Human cytomegalovirus UL7, a homologue of the SLAM-family receptor CD229, impairs cytokine production

Immunology and Cell Biology

Volumn 89, Issue 7, 2011, Pages 753-766

  Engel, Pablo ^a,b   Pérez Carmona, Natlia ^b   Albà, M Mar ^c,d   Robertson, Kevin ^e   Ghazal, Peter ^e   Angulo, Ana ^a,b  

^a UNIVERSITY OF BARCELONA   (Spain)

^b INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^c INST MUNIC D INVESTIGACIO MEDICA   (Spain)

^d INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

CD229; cytokine; cytomegalovirus; immune evasion; SLAM

Indexed keywords

CD150 ANTIGEN; GLYCOSYLATED PROTEIN; ILOMASTAT; INTERLEUKIN 6; INTERLEUKIN 8; MEMBRANE PROTEIN; METALLOPROTEINASE INHIBITOR; TUMOR NECROSIS FACTOR; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CANCER CELL CULTURE; CELL SURFACE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; GLYCOSYLATION; HUMAN; HUMAN CYTOMEGALOVIRUS; IMMUNE RESPONSE; LEUKOCYTE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DOMAIN; PROTEIN EXPRESSION; VIRUS STRAIN;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD; BASE SEQUENCE; CELL LINE; CYTOKINES; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; DENDRITIC CELLS; HUMANS; IMMUNE EVASION; IMMUNOLOGIC FACTORS; INTERLEUKIN-6; INTERLEUKIN-8; LEUKOCYTES; LYMPHOCYTE ACTIVATION; METALLOPROTEASES; MICE; MOLECULAR SEQUENCE DATA; PEPTIDE-N4-(N-ACETYL-BETA-GLUCOSAMINYL) ASPARAGINE AMIDASE; TUMOR NECROSIS FACTORS; VIRAL ENVELOPE PROTEINS; VIRAL MATRIX PROTEINS;

CYTOMEGALOVIRUS; HERPESVIRIDAE; HUMAN HERPESVIRUS 5;

EID: 80053903667     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2011.55     Document Type: Article

References (67)

