An assembly model of Rift Valley fever virus

Frontiers in Microbiology

Volumn 3, Issue JUL, 2012, Pages

  Rusu, Mirabela ^a,g   Bonneau, Richard ^b,c   Holbrook, Michael R ^d,e   Watowich, Stanley J ^d   Birmanns, Stefan ^a   Wriggers, Willy ^f,h   Freiberg, Alexander N ^d  

^a UNIVERSITY OF TEXAS   (United States)

^b NEW YORK UNIVERSITY   (United States)

^c POLYTECHNIC UNIVERSITY   (United States)

^d University of Texas Medical Branch School of Medicine   (United States)

^e NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^f WEILL CORNELL MEDICAL COLLEGE   (United States)

^g RUTGERS UNIVERSITY   (United States)

^h D E SHAW RESEARCH   (United States)

Author keywords

Bunyavirus assembly; Hybrid modeling; Multi body refinement; Multi resolution registration; Protein structure prediction

Indexed keywords

EID: 84870663235     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2012.00254     Document Type: Article

References (59)

1. Alam, S. L., Langelier, C., Whitby, F. G., Koirala, S., Robinson, H., Hill, C. P., and Sundquist, W. I. (2006). Structural basis for ubiquitin recognition by the human ESCRT-II EAP45 GLUE domain. Nat. Struct. Mol. Biol. 13, 1029-1030.
2. Battisti, A. J., Chu, Y. K., Chipman, P. R., Kaufmann, B., Jonsson, C. B., and Rossmann, M. G. (2011). Structural studies of Hantaan virus. J. Virol. 85, 835-841.
3. Besselaar, T. G., and Blackburn, N. K. (1991). Topological mapping of antigenic sites on the RiftValley fever virus envelope glycoproteins using monoclonal antibodies. Arch. Virol. 121, 111-124.
4. Besselaar, T. G., and Blackburn, N. K. (1994). The effect of neutraliz-ing monoclonal antibodies on early events in RiftValley fever virus infec-tivity. Res. Virol. 145, 13-19.
5. Birmanns, S., Rusu, M., and Wrig-gers, W. (2011). Using Sculptor and Situs for simultaneous assembly of atomic components into low-resolution shapes. J. Struct. Biol. 173, 428-435.
6. Cole, C., Barber, J. D., and Barton, G. J. (2008). The Jpred 3 secondary struc-ture prediction server. Nucleic Acids Res. 36, W197-W201.
7. Collett, M. S., Purchio, A. F., Keegan, K., Frazier, S., Hays, W., Anderson, D. K., Parker, M. D., Schmaljohn, C., Schmidt, J., and Dalrymple, J. M. (1985). Complete nucleotide sequence of the M RNA segment of Rift Valley fever virus. Virology 144, 228-245.
8. Elliott, R. M. (2009). Bunyaviruses and climate change. Clin. Microbiol. Infect. 15, 510-517.
9. Estrada,D. F.,Boudreaux,D. M.,Zhong, D., St Jeor, S. C., and De Guzman, R. N. (2009). The hantavirus glyco-protein G1 tail contains dual CCHC-type classical zinc fingers. J. Biol. Chem. 284, 8654-8660.
10. Estrada, D. F., Conner, M., Jeor, S. C., and Guzman, R. N. (2011). The structure of the hantavirus zinc finger domain is conserved and represents the only natively folded region of the Gn cytoplasmic tail. Front. Microbiol. 2:251. doi:10.3389/fmicb.2011.00251
11. Estrada, D. F., and De Guzman, R. N. (2011). Structural characterization of the Crimean-Congo hemorrhagic fever virus Gn tail provides insight into virus assembly. J. Biol. Chem. 286, 21678-21686.
12. Eswar, N., Webb, B., Marti-Renom, M. A., Madhusudhan, M. S., Eramian, D.,Shen,M.Y.,Pieper,U.,and Sali,A. (2006). Comparative protein struc-ture modeling using Modeller. Curr. Protoc. Bioinformatics Chap. 5, Unit 5.6.
13. Freiberg, A. N., Sherman, M. B., Morais, M. C., Holbrook, M. R., and Watowich, S. J. (2008). Three-dimensional organization of Rift Valley fever virus revealed by cry-oelectron tomography. J. Virol. 82, 10341-10348.
14. Garry, C. E., and Garry, R. F. (2004). Proteomics computational analyses suggest that the carboxyl termi-nal glycoproteins of Bunyaviruses are class II viral fusion protein (beta-penetrenes). Theor. Biol. Med. Model. 1, 10.
15. Garry, C. E., and Garry, R. F. (2008). Proteomics computational analy-ses suggest that baculovirus GP64 superfamily proteins are class III penetrenes. Virol. J. 5, 28.
16. Garry, C. E., and Garry, R. F. (2009). Proteomics computational analyses suggest that the bornavirus glycoprotein is a class III viral fusion pro-tein (gamma penetrene). Virol. J. 6, 145.
