3.3 Å Cryo-EM structure of a nonenveloped virus reveals a priming mechanism for cell entry

Cell

Volumn 141, Issue 3, 2010, Pages 472-482

  Zhang, Xing ^a   Jin, Lei ^a   Fang, Qin ^b   Hui, Wong H ^a   Zhou, Z Hong ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b WUHAN INSTITUTE OF VIROLOGY   (China)

Author keywords

Humdisease; Proteins

Indexed keywords

ASPARAGINE; GLUTAMINE; GLYCINE; LYSINE; MEMBRANE PROTEIN; PROLINE; PROTEIN N MYRISTOYLTRANSFERASE; UNCLASSIFIED DRUG; VALINE; VIRUS PROTEIN; VIRUS PROTEIN 5; CAPSID PROTEIN;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; COVALENT BOND; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; CRYSTALLIZATION; HYDROPHOBICITY; NONHUMAN; NUCLEOPHILICITY; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN STRUCTURE; REOVIRUS; VIRION; VIRUS ENTRY; VIRUS MORPHOLOGY; VIRUS PARTICLE; X RAY CRYSTALLOGRAPHY; CHEMICAL STRUCTURE; METABOLISM; TEMPERATURE; ULTRASTRUCTURE;

AQUAREOVIRUS; ORTHOMYXOVIRIDAE;

CAPSID PROTEINS; CRYOELECTRON MICROSCOPY; MODELS, MOLECULAR; REOVIRIDAE; TEMPERATURE; VIRUS INTERNALIZATION;

EID: 77951912692     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2010.03.041     Document Type: Article

References (61)

