Features of reovirus outer capsid protein μ1 revealed by electron cryomicroscopy and image reconstruction of the virion at 7.0 Å resolution

Structure

Volumn 13, Issue 10, 2005, Pages 1545-1557

  Zhang, Xing ^a   Ji, Yongchang ^b   Zhang, Lan ^c   Harrison, Stephen C ^c,d   Marinescu, Dan C ^b   Nibert, Max L ^d   Baker, Timothy S ^a,e  

^a PURDUE UNIVERSITY   (United States)

^b UNIVERSITY OF CENTRAL FLORIDA   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN;

ARTICLE; CONFORMATION; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; IMAGE RECONSTRUCTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REOVIRUS; THREE DIMENSIONAL IMAGING; VIRION; X RAY;

ALGORITHMS; AMINO ACID SEQUENCE; ANIMALS; CAPSID PROTEINS; CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; FOURIER ANALYSIS; L CELLS (CELL LINE); MICE; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MYRISTIC ACID; ORTHOREOVIRUS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; SEQUENCE HOMOLOGY, AMINO ACID; VIRION;

ANIMALIA; MIRIDAE; REOVIRUS SP.;

EID: 26444511104     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2005.07.012     Document Type: Article

References (55)

1. H. Attoui, Q. Fang, F.M. Jaafar, J.F. Cantaloube, P. Biagini, P. De Micco, and X. De Lamballerie Common evolutionary origin of aquareoviruses and orthoreoviruses revealed by genome characterization of Golden shiner reovirus, Grass carp reovirus, Striped bass reovirus and golden ide reovirus (genus Aquareovirus, family Reoviridae) J. Gen. Virol. 83 2002 1941 1951
2. T.S. Baker, N.H. Olson, and S.D. Fuller Adding the third dimension to virus life cycles: three-dimensional reconstruction of icosahedral viruses from cryo-electron micrographs Microbiol. Mol. Biol. Rev. 63 1999 862 922
3. A.T. Brünger, 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
4. CCP4 (Collaborative Computational Project, Number 4) The CCP4 suite: programs for protein crystallography Acta Crystallogr. D Biol. Crystallogr. 50 1994 760 763
5. P. Chacón, and W. Wriggers Multi-resolution contour-based fitting of macromolecular structures J. Mol. Biol. 317 2002 375 384
6. K. Chandran, and M.L. Nibert Animal cell invasion by a large nonenveloped virus: reovirus delivers the goods Trends Microbiol. 11 2003 374 382
7. K. Chandran, S.B. Walker, Y. Chen, C.M. Contreras, L.A. Schiff, T.S. Baker, and M.L. Nibert In vitro recoating of reovirus cores with baculovirus-expressed outer-capsid proteins μ1 and σ3 J. Virol. 73 1999 3941 3950
8. K. Chandran, X. Zhang, N.O. Olson, S.B. Walker, J.D. Chappell, T.S. Dermody, T.S. Baker, and M.L. Nibert Complete in vitro assembly of the reovirus outer capsid produces highly infectious particles suitable for genetic studies of the receptor-binding protein J. Virol. 75 2001 5335 5342
9. K. Chandran, D.L. Farsetta, and M.L. Nibert Strategy for nonenveloped virus entry: a hydrophobic conformer of reovirus penetration protein μ1 mediates membrane disruption J. Virol. 76 2002 9920 9933
10. K. Chandran, J.S.L. Parker, M. Ehrlich, T. Kirchhausen, and M.L. Nibert The δ region of outer-capsid protein μ1 undergoes conformational change and release from reovirus particles during cell entry J. Virol. 77 2003 13361 13375
11. J.D. Chappell, A.E. Porta, T.S. Dermody, and T. Stehle Crystal structure of reovirus attachment protein σ1 reveals evolutionary relationship to adenovirus fiber EMBO J. 21 2002 1 11
12. K.A. Dryden, G. 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 conformation: analysis of virions and subviral particles by cryoelectron microscopy and image reconstruction J. Cell Biol. 122 1993 1023 1041
13. K.A. Dryden, D.L. Farsetta, G. Wang, J.M. Keegan, B.N. Fields, T.S. Baker, and M.L. Nibert Internal structures containing transcriptase-related proteins in top component particles of mammalian orthoreovirus Virology 245 1998 33 46
