Cytomegalovirus immune evasion by perturbation of endosomal trafficking

Cellular and Molecular Immunology

Volumn 12, Issue 2, 2015, Pages 154-169

  Lučin, Pero ^a   Mahmutefendić, Hana ^a   Blagojević Zagorac, Gordana ^a   Ilić Tomaš, Maja ^a  

^a UNIVERSITY OF RIJEKA   (Croatia)

Author keywords

cytomegaloviruses; endocytic trafficking; herpesviruses; immune evasion

Indexed keywords

CD1B ANTIGEN; CD1C ANTIGEN; CD4 ANTIGEN; CD63 ANTIGEN; CD8 ANTIGEN; CELL PROTEIN; CLATHRIN; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; HERMES ANTIGEN; LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; T6 ANTIGEN; TRANSFERRIN RECEPTOR; VIRUS PROTEIN;

ADAPTIVE IMMUNITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL COMPARTMENTALIZATION; CELL SURFACE; CYTOMEGALOVIRUS; EFFECTOR CELL; ENDOCYTOSIS; ENDOSOME; HERPESVIRIDAE; HUMAN; IMMUNE EVASION; INHIBITION KINETICS; INNATE IMMUNITY; INTERNALIZATION; MOLECULAR RECOGNITION; NATURAL KILLER CELL; NONHUMAN; PINOCYTOSIS; PROTEIN ASSEMBLY; PROTEIN TRANSPORT; REVIEW; VIRAL CLEARANCE; ANIMAL; CYTOMEGALOVIRUS INFECTION; IMMUNOLOGY; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL; VIROLOGY;

CYTOMEGALOVIRUS; HERPESVIRIDAE;

ANIMALS; BIOLOGICAL TRANSPORT; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; ENDOSOMES; HUMANS; IMMUNE EVASION;

EID: 84929963322     PISSN: 16727681     EISSN: 20420226     Source Type: Journal    
DOI: 10.1038/cmi.2014.85     Document Type: Review

References (151)

1. Roizman B. Herpesviridae. In: Fields BN, Knipe DM, Howley PM, editors. Fields Virology. 3rd ed. Philadelphia, PA: Lippincott-Raven Publishers, 1996: 2221-2230.
2. Lilley BN, Ploegh HL. Viral modulation of antigen presentation: manipulation of cellular targets in the ER and beyond. Immunol Rev 2005; 207: 126-144.
3. Lodoen MB, Lanier LL. Viral modulation of NK cell immunity. Nat Rev 2005; 3: 59-69.
4. Slavuljica I, Krmpotic A, Jonjic S. Manipulation ofNKG2D ligands by cytomegaloviruses: impact on innate and adaptive immune response. Front Immunol 2011; 2: 85.
5. Terrazzini N, Kern F. Cell-mediated immunity to human CMV infection: a brief overview. F1000Prime Reports 2014; 6: 28.
6. Koenig JA, Edwardson JM. Endocytosis and recycling of G proteincoupled receptors. Trends Pharmacol Sci 1997; 18: 276-287.
7. Steinman RM, Mellman IS, Muller WA, Cohn ZA. Endocytosis and the recycling of plasma membrane. J Cell Biol 1983; 96: 1-27.
8. McMahon HT, Boucrot E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 2011; 12: 517-533.
9. Hansen CG, Nichols BJ. Molecular mechanisms of clathrinindependent endocytosis. J Cell Sci 2009; 122: 1713-1721.
10. LeRoy C, Wrana JL. Clathrin- and nonclathrin-mediated endocytic regulation of cell signalling. Nat Rev Mol Cell Biol 2005; 6: 112-26.
11. Gong Q, Huntsman C, Ma D. Clathrin-independent internalization and recycling. J Cell Mol Med 2008; 12: 126-144.
12. Kirkham M, Parton RG. Clathrin-independent endocytosis: new insights into caveolae and noncaveolar lipid raft carriers. Biochim Biophys Acta 2005; 1746: 349-63.
13. Sandvig K, Pust S, Skotland T, van Deurs B. Clathrin-independent endocytosis: mechanisms and function. Curr Opin Cell Biol 2011; 23: 413-420.