1. Agosto M.A., Middleton J.K., Freimont E.C., Yin J., Nibert M.L. Thermolabilizing pseudoreversions in reovirus outer-capsid protein micro 1 rescue the entry defect conferred by a thermostabilizing mutation. J. Virol. 2007, 81:7400-7409.
2. Agosto M.A., Myers K.S., Ivanovic T., Nibert M.L. A positive-feedback mechanism promotes reovirus particle conversion to the intermediate associated with membrane penetration. Proc. Natl. Acad. Sci. USA 2008, 105:10571-10576.
3. Banerjee M., Johnson J.E. Activation, exposure and penetration of virally encoded, membrane-active polypeptides during non-enveloped virus entry. Curr. Protein Pept. Sci. 2008, 9:16-27.
4. Bartlett G.J., Porter C.T., Borkakoti N., Thornton J.M. Analysis of catalytic residues in enzyme active sites. J. Mol. Biol. 2002, 324:105-121.
5. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., et al. Crystallography NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 1998, 54:905-921.
6. Chandran K., Nibert M.L. Protease cleavage of reovirus capsid protein mu1/mu1C is blocked by alkyl sulfate detergents, yielding a new type of infectious subvirion particle. J. Virol. 1998, 72:467-475.
7. Chandran K., Nibert M.L. Animal cell invasion by a large nonenveloped virus: reovirus delivers the goods. Trends Microbiol. 2003, 11:374-382.
8. Chandran K., Farsetta D.L., Nibert M.L. Strategy for nonenveloped virus entry: a hydrophobic conformer of the reovirus membrane penetration protein micro 1 mediates membrane disruption. J. Virol. 2002, 76:9920-9933.
9. Chen J.Z., Grigorieff N. SIGNATURE: a single-particle selection system for molecular electron microscopy. J. Struct. Biol. 2007, 157:168-173.
10. Cheng L., Fang Q., Shah S., Atanasov I.C., Zhou Z.H. Subnanometer-resolution structures of the grass carp reovirus core and virion. J. Mol. Biol. 2008, 382:213-222.
11. Cheng L., Zhu J., Hui W.H., Zhang X., Honig B., Fang Q., Zhou Z.H. Backbone model of an aquareovirus virion by cryo-electron microscopy and bioinformatics. J. Mol. Biol. 2010, 397:852-863.
12. Clarke P., Richardson-Burns S.M., DeBiasi R.L., Tyler K.L. Mechanisms of apoptosis during reovirus infection. Curr. Top. Microbiol. Immunol. 2005, 289:1-24.
13. Danthi P., Kobayashi T., Holm G.H., Hansberger M.W., Abel T.W., Dermody T.S. Reovirus apoptosis and virulence are regulated by host cell membrane penetration efficiency. J. Virol. 2008, 82:161-172.
14. DeLano W.L. The PyMOL User's Manual 2002, DeLano Scientific, Palo Alto, CA.
15. Dowell L.G., Rinfret A.P. Low-temperature Forms of Ice Studied by X-ray diffraction. Nature 1960, 188:1144-1148.
16. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 2004, 60:2126-2132.
17. Fang Q., Shah S., Liang Y., Zhou Z.H. 3D reconstruction and capsid protein characterization of grass carp reovirus. Sci. China C Life Sci. 2005, 48:593-600.
18. Fang Q., Seng E.K., Ding Q.Q., Zhang L.L. Characterization of infectious particles of grass carp reovirus by treatment with proteases. Arch. Virol. 2008, 153:675-682.
19. Fritz-Wolf K., Schnyder T., Wallimann T., Kabsch W. Structure of mitochondrial creatine kinase. Nature 1996, 381:341-345.
20. Furlong D.B., Nibert M.L., Fields B.N. Sigma 1 protein of mammalian reoviruses extends from the surfaces of viral particles. J. Virol. 1988, 62:246-256.
21. Greenleaf W.B., Shen J., Gai D., Chen X.S. Systematic study of the functions for the residues around the nucleotide pocket in simian virus 40 AAA+ hexameric helicase. J. Virol. 2008, 82:6017-6023.
22. Grigorieff N. FREALIGN: high-resolution refinement of single particle structures. J. Struct. Biol. 2007, 157:117-125.
23. Grimes J.M., Burroughs J.N., Gouet P., Diprose J.M., Malby R., Ziéntara S., Mertens P.P., Stuart D.I. The atomic structure of the bluetongue virus core. Nature 1998, 395:470-478.
24. Ivanovic T., Agosto M.A., Zhang L., Chandran K., Harrison S.C., Nibert M.L. Peptides released from reovirus outer capsid form membrane pores that recruit virus particles. EMBO J. 2008, 27:1289-1298.
25. Jiang W., Baker M.L., Jakana J., Weigele P.R., King J., Chiu W. Backbone structure of the infectious epsilon15 virus capsid revealed by electron cryomicroscopy. Nature 2008, 451:1130-1134.
26. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 1991, 47:110-119.
27. Kraulis P.J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Cryst. 1991, 24:946-950.
28. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
29. Laskowski R.A., MacArthur M.W., Moss D.S., Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Cryst. 1993, 26:283-291.
30. Li Y., Zhang Y. REMO: a new protocol to refine full atomic protein models from C-alpha traces by optimizing hydrogen-bonding networks. Proteins 2009, 76:665-676.
31. Liang Y., Ke E.Y., Zhou Z.H. IMIRS: a high-resolution 3D reconstruction package integrated with a relational image database. J. Struct. Biol. 2002, 137:292-304.
32. Liemann S., Chandran K., Baker T.S., Nibert M.L., Harrison S.C. Structure of the reovirus membrane-penetration protein, Mu1, in a complex with is protector protein, Sigma3. Cell 2002, 108:283-295.
