The varicellovirus UL49.5 protein blocks the transporter associated with antigen processing (TAP) by inhibiting essential conformational transitions in the 6+6 transmembrane TAP core complex

Journal of Immunology

Volumn 181, Issue 7, 2008, Pages 4894-4907

  Verweij, Marieke C ^a   Koppers Lalic, Danijela ^a   Loch, Sandra ^b   Klauschies, Florian ^b   De La Salle, Henri ^c   Quinten, Edwin ^a   Lehner, Paul J ^d   Mulder, Arend ^a   Knittler, Michael R ^e   Tampé, Robert ^b   Koch, Joachim ^b,f   Ressing, Maaike E ^a   Wiertz, Emmanuel J H J ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b GOETHE UNIVERSITY   (Germany)

^c ETABLISSEMENT FRANÇAIS DU SANG   (France)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^f INSTITUTE FOR TUMOR BIOLOGY AND EXPERIMENTAL THERAPY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; TAPASIN; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1; UNCLASSIFIED DRUG; VARICELLOVIRUS UL49.5 PROTEIN; VIRUS PROTEIN; ABC TRANSPORTER; CARRIER PROTEIN; HLA ANTIGEN CLASS 1; MEMBRANE PROTEIN; PEPTIDE; TAP1 PROTEIN, HUMAN; TAP2 PROTEIN, HUMAN; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING (TAP); UL49.5 PROTEIN, BOVINE HERPESVIRUS TYPE 1; VIRUS ENVELOPE PROTEIN;

ARTICLE; CELL SURFACE; CONFORMATIONAL TRANSITION; CYTOSOL; CYTOTOXIC T LYMPHOCYTE; DELETION MUTANT; ENDOPLASMIC RETICULUM; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INFECTIOUS BOVINE RHINOTRACHEITIS VIRUS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN TRANSPORT; VARICELLA ZOSTER VIRUS; VIRUS DETECTION; WESTERN BLOTTING; WILD TYPE; ANIMAL; BIOSYNTHESIS; CELL CULTURE; CELL LINE; DIMERIZATION; DRUG ANTAGONISM; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN CONFORMATION; PROTEIN SECONDARY STRUCTURE; RAT; TUMOR CELL LINE;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CELL LINE, TRANSFORMED; CELL LINE, TUMOR; CELLS, CULTURED; DIMERIZATION; HERPESVIRUS 1, BOVINE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; PEPTIDES; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; RATS; VIRAL ENVELOPE PROTEINS;

EID: 58149316657     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.7.4894     Document Type: Article

References (78)

1. Lehner, P. J., and J. Trowsdale. 1998. Antigen presentation: coming out gracefully. Curr. Biol. 8: R605-R608.
2. Wright, C. A., P. Kozik, M. Zacharias, and S. Springer. 2004. Tapasin and other chaperones: models of the MHC class I loading complex. Biol. Chem. 385: 763-778. (Pubitemid 39335298)
3. Cresswell, P., A. L. Ackerman, A. Giodini, D. R. Peaper, and P. A. Wearsch. 2005. Mechanisms of MHC class I-restricted antigen processing and cross-presentation. Immunol. Rev. 207: 145-157. (Pubitemid 41415014)
4. Knittler, M. R., P. Alberts, E. V. Deverson, and J. C. Howard. 1999. Nucleotide binding by TAP mediates association with peptide and release of assembled MHC class I molecules. Curr. Biol. 9: 999-1008.
5. Neefjes, J. J., F. Momburg, and G. J. Hammerling. 1993. Selective and ATPdependent translocation of peptides by the MHC-encoded transporter. Science 261: 769-771. (Pubitemid 23278394)
6. Van Endert, P. M., L. Saveanu, E. W. Hewitt, and P. Lehner. 2002. Powering the peptide pump: TAP crosstalk with energetic nucleotides. Trends Biochem. Sci. 27: 454-461.