14. Mayor S, Pagano RE. Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 2007; 8: 603-612.
15. Massol RH, Larsen JE, Kirchhausen T. Possible role of deep tubular invaginations of the plasma membrane in MHC-I trafficking. Exp Cell Res 2005; 306: 142-149.
16. Maldonado-Baez L, Williamson C, Donaldson JG. Clathrinindependent endocytosis: A cargo-centric view. Exp Cell Res 2013; 319: 2759-2769.
17. Coskun U, Simons K. Membrane rafting: from apical sorting to phase segregation. FEBS Lett 2010; 584: 1685-1693.
18. Berditchevski F, Odintsova E. Tetraspanins as regulators of protein trafficking. Traffic 2007; 8: 1-8.
19. Vereb G, Szollosi J, Matko J, Nagy P, Farkas T, Vigh L et al. Dynamic, yet structured: the cell membrane three decades after the Singer- Nicolson model. Proc Natl Acad Sci USA 2003; 100: 8053-8058.
20. Swanson JA, Watts C. Macropinocytosis. Trends Cell Biol 1995; 5: 424-428.
21. Huotari J, Helenius A. Endosome maturation. EMBO J 2011; 30: 3481-3500.
22. Jovic M, Sharma M, Rahajeng J, Caplan S. The early endosome: a busy sorting station for proteins at the crossroads. Histol Histopathol 2010; 25: 99-112.
23. Grant BD, Donaldson JG. Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 2009; 10: 597-608.
24. Hao M, Maxfield FR. Characterization of rapid membrane internalization and recycling. J Biol Chem 2000; 275: 15279-15286.
25. Weigert R, Yeung AC, Li J, Donaldson JG. Rab22a regulates the recycling of membrane proteins internalized independently of clathrin. Mol Biol Cell 2004; 15: 3758-3770.
26. Naslavsky N, Weigert R, Donaldson JG. Characterization of a nonclathrin endocytic pathway: membrane cargo and lipid requirements. Mol Biol Cell 2004; 15: 3542-3552.
27. Rink J, Ghigo E, Kalaidzidis Y, Zerial M. Rab conversion as a mechanism of progression from early to late endosomes. Cell 2005; 122: 735-749.
28. Lebrand C, Corti M, Goodson H, Cosson P, Cavalli V, Mayran N et al. Late endosome motility depends on lipids via the small GTPase Rab7. EMBO J 2002, 21: 1289-1300.
29. Marks MS, Heijnen HFG, Raposo G. Lysosome-related organelles: unusual compartments become mainstream. Curr Opin Cell Biol 2013; 19: 495-505.
30. Braulke T, Bonifacino JS. Sorting of lysosomal proteins. Biochim Biophys Acta 2009; 1793: 605-614.
31. Laulagnier K,Schieber NL, Maritzen T, Haucke V, Parton RG, Gruenberg J. Role of AP1 and Gadkin in the traffic of secretory endo-lysosomes. Mol Biol Cell 2011; 22: 2068-2082.
32. Ostrowski M, Carmo NB, Krumeich S, Fanget I, Raposo G, Savina A et al. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol 2010; 12: 19-30.
33. McMahon HT, Gallop JL. Membrane curvature and mechanisms of dynamic cell remodelling. Nature 2005; 438: 590-596.
34. DSouza-Schorey C, Chavrier P. ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 2006; 7: 347-358.
35. Hutagalung AH, Novick PJ. Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 2011; 91: 119-149.
36. Donaldson JG, Williams DB. Intracellular assembly and trafficking of MHC class I molecules. Traffic 2009; 10: 1745-1752.
37. Progida C, Cogli L, Piro F, de Luca A, Bakke O, Bucci C. Rab7b controls trafficking from endosomes to the TGN. J Cell Sci 2010; 123: 1480-1491.
38. Vanlandingham PA, Ceresa BP. Rab7 regulates late endocytic trafficking downstream of multivesicular body biogenesis and cargo sequestration. Biol Chem 2009; 284: 12110-12124.
39. Benmerah A, Lamaze C. Clathrin-coated pits: Vive la difference? Traffic 2007; 8: 970-982
40. Sorkin A, Goh LK. Endocytosis and intracellular trafficking of ErbBs. Exp Cell Res 2008; 314: 3093-3106.
41. Huang F, Kirkpatrick D, Jiang X, Gygi S, Sorkin A. Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol Cell 2006; 21: 737-748.