1. Mocarski Jr ES, Shenk T, Pass RF. Cytomegaloviruses. In: Knipe DM, Howley PM (eds). Fields Virology, vol. 2. Lippincott Williams & Wilkins: Philadelphia, pp. 2701-2772.
2. Murphy E, Yu D, Grimwood J, Schmutz J, Dickson M, Jarvis MA et al. Coding potential of laboratory and clinical strains of human cytomegalovirus. Proc Natl Acad Sci USA 2003; 100: 14976-14981. (Pubitemid 37518002)
3. Dolan A, Cunningham C, Hector RD, Hassan-Walker AF, Lee L, Addison C et al. Genetic content of wild-type human cytomegalovirus. J Gen Virol 2004; 85: 1301-1312. (Pubitemid 38659794)
4. Dölken L, Pfeffer S, Koszinowski UH. Cytomegalovirus microRNAs. Virus Genes 2009; 38: 355-364.
5. Chee MS, Bankier AT, Beck S, Bohni R, Brown CM, Cerny R et al. Analysis of the protein-coding content of the sequence of human cytomegalovirus strain AD169. Curr Top Microbiol Immunol 1990; 154: 125-169. (Pubitemid 20151030)
6. Dunn W, Chou C, Li H, Hai R, Patterson D, Stolc V et al. Functional profiling of a human cytomegalovirus genome. Proc Natl Acad Sci USA 2003; 100: 14223-14228. (Pubitemid 37499218)
7. Yu D, Silva MC, Shenk T. Functional map of human cytomegalovirus AD169 defined by global mutational analysis. Proc Natl Acad Sci USA 2003; 100: 12396-12401. (Pubitemid 37271571)
8. Powers C, DeFilippis V, Malouli D, Früh K. Cytomegalovirus immune evasion. Curr Top Microbiol Immunol 2008; 325: 333-359.
9. Miller-Kittrell M, Sparer TE. Feeling manipulated: cytomegalovirus immune manipulation. Virol J 2009; 6: 4.
10. Elde NC, Malik HS. The evolutionary conundrum of pathogen mimicry. Nat Rev Microbiol 2009; 7: 787-797.
11. Michelson S. Consequences of human cytomegalovirus mimicry. Hum Immunol 2004; 65: 465-475. (Pubitemid 38691129)
12. Raftery M, Müller A, Schönrich G. Herpesvirus homologues of cellular genes. Virus Genes 2000; 21: 65-75.
13. Holzerlandt R, Orengo C, Kellam P, Albá MM. Identification of new herpesvirus gene homologs in the human genome. Genome Res 2002; 12: 1739-1748. (Pubitemid 35363678)
14. Farrell HE, Davies-Poynter NJ, Andrews DM, Degli-Esposti MA. Function of CMV-encoded MHC class I homologues. Curr Opin Microbiol Immunol 2002; 269: 131-151. (Pubitemid 34851531)
15. Calpe S, Wang N, Romero X, Berger SB, Lanyi A, Engel P, Terhorst C. The SLAM and SAP gene families control innate and adaptive immune responses. Adv Immunol 2008; 97: 177-250. (Pubitemid 351697820)
16. Schwartzberg PL, Mueller KL, Qi H, Cannons JL. SLAM receptors and SAP influence lymphocyte interactions, development and function. Nat Rev Immunol 2009; 9: 39-46.
17. Engel P, Eck MJ, Terhorst C. The SAP and SLAM families in immune responses and X-linked lymphoproliferative disease. Nat Rev Immunol 2003; 10: 813-821. (Pubitemid 37328659)
18. Sayos J, Wu C, Morra M, Wang N, Zhang X, Allen D et al. The X-linked lymphoproli-ferative-disease gene product SAP regulates signals induced through the co-receptor SLAM. Nature 1998; 395: 462-469. (Pubitemid 28462434)
19. Morra M, Lu J, Poy F, Martin M, Sayos J, Calpe S et al. Structural basis for the interaction of the free SH2 domain EAT-2 with SLAM receptors in hematopoietic cells. EMBO J 2001; 20: 5840-5852. (Pubitemid 33049260)
20. Bhat R, Eissmann P, Endt J, Hoffmann S, Watzl C. Fine-tuning of immune responses by SLAM-related receptors. J Leukoc Biol 2006; 79: 417-424. (Pubitemid 44831218)
21. Tatsuo H, Ono N, Tanaka K, Yanagi Y. SLAM (CDw150) is a cellular receptor for measles virus. Nature 2000; 406: 893-897. (Pubitemid 30664265)
22. Hsu E, Iorio C, Sarangi F, Khine A, Richardson C. CDw150 (SLAM) is a receptor for a lymphotropic strain of measles virus and may account for the immunosuppressive properties of this virus. Virology 2001; 279: 9-21. (Pubitemid 34160994)
23. Koga R, Ohno S, Ikegame S, Yanagi Y. Measles virus-induced immunosuppression in SLAM knock-in mice. J Virol 2010; 84: 5360-5367.
24. Senkevich TG, Bugert JJ, Sisler JR, Koonin EV, Darai G, Moss B. Genome sequence of a human tumorigenic poxvirus: prediction of specific host response-evasion genes. Science 1996; 273: 813-816. (Pubitemid 26271530)
25. Bugert JJ, Darai G. Poxvirus homologues of cellular genes. Virus Genes 2000; 21: 111-133.
26. Sidorenko SP, Clark EA. The dual-function CD150 receptor subfamily: the viral attraction. Nat Immunol 2003; 4: 19-24. (Pubitemid 36104703)
