Viral evasion of the MHC class I antigen-processing machinery

Pflugers Archiv European Journal of Physiology

Volumn 451, Issue 3, 2005, Pages 409-417

  Loch, Sandra ^a   Tampé, Robert ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

ABC transporter; Antigen processing; Membrane proteins; MHC; Molecular immunology; Virus

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PEPTIDE;

ENDOPLASMIC RETICULUM; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; RECYCLING; REVIEW; VIRUS; VIRUS ADSORPTION; VIRUS ATTENUATION; VIRUS INTERFERENCE;

ANIMALS; ANTIGEN PRESENTATION; ATP-BINDING CASSETTE TRANSPORTERS; ENDOPLASMIC RETICULUM, ROUGH; GENES, MHC CLASS I; HERPESVIRIDAE INFECTIONS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; PROTEASOME ENDOPEPTIDASE COMPLEX; VIRAL PHYSIOLOGY; VIRULENCE FACTORS;

EID: 28344454052     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-005-1420-8     Document Type: Review

References (97)

1. Abele R, Tampé R (1999) Function of the transport complex TAP in cellular immune recognition. Biochim Biophys Acta 1461:405-419
2. Abele R, Tampé R (2004) The ABCs of immunology: structure and function of TAP, the transporter associated with antigen processing. Physiology 19:216-224
3. Abendroth A, Lin I, Slobedman B, Ploegh H, Arvin AM (2001) Varicella-zoster virus retains major histocompatibility complex class I proteins in the Golgi compartment of infected cells. J Virol 75:4878-4888
4. Ackerman AL, Kyritsis C, Tampé R, Cresswell P (2003) Early phagosomes in dendritic cells form a cellular compartment sufficient for cross presentation of exogenous antigens. Proc Natl Acad Sci USA 100:12889-12894
5. Ackerman AL, Cresswell P (2004) Cellular mechanisms governing cross-presentation of exogenous antigens. Nat Immunol 5:678-684
6. Ackerman AL, Kyritsis C, Tampé R, Cresswell P (2005) Access of soluble antigens to the endoplasmic reticulum can explain cross-presentation by dendritic cells. Nat Immunol 6:107-113
7. Ahn K, Meyer TH, Uebel S, Sempe P, Djaballah H, Yang Y, Peterson PA, Früh K, Tampé R (1996) Molecular mechanism and species specificity of TAP inhibition by herpes simplex virus ICP47. EMBO J 15:3247-3255
8. Ahn K, Gruhler A, Galocha B, Jones TR, Wiertz EJ, Ploegh HL, Peterson PA, Yang Y, Früh K (1997) The ER-luminal domain of the HCMV glycoprotein US6 inhibits peptide translocation by TAP. Immunity 6:613-621
9. Alexander M, Bor YC, Ravichandran KS, Hammarskjold ML, Rekosh D (2004) Human immunodeficiency virus type 1 Nef associates with lipid rafts to downmodulate cell surface CD4 and Class I major histocompatibility complex expression and to increase viral infectivity. J Virol 78:1685-1696
10. Ambagala AP, Hinkley S, Srikumaran S (2000) An early pseudorabies virus protein down-regulates porcine MHC class I expression by inhibition of transporter associated with antigen processing (TAP). J Immunol 164:93-99
11. Ambagala AP, Gopinath RS, Srikumaran S (2004) Peptide transport activity of the transporter associated with antigen processing (TAP) is inhibited by an early protein of equine herpesvirus-1. J Gen Virol 85:349-353
12. Andersson M, Paabo S, Nilsson T, Peterson PA (1985) Impaired intracellular transport of class I MHC antigens as a possible means for adenoviruses to evade immune surveillance. Cell 43:215-222
13. Barnett BC, Dolan A, Telford EA, Davison AJ, McGeoch DJ (1992) A novel herpes simplex virus gene (UL49A) encodes a putative membrane protein with counterparts in other herpesviruses. J Gen Virol 73:2167-2171
14. Bauer D, Tampé R (2002) Herpes viral proteins blocking the transporter associated with antigen processing TAP - from genes to function and structure. Curr Top Microbiol Immunol 269:87-99
15. Baumeister W, Walz J, Zühl F, Seemüller E (1998) The proteasome - paradigm of a self-compartmentalizing protease. Cell 92:367-380
