The ABCs of immunology: Structure and function of TAP, the transporter associated with antigen processing

Physiology

Volumn 19, Issue 4, 2004, Pages 216-224

  Abele, Rupert ^a   Tampé, Robert ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; GAMMA INTERFERON; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; HLA ANTIGEN CLASS 1; TAP1 PROTEIN, HUMAN; TAP2 PROTEIN, HUMAN;

ANTIGEN PRESENTATION; BARE LYMPHOCYTE SYNDROME; BINDING AFFINITY; CYTOSOL; CYTOTOXIC T LYMPHOCYTE; ENDOPLASMIC RETICULUM; HUMAN; IMMUNOLOGY; MALIGNANT TRANSFORMATION; NONHUMAN; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; REVIEW; TUMOR ESCAPE; VIRUS INFECTION; AMINO ACID SEQUENCE; ANIMAL; GENETICS; MOLECULAR GENETICS; T LYMPHOCYTE;

AMINO ACID SEQUENCE; ANIMALS; ANTIGEN PRESENTATION; ATP-BINDING CASSETTE TRANSPORTERS; ENDOPLASMIC RETICULUM; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; MOLECULAR SEQUENCE DATA; T-LYMPHOCYTES;

EID: 4544336851     PISSN: 15489213     EISSN: None     Source Type: Journal    
DOI: 10.1152/physiol.00002.2004     Document Type: Review

References (97)

1. Ackerman AL, Kyritsis C, Tampé R, and Cresswell P. Early phagosomes in dendritic cells form a cellular compartment sufficient for cross presentation of exogenous antigens. Proc Natl Acad Sci USA 100: 12889-12894, 2003.
2. Ahn K, Gruhler A, Galocha B, Jones TR, Wiertz EJ, Ploegh HL, Peterson PA, Yang Y, and Früh K. The ER-luminal domain of the HCMV glycoprotein US6 inhibits peptide translocation by TAP. Immunity 6: 613-621, 1997.
3. Ahn K, Meyer TH, Uebel S, Sempé P, Djaballah H, Yang Y, Peterson PA, Früh K, and Tampé R. Molecular mechanism and species specificity of TAP inhibition by herpes simplex virus ICP47. EMBO J 15: 3247-3255, 1996.
4. Alberts P, Daumke O, Deverson EV, Howard JC, and Knittler MR. Distinct functional properties of the TAP subunits coordinate the nucleotide-dependent transport cycle. Curr Biol 11: 242-251, 2001.
5. Ambagala AP, Hinkley S, and Srikumaran S. An early pseudorabies virus protein down-regulates porcine MHC class I expression by inhibition of transporter associated with antigen processing (TAP). J Immunol 164: 93-99, 2000.
6. Androlewicz MJ and Cresswell P. Human transporters associated with antigen processing possess a promiscuous peptide-binding site. Immunity 1: 7-14, 1994.
7. Arora S, Lapinski PE, and Raghavan M. Use of chimeric proteins to investigate the role of transporter associated with antigen processing (TAP) structural domains in peptide binding and translocation. Proc Natl Acad Sci USA 98: 7241-7246, 2001.
8. Bangia N, Lehner PJ, Hughes EA, Surman M, and Cresswell P. The N-terminal region of tapasin is required to stabilize the MHC class I loading complex. Eur J Immunol 29: 1858-1870, 1999.
9. Beinert D, Neumann L, Uebel S, and Tampé R. Structure of the viral TAP-inhibitor ICP47 induced by membrane association. Biochemistry 36: 4694-4700, 1997.
10. Bennett EM, Bennink JR, Yewdell JW, and Brodsky FM. Cutting edge: adenovirus E19 has two mechanisms for affecting class I MHC expression. J Immunol 162: 5049-5052, 1999.
11. Bouabe H and Knittler MR. 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, 2003.
12. Brooks P, Murray RZ, Mason GG, Hendil KB, and Rivett AJ. Association of immunoproteasomes with the endoplasmic reticulum. Biochem J 352: 611-615, 2000.
13. Browne BL, McClendon V, and Bedwell DM. Mutations within the first LSGGQ motif of Ste6p cause defects in a-factor transport and mating in Saccharomyces cerevisiae. J Bacteriol 178: 1712-1719, 1996.
14. Cascio P, Hilton C, Kisselev AF, Rock KL, and Goldberg AL. 26S proteasomes and immunoproteasomes produce mainly N-extended versions of an antigenic peptide. EMBO J 20: 2357-2366, 2001.