27. Borca MV, Kutish GF, Afonso CL, Irusta P, Carrillo C, Brun A. An African swine fever virus gene with similarity to the T-lymphocyte surface antigen CD2 mediates hemad-sorption. Virology 1994; 199: 463-468. (Pubitemid 24168986)
28. Rodríguez JM, Yáñez RJ, Almazán F, Viñuela E, Rodríguez JF. African swine fever virus encodes a CD2 homolog responsible for the adhesion of erythrocytes to infected cells. J Virol 1993; 67: 5312-5320. (Pubitemid 23241363)
29. Borca MV, Carrillo C, Zsak L, Laegreid WW, Kutish GF, Neilan JG et al. Deletion of a CD2-like gene, 8-DR, from African swine fever virus affects viral infection in domestic swine. J Virol 1998; 72: 2881-2889. (Pubitemid 28175525)
30. Davison AJ, Dolan A, Akter P, Addison C, Dargan DJ, Alcendor DJ et al. The human cytomegalovirus genome revisited: comparison with the chimpanzee cytomegalovirus genome. J Gen Virol 2003; 84: 17-28. (Pubitemid 36113546)
31. Sekulin K, Görzer I, Heiss-Czedik D, Puchhammer-Stöckl E. Analysis of the variability of CMV strains in the RL11D domain of the RL11 multigene family. Virus Genes 2007; 35: 577-583. (Pubitemid 350012786)
32. Jahn G, Stenglein S, Riegler S, Einsele H, Sinzger C. Human cytomegalovirus infection of immature dendritic cells and macrophages. Intervirology 1999; 42: 365-372. (Pubitemid 30122072)
33. Raftery MJ, Schwab M, Eibert SM, Samstag Y, Walczak H, Schonrich G. Targeting the function of mature dendritic cells by human cytomegalovirus: a multilayered viral defense strategy. Immunity 2001; 15: 997-1009. (Pubitemid 34075379)
34. Davison AJ, Akter P, Cunningham C, Dolan A, Addison C, Dargan DJ et al. Homology between the human cytomegalovirus RL11 gene family and human adenovirus E3 genes. J Gen Virol 2003; 84: 657-663. (Pubitemid 36267140)
35. Lilley BN, Ploegh HL, Tirabassi RS. Human cytomegalovirus open reading frame TRL11/IRL11 encodes an immunoglobulin G Fc-binding protein. J Virol 2001; 75: 11218-11221. (Pubitemid 33031588)
36. Atalay R, Zimmermann A, Wagner M, Borst E, Benz C, Messerle M et al. Identification and expression of human cytomegalovirus transcription units coding for two distinct Fcgamma receptor homologs. J Virol 2002; 76: 8596-8608. (Pubitemid 34864054)
37. Stanton RJ, Baluchova K, Dargan DJ, Cunningham C, Sheehy O, Seirafian S et al. Reconstruction of the complete human cytomegalovirus genome in a BAC reveals RL13 to be a potent inhibitor of replication. J Clin Invest 2010; 120: 3191-3208.
38. Chang CP, Vesole DH, Nelson J, Oldstone MB, Stinski MF. Identification and expression of a human cytomegalovirus early glycoprotein. J Virol 1989; 63: 3330-3337. (Pubitemid 19181391)
39. Buljan M, Bateman A. The evolution of protein domain families. Biochem Soc Trans 2009; 37: 751-755.
40. Murphy E, Rigoutso I, Shibuya T, Shenk TE. Reevaluation of human cytomegalovirus coding potential. Proc Natl Acad Sci USA 2003; 100: 13585-13590. (Pubitemid 37444784)
41. Classon BJ, Brown MH, Garnett D, Somoza C, Barclay AN, Willis AC et al. The hinge region of the CD8 alpha chain: structure, antigenicity, and utility in expression of immunoglobulin superfamily domains. Int Immunol 1992; 4: 215-225.
42. Chen A, Engel P, Tedder TF. Structural requirements regulate endoproteolytic release of the L-selectin (CD62 L) adhesion receptor from the cell surface of leukocytes. J Exp Med 1995; 182: 519-530.
43. Ehlers MR, Schwager SL, Scholle RR, Manji GA, Brandt WF, Riordan JF. Proteolytic release of membrane-bound angiotensin-converting enzyme: role of the juxtamembrane stalk sequence. Biochemistry 1996; 35: 9549-9559. (Pubitemid 26320063)
44. Beck S, Barrell BG. Human cytomegalovirus encodes a glycoprotein homologous to MHC class-I antigens. Nature 1998; 331: 269-272.
45. Wills MR, Ashiru O, Reeves MB, Okecha G, Trowsdale J, Tomasec P et al. Human cytomegalovirus encodes an MHC class I-like molecule (UL142) that functions to inhibit NK cell lysis. J Immunol 2005; 175: 7457-7465. (Pubitemid 41713443)
46. Park B, Oh H, Lee S, Song Y, Shin J, Sung YJ et al. 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 2002; 168: 3464-3469. (Pubitemid 34250412)
