Antigen translocation machineries in adaptive immunity and viral immune evasion

Journal of Molecular Biology

Volumn 427, Issue 5, 2015, Pages 1102-1118

  Mayerhofer, Peter U ^a   Tampé, Robert ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

antigen presentation; membrane protein; peptide transport; peptide loading complex; viral immune evasion

Indexed keywords

ABC TRANSPORTER; CHAPERONE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PEPTIDE; TAPASIN; TRANSLOCON; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1; HLA ANTIGEN CLASS 1; VIRUS ANTIGEN;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; ANTIGEN STRUCTURE; BINDING AFFINITY; CELL COMMUNICATION; ENDOPLASMIC RETICULUM; GENE TRANSLOCATION; IMMUNE EVASION; IMMUNE RESPONSE; IMMUNOSURVEILLANCE; LYSOSOME; MAJOR HISTOCOMPATIBILITY COMPLEX; MITOCHONDRIAL MEMBRANE; NONHUMAN; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN HOMEOSTASIS; PROTEIN INTERACTION; PROTEIN PROCESSING; QUALITY CONTROL; REVIEW; SIGNAL TRANSDUCTION; VIRAL IMMUNE EVASION; VIRUS INFECTION; ANIMAL; HUMAN; IMMUNOLOGY; PROTEIN TRANSPORT; VIRUS;

VERTEBRATA;

ADAPTIVE IMMUNITY; ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, VIRAL; ATP-BINDING CASSETTE TRANSPORTERS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNE EVASION; PROTEIN TRANSPORT; VIRUSES;

EID: 84923086971     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2014.09.006     Document Type: Review

References (189)

1. A. Ciechanover Intracellular protein degradation: from a vague idea through the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting Neurodegener Dis 10 2012 7 22
2. E. Reits, A. Griekspoor, J. Neijssen, T. Groothuis, K. Jalink, P. van Veelen et al Peptide diffusion, protection, and degradation in nuclear and cytoplasmic compartments before antigen presentation by MHC class I Immunity 18 2003 97 108
3. N. Marmiroli, and E. Maestri Plant peptides in defense and signaling Peptides 56 2014 30 44
4. S. Michaelis, and J. Barrowman Biogenesis of the Saccharomyces cerevisiae pheromone a-factor, from yeast mating to human disease Microbiol Mol Biol Rev 76 2012 626 651
5. A.L. Hilchie, K. Wuerth, and R.E. Hancock Immune modulation by multifaceted cationic host defense (antimicrobial) peptides Nat Chem Biol 9 2013 761 768
6. P.M. Silva, S. Goncalves, and N.C. Santos Defensins: antifungal lessons from eukaryotes Front Microbiol 5 2014 1 17
7. J.W. Yewdell, and A.B. Hill Viral interference with antigen presentation Nat Immunol 3 2002 1019 1025
8. J.L. Brodsky Cleaning up: ER-associated degradation to the rescue Cell 151 2012 1163 1167
9. J. Lykke-Andersen, and E.J. Bennett Protecting the proteome: eukaryotic cotranslational quality control pathways J Cell Biol 204 2014 467 476
10. T. Inobe, and A. Matouschek Paradigms of protein degradation by the proteasome Curr Opin Struct Biol 24 2014 156 164
11. S. Bhattacharyya, H. Yu, C. Mim, and A. Matouschek Regulated protein turnover: snapshots of the proteasome in action Nat Rev Mol Cell Biol 15 2014 122 133
12. M. Schmidt, and D. Finley Regulation of proteasome activity in health and disease Biochim Biophys Acta 2014 1843 13 25
13. T. Nitta, S. Murata, K. Sasaki, H. Fujii, A.M. Ripen, N. Ishimaru et al Thymoproteasome shapes immunocompetent repertoire of CD8 + T cells Immunity 32 2010 29 40
14. M. Basler, C.J. Kirk, and M. Groettrup The immunoproteasome in antigen processing and other immunological functions Curr Opin Immunol 25 2013 74 80
15. E.M. Huber, M. Basler, R. Schwab, W. Heinemeyer, C.J. Kirk, M. Groettrup et al Immuno- and constitutive proteasome crystal structures reveal differences in substrate and inhibitor specificity Cell 148 2012 727 738
16. T. Saric, S.C. Chang, A. Hattori, I.A. York, S. Markant, K.L. Rock et al An IFN-gamma-induced aminopeptidase in the ER, ERAP1, trims precursors to MHC class I-presented peptides Nat Immunol 3 2002 1169 1176
17. L. Saveanu, O. Carroll, V. Lindo, M. Del Val, D. Lopez, Y. Lepelletier et al Concerted peptide trimming by human ERAP1 and ERAP2 aminopeptidase complexes in the endoplasmic reticulum Nat Immunol 6 2005 689 697
18. T. Serwold, F. Gonzalez, J. Kim, R. Jacob, and N. Shastri ERAAP customizes peptides for MHC class I molecules in the endoplasmic reticulum Nature 419 2002 480 483
19. S. Hulpke, and R. Tampé The MHC I loading complex: a multitasking machinery in adaptive immunity Trends Biochem Sci 38 2013 412 420
20. D.R. Peaper, and P. Cresswell Regulation of MHC class I assembly and peptide binding Annu Rev Cell Dev Biol 24 2008 343 368
21. K.L. Rock, D.J. Farfan-Arribas, J.D. Colbert, and A.L. Goldberg Re-examining class-I presentation and the DRiP hypothesis Trends Immunol 35 2014 144 152
22. D. Bourdetsky, C.E. Schmelzer, and A. Admon The nature and extent of contributions by defective ribosome products to the HLA peptidome Proc Natl Acad Sci USA 111 2014 E1591 E1599
23. K. Hollenstein, R.J. Dawson, and K.P. Locher Structure and mechanism of ABC transporter proteins Curr Opin Struct Biol 17 2007 412 418