15. Chen HL, Gabrilovich D, Tampé R, Girgis KR, Nadaf S, and Carbone DP. A functionally defective allele of TAP1 results in loss of MHC class I antigen presentation in a human lung cancer. Nat Genet 13: 210-213, 1996.
16. Chen J, Lu G, Lin J, Davidson AL, and Quiocho FA. A tweezers-like motion of the ATP-binding cassette dimer in an ABC transport cycle. Mol Cell 12: 651-661, 2003.
17. Chen M, Abele R, and Tampé R. Peptides induce ATP hydrolysis at both subunits of the transporter associated with antigen processing. J Biol Chem 278: 29686-29692, 2003.
18. Daumke O and Knittler MR. Functional asymmetry of the ATP-binding-cassettes of the ABC transporter TAP is determined by intrinsic properties of the nucleotide binding domains. Eur J Biochem 268: 4776-4786, 2001.
19. De la Salle H, Hanau D, Fricker D, Urlacher A, Kelly A, Salamero J, Powis SH, Donato L, Bausinger H, Laforet M, Jeras M, Spehner D, Bieber T, Falkenrodt A, Cazenave JP, Trowsdale J, and Tongio MM. Homozygous human TAP peptide transporter mutation in HLA class I deficiency. Science 265: 237-241, 1994.
20. Dick TP, Bangia N, Peaper DR, and Cresswell P. Disulfide bond isomerization and the assembly of MHC class I-peptide complexes. Immunity 16: 87-98, 2002.
21. Fetsch EE and Davidson AL. Vanadate-catalyzed photocleavage of the signature motif of an ATP-binding cassette (ABC) transporter. Proc Natl Acad Sci USA 99: 9685-9690, 2002.
22. Früh K, Ahn K, Djaballah H, Sempé P, van Endert PM, Tampé R, Peterson PA, and Yang Y. A viral inhibitor of peptide transporters for antigen presentation. Nature 375: 415-418, 1995.
23. Gao B, Adhikari R, Howarth M, Nakamura K, Gold MC, Hill AB, Knee R, Michalak M, and Elliott T. Assembly and antigen-presenting function of MHC class I molecules in cells lacking the ER chaperone calreticulin. Immunity 16: 99-109, 2002.
24. Gaudet R and Wiley DC. Structure of the ABC ATPase domain of human TAP1, the transporter associated with antigen processing. EMBO J 20: 4964-4972, 2001.
25. Georgopoulos NT, Proffitt JL, and Blair GE. Transcriptional regulation of the major histocompatibility complex (MHC) class I heavy chain, TAP1 and LMP2 genes by the human papillomavirus (HPV) type 6b, 16 and 18 E7 oncoproteins. Oncogene 19: 4930-4935, 2000.
26. Goldberg AL, Cascio P, Saric T, and Rock KL. The importance of the proteasome and subsequent proteolytic steps in the generation of antigenic peptides. Mol Immunol 39: 147-164, 2002.
27. Gorbulev S, Abele R, and Tampé R. Allosteric crosstalk between peptide-binding, transport, and ATP hydrolysis of the ABC transporter TAP. Proc Natl Acad Sci USA 98: 3732-3737, 2001.
28. Grandea AG 3rd, Lehner PJ, Cresswell P, and Spies T. Regulation of MHC class I heterodimer stability and interaction with TAP by tapasin. Immunogenetics 46: 477-483, 1997.
29. Gromme M and Neefjes J. Antigen degradation or presentation by MHC class I molecules via classical and non-classical pathways. Mol Immunol 39: 181-202, 2002.
30. Guermonprez P, Saveanu L, Kleijmeer M, Davoust J, Van Endert P, and Amigorena S. ER-phagosome fusion defines an MHC class I cross-presentation compartment in dendritic cells. Nature 425: 397-402, 2003.
31. Hengel H, Koopmann JO, Flohr T, Muranyi W, Goulmy E, Hämmerling GJ, Koszinowski UH, and Momburg F. A viral ER-resident glycoprotein inactivates the MHC-encoded peptide transporter. Immunity 6: 623-632, 1997.
32. Hewitt EW, Gupta SS, and Lehner PJ. The human cytomegalovirus gene product US6 inhibits ATP binding by TAP. EMBO J 20: 387-396, 2001.
33. Higgins CF. ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8: 67-113, 1992.
34. Hill A, Jugovic P, York I, Russ G, Bennink J, Yewdell J, Ploegh H, and Johnson D. Herpes simplex virus turns off the TAP to evade host immunity. Nature 375: 411-415, 1995.
35. Hoof T, Demmer A, Hadam MR, Riordan JR, and Tümmler B. Cystic fibrosis-type mutational analysis in the ATP-binding cassette transporter signature of human P-glycoprotein MDR1. J Biol Chem 269: 20575-20583, 1994.
