A mechanism of viral immune evasion revealed by cryo-EM analysis of the TAP transporter

Nature

Volumn 529, Issue 7587, 2016, Pages 537-540

  Oldham, Michael L ^a,b   Hite, Richard K ^a,b   Steffen, Alanna M ^b   Damko, Ermelinda ^a   Li, Zongli ^b,c   Walz, Thomas ^a   Chen, Jue ^a,b  

^a ROCKEFELLER UNIVERSITY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; NUCLEOTIDE BINDING PROTEIN; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1; VIRUS ANTIGEN; ABC TRANSPORTER; ICP47 PROTEIN, HERPES SIMPLEX VIRUS; IMMEDIATE EARLY PROTEIN; PROTEIN BINDING; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING (TAP);

ANTIGEN; CELLS AND CELL COMPONENTS; IMMUNE SYSTEM; IMMUNITY; INHIBITION; INHIBITOR; MAJOR HISTOCOMPATIBILITY COMPLEX; PEPTIDE; PROTEIN; TRANSLOCATION; TUMOR; VIRUS;

ARTICLE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; CYTOSOL; CYTOTOXIC T LYMPHOCYTE; ENDOPLASMIC RETICULUM; HERPES SIMPLEX VIRUS; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; IMMUNE EVASION; IMMUNOSURVEILLANCE; NONHUMAN; PRIORITY JOURNAL; VIRUS INFECTION; VIRUS INHIBITION; AMINO ACID SEQUENCE; ANTAGONISTS AND INHIBITORS; CHEMICAL STRUCTURE; CHEMISTRY; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; PROTEIN CONFORMATION; ULTRASTRUCTURE;

SIMPLEXVIRUS;

AMINO ACID SEQUENCE; ANTIGENS, VIRAL; ATP-BINDING CASSETTE TRANSPORTERS; CRYOELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM; HERPESVIRUS 1, HUMAN; IMMEDIATE-EARLY PROTEINS; IMMUNE EVASION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 84956641350     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature16506     Document Type: Article

References (46)