17. Gerrard, S. R., and Nichol, S. T. (2002). Characterization of the golgi reten-tion motif of Rift Valley fever virus G(N) glycoprotein. J. Virol. 76, 12200-12210.
18. Gibbons, D. L., Vaney, M. C., Roussel, A., Vigouroux, A., Reilly, B., Lep-ault, J., Kielian, M., and Rey, F. A. (2004). Conformational change and protein-protein interactions of the fusion protein of Semliki Forest virus. Nature 427, 320-325.
19. Hepojoki, J., Strandin, T., Vaheri, A., and Lankinen, H. (2010). Interactions and oligomerization of hantavirus glycoproteins. J. Virol. 84, 227-242
20. Heyd, J., and Birmanns, S. (2009). Immersive structural biology: a new approach to hybrid modeling of macromolecular assemblies. Virtual Real. 13, 245-255.
21. Hirokawa, T., Boon-Chieng, S., and Mitaku, S. (1998). SOSUI: classifica-tion and secondary structure prediction system for membrane proteins. Bioinformatics 14, 378-379.
22. Huiskonen, J. T., Hepojoki, J., Lau-rinmaki, P., Vaheri, A., Lankinen, H., Butcher, S. J., and Grunewald, K. (2010). Electron cryotomogra-phy of Tula hantavirus suggests a unique assembly paradigm for enveloped viruses. J. Virol. 84, 4889-4897.
23. Huiskonen, J. T., Overby, A. K., Weber, F., and Grunewald, K. (2009). Elec-tron cryo-microscopy and single-particle averaging of Rift Valley fever virus: evidence for GN-GC glycoprotein heterodimers. J. Virol. 83, 3762-3769.
24. Ikegami, T., Won, S., Peters, C. J., and Makino, S. (2005). Rift Valley fever virus NSs mRNA is transcribed from an incoming anti-viral-sense S RNA segment. J. Virol. 79, 12106-12111.
25. Jaroszewski, L., Rychlewski, L., Li, Z., Li, W., and Godzik, A. (2005). FFAS03: a server for profile-profile sequence alignments. Nucleic Acids Res. 33, W284-W288.
26. Kajan, L., and Rychlewski, L. (2007). Evaluation of 3D-Jury on CASP7 models. BMC Bioinformatics 8, 304. doi:10.1186/1471-2105-8-304
27. Kakach, L. T., Suzich, J. A., and Collett, M. S. (1989). Rift Valley fever virus M segment: phlebovirus expression strategy and protein glycosylation. Virology 170, 505-510.
28. Keegan, K., and Collett, M. S. (1986). Use of bacterial expression cloning to define the amino acid sequences of antigenic determinants on the G2 glycoprotein of Rift Valley fever virus. J. Virol. 58, 263-270.
29. Kielian, M. (2006). Class II virus mem-brane fusion proteins. Virology 344, 38-47.
30. Kielian, M., and Rey, F. A. (2006). Virus membrane-fusion proteins: more than one way to make a hairpin. Nat. Rev. Microbiol. 4, 67-76.
31. Krogh, A., Larsson, B., Von Hei-jne, G., and Sonnhammer, E. L. (2001). Predicting transmembrane protein topology with a hidden Markov model: application to com-plete genomes. J. Mol. Biol. 305, 567-580.
32. Lee,M. S.,Lebeda,F. J.,and Olson,M. A. (2009). Fold prediction of VP24 pro-tein of Ebola and Marburg viruses using de novo fragment assembly. J. Struct. Biol. 167, 136-144.
33. Lee, S. S., Knott, V., Jovanovic, J., Har-los, K., Grimes, J. M., Choulier, L., Mardon, H. J., Stuart, D. I., and Handford, P. A. (2004). Structure of the integrin binding fragment from fibrillin-1 gives new insights into microfibril organization. Structure 12, 717-729.
34. Lescar, J., Roussel, A., Wien, M. W., Navaza, J., Fuller, S. D., Wengler, G., and Rey, F. A. (2001). The fusion glycoprotein shell of Semliki Forest virus: an icosahedral assembly primed for fusogenic activation at endosomal pH. Cell 105, 137-148.
35. Li, L., Jose, J., Xiang, Y., Kuhn, R. J., and Rossmann, M. G. (2010). Structural changes of envelope proteins during alphavirus fusion. Nature 468, 705-708.
36. Lozach, P. Y., Kuhbacher, A., Meier, R., Mancini, R., Bitto, D., Bouloy, M., and Helenius, A. (2011). DC-SIGN as a receptor for phleboviruses. Cell Host Microbe 10, 75-88.
37. Lozach, P. Y., Mancini, R., Bitto, D., Meier, R., Oestereich, L., Overby, A. K., Pettersson, R. F., and Helenius,A. (2010). Entry of bunyaviruses into mammalian cells. Cell Host Microbe 7, 488-499.
38. MMWR. (2007). Rift Valley fever out-break -Kenya, November 2006-January 2007. MMWR Morb. Mortal. Wkly. Rep. 56, 73-76.
39. Overby, A. K., Pettersson, R. F., Grunewald, K., and Huiskonen, J. T. (2008). Insights into bunyavirus architecture from electron cryoto-mography of Uukuniemi virus. Proc. Natl. Acad. Sci. U.S.A. 105, 2375-2379.
