Viral immune evasion molecules attack the ER peptide-loading complex and exploit ER-associated degradation pathways

Current Opinion in Immunology

Volumn 17, Issue 1, 2005, Pages 71-78

  Lybarger, Lonnie ^a   Wang, Xiaoli ^b   Harris, Michael ^b   Hansen, Ted H ^b  

^a UNIVERSITY OF ARIZONA   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; VIRUS PROTEIN;

ANTIGEN PRESENTATION; CELL SURFACE; ENDOPLASMIC RETICULUM; HOST PATHOGEN INTERACTION; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; VIRUS IMMUNITY; VIRUS TRANSMISSION;

ANIMALS; ANTIGEN PRESENTATION; ENDOPLASMIC RETICULUM; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; MULTIPROTEIN COMPLEXES; T-LYMPHOCYTES, CYTOTOXIC; VIRAL PROTEINS; VIRUSES;

EID: 11844257534     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.coi.2004.11.009     Document Type: Review

References (67)

1. J.L. Petersen, C.R. Morris, and J.C. Solheim Virus evasion of MHC class I molecule presentation J Immunol 171 2003 4473 4478
2. E.W. Hewitt The MHC class I antigen presentation pathway: strategies for viral immune evasion Immunology 110 2003 163 169
3. J.W. Yewdell, and A.B. Hill Viral interference with antigen presentation Nat Immunol 3 2002 1019 1025
4. J. Yewdell To DRiP or not to DRiP: generating peptide ligands for MHC class I molecules from biosynthesized proteins Mol Immunol 39 2002 139 146
5. J.W. Yewdell, E. Reits, and J. Neefjes Making sense of mass destruction: quantitating MHC class I antigen presentation Nat Rev Immunol 3 2003 952 961
6. M. Howarth, and T. Elliott The processing of antigens delivered as DNA vaccines Immunol Rev 199 2004 27 39
7. A.L. Ackerman, and P. Cresswell Cellular mechanisms governing cross-presentation of exogenous antigens Nat Immunol 5 2004 678 684
8. M. Bouvier Accessory proteins and the assembly of human class I MHC molecules: a molecular and structural perspective Mol Immunol 39 2003 697 706
9. C.M. Radcliffe, G. Diedrich, D.J. Harvey, R.A. Dwek, P. Cresswell, and P.M. Rudd Identification of specific glycoforms of major histocompatibility complex class I heavy chains suggests that class I peptide loading is an adaptation of the quality control pathway involving calreticulin and ERp57 J Biol Chem 277 2002 46415 46423
10. P.A. Wearsch, C.A. Jakob, A. Vallin, R.A. Dwek, P.M. Rudd, and P. Cresswell Major histocompatibility complex class I molecules expressed with monoglucosylated N-linked glycans bind calreticulin independently of their assembly status J Biol Chem 279 2004 25112 25121
11. T.P. Dick, N. Bangia, D.R. Peaper, and P. Cresswell Disulfide bond isomerization and the assembly of MHC class I-peptide complexes Immunity 16 2002 87 98
12. B. Ortmann, J. Copeman, P.J. Lehner, B. Sadasivan, J.A. Herberg, A.G. Grandea, S.R. Riddell, R. Tampe, T. Spies, J. Trowsdale, and P. Cresswell A critical role for tapasin in the assembly and function of multimeric MHC class I-TAP complexes Science 277 1997 1306 1309
13. B. Gao, R. Adhikari, M. Howarth, K. Nakamura, M.C. Gold, A.B. Hill, R. Knee, M. Michalak, and T. Elliott Assembly and antigen-presenting function of MHC class I molecules in cells lacking the ER chaperone calreticulin Immunity 16 2002 99 109
14. A.P. Williams, C.A. Peh, A.W. Purcell, J. McCluskey, and T. Elliott Optimization of the MHC class I peptide cargo is dependent on tapasin Immunity 16 2002 509 520
15. M.C. Gold, M.W. Munks, M. Wagner, C.W. McMahon, A. Kelly, D.G. Kavanagh, M.K. Slifka, U.H. Koszinowski, D.H. Raulet, and A.B. Hill Murine cytomegalovirus interference with antigen presentation has little effect on the size or the effector memory phenotype of the CD8 T cell response J Immunol 172 2004 6944 6953
