A sensor-adaptor mechanism for enterovirus uncoating from structures of EV71

Nature Structural and Molecular Biology

Volumn 19, Issue 4, 2012, Pages 424-429

  Wang, Xiangxi ^a   Peng, Wei ^a   Ren, Jingshan ^b   Hu, Zhongyu ^c   Xu, Jiwei ^a   Lou, Zhiyong ^d   Li, Xumei ^a   Yin, Weidong ^c   Shen, Xinliang ^c   Porta, Claudine ^b   Walter, Thomas S ^b   Evans, Gwyndaf ^e   Axford, Danny ^e   Owen, Robin ^e   Rowlands, David J ^f   Wang, Junzhi ^c   Stuart, David I ^b,e   Fry, Elizabeth E ^b   Rao, Zihe ^a,d  

^a INSTITUTE OF BIOPHYSICS   (China)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c NATIONAL INSTITUTES FOR FOOD AND DRUG CONTROL   (China)

^d Tsinghua University   (China)

^e DIAMOND LIGHT SOURCE LTD   (United Kingdom)

^f UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR; CAPSID PROTEIN;

ARTICLE; CELL ADHESION; CONTROLLED STUDY; ENTEROVIRUS 71; HAND FOOT AND MOUTH DISEASE; HYDROPHOBICITY; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; SENSOR; VIRUS CAPSID; VIRUS MORPHOLOGY; VIRUS PARTICLE; VIRUS UNCOATING; CHEMICAL STRUCTURE; CHEMISTRY; ENTEROVIRUS; ENTEROVIRUS INFECTION; HUMAN; VIRION; VIROLOGY; X RAY CRYSTALLOGRAPHY;

ENTEROVIRUS; HUMAN ENTEROVIRUS 71; MIRIDAE;

CAPSID; CAPSID PROTEINS; CRYSTALLOGRAPHY, X-RAY; ENTEROVIRUS A, HUMAN; ENTEROVIRUS INFECTIONS; HAND, FOOT AND MOUTH DISEASE; HUMANS; MODELS, MOLECULAR; VIRION;

EID: 84861316194     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2255     Document Type: Article

References (58)

