Immune modulation by the human cytomegalovirus-encoded molecule UL18, a mystery yet to be solved

Journal of Immunology

Volumn 180, Issue 1, 2008, Pages 19-24

  Wagner, Claudia S ^a,b   Ljunggren, Hans Gustaf ^a   Achour, Adnane ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIR 1 PROTEIN; LYMPHOCYTE ANTIGEN RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; UL18 PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; CAPSID PROTEIN; HLA ANTIGEN CLASS 1; VP23 PROTEIN, HUMAN HERPESVIRUS 1;

CYTOMEGALOVIRUS INFECTION; DENDRITIC CELL; HUMAN; HUMAN CYTOMEGALOVIRUS; IMMUNE RESPONSE; IMMUNOMODULATION; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; RECEPTOR BINDING; SHORT SURVEY; T LYMPHOCYTE; CHEMISTRY; GENETICS; IMMUNOLOGY; METABOLISM; PROTEIN CONFORMATION; REVIEW; VIROLOGY;

CAPSID PROTEINS; CYTOMEGALOVIRUS INFECTIONS; DENDRITIC CELLS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; KILLER CELLS, NATURAL; PROTEIN CONFORMATION; T-LYMPHOCYTES;

EID: 40449131655     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.1.19     Document Type: Short Survey

References (66)