16. A. Krmpotic, M. Messerle, I. Crnkovic-Mertens, B. Polic, S. Jonjic, and U.H. Koszinowski The immunoevasive function encoded by the mouse cytomegalovirus gene m152 protects the virus against T cell control in vivo J Exp Med 190 1999 1285 1296
17. + T-cell evasion.
18. P.G. Stevenson, J.S. May, X.G. Smith, S. Marques, H. Adler, U.H. Koszinowski, J.P. Simas, and S. Efstathiou K3-mediated evasion of CD8(+) T cells aids amplification of a latent gamma-herpesvirus Nat Immunol 3 2002 733 740
19. A. Hill, P. Jugovic, I. York, G. Russ, J. Bennink, J. Yewdell, H. Ploegh, and D. Johnson Herpes simplex virus turns off the TAP to evade host immunity Nature 375 1995 411 415
20. K. Fruh, K. Ahn, H. Djaballah, P. Sempe, P.M. van Endert, R. Tampe, P.A. Peterson, and Y. Yang A viral inhibitor of peptide transporters for antigen presentation Nature 375 1995 415 418
21. K. Ahn, A. Gruhler, B. Galocha, T.R. Jones, E.J. Wiertz, H.L. Ploegh, P.A. Peterson, Y. Yang, and K. Fruh The ER-luminal domain of the HCMV glycoprotein US6 inhibits peptide translocation by TAP Immunity 6 1997 613 621
22. H. Hengel, J.O. Koopmann, T. Flohr, W. Muranyi, E. Goulmy, G.J. Hammerling, U.H. Koszinowski, and F. Momburg A viral ER-resident glycoprotein inactivates the MHC-encoded peptide transporter Immunity 6 1997 623 632
23. P.J. Lehner, J.T. Karttunen, G.W. Wilkinson, and P. Cresswell The human cytomegalovirus US6 glycoprotein inhibits transporter associated with antigen processing-dependent peptide translocation Proc Natl Acad Sci USA 94 1997 6904 6909
24. D. Bauer, and R. Tampe Herpes viral proteins blocking the transporter associated with antigen processing TAP-from genes to function and structure Curr Top Microbiol Immunol 269 2002 87 99
25. F. Momburg, and H. Hengel Corking the bottleneck: the transporter associated with antigen processing as a target for immune subversion by viruses Curr Top Microbiol Immunol 269 2002 57 74
26. K. Ahn, T.H. Meyer, S. Uebel, P. Sempe, H. Djaballah, Y. Yang, P.A. Peterson, K. Fruh, and R. Tampe Molecular mechanism and species specificity of TAP inhibition by herpes simplex virus ICP47 EMBO J 15 1996 3247 3255
27. R. Tomazin, A.B. Hill, P. Jugovic, I. York, P. van Endert, H.L. Ploegh, D.W. Andrews, and D.C. Johnson Stable binding of the herpes simplex virus ICP47 protein to the peptide binding site of TAP EMBO J 15 1996 3256 3266
28. E.W. Hewitt, S.S. Gupta, and P.J. Lehner The human cytomegalovirus gene product US6 inhibits ATP binding by TAP EMBO J 20 2001 387 396
29. C. Kyritsis, S. Gorbulev, S. Hutschenreiter, K. Pawlitschko, R. Abele, and R. Tampe Molecular mechanism and structural aspects of transporter associated with antigen processing inhibition by the cytomegalovirus protein US6 J Biol Chem 276 2001 48031 48039
30. M. Andersson, S. Paabo, T. Nilsson, and P.A. Peterson Impaired intracellular transport of class I MHC antigens as a possible means for adenoviruses to evade immune surveillance Cell 43 1985 215 222
31. H.G. Burgert, and S. Kvist An adenovirus type 2 glycoprotein blocks cell surface expression of human histocompatibility class I antigens Cell 41 1985 987 997
32. E.M. Bennett, J.R. Bennink, J.W. Yewdell, and F.M. Brodsky Cutting edge: adenovirus E19 has two mechanisms for affecting class I MHC expression J Immunol 162 1999 5049 5052
33. T.R. Jones, E.J. Wiertz, L. Sun, K.N. Fish, J.A. Nelson, and H.L. Ploegh Human cytomegalovirus US3 impairs transport and maturation of major histocompatibility complex class I heavy chains Proc Natl Acad Sci USA 93 1996 11327 11333