40. Overby,A. K.,Popov,V. L.,Pettersson,R. F., and Neve, E. P. (2007). The cyto-plasmic tails of Uukuniemi virus (Bunyaviridae) G(N) and G(C) gly-coproteins are important for intra-cellular targeting and the budding of virus-like particles. J. Virol. 81, 11381-11391.
41. 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 visualiza-tion system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612.
42. Piper, M. E., Sorenson, D. R., and Gerrard, S. R. (2011). Efficient cellular release of Rift Valley fever virus requires genomic RNA. PLoS ONE 6, e18070. doi:10.1371/journal.pone.0018070
43. Plassmeyer, M. L., Soldan, S. S., Stachelek, K. M., Martin-Garcia, J., and Gonzalez-Scarano, F. (2005). California serogroup Gc (G1) gly-coprotein is the principal determi-nant of pH-dependent cell fusion and entry. Virology 338, 121-132.
44. Plassmeyer, M. L., Soldan, S. S., Stachelek, K. M., Roth, S. M., Martin-Garcia, J., and Gonzalez-Scarano, F. (2007). Mutagenesis of the La Crosse virus glycoprotein sup-ports a role for Gc (1066-1087) as the fusion peptide. Virology 358, 273-282.
45. Pletnev, S. V., Zhang, W., Mukhopad-hyay, S., Fisher, B. R., Hernandez, R., Brown, D. T., Baker, T. S., Ross-mann, M. G., and Kuhn, R. J. (2001). Locations of carbohydrate sites on alphavirus glycoproteins show that E1 forms an icosahedral scaffold. Cell 105, 127-136.
46. Ramachandran, G. N., and Sasisekharan, V. (1968). Conformation of polypeptides and proteins. Adv. Pro-tein Chem. 23, 283-438.
47. Roussel,A.,Lescar,J.,Vaney,M. C.,Wen-gler, G., and Rey, F. A. (2006). Struc-ture and interactions at the viral surface of the envelope protein E1 of Semliki forest virus. Structure 14, 75-86.
48. Sherman, M. B., Freiberg, A. N., Holbrook, M. R., and Watowich, S. J. (2009). Single-particle cryo-electron microscopy of Rift Valley fever virus. Virology 387, 11-15.
49. Shi, X., Goli, J., Clark, G., Brauburger, K., and Elliott, R. M. (2009). Functional analysis of the Bun-yamwera orthobunyavirus Gc glycoprotein. J. Gen. Virol. 90, 2483-2492.
50. Soldan, S. S., Hollidge, B. S., Wag-ner, V., Weber, F., and Gonzalez-Scarano, F. (2010). La Crosse virus (LACV) Gc fusion peptide mutants have impaired growth and fusion phenotypes, but remain neurotoxic. Virology 404, 139-147.
51. Stevens, J., Corper, A. L., Basler, C. F., Taubenberger, J. K., Palese, P., and Wilson, I. A. (2004). Structure of the uncleaved human H1 hemagglutinin from the extinct 1918 influenza virus. Science 303, 1866-1870.
52. Tischler, N. D., Gonzalez, A., Perez-Acle, T., Rosemblatt, M., and Valen-zuela, P. D. (2005). Hantavirus Gc glycoprotein: evidence for a class II fusion protein. J. Gen. Virol. 86, 2937-2947.
53. Tusnady, G. E., and Simon, I. (1998). Principles governing amino acid composition of integral membrane proteins: application to topology prediction. J. Mol. Biol. 283, 489-506.
54. Voss, J. E., Vaney, M. C., Duquerroy, S., Vonrhein, C., Girard-Blanc, C., Crublet,E.,Thompson,A.,Bricogne, G., and Rey, F. A. (2010). Gly-coprotein organization of Chikun-gunya virus particles revealed by X-ray crystallography. Nature 468, 709-712.
55. Wasmoen, T. L., Kakach, L. T., and Col-lett, M. S. (1988). Rift Valley fever virus M segment: cellular local-ization of M segment-encoded proteins. Virology 166, 275-280.
56. Willard, L., Ranjan, A., Zhang, H., Monzavi, H., Boyko, R. F., Sykes, B. D., and Wishart, D. S. (2003). VADAR: a web server for quanti-tative evaluation of protein struc-ture quality. Nucleic Acids Res. 31, 3316-3319.
57. Wriggers, W. (2010). Using Situs for the integration of multi-resolution structures. Biophys. Rev. 2, 21-27.
58. Zhang, W., Chipman, P. R., Corver, J., Johnson, P. R., Zhang, Y., Mukhopadhyay, S., Baker, T. S., Strauss, J. H., Rossmann, M. G., and Kuhn, R. J. (2003). Visualization of membrane protein domains by cryo-electron microscopy of dengue virus. Nat. Struct. Biol. 10, 907-912.
59. Zhang, W., Mukhopadhyay, S., Plet-nev, S. V., Baker, T. S., Kuhn, R. J., and Rossmann, M. G. (2002). Placement of the structural pro-teins in Sindbis virus. J. Virol. 76, 11645-11658.