42. Pompey S, Zhao Z, Luby-Phelps K, Michaely P. Quantitative fluorescence imaging reveals point of release for lipoproteins during LDLR-dependent uptake. J Lipid Res 2013; 54: 744-753.
43. van der Kant R, Fish A, Janssen L, Janssen H, Krom S, Ho N et al. Late endosomal transport and tethering are coupled processes controlled by RILP and the cholesterol sensor ORP1L. J Cell Sci 2013; 126: 3462-3474.
44. Berditchevski F, Odintsova E. Tetraspanins as regulators of protein trafficking. Traffic 2007; 8: 89-96.
45. Sabharanjak S, Sharma P, Parton RG, Mayor S. GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev Cell 2002; 2: 411-423.
46. Fivaz M, Vilbois F, Thurnheer S, Pasquali C, Abrami L, Bickel PE et al. Differential sorting and fate of endocytosed GPI-anchored proteins. EMBO J 2002; 21: 3989-4000.
47. Naslavsky N, Weigert R, Donaldson JG. Convergence of non-clathrinand clathrin-derived endosomes involves Arf6 inactivation and changes in phosphoinositides. Mol Biol Cell 2003; 14: 417-431.
48. Mahmutefendic H, Blagojevic G, Ilic Tomas M, Kucic N, Lucin P. Segregation of open Major Histocompatibility class I conformers at the plasma membrane and during endosomal trafficking reveals conformation-based sorting in the endosomal system. Int J Biochem Cell Biol 2011; 43: 504-515.
49. Zagorac GB, Mahmutefendic H, Ilic Tomas M, Kucic N, Le Bouteiller P, Lucin P. Early endosomal rerouting of Major Histocompatibility class I conformers. J Cell Physiol 2012; 227: 2953-64.
50. Mahmutefendic H, Zagorac GB, Tomas MI, Groettrup M, Momburg F, Lucin P. Endosomal trafficking of open Major Histocompatibility Class I conformers-implications for presentation of endocytosed antigens. Mol Immunol 2013; 55: 149-52.
51. Walseng E, Bakke O, Roche PA. Major histocompatibility complex class II-peptide complexes internalize using a clathrin- and dynamin-independent endocytosis pathway. J Biol Chem 2008; 283: 14717-14727.
52. Sugita M, van der Wel N, Rogers RA, Peters PJ, Brenner MB. CD1c molecules broadly survey the endocytic system. Proc Natl Acad Sci USA 2000, 97: 8445-8450.
53. Barral DC, Cavallari M, McCormick PJ, Garg S, Magee AI, Bonifacino JS et al. CD1a and MHC class I follow a similar endocytic recycling pathway. Traffic 2008; 9: 1446-57.
54. Barral DC, Brenner MB. CD1 antigen presentation: how it works. Nat Rev Immunol 2007; 7: 929-941.
55. Hansen TH, Bouvier M. MHC class I antigen presentation: learning from viral evasion strategies. Nat Rev Immunol 2009; 9: 503-513.
56. Alcami A, Koszinowski UH. Viral mechanisms of immune evasion. Immunol Today 2000; 21: 447.
57. Mitrovic M, Arapovic J, Jordan S, Fodil-Cornu N, Ebert S, Vidal SM et al. The NK cell response to mouse cytomegalovirus infection affects the level and kinetics of the early CD81 T-cell response. J Virol 2012; 86: 2165-2175.
58. Pamer E, Cresswell P. Mechanisms ofMHCclass I-restricted antigen processing. Annu Rev Immunol 1998; 16: 323-358.
59. Jovanovic OA, Brown FD, Donaldson JG. An effector domain mutant of Arf6 implicates phospholipase D in endosomal membrane recycling. Mol Biol Cell 2006; 17:327-335.
60. Bevan MJ. Cross-priming. Nat Immunol 2006; 7: 363-365.
61. Heath WR, Carbone FR. Cross-presentation in viral immunity and self-tolerance. Nat Rev Immunol 2001; 1: 126-134.
62. Neefjes J, Jongsma ML, Paul P, Bakke O. Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat Rev Immunol 2011; 11: 823-836.