14. D.L. Farsetta, K. Chandran, and M.L. Nibert Transcriptional activities of reovirus RNA polymerase in recoated cores. Initiation and elongation are regulated by separate mechanisms J. Biol. Chem. 275 2000 39693 39701
15. J.C. Forrest, and T.S. Dermody Reovirus receptors and pathogenesis J. Virol. 77 2003 9109 9115
16. A. Fotin, Y. Cheng, P. Sliz, N. Grigorieff, S.C. Harrison, T. Kirchhausen, and T. Walz Molecular model for a complete clathrin lattice from electron cryomicroscopy Nature 432 2004 573 579
17. D.B. Furlong, M.L. Nibert, and B.N. Fields Sigma 1 protein of mammalian reoviruses extends from the surfaces of viral particles J. Virol. 62 1988 246 256
18. Y. Furuichi, and A.J. Shatkin Viral and cellular mRNA capping: past and prospects Adv. Virus Res. 55 2000 135 184
19. W.A. Havelka, R. Henderson, and D. Oesterhelt Three-dimensional structure of halorhodopsin at 7 Å resolution J. Mol. Biol. 247 1995 726 738
20. R. Henderson Realising the potential of electron cryomicroscopy Q. Rev. Biophys. 37 2004 3 13
21. Ji, Y., Marinescu, D.C., Zhang, W., Zhang, X., Yan, X., and Baker, T.S. (2005) A model-based parallel origin and orientation refinement algorithm for cryoTEM and its application to the study of virus structures. J. Struct. Biol., in press.
22. W. Jiang, Z. Li, Z. Zhang, M.L. Baker, P.E. Prevelige Jr., and W. Chiu Coat protein fold and maturation transition of bacteriophage P22 seen at subnanometer resolutions Nat. Struct. Biol. 10 2003 131 135
23. J. Kim, Y. Tao, K.M. Reinisch, S.C. Harrison, and M.L. Nibert Orthoreovirus and Aquareovirus core proteins: conserved enzymatic surfaces, but not protein-protein interfaces Virus Res. 101 2004 15 28
24. G.J. Kleywegt, and T.A. Jones Software for handling macromolecular envelopes Acta Crystallogr. D Biol. Crystallogr. 55 1999 941 944
25. G.J. Kleywegt, and R.J. Read Not your average density Structure 5 1997 1557 1569
26. P.W. Lee, E.C. Hayes, and W.K. Joklik Characterization of anti-reovirus immunoglobulins secreted by cloned hybridoma cell lines Virology 108 1981 134 146
27. S. Liemann, K. Chandran, T.S. Baker, M.L. Nibert, and S.C. Harrison Structure of the reovirus membrane-penetration, μ1, in a complex with its protector protein, σ3 Cell 108 2002 283 295
28. C.L. Luongo, X. Zhang, S.B. Walker, Y. Chen, T.J. Broering, D.L. Farsetta, V.D. Bowman, T.S. Baker, and M.L. Nibert Loss of activities for mRNA synthesis accompanies loss of λ2 spikes from reovirus cores: an effect of λ2 on λ1 shell structure Virology 296 2002 24 38
29. Lynch, R.E., Marinescu, D.C., Lin, H., and Baker, T.S. (1999). Parallel algorithms for 3D reconstruction of asymmetric objects from electron micrographs. 13th International Parallel Processing Symposium/10th Symposium on Parallel and Distributed Processing (San Juan, Puerto Rico), pp. 632-637.
30. D.C. Marinescu, Y. Ji, and R.E. Lynch Space-time tradeoffs for parallel 3D reconstruction algorithms for virus structure determination Concurrency and Computation. Practice & Experience 13 2001 1083 1106
31. I.I. Mendez, Y.M. She, W. Ens, and K.M. Coombs Digestion pattern of reovirus outer capsid protein σ3 determined by mass spectrometry Virology 311 2003 289 304
32. P. Metcalf, M. Cyrklaff, and M. Adrian The three-dimensional structure of reovirus obtained by cryo-electron microscopy EMBO J. 10 1991 3129 3136
33. J.K. Middleton, T.F. Severson, K. Chandran, A.L. Gillian, J. Yin, and M.L. Nibert Thermostability of reovirus disassembly intermediates (ISVPs) correlates with genetic, biochemical, and thermodynamic properties of major surface protein μ1 J. Virol. 76 2002 1051 1061
34. E.L. Nason, J.D. Wetzel, S.K. Mukherjee, E.S. Barton, B.V.V. Prasad, and T.S. Dermody A monoclonal antibody specific for reovirus outer-capsid protein σ3 inhibits σ1-mediated hemagglutination by steric hindrance J. Virol. 75 2001 6625 6634
