The macromolecular peptide-loading complex in MHC class I-dependent antigen presentation

Cellular and Molecular Life Sciences

Volumn 63, Issue 6, 2006, Pages 653-662

  Koch, J ^a   Tampe R ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

ABC transporter; Antigen processing; MHC class I; Peptide loading complex; TAP; Tapasin; Translocation pore

Indexed keywords

ABC TRANSPORTER; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MEMBRANE PROTEIN; PEPTIDE; PROTEASOME; TAPASIN; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1;

ANTIGEN PRESENTATION; CELL SURFACE; COMPLEX FORMATION; CYTOTOXIC T LYMPHOCYTE; EFFECTOR CELL; ENDOPLASMIC RETICULUM; HOST RESISTANCE; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REVIEW; RIBOSOME;

ANIMALS; ANTIGEN PRESENTATION; ANTIPORTERS; ATP-BINDING CASSETTE TRANSPORTERS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNOGLOBULINS; MEMBRANE TRANSPORT PROTEINS; MULTIPROTEIN COMPLEXES; PEPTIDES;

VERTEBRATA;

EID: 33645057449     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-005-5462-z     Document Type: Review

References (122)

1. Flajnik M. F. and Kasahara M. (2001) Comparative genomics of the MHC: glimpses into the evolution of the adaptive immune system. Immunity 15: 351-362
2. Pamer E. and Cresswell P. (1998) Mechanisms of MHC class I-restricted antigen processing. Annu. Rev. Immunol. 16: 323-358
3. Yewdell J. W., Reits E. and Neefjes J. (2003) Making sense of mass destruction: quantitating MHC class I antigen presentation. Nat. Rev. Immunol. 3: 952-961
4. Vossen M. T., Westerhout E. M., Soderberg-Naucler C. and Wiertz E. J. (2002) Viral immune evasion: a masterpiece of evolution. Immunogenetics 54: 527-542
5. Loch S. and Tampé. R. (2005) Viral evasion of the MHC class I antigen-processing machinery. Pflugers Arch. 451: 409-417
6. Hewitt E. W. (2003) The MHC class I antigen presentation pathway: strategies for viral immune evasion. Immunology 110: 163-169
7. Früh K., Ahn K. and Peterson P. A. (1997) Inhibition of MHC class I antigen presentation by viral proteins. J. Mol. Med. 75: 18-27
8. Rock K. L., Gramm C., Rothstein L., Clark K., Stein R., Dick L. et al. (1994) Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78: 761-771
9. Yewdell J. W., Anton L. C. and Bennink J. R. (1996) Defective ribosomal products (DRiPs): a major source of antigenic peptides for MHC class I molecules? J. Immunol. 157: 1823-1826
10. Kisselev A. F., Akopian T. N., Woo K. M. and Goldberg A. L. (1999) The sizes of peptides generated from protein by mammalian 26 and 20 S proteasomes: implications for understanding the degradative mechanism and antigen presentation. J. Biol. Chem. 274: 3363-3371
11. Reits E., Griekspoor A., Neijssen J., Groothuis T., Jalink K., Veelen P. van et al. (2003) Peptide diffusion, protection, and degradation in nuclear and cytoplasmic compartments before antigen presentation by MHC class I. Immunity 18: 97-108
12. Stoltze L., Schirle M., Schwarz G., Schroter C., Thompson M. W., Hersh L. B. et al. (2000) Two new proteases in the MHC class I processing pathway. Nat. Immunol. 1: 413-418
13. Reits E., Neijssen J., Herberts C., Benckhuijsen W., Janssen L., Drijfhout J. W. et al. (2004) A major role for TPPII in trimming proteasomal degradation products for MHC class I antigen presentation. Immunity 20: 495-506
14. Saric T., Chang S. C., Hattori A., York I. A., Markant S., Rock K. L. et al. (2002) An IFN-gamma-induced aminopeptidase in the E. R., ERAP1, trims precursors to MHC class I-presented peptides. Nat. Immunol. 3: 1169-1176
15. Saveanu L., Carroll O., Undo V., Del Val M., Lopez D., Lepelletier Y. et al. (2005) Concerted peptide trimming by human ERAP1 and ERAP2 aminopeptidase complexes in the endoplasmic reticulum. Nat. Immunol. 6: 689-697
16. Serwold T., Gonzalez F., Kim J., Jacob R. and Shastri N. (2002) ERAAP customizes peptides for MHC class I molecules in the endoplasmic reticulum. Nature 419: 480-483