63. Rocha N, Neefjes J. MHC class II molecules on the move for successful antigen presentation. EMBO J 2008; 27: 1-5.
64. Dani A, Chaudhry A, Mukherjee P, Rajagopal D, Bhatia S, George A et al. The pathway for MHC II-mediated presentation of endogenous proteins involves peptide transport to the endo-lysosomal compartment. J Cell Sci 2004; 117: 4219-4230.
65. Jonjic S, Babic M, Polic B, Krmpotic A. Immune evasion of natural killer cells by viruses. Curr Opin Immunol 2008; 20: 30-38.
66. Wilkinson GW, Tomasec P, Stanton RJ, Armstrong M, Prodhomme V, Aicheler R et al. Modulation of natural killer cells by human cytomegalovirus. J Clin Virol 2008; 41: 206-212.
67. Rao P, Pham HT, Kulkarni A, Yang Y, Liu X, Knipe DM et al. Herpes simplex virus 1 glycoprotein B and US3 collaborate to inhibit CD1d antigen presentation and NKT cell function. J Virol 2011; 85: 8093-8104.
68. Brigl M, Brenner MB. CD1: antigen presentation and T cell function. Annu Rev Immunol 2004; 22: 817-890.
69. del Val M, Hengel H, Hacker H, Hartlaub U, Ruppert T, Lucin P et al. Cytomegalovirus prevents antigen presentation by blocking the transport of peptide-loaded major histocompatibility complex class I molecules into the medial-Golgi compartment. J Exp Med 1992; 176: 729-738.
70. Ziegler H, Thale R, Lucin P, Muranyi W, Flohr T, Hengel H et al. A mouse cytomegalovirus glycoprotein retains MHC class I complexes in the ERGIC/cis-Golgi compartments. Immunity 1997; 6: 57-66.
71. Hengel H, Reusch U, Gutermann A, Ziegler H, Jonjic S, Lucin P et al. Cytomegaloviral control of MHC class I function in the mouse. Immunol Rev 1999; 168: 167-176.
72. Kleijnen MF, Huppa JB, Lucin P, Mukherjee S, Farrell H, Campbell AE et al. A mouse cytomegalovirus glycoprotein, gp34, forms a complex with folded class I MHC molecules in the ER which is not retained but is transported to the cell surface. EMBO J 1997; 16: 685-694.
73. Reusch U, Muranyi W, Lucin P, Burgert HG, Hengel H, Koszinowski UH. A cytomegalovirus glycoprotein re-routes MHC class I complexes to lysosomes for degradation. EMBO J 1999; 18: 1081-1091.
74. Wagner M, Gutermann A, Podlech J, Reddehase MJ, Koszinowski UH. Major histocompatibility complex class I allele-specific cooperative and competitive interactions between immune evasion proteins of cytomegalovirus. J Exp Med 2002; 16: 805-816.
75. Ilic Tomas M, Kucic N, Mahmutefendic H, Blagojevic G, Lucin P. Murine cytomegalovirus perturbs endosomal trafficking of MHC class I molecules in the early phase of infection. J Virol 2010; 84: 11101-11112.
76. Mahmutefendic H, Blagojevic G, Kucic N, Lucin P. Constitutive internalization of murine MHC class I molecules. J Cell Physiol 2007; 210: 445-455.
77. Kucic N, Ilic Tomas M, Mahmutefendic H, Blagojevic G, Lucin P. Early endosomal retention of murine cytomegalovirus m06 protein. Croat Chem Acta 2012; 85: 213-221.
78. Lenac T, Budt M, Arapovic J, Hasan M, Zimmermann A, Simic H et al. The herpesviral Fc receptor fcr-1down-regulates the NKG2D ligands MULT-1 and H60. J Exp Med 2006; 203: 1843-1850.
79. Jefferies WA, Burgert GH. E3/19K from adenovirus 2 is an immunosubversive protein that binds to a structural motif regulating the intracellular transport of major histocompatibility complex class I proteins. J ExpMed 1990; 172: 1653-1664.