34. K. Ahn, A. Angulo, P. Ghazal, P.A. Peterson, Y. Yang, and K. Fruh Human cytomegalovirus inhibits antigen presentation by a sequential multistep process Proc Natl Acad Sci USA 93 1996 10990 10995
35. A. Gruhler, P.A. Peterson, and K. Fruh Human cytomegalovirus immediate early glycoprotein US3 retains MHC class I molecules by transient association Traffic 1 2000 318 325
36. B. Park, Y. Kim, J. Shin, S. Lee, K. Cho, K. Fruh, S. Lee, and K. Ahn Human cytomegalovirus inhibits tapasin-dependent peptide loading and optimization of the MHC class I peptide cargo for immune evasion Immunity 20 2004 71 85 This is a demonstration that the HCMV protein US3 results in suboptimal peptide loading. US3 can be detected in physical association with tapasin, and also with class I and TAP. These data are consistent with US3 binding tapasin and impairing its role as a peptide editor.
37. C.A. Peh, S.R. Burrows, M. Barnden, R. Khanna, P. Cresswell, D.J. Moss, and J. McCluskey HLA-B27-restricted antigen presentation in the absence of tapasin reveals polymorphism in mechanisms of HLA class I peptide loading Immunity 8 1998 531 542
38. N.R. Hegde, R.A. Tomazin, T.W. Wisner, C. Dunn, J.M. Boname, D.M. Lewinsohn, and D.C. Johnson Inhibition of HLA-DR assembly, transport, and loading by human cytomegalovirus glycoprotein US3: a novel mechanism for evading major histocompatibility complex class II antigen presentation J Virol 76 2002 10929 10941
39. S. Misaghi, Z.Y. Sun, P. Stern, R. Gaudet, G. Wagner, and H. Ploegh Structural and functional analysis of human cytomegalovirus US3 protein J Virol 78 2004 413 423
40. P.G. Stevenson, S. Efstathiou, P.C. Doherty, and P.J. Lehner Inhibition of MHC class I-restricted antigen presentation by gamma 2-herpesviruses Proc Natl Acad Sci USA 97 2000 8455 8460
41. S. Ishido, C. Wang, B.S. Lee, G.B. Cohen, and J.U. Jung Downregulation of major histocompatibility complex class I molecules by Kaposi's sarcoma-associated herpesvirus K3 and K5 proteins J Virol 74 2000 5300 5309
42. L. Coscoy, and D. Ganem 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 2000 8051 8056
43. M. Mansouri, E. Bartee, K. Gouveia, B.T. Hovey Nerenberg, J. Barrett, L. Thomas, G. Thomas, G. McFadden, and K. Fruh The PHD/LAP-domain protein M153R of myxomavirus is a ubiquitin ligase that induces the rapid internalization and lysosomal destruction of CD4 J Virol 77 2003 1427 1440
44. •].
45. •] present evidence that human cellular homologs of K3 viral proteins have ubiquitin ligase activity and regulate immune molecules. These host proteins are likely to be the progenitors of viral K3 homologs that were stolen by the virus and exploited for immune evasion.
46. P.J. Lehner, and P. Cresswell Recent developments in MHC-class-I-mediated antigen presentation Curr Opin Immunol 16 2004 82 89
47. J.M. Boname, and P.G. Stevenson MHC class I ubiquitination by a viral PHD/LAP finger protein Immunity 15 2001 627 636
48. Y.Y. Yu, M.R. Harris, L. Lybarger, L.A. Kimpler, N.B. Myers, H.W. Virgin, and T.H. Hansen Physical association of the K3 protein of gamma-2 herpesvirus 68 with major histocompatibility complex class I molecules with impaired peptide and beta(2)-microglobulin assembly J Virol 76 2002 2796 2803
49. L. Lybarger, X. Wang, M.R. Harris, H.W. Virgin, and T.H. Hansen Virus subversion of the MHC class I peptide-loading complex Immunity 18 2003 121 130 The original report that TAP-tapasin are required for mK3 to specifically target the rapid degradation of nascent class I molecules.