7. Koch, J., R. Guntrum, S. Heintke, C. Kyritsis, and R. Tampe. 2004. Functional dissection of the transmembrane domains of the transporter associated with antigen processing (TAP). J. Biol. Chem. 279: 10142-10147. (Pubitemid 38372619)
8. Wearsch, P. A., and P. Cresswell. 2007. Selective loading of high-affinity peptides onto major histocompatibility complex class I molecules by the tapasin- ERp57 heterodimer. Nat. Immunol. 8: 873-881. (Pubitemid 47099039)
9. Oliver, J. D., H. L. Roderick, D. H. Llewellyn, and S. High. 1999. ERp57 functions as a subunit of specific complexes formed with the ER lectins calreticulin and calnexin. Mol. Biol. Cell 10: 2573-2582.
10. Peh, C. A., N. Laham, S. R. Burrows, Y. Zhu, and J. McCluskey. 2000. Distinct functions of tapasin revealed by polymorphism in MHC class I peptide loading. J. Immunol. 164: 292-299.
11. Grandea, A. G., III, and L. Van Kaer. 2001. Tapasin: an ER chaperone that controls MHC class I assembly with peptide. Trends Immunol. 22: 194-199.
12. Peaper, D. R., P. A. Wearsch, and P. Cresswell. 2005. Tapasin and ERp57 form a stable disulfide-linked dimer within the MHC class I peptide-loading complex. EMBO J. 24: 3613-3623.
13. Grandea, A. G., III, M. J. Androlewicz, R. S. Athwal, D. E. Geraghty, and T. Spies. 1995. Dependence of peptide binding by MHC class I molecules on their interaction with TAP. Science 270: 105-108.
14. Bangia, N., P. J. Lehner, E. A. Hughes, M. Surman, and P. Cresswell. 1999. The N-terminal region of tapasin is required to stabilize the MHC class I loading complex. Eur. J. Immunol. 29: 1858-1870. (Pubitemid 29265541)
15. Garbi, N., N. Tiwari, F. Momburg, and G. J. Hammerling. 2003. A major role for tapasin as a stabilizer of the TAP peptide transporter and consequences for MHC class I expression. Eur. J. Immunol. 33: 264-273. (Pubitemid 36157664)
16. Lehner, P. J., M. J. Surman, and P. Cresswell. 1998. Soluble tapasin restores MHC class I expression and function in the tapasin-negative cell line. 220. Immunity 8: 221-231.
17. Papadopoulos, M., and F. Momburg. 2007. Multiple residues in the transmembrane helix and connecting peptide of mouse tapasin stabilize the transporter associated with the antigen-processing TAP2 subunit. J. Biol. Chem. 282: 9401-9410.
18. Tan, P., H. Kropshofer, O. Mandelboim, N. Bulbuc, G. J. Hammerling, and F. Momburg. 2002. Recruitment of MHC class I molecules by tapasin into the transporter associated with antigen processing-associated complex is essential for optimal peptide loading. J. Immunol. 168: 1950-1960. (Pubitemid 34135798)
19. Koch, J., R. Guntrum, and R. Tampe. 2006. The first N-terminal transmembrane helix of each subunit of the antigenic peptide transporter TAP is essential for independent tapasin binding. FEBS Lett. 580: 4091-4096. (Pubitemid 44037575)
20. Leonhardt, R. M., K. Keusekotten, C. Bekpen, and M. R. Knittler. 2005. Critical role for the tapasin-docking site of TAP2 in the functional integrity of the MHC class I-peptide-loading complex. J. Immunol. 175: 5104-5114.