80. Sanchez V, Greis KD, Sztul E, BrittWJ. Accumulation of virion tegument and envelope proteins in a stable cytoplasmic compartment during human cytomegalovirus replication: characterization of a potential site of virus assembly. J Virol 2000; 74: 975-986.
81. Homman-Loudiyi M, Hultenby K, Britt W, Soderberg-Naucler C. Envelopment of human cytomegalovirus occurs by budding into Golgi derived vacuole compartments positive for gB, Rab 3, trans- Golgi network 46, and mannosidase II. J Virol 2003; 77: 3191-3203.
82. Fraile-Ramos A, Pelchen-Matthews A, Kledal TN, Browne H, Schwartz TW, Marsh M. Localization of HCMV UL33 and US27 in endocytic compartments and viral membranes. Traffic 2002; 3: 218-232.
83. Seo JY, Britt WJ. Sequence requirements for localization of human cytomegalovirus tegument protein pp28 to the virus assembly compartment and for assembly of infectious virus. J Virol 2006; 80: 5611-5626.
84. Das S, Vasanji A, Pellett PE. Three dimensional structure of the human cytomegalovirus cytoplasmic virion assembly complex includes a reoriented secretory apparatus. J Virol 2007; 81: 11861-11869.
85. Schauflinger M, Fischer D, Schreiber A, Chevillotte M, Walther P, Mertens T et al. The tegument protein UL71 of human cytomegalovirus is involved in late envelopment and affects multivesicular bodies. J Virol 2011; 85: 3821-3832.
86. Tandon R, Mocarski ES. Viral and host control of cytomegalovirus maturation. Trends Microbiol 2012; 20: 392-401.
87. Cepeda V, Esteban M, Fraile-Ramos A. Human cytomegalovirus final envelopment on membranes containing both trans-Golgi network and endosomal markers. Cell Microbiol 2010; 12: 386-404.
88. Das S, Pellett PE. Spatial relationships between markers for secretory and endosomal machinery in human cytomegalovirusinfected cells versus those in uninfected cells. J Virol 2011; 85: 5864-5879.
89. Hertel L, Mocarski ES. Global analysis of host cell gene expression late during cytomegalovirus infection reveals extensive dysregulation of cell cycle expression and induction of pseudomitosis independent of US28 function. J Virol 2004; 78: 11988-12011.
90. Tooze J, Hollinshead M, Reis B, Radsak K, Kern H. Progeny vaccinia and human cytomegalovirus particles utilize early endosomal cisternae for their envelopes. Eur J Cell Biol 1993; 60: 163-178.
91. Fraile-Ramos A, Cepeda V, Elstak E, van der Sluijs P. Rab27a is required for human cytomegalovirus assembly. PLoS One 2010; 5: e15318.
92. Krzyzaniak MA, Mach M, Britt WJ. HCMV-encoded glycoprotein M (UL100) interacts with Rab11 effector protein FIP4. Traffic 2009; 10: 1439-1457.
93. Hook LM, Grey F, Grabski R, Tirabassi R, Doyle T, Hancock M et al. Cytomegalovirus miRNAs target secretory pathway genes to facilitate formation of the virion assembly compartment and reduce cytokine secretion. Cell Host Microbe 2014; 15: 363-373.
94. Hengel H, Koopmann JO, Flohr T, Muranyi W, Goulmy E, Hammerling GJ et al. A viral ER-resident glycoprotein inactivates the MHC-encoded peptide transporter. Immunity 1997; 6: 623-632.
95. Wiertz EJ, Jones TR, Sun L, Bogyo M, Geuze HJ, Ploegh HL. The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell 1996; 84: 769-779.
96. Wiertz EJ, Tortorella D, Bogyo M, Yu J, Mothes W, Jones TR et al. Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 1996; 384: 432-438.
97. Ahn K, Angulo A, Ghazal P, Peterson PA, Yang Y, Fruh K. Human cytomegalovirus inhibits antigen presentation by a sequential multistep process. Proc Natl Acad Sci USA 1996; 93: 10990-10995.
98. Jones TR, Wiertz EJ, Sun L, Fish KN, Nelson JA, Ploegh HL. Human cytomegalovirus US3 impairs transport and maturation of major histocompatibility complex class I heavy chains. Proc Natl Acad Sci USA 1996; 93: 11327-11333.