35. Nibert, M.L. (1993). Structure and function of reovirus outer capsid proteins as they relate to early steps in infection. PhD thesis, Harvard University, Cambridge, Massachusetts.
36. M.L. Nibert, D.B. Furlong, and B.N. Fields Mechanisms of viral pathogenesis. Distinct forms of reoviruses and their roles during replication in cells and host J. Clin. Invest. 88 1991 727 734
37. M.L. Nibert, L.A. Schiff, and B.N. Fields Mammalian reoviruses contain a myristoylated structural protein J. Virol. 65 1991 1960 1967
38. M.L. Nibert, A.L. Odegard, M.A. Agosto, K. Chandran, and L.A. Schiff Putative autocleavage of reovirus μ1 protein in concert with outer-capsid disassembly and activation for membrane permeabilization J. Mol. Biol. 345 2005 461 474
39. Noad, L., Shou, J., Coombs, K.M., and Duncan, R. (2005). Sequences of avian reovirus M1, M2, and M3 genes and structural function of the encoded μ proteins. Virus, in press.
40. A.L. Odegard, K. Chandran, S. Liemann, S.C. Harrison, and M.L. Nibert Disulfide bonding among μ1 trimers in mammalian reovirus outer capsid: a late and reversible step in virion morphogenesis J. Virol. 77 2003 5389 5400
41. A.L. Odegard, K. Chandran, X. Zhang, J.S.L. Parker, T.S. Baker, and M.L. Nibert Putative autocleavage of outer capsid protein μ1, allowing release of myristoylated peptide μ1N during particle uncoating, is critical for cell entry by reovirus J. Virol. 78 2004 8732 8745
42. V.S. Reddy, P. Natarajan, B. Okerberg, K. Li, K.V. Damodaran, R.T. Morton, C.L. Brooks 3rd, and J.E. Johnson Virus Particle Explorer (VIPER), a website for virus capsid structures and their computational analyses J. Virol. 75 2001 11943 11947
43. K.M. Reinisch, M.L. Nibert, and S.C. Harrison Structure of the reovirus core at 3.6 Å resolution Nature 404 2000 960 967
44. 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
45. M.G. Rossmann, R. Bernal, and S.V. Pletnev Combining electron microscopic with X-ray crystallographic structures J. Struct. Biol. 136 2001 190 200
46. A.H. Sharpe, and B.N. Fields Pathogenesis of viral infections. Basic concepts derived from the reovirus model N. Engl. J. Med. 312 1985 486 497
47. M. Shing, and K.M. Coombs Assembly of the reovirus outer capsid requires μ1/σ3 interactions which are prevented by misfolded σ3 protein in temperature-sensitive mutant tsG453 Virus Res. 46 1996 19 29
48. R.E. Smith, H.J. Zweerink, and W.K. Joklik Polypeptide components of virions, top component and cores of reovirus type 3 Virology 39 1969 791 810
49. Y. Tao, D.L. Farsetta, M.L. Nibert, and S.C. Harrison RNA synthesis in a cage - structural studies of the reovirus polymerase λ3 Cell 111 2002 733 745
50. L. Tillotson, and A.J. Shatkin Reovirus polypeptide σ3 and N-terminal myristoylation of polypeptide μ1 are required for site-specific cleavage to μ1C in transfected cells J. Virol. 66 1992 2180 2186
51. K.L. Tyler, P. Clarke, R.L. DeBiasi, D. Kominsky, and G.J. Poggioli Reoviruses and the host cell Trends Microbiol. 9 2001 560 564
52. G.J. Wilson, E.L. Nason, C.S. Hardy, D.H. Ebert, J.D. Wetzel, B.V.V. Prasad, and T.S. Dermody A single mutation in the carboxy terminus of reovirus outer-capsid protein σ3 confers enhanced kinetics of σ3 proteolysis, resistance to inhibitors of viral disassembly, and alterations in σ3 structure J. Virol. 76 2002 9832 9843
53. X. Zhang, S.B. Walker, P.R. Chipman, M.L. Nibert, and T.S. Baker Reovirus polymerase λ3 localized by cryo-electron microscopy of virions at a resolution of 7.6 Å Nat. Struct. Biol. 10 2003 1011 1018
54. Z.H. Zhou, M. Dougherty, J. Jakana, J. He, F.J. Rixon, and W. Chiu Seeing the herpesvirus capsid at 8.5 Å Science 288 2000 877 880
55. 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