21. Denis, M., E. Hanon, F. A. Rijsewijk, M. J. Kaashoek, J. T. van Oirschot, E. Thiry, and P. P. Pastoret. 1996. The role of glycoproteins gC, gE, gI, and gG in the induction of cell-mediated immune responses to bovine herpesvirus 1. Vet. Microbiol. 53: 121-132. (Pubitemid 27013950)
22. Abendroth, A., and A. Arvin. 1999. Varicella-zoster virus immune evasion. Immunol. Rev. 168: 143-156.
23. Arvin, A. M., M. Sharp, M. Moir, P. R. Kinchington, M. Sadeghi-Zadeh, W. T. Ruyechan, and J. Hay. 2002. Memory cytotoxic T cell responses to viral tegument and regulatory proteins encoded by open reading frames 4, 10, 29, and 62 of varicella-zoster virus. Viral Immunol. 15: 507-516.
24. + T cells against cytomegalovirus in very old subjects. J. Immunol. 179: 4283-4291.
25. Slezak, S. L., M. Bettinotti, S. Selleri, S. Adams, F. M. Marincola, and D. F. Stroncek. 2007. CMV pp65 and IE-1 T cell epitopes recognized by healthy subjects. J. Transl. Med. 5: 17.
26. + immunodominance among Epstein-Barr virus lytic cycle antigens directly reflects the efficiency of antigen presentation in lytically infected cells. J. Exp. Med. 201: 349-360.
27. Fruh, K., K. Ahn, H. Djaballah, P. Sempe, P. M. van Endert, R. Tampe, P. A. Peterson, and Y. Yang. 1995. A viral inhibitor of peptide transporters for antigen presentation. Nature 375: 415-418.
28. Hill, A., P. Jugovic, I. York, G. Russ, J. Bennink, J. Yewdell, H. Ploegh, and D. Johnson. 1995. Herpes simplex virus turns off the TAP to evade host immunity. Nature 375: 411-415.
29. Ahn, K., T. H. Meyer, S. Uebel, P. Sempe, H. Djaballah, Y. Yang, P. A. Peterson, K. Fruh, and R. Tampe. 1996. Molecular mechanism and species specificity of TAP inhibition by herpes simplex virus ICP47. EMBO J. 15: 3247-3255. (Pubitemid 26231930)
30. Tomazin, R., A. B. Hill, P. Jugovic, I. York, P. van Endert, H. L. Ploegh, D. W. Andrews, and D. C. Johnson. 1996. Stable binding of the herpes simplex virus ICP47 protein to the peptide binding site of TAP. EMBO J. 15: 3256-3266. (Pubitemid 26231931)
31. Aisenbrey, C., C. Sizun, J. Koch, M. Herget, R. Abele, B. Bechinger, and R. Tampe. 2006. Structure and dynamics of membrane-associated ICP47, a viral inhibitor of the MHC I antigen-processing machinery. J. Biol. Chem. 281: 30365-30372. (Pubitemid 44582092)
32. Ahn, K., A. Gruhler, B. Galocha, T. R. Jones, E. J. Wiertz, H. L. Ploegh, P. A. Peterson, Y. Yang, and K. Fruh. 1997. The ER-luminal domain of the HCMV glycoprotein US6 inhibits peptide translocation by TAP. Immunity 6: 613-621. (Pubitemid 27239352)
33. Hewitt, E. W., S. S. Gupta, and P. J. Lehner. 2001. The human cytomegalovirus gene product US6 inhibits ATP binding by TAP. EMBO J. 20: 387-396.
34. Lehner, P. J., J. T. Karttunen, G. W. Wilkinson, and P. Cresswell. 1997. The human cytomegalovirus US6 glycoprotein inhibits transporter associated with antigen processing-dependent peptide translocation. Proc. Natl. Acad. Sci. USA 94: 6904-6909. (Pubitemid 27281963)
35. Hengel, H., J. O. Koopmann, T. Flohr, W. Muranyi, E. Goulmy, G. J. Hammerling, U. H. Koszinowski, and F. Momburg. 1997. A viral ERresident glycoprotein inactivates the MHC-encoded peptide transporter. Immunity 6: 623-632. (Pubitemid 27239353)
36. Kyritsis, C., S. Gorbulev, S. Hutschenreiter, K. Pawlitschko, R. Abele, and R. Tampe. 2001. Molecular mechanism and structural aspects of transporter associated with antigen processing inhibition by the cytomegalovirus protein US6. J. Biol. Chem. 276: 48031-48039. (Pubitemid 37370704)
37. + T cell immune evasion protein specific to Epstein-Barr virus and its close relatives in Old World primates. J. Exp. Med. 204: 1863-1873.