16. Beier DC, Cox JH, Vining DR, Cresswell P, Engelhard VH (1994) Association of human class I MHC alleles with the adenovirus E3/19K protein. J Immunol 152:3862-3872
17. Beinert D, Neumann L, Uebel S, Tampé R (1997) Structure of the viral TAP-inhibitor ICP47 induced by membrane association. Biochemistry 36:4694-4700
18. Beismann-Driemeyer S, Tampé R (2004) Function of the antigen transport complex TAP in cellular immunity. Angew Chem Int Ed Engl 43:4014-4031
19. Bennett EM, Bennink JR, Yewdell JW, Brodsky FM (1999) Cutting edge: adenovirus E19 has two mechanisms for affecting class I MHC expression. J Immunol 162:5049-5052
20. Bigger JE, Martin DW (2004) Identification of an ICP47 homologue in simian agent 8 (SA8). Virus Genes 28:223-225
21. Blom D, Hirsch C, Stern P, Tortorella D, Ploegh HL (2004) A glycosylated type I membrane protein becomes cytosolic when peptide: N-glycanase is compromised. EMBO J 23:650-658
22. Boname JM, Stevenson PG (2001) MHC class I ubiquitination by a viral PHD/LAP finger protein. Immunity 15:627-636
23. Boname JM, de Lima BD, Lehner PJ, Stevenson PG (2004) Viral degradation of the MHC class I peptide loading complex. Immunity 20:305-317
24. Boname JM, May JS, Stevenson PG (2004) The murine gamma-herpesvirus-68 MK3 protein causes TAP degradation independent of MHC class I heavy chain degradation. Eur J Immunol 35:171-179
25. Browne H, Smith G, Beck S, Minson T (1990) A complex between the MHC class I homologue encoded by human cytomegalovirus and β2 microglobulin. Nature 347:770-772
26. Chapman TL, Bjorkman PJ (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
27. Coscoy L, Ganem D (2000) Kaposi's 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 97:8051-8056
28. Cox J, Bennink J, Yewdell J (1991) Retention of adenovirus E19 glycoprotein in the endoplasmic reticulum is essential to its ability to block antigen presentation. J Exp Med 174:1629-1637
29. Cox JH, Yewdell JW, Eisenlohr LC, Johnson PR, Bennink JR (1990) Antigen presentation requires transport of MHC class I molecules from the endoplasmic reticulum. Science 247:715-718
30. Cresswell P, Bangia N, Dick T, Diedrich G (1999) The nature of the MHC class I peptide loading complex. Immunol Rev 172:21-28
31. Fahnestock ML, Johnson JL, Feldman RM, Neveu JM, Lane WS, Bjorkman PJ (1995) The MHC class I homolog encoded by human cytomegalovirus binds endogenous peptides. Immunity 3:583-590
32. Farrell H, Degli-Esposti M, Densley E, Cretney E, Smyth M, Davis-Poynter N (2000) Cytomegalovirus MHC class I homologues and natural killer cells: an overview. Microbes Infect 2:521-532
33. Farrell HE, Vally H, Lynch DM, Fleming P, Shellam GR, Scalzo AA, Davis-Poynter NJ (1997) Inhibition of natural killer cells by a cytomegalovirus MHC class I homologue in vivo. Nature 386:510-514
34. Früh K, Ahn K, Djaballah H, Sempe P, van Endert PM, Tampé R, Peterson PA, Yang Y (1995) A viral inhibitor of peptide transporters for antigen presentation. Nature 375:415-418
35. Furman MH, Dey N, Tortorella D, Ploegh HL (2002) The human cytomegalovirus US10 gene product delays trafficking of major histocompatibility complex class I molecules. J Virol 76:11753-11756
36. Gewurz BE, Gaudet R, Tortorella D, Wang EW, Ploegh HL, Wiley DC (2001) From the cover: antigen presentation subverted: structure of the human cytomegalovirus protein US2 bound to the class I molecule HLA-A2. Proc Natl Acad Sci USA 98:6794-6799
37. Gorbulev S, Abele R, Tampé R (2001) Allosteric crosstalk between peptide-binding, transport, and ATP hydrolysis of the ABC transporter TAP. Proc Natl Acad Sci USA 98:3732-3737
38. Grandea AG, Van Kaer L (2001) Tapasin: an ER chaperone that controls MHC class I assembly with peptide. Trends Immunol 22:194-199