36. Horn C, Bremer E, and Schmitt L. Nucleotide dependent monomer/dimer equilibrium of OpuAA, the nucleotide-binding protein of the osmotically regulated ABC transporter OpuA from Bacillus subtilis. J Mol Biol 334: 403-419, 2003.
37. Houde M, Bertholet S, Gagnon E, Brunet S, Goyette G, Laplante A, Princiotta MF, Thibault P, Sacks D, and Desjardins M. Phagosomes are competent organelles for antigen cross-presentation. Nature 425: 402-406, 2003.
38. Hung LW, Wang IX, Nikaido K, Liu PQ, Ames GF, and Kim SH. Crystal structure of the ATP-binding subunit of an ABC transporter. Nature 396: 703-707, 1998.
39. Janas E, Hofacker M, Chen M, Gompf S, van der Does C, and Tampé R. The ATP hydrolysis cycle of the nucleotide-binding domain of the mitochondrial ATP-binding cassette transporter Mdl1p. J Biol Chem 278: 26862-26869, 2003.
40. Johnsen A, France J, Sy MS, and Harding CV. Down-regulation of the transporter for antigen presentation, proteasome subunits, and class I major histocompatibility complex in tumor cell lines. Cancer Res 58: 3660-3667, 1998.
41. Karpowich N, Martsinkevich O, Millen L, Yuan YR, Dai PL, MacVey K, Thomas PJ, and Hunt JF. Crystal structures of the MJ1267 ATP binding cassette reveal an induced-fit effect at the ATPase active site of an ABC transporter. Structure (Camb) 9: 571-586, 2001.
42. Karttunen JT, Lehner PJ, Gupta SS, Hewitt EW, and Cresswell P. Distinct functions and cooperative interaction of the subunits of the transporter associated with antigen processing (TAP). Proc Natl Acad Sci USA 98: 7431-7436, 2001.
43. Kisselev AF, Akopian TN, Woo KM, and Goldberg AL. 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, 1999.
44. Kleijmeer MJ, Kelly A, Geuze HJ, Slot JW, Townsend A, and Trowsdale J. Location of MHC-encoded transporters in the endoplasmic reticulum and cis-Golgi. Nature 357: 342-344, 1992.
45. Knittler MR, Alberts P, Deverson EV, and Howard JC. Nucleotide binding by TAP mediates association with peptide and release of assembled MHC class I molecules. Curr Biol 9: 999-1008, 1999.
46. Koch J, Guntrum R, Heintke S, Kyritsis C, and Tampé R. Functional dissection of the transmembrane domains of the transporter associated with antigen processing (TAP). J Biol Chem 279: 10142-10147 2003.
47. Koppers-Lalic D, Rychlowski M, van Leeuwen D, Rijsewijk FA, Ressing ME, Neefjes JJ, Bienkowska-Szewczyk K, and Wiertz EJ. Bovine herpesvirus 1 interferes with TAP-dependent peptide transport and intracelluiar trafficking of MHC class I molecules in human cells. Arch Virol 148: 2023-2037, 2003.
48. Kutsch O, Vey T, Kerkau T, Hünig T, and Schimpl A. HIV type 1 abrogates TAP-mediated transport of antigenic peptides presented by MHC class I. Transporter associated with antigen presentation. AIDS Res Hum Retroviruses 18: 1319-1325, 2002.
49. Kyritsis C, Gorbulev S, Hutschenreiter S, Pawlitschko K, Abele R, and Tampé R. Molecular mechanism and structural aspects of transporter associated with antigen processing inhibition by the cytomegalovirus protein US6. J Biol Chem 276: 48031-48039, 2001.
50. Lacaille VG and Androlewicz MJ. Herpes simplex virus inhibitor ICP47 destabilizes the transporter associated with antigen processing (TAP) heterodimer. J Biol Chem 273: 17386-17390, 1998.
51. Lankat-Buttgereit B and Tampé R. The transporter associated with antigen processing: function and implications in human diseases. Physiol Rev 82: 187-204, 2002.
52. Lapinski PE, Neubig RR, and Raghavan M. Walker A lysine mutations of TAP1 and TAP2 interfere with peptide translocation but not peptide binding. J Biol Chem 276: 7526-7533, 2001.
53. Lapinski PE, Raghuraman G, and Raghavan M. Nucleotide interactions with membrane-bound transporter associated with antigen processing proteins. J Biol Chem 278: 8229-8237, 2003.