17. Falk K., Rotzschke O., Stevanovic S., Jung G. and Rammensee H. G. (1991) Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature 351: 290-296
18. York I. A., Chang S. C., Saric T., Keys J. A., Favreau J. M., Goldberg A. L. et al. (2002) The ER aminopeptidase ERAP1 enhances or limits antigen presentation by trimming epitopes to 8-9 residues. Nat. Immunol. 3: 1177-1184
19. Antoniou A. N., Ford S., Pilley E. S., Blake N. and Powis S. J. (2002) Interactions formed by individually expressed TAP1 and TAP2 polypeptide subunits. Immunology 106: 182-189
20. Ortmann B., Copeman J., Lehner P. J., Sadasivan B., Herberg J. A., Grandea A. G. et al. (1997) A critical role for tapasin in the assembly and function of multimeric MHC class I-TAP complexes. Science 277: 1306-1309
21. Princiotta M. F., Finzi D., Qian S. B., Gibbs J., Schuchmann S., Buttgereit F. et al. (2003) Quantitating protein synthesis, degradation, and endogenous antigen processing. Immunity 18: 343-354
22. Momburg F., Roelse J., Hammerling G. J. and Neefjes J. J. (1994) Peptide size selection by the major histocompatibility complex-encoded peptide transporter. J. Exp. Med. 179: 1613-1623
23. Androlewicz M. J. and Cresswell P. (1994) Human transporters associated with antigen processing possess a promiscuous peptide-binding site. Immunity 1: 7-14
24. Endert P. M. van, Tampé, R., Meyer T. H., Tisch R., Bach J. F. and McDevitt H. O. (1994) A sequential model for peptide binding and transport by the transporters associated with antigen processing. Immunity 1: 491-500
25. Uebel S., Meyer T. H., Kraas W., Kienle S., Jung G., Wiesmuller K. H. et al. (1995) Requirements for peptide binding to the human transporter associated with antigen processing revealed by peptide scans and complex peptide libraries. J. Biol. Chem. 270: 18512-18516
26. Koopmann J. O., Post M., Neefjes J. J., Hämmerling G. J. and Momburg F. (1996) Translocation of long peptides by transporters associated with antigen processing (TAP). Eur. J. Immunol. 26: 1720-1728
27. Gromme M. and Neefjes J. (2002) Antigen degradation or presentation by MHC class I molecules via classical and non-classical pathways. Mol. Immunol. 39: 181-202
28. Neumann L. and Tampé, R. (1999) Kinetic analysis of peptide binding to the TAP transport complex: evidence for structural rearrangements induced by substrate binding. J. Mol. Biol. 294: 1203-1213
29. Kloetzel P. M. and Ossendorp F. (2004) Proteasome and peptidase function in MHC-class-I-mediated antigen presentation. Curr. Opin. Immunol. 16: 76-81
30. Uebel S. and Tampé, R. (1999) Specificity of the proteasome and the TAP transporter. Curr. Opin. Immunol. 11: 203-208
31. Uebel S., Kraas W., Kienle S., Wiesmuller K. H., Jung G. and Tampé. R. (1997) Recognition principle of the TAP transporter disclosed by combinatorial peptide libraries. Proc. Natl. Acad. Sci. USA 94: 8976-8981
32. Trowsdale J., Hanson I., Mockridge I., Beck S., Townsend A. and Kelly A. (1990) Sequences encoded in the class II region of the MHC related to the 'ABC' superfamily of transporters. Nature 348: 741-744
33. Spies T. and DeMars R. (1991) Restored expression of major histocompatibility class I molecules by gene transfer of a putative peptide transporter. Nature 351: 323-324
34. Powis S. J., Townsend A. R., Deverson E. V., Bastin J., Butcher G. W. and Howard J. C. (1991) Restoration of antigen presentation to the mutant cell line RMA-S by an MHC-linked transporter. Nature 354: 528-531
35. Gorbulev S., Abele R. and 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
36. Neumann L., Abele R. and Tampé, R. (2002) Thermodynamics of peptide binding to the transporter associated with antigen processing (TAP). J. Mol. Biol. 324: 965-973
37. Abele R. and Tampé, R. (1999) Function of the transport complex TAP in cellular immune recognition. Biochim. Biophys. Acta 1461: 405-419
38. Koch J., Guntrum R. and Tampé, R. (2005) Exploring the minimal functional unit of the transporter associated with antigen processing. FEBS Lett. 579: 4413-4416