39. Gruhler A, Peterson PA, Früh K (2000) Human cytomegalovirus immediate early glycoprotein US3 retains MHC class I molecules by transient association. Traffic 1:318-325
40. Hengel H, Koopmann JO, Flohr T, Muranyi W, Goulmy E, Hammerling GJ, Koszinowski UH, Momburg F (1997) A viral ER-resident glycoprotein inactivates the MHC-encoded peptide transporter. Immunity 6:623-632
41. Hengel H, Brune W, Koszinowski UH (1998) Immune evasion by cytomegalovirus - survival strategies of a highly adapted opportunist. Trends Microbiol 6:190-197
42. Hewitt EW, Gupta SS, Lehner PJ (2001) The human cytomegalovirus gene product US6 inhibits ATP binding by TAP. EMBO J 20:387-396
43. Hewitt EW, Duncan L, Mufti D, Baker J, Stevenson PG, Lehner PJ (2002) Ubiquitylation of MHC class I by the K3 viral protein signals internalization and TSG101-dependent degradation. EMBO J 21:2418-2429
44. Hill A, Jugovic P, York I, Russ G, Bennink J, Yewdell J, Ploegh H, Johnson D (1995) Herpes simplex virus turns off the TAP to evade host immunity. Nature 375:411-415
45. Hudson AW, Howley PM, Ploegh HL (2001) A human herpesvirus 7 glycoprotein, U21, diverts major histocompatibility complex class I molecules to lysosomes. J Virol 75:12347-12358
46. Hudson AW, Blom D, Howley PM, Ploegh HL (2003) The ER-lumenal domain of the HHV-7 immunoevasin U21 directs class I MHC molecules to lysosomes. Traffic 4:824-837
47. Ishido S, Wang C, Lee BS, Cohen GB, Jung JU (2000) Downregulation of major histocompatibility complex class I molecules by Kaposi's sarcoma-associated herpesvirus K3 and K5 proteins. J Virol 74:5300-5309
48. Jackson MR, Nilsson T, Peterson PA (1990) Identification of a consensus motif for retention of transmembrane proteins in the endoplasmic reticulum. EMBO J 9:3153-3162
49. Jugovic P, Hill AM, Tomazin R, Ploegh H, Johnson DC (1998) Inhibition of major histocompatibility complex class I antigen presentation in pig and primate cells by herpes simplex virus type 1 and 2 ICP47. J Virol 72:5076-5084
50. Kasper MR, Roeth JF, Williams M, Filzen TM, Fleis RI, Collins KL (2005) HIV-1 Nef disrupts antigen presentation early in the secretory pathway. J Biol Chem 280:12840-12848
51. Kavanagh DG, Gold MC, Wagner M, Koszinowski UH, Hill AB (2001) The multiple immune-evasion genes of murine cytomegalovirus are not redundant: m4 and m152 inhibit antigen presentation in a complementary and cooperative fashion. J Exp Med 194:967-978
52. Kerkau T, Bacik I, Bennink JR, Yewdell JW, Hunig T, Schimpl A, Schubert U (1997) The human immunodeficiency virus type 1 (HIV-1) Vpu protein interferes with an early step in the biosynthesis of major histocompatibility complex (MHC) class I molecules. J Exp Med 185:1295-1305
53. Kleijnen MF, Huppa JB, Lucin P, Mukherjee S, Farrell H, Campbell AE, Koszinowski UH, Hill AB, Ploegh HL (1997) 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 16:685-694
54. Koppers-Lalic D, Rijsewijk FA, Verschuren SB, van Gaans-Van den Brink JA, Neisig A, Ressing ME, Neefjes J, Wiertz EJ (2001) 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 82:2071-2081
55. Koppers-Lalic D, Reits EAD, Ressing ME, Lipinska AD, Abele R, Koch J, Rezende MM, Admiraal P, van Leeuwen D, Bienkowska-Szewczyk K, Mettenleiter TC, Rijsewijk FA, Tampé R, Neefjes JJ, Wiertz EJ (2005) Varicelloviruses avoid T cell recognition by UL49.5-mediated inactivation of the Transporter associated with Antigen Processing (TAP). Proc Natl Acad Sci USA 102:5144-5149
56. Kyritsis C, Gorbulev S, Hutschenreiter S, Pawlitschko K, Abele R, Tampé R (2001) Molecular mechanism and structural aspects of transporter associated with antigen processing inhibition by the cytomegalovirus protein US6. J Biol Chem 276:48031-48039