1. Alcami, A., and U. H. Koszinowski. 2000. Viral mechanisms of immune evasion. Immunol. Today 21: 447-455.
2. Yewdell, J. W., and A. B. Hill. 2002. Viral interference with antigen presentation. Nat. Immunol. 3: 1019-1025.
3. Mocarski, E. S., Jr. 2002. Immunomodulation by cytomegaloviruses: manipulative strategies beyond evasion. Trends Microbiol. 10: 332-339.
4. Lopez-Botet, M., A. Angulo, and M. Guma. 2004. Natural killer cell receptors for major histocompatibility complex class I and related molecules in cytomegalovirus infection. Tissue Antigens 63: 195-203.
5. Sissons, J. G., A. J. Carmichael, N. McKinney, J. H. Sinclair, and M. R. Wills. 2002. Human cytomegalovirus and immunopathology. Springer Semin. Immunopathol. 24: 169-185.
6. Beck, S., and B. G. Barrell. 1988. Human cytomegalovirus encodes a glycoprotein homologous to MHC class-I antigens. Nature 331: 269-272.
7. 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.
8. 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.
9. 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.
10. + NK cells. J. Immunol. 178: 4473-4481.
11. Park, B., Y. Kim, J. Shin, S. Lee, K. Cho, K. Fruh, S. Lee, and K. Ahn. 2004. Human cytomegalovirus inhibits tapasin-dependent peptide loading and optimization of the MHC class I peptide cargo for immune evasion. Immunity 20: 71-85.
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. Chapman, T. L., and P. J. Bjorkman. 1998. Characterization of a murine cytomegalovirus class I major histocompatibility complex (MHC) homolog: comparison to MHC molecules and to the human cytomegalovirus MHC homolog. J. Virol. 72: 460-466.
15. 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.
16. Wagner, C. S., A. Rölle, D. Cosman, H.-G. Ljunggren, K. Berndt, and A. Achour. 2007. Structural elements underlying the high binding affinity of human cytomegalovirus UL18 to leukocyte immunoglobulin-like receptor-1. J. Mol. Biol. 373: 695-705.
17. Bjorkman, P. J., M. A. Saper, B. Samraoui, W. S. Bennett, J. L. Strominger, and D. C. Wiley. 1987. Structure of the human class I histocompatibility antigen, HLA-A2. Nature 329: 506-512.
18. Cebulla, C. M., D. M. Miller, D. A. Knight, B. R. Briggs, V. McGaughy, and D. D. Sedmak. 2000. Cytomegalovirus induces sialyl Lewis(x) and Lewis(x) on human endothelial cells. Transplantation 69: 1202-1209.
19. 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.
20. 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.
21. Natarajan, K., A. Hicks, J. Mans, H. Robinson, R. Guan, R. A. Mariuzza, and D. H. Margulies. 2006. Crystal structure of the murine cytomegalovirus MHC-I homolog m144. J. Mol. Biol. 358: 157-171.
22. Rudd, P. M., T. Elliott, P. Cresswell, I. A. Wilson, and R. A. Dwek. 2001. Glycosylation and the immune system. Science 291: 2370-2376.
23. 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 down-regulation mediated by the unique short region protein (US)2, US3, US6, and US11 gene products. J. Immunol. 168: 3464-3469.
24. 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.
25. Lankat-Buttgereit, B., and R. Tampe. 1999. The transporter associated with antigen processing TAP: structure and function. FEBS Lett. 464: 108-112.
26. Varnum, S. M., D. N. Streblow, M. E. Monroe, P. Smith, K. J. Auberry, L. Pasa-Tolic, D. Wang, D. G. Camp II, K. Rodland, S. Wiley, et al. 2004. Identification of proteins in human cytomegalovirus (HCMV) particles: the HCMV proteome. J. Virol. 78: 10960-10966.
27. 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.
28. Hassan-Walker, A. F., F. M. Mattes, P. D. Griffiths, and V. C. Emery. 2001. Quantity of cytomegalovirus DNA in different leukocyte populations during active infection in vivo and the presence of gB and UL18 transcripts. J. Med. Virol. 64: 283-289.
29. 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.
30. 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.
31. 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.
32. 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.
33. Brown, D., J. Trowsdale, and R. Allen. 2004. The LILR family: modulators of innate and adaptive immune pathways in health and disease. Tissue Antigens 64: 215-225.
34. 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.
35. Andre, P., R. Biassoni, M. Colonna, D. Cosman, L. L. Lanier, E. O. Long, M. Lopez-Botet, A. Moretta, L. Moretta, P. Parham, et al. 2001. New nomenclature for MHC receptors. Nat. Immunol. 2: 661.
36. Tenca, C., A. Merlo, E. Merck, E. E. Bates, D. Saverino, R. Simone, D. Zarcone, G. Trinchieri, C. E. Grossi, and E. Ciccone. 2005. CD85j (leukocyte Ig-like receptor-1/Ig-like transcript 2) inhibits human osteoclast-associated receptor-mediated activation of human dendritic cells. J. Immunol. 174: 6757-6763.