50. X. Wang, L. Lybarger, R. Connors, M. Harris, and T.H. Hansen Model for the interaction of g-herpesvirus 68 RING-CH finger protein mK3 with MHC-I and the peptide-loading complex J Virol 78 2004 8673 8686
51. ••] represents a conceptual advance showing that TAP can be an mK3 substrate (at least in certain cell types) and that IFN-γ induction of mK3 is a mechanism by which it can coordinate its expression with that of class I.
52. E.W. Hewitt, L. Duncan, D. Mufti, J. Baker, P.G. Stevenson, and P.J. Lehner Ubiquitylation of MHC class I by the K3 viral protein signals internalization and TSG101-dependent degradation EMBO J 21 2002 2418 2429
53. L. Coscoy, D.J. Sanchez, and D. Ganem A novel class of herpesvirus-encoded membrane-bound E3 ubiquitin ligases regulates endocytosis of proteins involved in immune recognition J Cell Biol 155 2001 1265 1273
54. E.J. Wiertz, T.R. Jones, L. Sun, M. Bogyo, H.J. Geuze, and H.L. Ploegh The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol Cell 84 1996 769 779
55. E.J. Wiertz, D. Tortorella, M. Bogyo, J. Yu, W. Mothes, T.R. Jones, T.A. Rapoport, and H.L. Ploegh Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction Nature 384 1996 432 438
56. M. Kikkert, G. Hassink, M. Barel, C. Hirsch, F.J. van der Wal, and E. Wiertz Ubiquitination is essential for human cytomegalovirus US11-mediated dislocation of MHC class I molecules from the endoplasmic reticulum to the cytosol Biochem J 358 2001 369 377
57. C.E. Shamu, D. Flierman, H.L. Ploegh, T.A. Rapoport, and V. Chau Polyubiquitination is required for US11-dependent movement of MHC class I heavy chain from endoplasmic reticulum into cytosol Mol Biol Cell 12 2001 2546 2555
58. B.E. Gewurz, R. Gaudet, D. Tortorella, E.W. Wang, H.L. Ploegh, and D.C Wiley Antigen presentation subverted: Structure of the human cytomegalovirus protein US2 bound to the class I molecule HLA-A2 Proc Natl Acad Sci USA 98 2001 6794 6799
59. A.A. McCracken, and J.L. Brodsky Evolving questions and paradigm shifts in endoplasmic-reticulum-associated degradation (ERAD) Bioessays 25 2003 868 877
60. Z. Kostova, and D.H. Wolf For whom the bell tolls: protein quality control of the endoplasmic reticulum and the ubiquitin-proteasome connection EMBO J 22 2003 2309 2317
61. ••].
62. ••] show that US11 is associated with the newly defined Derlin-1 protein that might function as a pore required for US11-dislocation of class I from the ER lumen.
63. M. Knop, A. Finger, T. Braun, K. Hellmuth, and D.H. Wolf Der1, a novel protein specifically required for endoplasmic reticulum degradation in yeast EMBO J 15 1996 753 763
64. A.W. Purcell, J.J. Gorman, M. Garcia-Peydro, A. Paradela, S.R. Burrows, G.H. Talbo, N. Laham, C.A. Peh, E.C. Reynolds, J.A. Lopez De Castro, and J. McCluskey Quantitative and qualitative influences of tapasin on the class I peptide repertoire J Immunol 166 2001 1016 1027
65. D. Zernich, A.W. Purcell, W.A. Macdonald, L. Kjer-Nielsen, L.K. Ely, N. Laham, T. Crockford, N.A. Mifsud, M. Bharadwaj, and L. Chang Natural HLA class I polymorphism controls the pathway of antigen presentation and susceptibility to viral evasion J Exp Med 200 2004 13 24 This study provides supporting evidence for the authors' earlier proposal that PLC-independent class I molecules are selected in response to VIPRs.
66. S. Basta, and J.R. Bennink A survival game of hide and seek: cytomegaloviruses and MHC class I antigen presentation pathways Viral Immunol 16 2003 231 242
67. Wang X, Connors R, Harris MR, Hansen TH, Lybarger L: Requirements for the selective degradation of ER-resident MHC class I proteins by the viral immune evasion molecule, mK3. J Virology 2005, in press.