Molecular mechanism and species specificity of TAP inhibition by herpes simplex virus protein ICP47

EMBO Journal

Volumn 15, Issue 13, 1996, Pages 3247-3255

  Ahn, Kwaangseog ^a   Meyer, Thomas H ^b   Uebel, Stephan ^b   Sempé, Pascal ^a   Djaballah, Hakim ^a   Yang, Young ^a   Peterson, Per A ^a   Früh, Klaus ^a   Tampé, Robert ^b,c  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

ABC transporter; Antigen presentation; Antigen processing; Herpes simplex; Immune evasion

Indexed keywords

CARRIER PROTEIN; IMMEDIATE EARLY PROTEIN; RECOMBINANT PROTEIN; VIRUS PROTEIN;

ANIMAL CELL; ANTIGEN PRESENTATION; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; HERPES SIMPLEX VIRUS; HUMAN; INSECT; MICROSOME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SPECIES DIFFERENCE;

ANIMALIA; HERPES; INSECTA; MURINAE; SIMPLEXVIRUS;

EID: 0030016036     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00689.x     Document Type: Article

References (47)

1. Andersson, M., Pääbo, S., Nilsson, T. and Peterson, P.A. (1985) Impaired intracellular transport of class I MHC antigens as a possible means for adenoviruses to evade immune surveillance. Cell, 43, 215-222.
2. Androlewicz, M.J. and Cresswell, P. (1994) Human transporters associated with antigen processing possess a promiscuous peptide-binding site. Immunity, 1, 7-14.
3. Androlewicz, M.J., Anderson, K.S. and Cresswell, P. (1993) Evidence that transporters associated with antigen processing translocate a major histocompatibility complex class I-binding peptide into the endoplasmic reticulum in an ATP-dependent manner. Proc, Natl Acad. Sci. USA, 90, 9130-9134.
4. Androlewicz, M.J., Ortmann, B., Van Endert, P.M., Spies, T. and Cresswell, P. (1994) Characteristics of peptide binding and major histocompatibility complex class I/β2-microglobulin binding to the transporters associated with antigen processing (TAP1 and TAP2). Proc. Natl Acad. Sci. USA, 91, 12716-12720.
5. Brutkiewicz, R.R. and Welsh, R.M. (1995) Major histocompatibility complex class I antigens and the control of viral infections by natural killer cells. J. Virol., 69, 3967-3971.
6. Burgert, H.-G. and Kvist, S. (1985) An adenovirus type 2 glycoprotein blocks cell surface expression of human histocompatibility class I antigens. Cell, 41, 987-997.
7. Deverson, E., Gow, I.R., Coadwell, W.J., Monaco, J.J., Butcher, G.W. and Howard, J.C. (1990) MHC class II region encoding proteins related to the multidrug resistance family of transmembrane transporters. Nature, 348, 738-741.
8. Früh, K., Yang, Y., Arnold, D., Chambers, J., Wu, L., Waters, J.B., Spies, T. and Peterson, P.A. (1992) Alternative exon usage and processing of the major histocompatibility complex-encoded proteasome subunits. J. Biol. Chem., 267, 22131-22140.
9. Früh, K., Ahn, K., Djaballah, H., Sempé, P., van Endert, P.M., Tampé, R., Peterson, P.A. and Yang, Y. (1995) A viral inhibitor of peptide transporters for antigen presentation. Nature, 375, 415-418.
10. Heemels, M.T., Schumacher, T.N., Wonigeit, K. and Ploegh, H.L. (1993) Peptide translocation by variants of the transporter associated with antigen processing. Science, 262, 2059-2063.
11. Higgins, C.F. (1992) ABC transporters: from microorganisms to man. Annu. Rev. Cell Biol., 8, 67-113.
12. Hill, A. and Ploegh, H. (1995) Getting the inside out: the transporters associated with antigen processing and the presentation of viral antigen. Proc. Natl Acad. Sci. USA, 92, 341-343.
13. Hill, A.B., Barnett, B.C., McMichael, A.J. and McGeoch, D.J. (1994) HLA class I molecules are not transported to the cell surface in cells infected with Herpes simplex virus types 1 and 2. J. Immunol., 152, 2736-2741.
14. Hill, A., Jugovic, P. York, I., Rus, G., Bennink, J., Yewdell, J., Ploegh, H. and Johnson, D. (1995) Herpes simplex virus turns off the TAP to evade host immunity. Nature, 375, 411-415.
15. Hochuli, E., Bannwarth, W., Döbeli, H., Gentz, R. and Stüber, D. (1988) Genetic approach to facilitate purification of recombinant proteins with a novel metal chelate adsorbent. Biotechnology, 6, 1321-1325.
16. Howard, J.C. (1995) Supply and transport of peptides presented by class I MHC molecules. Curr. Opin. Immunol., 7, 69-76.
17. Jackson, M.R. and Peterson, P.A. (1993) Assembly and intracellular transport of MHC class I molecules. Annu. Rev. Cell Biol., 9, 207-235.
18. Jackson, M.R., Song, E.S., Yang, Y. and Peterson, P.A. (1992) Empty and peptide-containing conformers of class I major histocompatibility complex molecules expressed in Drosophila melanogaster cells. Proc. Natl Acad. Sci. USA, 89, 12117-12121.
19. Jennings, S.R., Rice, P.L., Kloszewski, E.D., Anderson, R.W., Thompson, D.L. and Tevethia, S.S. (1985) Effect of Herpes simplex virus types 1 and 2 on surface expression of class I major histocompatibility antigens on infected cells. J. Virol., 56, 757-766.