1. Brown, B.A. & Pallansch, M.A. Complete nucleotide sequence of enterovirus 71 is distinct from poliovirus. Virus Res. 39, 195-205 (1995). (Pubitemid 26054785)
2. McMinn, P.C. An overview of the evolution of enterovirus 71 and its clinical and public health significance. FEMS Microbiol. Rev. 26, 91-107 (2002). (Pubitemid 34454778)
3. Wu, Y. et al. Structures of EV71 RNA-dependent RNA polymerase in complex with substrate and analogue provide a drug target against the hand-foot-and-mouth disease pandemic in China. Protein Cell 1, 491-500 (2010).
4. Basavappa, R. et al. Role and mechanism of the maturation cleavage of VP0 in poliovirus assembly: structure of the empty capsid assembly intermediate at 2.9 resolution. Protein Sci. 3, 1651-1669 (1994). (Pubitemid 24356589)
5. Curry, S. et al. Dissecting the roles of VP0 cleavage and RNA packaging in picornavirus capsid stabilization: the structure of empty capsids of foot-and-mouth disease virus. J. Virol. 71, 9743-9752 (1997). (Pubitemid 27492423)
6. Tuthill, T.J., Groppelli, E., Hogle, J.M. & Rowlands, D.J. Picornaviruses. Curr. Top. Microbiol. Immunol. 343, 43-89 (2010).
7. Ansardi, D.C. & Morrow, C.D. Amino acid substitutions in the poliovirus maturation cleavage site affect assembly and result in accumulation of provirions. J. Virol. 69, 1540-1547 (1995).
8. Jacobson, M.F. & Baltimore, D. Morphogenesis of poliovirus. I. Association of the viral RNA with coat protein. J. Mol. Biol. 33, 369-378 (1968).
9. Liu, C.C. et al. Purification and characterization of enterovirus 71 viral particles produced from Vero cells grown in a serum-free microcarrier bioreactor system. PLoS ONE 6, e20005 (2011).
10. Guttman, N. & Baltimore, D. A plasma membrane component able to bind and alter virions of poliovirus type 1: studies on cell-free alteration using a simplified assay. Virology 82, 25-36 (1977). (Pubitemid 8193016)
11. Marongiu, M.E., Pani, A., Corrias, M.V., Sau, M. & La Colla, P. Poliovirus morphogenesis. I. Identification of 80S dissociable particles and evidence for the artifactual production of procapsids. J. Virol. 39, 341-347 (1981). (Pubitemid 11042700)
12. Le Bouvier, G.L. The modification of poliovirus antigens by heat and ultraviolet light. Lancet 269, 1013-1016 (1955).
13. Blondel, B., Akacem, O., Crainic, R., Couillin, P. & Horodniceanu, F. Detection by monoclonal antibodies of an antigenic determinant critical for poliovirus neutralization present on VP1 and on heat-inactivated virions. Virology 126, 707-710 (1983). (Pubitemid 13089891)
14. Hogle, J.M. Poliovirus cell entry: common structural themes in viral cell entry pathways. Annu. Rev. Microbiol. 56, 677-702 (2002). (Pubitemid 35217471)
15. Olson, N.H. et al. Structure of a human rhinovirus complexed with its receptor molecule. Proc. Natl. Acad. Sci. USA 90, 507-511 (1993). (Pubitemid 23028892)
16. Rossmann, M.G. et al. Structure of a human common cold virus and functional relationship to other picornaviruses. Nature 317, 145-153 (1985). (Pubitemid 16243130)
17. Zhang, P. et al. Crystal structure of CD155 and electron microscopic studies of its complexes with polioviruses. Proc. Natl. Acad. Sci. USA 105, 18284-18289 (2008).
18. Crowell, R.L. & Philipson, L. Specific alterations of coxsackievirus B3 eluted from HeLa cells. J. Virol. 8, 509-515 (1971).
19. Kaplan, G. et al. Identification of a surface glycoprotein on African green monkey kidney cells as a receptor for hepatitis A virus. EMBO J. 15, 4282-4296 (1996). (Pubitemid 26278711)
20. Lonberg-Holm, K., Gosser, L.B. & Kauer, J.C. Early alteration of poliovirus in infected cells and its specific inhibition. J. Gen. Virol. 27, 329-342 (1975).
21. Fricks, C.E. & Hogle, J.M. Cell-induced conformational change in poliovirus: externalization of the amino terminus of VP1 is responsible for liposome binding. J. Virol. 64, 1934-1945 (1990). (Pubitemid 20148434)
22. Greve, J.M. et al. Mechanisms of receptor-mediated rhinovirus neutralization defined by two soluble forms of ICAM-1. J. Virol. 65, 6015-6023 (1991).
23. Bostina, M., Levy, H., Filman, D.J. & Hogle, J.M. Poliovirus RNA is released from the capsid near a twofold symmetry axis. J. Virol. 85, 776-783 (2011).
24. Bubeck, D. et al. The structure of the poliovirus 135S cell entry intermediate at 10-angstrom resolution reveals the location of an externalized polypeptide that binds to membranes. J. Virol. 79, 7745-7755 (2005). (Pubitemid 40756808)
25. Levy, H.C., Bostina, M., Filman, D.J. & Hogle, J.M. Catching a virus in the act of RNA release: a novel poliovirus uncoating intermediate characterized by cryo-electron microscopy. J. Virol. 84, 4426-4441 (2010).
26. Hendry, E. et al. The crystal structure of coxsackievirus A9: new insights into the uncoating mechanisms of enteroviruses. Structure 7, 1527-1538 (1999). (Pubitemid 30007238)
27. Belnap, D.M. et al. Molecular tectonic model of virus structural transitions: the putative cell entry states of poliovirus. J. Virol. 74, 1342-1354 (2000). (Pubitemid 30044084)