1. Blum, J. S., Wearsch, P. A. & Cresswell, P. Pathways of antigen processing. Annu. Rev. Immunol. 31, 443-473 (2013).
2. van de Weijer, M. L., Luteijn, R. D. & Wiertz, E. J. Viral immune evasion: lessons in MHC class I antigen presentation. Semin. Immunol. 27, 125-137 (2015).
3. Verweij, M. C. et al. Viral inhibition of the transporter associated with antigen processing (TAP): a striking example of functional convergent evolution. PLoS Pathog. 11, e1004743 (2015).
4. Koch, J., Guntrum, R., Heintke, S., Kyritsis, C. & Tampé, R. Functional dissection of the transmembrane domains of the transporter associated with antigen processing (TAP). J. Biol. Chem. 279, 10142-10147 (2004).
5. Hill, A. B., Barnett, B. C., McMichael, A. J. & McGeoch, D. J. 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 (1994).
6. + T lymphocytes. Cell 77, 525-535 (1994).
7. Hill, A. et al. Herpes simplex virus turns off the TAP to evade host immunity. Nature 375, 411-415 (1995).
8. Früh, K. et al. A viral inhibitor of peptide transporters for antigen presentation. Nature 375, 415-418 (1995).
9. Tomazin, R. et al. Stable binding of the herpes simplex virus ICP47 protein to the peptide binding site of TAP. EMBO J. 15, 3256-3266 (1996).
10. Ahn, K. et al. Molecular mechanism and species specificity of TAP inhibition by herpes simplex virus ICP47. EMBO J. 15, 3247-3255 (1996).
11. 2-terminal 35 residues. J. Exp. Med. 185, 1565-1572 (1997).
12. Neumann, L., Kraas, W., Uebel, S., Jung, G. & 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).
13. Aisenbrey, C. et al. Structure and dynamics of membrane-associated ICP47, a viral inhibitor of the MHC I antigen-processing machinery. J. Biol. Chem. 281, 30365-30372 (2006).
14. Powis, S. H. et al. Polymorphism in a second ABC transporter gene located within the class II region of the human major histocompatibility complex. Proc. Natl Acad. Sci. USA 89, 1463-1467 (1992).
15. Henderson, R. et al. Outcome of the first electron microscopy validation task force meeting. Structure 20, 205-214 (2012).
16. Ward, A., Reyes, C. L., Yu, J., Roth, C. B. & Chang, G. Flexibility in the ABC transporter MsbA: alternating access with a twist. Proc. Natl Acad. Sci. USA 104, 19005-19010 (2007).
17. Lin, D. Y., Huang, S. & Chen, J. Crystal structures of a polypeptide processing and secretion transporter. Nature 523, 425-430 (2015).
18. Aller, S. G. et al. Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 323, 1718-1722 (2009).
19. Jin, M. S., Oldham, M. L., Zhang, Q. & Chen, J. Crystal structure of the multidrug transporter P-glycoprotein from Caenorhabditis elegans. Nature 490, 566-569 (2012).
20. Leonhardt, R. M., Keusekotten, K., Bekpen, C. & Knittler, M. R. Critical role for the tapasin-docking site of TAP2 in the functional integrity of the MHC class I-peptide-loading complex. J. Immunol. 175, 5104-5114 (2005).
21. Nijenhuis, M. & Hämmerling, G. J. Multiple regions of the transporter associated with antigen processing (TAP) contribute to its peptide binding site. J. Immunol. 157, 5467-5477 (1996).
22. Corradi, V., Singh, G. & Tieleman, D. P. The human transporter associated with antigen processing: molecular models to describe peptide binding competent states. J. Biol. Chem. 287, 28099-28111 (2012).
23. Gorbulev, S., Abele, R. & 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).
24. Geng, J., Sivaramakrishnan, S. & Raghavan, M. Analyses of conformational states of the transporter associated with antigen processing (TAP) protein in a native cellular membrane environment. J. Biol. Chem. 288, 37039-37047 (2013).
25. Herget, M. et al. Conformation of peptides bound to the transporter associated with antigen processing (TAP). Proc. Natl Acad. Sci. USA 108, 1349-1354 (2011).
26. Chen, S., Oldham, M. L., Davidson, A. L. & Chen, J. Carbon catabolite repression of the maltose transporter revealed by X-ray crystallography. Nature 499, 364-368 (2013).
27. Kadaba, N. S., Kaiser, J. T., Johnson, E., Lee, A. & Rees, D. C. The high-affinity E. coli methionine ABC transporter: structure and allosteric regulation. Science 321, 250-253 (2008).
28. Gerber, S., Comellas-Bigler, M., Goetz, B. A. & Locher, K. P. Structural basis of trans-inhibition in a molybdate/tungstate ABC transporter. Science 321, 246-250 (2008).
29. Li, X. et al. Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nature Methods 10, 584-590 (2013).
30. Penczek, P. A. et al. CTER-rapid estimation of CTF parameters with error assessment. Ultramicroscopy 140, 9-19 (2014).
31. Ludtke, S. J., Baldwin, P. R. & Chiu, W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82-97 (1999).
32. Yang, Z., Fang, J., Chittuluru, J., Asturias, F. J. & Penczek, P. A. Iterative stable alignment and clustering of 2D transmission electron microscope images. Structure 20, 237-247 (2012).
33. Hohn, M. et al. SPARX, a new environment for cryo-EM image processing. J. Struct. Biol. 157, 47-55 (2007).
34. Mastronarde, D. N. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152, 36-51 (2005).
35. Brilot, A. F. et al. Beam-induced motion of vitrified specimen on holey carbon film. J. Struct. Biol. 177, 630-637 (2012).
36. Campbell, M. G. et al. Movies of ice-embedded particles enhance resolution in electron cryo-microscopy. Structure 20, 1823-1828 (2012).
37. Rohou, A. & Grigorieff, N. CTFFIND4: fast and accurate defocus estimation from electron micrographs. J. Struct. Biol. 192, 216-221 (2015).
38. Grant, T. & Grigorieff, N. Measuring the optimal exposure for single particle cryo-EM using a 2.6 Å reconstruction of rotavirus VP6. eLife 4, e06980 (2015).
39. Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530 (2012).
40. Grigorieff, N. FREALIGN: high-resolution refinement of single particle structures. J. Struct. Biol. 157, 117-125 (2007).
41. Gaudet, R. & Wiley, D. C. Structure of the ABC ATPase domain of human TAP1, the transporter associated with antigen processing. EMBO J. 20, 4964-4972 (2001).
42. Eswar, N. et al. Comparative protein structure modeling using Modeller. Curr. Protoc. Bioinformat. Chapter 5, Unit 5.6 (2006).
43. Shintre, C. A. et al. Structures of ABCB10, a human ATP-binding cassette transporter in apo- and nucleotide-bound states. Proc. Natl Acad. Sci. USA 110, 9710-9715 (2013).
44. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486-501 (2010).
45. DeLano, W. L. The PyMOL molecular graphics system (DeLano Scientific, 2002).
46. Pettersen, E. F. et al. UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).