Membrane topology and dimerization of the two subunits of the transporter associated with antigen processing reveal a three-domain structure

Journal of Immunology

Volumn 163, Issue 12, 1999, Pages 6679-6685

  Vos, Jan C ^a   Spee, Pieter ^a   Momburg, Frank ^b   Neefjes, Jacques ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; PROTEIN SUBUNIT;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANTIGEN PRESENTATION; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOPLASM; DIMERIZATION; ENDOPLASMIC RETICULUM; GENE DELETION; MEMBRANE STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN;

EID: 0032757721     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.163.12.6679     Document Type: Article

References (40)

1. Trowsdale, J., I. Hanson, I. Mockridge, S. Beck, A. Townsend, and A. Kelly. 1990. Sequences encoded in the class II region of the MHC related to the "ABC" superfamily of transporters. Nature 34:741.
2. Bahram, S., D. Arnold, M. Bresnahan, J. L. Strominger, and T. Spies. 1991. Two putative subunits of a peptide pump encoded in the human major histocompatibility complex class II region. Proc. Natl. Acad. Sci. USA 88:10094.
3. Kelly, A., S. H. Powis, L.-A. Kerr, I. Mockridge, T. Elliot, J. Bastin, B. Uchanska-Ziegler, A. Ziegler, J. Trowsdale, and A. Townsend. 1992. Assembly and function of the two ABC transporter proteins encoded in the human major histocompatibility complex. Nature 355:641.
4. Spies, T., V. Cerundolo, M. Colonna, P. Creswell, A. Townsend, and R. DeMars. 1992. Presentation of viral antigen by MHC class I molecules is dependent on a putative peptide transporter heterodimer. Nature 355:644.
5. Higgins, C. F. 1992. ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol. 8:67.
6. Koopmann, J.-O., G. J. Hämmerling, and F. Momburg. 1997. Generation, intracellular transport and loading of peptides associated with MHC class I molecules. Curr. Opin. Immunol. 9:80.
7. Pamer, E., and P. Cresswell. 1998. Mechanism of MHC class I-restricted antigen processing. Annu. Rev. Immunol. 16:323.
8. Ortmann, B., J. Copeman, P. J. Lehner, B. Sadasivan, J. A. Herberg, A. G. Grandea, S. R. Riddell, R. Tampé, T. Spies, J. Trowsdale, and P. Cresswell. 1997. A critical role for tapasin in the assembly and function of multimeric MHC Class I-TAP complexes. Science 277:1306.
9. Li, S., H.-O. Sjögren, U. Hellman, R. F. Pettersson, and P. Wang. 1997. Cloning and functional characterization of a subunit of the transporter associated with antigen processing. Proc. Natl. Acad. Sci. USA 94:8708.
10. Androlewicz, M. J., and P. Cresswell. 1994. Human transporters associated with antigen processing possess a promiscuous peptide-binding site. Immunity 1:7.
11. Momburg, F., J. Roelse, G. J. Hämmerling, and J. Neefjes. 1994. Peptide size selection by the major histocompatibility complex-encoded peptide transporter. J. Exp. Med. 179:1613.
12. Grommé, M., R. van der Valk, K. Sliedrecht, L. Vernie, R. Liskamp, G. Hämmerling, J.-O. Koopmann, F. Momburg, and J. Neefjes. 1997. The rational design of TAP inhibitors using peptide substrate modifications and peptidomimetics. Eur. J. Immunol. 27:898.
13. Heemels, M.-T., T. N. M. Schumacher, K. Wonigeit, and H. L. Ploegh. 1993. Peptide translocation by variants of the transporter associated with antigen processing. Science 262:2059.
14. Momburg, F., J. Roelse, J. C. Howard, G. W. Butcher, G. J. Hämmerling, and J. J. Neefjes. 1994. Selectivity of MHC-encoded peptide transporters from human, mouse and rat. Nature 367:648.
15. Deverson, E. V., L. Leong, A. Seelig, W. J. Coadwell, E. M. Tredgett, G. W. Butcher, and J. C. Howard. 1998. Functional analysis by site-directed mutagenesis of the complex polymorphism in rat transporter associated with antigen processing. J. Immunol. 160:2767.
16. Van Endert, P. M., R. Tampé, 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.
17. 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.
18. Früh, K., K. Ahn, H. Djaballah, P. Sempe, P. M. van Endert, R. Tampé, P. A. Peterson, and Y. Yang. 1995. A viral inhibitor of peptide transporters for antigen presentation. Nature 375:415.
19. Ahn, K., A. Gruhler, B. Galocha, T. R. Jones, E. J. H. J. Wiertz, H. L. Ploegh, P. A. Peterson, Y. Yang, and K. Früh. 1997. The ER-luminal domain of the HCMV glycoprotein US6 inhibits peptide translocation by TAP. Immunity 6:613.