24. K.P. Locher Review. Structure and mechanism of ATP-binding cassette transporters Philos Trans R Soc Lond B Biol Sci 364 2009 239 245
25. M.H. Saier, V.S. Reddy, D.G. Tamang, and A. Vastermark The transporter classification database Nucleic Acids Res 42 2014 D251 D258
26. D.C. Rees, E. Johnson, and O. Lewinson ABC transporters: the power to change Nat Rev Mol Cell Biol 10 2009 218 227
27. F. Quazi, S. Lenevich, and R.S. Molday ABCA4 is an N-retinylidene-phosphatidylethanolamine and phosphatidylethanolamine importer Nat Commun 3 2012 925
28. M. Dean, A. Rzhetsky, and R. Allikmets The human ATP-binding cassette (ABC) transporter superfamily Genome Res 11 2001 1156 1166
29. E. Nürenberg, and R. Tampé Tying up loose ends: ribosome recycling in eukaryotes and archaea Trends Biochem Sci 38 2013 64 74
30. J.E. Walker, M. Saraste, M.J. Runswick, and N.J. Gay Distantly related sequences in the α- and β-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold EMBO J 1 1982 945 951
31. P.C. Smith, N. Karpowich, L. Millen, J.E. Moody, J. Rosen, P.J. Thomas et al ATP binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer Mol Cell 10 2002 139 149
32. E.E. Fetsch, and A.L. Davidson Vanadate-catalyzed photocleavage of the signature motif of an ATP-binding cassette (ABC) transporter Proc Natl Acad Sci USA 99 2002 9685 9690
33. K.P. Hopfner, A. Karcher, D.S. Shin, L. Craig, L.M. Arthur, J.P. Carney et al Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily Cell 101 2000 789 800
34. J. Zaitseva, S. Jenewein, T. Jumpertz, I.B. Holland, and L. Schmitt H662 is the linchpin of ATP hydrolysis in the nucleotide-binding domain of the ABC transporter HlyB EMBO J 24 2005 1901 1910
35. R.J. Dawson, and K.P. Locher Structure of a bacterial multidrug ABC transporter Nature 443 2006 180 185
36. K.P. Locher, A.T. Lee, and D.C. Rees The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism Science 296 2002 1091 1098
37. G. Oancea, M.L. O'Mara, W.F. Bennett, D.P. Tieleman, R. Abele, and R. Tampé Structural arrangement of the transmission interface in the antigen ABC transport complex TAP Proc Natl Acad Sci USA 106 2009 5551 5556
38. E. Janas, M. Hofacker, M. Chen, S. Gompf, C. van der Does, and R. Tampé The ATP hydrolysis cycle of the nucleotide-binding domain of the mitochondrial ATP-binding cassette transporter Mdl1p J Biol Chem 278 2003 26862 26869
39. C. van der Does, and R. Tampé How do ABC transporters drive transport? Biol Chem 385 2004 927 933
40. R. Abele, and R. Tampé The ABCs of immunology: structure and function of TAP, the transporter associated with antigen processing Physiology (Bethesda) 19 2004 216 224
41. A.E. Senior, and D.C. Gadsby ATP hydrolysis cycles and mechanism in P-glycoprotein and CFTR Semin Cancer Biol 8 1997 143 150
42. P.M. Jones, and A.M. George Mechanism of the ABC transporter ATPase domains: catalytic models and the biochemical and biophysical record Crit Rev Biochem Mol Biol 48 2013 39 50
43. O. Demirel, Z. Waibler, U. Kalinke, F. Grünebach, S. Appel, P. Brossart et al Identification of a lysosomal peptide transport system induced during dendritic cell development J Biol Chem 282 2007 37836 37843
44. F. Zhang, W. Zhang, L. Liu, C.L. Fisher, D. Hui, S. Childs et al Characterization of ABCB9, an ATP binding cassette protein associated with lysosomes J Biol Chem 275 2000 23287 23294
45. J.C. Wolters, R. Abele, and R. Tampé Selective and ATP-dependent translocation of peptides by the homodimeric ATP binding cassette transporter TAP-like (ABCB9) J Biol Chem 280 2005 23631 23636
46. L. Young, K. Leonhard, T. Tatsuta, J. Trowsdale, and T. Langer Role of the ABC transporter Mdl1 in peptide export from mitochondria Science 291 2001 2135 2138
47. C.M. Haynes, Y. Yang, S.P. Blais, T.A. Neubert, and D. Ron The matrix peptide exporter HAF-1 signals a mitochondrial UPR by activating the transcription factor ZC376.7 in C. elegans Mol Cell 37 2010 529 540
48. B.M. Baker, and C.M. Haynes Mitochondrial protein quality control during biogenesis and aging Trends Biochem Sci 36 2011 254 261
49. J.P. McGrath, and A. Varshavsky The yeast STE6 gene encodes a homologue of the mammalian multidrug resistance P-glycoprotein Nature 340 1989 400 404
50. S. Ricardo, and R. Lehmann An ABC transporter controls export of a Drosophila germ cell attractant Science 323 2009 943 946
51. J. Koch, R. Guntrum, S. Heintke, C. Kyritsis, and R. Tampé Functional dissection of the transmembrane domains of the transporter associated with antigen processing (TAP) J Biol Chem 279 2004 10142 10147
52. B. Sadasivan, P.J. Lehner, B. Ortmann, T. Spies, and P. Cresswell Roles for calreticulin and a novel glycoprotein, tapasin, in the interaction of MHC class-I molecules with TAP Immunity 5 1996 103 114
53. B. Ortmann, M.J. Androlewicz, and P. Cresswell MHC class I/beta 2-microglobulin complexes associate with TAP transporters before peptide binding Nature 368 1994 864 867
54. F. Seyffer, and R. Tampé ABC transporters in adaptive immunity Biochim Biophys Acta 2014 http://dx.doi.org/10.1016/j.bbagen.2014.05.022.
