Electron cryotomography of tula hantavirus suggests a unique assembly paradigm for enveloped viruses

Journal of Virology

Volumn 84, Issue 10, 2010, Pages 4889-4897

  Huiskonen, Juha T ^a,b,e   Hepojoki, Jussi ^c   Laurinmäki, Pasi ^b,d   Vaheri, Antti ^c   Lankinen, Hilkka ^c   Butcher, Sarah J ^b,d   Grünewald, Kay ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

^d UNIVERSITY OF HELSINKI   (Finland)

^e UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

RIBONUCLEOPROTEIN; VIRUS GLYCOPROTEIN;

ARTICLE; CRYOELECTRON MICROSCOPY; HANTAVIRUS; NONHUMAN; PRIORITY JOURNAL; TOMOGRAPHY; VIRION; VIRUS ENVELOPE; VIRUS NUCLEOCAPSID; VIRUS PARTICLE;

ANIMALS; CERCOPITHECUS AETHIOPS; CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPE TOMOGRAPHY; HANTAVIRUS; IMAGING, THREE-DIMENSIONAL; VERO CELLS; VIRION; VIRUS ASSEMBLY;

BUNYAVIRIDAE; HANTAVIRUS; RODENTIA;

EID: 77951477375     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00057-10     Document Type: Article

References (39)