28. Siebert, X. & Navaza, J. UROX 2.0: an interactive tool for fitting atomic models into electron-microscopy reconstructions. Acta Crystallogr. D Biol. Crystallogr. 65, 651-658 (2009).
29. Filman, D.J. et al. Structural factors that control conformational transitions and serotype specificity in type 3 poliovirus. EMBO J. 8, 1567-1579 (1989). (Pubitemid 19274384)
30. Grant, R.A. et al. Structures of poliovirus complexes with anti-viral drugs: implications for viral stability and drug design. Curr. Biol. 4, 784-797 (1994). (Pubitemid 124001574)
31. Smith, T.J. et al. The site of attachment in human rhinovirus 14 for antiviral agents that inhibit uncoating. Science 233, 1286-1293 (1986). (Pubitemid 16002229)
32. McSharry, J.J., Caliguiri, L.A. & Eggers, H.J. Inhibition of uncoating of poliovirus by arildone, a new antiviral drug. Virology 97, 307-315 (1979). (Pubitemid 10222403)
33. Hogle, J.M., Chow, M. & Filman, D.J. Three-dimensional structure of poliovirus at 2.9Å resolution. Science 229, 1358-1365 (1985). (Pubitemid 16222374)
34. Smyth, M. et al. Implications for viral uncoating from the structure of bovine enterovirus. Nat. Struct. Biol. 2, 224-231 (1995).
35. Foo, D.G. et al. Identification of neutralizing linear epitopes from the VP1 capsid protein of Enterovirus 71 using synthetic peptides. Virus Res. 125, 61-68 (2007). (Pubitemid 46413387)
36. Liu, C.C. et al. Identification and characterization of a cross-neutralization epitope of Enterovirus 71. Vaccine 29, 4362-4372 (2011).
37. Yang, S.L., Chou, Y.T., Wu, C.N. & Ho, M.S. Annexin II binds to capsid protein VP1 of enterovirus 71 and enhances viral infectivity. J. Virol. 85, 11809-11820 (2011).
38. Nishimura, Y. et al. Human P-selectin glycoprotein ligand-1 is a functional receptor for enterovirus 71. Nat. Med. 15, 794-797 (2009).
39. Yamayoshi, S. et al. Scavenger receptor B2 is a cellular receptor for enterovirus 71. Nat. Med. 15, 798-801 (2009).
40. Rossmann, M.G., He, Y. & Kuhn, R.J. Picornavirus-receptor interactions. Trends Microbiol. 10, 324-331 (2002). (Pubitemid 34756532)
41. He, Y. et al. Complexes of poliovirus serotypes with their common cellular receptor, CD155. J. Virol. 77, 4827-4835 (2003). (Pubitemid 36402832)
42. Xiao, C. et al. The crystal structure of coxsackievirus A21 and its interaction with ICAM-1. Structure 13, 1019-1033 (2005). (Pubitemid 40943333)
43. Oliveira, M.A. et al. The structure of human rhinovirus 16. Structure 1, 51-68 (1993).
44. Kim, S. et al. Conformational variability of a picornavirus capsid: pH-dependent structural changes of Mengo virus related to its host receptor attachment site and disassembly. Virology 175, 176-190 (1990). (Pubitemid 20093073)
45. McDermott, B.M. Jr., Rux, A.H., Eisenberg, R.J., Cohen, G.H. & Racaniello, V.R. Two distinct binding affinities of poliovirus for its cellular receptor. J. Biol. Chem. 275, 23089-23096 (2000). (Pubitemid 30646200)
46. Giranda, V.L. et al. Acid-induced structural changes in human rhinovirus 14: possible role in uncoating. Proc. Natl. Acad. Sci. USA 89, 10213-10217 (1992).
47. Davis, M.P. et al. Recombinant VP4 of human rhinovirus induces permeability in model membranes. J. Virol. 82, 4169-4174 (2008). (Pubitemid 351521253)
48. Racaniello, V.R. Early events in poliovirus infection: virus-receptor interactions. Proc. Natl. Acad. Sci. USA 93, 11378-11381 (1996). (Pubitemid 26347129)
49. Lin, J. et al. An externalized polypeptide partitions between two distinct sites on genome-released poliovirus particles. J. Virol. 85, 9974-9983 (2011).
50. Kay, B.K., Williamson, M.P. & Sudol, M. The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J. 14, 231-241 (2000). (Pubitemid 30086060)
51. Stuart, D.I., Levine, M., Muirhead, H. & Stammers, D.K. Crystal structure of cat muscle pyruvate kinase at a resolution of 2.6Å. J. Mol. Biol. 134, 109-142 (1979).
52. Walter, T.S. et al. A procedure for setting up high-throughput nanolitre crystallization experiments. Crystallization workflow for initial screening, automated storage, imaging and optimization. Acta Crystallogr. D Biol. Crystallogr. 61, 651-657 (2005). (Pubitemid 43951502)
53. Axford, D. et al. In situ macromolecular crystallography using microbeams. Acta Crystallogr. D Biol. Crystallogr. (in the press).
54. Borek, D., Cymborowski, M., Machius, M., Minor, W. & Otwinowski, Z. Diffraction data analysis in the presence of radiation damage. Acta Crystallogr. D Biol. Crystallogr. 66, 426-436 (2010).
55. Brünger, A.T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921 (1998).
56. Emsley, P., Lohkamp, B., Scott, W.G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
57. Blanc, E. et al. Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr. D Biol. Crystallogr. 60, 2210-2221 (2004). (Pubitemid 41742773)
58. Laskowski, R.A., Moss, D.S. & Thornton, J.M. Main-chain bond lengths and bond angles in protein structures. J. Mol. Biol. 231, 1049-1067 (1993). (Pubitemid 23209879)