55. R.J. Dawson, and K.P. Locher Structure of the multidrug ABC transporter Sav 1866 from Staphylococcus aureus in complex with AMP-PNP FEBS Lett 581 2007 935 938
56. M. Hohl, C. Briand, M.G. Grütter, and M.A. Seeger Crystal structure of a heterodimeric ABC transporter in its inward-facing conformation Nat Struct Mol Biol 19 2012 395 402
57. C.A. Shintre, A.C. Pike, Q. Li, J.I. Kim, A.J. Barr, S. Goubin et al Structures of ABCB10, a human ATP-binding cassette transporter in apo- and nucleotide-bound states Proc Natl Acad Sci USA 110 2013 9710 9715
58. S.G. Aller, J. Yu, A. Ward, Y. Weng, S. Chittaboina, R. Zhuo et al Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding Science 323 2009 1718 1722
59. M.S. Jin, M.L. Oldham, Q. Zhang, and J. Chen Crystal structure of the multidrug transporter P-glycoprotein from Caenorhabditis elegans Nature 490 2012 566 569
60. A. Kodan, T. Yamaguchi, T. Nakatsu, K. Sakiyama, C.J. Hipolito, A. Fujioka et al Structural basis for gating mechanisms of a eukaryotic P-glycoprotein homolog Proc Natl Acad Sci USA 111 2014 4049 4054
61. A.B. Ward, P. Szewczyk, V. Grimard, C.W. Lee, L. Martinez, R. Doshi et al Structures of P-glycoprotein reveal its conformational flexibility and an epitope on the nucleotide-binding domain Proc Natl Acad Sci USA 110 2013 13386 13391
62. V. Srinivasan, A.J. Pierik, and R. Lill Crystal structures of nucleotide-free and glutathione-bound mitochondrial ABC transporter Atm1 Science 343 2014 1137 1140
63. J.Y. Lee, J.G. Yang, D. Zhitnitsky, O. Lewinson, and D.C. Rees Structural basis for heavy metal detoxification by an Atm1-type ABC exporter Science 343 2014 1133 1136
64. V. Corradi, G. Singh, and D.P. Tieleman The human transporter associated with antigen processing: molecular models to describe peptide binding competent states J Biol Chem 287 2012 28099 28111
65. A.W. Serohijos, T. Hegedus, A.A. Aleksandrov, L. He, L. Cui, N.V. Dokholyan et al Phenylalanine-508 mediates a cytoplasmic-membrane domain contact in the CFTR 3D structure crucial to assembly and channel function Proc Natl Acad Sci USA 105 2008 3256 3261
66. O. Dalmas, C. Orelle, A.E. Foucher, C. Geourjon, S. Crouzy, A. Di Pietro et al The Q-loop disengages from the first intracellular loop during the catalytic cycle of the multidrug ABC transporter BmrA J Biol Chem 280 2005 36857 36864
67. A. Ward, C.L. Reyes, J. Yu, C.B. Roth, and G. Chang Flexibility in the ABC transporter MsbA: alternating access with a twist Proc Natl Acad Sci USA 104 2007 19005 19010
68. P.M. van Endert, R. Tampé, T.H. Meyer, R. Tisch, J.F. Bach, and H.O. McDevitt A sequential model for peptide binding and transport by the transporters associated with antigen processing Immunity 1 1994 491 500
69. J.O. Koopmann, M. Post, J.J. Neefjes, G.J. Hämmerling, and F. Momburg Translocation of long peptides by transporters associated with antigen processing (TAP) Eur J Immunol 26 1996 1720 1728
70. M.J. Androlewicz, and P. Cresswell Human transporters associated with antigen processing possess a promiscuous peptide-binding site Immunity 1 1994 7 14
71. S. Uebel, T.H. Meyer, W. Kraas, S. Kienle, G. Jung, K.H. Wiesmüller et al Requirements for peptide binding to the human transporter associated with antigen processing revealed by peptide scans and complex peptide libraries J Biol Chem 270 1995 18512 18516
72. T.N. Schumacher, D.V. Kantesaria, M.T. Heemels, P.G. Ashton-Rickardt, J.C. Shepherd, K. Früh et al Peptide length and sequence specificity of the mouse TAP1/TAP2 translocator J Exp Med 179 1994 533 540
73. S. Uebel, W. Kraas, S. Kienle, K.H. Wiesmüller, G. Jung, and R. Tampé Recognition principle of the TAP transporter disclosed by combinatorial peptide libraries Proc Natl Acad Sci USA 94 1997 8976 8981
74. A. Neisig, J. Roelse, A.J.A. Sijts, F. Ossendorp, M.C.W. Feltkamp, W.M. Kast et al Major differences in transporter associated with antigen presentation (TAP)-dependent translocation of MHC class I-presentable peptides and the effect of flanking sequences J Immunol 154 1995 1273 1279
75. F. Momburg, J. Roelse, J.C. Howard, G.W. Butcher, G.J. Hämmerling, and J.J. Neefjes Selectivity of MHC-encoded peptide transporters from human, mouse and rat Nature 367 1994 648 651
76. M.T. Heemels, and H.L. Ploegh Substrate specificity of allelic variants of the TAP peptide transporter Immunity 1 1994 775 784