39. Koch J., Guntrum R., Heintke S., Kyritsis C. and Tampé, R. (2004) Functional dissection of the transmembrane domains of the transporter associated with antigen processing (TAP). J. Biol. Chem. 279: 10142-10147
40. Nijenhuis M., Schmitt S., Armandola E. A., Obst R., Brunner J. and Hämmerling G. J. (1996) Identification of a contact region for peptide on the TAP1 chain of the transporter associated with antigen processing. J. Immunol. 156: 2186-2195
41. Nijenhuis M. and Hämmerling G. J. (1996) Multiple regions of the transporter associated with antigen processing (TAP) contribute to its peptide binding site. J. Immunol. 157: 5467-5477
42. Gaudet R. and Wiley D. C. (2001) Structure of the ABC ATPase domain of human TAP1, the transporter associated with antigen processing. EMBO J. 20: 4964-4972
43. Velarde G., Ford R. C., Rosenberg M. F. and Powis S. J. (2001) Three-dimensional structure of transporter associated with antigen processing (TAP) obtained by single particle image analysis. J. Biol. Chem. 276: 46054-46063
44. Dick T. P., Bangia N., Peaper D. R. and Cresswell P. (2002) Disulfide bond isomerization and the assembly of MHC class I-peptide complexes. Immunity 16: 87-98
45. Bangia N., Lehner P. J., Hughes E. A., Surman M. and Cresswell P. (1999) The N-terminal region of tapasin is required to stabilize the MHC class I loading complex. Eur. J. Immunol. 29: 1858-1870
46. Garbi N., Tiwari N., Momburg F. and Hammerling G. J. (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
47. Lehner P. J., Surman M. J. and Cresswell P. (1998) Soluble tapasin restores MHC class I expression and function in the tapasin-negative cell line.220. Immunity 8: 221-231
48. Raghuraman G., Lapinski P. E. and Raghavan M. (2002) Tapasin interacts with the membrane-spanning domains of both TAP subunits and enhances the structural stability of TAP1xTAP2 complexes. J. Biol. Chem. 277: 41786-41794
49. Garbi N., Tan P., Diehl A. D., Chambers B. J., Ljunggren H. G., Momburg F. et al. (2000) Impaired immune responses and altered peptide repertoire in tapasin-deficient mice. Nat. Immunol. 1: 234-238
50. Grandea A. G. 3rd and Van Kaer L. (2001) Tapasin: an ER chaperone that controls MHC class I assembly with peptide. Trends Immunol. 22: 194-199
51. Li S., Sjogren H. O., Hellman U., Pettersson R. F. and Wang P. (1997) Cloning and functional characterization of a subunit of the transporter associated with antigen processing. Proc. Natl. Acad. Sci. USA 94: 8708-8713
52. Williams A. P., Peh C. A., Purcell A. W., McCluskey J. and Elliott T. (2002) Optimization of the MHC class I peptide cargo is dependent on tapasin. Immunity 16: 509-520
53. Zarling A. L., Luckey C. J., Marto J. A., White F. M., Brame C. J., Evans A. M. et al. (2003) Tapasin is a facilitator, not an editor, of class I MHC peptide binding. J. Immunol. 171: 5287-5295
54. Tan P., Kropshofer H., Mandelboim O., Bulbuc N., Hämmerling G. J. and Momburg F. (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
55. Peaper D. R., Wearsch P. A. and Cresswell P. (2005) Tapasin and ERp57 form a stable disulfide-linked dimer within the MHC class I peptide-loading complex. EMBO J. 24: 3613-3623
56. Bangia N. and Cresswell P. (2005) Stoichiometric tapasin interactions in the catalysis of major histocompatibility complex class I molecule assembly. Immunology 114: 346-353
57. Turnquist H. R., Vargas S. E., Reber A. J., McIlhaney M. M., Li S., Wang P. et al. (2001) A region of tapasin that affects L(d) binding and assembly. J. Immunol. 167: 4443-4449
58. Harris M. R., Lybarger L., Myers N. B., Hilbert C., Solheim J. C., Hansen T. H. et al. (2001) Interactions of HLA-B27 with the peptide loading complex as revealed by heavy chain mutations. Int. Immunol. 13: 1275-1282
59. Madden D. R., Gorga J. C., Strominger J. L. and Wiley D. C. (1992) The three-dimensional structure of HLA-B27 at 2.1 Å resolution suggests a general mechanism for tight peptide binding to MHC. Cell 70: 1035-1048