57. Le Gall S, Erdtmann L, Benichou S, Berlioz-Torrent C, Liu L, Benarous R, Heard JM, Schwartz O (1998) Nef interacts with the mu subunit of clathrin adaptor complexes and reveals a cryptic sorting signal in MHC I molecules. Immunity 8:483-495
58. Lee S, Yoon J, Park B, Jun Y, Jin M, Sung HC, Kim I-H, Kang S, Choi E-J, Ahn BY, Ahn K (2000) Structural and functional dissection of human cytomegalovirus US3 in binding major histocompatibility complex Class 1 molecules. J Virol 74:11262-11269
59. Lehner PJ, Karttunen JT, Wilkinson GW, Cresswell P (1997) The human cytomegalovirus US6 glycoprotein inhibits transporter associated with antigen processing-dependent peptide translocation. Proc Natl Acad Sci USA 94:6904-6909
60. Levitskaya J, Sharipo A, Leonchiks A, Ciechanover A, Masucci MG (1997) Inhibition of ubiquitin/proteasome-dependent protein degradation by the Gly-Ala repeat domain of the Epstein-Barr virus nuclear antigen 1. Proc Natl Acad Sci USA 94:12616-12621
61. Liang X, Chow B, Raggo C, Babiuk L (1996) Bovine herpesvirus 1 UL49.5 homolog gene encodes a novel viral envelope protein that forms a disulfide-linked complex with a second virion structural protein. J Virol 70:1448-1454
62. Lilley BN, Tortorella D, Ploegh HL (2003) Dislocation of a type I membrane protein requires interactions between membrane-spanning segments within the lipid bilayer. Mol Biol Cell 14:3690-3698
63. Lilley BN, Ploegh HL (2004) A membrane protein required for dislocation of misfolded proteins from the ER. Nature 429:834-840
64. Lybarger L, Wang X, Harris MR, Virgin HWt, Hansen TH (2003) Virus subversion of the MHC class I peptide-loading complex. Immunity 18:121-130
65. Means RE, Ishido S, Alvarez X, Jung JU (2002) Multiple endocytic trafficking pathways of MHC class I molecules induced by a Herpesvirus protein. EMBO J 21:1638-1649
66. Misaghi S, Sun Z-YJ, Stern P, Gaudet R, Wagner G, Ploegh H (2004) Structural and functional analysis of human cytomegalovirus US3 protein. J Virol 78:413-423
67. Neumann L, Kraas W, Uebel S, Jung G, Tampé R (1997) The active domain of the herpes simplex virus protein ICP47: a potent inhibitor of the transporter associated with antigen processing. J Mol Biol 272:484-492
68. Neumann L, Tampé R (1999) Kinetic analysis of peptide binding of the TAP transporter complex: evidence for structural rearrangements induced by substrate binding. J Mol Biol 294:1203-1213
69. Park B, Oh H, Lee S, Song Y, Shin J, Sung YC, Hwang SY, Ahn K (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
70. Park B, Kim Y, Shin J, Lee S, Cho K, Früh K, Ahn K (2004) Human cytomegalovirus inhibits tapasin-dependent peptide loading and optimization of the MHC class I peptide cargo for immune evasion. Immunity 20:71-85
71. Pfänder R, Neumann L, Zweckstetter M, Seger C, Holak TA, Tampé R (1999) Structure of the active domain of the herpes simplex virus protein ICP47 in water/sodium dodecyl sulfate solution determined by nuclear magnetic resonance spectroscopy. Biochemistry 38:13692-13698
72. Ploegh HL (1998) Viral strategies of immune evasion. Science 280:248-253
73. Reusch U, Muranyi W, Lucin P, Burgert HG, Hengel H, Koszinowski UH (1999) A cytomegalovirus glycoprotein reroutes MHC class I complexes to lysosomes for degradation. EMBO J 18:1081-1091
74. Reyburn HT, Mandelboim O, Vales-Gomez M, Davis DM, Pazmany L, Strominger JL (1997) The class I MHC homologue of human cytomegalovirus inhibits attack by natural killer cells. Nature 386:514-517
75. Schubert U, Anton LC, Gibbs J, Norbury CC, Yewdell JW, Bennink JR (2000) Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 404:770-774
76. Schwartz O, Marechal V, Le Gall S, Lemonnier F, Heard JM (1996) Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein. Nat Med 2:338-342
77. Severinsson L, Martens I, Peterson P (1986) Differential association between two human MHC class I antigens and an adenoviral glycoprotein. J Immunol 137:1003-1009