54. Lauvau G, Gubler B, Cohen H, Daniel S, Caillat-Zucman S, and van Endert PM. Tapasin enhances assembly of transporters associated with antigen processing-dependent and -independent peptides with HLA-A2 and HLA-B27 expressed in insect cells. J Biol Chem 274: 31349-31358, 1999.
55. Lehner PJ, Karttunen JT, Wilkinson GW, and Cresswell P. The human cytomegalovirus US6 glycoprotein inhibits transporter associated with antigen processing-dependent peptide translocation. Proc Natl Acad Sci USA 94: 6904-6909, 1997.
56. Lehner PJ, Surman MJ, and Cresswell P. Soluble tapasin restores MHC class I expression and function in the tapasin-negative cell line 220. Immunity 8: 221-231, 1998.
57. Li S, Paulsson KM, Chen S, Sjogren HO, and Wang P. Tapasin is required for efficient peptide binding to transporter associated with antigen processing. J Biol Chem 275: 1581-1586, 2000.
58. Lindquist JA, Hämmerling GJ, and Trowsdale J. ER60/ERp57 forms disulfide-bonded intermediates with MHC class I heavy chain. FASEB J 15: 1448-1450, 2001.
59. Lindquist JA, Jensen ON, Mann M, and Hämmerling GJ. ER-60, a chaperone with thiol-dependent reductase activity involved in MHC class I assembly. EMBO J 17: 2186-2195, 1998.
60. Locher KP, Lee AT, and Rees DC. The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science 296: 1091-1098, 2002.
61. Loo TW, Bartlett MC, and Clarke DM. The "LSGGQ" motif in each nucleotide-binding domain of human P-glycoprotein is adjacent to the opposing walker A sequence. J Biol Chem 277: 41303-41306, 2002.
62. Lybarger L, Wang X, Harris MR, Virgin HW 4th, and Hansen TH. Virus subversion of the MHC class I peptide-loading complex. Immunity 18: 121-130, 2003.
63. MacAry PA, Lindsay M, Scott MA, Craig JI, Luzio JP, and Lehner PJ. Mobilization of MHC class I molecules from late endosomes to the cell surface following activation of CD34-derived human Langerhans cells. Proc Natl Acad Sci USA 98: 3982-3987, 2001.
64. Matsui M, Machida S, Itani-Yohda T, and Akatsuka T. Downregulation of the proteasome subunits, transporter, and antigen presentation in hepatocellular carcinoma, and their restoration by interferon-γ. J Gastroenterol Hepatol 17: 897-907, 2002.
65. Mellman I and Steinman RM. Dendritic cells: specialized and regulated antigen processing machines. Cell 106: 255-258, 2001.
66. Momburg F and Tan P. Tapasin - the keystone of the loading complex optimizing peptide binding by MHC class I molecules in the endoplasmic reticulum. Mol Immunol 39: 217-233, 2002.
67. Neefjes JJ, Momburg F, and Hämmerling GJ. Selective and ATP-dependent translocation of peptides by the MHC-encoded transporter. Science 261: 769-771, 1993.
68. Neumann L, Abele R, and Tampé R. Thermodynamics of peptide binding to the transporter associated with antigen processing (TAP). J Mol Biol 324: 965-973, 2002.
69. Neumann L, Kraas W, Uebel S, Jung G, and Tampé R. 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, 1997.
70. Neumann L and Tampé R. Kinetic analysis of peptide binding to the TAP transport complex: evidence for structural rearrangements induced by substrate binding. J Mol Biol 294: 1203-1213, 1999.
71. Nijenhuis M and Hämmerling GJ. Multiple regions of the transporter associated with antigen processing (TAP) contribute to its peptide binding site. J Immunol 157: 5467-5477, 1996.
72. Ortmann B, Copeman J, Lehner PJ, Sadasivan B, Herberg JA, Grandea AG, Riddell SR, Tampé R, Spies T, Trowsdale J, and Cresswell P. A critical role for tapasin in the assembly and function of multimeric MHC class I-TAP complexes. Science 277: 1306-1309, 1997.
73. Owen BA and Pease LR. TAP association influences the conformation of nascent MHC class I molecules. J Immunol 162: 4677-4684, 1999.
74. Patzlaff JS, van der Heide T, and Poolman B. The ATP/substrate stoichiometry of the ATP-binding cassette (ABC) transporter OpuA. J Biol Chem 278: 29546-29551, 2003.
75. Pfänder R, Neumann L, Zweckstetter M, Seger C, Holak TA, and Tampé R. 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, 1999.
