Structural analysis of coxsackievirus A7 reveals conformational: Changes associated with uncoating

Journal of Virology

Volumn 86, Issue 13, 2012, Pages 7207-7215

  Seitsonen, Jani J T ^a,e   Shakeel, Shabih ^a   Susi, Petri ^b,f   Pandurangan, Arun P ^c   Sinkovits, Robert S ^d,g   Hyvönen, Heini ^a,h   Laurinmäki, Pasi ^a   Ylä Pelto, Jani ^b,f   Topf, Maya ^c   Hyypiä, Timo ^b   Butcher, Sarah J ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF TURKU   (Finland)

^c UNIVERSITY OF LONDON   (United Kingdom)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e AALTO UNIVERSITY   (Finland)

^f TURKU UNIVERSITY OF APPLIED SCIENCES   (Finland)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h Haartmaninkatu 8   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN VP1; PROTEIN VP2; PROTEIN VP3; PROTEIN VP4;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; CONFORMATIONAL TRANSITION; COXSACKIE VIRUS A; COXSACKIE VIRUS A7; CRYOELECTRON MICROSCOPY; DNA SEQUENCE; GENE SEQUENCE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLIOMYELITIS VIRUS 1; PREDICTION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FUNCTION; RECEPTOR BINDING; RNA SYNTHESIS; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; STRAIN DIFFERENCE; STRUCTURE ANALYSIS; THREE DIMENSIONAL IMAGING; VIRAL TROPISM; VIRION; VIRUS CAPSID; VIRUS MORPHOLOGY; VIRUS STRAIN; VIRUS UNCOATING; VIRUS VIRULENCE;

CAPSID PROTEINS; CRYOELECTRON MICROSCOPY; ENTEROVIRUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; SEQUENCE ANALYSIS, DNA; VIRUS INTERNALIZATION;

COXSACKIEVIRUS; ENTEROVIRUS; HUMAN ENTEROVIRUS A; HUMAN POLIOVIRUS 1; MIRIDAE; PICORNAVIRIDAE; POLIOVIRUS;

EID: 84864123281     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.06425-11     Document Type: Article

References (93)