77. S. Gorbulev, R. Abele, and R. Tampé Allosteric crosstalk between peptide-binding, transport, and ATP hydrolysis of the ABC transporter TAP Proc Natl Acad Sci USA 98 2001 3732 3737
78. C. Baldauf, S. Schrodt, M. Herget, J. Koch, and R. Tampé Single residue within the antigen translocation complex TAP controls the epitope repertoire by stabilizing a receptive conformation Proc Natl Acad Sci USA 107 2010 9135 9140
79. M. Grommé, R. van der Valk, K. Sliedregt, L. Vernie, R. Liskamp, G.J. Hämmerling et al The rational design of TAP inhibitors using peptide substrate modifications and peptidomimetics Eur J Immunol 27 1997 898 904
80. M. Nijenhuis, and G.J. Hämmerling Multiple regions of the transporter associated with antigen processing (TAP) contribute to its peptide binding site J Immunol 157 1996 5467 5477
81. F. Momburg, E.A. Armandola, M. Post, and G.J. Hämmerling Residues in TAP2 peptide transporters controlling substrate specificity J Immunol 156 1996 1756 1763
82. E.A. Armandola, F. Momburg, M. Nijenhuis, N. Bulbuc, K. Früh, and G.J. Hämmerling A point mutation in the human transporter associated with antigen processing (TAP2) alters the peptide transport specificity Eur J Immunol 26 1996 1748 1755
83. M. Herget, G. Oancea, S. Schrodt, M. Karas, R. Tampé, and R. Abele Mechanism of substrate sensing and signal transmission within an ABC transporter: use of a Trojan horse strategy J Biol Chem 282 2007 3871 3880
84. M. Herget, C. Baldauf, C. Schölz, D. Parcej, K.H. Wiesmuller, R. Tampé et al Conformation of peptides bound to the transporter associated with antigen processing (TAP) Proc Natl Acad Sci USA 108 2011 1349 1354
85. J.J. Neefjes, F. Momburg, and G.J. Hämmerling Selective and ATP-dependent translocation of peptides by the MHC-encoded transporter Science 261 1993 769 771
86. M. Chen, R. Abele, and R. Tampé Functional non-equivalence of ATP-binding cassette signature motifs in the transporter associated with antigen processing (TAP) J Biol Chem 279 2004 46073 46081
87. R. Ernst, J. Koch, C. Horn, R. Tampé, and L. Schmitt Engineering ATPase activity in the isolated ABC cassette of human TAP1 J Biol Chem 281 2006 27471 27480
88. M. Chen, R. Abele, and R. Tampé Peptides induce ATP hydrolysis at both subunits of the transporter associated with antigen processing J Biol Chem 278 2003 29686 29692
89. E. Procko, and R. Gaudet Functionally important interactions between the nucleotide-binding domains of an antigenic peptide transporter Biochemistry 47 2008 5699 5708
90. P.E. Lapinski, G. Raghuraman, and M. Raghavan Nucleotide interactions with membrane-bound transporter associated with antigen processing proteins J Biol Chem 278 2003 8229 8237
91. J.T. Karttunen, P.J. Lehner, S.S. Gupta, E.W. Hewitt, and P. Cresswell Distinct functions and cooperative interaction of the subunits of the transporter associated with antigen processing (TAP) Proc Natl Acad Sci USA 98 2001 7431 7436
92. L. Saveanu, S. Daniel, and P.M. van Endert Distinct functions of the ATP binding cassettes of transporters associated with antigen processing: a mutational analysis of Walker A and B sequences J Biol Chem 276 2001 22107 22113
93. P.E. Lapinski, R.R. Neubig, and M. Raghavan Walker A lysine mutations of TAP1 and TAP2 interfere with peptide translocation but not peptide binding J Biol Chem 276 2001 7526 7533
94. C.L. Perria, V. Rajamanickam, P.E. Lapinski, and M. Raghavan Catalytic site modifications of TAP1 and TAP2 and their functional consequences J Biol Chem 281 2006 39839 39851
95. J. Geng, S. Sivaramakrishnan, and M. Raghavan Analyses of conformational states of the transporter associated with antigen processing (TAP) protein in a native cellular membrane environment J Biol Chem 288 2013 37039 37047
96. S. Schrodt, J. Koch, and R. Tampé Membrane topology of the transporter associated with antigen processing (TAP1) within an assembled functional peptide-loading complex J Biol Chem 281 2006 6455 6462
97. S. Hulpke, M. Tomioka, E. Kremmer, K. Ueda, R. Abele, and R. Tampé Direct evidence that the N-terminal extensions of the TAP complex act as autonomous interaction scaffolds for the assembly of the MHC I peptide-loading complex Cell Mol Life Sci 69 2012 3317 3327
98. S. Hulpke, C. Baldauf, and R. Tampé Molecular architecture of the MHC I peptide-loading complex: one tapasin molecule is essential and sufficient for antigen processing FASEB J 26 2012 5071 5080
99. J. Koch, R. Guntrum, and R. Tampé Exploring the minimal functional unit of the transporter associated with antigen processing FEBS Lett 579 2005 4413 4416