38. Koppers-Lalic, D., E. A. Reits, M. E. Ressing, A. D. Lipinska, R. Abele, J. Koch, R. M. Marcondes, P. Admiraal, D. van Leeuwen, K. Bienkowska-Szewczyk, et al. 2005. Varicelloviruses avoid T cell recognition by UL49.5-mediated inactivation of the transporter associated with antigen processing. Proc. Natl. Acad. Sci. USA 102: 5144-5149. (Pubitemid 40503753)
39. Koppers-Lalic, D., M. C. Verweij, A. D. Lipinska, Y. Wang, E. Quinten, E. A. Reits, J. Koch, S. Loch, M. M. Rezende, F. Daus, et al. 2008. Varicellovirus UL 49.5 proteins differentially affect the function of the transporter associated with antigen processing, TAP. PLoS Pathog. 4: e1000080. (Pubitemid 351811516)
40. Reits, E. A., J. C. Vos, M. Gromme, and J. Neefjes. 2000. The major substrates for TAP in vivo are derived from newly synthesized proteins. Nature 404: 774-778.
41. Copeman, J., N. Bangia, J. C. Cross, and P. Cresswell. 1998. Elucidation of the genetic basis of the antigen presentation defects in the mutant cell line: 220 reveals polymorphism and alternative splicing of the tapasin gene. Eur. J. Immunol. 28: 3783-3791. (Pubitemid 28510789)
42. Salter, R. D., D. N. Howell, and P. Cresswell. 1985. Genes regulating HLA class I antigen expression in T-B lymphoblast hybrids. Immunogenetics 21: 235-246. (Pubitemid 15117182)
43. Momburg, F., V. Ortiz-Navarrete, J. Neefjes, E. Goulmy, Y. van de Wal, H. Spits, S. J. Powis, G. W. Butcher, J. C. Howard, and P. Walden. 1992. Proteasome subunits encoded by the major histocompatibility complex are not essential for antigen presentation. Nature 360: 174-177.
44. De la Salle, H., D. Hanau, D. Fricker, A. Urlacher, A. Kelly, J. Salamero, S. H. Powis, L. Donato, H. Bausinger, and M. Laforet. 1994. Homozygous human TAP peptide transporter mutation in HLA class I deficiency. Science 265: 237-241.
45. Meyer, T. H., P. M. van Endert, S. Uebel, B. Ehring, and R. Tampe. 1994. Functional expression and purification of the ABC transporter complex associated with antigen processing (TAP) in insect cells. FEBS Lett. 351: 443-447.
46. Barnstable, C. J., W. F. Bodmer, G. Brown, G. Galfre, C. Milstein, A. F. Williams, and A. Ziegler. 1978. Production of monoclonal antibodies to group A erythrocytes, HLA and other human cell surface antigens: new tools for genetic analysis. Cell 14: 9-20.
47. Parham, P., and F. M. Brodsky. 1981. Partial purification and some properties of BB7.2: a cytotoxic monoclonal antibody with specificity for HLA-A2 and a variant of HLA-A28. Hum. Immunol. 3: 277-299.
48. Mulder, A., M. J. Kardol, C. M. Uit het Broek, J. Tanke-Visser, N. T. Young, and F. H. Claas. 1998. A human monoclonal antibody against HLA-Cw1 and a human monoclonal antibody against an HLA-A locus determinant derived from a single uniparous female. Tissue Antigens 52: 393-396.