1. Abraham G, Colonno RJ. 1984. Many rhinovirus serotypes share the same cellular receptor. J. Virol. 51: 340-345.
2. Ang LW, et al. 2009. Epidemiology and control of hand, foot and mouth disease in Singapore, 2001-2007. Ann. Acad. Med. Singap. 38: 106-112.
3. Arita M, Koike S, Aoki J, Horie H, Nomoto A. 1998. Interaction of poliovirus with its purified receptor and conformational alteration in the virion. J. Virol. 72: 3578-3586.
4. Arnold E, Rossmann MG. 1988. The use of molecular-replacement phases for the refinement of the human rhinovirus 14 structure. Acta Crystallogr. A 44: 270-282.
5. Baker TS, Olson NH, Fuller SD. 1999. Adding the third dimension to virus life cycles: three-dimensional reconstruction of icosahedral viruses from cryo-electron micrographs. Microbiol. Mol. Biol. Rev. 63: 862-922.
6. Basavappa R, et al. 1994. Role and mechanism of the maturation cleavage of VP0 in poliovirus assembly: structure of the empty capsid assembly intermediate at 2.9 A resolution. Protein Sci. 3: 1651-1669.
7. Belnap DM, et al. 2000. Molecular tectonic model of virus structural transitions: the putative cell entry states of poliovirus. J. Virol. 74: 1342-1354.
8. Blomqvist S, Paananen A, Savolainen-Kopra C, Hovi T, Roivainen M. 2008. Eight years of experience with molecular identification of human enteroviruses. J. Clin. Microbiol. 46: 2410-2413.
9. Bostina M, Levy H, Filman DJ, Hogle JM. 2011. Poliovirus RNA is released from the capsid near a twofold symmetry axis. J. Virol. 85: 776-783.
10. Bubeck D, et al. 2005. The structure of the poliovirus 135S cell entry intermediate at 10-Å resolution reveals the location of an externalized polypeptide that binds to membranes. J. Virol. 79: 7745-7755.
11. Bubeck D, Filman DJ, Hogle JM. 2005. Cryo-electron microscopy reconstruction of a poliovirus-receptor-membrane complex. Nat. Struct. Mol. Biol. 12: 615-618.
12. Chambon M, et al. 2001. Circulation of enteroviruses and persistence of meningitis cases in the winter of 1999-2000. J. Med. Virol. 65: 340-347.
13. Chaves SS, Lobo S, Kennett M, Black J. 2001. Coxsackie virus A24 infection presenting as acute flaccid paralysis. Lancet 357: 605.
14. Chow M, et al. 1987. Myristylation of picornavirus capsid protein VP4 and its structural significance. Nature 327: 482-486.
15. Chumakov MP, et al. 1956. Isolation and investigation of the IV immunological type of poliomyelitis virus. Vopr. Virusol. 1(1): 16-19. (In Russian.)
16. Dalldorf G, Sickles GM. 1948. An unidentified, filtrable agent isolated from the feces of children with paralysis. Science 108: 61-62.
17. Dalldorf G, et al. 1949. A virus recovered from the feces of poliomyelitis patients pathogenic for suckling mice. J. Exp. Med. 89: 567-582.
18. Eswar N, et al. 2006. Comparative protein structure modeling using Modeller. Curr. Protoc. Bioinformatics Chapter 5: Unit 5.6.
19. Felsenstein J. 1989. PHYLIP - phylogeny inference package (version 3.2). Cladistics 5: 164-166.
20. Fendrick AM, Monto AS, Nightengale B, Sarnes M. 2003. The economic burden of non-influenza-related viral respiratory tract infection in the United States. Arch. Intern. Med. 163: 487-494.
21. Fernandez JJ. 2008. High performance computing in structural determination by electron cryomicroscopy. J. Struct. Biol. 164: 1-6.
22. Figueroa JP, Ashley D, King D, Hull B. 1989. An outbreak of acute flaccid paralysis in Jamaica associated with echovirus type 22. J. Med. Virol. 29: 315-319.
23. Filman DJ, Wien MW, Cunningham JA, Bergelson JM, Hogle JM. 1998. Structure determination of echovirus 1. Acta Crystallogr. D Biol. Crystallogr. 54: 1261-1272.
24. Fricks CE, Hogle JM. 1990. Cell-induced conformational change in poliovirus: externalization of the amino terminus of VP1 is responsible for liposome binding. J. Virol. 64: 1934-1945.
25. Fry EE, et al. 2003. Crystal structure of swine vesicular disease virus and implications for host adaptation. J. Virol. 77: 5475-5486.
26. Fry EE, et al. 2010. Crystal structure of equine rhinitis A virus in complex with its sialic acid receptor. J. Gen. Virol. 91: 1971-1977.
27. Garriga D, et al. 2012. Insights into minor group rhinovirus uncoating: the X-ray structure of the HRV2 empty capsid. PLoS Pathog. 8: e1002473. doi: 10.1371/journal.ppat.1002473.
28. Gear JH. 1984. Nonpolio causes of polio-like paralytic syndromes. Rev. Infect. Dis. 6(Suppl. 2): S379-S384.
29. Goodfellow IG, et al. 2005. Inhibition of coxsackie B virus infection by soluble forms of its receptors: binding affinities, altered particle formation, and competition with cellular receptors. J. Virol. 79: 12016-12024.