100. E. Procko, G. Raghuraman, D.C. Wiley, M. Raghavan, and R. Gaudet Identification of domain boundaries within the N-termini of TAP1 and TAP2 and their importance in tapasin binding and tapasin-mediated increase in peptide loading of MHC class I Immunol Cell Biol 83 2005 475 482
101. B. Ortmann, J. Copeman, P.J. Lehner, B. Sadasivan, J.A. Herberg, A.G. Grandea et al A critical role for tapasin in the assembly and function of multimeric MHC class I-TAP complexes Science 277 1997 1306 1309
102. G. Dong, P.A. Wearsch, D.R. Peaper, P. Cresswell, and K.M. Reinisch Insights into MHC class I peptide loading from the structure of the tapasin-ERp57 thiol oxidoreductase heterodimer Immunity 30 2009 21 32
103. D.R. Peaper, P.A. Wearsch, and P. Cresswell Tapasin and ERp57 form a stable disulfide-linked dimer within the MHC class I peptide-loading complex EMBO J 24 2005 3613 3623
104. 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
105. N. Garbi, S. Tanaka, F. Momburg, and G.J. Hämmerling Impaired assembly of the major histocompatibility complex class I peptide-loading complex in mice deficient in the oxidoreductase ERp57 Nat Immunol 7 2006 93 102
106. D. Stepensky, N. Bangia, and P. Cresswell Aggregate formation by ERp57-deficient MHC class I peptide-loading complexes Traffic 8 2007 1530 1542
107. D.R. Peaper, and P. Cresswell The redox activity of ERp57 is not essential for its functions in MHC class I peptide loading Proc Natl Acad Sci USA 105 2008 10477 10482
108. Y. Zhang, G. Kozlov, C.L. Pocanschi, U. Brockmeier, B.S. Ireland, P. Maattanen et al ERp57 does not require interactions with calnexin and calreticulin to promote assembly of class I histocompatibility molecules, and it enhances peptide loading independently of its redox activity J Biol Chem 284 2009 10160 10173
109. P. Tan, H. Kropshofer, O. Mandelboim, N. Bulbuc, G.J. Hämmerling, and F. Momburg 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 2002 1950 1960
110. J.L. Petersen, H.D. Hickman-Miller, M.M. McIlhaney, S.E. Vargas, A.W. Purcell, W.H. Hildebrand et al A charged amino acid residue in the transmembrane/cytoplasmic region of tapasin influences MHC class I assembly and maturation J Immunol 174 2005 962 969
111. M. Papadopoulos, and F. Momburg 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 2007 9401 9410
112. M. Chen, and M. Bouvier Analysis of interactions in a tapasin/class I complex provides a mechanism for peptide selection EMBO J 26 2007 1681 1690
113. 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
114. P.V. Praveen, R. Yaneva, H. Kalbacher, and S. Springer Tapasin edits peptides on MHC class I molecules by accelerating peptide exchange Eur J Immunol 40 2010 214 224
115. P.A. Wearsch, and P. Cresswell Selective loading of high-affinity peptides onto major histocompatibility complex class I molecules by the tapasin-ERp57 heterodimer Nat Immunol 8 2007 873 881
116. M. Howarth, A. Williams, A.B. Tolstrup, and T. Elliott Tapasin enhances MHC class I peptide presentation according to peptide half-life Proc Natl Acad Sci USA 101 2004 11737 11742
117. C.A. Peh, S.R. Burrows, M. Barnden, R. Khanna, P. Cresswell, D.J. Moss et al 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
118. A. Neisig, R. Wubbolts, X.S. Zang, C. Melief, and J. Neefjes Allele-specific differences in the interaction of MHC class-I molecules with transporters associated with antigen-processing J Immunol 156 1996 3196 3206
119. A.L. Zarling, C.J. Luckey, J.A. Marto, F.M. White, C.J. Brame, A.M. Evans et al Tapasin is a facilitator, not an editor, of class I MHC peptide binding J Immunol 171 2003 5287 5295
120. G. Roder, L. Geironson, M. Rasmussen, M. Harndahl, S. Buus, and K. Paulsson Tapasin discriminates peptide-human leukocyte antigen-A∗02:01 complexes formed with natural ligands J Biol Chem 286 2011 20547 20557
121. G. Raghuraman, P.E. Lapinski, and M. Raghavan Tapasin interacts with the membrane-spanning domains of both TAP subunits and enhances the structural stability of TAP1 x TAP2 Complexes J Biol Chem 277 2002 41786 41794
122. P.J. Lehner, M.J. Surman, and P. Cresswell Soluble tapasin restores MHC class I expression and function in the tapasin-negative cell line.220 Immunity 8 1998 221 231
123. N. Bangia, P.J. Lehner, E.A. Hughes, M. Surman, and P. Cresswell The N-terminal region of tapasin is required to stabilize the MHC class I loading complex Eur J Immunol 29 1999 1858 1870