49. Van den Born, E., C. C. Posthuma, K. Knoops, and E. J. Snijder. 2007. An infectious recombinant equine arteritis virus expressing green fluorescent protein from its replicase gene. J. Gen. Virol. 88: 1196-1205. (Pubitemid 46523508)
50. Meyer, T. H., P. M. van Endert, S. Uebel, B. Ehring, and R. Tampe. 1994. Functional expression and purification of the ABC transporter complex associated with antigen processing (TAP) in insect cells. FEBS Lett. 351: 443-447.
51. Plewnia, G., K. Schulze, C. Hunte, R. Tampe, and J. Koch. 2007. Modulation of the antigenic peptide transporter TAP by recombinant antibodies binding to the last five residues of TAP1. J. Mol. Biol. 369: 95-107. (Pubitemid 46635432)
52. Van Endert, P. M., R. Tampe, T. H. Meyer, R. Tisch, J. F. Bach, and H. O. McDevitt. 1994. A sequential model for peptide binding and transport by the transporters associated with antigen processing. Immunity 1: 491-500. (Pubitemid 2142273)
53. Powis, S. J., A. R. Townsend, E. V. Deverson, J. Bastin, G. W. Butcher, and J. C. Howard. 1991. Restoration of antigen presentation to the mutant cell line RMA-S by an MHC-linked transporter. Nature 354: 528-531.
54. Knittler, M. R., K. Gulow, A. Seelig, and J. C. Howard. 1998. MHC class I molecules compete in the endoplasmic reticulum for access to transporter associated with antigen processing. J. Immunol. 161: 5967-5977.
55. Brodsky, F. M., P. Parham, C. J. Barnstable, M. J. Crumpton, and W. F. Bodmer. 1979. Monoclonal antibodies for analysis of the HLA system. Immunol. Rev. 47: 3-61. (Pubitemid 10173014)
56. Lipinska, A. D., D. Koppers-Lalic, M. Rychlowski, P. Admiraal, F. A. Rijsewijk, K. Bienkowska-Szewczyk, and E. J. Wiertz. 2006. Bovine herpesvirus 1 UL49.5 protein inhibits the transporter associated with antigen processing despite complex formation with glycoprotein M. J. Virol. 80: 5822-5832.
57. Seliger, B., U. Ritz, R. Abele, M. Bock, R. Tampe, G. Sutter, I. Drexler, C. Huber, and S. Ferrone. 2001. Immune escape of melanoma: first evidence of structural alterations in two distinct components of the MHC class I antigen processing pathway. Cancer Res. 61: 8647-8650. (Pubitemid 34013870)
58. Williams, A. P., C. A. Peh, A. W. Purcell, J. McCluskey, and T. Elliott. 2002. Optimization of the MHC class I peptide cargo is dependent on tapasin. Immunity 16: 509-520.
59. Bouabe, H., and M. R. Knittler. 2003. The distinct nucleotide binding states of the transporter associated with antigen processing (TAP) are regulated by the nonhomologous C-terminal tails of TAP1 and TAP2. Eur. J. Biochem. 270: 4531-4546. (Pubitemid 37452530)
60. Van Hall, T., S. Laban, D. Koppers-Lalic, J. Koch, C. Precup, P. Asmawidjaja, R. Offringa, and E. J. H. J. Wiertz. 2007. The varicellovirus- encoded TAP inhibitor UL49.5 regulates the presentation of CTL epitopes by Qa-1. J. Immunol. 178: 657-662. (Pubitemid 46095137)
61. Loch, S., F. Klauschies, C. Scholz, M. C. Verweij, E. J. Wiertz, J. Koch, and R. Tampe. 2008. Signaling of a varicelloviral factor across the endoplasmic reticulum membrane induces destruction of the peptide-loading complex and immune evasion. J. Biol. Chem. 283: 13428-13436.
62. Antoniou, A. N., S. Ford, E. S. Pilley, N. Blake, and S. J. Powis. 2002. Interactions formed by individually expressed TAP1 and TAP2 polypeptide subunits. Immunology 106: 182-189.