60. Bjorkman P. J., Saper M. A., Samraoui B., Bennett W. S., Strominger J. L. and Wiley D. C. (1987) Structure of the human class I histocompatibility antigen, HLA-A2. Nature 329: 506-512
61. Helenius A. and Aebi M. (2001) Intracellular functions of N-linked glycans. Science 291: 2364-2369
62. Sadasivan B., Lehner P. J., Ortmann B., Spies T. and Cresswell P. (1996) Roles for calreticulin and a novel glycoprotein, tapasin, in the interaction of MHC class I molecules with TAP. Immunity 5: 103-114
63. Solheim J. C., Harris M. R., Kindle C. S. and Hansen T. H. (1997) Prominence of beta 2-microglobulin, class I heavy chain conformation, and tapasin in the interactions of class I heavy chain with calreticulin and the transporter associated with antigen processing. J. Immunol. 158: 2236-2241
64. Suh W. K., Cohen-Doyle M. F., Früh K., Wang K., Peterson P. A. and Williams D. B. (1994) Interaction of MHC class I molecules with the transporter associated with antigen processing. Science 264: 1322-1326
65. Ortmann B., Androlewicz M. J. and Cresswell P. (1994) MHC class I/beta 2-microglobulin complexes associate with TAP transporters before peptide binding. Nature 368: 864-867
66. Leeuwen J. E. van and Kearse K. P. (1996) Deglucosylation of N-linked glycans is an important step in the dissociation of calreticulin-class I-TAP complexes. Proc. Natl. Acad. Sci. USA 93: 13997-14001
67. Dick T. B. (2004) Assembly of MHC class I peptide complexes from the perspective of disulfide bond formation. Cell. Mol. Life Sci. 61: 547-556
68. Bouvier M. (2003) Accessory proteins and the assembly of human class I MHC molecules: a molecular and structural perspective. Mol. Immunol. 39: 697-706
69. Ostergaard Pedersen L., Nissen M. H., Hansen N. J., Nielsen L. L., Lauenmoller S. L., Blicher T. et al. (2001) Efficient assembly of recombinant major histocompatibility complex class I molecules with preformed disulfide bonds. Eur. J. Immunol. 31: 2986-2996
70. Oliver J. D., Roderick H. L., Llewellyn D. H. and High S. (1999) ERp57 functions as a subunit of specific complexes formed with the ER lectins calreticulin and calnexin. Mol. Biol. Cell. 10: 2573-2582
71. Oliver J. D., Wal F. J. van der, Bulleid N. J. and High S. (1997) Interaction of the thiol-dependent reductase ERp57 with nascent glycoproteins. Science 275: 86-88
72. Hammond C., Braakman I. and Helenius A. (1994) Role of N-linked oligosaccharide recognition, glucose trimming, and calnexin in glycoprotein folding and quality control. Proc. Natl. Acad. Sci. USA 91: 913-917
73. Morrice N. A. and Powis S. J. (1998) A role for the thiol-dependent reductase ERp57 in the assembly of MHC class I molecules. Curr. Biol. 8: 713-716
74. Peterson J. R., Ora A., Van P. N. and Helenius A. (1995) Transient, lectin-like association of calreticulin with folding intermediates of cellular and viral glycoproteins. Mol. Biol. Cell. 6: 1173-1184
75. Gao B., Adhikari R., Howarth M., Nakamura K., Gold M. C., Hill A. B. et al. (2002) Assembly and antigen-presenting function of MHC class I molecules in cells lacking the ER chaperone calreticulin. Immunity 16: 99-109
76. Lindquist J. A., Jensen O. N., Mann M. and Hämmerling G. J. (1998) ER-60, a chaperone with thiol-dependent reductase activity involved in MHC class I assembly. EMBO J. 17: 2186-2195
77. Ferrari D. M. and Soling H. D. (1999) The protein disulphide-isomerase family: unravelling a string of folds. Biochem. J. 339: 1-10
78. Molinari M. and Helenius A. (1999) Glycoproteins form mixed disulphides with oxidoreductases during folding in living cells. Nature 402: 90-93
79. Chivers P. T., Laboissiere M. C. and Raines R. T. (1996) The CXXC motif: imperatives for the formation of native disulfide bonds in the cell. EMBO J. 15: 2659-2667
80. Schrag J. D., Bergeron J. J., Li Y., Borisova S., Hahn M., Thomas D. Y. et al. (2001) The structure of calnexin, an ER chaperone involved in quality control of protein folding. Mol. Cell 8: 633-644