30. Grimwood K, et al. 2003. Acute flaccid paralysis from echovirus type 33 infection. J. Clin. Microbiol. 41: 2230-2232.
31. Grist NR. 1962. Type A7 Coxsackie (type 4 poliomyelitis) virus infection in Scotland. J. Hyg. (Lond.) 60: 323-332.
32. Grist NR, Bell EJ, Assaad F. 1978. Enteroviruses in human disease. Prog. Med. Virol. 24: 114-157.
33. Habel K, Loomis LN. 1957. Coxsackie A7 virus and the Russian poliovirus Type 4. Proc. Soc. Exp. Biol. Med. 95: 597-605.
34. Hadfield AT, et al. 1997. The refined structure of human rhinovirus 16 at 2.15Aresolution: implications for the viral life cycle. Structure 5: 427-441.
35. He Y, et al. 2000. Interaction of the poliovirus receptor with poliovirus. Proc. Natl. Acad. Sci. U. S. A. 97: 79-84.
36. He Y, et al. 2001. Interaction of coxsackievirus B3 with the full length coxsackievirus-adenovirus receptor. Nat. Struct. Biol. 8: 874-878.
37. Hendry E, et al. 1999. The crystal structure of coxsackievirus A9: new insights into the uncoating mechanisms of enteroviruses. Structure 7: 1527-1538.
38. Hewat EA, Blaas D. 2004. Cryoelectron microscopy analysis of the structural changes associated with human rhinovirus type 14 uncoating. J. Virol. 78: 2935-2942.
39. Hewat EA, Neumann E, Blaas D. 2002. The concerted conformational changes during human rhinovirus 2 uncoating. Mol. Cell 10: 317-326.
40. Ho M, et al. 1999. An epidemic of enterovirus 71 infection in Taiwan. Taiwan Enterovirus Epidemic Working Group. N. Engl. J. Med. 341: 929-935.
41. Huang CC, et al. 1999. Neurologic complications in children with enterovirus 71 infection. N. Engl. J. Med. 341: 936-942.
42. Kamitsuka PS, Lou TY, Fabiyi A, Wenner HA. 1965. Preparation and standardization of coxsackievirus reference antisera. I. For twenty-four group A viruses. Am. J. Epidemiol. 81: 283-306.
43. Kim SS, et al. 1989. Crystal structure of human rhinovirus serotype 1A (HRV1A). J. Mol. Biol. 210: 91-111.
44. Kivioja T, Ravantti J, Verkhovsky A, Ukkonen E, Bamford D. 2000. Local average intensity-based method for identifying spherical particles in electron micrographs. J. Struct. Biol. 131: 126-134.
45. Kolatkar PR, et al. 1999. Structural studies of two rhinovirus serotypes complexed with fragments of their cellular receptor. EMBO J. 18: 6249-6259.
46. Korant BD, Lonberg-Holm K, Noble J, Stasny JT. 1972. Naturally occurring and artificially produced components of three rhinoviruses. Virology 48: 71-86.
47. Krissinel E, Henrick K. 2004. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D Biol. Crystallogr. 60: 2256-2268.
48. Lee BE, Davies HD. 2007. Aseptic meningitis. Curr. Opin. Infect. Dis. 20: 272-277.
49. Levy HC, Bostina M, Filman DJ, Hogle JM. 2010. Catching a virus in the act of RNA release: a novel poliovirus uncoating intermediate characterized by cryo-electron microscopy. J. Virol. 84: 4426-4441.
50. Lin J, et al. 2011. An externalized polypeptide partitions between two distinct sites on genome-released poliovirus particles. J. Virol. 85: 9974-9983.
51. Lönnrot M, et al. 2000. Enterovirus infection as a risk factor for beta-cell autoimmunity in a prospectively observed birth cohort: the Finnish Diabetes Prediction and Prevention Study. Diabetes 49: 1314-1318.
52. Lönnrot M, et al. 2000. Enterovirus RNA in serum is a risk factor for beta-cell autoimmunity and clinical type 1 diabetes: a prospective study. Childhood Diabetes in Finland (DiMe) Study Group. J. Med. Virol. 61: 214-220.
53. Ludtke SJ, Baldwin PR, Chiu W. 1999. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128: 82-97.
54. Miller ST, Hogle JM, Filman DJ. 2001. Ab initio phasing of highsymmetry macromolecular complexes: successful phasing of authentic poliovirus data to 3.0 A resolution. J. Mol. Biol. 307: 499-512.
55. Mindell JA, Grigorieff N. 2003. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142: 334-347.
56. Muckelbauer JK, et al. 1995. Structure determination of coxsackievirus B3 to 3.5 Å resolution. Acta Crystallogr. D Biol. Crystallogr. 51: 871-887.
57. Nishimura Y, et al. 2009. Human P-selectin glycoprotein ligand-1 is a functional receptor for enterovirus 71. Nat. Med. 15: 794-797.
58. Oberste MS, et al. 1999. Typing of human enteroviruses by partial sequencing of VP1. J. Clin. Microbiol. 37: 1288-1293.
59. Oberste MS, Pallansch MA. 2003. Establishing evidence for enterovirus infection in chronic disease. Ann. N. Y. Acad. Sci. 1005: 23-31.
60. Oberste MS, Penaranda S, Maher K, Pallansch MA. 2004. Complete genome sequences of all members of the species human enterovirus A. J. Gen. Virol. 85: 1597-1607.
61. Oliveira MA, et al. 1993. The structure of human rhinovirus 16. Structure 1: 51-68.
