberculosis. Infect. Immun. 69: 6022-6029.
24. Saverino, D., A. Merlo, S. Bruno, V. Pistoia, C. E. Grossi, and E. Ciccone. 2002. Dual effect of CD85/leukocyte Ig-like receptor-1/Ig-like transcript 2 and CD152 (CTLA-4) on cytokine production by antigen-stimulated human T cells. J. Immunol. 168: 207-215.
25. Reyburn, H. T., O. Mandelboim, M. Vales-Gomez, D. M. Davis, L. Pazmany, and J. L. Strominger. 1997. The class I MHC homologue of human cytomegalovirus inhibits attack by natural killer cells. Nature 386: 514-517.
26. Kim, J. S., S. E. Choi, I. H. Yun, J. Y. Kim, C. Ahn, S. J. Kim, J. Ha, E. S. Hwang, C. Y. Cha, S. Miyagawa, and C. G. Park. 2004. Human cytomegalovirus UL18 alleviated human NK-mediated swine endothelial cell lysis. Biochem. Biophys. Res. Commun. 315: 144-150.
27. Leong, C. C., T. L. Chapman, P. J. Bjorkman, D. Formankova, E. S. Mocarski, J. H. Phillips, and L. L. Lanier. 1998. Modulation of natural killer cell cytotoxicity in human cytomegalovirus infection: the role of endogenous class I major histocompatibility complex and a viral class I homolog. J. Exp. Med. 187: 1681-1687.
28. + T cells mediates the non-MHC-restricted lysis of human cytomegalovirus-infected cells. J. Immunol. 172: 5629-5637.
29. Wagner, C. S., G. C. Riise, T. Bergstrom, K. Karre, E. Carbone, and L. Berg. 2007. Increased expression of leukocyte Ig-like receptor-1 and activating role of UL18 in the response to cytomegalovirus infection. J. Immunol. 178: 3536-3543.
30. 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.
31. Chapman, T. L., A. P. Heikema, A. P. West, Jr., and P. J. Bjorkman. 2000. Crystal structure and ligand binding properties of the D1D2 region of the inhibitory receptor LIR-1 (ILT2). Immunity 13: 727-736.
32. Antrobus, R. D., N. Khan, A. D. Hislop, D. Montamatt-Sicotte, L. I. Garner, A. B. Rickinson, P. A. Moss, and B. E. Willcox. 2005. 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. 191: 1842-1853.
33. Northfield, J., M. Lucas, H. Jones, N. T. Young, and P. Klenerman. 2005. Does memory improve with age? CD85j (ILT-2/LIR-1) expression on CD8 T cells correlates with 'memory inflation' in human cytomegalovirus infection. Immunol. Cell Biol. 83: 182-188.
34. Berg, L., G. C. Riise, D. Cosman, T. Bergstrom, S. Olofsson, K. Karre, and E. Carbone. 2003. LIR-1 expression on lymphocytes, and cytomegalovirus disease in lung-transplant recipients. Lancet 361: 1099-1101.
35. Griffin, C., E. C. Wang, B. P. McSharry, C. Rickards, H. Browne, G. W. Wilkinson, and P. Tomasec. 2005. Characterization of a highly glycosylated form of the human cytomegalovirus HLA class I homologue gpUL18. J. Gen. Virol. 86: 2999-3008.
36. - NK cells. J. Immunol. 178: 4473-4481.
37. Fedorova, E., L. Battini, A. Prakash-Cheng, D. Marras, and G. L. Gusella. 2006. Lentiviral gene delivery to CNS by spinal intrathecal administration to neonatal mice. J. Gene Med. 8: 414-424.
38. Naldini, L., U. Blomer, F. H. Gage, D. Trono, and I. M. Verma. 1996. Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc. Natl. Acad. Sci. USA 93: 11382-11388.
39. Ishido, S., C. Wang, B. S. Lee, G. B. Cohen, and J. U. Jung. 2000. Downregulation of major histocompatibility complex class I molecules by Kaposi's sarcoma-associated herpesvirus K3 and K5 proteins. J. Virol. 74: 5300-5309.
40. Horton, P., and K. Nakai. 1997. Better prediction of protein cellular localization sites with the k nearest neighbors classifier. Proc. Int. Conf. Intell. Syst. Mol. Biol. 5: 147-152.
41. Puntervoll, P., R. Linding, C. Gemund, S. Chabanis-Davidson, M. Mattingsdal, S. Cameron, D. M. Martin, G. Ausiello, B. Brannetti, A. Costantini, et al. 2003. ELM server: a new resource for investigating short functional sites in modular eukaryotic proteins. Nucleic Acids Res. 31: 3625-3630.
42. Jones, T. R., L. K. Hanson, L. Sun, J. S. Slater, R. M. Stenberg, and A. E. Campbell. 1995. Multiple independent loci within the human cytomegalovirus unique short region down-regulate expression of major histocompatibility complex class I heavy chains. J. Virol. 69: 4830-4841.
43. Ohno, H., J. Stewart, M. C. Fournier, H. Bosshart, I. Rhee, S. Miyatake, T. Saito, A. Gallusser, T. Kirchhausen, and J. S. Bonifacino. 1995. Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science 269: 1872-1875.
44. Marks, M. S., L. Woodruff, H. Ohno, and J. S. Bonifacino. 1996. Protein targeting by tyrosine- and di-leucine-based signals: evidence for distinct saturable components. J. Cell Biol. 135: 341-354.
45. Cosson, P., Y. Lefkir, C. Demolliere, and F. Letourneur. 1998. New COP1-binding motifs involved in ER retrieval. EMBO J. 17: 6863-6870.
46. Gaynor, E. C., S. te Heesen, T. R. Graham, M. Aebi, and S. D. Emr. 1994. Signal-mediated retrieval of a membrane protein from the Golgi to the ER in yeast. J. Cell Biol. 127: 653-665.
47. Park, B., H. Oh, S. Lee, Y. Song, J. Shin, Y. C. Sung, S. Y. Hwang, and K. Ahn. 2002. The MHC class I homolog of human cytomegalovirus is resistant to downregulation mediated by the unique short region protein (US)2, US3, US6, and US11 gene products. J. Immunol. 168: 3464-3469.
48. Antonsson, A., and P. J. Hugo Johansson. 2001. Binding of human and animal immunoglobulins to the IgG Fc receptor induced by cytomegalovirus. J. Gen. Virol. 82: 1137-1145.
49. Vales-Gomez, M., M. Shiroishi, K. Maenaka, and H. T. Reyburn. 2005. Genetic variability of the major histocompatibility complex class I homologue encoded by human cytomegalovirus leads to differential binding to the inhibitory receptor ILT2. J. Virol. 79: 2251-2260.
50. Cerboni, C., A. Achour, A. Warnmark, M. Mousavi-Jazi, T. Sandalova, M. L. Hsu, D. Cosman, K. Karre, and E. Carbone. 2006. Spontaneous mutations in the human CMV HLA class I homologue UL18 affect its binding to the inhibitory receptor LIR-1/ILT2/CD85j. Eur. J. Immunol. 36: 732-741.
51. Occhino, M., F. Ghiotto, S. Soro, M. Mortarino, S. Bosi, M. Maffei, S. Bruno, N. Nardini, M. Figini, A. Tramontano, and E. Ciccone. 2008. Dissecting the structural determinants of the interaction between the human cytomegalovirus UL18 protein and the CD85j immune receptor. J. Immunol. 180: 957-968.