99. Barnes PD, Grundy JE. Down-regulation of the class I HLA heterodimer and b2-microglobulin on the surface of cells infected with cytomegalovirus. J Gen Virol 1992; 73: 2395-2403.
100. Fairley JA, Baillie J, Bain M, Sinclair JH. Human cytomegalovirus infection inhibits epidermal growth factor (EGF) signalling by targeting EGF receptors. J Gen Virol 2002; 83: 2803-2810.
101. Hassink GC, Duijvestijn-van Dam JG, Koppers-Lalic D, van Gaansvan den Brink J, van Leeuwen D, Vink C et al. Rat cytomegalovirus induces a temporal downregulation of major histocompatibility complex class I cell surface expression. Viral Immunol 2005; 18: 607-615.
102. Baca Jones CC, Kreklywich CN, Messaoudi I, Vomaske J, McCartney E, Orloff SL et al. Rat cytomegalovirus infection depletes MHC II in bone marrow derived dendritic cells. Virology 2009; 388: 78-90.
103. Emery VC, Cope AV, Bowen EF, Gor D, Griffiths PD. The dynamics of human cytomegalovirus replication in vivo. J Exp Med 1999; 190: 177-182.
104. Riegler S, Hebart H, Einsele H, Brossart P, Jahn G, Sinzger C. Monocyte-derived dendritic cells are permissive to the complete replicative cycle of human cytomegalovirus. J Gen Virol 2000; 81: 393-399.
105. 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.
106. Odeberg J, Soderberg-Naucler C. Reduced expression of HLA class II molecules and Iinterleukin-10- and transforming growth factor beta1-independent suppression of T-cell proliferation in human cytomegalovirus-infected macrophage cultures. J Virol 2001; 75: 5174-5181.
107. Spencer JV, Lockridge KM, Barry PA, Lin G, Tsang M, Penfold ME et al. Potent immunosuppressive activities of cytomegalovirusencoded interleukin-10. J Virol 2002; 76: 1285-1292.
108. Lee AW, Hertel L, Louie RK, Burster T, Lacaille V, Pashine A et al. Human cytomegalovirus alters localization of MHC class II and dendrite morphology in mature Langerhans cells. J Immunol 2006; 177: 3960-3971.
109. Cebulla CM, Miller DM, Zhang Y, Rahill BM, Zimmerman P, Robinson JM et al. Human cytomegalovirus disrupts constitutive MHC class II expression. J Immunol 2002; 169: 167-176.
110. Loewendorf AI, Steinbrueck L, Peter C, Busche A, Benedict CA, Kay- Jackson PC. The mouse cytomegalovirus glycoproteinm155inhibits CD40 expression and restricts CD4 T cell responses. J Virol 2011; 85: 5208-5212.
111. Mintern JD, Klemm EJ, Wagner M, Paquet ME, Napier MD, Kim YM et al. Viral interference with B7-1 costimulation: a new role for murine cytomegalovirus Fc receptor-1. J Immunol 2006; 177: 8422-8431.
112. Moutaftsi M, Mehl AM, Borysiewicz LK, Tabi Human Z. cytomegalovirus inhibits maturation and impairs function of monocytederived dendritic cells. Blood 2002, 99: 2913-2921.
113. Hertel L, Lacaille VG, Strobl H, Mellins ED, Mocarski ES. Susceptibility of immature and mature Langerhans cell-type dendritic cells to infection and immunomodulation by human cytomegalovirus. J Virol 2003; 77: 7563-7574.
114. Beck K, Meyer-Konig U, Weidmann M, Nern C, Hufert FT. Human cytomegalovirus impairs dendritic cell function: a novel mechanism of human cytomegalovirus immune escape. Eur J Immunol 2003; 33: 1528-1538.
115. Reeves M, Sinclair J. Regulation of human cytomegalovirus transcription in latency: beyond the mayor immediate-early promoter. Viruses 2013; 5: 1395-1413.