63. Lapinski, P. E., G. G. Miller, R. Tampe, and M. Raghavan. 2000. Pairing of the nucleotide binding domains of the transporter associated with antigen processing. J. Biol. Chem. 275: 6831-6840. (Pubitemid 30146223)
64. Boname, J. M., J. S. May, and P. G. Stevenson. 2005. The murine γ-herpesvirus- 68 MK3 protein causes TAP degradation independent of MHC class I heavy chain degradation. Eur. J. Immunol. 35: 171-179.
65. Boname, J. M., B. D. de Lima, P. J. Lehner, and P. G. Stevenson. 2004. Viral degradation of the MHC class I peptide loading complex. Immunity 20: 305-317. (Pubitemid 38388232)
66. Boname, J. M., and P. G. Stevenson. 2001. MHC class I ubiquitination by a viral PHD/LAP finger protein. Immunity 15: 627-636.
67. Stevenson, P. G., S. Efstathiou, P. C. Doherty, and P. J. Lehner. 2000. Inhibition of MHC class I-restricted antigen presentation by γ2-herpesviruses. Proc. Natl. Acad. Sci. USA 97: 8455-8460. (Pubitemid 30639694)
68. Wang, X., R. Connors, M. R. Harris, T. H. Hansen, and L. Lybarger. 2005. Requirements for the selective degradation of endoplasmic reticulum-resident major histocompatibility complex class I proteins by the viral immune evasion molecule mK3. J. Virol. 79: 4099-4108. (Pubitemid 40388348)
69. Wang, X., L. Lybarger, R. Connors, M. R. Harris, and T. H. Hansen. 2004. Model for the interaction of γherpesvirus 68 RING-CH finger protein mK3 with major histocompatibility complex class I and the peptide-loading complex. J. Virol. 78: 8673-8686. (Pubitemid 39025133)
70. Lybarger, L., X. Wang, M. R. Harris, H. W. Virgin, and T. H. Hansen. 2003. Virus subversion of the MHC class I peptide-loading complex. Immunity 18: 121-130. (Pubitemid 36120693)
71. + T cells aids amplification of a latent γ-herpesvirus. Nat. Immunol. 3: 733-740.
72. Pickart, C. M. 2001. Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70: 503-533.
73. Cadwell, K., and L. Coscoy. 2005. Ubiquitination on nonlysine residues by a viral E3 ubiquitin ligase. Science 309: 127-130. (Pubitemid 40934990)
74. Wang, X., R. A. Herr, W. J. Chua, L. Lybarger, E. J. Wiertz, and T. H. Hansen. 2007. Ubiquitination of serine, threonine, or lysine residues on the cytoplasmic tail can induce ERAD of MHC-I by viral E3 ligase mK3. J. Cell Biol. 177: 613-624. (Pubitemid 46799833)
75. Glavinas, H., P. Krajcsi, J. Cserepes, and B. Sarkadi. 2004. The role of ABC transporters in drug resistance, metabolism and toxicity. Curr. Drug Deliv. 1: 27-42.
76. Gillet, J. P., T. Efferth, and J. Remacle. 2007. Chemotherapy-induced resistance by ATP-binding cassette transporter genes. Biochim. Biophys. Acta 1775: 237-262. (Pubitemid 46899341)
77. Oosten, L. E., D. Koppers-Lalic, E. Blokland, A. Mulder, M. E. Ressing, T. Mutis, A. G. van Halteren, E. J. Wiertz, and E. Goulmy. 2007. TAP-inhibiting proteins US6, ICP47 and UL49.5 differentially affect minor and major histocompatibility antigen-specific recognition by cytotoxic T lymphocytes. Int. Immunol. 19: 1115-1122.
78. Chambers, B., P. Grufman, V. Fredriksson, K. Andersson, M. Roseboom, S. Laban, M. Camps, E. Z. Wolpert, E. J. Wiertz, R. Offringa, et al. 2007. Induction of protective CTL immunity against peptide transporter TAP-deficient tumors through dendritic cell vaccination. Cancer Res. 67: 8450-8455. (Pubitemid 47437417)