1. Adrian, M., J. Dubochet, J. Lepault, and A. W. McDowall. 1984. Cryoelectron microscopy of viruses. Nature 308:32-36.
2. Baker, T. S., N. H. Olson, and S. D. Fuller. 1999. Adding the third dimension to virus life cycles: three-dimensional reconstruction of icosahedral viruses from cryo-electron micrographs. Microbiol. Mol. Biol. Rev. 63:862-922.
3. Butan, C., D. C. Winkler, J. B. Heymann, R. C. Craven, and A. C. Steven. 2008. RSV capsid polymorphism correlates with polymerization efficiency and envelope glycoprotein content: implications that nucleation controls morphogenesis. J. Mol. Biol. 376:1168-1181.
4. Cardone, G., J. G. Purdy, N. Cheng, R. C. Craven, and A. C. Steven. 2009. Visualization of a missing link in retrovirus capsid assembly. Nature 457:694-698.
5. Deyde, V. M., A. A. Rizvanov, J. Chase, E. W. Otteson, and S. C. St. Jeor. 2005. Interactions and trafficking of Andes and Sin Nombre Hantavirus glycoproteins G1 and G2. Virology 331:307-315.
6. Elliott, L. H., M. P. Kiley, and J. B. McCormick. 1984. Hantaan virus: identification of virion proteins. J. Gen. Virol. 65:1285-1293.
7. Elliott, R. M. 1996. The Bunyaviridae. Plenum Press, New York, NY.
8. Estrada, D. F., D. M. Boudreaux, D. Zhong, S. C. St. Jeor, and R. N. De Guzman. 2009. The hantavirus glycoprotein G1 tail contains dual CCHC-type classical zinc fingers. J. Biol. Chem. 284:8654-8660.
9. Fontana, J., N. Lopez-Montero, R. M. Elliott, J. J. Fernandez, and C. Risco. 2008. The unique architecture of Bunyamwera virus factories around the Golgi complex. Cell. Microbiol. 10:2012-2028.
10. Freiberg, A. N., M. B. Sherman, M. C. Morais, M. R. Holbrook, and S. J. Watowich. 2008. Three-dimensional organization of Rift Valley fever virus revealed by cryoelectron tomography. J. Virol. 82:10341-10348.
11. Gavrilovskaya, I. N., M. Shepley, R. Shaw, M. H. Ginsberg, and E. R. Mackow. 1998. β3 Integrins mediate the cellular entry of hantaviruses that cause respiratory failure. Proc. Natl. Acad. Sci. U. S. A. 95:7074-7079.
12. Grünewald, K., and M. Cyrklaff. 2006. Structure of complex viruses and virus-infected cells by electron cryo-tomography. Curr. Opin. Microbiol. 9:437-442.
13. Hepojoki, J., T. Strandin, A. Vaheri, and H. Lankinen. 2010. Interactions and oligomerization of hantavirus glycoproteins. J. Virol. 84:227-242.
14. Heymann, J. B., and D. M. Belnap. 2007. Bsoft: image processing and molecular modeling for electron microscopy. J. Struct. Biol. 157:3-18.
15. Huiskonen, J. T., and S. J. Butcher. 2007. Membrane-containing viruses with icosahedrally symmetric capsids. Curr. Opin. Struct. Biol. 17:229-236.
16. C glycoprotein heterodimers. J. Virol. 83:3762-3769.
17. Jonsson, C. B., J. Hooper, and G. Mertz. 2008. Treatment of hantavirus pulmonary syndrome. Antiviral Res. 78:162-169.
18. Kallio, E. R., J. Klingstrom, E. Gustafsson, T. Manni, A. Vaheri, H. Henttonen, O. Vapalahti, and A. Lundkvist. 2006. Prolonged survival of Puumala hantavirus outside the host: evidence for indirect transmission via the environment. J. Gen. Virol. 87:2127-2134.
19. Klempa, B. 2009. Hantaviruses and climate change. Clin. Microbiol. Infect. 15:518-523.
20. Kremer, J. R., D. N. Mastronarde, and J. R. McIntosh. 1996. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116:71-76.
21. Maes, P., J. Clement, and M. Van Ranst. 2009. Recent approaches in hantavirus vaccine development. Expert Rev. Vaccines 8:67-76.
22. Martin, M. L., H. Lindsey-Regnery, D. R. Sasso, J. B. McCormick, and E. Palmer. 1985. Distinction between Bunyaviridae genera by surface structure and comparison with Hantaan virus using negative stain electron microscopy. Arch. Virol. 86:17-28.
23. Mastronarde, D. N. 2005. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152:36-51.
24. Nichol, S. T., B. J. Beaty, R. M. Elliott, R. W. Goldbach, A. Plyusnin, and R. B. Tesh. 2005. The Bunyaviridae, p. 695-716. In C. M. Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger, and L. A. Ball (ed.), Virus taxonomy: classification and nomenclature of viruses. Eighth report of the International Committee on Taxonomy of Viruses. Elsevier/Academic Press, London, United Kingdom.
25. Överby, A. K., R. F. Pettersson, K. Grünewald, and J. T. Huiskonen. 2008. Insights into bunyavirus architecture from electron cryotomography of Uukuniemi virus. Proc. Natl. Acad. Sci. U. S. A. 105:2375-2379.
26. C glycoproteins are important for intracellular targeting and the budding of virus-like particles. J. Virol. 81:11381-11391.
27. Pettersen, E. F., T. D. Goddard, C. C. Huang, G. S. Couch, D. M. Greenblatt, E. C. Meng, and T. E. Ferrin. 2004. UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605-1612.
28. Plyusnin, A., O. Vapalahti, H. Lankinen, H. Lehvaslaiho, N. Apekina, Y. Myasnikov, H. Kallio-Kokko, H. Henttonen, A. Lundkvist, M. Brummer-Korvenkontio, I. Gavrilovskaya, and A. Vaheri. 1994. Tula virus: a newly detected hantavirus carried by European common voles. J. Virol. 68:7833-7839.
29. Plyusnin, A., O. Vapalahti, and A. Vaheri. 1996. Hantaviruses: genome structure, expression and evolution. J. Gen. Virol. 77:2677-2687.
30. Schmaljohn, C. S., and S. T. Nichol. 2007. Bunyaviridae, p. 1741-1789. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
31. Schmaljohn, C., and B. Hjelle. 1997. Hantaviruses: a global disease problem. Emerg. Infect. Dis. 3:95-104.
32. Schmaljohn, C. S., S. E. Hasty, J. M. Dalrymple, J. W. LeDuc, H. W. Lee, C. H. von Bonsdorff, M. Brummer-Korvenkontio, A. Vaheri, T. F. Tsai, and H. L. Regnery. 1985. Antigenic and genetic properties of viruses linked to hemorrhagic fever with renal syndrome. Science 227:1041-1044.
33. Sherman, M. B., A. N. Freiberg, M. R. Holbrook, and S. J. Watowich. 2009. Single-particle cryo-electron microscopy of Rift Valley fever virus. Virology 387:11-15.
34. Shi, X., and R. M. Elliott. 2002. Golgi localization of Hantaan virus glycoproteins requires coexpression of G1 and G2. Virology 300:31-38.
35. Shi, X., A. Kohl, P. Li, and R. M. Elliott. 2007. Role of the cytoplasmic tail domains of Bunyamwera orthobunyavirus glycoproteins Gn and Gc in virus assembly and morphogenesis. J. Virol. 81:10151-10160. (Pubitemid 350067718)
36. Song, J. W., L. J. Baek, C. S. Schmaljohn, and R. Yanagihara. 2007. Thottapalayam virus, a prototype shrewborne hantavirus. Emerg. Infect. Dis. 13:980-985.
37. Subramaniam, S., A. Bartesaghi, J. Liu, A. E. Bennett, and R. Sougrat. 2007. Electron tomography of viruses. Curr. Opin. Struct. Biol. 17:596-602.
38. Tischler, N. D., A. Gonzalez, T. Perez-Acle, M. Rosemblatt, and P. D. Valenzuela. 2005. Hantavirus Gc glycoprotein: evidence for a class II fusion protein. J. Gen. Virol. 86:2937-2947.
39. Vapalahti, O., A. Lundkvist, S. K. Kukkonen, Y. Cheng, M. Gilljam, M. Kanerva, T. Manni, M. Pejcoch, J. Niemimaa, A. Kaikusalo, H. Henttonen, A. Vaheri, and A. Plyusnin. 1996. Isolation and characterization of Tula virus, a distinct serotype in the genus Hantavirus, family Bunyaviridae. J. Gen. Virol. 77:3063-3067.