116. Slobedman B, Mocarski ES, Arvin AM, Mellins ED, Abendroth A. Latent cytomegalovirus down-regulates major histocompatibility complex class II expression on myeloid progenitors. Blood 2002; 100: 2867-2873
117. Bacon L, Eagle RA, Meyer M, Easom N, Young NT, Trowsdale J. Two human ULBP/RAET1 molecules with transmembrane regions are ligands for NKG2D. J Immunol 2004; 178: 21078-21084.
118. Nachmani D, Lankry D, Wolf DG, Mandelboim O. The human cytomegalovirus microRNA miR-UL112 acts synergistically with a cellular microRNA to escape immune elimination. Nat Immunol 2010; 11: 806-813.
119. Muller S, Zocher G, Steinle A, Stehle T. Structure of the HCMV UL16-MICB complex elucidates select binding of a viral immunoevasin to diverse NKG2D ligands. PloS Pathog 2010; 6: 1000723.
120. Ashiru O, Bennett NJ, Boyle LH, Thomas M, Trowsdale J, Wills MR. NKG2D ligand MICA is retained in the cis-Golgi apparatus by human cytomegalovirus protein UL142. J Virol 2009; 83: 12345-12354.
121. Fielding CA, Aicheler R, Stanton RJ, Wang EC, Han S, Seirafian S. Two novel human cytomegalovirus NK cell evasion functions target MICA for lysosomal degradation. PLoS Pathog 2014; 10: e1004058.
122. Aguera-Gonzalez S, Boutet P, Reyburn HT, Vales-Gomez M. Brief residence at the plasma membrane of the MHC class I-related chain B is due to clathrin-mediated cholesterol-dependent endocytosis and shedding. J Immunol 2009; 182: 4800-4808.
123. Hill A, Jugovic P, York I, Russ G, Bennink J, Yewdell J et al. Herpes simplex virus turns off the TAP to evade host immunity. Nature 1995; 375: 411-415.
124. Fruh K, Ahn K, Djaballah H, Sempe P, van Endert PM, Tampe R, et al. A viral inhibitor of peptide transporters for antigen presentation. Nature 1995; 375: 415-418.
125. Levitskaya J, Coram M, Levitsky V, Imreh S, Steigerwald-Mullen PM, Klein G et al. Inhibition of antigen processing by the internal repeat region of the Epstein-Barr virus nuclear antigen-1. Nature 1995; 375: 685-688.
126. Kwun HJ, da Silva SR, Shah IM, Blake N, Moore PS, Chang Y. Kaposis sarcoma-associated herpesvirus latency-associated nuclear antigen 1 mimics Epstein-Barr virus EBNA1 immune evasion through central repeat domain effects on protein processing. J Virol 2007; 81: 8225-8235.
127. Bennett NJ, May JS, Stevenson PG. Gamma-herpesvirus latency requires T cell evasion during episome maintenance. PLoS Biol 2005; 3: e120.
128. Abendroth A, Lin I, Slobedman B, Ploegh H, Arvin AM. Varicellazoster virus retains major histocompatibility complex class I proteins in the Golgi compartment of infected cells. J Virol 2001; 75: 4878-4888.
129. Hudson AW, Howley PM, Ploegh HL. A human herpesvirus 7 glycoprotein, U21, diverts major histocompatibility complex class I molecules to lysosomes. J Virol 2001; 75: 12347-12358.
130. May NA, Glosson NL, Hudson AW. HHV-7 U21 downregulates classical and non-classical class I MHC molecules from the cell surface. J Virol 2010; 84: 3738-3751.
131. Schneider CL, Hudson AW. The Human Herpesvirus-7 (HHV-7) U21 immunoevasin subverts NK-mediated cytotoxicity through modulation of MICA and MICB. PLoS Pathog 2011; 7: e1002362.
132. Sullivan BM, Coscoy L. Downregulation of the T cell receptor complex and impairment of T-cell activation by human herpesvirus 6 U24 protein. J Virol 2008; 82: 602-608.
133. Yuan W, Dasgupta A, Cresswell P. Herpes simplex virus evades natural killer T cell recognition by suppressing CD1d recycling. Nat Immunol 2006; 7: 835-842.
134. Raftery MJ, Winau F, Kaufmann SH, Schaible UE, Schonrich G. CD1 antigen presentation by human dendritic cells as a target for herpes simplex virus immune evasion. J Immunol 2006; 177: 6207-6214.