124. N. Garbi, N. Tiwari, F. Momburg, and G.J. Hämmerling A major role for tapasin as a stabilizer of the TAP peptide transporter and consequences for MHC class I expression Eur J Immunol 33 2003 264 273
125. R.M. Leonhardt, K. Keusekotten, C. Bekpen, and M.R. Knittler Critical role for the tapasin-docking site of TAP2 in the functional integrity of the MHC class I-peptide-loading complex J Immunol 175 2005 5104 5114
126. R.M. Leonhardt, P. Abrahimi, S.M. Mitchell, and P. Cresswell Three tapasin docking sites in TAP cooperate to facilitate transporter stabilization and heterodimerization J Immunol 192 2014 2480 2494
127. N. Bangia, and P. Cresswell Stoichiometric tapasin interactions in the catalysis of major histocompatibility complex class I molecule assembly Immunology 114 2005 346 353
128. M.S. Panter, A. Jain, R.M. Leonhardt, T. Ha, and P. Cresswell Dynamics of major histocompatibility complex class I association with the human peptide-loading complex J Biol Chem 287 2012 31172 31184
129. E.A.J. Reits, J.C. Vos, M. Grommé, and J. Neefjes The major substrates for TAP in vivo are derived from newly synthesized proteins Nature 404 2000 774 778
130. A.L. Ackerman, C. Kyritsis, R. Tampé, and P. Cresswell Early phagosomes in dendritic cells form a cellular compartment sufficient for cross presentation of exogenous antigens Proc Natl Acad Sci USA 100 2003 12889 12894
131. A.L. Ackerman, A. Giodini, and P. Cresswell A role for the endoplasmic reticulum protein retrotranslocation machinery during crosspresentation by dendritic cells Immunity 25 2006 607 617
132. S. Burgdorf, C. Schölz, A. Kautz, R. Tampé, and C. Kurts Spatial and mechanistic separation of cross-presentation and endogenous antigen presentation Nat Immunol 9 2008 558 566
133. J.M. Boname, J.S. May, and P.G. Stevenson The murine gamma-herpesvirus-68 MK3 protein causes TAP degradation independent of MHC class I heavy chain degradation Eur J Immunol 35 2005 171 179
134. R.A. Herr, J. Harris, S. Fang, X. Wang, and T.H. Hansen Role of the RING-CH domain of viral ligase mK3 in ubiquitination of non-lysine and lysine MHC I residues Traffic 10 2009 1301 1317
135. X. Wang, Y. Ye, W. Lencer, and T.H. Hansen The viral E3 ubiquitin ligase mK3 uses the Derlin/p97 endoplasmic reticulum-associated degradation pathway to mediate down-regulation of major histocompatibility complex class I proteins J Biol Chem 281 2006 8636 8644
136. J.M. Bomberger, K.H. Ely, N. Bangia, S. Ye, K.A. Green, W.R. Green et al Pseudomonas aeruginosa Cif protein enhances the ubiquitination and proteasomal degradation of the transporter associated with antigen processing (TAP) and reduces major histocompatibility complex (MHC) class I antigen presentation J Biol Chem 289 2014 152 162
137. K. Ahn, T.H. Meyer, S. Uebel, P. Sempé, H. Djaballah, Y. Yang et al Molecular mechanism and species specificity of TAP inhibition by herpes simplex virus ICP47 EMBO J 15 1996 3247 3255
138. R. Tomazin, A.B. Hill, P. Jugovic, I. York, P. van Endert, H.L. Ploegh et al Stable binding of the herpes simplex virus ICP47 protein to the peptide binding site of TAP EMBO J 15 1996 3256 3266
139. K. Früh, K. Ahn, H. Djaballah, P. Sempé, P.M. van Endert, R. Tampé et al A viral inhibitor of peptide transporters for antigen presentation Nature 375 1995 415 418
140. A. Hill, P. Jugovic, I. York, G. Russ, J. Bennink, J. Yewdell et al Herpes simplex virus turns off the TAP to evade host immunity Nature 375 1995 411 415
141. V.G. Lacaille, and M.J. Androlewicz Herpes simplex virus inhibitor ICP47 destabilizes the transporter associated with antigen processing (TAP) heterodimer J Biol Chem 273 1998 17386 17390
142. B. Galocha, A. Hill, B.C. Barnett, A. Dolan, A. Raimondi, R.F. Cook et al 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 1997 1565 1572
143. L. Neumann, W. Kraas, S. Uebel, G. Jung, and R. Tampé The active domain of the herpes simplex virus protein ICP47: a potent inhibitor of the transporter associated with antigen processing J Mol Biol 272 1997 484 492
144. C. Aisenbrey, C. Sizun, J. Koch, M. Herget, R. Abele, B. Bechinger et al Structure and dynamics of membrane-associated ICP47, a viral inhibitor of the MHC I antigen-processing machinery J Biol Chem 281 2006 30365 30372
145. D. Beinert, L. Neumann, S. Uebel, and R. Tampé Structure of the viral TAP-inhibitor ICP47 induced by membrane association Biochemistry 36 1997 4694 4700
