The Enterovirus 71 A-particle Forms a Gateway to Allow Genome Release: A CryoEM Study of Picornavirus Uncoating

PLoS Pathogens

Volumn 9, Issue 3, 2013, Pages

  Shingler, Kristin L ^a   Yoder, Jennifer L ^a   Carnegie, Michael S ^a   Ashley, Robert E ^a   Makhov, Alexander M ^b   Conway, James F ^b   Hafenstein, Susan ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN VP1; VIRUS RNA;

ARTICLE; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; ENDOCYTOSIS; ENTEROVIRUS 71; HUMAN; HUMAN CELL; NONHUMAN; PICORNAVIRUS; SURFACE CHARGE; TRANSMISSION ELECTRON MICROSCOPY; VIRUS CAPSID; VIRUS GENOME; VIRUS PURIFICATION;

CAPSID; CAPSID PROTEINS; CRYOELECTRON MICROSCOPY; ENDOCYTOSIS; ENTEROVIRUS A, HUMAN; ENTEROVIRUS INFECTIONS; GENOME, VIRAL; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; PROTEIN BINDING; RECEPTORS, CELL SURFACE; RNA, VIRAL; VIRION; VIRUS UNCOATING;

HUMAN ENTEROVIRUS 71; MIRIDAE; PICORNAVIRIDAE;

EID: 84875993737     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003240     Document Type: Article

References (52)