20. Hengel, H., J.-O. Koopmann, T. Flohr, W. Muranyi, E. Goulmy, G. J. Hämmerling, U. H. Koszinowski, and F. Momburg. 1997. A viral ER-resident glycoprotein inactivates the MHC-encoded peptide transporter. Immunity 6:623.
21. Nijenhuis, M., S. Schmitt, E. A. Armandola, R. Obst, J. Brunner, and G. J. Hämmerling. 1996. Identification of a contact region for peptide on the TAP1 chain of the transporter associated with antigen processing. J. Immunol. 156: 2186.
22. Claesson, L., D. Larhammer, L. Rask, and P. A. Peterson. 1983. cDNA clone for the human invariant gamma chain of class II histocompatibility antigens and its implications for the protein structure. Proc. Natl. Acad. Sci. USA 80:7395.
23. Powis, S. H., S. Tonks, I. Mockridge, A. P. Kelly, J. G. Bodmer, and J. Trowsdale. 1993. Alleles and haplotypes of the MHC-encoded ABC transporters TAP1 and TAP2. Immunogenetics 37:373.
24. Nilsson, T., M. Jackson, and P. A. Peterson. 1989. Short cytoplasmic sequences serve as retention signals for transmembrane proteins in the endoplasmic reticulum. Cell 58:707.
25. Gileadi, U., and C. F. Higgins. 1997. Membrane topology of the ATP-binding cassette transporter associated with antigen presentation (Tap1) expressed in Escherichia coli. J. Biol. Chem. 272:11103.
26. Kleijmeer, M. J., A. Kelly, H. J. Geuze, J. W. Slot, A. Townsend, and J. Trowsdale. 1992. Location of MHC-encoded transporters in the endoplasmic reticulum and cis-Golgi. Nature 357:342.
27. Russ, G., F. Esquivel, J. W. Yewdell, P. Cresswell, T. Spies, and J. R. Bennink. 1995. Assembly, intracellular localization, and nucleotide binding properties of the human peptide transporters TAP1 and TAP2 expressed by recombinant vaccinia virus. J. Biol. Chem. 270:21312.
28. Bakke, O., and B. Dobberstein. 1990. MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell 63:707.
29. Wilkinson, B. M., A. J. Critchley, and C. J. Stirling. 1996. Determination of the transmembrane topology of yeast Sec61p, an essential component of the endoplasmic reticulum translocation complex. J. Biol. Chem. 271:25590.
30. Zhang, J. T., and V. Ling. 1995. Involvement of cytoplasmic factors regulating the membrane orientation of P-glycoprotein sequences. Biochemistry 34:9159.
31. Skach, W. R., and V. R. Lingappa. 1993. Amino-terminal assembly of human P-glycoprotein at the endoplasmic reticulum is directed by cooperative action of two internal sequences. J. Biol. Chem. 268:23552.
32. Powis, S. J., E. V. Deverson, W. J. Coadwel, A. Ciruela, N. S. Smith, G. W. Butcher, and J. C. Howard. 1992. Effect of polymorphism of an MHC-linked transporter on the peptides assembled in a class I molecule. Nature 357: 211.
33. Armandola, E. A., F. Momburg, M. Nijenhuis, N. Bulbuc, K. Früh, and G. J. Hämmerling. 1996. A point mutation in the human transporter associated with antigen processing (TAP2) alters the peptide specificity. Eur. J. Immunol. 26: 1748.
34. Momburg, F., E. A. Armandola, M. Post, and G. J. Hämmerling. 1996. Residues in TAP2 peptide transporters controlling substrate specificity. J. Immunol. 156: 1756.
35. Nijenhuis, M., and G. J. Hämmerling. 1996. Multiple regions of the transporter associated with antigen processing (TAP) contribute to its peptide binding site. J. Immunol. 157:5467.
36. Shin, J., R. L. Dunbrack, Jr., S. Lee, and J. L. Strominger. 1991. Signals for retention of transmembrane proteins in the endoplasmic reticulum studied with CD4 truncation mutants. Proc. Natl. Acad Sci. USA 88:1918.
37. Schutze, M.-P., P. A. Peterson, and M. R. Jackson. 1994. An N-terminal double-arginine motif maintains type II membrane proteins in the endoplasmic reticulum. EMBO J. 13:1696.
38. Ahn, K., E. Szczesna-Skorupa, and B. Kemper. 1993. The amino-terminal 29 amino acids of cytochrome P450 2C1 are sufficient for retention in the endoplasmic reticulum. J. Biol. Chem. 268:18726.
39. Sato, M., K. Sato, and A. Nakano. 1996. Endoplasmic reticulum localization of Sec12p is achieved by two mechanisms: Rer1p-dependent retrieval that requires the transmembrane domain and Rer1p-independent retention that involves the cytoplasmic domain. J. Cell Biol. 134:279.
40. Vos, J. C., E. A. J. Reits, E. Wojcik-Jacobs, and J. Neefjes. 2000. Head-head/ tail-tail relative orientation of the pore-forming domains of the heterodimeric ABC transporter TAP. Curr. Biol., In press.