Structural insights into RNA encapsidation and helical assembly of the Toscana virus nucleoprotein

Nucleic Acids Research

Volumn 42, Issue 9, 2014, Pages 6025-6037

  Olal, Daniel ^a,b   Dick, Alexej ^a   Woods, Virgil L ^c   Liu, Tong ^c   Li, Sheng ^c   Devignot, Stephanie ^d   Weber, Friedemann ^d   Saphire, Erica Ollmann ^b   Daumke, Oliver ^a,e  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d PHILIPPS UNIVERSITY MARBURG   (Germany)

^e FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; RIBONUCLEOPROTEIN; SINGLE STRANDED RNA;

ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN RNA BINDING; PROTEIN STRUCTURE; RNA VIRUS; STRUCTURE ANALYSIS; TOSCANA VIRUS;

BINDING SITES; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; NUCLEOCAPSID PROTEINS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; RNA, VIRAL; SANDFLY FEVER NAPLES VIRUS; VIRUS ASSEMBLY;

EID: 84901347557     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku229     Document Type: Article

References (45)

1. Valassina, M., Cusi, M.G. and Valensin, P.E. (1996) Rapid identification of Toscana virus by nested PCR during an outbreak in the Siena area of Italy. J. Clin. Microbiol., 34, 2500-2502.
2. Valassina, M., Cusi, M.G. and Valensin, P.E. (2003) A Mediterranean arbovirus: The Toscana virus. J. Neurovirol., 9, 577-583. (Pubitemid 37536713
3. Le May, N., Dubaele, S., Proietti De Santis, L., Billecocq, A., Bouloy, M. and Egly, J.M. (2004) TFIIH transcription factor, a target for the Rift Valley hemorrhagic fever virus. Cell, 116, 541-550. (Pubitemid 38264431
4. Yu, X.J., Liang, M.F., Zhang, S.Y., Liu, Y., Li, J.D., Sun, Y.L., Zhang, L., Zhang, Q.F., Popov, V.L., Li, C. et al. (2011) Fever with thrombocytopenia associated with a novel bunyavirus in China. N. Engl. J. Med., 364, 1523-1532.
5. Le May, N., Gauliard, N., Billecocq, A. and Bouloy, M. (2005) The N terminus of Rift Valley fever virus nucleoprotein is essential for dimerization. J. Virol., 79, 11974-11980. (Pubitemid 41279314
6. Ruigrok, R.W. and Crepin, T. (2010) Nucleoproteins of negative strand RNA viruses; RNA binding, oligomerisation and binding to polymerase co-factor. Viruses, 2, 27-32.
7. Reguera, J., Weber, F. and Cusack, S. (2010) Bunyaviridae RNA polymerases (L-protein) have an N-Terminal, influenza-like endonuclease domain, essential for viral cap-dependent transcription. PLoS Pathog., 6, e1001101.
8. Morin, B., Coutard, B., Lelke, M., Ferron, F., Kerber, R., Jamal, S., Frangeul, A., Baronti, C., Charrel, R., de Lamballerie, X. et al. The N-Terminal domain of the arenavirus L protein is an RNA endonuclease essential in mRNA transcription. PLoS Pathog., 6, e1001038.
9. Overby, A.K., Pettersson, R.F. and Neve, E.P. (2007) The glycoprotein cytoplasmic tail of Uukuniemi virus (Bunyaviridae) interacts with ribonucleoproteins and is critical for genome packaging. J. Virol., 81, 3198-3205. (Pubitemid 46456629
10. Overby, A.K., Pettersson, R.F., Grunewald, K. and Huiskonen, J.T. (2008) Insights into bunyavirus architecture from electron cryotomography of Uukuniemi virus. Proc. Natl. Acad. Sci. U.S.A., 105, 2375-2379.
11. Tawar, R.G., Duquerroy, S., Vonrhein, C., Varela, P.F., Damier-Piolle, L., Castagne, N., MacLellan, K., Bedouelle, H., Bricogne, G., Bhella, D. et al. (2009) Crystal structure of a nucleocapsid-like nucleoprotein-RNA complex of respiratory syncytial virus. Science, 326, 1279-1283.
