Atomic model of CPV reveals the mechanism used by this single-shelled virus to economically carry out functions conserved in multishelled reoviruses

Structure

Volumn 19, Issue 5, 2011, Pages 652-661

  Yu, Xuekui ^a   Ge, Peng ^a   Jiang, Jiansen ^a   Atanasov, Ivo ^a   Zhou, Z Hong ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN CSP A; PROTEIN CSP B; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; CRYOELECTRON MICROSCOPY; ECONOMIC ASPECT; GENETIC CONSERVATION; NONHUMAN; POLYHEDROSIS VIRUS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STRUCTURE; REOVIRUS; VIRUS CAPSID;

AMINO ACID SEQUENCE; CAPSID; CAPSID PROTEINS; CRYOELECTRON MICROSCOPY; EVOLUTION, MOLECULAR; IMAGE PROCESSING, COMPUTER-ASSISTED; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN STABILITY; REOVIRIDAE; REOVIRIDAE INFECTIONS; RNA, VIRAL;

CYPOVIRUS; MIRIDAE; ORTHOREOVIRUS; REOVIRIDAE;

EID: 79955867558     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2011.03.003     Document Type: Article

References (37)

1. A.T. Brunger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, R.W. Grosse-Kunstleve, J.S. Jiang, J. Kuszewski, M. Nilges, and N.S. Pannu Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallogr. D Biol. Crystallogr. 54 1998 905 921
2. J. Chen, J. Sun, I. Atanasov, S. Ryazantsev, and Z.H. Zhou Electron tomography reveals polyhedrin binding ane existence of both empty and full cytoplamic polyhedrosis virus particles inside infectious polyhedra J. Virol. 85 2011 10.1128/JVI.00103-11 in press. Published online April 6, 2011
3. L. Cheng, J. Zhu, W.H. Hui, X. Zhang, B. Honig, Q. Fang, and Z.H. Zhou Backbone model of an aquareovirus virion by cryo-electron microscopy and bioinformatics J. Mol. Biol. 397 2010 852 863
4. K.A. Dryden, G.J. Wang, M. Yeager, M.L. Nibert, K.M. Coombs, D.B. Furlong, B.N. Fields, and T.S. Baker Early steps in reovirus infection are associated with dramatic changes in supramolecular structure and protein conformations J. Cell Biol. 122 1993 1023 1041
5. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132 (Pubitemid 41742764)
6. J.M. Grimes, J.N. Burroughs, P. Gouet, J.M. Diprose, R. Malby, S. Zientara, P.P.C. Mertens, and D.I. Stuart The atomic structure of the bluetongue virus core Nature 395 1998 470 478 (Pubitemid 28462435)
7. K. Hagiwara, and T. Matsumoto Nucleotide sequences of genome segments 6 and 7 of Bombyx mori cypovirus 1, encoding the viral structural proteins V4 and V5, respectively J. Gen. Virol. 81 2000 1143 1147 (Pubitemid 30189657)
8. K. Hagiwara, and H. Naitow Assembly into single-shelled virus-like particles by major capsid protein VP1 encoded by genome segment S1 of Bombyx mori cypovirus 1 J. Gen. Virol. 84 2003 2439 2441 (Pubitemid 37063133)
9. C.L. Hill, T.F. Booth, B.V. Prasad, J.M. Grimes, P.P. Mertens, G.C. Sutton, and D.I. Stuart The structure of a cypovirus and the functional organization of dsRNA viruses Nat. Struct. Biol. 6 1999 565 568 (Pubitemid 29252838)
10. H. Ijiri, F. Coulibaly, G. Nishimura, D. Nakai, E. Chiu, C. Takenaka, K. Ikeda, H. Nakazawa, N. Hamada, and E. Kotani Structure-based targeting of bioactive proteins into cypovirus polyhedra and application to immobilized cytokines for mammalian cell culture Biomaterials 30 2009 4297 4308
11. K. Ikeda, H. Nakazawa, A. Shimo-Oka, K. Ishio, S. Miyata, Y. Hosokawa, S. Matsumura, H. Masuhara, S. Belloncik, and R. Alain Immobilization of diverse foreign proteins in viral polyhedra and potential application for protein microarrays Proteomics 6 2006 54 66 (Pubitemid 43142933)
12. P.J. Kraulis MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures J. Appl. Crystallogr. 24 1991 946 950
13. J.A. Lawton, M.K. Estes, and B.V. Prasad Three-dimensional visualization of mRNA release from actively transcribing rotavirus particles Nat. Struct. Biol. 4 1997 118 121 (Pubitemid 27066386)
14. J.A. Lawton, M.K. Estes, and B.V. Prasad Mechanism of genome transcription in segmented dsRNA viruses Adv. Virus Res. 55 2000 185 229
15. Y. Li, and Y. Zhang REMO: a new protocol to refine full atomic protein models from C-alpha traces by optimizing hydrogen-bonding networks Proteins 76 2009 665 676
16. Y. Liang, E.Y. Ke, and Z.H. Zhou IMIRS: a high-resolution 3D reconstruction package integrated with a relational image database J. Struct. Biol. 137 2002 292 304 (Pubitemid 35304474)