20. Judd, R.C. (1990) Peptide mapping. Methods Enzymol., 182, 613-618.
21. Koup, R.A. (1994) Virus escape from CTL recognition. J. Exp. Med., 180, 779-782.
22. Leibson, P.J. (1995) MHC-recognizing receptors: they're not just for T-cells anymore. Immunity, 3, 5-8.
23. Mester, J.C. and Rouse, B. (1991) The mouse model and understanding immunity to Herpes simplex virus. Rev. Infect. Dis., 13 (Suppl. 11), S935-945.
24. Meyer, T.H., Van Endert, P.M., Uebel, S., Ehring, B. and Tampé, R. (1994) Functional expression and purification of the ABC transporter complex associated with antigen processing (TAP) in insect cells. FEBS Lett., 351, 443-447.
25. Michaelek, M.T., Grant, E.P., Gramm, C., Goldberg, A.L. and Rock, K.L. (1993) A role for the ubiquitin dependent proteolytic pathway in MHC class I-restricted antigen presentation. Nature, 363, 552-554.
26. Momburg, F., Roelse, J., Hammerling, G.J. and Neefjes, J.J. (1994a) Peptide size selection by the major histocompatibility complex-encoded peptide transporters. J. Exp. Med., 179, 1613-1623.
27. Momburg, F., Roelse, J., Howard, J.C., Butcher, G.W., Hammerling, G.J. and Neefjes, J.J. (1994b) Selectivity of MHC-encoded peptide transporters from human, mouse and rat. Nature, 367, 648-651.
28. Monaco, J.J., Cho, S. and Attaya, M. (1990) Transport protein genes in the murine MHC: possible implications for antigen processing. Science, 250, 1723-1726.
29. Müller, K.M., Ebensperger, K.M. and Tampé, R. (1994) Nucleotide binding to the hydrophilic C-terminal domain of the transporter associated with antigen-processing (TAP). J. Biol. Chem., 269, 14032-14037.
30. Neefjes, J.J., Momburg, F. and Hammerling, G.J. (1993) Selective and ATP-dependent translocation of peptides by the MHC-encoded transporter. Science, 261, 769-771.
31. Ortmann, B., Androlewicz, M.J. and Cresswell, P. (1994) MHC class II β2-microglobulin complexes associate with transporters before peptide binding. Nature, 368, 864-867.
32. Powis, S.J., Deverson, E.V., Coadwell, W.J., Ciruela, A., Huskisson, N.S., Smith, H., Butcher, G.W. and Howard, J.C. (1992) Effect of polymorphism of an MHC-linked transporter on peptides assembled in a class I molecule. Nature, 357, 211-215.
33. Rammensee, H.G., Falk, K. and Rotschke, O. (1993) Peptides naturally presented by MHC class I molecules. Annu. Rev. Immunol., 11, 213-244.
34. Rock, K.L., Gramm, C., Rothstein, L., Clark, K., Stein, R., Dick, L., Hwang, D. and Goldberg, A.L. (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.
35. Russ, G., Esquivel, F., Yewdell, J.W., Cresswell, P., Spies, T. and Bennink, J.R. (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, 21312-21318.
36. Schumacher, T.N. et al. (1994) Peptide length and sequence specificity of the mouse TAP1/TAP2 translocator. J. Exp. Med., 179, 533-540.
37. Shepherd, J.C., Schumacher, T.N.M., Ashton-Rickardt, P.G., Imaeda, S., Ploegh, H., Janeway, C.A. and Tonegawa, S. (1993) TAP1-dependent peptide translocation in vitro is ATP-dependent and selective. Cell, 74, 577-584.
38. Spies, T., Bresnahan, M., Bahram, S., Arnold, M., Blanck, G., Mellins, E., Pious, D. and DeMars, R. (1990) A gene in the human major histocompatibility complex class II region controlling the class I antigen presentation pathway. Nature, 348, 744-747.
39. 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.
40. Townsend, A. and Bodmer, H. (1989) Antigen recognition by class I-restricted T lymphocytes. Annu. Rev. Immunol., 7, 601-624.
41. Trowsdale, J., Hanson, I., Mockridge, I., Beck, S., Townsend, A. and Kelly, A. (1990) Sequences encoded in the class II region of the MHC relatedtothe 'ABC' superfamily of transporters. Nature, 348, 741-744.
42. Uebel, S., Meyer, T.M., Kraas, W., Kienle, S., Jung, G., Wiesmüller, K.-H. and Tampé, R. (1995) Requirements for peptide binding to the human transporter associated with antigen processing (TAP) revealed by peptide scans and complex libraries. J. Biol. Chem., 270, 18512-18516.
43. Van Endert, P.M., 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.
44. Wang, K., Früh, K., Peterson, P.A. and Yang, Y. (1994) Nucleotide binding of the C-terminal domains of the major histocompatibility complex-encoded transporter expressed in Drosophila melanogaster cells. FEBS Lett., 350, 337-341.
45. Watson, R.J. and Vande Woude, G.F. (1982) DNA sequence of an immediate-early gene (IE mRNA-5) of herpes simplex virus type 1. Nucleic Acids Res., 10, 979-991.
46. Yang, Y., Früh, K., Chambers, J., Waters, J.B., Wu, L. Spies, T. and Peterson, P.A. (1992) Major Histocompatibility Complex (MHC)-encoded HAM2 is necessary for peptide loading onto class I MHC molecules. J. Biol. Chem., 267, 11669-11672.
47. York, I.A., Roop, C., Andrews, D.W., Riddell, S.R., Graham, F.L. and Johnson, D.C. (1994) A cytosolic Herpes simplex protein inhibits antigen presentation to CD8+ T lymphocytes. Cell, 77, 525-535.