Crystal structures of enterovirus 71 (EV71) recombinant virus particles provide insights into vaccine design

Journal of Biological Chemistry

Volumn 290, Issue 6, 2015, Pages 3198-3208

  Lyu, Ke ^a   Wang, Guang Chuan ^b,c   He, Ya Ling ^a   Han, Jian Feng ^b   Ye, Qing ^b   Qin, Cheng Feng ^b   Chen, Rong ^a  

^a INSTITUTE PASTEUR OF SHANGHAI   (China)

^b BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^c ZHEJIANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

PEPTIDES; VACCINES;

ENTEROVIRUS 71; PARTICLE SURFACE; VACCINE DEVELOPMENT; VIRUS PARTICLES;

VIRUSES;

VIRUS VACCINE; VIRUS LIKE PARTICLE VACCINE;

AMINO TERMINAL SEQUENCE; ARTICLE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DRUG DESIGN; ENTEROVIRUS 71; EXPOSURE; NONHUMAN; VIRUS CAPSID; VIRUS PARTICLE; VIRUS RECOMBINANT; VIRUS STRAIN; VIRUS UNCOATING; AMINO ACID SEQUENCE; CHEMISTRY; ENTEROVIRUS A; GENETICS; IMMUNOLOGY; MOLECULAR GENETICS; ULTRASTRUCTURE; X RAY CRYSTALLOGRAPHY;

HUMAN ENTEROVIRUS 71; MIRIDAE;

AMINO ACID SEQUENCE; CAPSID; CRYSTALLOGRAPHY, X-RAY; ENTEROVIRUS A, HUMAN; MOLECULAR SEQUENCE DATA; VACCINES, VIRUS-LIKE PARTICLE;

EID: 84922358434     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.624536     Document Type: Article

References (38)