37. Ince, M. N., B. Harnisch, Z. Xu, S. K. Lee, C. Lange, L. Moretta, M. Lederman, and J. Lieberman. 2004. Increased expression of the natural killer cell inhibitory receptor CD85j/ILT2 on antigen-specific effector CD8 T cells and its impact on CD8 T-cell function. Immunology 112: 531-542.
38. 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.
39. 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.
40. Shiroishi, M., K. Tsumoto, K. Amano, Y. Shirakihara, M. Colonna, V. M. Braud, D. S. Allan, A. Makadzange, S. Rowland-Jones, B. Willcox, et al. 2003. Human inhibitory receptors Ig-like transcript 2 (ILT2) and ILT4 compete with CD8 for MHC class I binding and bind preferentially to HLA-G. Proc. Natl. Acad. Sci. USA 100: 8856-8861.
41. Willcox, B. E., L. M. Thomas, and P. J. Bjorkman. 2003. Crystal structure of HLA-A2 bound to LIR-1, a host and viral major histocompatibility complex receptor. Nat. Immunol. 4: 913-919.
42. Merlo, A., C. Tenca, F. Fais, L. Battini, E. Ciccone, C. E. Grossi, and D. Saverino. 2005. Inhibitory receptors CD85j, LAIR-1, and CD152 down-regulate immunoglobulin and cytokine production by human B lymphocytes. Clin. Diagn. Lab. Immunol. 12: 705-712.
43. Kirwan, S. E., and D. N. Burshtyn. 2005. Killer cell Ig-like receptor-dependent signaling by Ig-like transcript 2 (ILT2/CD85j/LILRB1/LIR-1). J. Immunol. 175: 5006-5015.
44. 2- microglobulin-free HLA-G molecules. J. Immunol. 175: 4866-4874.
45. Lepin, E. J., J. M. Bastin, D. S. Allan, G. Roncador, V. M. Braud, D. Y. Mason, P. A. van der Merwe, A. J. McMichael, J. I. Bell, S. H. Powis, and C. A. O'Callaghan. 2000. Functional characterization of HLA-F and binding of HLA-F tetramers to ILT2 and ILT4 receptors. Eur. J. Immunol. 30: 3552-3561.
46. Navarro, F., M. Llano, T. Bellon, M. Colonna, D. E. Geraghty, and M. Lopez-Botet. 1999. The ILT2(LIR1) and CD94/NKG2A NK cell receptors respectively recognize HLA-G1 and HLA-E molecules coexpressed on target cells. Eur. J. Immunol. 29: 277-283.
47. 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.
48. 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.
49. Willcox, B. E., L. M. Thomas, T. L. Chapman, A. P. Heikema, A. P. West, Jr., and P. J. Bjorkman. 2002. Crystal structure of LIR-2 (ILT4) at 1.8 A: differences from LIR-1 (ILT2) in regions implicated in the binding of the Human Cytomegalovirus class I MHC homolog UL18. BMC Struct. Biol. 2: 6.
50. + T cells mediates the non-MHC-restricted lysis of human cytomegalovirus-infected cells. J. Immunol. 172: 5629-5637.
51. 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.
52. Odeberg, J., C. Cerboni, H. Browne, K. Karre, E. Moller, E. Carbone, and C. Soderberg-Naucler. 2002. Human cytomegalovirus (HCMV)-infected endothelial cells and macrophages are less susceptible to natural killer lysis independent of the downregulation of classical HLA class I molecules or expression of the HCMV class I homologue, UL18. Scand. J. Immunol. 55: 149-161.
53. Cosman, D., N. Fanger, and L. Borges. 1999. Human cytomegalovirus, MHC class I and inhibitory signalling receptors: more questions than answers. Immunol. Rev. 168: 177-185.
54. Lodoen, M. B., and L. L. Lanier. 2005. Viral modulation of NK cell immunity. Nat. Rev. Microbiol. 3: 59-69.
55. Wagner, C. S., L. Walther-Jallow, E. Buentke, H. G. Ljunggren, A. Achour, and B. J. Chambers. Human cytomegalovirus-derived protein UL18 alters the phenotype and function of monocyte-derived dendritic cells. J. Leukocyte Biol. In press.
56. +-T-cell responses to human cytomegalovirus reveals broad and multispecific reactivities in healthy virus carriers. J. Virol. 77: 5226-5240.
57. He, H., C. R. Rinaldo, Jr., and P. A. Morel. 1995. T cell proliferative responses to five human cytomegalovirus proteins in healthy seropositive individuals: implications for vaccine development. J. Gen. Virol. 76: 1603-1610.
58. 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.
59. Antrobus, R. D., N. Khan, A. D. Hislop, D. Montamat-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.
60. 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.
61. Dick, T. P. 2004. Assembly of MHC class I peptide complexes from the perspective of disulfide bond formation. Cell. Mol. Life Sci. 61: 547-556.
62. Ziegler, H., W. Muranyi, H. G. Burgert, E. Kremmer, and U. H. Koszinowski. 2000. The luminal part of the murine cytomegalovirus glycoprotein gp40 catalyzes the retention of MHC class I molecules. EMBO J. 19: 870-881.
63. 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.
64. Gilbert, M. J., S. R. Riddell, B. Plachter, and P. D. Greenberg. 1996. Cytomegalovirus selectively blocks antigen processing and presentation of its immediate-early gene product. Nature 383: 720-722.
65. 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.
66. Trgovcich, J., C. Cebulla, P. Zimmerman, and D. D. Sedmak. 2006. Human cytomegalovirus protein pp71 disrupts major histocompatibility complex class I cell surface expression. J. Virol. 80: 951-963.