76. Powis SJ, Townsend AR, Deverson EV, Bastin J, Butcher GW, and Howard JC. Restoration of antigen presentation to the mutant cell line RMA-S by an MHC-linked transporter. Nature 354: 528-531, 1991.
77. Princiotta MF, Finzi D, Qian SB, Gibbs J, Schuchmann S, Buttgereit F, Bennink JR, and Yewdell JW. Quantitating protein synthesis, degradation, and endogenous antigen processing. Immunity 18: 343-354, 2003.
78. Purcell AW, Gorman JJ, Garcia-Peydro M, Paradela A, Burrows SR, Talbo GH, Laham N, Peh CA, Reynolds EC, Lopez De Castro JA, and McCluskey J. Quantitative and qualitative influences of tapasin on the class I peptide repertoire. J Immunol 166: 1016-1027, 2001.
79. Raghuraman G, Lapinski PE, and Raghavan M. 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: 41786-41794, 2002.
80. Reits EA, Vos JC, Gromme M, and Neefjes J. The major substrates for TAP in vivo are derived from newly synthesized proteins. Nature 404: 774-778, 2000.
81. Saveanu L, Daniel S, and van Endert PM. 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: 22107-22113, 2001.
82. Schoenhals GJ, Krishna RM, Grandea AG 3rd, Spies T, Peterson PA, Yang Y, and Früh K. Retention of empty MHC class I molecules by tapasin is essential to reconstitute antigen presentation in invertebrate cells. EMBO J 18: 743-753, 1999.
83. Schwede T, Kopp J, Guex N, and Peitsch MC. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31: 3381-3385, 2003.
84. Serwold T, Gonzalez F, Kim J, Jacob R, and Shastri N. ERAAP customizes peptides for MHC class I molecules in the endoplasmic reticulum. Nature 419: 480-483, 2002.
85. Shyamala V, Baichwal V, Beall E, and Ames GF. Structure-function analysis of the histidine permease and comparison with cystic fibrosis mutations. J Biol Chem 266: 18714-18719, 1991.
86. Smith PC, Karpowich N, Millen L, Moody JE, Rosen J, Thomas PJ, and Hunt JF. ATP binding to the motor domain from an ABC transporter drives formation of a nucleotide sandwich dimer. Mol Cell 10: 139-149, 2002.
87. Spies T and DeMars R. Restored expression of major histocompatibility class I molecules by gene transfer of a putative peptide transporter. Nature 351: 323-324, 1991.
88. Tan P, Kropshofer H, Mandelboim O, Bulbuc N, Hämmerling GJ, and Momburg F. 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, 2002.
89. Tomazin R, Hill AB, Jugovic P, York I, van Endert P, Ploegh HL, Andrews DW, and Johnson DC. Stable binding of the herpes simplex virus ICP47 protein to the peptide binding site of TAP. EMBO J 15: 3256-3266, 1996.
90. Turnquist HR, Vargas SE, McIlhaney MM, Li S, Wang P, and Solheim JC. Calreticulin binds to the alphal domain of MHC class I independently of tapasin. Tissue Antigens 59: 18-24, 2002.
91. Uebel S, Kraas W, Kienle S, Wiesmüller KH, Jung G, and Tampé R. Recognition principle of the TAP transporter disclosed by combinatorial peptide libraries. Proc Natl Acad Sci USA 94: 8976-8981, 1997.
92. Uebel S, Meyer TH, Kraas W, Kienle S, Jung G, Wiesmüller KH, and Tampé R. 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, 1995.
93. Van Endert PM, Tampé R, Meyer TH, Tisch R, Bach JF, and McDevitt HO. A sequential model for peptide binding and transport by the transporters associated with antigen processing. Immunity 1: 491-500, 1994.
94. Walter C, Wilken S, and Schneider E. Characterization of site-directed mutations in conserved domains of MalK, a bacterial member of the ATP-binding cassette (ABC) family. FEBS Lett 303: 41-44, 1992.
95. Williams AP, Peh CA, Purcell AW, McCluskey J, and Elliott T. Optimization of the MHC class I peptide cargo is dependent on tapasin. Immunity 16: 509-520, 2002.
96. Yang T, McNally BA, Ferrone S, Liu Y, and Zheng P. A single-nucleotide deletion leads to rapid degradation of TAP-1 mRNA in a melanoma cell line. J Biol Chem 278: 15291-15296, 2003.
97. Zarling AL, Luckey CJ, Marto JA, White FM, Brame CJ, Evans AM, Lehner PJ, Cresswell P, Shabanowitz J, Hunt DF, and Engelhard VH. Tapasin is a facilitator, not an editor, of class I MHC Peptide binding. J Immunol 171: 5287-5295, 2003.