78. Shamu CE, Story CM, Rapoport TA, Ploegh HL (1999) The pathway of US11-dependent degradation of MHC class I heavy chains involves a ubiquitin-conjugated intermediate. J Cell Biol 147:45-58
79. Shamu CE, Flierman D, Ploegh HL, Rapoport TA, Chau V (2001) Polyubiquitination is required for US11-dependent movement of MHC class I heavy chain from endoplasmic reticulum into cytosol. Mol Biol Cell 12:2546-2555
80. Sharipo A, Imreh M, Leonchiks A, Imreh S, Masucci MG (1998) A minimal glycine-alanine repeat prevents the interaction of ubiquitinated I kappaB alpha with the proteasome: a new mechanism for selective inhibition of proteolysis. Nat Med 4:939-944
81. Signas C, Katze MG, Persson H, Philipson L (1982) An adenovirus glycoprotein binds heavy chains of class I transplantation antigens from man and mouse. Nature 299:175-178
82. Spiliotis ET, Osorio M, Zuniga MC, Edidin M (2000) Selective export of MHC class I molecules from the ER after their dissociation from TAP. Immunity 13:841-851
83. Stevenson PG, Efstathiou S, Doherty PC, Lehner PJ (2000) Inhibition of MHC class I-restricted antigen presentation by gamma 2-herpesviruses. Proc Natl Acad Sci USA 97:8455-8460
84. Tellam J, Connolly G, Green KJ, Miles JJ, Moss DJ, Burrows SR, Khanna R (2004) Endogenous presentation of CD8+ T cell epitopes from Epstein-Barr virus-encoded nuclear antigen 1. J Exp Med 199:1421-1431
85. Tomazin R, Hill AB, Jugovic P, York I, van Endert P, Ploegh HL, Andrews DW, Johnson DC (1996) Stable binding of the herpes simplex virus ICP47 protein to the peptide binding site of TAP. EMBO J 15:3256-3266
86. Tomazin R, van Schoot NEG, Goldsmith K, Jugovic P, Sempe P, Früh K, Johnson DC (1998) herpes simplex virus type 2 ICP47 inhibits human TAP but not mouse TAP. J Virol 72:2560-2563
87. Tsai B, Ye Y, Rapoport TA (2002) Retro-translocation of proteins from the endoplasmic reticulum into the cytosol. Nat Rev Mol Cell Biol 3:246-255
88. Uebel S, Tampé R (1999) Specificity of the proteasome and the TAP transporter. Curr Opin Immunol 11:203-208
89. Wagner M, Gutermann A, Podlech J, Reddehase MJ, Koszinowski UH (2002) Major histocompatibility complex class I allele-specific cooperative and competitive interactions between immune evasion proteins of cytomegalovirus. J Exp Med 196:805-816
90. Wang X, Lybarger L, Connors R, Harris MR, Hansen TH (2004) Model for the interaction of gammaherpesvirus 68 RING-CH finger protein mK3 with major histocompatibility complex class I and the peptide-loading complex. J Virol 78:8673-8686
91. Wiertz EJ, Jones TR, Sun L, Bogyo M, Geuze HJ, Ploegh HL (1996) The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell 84:769-779
92. Wiertz EJ, Tortorella D, Bogyo M, Yu J, Mothes W, Jones TR, Rapoport TA, Ploegh HL (1996) Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 384:432-438
93. Wu H, Kapoor P, Frappier L (2002) Separation of the DNA replication, segregation, and transcriptional activation functions of Epstein-Barr nuclear antigen 1. J Virol 76:2480-2490
94. Wu SX, Zhu XP, Letchworth GJ (1998) Bovine herpesvirus 1 glycoprotein M forms a disulfide-linked heterodimer with the U(L)49.5 protein. J Virol 72:3029-3036
95. Yin Y, Manoury B, Fahraeus R (2003) Self-inhibition of synthesis and antigen presentation by Epstein-Barr virus-encoded EBNA1. Science 301:1371-1374
96. Ziegler H, Thale R, Lucin P, Muranyi W, Flohr T, Hengel H, Farrell H, Rawlinson W, Koszinowski UH (1997) A mouse cytomegalovirus glycoprotein retains MHC class I complexes in the ERGIC/cis-Golgi compartments. Immunity 6:57-66
97. Ziegler H, Muranyi W, Burgert HG, Kremmer E, Koszinowski UH (2000) The luminal part of the murine cytomegalovirus glycoprotein gp40 catalyzes the retention of MHC class I molecules. EMBO J 19:870-881