33. Locher K.P., Lee A.T., Rees D.C. The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science 2002, 296:1091-1098.
34. Middleton J.K., Agosto M.A., Severson T.F., Yin J., Nibert M.L. Thermostabilizing mutations in reovirus outer-capsid protein mu1 selected by heat inactivation of infectious subvirion particles. Virology 2007, 361:412-425.
35. Mindell J.A., Grigorieff N. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 2003, 142:334-347.
36. Nason E.L., Samal S.K., Venkataram Prasad B.V. Trypsin-induced structural transformation in aquareovirus. J. Virol. 2000, 74:6546-6555.
37. Nibert M.L., Fields B.N. A carboxy-terminal fragment of protein mu 1/mu 1C is present in infectious subvirion particles of mammalian reoviruses and is proposed to have a role in penetration. J. Virol. 1992, 66:6408-6418.
38. Nibert M.L., Furlong D.B., Fields B.N. Mechanisms of viral pathogenesis. Distinct forms of reoviruses and their roles during replication in cells and host. J. Clin. Invest. 1991, 88:727-734.
39. Nibert M.L., Schiff L.A., Fields B.N. Mammalian reoviruses contain a myristoylated structural protein. J. Virol. 1991, 65:1960-1967.
40. Nibert M.L., Odegard A.L., Agosto M.A., Chandran K., Schiff L.A. Putative autocleavage of reovirus mu1 protein in concert with outer-capsid disassembly and activation for membrane permeabilization. J. Mol. Biol. 2005, 345:461-474.
41. Noad L., Shou J., Coombs K.M., Duncan R. Sequences of avian reovirus M1, M2 and M3 genes and predicted structure/function of the encoded mu proteins. Virus Res. 2006, 116:45-57.
42. Odegard A.L., Chandran K., Zhang X., Parker J.S., Baker T.S., Nibert M.L. Putative autocleavage of outer capsid protein micro1, allowing release of myristoylated peptide micro1N during particle uncoating, is critical for cell entry by reovirus. J. Virol. 2004, 78:8732-8745.
43. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25:1605-1612.
44. Reddy V., Schneemann A., Johnson J.E. Nodavirus Endopeptidase 2004, Volume 1. Handbook of Proteolytic Enzymes, London. Second Edition.
45. Reinisch K.M., Nibert M.L., Harrison S.C. Structure of the reovirus core at 3.6 A resolution. Nature 2000, 404:960-967.
46. Rivas C., Noya M., Cepeda C., Bandin I., Barja J.L., Dopazo C.P. Replication and morphogenesis of the turbot aquareovirus (TRV) in cell culture. Aquaculture 1998, 160:47-62.
47. Rosenthal P.B., Henderson R. Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. J. Mol. Biol. 2003, 333:721-745.
48. Schluenzen F., Tocilj A., Zarivach R., Harms J., Gluehmann M., Janell D., Bashan A., Bartels H., Agmon I., Franceschi F., Yonath A. Structure of functionally activated small ribosomal subunit at 3.3 angstroms resolution. Cell 2000, 102:615-623.
49. Shing M., Coombs K.M. Assembly of the reovirus outer capsid requires mu 1/sigma 3 interactions which are prevented by misfolded sigma 3 protein in temperature-sensitive mutant tsG453. Virus Res. 1996, 46:19-29.
50. Taylor D.J., Johnson J.E. Folding and particle assembly are disrupted by single-point mutations near the autocatalytic cleavage site of Nudaurelia capensis omega virus capsid protein. Protein Sci. 2005, 14:401-408.
51. Tillotson L., Shatkin A.J. Reovirus polypeptide sigma 3 and N-terminal myristoylation of polypeptide mu 1 are required for site-specific cleavage to mu 1C in transfected cells. J. Virol. 1992, 66:2180-2186.
52. Towler D.A., Gordon J.I., Adams S.P., Glaser L. The biology and enzymology of eukaryotic protein acylation. Annu. Rev. Biochem. 1988, 57:69-99.
53. Tsai B. Penetration of nonenveloped viruses into the cytoplasm. Annu. Rev. Cell Dev. Biol. 2007, 23:23-43.
54. White J.M., Delos S.E., Brecher M., Schornberg K. Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Crit. Rev. Biochem. Mol. Biol. 2008, 43:189-219.
55. Wynne S.A., Crowther R.A., Leslie A.G. The crystal structure of the human hepatitis B virus capsid. Mol. Cell 1999, 3:771-780.
56. Yu X., Jin L., Zhou Z.H. 3.88 A structure of cytoplasmic polyhedrosis virus by cryo-electron microscopy. Nature 2008, 453:415-419.
57. Zhang X., Ji Y., Zhang L., Harrison S.C., Marinescu D.C., Nibert M.L., Baker T.S. Features of reovirus outer capsid protein mu1 revealed by electron cryomicroscopy and image reconstruction of the virion at 7.0 Angstrom resolution. Structure 2005, 13:1545-1557.
58. Zhang X., Tang J., Walker S.B., O'Hara D., Nibert M.L., Duncan R., Baker T.S. Structure of avian orthoreovirus virion by electron cryomicroscopy and image reconstruction. Virology 2005, 343:25-35.
59. Zhang L., Chandran K., Nibert M.L., Harrison S.C. Reovirus mu1 structural rearrangements that mediate membrane penetration. J. Virol. 2006, 80:12367-12376.
60. Zhang X., Settembre E., Xu C., Dormitzer P.R., Bellamy R., Harrison S.C., Grigorieff N. Near-atomic resolution using electron cryomicroscopy and single-particle reconstruction. Proc. Natl. Acad. Sci. USA 2008, 105:1867-1872.
61. Zhou Z.H. Towards atomic resolution structural determination by single-particle cryo-electron microscopy. Curr. Opin. Struct. Biol. 2008, 18:218-228.