81. Leach M. R., Cohen-Doyle M. F., Thomas D. Y. and Williams D. B. (2002) Localization of the lectin, ERp57 binding, and polypeptide binding sites of calnexin and calreticulin. J. Biol. Chem. 277: 29686-29697
82. Frickel E. M., Riek R., Jelesarov I., Helenius A., Wuthrich K. and Ellgaard L. (2002) TROSY-NMR reveals interaction between ERp57 and the tip of the calreticulin P-domain. Proc. Natl. Acad. Sci. USA 99: 1954-1959
83. Paulsson K. and Wang P. (2003) Chaperones and folding of MHC class I molecules in the endoplasmic reticulum. Biochim. Biophys. Acta 1641: 1-12
84. David V., Hochstenbach F., Rajagopalan S. and Brenner M. B. (1993) Interaction with newly synthesized and retained proteins in the endoplasmic reticulum suggests a chaperone function for human integral membrane protein IP90 (calnexin). J. Biol. Chem. 268: 9585-9592
85. Ahluwalia N., Bergeron J. J., Wada L., Degen E. and Williams D. B. (1992) The p88 molecular chaperone is identical to the endoplasmic reticulum membrane protein, calnexin. J. Biol. Chem. 267: 10914-10918
86. Hughes E. A., Hammond C. and Cresswell P. (1997) Misfolded major histocompatibility complex class I heavy chains, are translocated into the cytoplasm and degraded by the proteasome. Proc. Natl. Acad. Sci. USA 94: 1896-1901
87. Diedrich G., Bangia N., Pan M. and Cresswell P. (2001) A role for calnexin in the assembly of the MHC class I loading complex in the endoplasmic reticulum. J. Immunol. 166: 1703-1709
88. Suh W. K., Mitchell E. K., Yang Y., Peterson P. A., Waneck G. L. and Williams D. B. (1996) MHC class I molecules form ternary complexes with calnexin and TAP and undergo peptide-regulated interaction with TAP via their extracellular domains. J. Exp. Med. 184: 337-348
89. Schoenhals G. J., Krishna R. M., Grandea A. G. 3rd, Spies T., Peterson P. A., Yang Y. et al. (1999) Retention of empty MHC class I molecules by tapasin is essential to reconstitute antigen presentation in invertebrate cells. EMBO J. 18: 743-753
90. Loo T. W. and Clarke D. M. (2000) The packing of the transmembrane segments of human multidrug resistance P-glycoprotein is revealed by disulfide cross-linking analysis. J. Biol. Chem. 275: 5253-5256
91. Reyes C. L. and Chang G. (2005) Structure of the ABC transporter MsbA in complex with ADP.vanadate and lipopolysaccharide. Science 308: 1028-1031
92. Chang G. and Roth C. B. (2001) Structure of MsbA from E. coli: a homolog of the multidrug resistance ATP binding cassette (ABC) transporters. Science 293: 1793-1800
93. Chang G. (2003) Structure of MsbA from Vibrio cholera: a multidrug resistance ABC transporter homolog in a closed conformation. J. Mol. Biol. 330: 419-430
94. Fra A. M., Fagioli C., Finazzi D., Sitia R. and Alberini C. M. (1993) Quality control of ER synthesized proteins: an exposed thiol group as a three-way switch mediating assembly, retention and degradation. EMBO J. 12: 4755-4761
95. Creighton T. E. (1988) Disulphide bonds and protein stability. Bioessays 8: 57-63
96. Reits E. A., Vos J. C., Gromme M. and Neefjes J. (2000) The major substrates for TAP in vivo are derived from newly synthesized proteins. Nature 404: 774-778
97. Jardetzky T. S., Lane W. S., Robinson R. A., Madden D. R. and Wiley D. C. (1991) Identification of self peptides bound to purified HLA-B27. Nature 353: 326-329
98. Ahn K., Meyer T. H., Uebel S., Sempe P., Djaballah H., Yang Y. et al. (1996) Molecular mechanism and species specificity of TAP inhibition by herpes simplex virus ICP47. EMBO J. 15: 3247-3255
99. Tomazin R., Hill A. B., Jugovic P., York I., Endert P. van, Ploegh H. L. et al. (1996) Stable binding of the herpes simplex virus ICP47 protein to the peptide binding site of TAP. EMBO J. 15: 3256-3266
100. Townsend A., Ohlen C., Bastin J., Ljunggren H. G., Foster L. and Karre K. (1989) Association of class I major histocompatibility heavy and light chains induced by viral peptides. Nature 340: 443-448