146. R. Pfänder, L. Neumann, M. Zweckstetter, C. Seger, T.A. Holak, and R. Tampé 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 1999 13692 13698
147. K. Ahn, A. Gruhler, B. Galocha, T.R. Jones, E.J. Wiertz, H.L. Ploegh et al The ER-luminal domain of the HCMV glycoprotein US6 inhibits peptide translocation by TAP Immunity 6 1997 613 621
148. H. Hengel, J.O. Koopmann, T. Flohr, W. Muranyi, E. Goulmy, G.J. Hämmerling et al A viral ER-resident glycoprotein inactivates the MHC-encoded peptide transporter Immunity 6 1997 623 632
149. 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
150. 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
151. C. Kyritsis, S. Gorbulev, S. Hutschenreiter, K. Pawlitschko, R. Abele, and R. Tampé Molecular mechanism and structural aspects of transporter associated with antigen processing inhibition by the cytomegalovirus protein US6 J Biol Chem 276 2001 48031 48039
152. A. Halenius, F. Momburg, H. Reinhard, D. Bauer, M. Lobigs, and H. Hengel Physical and functional interactions of the cytomegalovirus US6 glycoprotein with the transporter associated with antigen processing J Biol Chem 281 2006 5383 5390
153. P. Nair-Gupta, and J.M. Blander An updated view of the intracellular mechanisms regulating cross-presentation Front Immunol 4 2013 401
154. B. Platzer, M. Stout, and E. Fiebiger Antigen cross-presentation of immune complexes Front Immunol 5 2014 140
155. D. Koppers-Lalic, E.A. Reits, M.E. Ressing, A.D. Lipinska, R. Abele, J. Koch et al Varicelloviruses avoid T cell recognition by UL49.5-mediated inactivation of the transporter associated with antigen processing Proc Natl Acad Sci USA 102 2005 5144 5149
156. D. Koppers-Lalic, M.C. Verweij, A.D. Lipinska, Y. Wang, E. Quinten, E.A. Reits et al Varicellovirus UL 49.5 proteins differentially affect the function of the transporter associated with antigen processing, TAP PLoS Pathog 4 2008 e1000080
157. M.C. Verweij, D. Koppers-Lalic, S. Loch, F. Klauschies, H. de la Salle, E. Quinten et al The varicellovirus UL49.5 protein blocks the transporter associated with antigen processing (TAP) by inhibiting essential conformational transitions in the 6 + 6 TAP core complex J Immunol 181 2008 4894 4907
158. S. Loch, F. Klauschies, C. Scholz, M.C. Verweij, E.J. Wiertz, J. Koch et al Signaling of a varicelloviral factor across the endoplasmic reticulum membrane induces destruction of the peptide-loading complex and immune evasion J Biol Chem 283 2008 13428 13436
159. N.P. Croft, C. Shannon-Lowe, A.I. Bell, D. Horst, E. Kremmer, M.E. Ressing et al Stage-specific inhibition of MHC class I presentation by the Epstein-Barr virus BNLF2a protein during virus lytic cycle PLoS Pathog 5 2009 e1000490
160. D. Horst, D. van Leeuwen, N.P. Croft, M.A. Garstka, A.D. Hislop, E. Kremmer et al Specific targeting of the EBV lytic phase protein BNLF2a to the transporter associated with antigen processing results in impairment of HLA class I-restricted antigen presentation J Immunol 182 2009 2313 2324
161. M.E. Ressing, S.E. Keating, D. van Leeuwen, D. Koppers-Lalic, I.Y. Pappworth, E.J. Wiertz et al Impaired transporter associated with antigen processing-dependent peptide transport during productive EBV infection J Immunol 174 2005 6829 6838
162. D. Horst, V. Favaloro, F. Vilardi, H.C. van Leeuwen, M.A. Garstka, A.D. Hislop et al EBV protein BNLF2a exploits host tail-anchored protein integration machinery to inhibit TAP J Immunol 186 2011 3594 3605
163. A.I. Wycisk, J. Lin, S. Loch, K. Hobohm, J. Funke, R. Wieneke et al Epstein-Barr viral BNLF2a protein hijacks the tail-anchored protein insertion machinery to block antigen processing by the transport complex TAP J Biol Chem 286 2011 41402 41412
164. D. Horst, S.R. Burrows, D. Gatherer, B. van Wilgenburg, M.J. Bell, I.G. Boer et al Epstein-Barr virus isolates retain their capacity to evade T cell immunity through BNLF2a despite extensive sequence variation J Virol 86 2012 572 577
165. D. Alzhanova, D.M. Edwards, E. Hammarlund, I.G. Scholz, D. Horst, M.J. Wagner et al Cowpox virus inhibits the transporter associated with antigen processing to evade T cell recognition Cell Host Microbe 6 2009 433 445
166. M. Byun, M.C. Verweij, D.J. Pickup, E.J. Wiertz, T.H. Hansen, and W.M. Yokoyama Two mechanistically distinct immune evasion proteins of cowpox virus combine to avoid antiviral CD8 T cells Cell Host Microbe 6 2009 422 432