135. Imai T, Koyanagi N, Ogawa R, Shindo K, Suenaga T, Sato A et al. Us3 kinase encoded by herpes simplex virus 1 mediates downregulation of cell surface major histocompatibility complex class I and evasion of CD81 T cells. PLoS ONE 2013; 8: e72050.
136. Rappocciolo G, Birch J, Ellis SA. Down-regulation of MHC class I expression by equine herpesvirus-1. J Gen Virol 2003; 84: 293-300.
137. Said A, Azab W, Damiani A, Osterrieder N. Equine herpesvirus type 4 UL56 and UL49.5 proteins downregulate cell surface major histocompatibility complex class I expression independently of each other. J Virol 2012; 86: 8059-8071.
138. Koppers-Lalic D, Rijsewijk FA, Verschuren SB, van Gaans-Van den Brink JA, Neisig A, Ressing ME et al. The UL41-encoded virion host shutoff (vhs) protein and vhs-independent mechanisms are responsible for down-regulation of MHC class I molecules by bovine herpesvirus 1. J Gen Virol 2001; 82: 2071-2081.
139. Coscoy L, Ganem D. Kaposis sarcoma-associated herpesvirus encodes two proteins that block cell surface display of MHC class I chains by enhancing their endocytosis. Proc Natl Acad Sci USA 2000; 97: 8051-8056.
140. Ishido S, Wang C, Lee BS, Cohen GB, Jung JU. Downregulation of major histocompatibility complex class I molecules by Kaposis sarcoma-associated herpesvirus K3 and K5 proteins. J Virol 2000; 74: 5300-5309.
141. Duncan LM, Piper S, Dodd RB, Saville MK, Sanderson CM, Luzio JP et al. Lysine-63-linked ubiquitination is required for endolysosomal degradation of class I molecules. EMBO J 2006; 25: 1635-1645.
142. Hewitt EW, Duncan L, Mufti D, Baker J, Stevenson PG, Lehner PJ. Ubiquitylation of MHC class I by the K3 viral protein signals internalization and TSG101-dependent degradation. EMBO J 2002; 21: 2418-2429.
143. Coscoy L, Ganem D. A viral protein that selectively downregulates ICAM-1 and B7-2 and modulates T cell costimulation. J Clin Invest 2001; 107: 1599-1606.
144. Sanchez DJ, Gumperz JE, Ganem D. Regulation of CD1d expression and function by a herpesvirus infection. J Clin Invest 2005; 115: 1369-1378.
145. Thomas M, Wills M, Lehner PJ. Natural killer cell evasion by an E3 ubiquitin ligase from Kaposis sarcoma-associated herpesvirus. Biochem Soc Trans 2008; 36: 459-463.
146. Mansouri M, Douglas J, Rose PP, Gouveia K, Thomas G, Means RE et al. Kaposi sarcoma herpesvirus K5 removes CD31/PECAM from endothelial cells. Blood 2006; 108: 1932-1940.
147. Bartee E, McCormack A, Fruh K. Quantitative membrane proteomics reveals new cellular targets of viral immune modulators. PLoS Pathog 2006; 2: e107.
148. Li Q, Means R, Lang S, Jung JU. Downregulation of gamma interferon receptor 1 by Kaposis sarcoma-associated herpesvirus K3 and K5. J Virol 2007; 81: 2117-2127.
149. Zuo J, Currin A, Griffin BD, Shannon-Lowe C, Thomas WA, Ressing ME et al. The Epstein-Barr virus G-protein coupled receptor contributes to immune evasion by targeting MHC class I molecules for degradation. PLoS Pathog 2009; 5: e1000255.
150. Zuo J, Quinn LL, Tamblyn J, Thomas WA, Feederle R, Delecluse HJ et al. The Epstein-Barr virus-encoded BILF1 protein modulates immune recognition of endogenously processed antigen by targeting major histocompatibility complex class I molecules trafficking on both the exocytic and endocytic pathways. J Virol 2011; 85: 1604-1614.
151. Morrow G, Slobedman B, Cunningham AL, Abendroth A. Varicella zoster virus productively infects mature dendritic cells and alters their immune function. J Virol 2003; 77: 4950-4959.