1. McMinn, P. C. (2012) Recent advances in the molecular epidemiology and control of human enterovirus 71 infection. Curr. Opin. Virol. 2, 199-205.
2. Wang, G., Cao, R. Y., Chen, R., Mo, L., Han, J. F., Wang, X., Xu, X., Jiang, T., Deng, Y. Q., Lyu, K., Zhu, S. Y., Qin, E. D., Tang, R., and Qin, C. F. (2013) Rational design of thermostable vaccines by engineered peptideinduced virus self-biomineralization under physiological conditions. Proc. Natl. Acad. Sci. U.S.A. 110, 7619-7624.
3. Martin, A., Wychowski, C., Couderc, T., Crainic, R., Hogle, J., and Girard, M. (1988) Engineering a poliovirus type 2 antigenic site on a type 1 capsid results in a chimaeric virus which is neurovirulent for mice. EMBO J. 7, 2839-2847.
4. Murray, M. G., Kuhn, R. J., Arita, M., Kawamura, N., Nomoto, A., and Wimmer, E. (1988) Poliovirus type 1/type 3 antigenic hybrid virus constructed in vitro elicits type 1 and type 3 neutralizing antibodies in rabbits and monkeys. Proc. Natl. Acad. Sci. U.S.A. 85, 3203-3207.
5. Evans, D. J., McKeating, J., Meredith, J. M., Burke, K. L., Katrak, K., John, A., Ferguson, M., Minor, P. D., Weiss, R. A., and Almond, J. W. (1989) An engineered poliovirus chimaera elicits broadly reactive HIV-1 neutralizing antibodies. Nature 339, 385-388, 340.
6. Yeates, T. O., Jacobson, D. H., Martin, A., Wychowski, C., Girard, M., Filman, D. J., and Hogle, J. M. (1991) Three-dimensional structure of a mouse-adapted type 2/type 1 poliovirus chimera. EMBO J. 10, 2331-2341.
7. Ding, J., Smith, A. D., Geisler, S. C., Ma, X., Arnold, G. F., and Arnold, E. (2002) Crystal structure of a human rhinovirus that displays part of the HIV-1 V3 loop and induces neutralizing antibodies against HIV-1. Structure 10, 999-1011.
8. Lin, T., Porta, C., Lomonossoff, G., and Johnson, J. E. (1996) Structurebased design of peptide presentation on a viral surface: The crystal structure of a plant/animal virus chimera at 2.8 Å resolution. Fold Des. 1, 179-187.
9. Basavappa, R., Syed, R., Flore, O., Icenogle, J. P., Filman, D. J., and Hogle, J. M. (1994) Role and mechanism of the maturation cleavage of VP0 in poliovirus assembly: structure of the empty capsid assembly intermediate at 2.9 Å resolution. Protein Sci. 3, 1651-1669.
10. Ansardi, D. C., and Morrow, C. D. (1995) Amino acid substitutions in the poliovirus maturation cleavage site affect assembly and result in accumulation of provirions. J. Virol. 69, 1540-1547.
11. Jacobson, M. F., and Baltimore, D. (1968) Morphogenesis of poliovirus. I. Association of the viral RNA with coat protein. J. Mol. Biol. 33, 369-378.
12. Guttman, N., and Baltimore, D. (1977) Morphogenesis of poliovirus. IV. existence of particles sedimenting at 150S and having the properties of provirion. J. Virol. 23, 363-367.
13. Marongiu, M. E., Pani, A., Corrias, M. V., Sau, M., and La Colla, P. (1981) Poliovirus morphogenesis. I. Identification of 80S dissociable particles and evidence for the artifactual production of procapsids. J. Virol. 39, 341-347.
14. Le Bouvier, G. L. (1955) The modification of poliovirus antigens by heat and ultraviolet light. Lancet 269, 1013-1016.
15. Blondel, B., Akacem, O., Crainic, R., Couillin, P., and Horodniceanu, F. (1983) Detection by monoclonal antibodies of an antigenic determinant critical for poliovirus neutralization present on VP1 and on heat-inactivated virions. Virology 126, 707-710.
16. Liu, C. C., Guo, M. S., Lin, F. H., Hsiao, K. N., Chang, K. H., Chou, A. H., Wang, Y. C., Chen, Y. C., Yang, C. S., and Chong, P. C. (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.
17. Wang, X., Peng, W., Ren, J., Hu, Z., Xu, J., Lou, Z., Li, X., Yin, W., Shen, X., Porta, C., Walter, T. S., Evans, G., Axford, D., Owen, R., Rowlands, D. J., Wang, J., Stuart, D. I., Fry, E. E., and Rao, Z. (2012) A sensor-adaptor mechanism for enterovirus uncoating from structures of EV71. Nat. Struct. Mol. Biol. 19, 424-429.
18. Plevka, P., Perera, R., Cardosa, J., Kuhn, R. J., and Rossmann, M. G. (2012) Crystal structure of human enterovirus 71. Science 336, 1274.
19. Cifuente, J. O., Lee, H., Yoder, J. D., Shingler, K. L., Carnegie, M. S., Yoder, J. L., Ashley, R. E., Makhov, A. M., Conway, J. F., and Hafenstein, S. (2013) Structures of the procapsid and mature virion of enterovirus 71 strain 1095. J. Virol. 87, 7637-7645.
20. Lyu, K., Ding, J., Han, J. F., Zhang, Y., Wu, X. Y., He, Y. L., Qin, C. F., and Chen, R. (2014) Human enterovirus 71 uncoating captured at atomic resolution. J. Virol. 88, 3114-3126.
21. Shingler, K. L., Yoder, J. L., Carnegie, M. S., Ashley, R. E., Makhov, A. M., Conway, J. F., and Hafenstein, S. (2013) The enterovirus 71 A-particle forms a gateway to allow genome release: A cryoEM study of picornavirus uncoating. PLoS Pathog. 9, e1003240.
22. Liu, C. C., Chou, A. H., Lien, S. P., Lin, H. Y., Liu, S. J., Chang, J. Y., Guo, M. S., Chow, Y. H., Yang, W. S., Chang, K. H., Sia, C., and Chong, P. (2011) Identification and characterization of a cross-neutralization epitope of enterovirus 71. Vaccine 29, 4362-4372.
23. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326.
24. Tong, L., and Rossmann, M. G. (1997) Rotation function calculations with GLRF program. Methods Enzymol. 276, 594-611.
25. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., Mc- Coy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221.
26. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501.
27. DeLano, W. L. (2010) The PyMOL Molecular Graphics System, version 1.3r1, Schrodinger, LLC, New York.
28. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612.
29. Foo, D. G., Ang, R. X., Alonso, S., Chow, V. T., Quak, S. H., and Poh, C. L. (2008) Identification of immunodominant VP1 linear epitope of enterovirus 71 (EV71) using synthetic peptides for detecting human anti-EV71 IgG antibodies in Western blots. Clin. Microbiol. Infect. 14, 286-288.
30. Roy, M. D., Stanley, S. K., Amis, E. J., and Becker, M. L. (2008) Identification of a highly specific hydroxyapatite-binding peptide using phage display. Adv. Mater. 20, 1830-1836.
31. Foo, D. G., Alonso, S., Phoon, M. C., Ramachandran, N. P., Chow, V. T., and Poh, C. L. (2007) Identification of neutralizing linear epitopes from the VP1 capsid protein of Enterovirus 71 using synthetic peptides. Virus Res. 125, 61-68.
32. Kelley, L. A., and Sternberg, M. J. (2009) Protein structure prediction on the web: A case study using the Phyre server. Nat. Protoc. 4, 363-371.
33. Fricks, C. E., Icenogle, J. P., and Hogle, J. M. (1985) Trypsin sensitivity of the Sabin strain of type 1 poliovirus: cleavage sites in virions and related particles. J. Virol. 54, 856-859.
34. Burke, K. L., Dunn, G., Ferguson, M., Minor, P. D., and Almond, J. W. (1988) Antigen chimaeras of poliovirus as potential new vaccines. Nature 332, 81-82.
35. Jenkins, O., Cason, J., Burke, K. L., Lunney, D., Gillen, A., Patel, D., McCance, D. J., and Almond, J. W. (1990) An antigen chimera of poliovirus induces antibodies against human papillomavirus type 16. J. Virol. 64, 1201-1206.
36. Colbère-Garapin, F., Christodoulou, C., Crainic, R., Garapin, A. C., and Candrea, A. (1988) Addition of a foreign oligopeptide to the major capsid protein of poliovirus. Proc. Natl. Acad. Sci. U.S.A. 85, 8668-8672.
37. Murdin, A. D., and Wimmer, E. (1989) Construction of a poliovirus type 1/type 2 antigenic hybrid by manipulation of neutralization antigenic site II. J. Virol. 63, 5251-5257.
38. Nugent, C. I., and Kirkegaard, K. (1995) RNA binding properties of poliovirus subviral particles. J. Virol. 69, 13-22.