167. K. Kuchler, R.E. Sterne, and J. Thorner Saccharomyces cerevisiae STE6 gene product: a novel pathway for protein export in eukaryotic cells EMBO J 8 1989 3973 3984
168. R.J. Anderegg, R. Betz, S.A. Carr, J.W. Crabb, and W. Duntze Structure of Saccharomyces cerevisiae mating hormone a-factor. Identification of S-farnesyl cysteine as a structural component J Biol Chem 263 1988 18236 18240
169. V.N. Kotiadis, M.R. Duchen, and L.D. Osellame Mitochondrial quality control and communications with the nucleus are important in maintaining mitochondrial function and cell health Biochim Biophys Acta 2014 1840 1254 1265
170. M.W. Pellegrino, A.M. Nargund, and C.M. Haynes Signaling the mitochondrial unfolded protein response Biochim Biophys Acta 2013 1833 410 416
171. B. Loveland, C.R. Wang, H. Yonekawa, E. Hermel, and K.F. Lindahl Maternally transmitted histocompatibility antigen of mice: a hydrophobic peptide of a mitochondrially encoded protein Cell 60 1990 971 980
172. M. Liesa, W. Qiu, and O.S. Shirihai Mitochondrial ABC transporters function: the role of ABCB10 (ABC-me) as a novel player in cellular handling of reactive oxygen species Biochim Biophys Acta 2012 1823 1945 1957
173. A. Zutz, S. Gompf, H. Schagger, and R. Tampe Mitochondrial ABC proteins in health and disease Biochim Biophys Acta 1787 2009 681 690
174. P.C. Krishnamurthy, G. Du, Y. Fukuda, D. Sun, J. Sampath, K.E. Mercer et al Identification of a mammalian mitochondrial porphyrin transporter Nature 443 2006 586 589
175. S.A. Graf, S.E. Haigh, E.D. Corson, and O.S. Shirihai Targeting, import, and dimerization of a mammalian mitochondrial ATP binding cassette (ABC) transporter, ABCB10 (ABC-me) J Biol Chem 279 2004 42954 42963
176. S. Gompf, A. Zutz, M. Hofacker, W. Haase, C. van der Does, and R. Tampe Switching of the homooligomeric ATP-binding cassette transport complex MDL1 from post-translational mitochondrial import to endoplasmic reticulum insertion FEBS J 274 2007 5298 5310
177. M. Hofacker, S. Gompf, A. Zutz, C. Presenti, W. Haase, C. van der et al Does Structural and functional fingerprint of the mitochondrial ATP-binding cassette transporter Mdl1 from Saccharomyces cerevisiae J Biol Chem 282 2007 3951 3961
178. W. Chen, P.N. Paradkar, L. Li, E.L. Pierce, N.B. Langer, and N. Takahashi-Makise Abcb10 physically interacts with mitoferrin-1 (Slc25a37) to enhance its stability and function in the erythroid mitochondria Proc Natl Acad Sci USA 106 2009 16263 16268
179. G. Kispal, P. Csere, C. Prohl, and R. Lill The mitochondrial proteins Atm1p and Nfs1p are essential for biogenesis of cytosolic Fe/S proteins EMBO J 18 1999 3981 3989
180. T.S. Uinuk-ool, W.E. Mayer, A. Sato, N. Takezaki, L. Benyon, M.D. Cooper et al Identification and characterization of a TAP-family gene in the lamprey Immunogenetics 55 2003 38 48
181. Y. Yamaguchi, M. Kasano, T. Terada, R. Sato, and M. Maeda An ABC transporter homologous to TAP proteins FEBS Lett 457 1999 231 236
182. I. Bangert, F. Tumulka, and R. Abele The lysosomal polypeptide transporter TAPL: more than a housekeeping factor? Biol Chem 392 2011 61 66
183. C. Zhao, W. Haase, R. Tampé, and R. Abele Peptide specificity and lipid activation of the lysosomal transport complex ABCB9 (TAPL) J Biol Chem 283 2008 17083 17091
184. O. Demirel, I. Bangert, R. Tampé, and R. Abele Tuning the cellular trafficking of the lysosomal peptide transporter TAPL by its N-terminal domain Traffic 11 2010 383 393
185. O. Demirel, I. Jan, D. Wolters, J. Blanz, P. Saftig, R. Tampé et al The lysosomal polypeptide transporter TAPL is stabilized by interaction with LAMP-1 and LAMP-2 J Cell Sci 125 2012 4230 4240
186. A. Kobayashi, M. Kasano, T. Maeda, S. Hori, K. Motojima, M. Suzuki et al A half-type ABC transporter TAPL is highly conserved between rodent and man, and the human gene is not responsive to interferon-gamma in contrast to TAP1 and TAP2 J Biochem (Tokyo) 128 2000 711 718
187. T. Tanji, K. Nishikori, H. Shiraishi, M. Maeda, and A. Ohashi-Kobayashi Co-operative function and mutual stabilization of the half ATP-binding cassette transporters HAF-4 and HAF-9 in Caenorhabditis elegans Biochem J 452 2013 467 475
188. B. Lankat-Buttgereit, and R. Tampé The transporter associated with antigen processing: function and implications in human diseases Physiol Rev 82 2002 187 204
189. A. Hinz, and R. Tampé ABC transporters and immunity: mechanism of self-defense Biochemistry 51 2012 4981 4989