101. York I. A., Roop C., Andrews D. W., Riddell S. R., Graham F. L. and Johnson D. C. (1994) A cytosolic herpes simplex virus protein inhibits antigen presentation to CD8+ T lymphocytes. Cell 77: 525-535
102. Neumann L., Kraas W., Uebel S., Jung G. and 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
103. Galocha B., Hill A., Barnett B. C., Dolan A., Raimondi A., Cook R. F. et al. (1997) The active site of ICP47, a herpes simplex virus-encoded inhibitor of the major histocompatibility complex (MHC)-encoded peptide transporter associated with antigen processing (TAP), maps to the NH2-terminal 35 residues. J. Exp. Med. 185: 1565-1572
104. Pfänder R., Neumann L., Zweckstetter M., Seger C., Holak T. A. and 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
105. Beinert D., Neumann L., Uebel S. and Tampé, R. (1997) Structure of the viral TAP-inhibitor ICP47 induced by membrane association. Biochemistry 36: 4694-4700
106. Ahn K., Gruhler A., Galocha B., Jones T. R., Wiertz E. J., Ploegh H. L. et al. (1997) The ER-luminal domain of the HCMV glycoprotein US6 inhibits peptide translocation by TAP. Immunity 6: 613-621
107. Hengel H., Koopmann J. O., Flohr T., Muranyi W., Goulmy E., Hämmerling G. J. et al. (1997) A viral ER-resident glycoprotein inactivates the MHC-encoded peptide transporter. Immunity 6: 623-632
108. Lehner P. J., Karttunen J. T., Wilkinson G. W. and 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
109. Hewitt E. W., Gupta S. S. and Lehner P. J. (2001) The human cytomegalovirus gene product US6 inhibits ATP binding by TAP. EMBO J. 20: 387-396
110. Kyritsis C., Gorbulev S., Hutschenreiter S., Pawlitschko K., Abele R. and 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
111. Lybarger L., Wang X., Harris M. R., Virgin H. W. T. and Hansen T. H. (2003) Virus subversion of the MHC class I peptide-loading complex. Immunity 18: 121-130
112. Boname J. M. and Stevenson P. G. (2001) MHC class I ubiquitination by a viral PHD/LAP finger protein. Immunity 15: 627-636
113. Koppers-Lalic D., Rychlowski M., Leeuwen D. van, Rijsewijk F. A., Ressing M. E., Neefjes J. J. et al. (2003) Bovine herpesvirus 1 interferes with TAP-dependent peptide transport and intracellular trafficking of MHC class I molecules in human cells. Arch. Virol. 148: 2023-2037
114. Koppers-Lalic D., Reits E. A., Ressing M. E., Lipinska A. D., Abele R., Koch J. 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
115. Boname J. M., May J. S. and Stevenson P. G. (2005) The murine gamma-herpesvirus-68 MK3 protein causes TAP degradation independent of MHC class I heavy chain degradation. Eur. J. Immunol. 35: 171-179
116. Boname J. M., Lima B. D. de, Lehner P. J. and Stevenson P. G. (2004) Viral degradation of the MHC class I peptide loading complex. Immunity 20: 305-317
117. Jöns A., Granzow H., Kuchling R. and Mettenleiter T. C. (1996) The UL49.5 gene of pseudorabies virus codes for an O-glycosylated structural protein of the viral envelope. J. Virol. 70: 1237-1241
118. Barker D. E. and Roizman B. (1992) The unique sequence of the herpes simplex virus 1 L component contains an additional translated open reading frame designated UL49.5. J. Virol. 66: 562-566
119. Barnett B. C., Dolan A., Telford E. A., Davison A. J. and McGeoch D. J. (1992) A novel herpes simplex virus gene (UL49A) encodes a putative membrane protein with counterparts in other herpesviruses. J. Gen. Virol. 73: 2167-2171
120. Ambagala A. P., Gopinath R. S. and 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
121. Heintke S., Chen M., Ritz U., Lankat-Buttgereit B., Koch J., Abele R. et al. (2003) Functional cysteine-less subunits of the transporter associated with antigen processing (TAP1 and TAP2) by de novo gene assembly. FEBS Lett. 533: 42-46
122. Schrodt S., Koch J. and Tampé R. (2006) Membrane topology of the transporter associated with antigen processing (TAP1) within an assembled functional peptide-loading complex. J. Biol. Chem. Jan 5 [Epub ahead of print]