1. Chan LG, Parashar UD, Lye MS, Ong FG, Zaki SR, et al. (2000) Deaths of children during an outbreak of hand, foot, and mouth disease in sarawak, malaysia: clinical and pathological characteristics of the disease. For the Outbreak Study Group. Clin Infect Dis 31: 678-683.
2. Schmidt NJ, Lennette EH, Ho HH, (1974) An apparently new enterovirus isolated from patients with disease of the central nervous system. J Infect Dis 129: 304-309.
3. Brown BA, Pallansch MA, (1995) Complete nucleotide sequence of enterovirus 71 is distinct from poliovirus. Virus Res 39: 195-205.
4. Alexander JP Jr, Baden L, Pallansch MA, Anderson LJ, (1994) Enterovirus 71 infections and neurologic disease-United States, 1977-1991. J Infect Dis 169: 905-908.
5. McMinn PC, (2002) An overview of the evolution of enterovirus 71 and its clinical and public health significance. FEMS Microbiol Rev 26: 91-107.
6. Rossmann MG, Arnold E, Erickson JW, Frankenberger EA, Griffith JP, et al. (1985) Structure of a human common cold virus and functional relationship to other picornaviruses. Nature (London) 317: 145-153.
7. Hogle JM, Chow M, Filman DJ, (1985) Three-dimensional structure of poliovirus at 2.9 Å resolution. Science 229: 1358-1365.
8. Stuart AD, McKee TA, Williams PA, Harley C, Shen S, et al. (2002) Determination of the structure of a decay accelerating factor-binding clinical isolate of echovirus 11 allows mapping of mutants with altered receptor requirements for infection. J Virol 76: 7694-7704.
9. Belnap DM, Filman DJ, Trus BL, Cheng N, Booy FP, et al. (2000) Molecular tectonic model of virus structural transitions: the putative cell entry states of poliovirus. J Virol 74: 1342-1354.
10. Huang Y, Hogle JM, Chow M, (2000) Is the 135S poliovirus particle an intermediate during cell entry? J Virol 74: 8757-8761.
11. Tuthill TJ, Bubeck D, Rowlands DJ, Hogle JM, (2006) Characterization of early steps in the poliovirus infection process: receptor-decorated liposomes induce conversion of the virus to membrane-anchored entry-intermediate particles. J Virol 80: 172-180.
12. Garriga D, Pickl-Herk A, Luque D, Wruss J, Caston JR, et al. (2012) Insights into minor group rhinovirus uncoating: the X-ray structure of the HRV2 empty capsid. PLoS Pathog 8: e1002473 Epub 2012 Jan 5.
13. Watanabe Y, Watanabe K, Katagiri S, Hinuma Y, (1965) Virus-specific proteins produced in HeLa cells infected with poliovirus: characterization of subunit-like protein. J Biochem 57: 733-741.
14. Phillips BA, Fennell R, (1973) Polypeptide composition of poliovirions, naturally occurring empty capsids, and 14S precursor particles. J Virol 12: 291-299.
15. Jacobson MF, Baltimore D, (1968) Morphogenesis of poliovirus. I. Association of the viral RNA with coat protein. J Mol Biol 33: 369-378.
16. Phillips BA, Summers DF, Maizel JV Jr, (1968) In vitro assembly of poliovirus-related particles. Virology 35: 216-226.
17. Jacobson MF, Asso J, Baltimore D, (1970) Further evidence on the formation of poliovirus proteins. J Mol Biol 49: 657-669.
18. Oppermann H, Koch G, (1973) Kinetics of poliovirus replication in HeLa cells infected by isolated RNA. Biochem Biophys Res Commun 52: 635-640.
19. Ghendon Y, Yakobson E, Mikhejeva A, (1972) Study of some stages of poliovirus morphogenesis in MiO cells. J Virol 10: 261-266.
20. Basavappa R, Syed R, Flore O, Icenogle JP, Filman DJ, 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.
21. Curry S, Fry E, Blakemore W, Abu-Ghazaleh R, Jackson T, et al. (1997) 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.
22. Liu CC, Guo MS, Lin FH, Hsiao KN, Chang KH, et al. (2011) Purification and characterization of enterovirus 71 viral particles produced from vero cells grown in a serum-free microcarrier bioreactor system. PLoS One 6: e20005.
23. Holland JJ, Kiehn ED, (1968) Specific cleavage of viral proteins as steps in the synthesis and maturation of enteroviruses. Proc Natl Acad Sci U S A 60: 1015-1022.
24. Ansardi DC, Morrow CD, (1995) Amino acid substitutions in the poliovirus maturation cleavage site affect assembly and result in accumulation of provirions. J Virol 69: 1540-1547.
25. Rossmann MG, He Y, Kuhn RJ, (2002) Picornavirus-receptor interactions. Trends Microbiol 10: 324-331.
26. Zhang P, Mueller S, Morais MC, Bator CM, Bowman VD, et al. (2008) Crystal structure of CD155 and electron microscopic studies of its complexes with polioviruses. Proc Natl Acad Sci U S A 105: 18284-18289.
27. Hadfield AT, Diana GD, Rossmann MG, (1999) Analysis of three structurally related antiviral compounds in complex with human rhinovirus 16. Proc Natl Acad Sci U S A 96: 14730-14735.
28. 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.
29. Greve JM, Forte CP, Marlor CW, Meyer AM, Hoover-Litty H, et al. (1991) Mechanisms of receptor-mediated rhinovirus neutralization defined by two soluble forms of ICAM-1. J Virol 65: 6015-6023.
30. Wang X, Peng W, Ren J, Hu Z, Xu J, et al. (2012) A sensor-adaptor mechanism for enterovirus uncoating from structures of EV71. Nat Struct Mol Biol 19: 424-429 doi:410.1038/nsmb.2255.
31. Plevka P, Perera R, Cardosa J, Kuhn RJ, Rossmann MG, (2012) Crystal structure of human enterovirus 71. Science 336: 1274.
32. Yang SL, Chou YT, Wu CN, Ho MS, (2011) Annexin II binds to capsid protein VP1 of enterovirus 71 and enhances viral infectivity. J Virol 85: 11809-11820.
33. Nishimura Y, Shimojima M, Tano Y, Miyamura T, Wakita T, et al. (2009) Human P-selectin glycoprotein ligand-1 is a functional receptor for enterovirus 71. Nat Med 15: 794-797.
34. Yamayoshi S, Yamashita Y, Li J, Hanagata N, Minowa T, et al. (2009) Scavenger receptor B2 is a cellular receptor for enterovirus 71. Nat Med 15: 798-801.
35. Tan CW, Poh CL, Sam IC, Chan YF, (2012) Enterovirus 71 uses cell surface heparan sulfate glycosaminoglycan as an attachment receptor. J Virol 24: 24.
36. 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.
37. Su PY, Liu YT, Chang HY, Huang SW, Wang YF, et al. (2012) Cell surface sialylation affects binding of enterovirus 71 to rhabdomyosarcoma and neuroblastoma cells. BMC Microbiol 12: 162.
38. Yamayoshi S, Koike S, (2011) Identification of a human SCARB2 region that is important for enterovirus 71 binding and infection. J Virol 85: 4937-4946.
39. Curry S, Chow M, Hogle JM, (1996) The poliovirus 135S particle is infectious. J Virol 70: 7125-7131.
40. Yoder JD, Cifuente JO, Pan J, Bergelson JM, Hafenstein S, (2012) The crystal structure of a coxsackievirus B3-RD variant, and a refined 9A cryoEM reconstruction of the virus complexed with decay accelerating factor (DAF), provide a new footprint of DAF onto the virus surface. J Virol 12: 12.
41. Bilek G, Matscheko NM, Pickl-Herk A, Weiss VU, Subirats X, et al. (2011) Liposomal Nanocontainers as Models for Viral Infection: Monitoring Viral Genomic RNA Transfer through Lipid Membranes. J Virol 85: 8368-8375.
42. Danthi P, Tosteson M, Li QH, Chow M, (2003) Genome delivery and ion channel properties are altered in VP4 mutants of poliovirus. J Virol 77: 5266-5274.
43. Bubeck D, Filman DJ, Hogle JM, (2005) Cryo-electron microscopy reconstruction of a poliovirus-receptor-membrane complex. Nat Struct Mol Biol 12: 615-618.
44. Lin J, Cheng N, Chow M, Filman DJ, Steven AC, et al. (2011) An externalized polypeptide partitions between two distinct sites on genome-released poliovirus particles. J Virol 85: 9974-9983.
45. 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.
46. Li Q, Yafal AG, Lee YM, Hogle J, Chow M, (1994) Poliovirus neutralization by antibodies to internal epitopes of VP4 and VP1 results from reversible exposure of these sequences at physiological temperature. J Virol 68: 3965-3970.
47. Lewis JK, Bothner B, Smith TJ, Siuzdak G, (1998) Antiviral agent blocks breathing of the common cold virus. Proc Natl Acad Sci U S A 95: 6774-6778.
48. Verdino P, Witherden DA, Havran WL, Wilson IA, (2010) The molecular interaction of CAR and JAML recruits the central cell signal transducer PI3K. Science 329: 1210-1214.
49. Tang G, Peng L, Baldwin PR, Mann DS, Jiang W, et al. (2006) EMAN2: An extensible image processing suite for electron microscopy. J Struct Biol 157: 38-46.
50. 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.
51. Chacon P, Wriggers W, (2002) Multi-resolution contour-based fitting of macromolecular structures. J Mol Biol 317: 375-384.
52. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF Chimera- A Visualization System for Exploratory Research and Analysis. J Comput Chem 24: 1605-1612.