62. Pandurangan AP, Topf M. 2012. Finding rigid bodies in protein structures: application to flexible fitting into cryoEM maps. J. Struct. Biol. 177: 520-531.
63. Pettersen EF, et al. 2004. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25: 1605-1612.
64. Plevka P, Perera R, Cardosa J, Kuhn RJ, Rossmann MG. 1 March 2012, posting date. Crystal structure of human enterovirus 71. Science. doi: 10.1126/science.1218713.
65. Pulli T, Koskimies P, Hyypiä T. 1995. Molecular comparison of coxsackie A virus serotypes. Virology 212: 30-38.
66. Richter FA, Rhodes AJ, Macpherson LW, Labzoffsky NA. 1971. A possible new enterovirus serotype isolated in Ontario. Arch. Gesamte Virusforsch. 35: 218-222.
67. Rosenthal PB, Henderson R. 2003. Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. J. Mol. Biol. 333: 721-745.
68. Roy A, Kucukural A, Zhang Y. 2010. I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 5: 725-738.
69. Salminen K, et al. 2003. Enterovirus infections are associated with the induction of beta-cell autoimmunity in a prospective birth cohort study. J. Med. Virol. 69: 91-98.
70. Seitsonen JJ, Susi P, Lemmetty A, Butcher SJ. 2008. Structure of the mite-transmitted Blackcurrant reversion nepovirus using electron cryomicroscopy. Virology 378: 162-168.
71. Shepherd CM, et al. 2006. VIPERdb: a relational database for structural virology. Nucleic Acids Res. 34: D386-D389.
72. Smyth M, et al. 1995. Implications for viral uncoating from the structure of bovine enterovirus. Nat. Struct. Biol. 2: 224-231.
73. Stanway G, et al. 2005. Family Picornaviridae, p 757-778. In Fauquet C, Mayo MA, Maniloff J, Desselberger U, Ball LA (ed), Virus taxonomy. VIIIth Report of the International Committee on Taxonomy of Viruses. Elsevier, London, United Kingdom.
74. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
75. Topf M, et al. 2008. Protein structure fitting and refinement guided by cryo-EM density. Structure 16: 295-307.
76. Tuthill TJ, et al. 2009. Equine rhinitis A virus and its low pH empty particle: clues towards an aphthovirus entry mechanism? PLoS Pathog. 5: e1000620. doi: 10.1371/journal.ppat.1000620.
77. van Heel M, Harauz G. 1986. Resolution criteria for three dimensional reconstruction. Optik 73: 119-122.
78. Venkataraman S, et al. 2008. Crystallization and preliminary X-ray diffraction studies of Seneca Valley virus-001, a new member of the Picornaviridae family. Acta Crystallogr. F Struct. Biol. Cryst. Commun. 64: 293-296.
79. Voroshilova MK, Chumakov MP. 1959. Poliomyelitis-like properties of AB-IV-coxsackie A7 group of viruses. Prog. Med. Virol. 2: 106-170.
80. Vuorinen T, Vainionpaa R, Hyypiä T. 2003. Five years' experience of reverse-transcriptase polymerase chain reaction in daily diagnosis of enterovirus and rhinovirus infections. Clin. Infect. Dis. 37: 452-455.
81. Wang X, et al. 2012. A sensor-adaptor mechanism for enterovirus uncoating from structures of EV71. Nat. Struct. Mol. Biology. 19: 424-429.
82. Wien MW, Curry S, Filman DJ, Hogle JM. 1997. Structural studies of poliovirus mutants that overcome receptor defects. Nat. Struct. Biol. 4: 666-674.
83. Winn MD, et al. 2011. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67: 235-242.
84. Xiao C, et al. 2005. The crystal structure of coxsackievirus A21 and its interaction with ICAM-1. Structure 13: 1019-1033.
85. Xing L, Casasnovas JM, Cheng RH. 2003. Structural analysis of human rhinovirus complexed with ICAM-1 reveals the dynamics of receptormediated virus uncoating. J. Virol. 77: 6101-6107.
86. Yamada K, et al. 2002. Crystal structure of the RuvA-RuvB complex: a structural basis for the Holliday junction migrating motor machinery. Mol. Cell 10: 671-681.
87. Yamayoshi S, et al. 2009. Scavenger receptor B2 is a cellular receptor for enterovirus 71. Nat. Med. 15: 798-801.
88. Yan X, Dryden KA, Tang J, Baker TS. 2007. Ab initio random model method facilitates 3D reconstruction of icosahedral particles. J. Struct. Biol. 157: 211-225.
89. Yan X, Sinkovits RS, Baker TS. 2007. AUTO3DEM-an automated and high throughput program for image reconstruction of icosahedral particles. J. Struct. Biol. 157: 73-82.
90. Yang B, Chuang H, Yang KD. 2009. Sialylated glycans as receptor and inhibitor of enterovirus 71 infection to DLD-1 intestinal cells. Virol. J. 6: 141.
91. Zhang Y. 2007. Template-based modeling and free modeling by ITASSER in CASP7. Proteins 69: 108-117.
92. Zhang Y, et al. 2009. An outbreak of hand, foot, and mouth disease associated with subgenotype C4 of human enterovirus 71 in Shandong, China. J. Clin. Virol. 44: 262-267.
93. Zhao R, et al. 1996. Human rhinovirus 3 at 3.0 A resolution. Structure 4: 1205-1220.