17. H. Liu, L. Cheng, S. Zeng, C. Cai, Z.H. Zhou, and Q. Yang Symmetry-adapted spherical harmonics method for high-resolution 3D single-particle reconstructions J. Struct. Biol. 161 2008 64 73 (Pubitemid 350298264)
18. S.J. Ludtke, P.R. Baldwin, and W. Chiu EMAN: semi-automated software for high resolution single particle reconstructions J. Struct. Biol. 128 1999 82 97
19. B. McClain, E. Settembre, B.R. Temple, A.R. Bellamy, and S.C. Harrison X-ray crystal structure of the rotavirus inner capsid particle at 3.8 A resolution J. Mol. Biol. 397 2010 587 599
20. P.P.C. Mertens, M. Arella, H. Attoui, S. Belloncik, M. Bergoin, G. Boccardo, T.F. Booth, W. Chiu, J.M. Diprose, and R. Duncan Family Reoviridae M.H.V. van Regenmortel, C.M. Fauguet, D.H.L. Bishop, E.B. Carstens, M.K. Estes, S.M. Lemon, J. Maniloff, M.A. Mayo, D.J. McGeoch, C.R. Pringle, R.B. Wickner, Virus Taxonomy 2000 Academic Press San Diego, CA 395 480
21. P.P.C. Mertens, S. Rao, and Z.H. Zhou Cypovirus, Reoviridae C.M. Fauquet, M.A. Mayo, J. Maniloff, U. Desselberger, L.A. Ball, Virus Taxonomy, VIIIth Report of the ICTV 2004 Elsevier/Academic Press London 522 533
22. J.A. Mindell, and N. Grigorieff Accurate determination of local defocus and specimen tilt in electron microscopy J. Struct. Biol. 142 2003 334 347 (Pubitemid 36638267)
23. H. Mori, C. Shukunami, A. Furuyama, H. Notsu, Y. Nishizaki, and Y. Hiraki Immobilization of bioactive fibroblast growth factor-2 into cubic proteinous microcrystals (Bombyx mori cypovirus polyhedra) that are insoluble in a physiological cellular environment J. Biol. Chem. 282 2007 17289 17296 (Pubitemid 47093237)
24. C.C. Payne, and K.A. Harrap Cytoplasmic polyhedrosis viruses K. Maramorosch, The Atlas of Insect and Plant Viruses 1977 Academic Press New York 105 129
25. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and T.E. Ferrin UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
26. B.V.V. Prasad, J.W. Burns, E. Marietta, M.K. Estes, and W. Chiu Localization of VP4 neutralization sites in rotavirus by three-dimensional cryo-electron microscopy Nature 343 1990 476 479
27. K.M. Reinisch, M.L. Nibert, and S.C. Harrison Structure of the reovirus core at 3.6 resolution Nature 404 2000 960 967 (Pubitemid 30243583)
28. P.B. Rosenthal, and R. Henderson Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy J. Mol. Biol. 333 2003 721 745 (Pubitemid 37268015)
29. X. Yu, L. Jin, and Z.H. Zhou 3.88 structure of cytoplasmic polyhedrosis virus by cryo-electron microscopy Nature 453 2008 415 419 (Pubitemid 351693126)
30. H. Zhang, J. Zhang, X. Yu, X. Lu, Q. Zhang, J. Jakana, D.H. Chen, X. Zhang, and Z.H. Zhou Visualization of protein-RNA interactions in cytoplasmic polyhedrosis virus J. Virol. 73 1999 1624 1629 (Pubitemid 29036819)
31. H. Zhang, X.K. Yu, X.Y. Lu, J.Q. Zhang, and Z.H. Zhou Molecular interactions and viral stability revealed by structural analyses of chemically treated cypovirus capsids Virology 298 2002 45 52 (Pubitemid 34734878)
32. X. Zhang, S.B. Walker, P.R. Chipman, M.L. Nibert, and T.S. Baker Reovirus polymerase lambda 3 localized by cryo-electron microscopy of virions at a resolution of 7.6 A Nat. Struct. Biol. 10 2003 1011 1018 (Pubitemid 37500493)
33. X. Zhang, E. Settembre, C. Xu, P.R. Dormitzer, R. Bellamy, S.C. Harrison, and N. Grigorieff Near-atomic resolution using electron cryomicroscopy and single-particle reconstruction Proc. Natl. Acad. Sci. USA 105 2008 1867 1872 (Pubitemid 351439431)
34. X. Zhang, L. Jin, Q. Fang, W.H. Hui, and Z.H. Zhou 3.3 A cryo-EM structure of a nonenveloped virus reveals a priming mechanism for cell entry Cell 141 2010 472 482
35. Z.H. Zhou Cypovirus J.T. Patton, Segmented Double-Stranded RNA Viruses: Structure and Molecular Biology 2008 Caister Academic Press Norfolk, UK 27 43
36. Z.H. Zhou, M.L. Baker, W. Jiang, M. Dougherty, J. Jakana, G. Dong, G. Lu, and W. Chiu Electron cryomicroscopy and bioinformatics suggest protein fold models for rice dwarf virus Nat. Struct. Biol. 8 2001 868 873 (Pubitemid 32923606)
37. Z.H. Zhou, H. Zhang, J. Jakana, X.Y. Lu, and J.-Q. Zhang Cytoplasmic polyhedrosis virus structure at 8 by electron cryomicroscopy: structural basis of capsid stability and mRNA processing regulation Structure 11 2003 651 663 (Pubitemid 37281181)