47. Sagar M, Wu X, Lee S, Overbaugh J. Human immunodeficiency virus type 1 V1-V2 envelope loop sequences expand and add glycosylation sites over the course of infection, and these modifications affect antibody neutralization sensitivity. J Virol 2006; 80: 9586-9598. (Pubitemid 44435633)
48. Rudd PM, Elliott T, Cresswell P, Wilson IA, Dwek RA. Glycosylationand the immune system. Science 2001; 291: 2370-2376.
49. Chambers J, Angulo A, Amaratunga D, Guo H, Jiang Y, Wan JS et al. DNA microarrays of the complex human cytomegalovirus genome: profiling kinetic class with drug sensitivity of viral gene expression. J Virol 1999; 73: 5757-5766. (Pubitemid 29274862)
50. Varnum SM, Streblow DN, Monroe ME, Smith P, Auberry KJ, Pasa-Tolic L et al. Identification of proteins in human cytomegalovirus (HCMV) particles: the HCMV proteome. J Virol 2004; 78: 10960-10966. (Pubitemid 39299636)
51. Budagian V, Bulanova E, Orinska Z, Duitman E, Brandt K, Ludwig A et al. Soluble Axl is generated by ADAM10-dependent cleavage and associates with Gas6 in mouse serum. Mol Cell Biol 2005; 25: 9324-9339. (Pubitemid 41507834)
52. Peschon JJ. An essential role for ectodomain shedding in mammalian development. Science 1998; 282: 1281-1284. (Pubitemid 28524483)
53. Garton KJ, Gough PJ, Raines EW. Emerging roles for ectodomain shedding in the regulation of inflammatory responses. J Leukoc Biol 2006; 79: 1105-1116. (Pubitemid 44835543)
54. Engel P, Angulo A. Viral immunomodulatory proteins: usurping host genes as a survival strategy. In: López-Larrea C (ed.). Self and Nonself. Landes Bioscience: Austin, (in press).
55. Romero X, Zapater N, Calvo M, Kalko SG, de la Fuente MA, Tovar V et al. CD229 (Ly9) lymphocyte cell surface receptor interacts homophilically through its N-terminal domain and relocalizes to the immunological synapse. J Immunol 2005; 174: 7033-7042. (Pubitemid 40705668)
56. Velikovsky CA, Deng L, Chlewicki LK, Fernández MM, Kumar V, Mariuzza RA. Structure of natural killer receptor 2B4 bound to CD48 reveals basis for heterophilic recognition in signaling lymphocyte activation molecule family. Immunity 2007; 27: 572-584. (Pubitemid 47615510)
57. Yan Q, Malashkevich VN, Fedorov A, Fedorov E, Cao E, Lary JW et al. Structure of CD84 provides insight into SLAM family function. Proc Natl Acad Sci USA 2007; 104: 10583-10588. (Pubitemid 47185708)
58. Simmen KA, Singh J, Luukkonen BG, Lopper M, Bittner A, Miller NE et al. Global modulation of cellular transcription by human cytomegalovirus is initiated by viral glycoprotein B. Proc Natl Acad Sci USA 2001; 98: 7140-7145. (Pubitemid 32567916)
59. Yurochko AD, Huang ES. Human cytomegalovirus binding to human monocytes induces immunoregulatory gene expression. J Immunol 1999; 162: 4806-4816. (Pubitemid 29314884)
60. Compton T, Kurt-Jones EA, Boehme KW, Belko J, Latz E, Golenbock DT et al. Human cytomegalovirus activates inflammatory cytokine responses via CD14 and Toll-like receptor 2. J Virol 2003; 77: 4588-4596. (Pubitemid 36402808)
61. Taylor RT, Bresnahan WA. Human cytomegalovirus immediate-early 2 gene expression blocks virus-induced beta interferon production. J Virol 2005; 79: 3873-3877. (Pubitemid 40327977)
62. Martin M, Romero X, de la Fuente MA, Tovar V, Zapater N, Esplugues E et al. CD84 functions as a homophilic adhesion molecule and enhances IFN-gamma secretion: adhesion is mediated by Ig-like domain 1. J Immunol 2001; 167: 3668-3676. (Pubitemid 32910809)
63. de la Fuente MA, Tovar V, Villamar N, Zapater N, Pizcueta P, Campo E et al. Molecular characterization and expression of a novel human leukocyte cell-surface marker homologous to mouse Ly-9. Blood 2001; 97: 3513-3520.
64. Kondo K, Kaneshima H, Mocarski ES. Human cytomegalovirus latent infection of granulocyte-macrophage progenitors. Proc Natl Acad Sci USA 1994; 91: 11879-11883. (Pubitemid 24368567)
65. García-Ramírez JJ, Ruchti F, Huang H, Simmen K, Angulo A, Ghazal P. Dominance of virus over host factors in cross-species activation of human cytomegalovirus early gene expression. J Virol 2001; 75: 26-35.
66. Cole C, Barber JD, Barton GJ. The Jpred 3 secondary structure prediction server. Nucleic Acids Res 2008; 36 (Web Server Issue): W197-W201.
67. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F et al. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 2008; 36 (Web Server Issue): W465-W469.