12. Albertini, A.A., Wernimont, A.K., Muziol, T., Ravelli, R.B., Clapier, C.R., Schoehn, G., Weissenhorn, W. and Ruigrok, R.W. (2006) Crystal structure of the rabies virus nucleoprotein-RNA complex. Science, 313, 360-363. (Pubitemid 44480962
13. Hastie, K.M., Liu, T., Li, S., King, L.B., Ngo, N., Zandonatti, M.A., Woods, V.L. Jr, de la Torre, J.C. and Saphire, E.O. (2011) Crystal structure of the Lassa virus nucleoprotein-RNA complex reveals a gating mechanism for RNA binding. Proc. Natl. Acad. Sci. U.S.A., 108, 19365-19370.
14. Hastie, K.M., Kimberlin, C.R., Zandonatti, M.A., MacRae, I.J. and Saphire, E.O. (2011) Structure of the Lassa virus nucleoprotein reveals a dsRNA-specific 3-To 5-exonuclease activity essential for immune suppression. Proc. Natl. Acad. Sci. U.S.A., 108, 2396-2401.
15. Qi, X., Lan, S., Wang, W., Schelde, L.M., Dong, H., Wallat, G.D., Ly, H., Liang, Y. and Dong, C. (2010) Cap binding and immune evasion revealed by Lassa nucleoprotein structure. Nature, 468, 779-783.
16. Hastie, K.M., King, L.B., Zandonatti, M.A. and Saphire, E.O. (2012) Structural basis for the dsRNA specificity of the Lassa virus NP exonuclease. PLoS ONE, 7, e44211.
17. Li, B., Wang, Q., Pan, X., Fernandez de Castro, I., Sun, Y., Guo, Y., Tao, X., Risco, C., Sui, S.F. and Lou, Z. (2013) Bunyamwera virus possesses a distinct nucleocapsid protein to facilitate genome encapsidation. Proc. Natl. Acad. Sci. U.S.A., 110, 9048-9053.
18. Ariza, A., Tanner, S.J., Walter, C.T., Dent, K.C., Shepherd, D.A., Wu, W., Matthews, S.V., Hiscox, J.A., Green, T.J., Luo, M. et al. (2013) Nucleocapsid protein structures from orthobunyaviruses reveal insight into ribonucleoprotein architecture and RNA polymerization. Nucleic Acids Res., 41, 5912-5926.
19. Dong, H., Li, P., Bottcher, B., Elliott, R.M. and Dong, C. (2013) Crystal structure of Schmallenberg orthobunyavirus nucleoprotein-RNA complex reveals a novel RNA sequestration mechanism. RNA, 19, 1129-1136.
20. Niu, F., Shaw, N., Wang, Y.E., Jiao, L., Ding, W., Li, X., Zhu, P., Upur, H., Ouyang, S., Cheng, G. et al. (2013) Structure of the Leanyer orthobunyavirus nucleoprotein-RNA complex reveals unique architecture for RNA encapsidation. Proc. Natl. Acad. Sci. U.S.A., 110, 9054-9059.
21. Reguera, J., Malet, H., Weber, F. and Cusack, S. (2013) Structural basis for encapsidation of genomic RNA by La Crosse Orthobunyavirus nucleoprotein. Proc. Natl. Acad. Sci. U.S.A., 110, 7246-7251.
22. Ferron, F., Li, Z., Danek, E.I., Luo, D., Wong, Y., Coutard, B., Lantez, V., Charrel, R., Canard, B., Walz, T. et al. (2011) The hexamer structure of Rift Valley fever virus nucleoprotein suggests a mechanism for its assembly into ribonucleoprotein complexes. PLoS Pathog., 7, e1002030.
23. Raymond, D.D., Piper, M.E., Gerrard, S.R., Skiniotis, G. and Smith, J.L. (2012) Phleboviruses encapsidate their genomes by sequestering RNA bases. Proc. Natl. Acad. Sci. U.S.A., 109, 19208-19213.
24. Raymond, D.D., Piper, M.E., Gerrard, S.R. and Smith, J.L. (2010) Structure of the Rift Valley fever virus nucleocapsid protein reveals another architecture for RNA encapsidation. Proc. Natl. Acad. Sci. U.S.A., 107, 11769-11774.
25. Habjan, M., Penski, N., Wagner, V., Spiegel, M., Overby, A.K., Kochs, G., Huiskonen, J.T. and Weber, F. (2009) Efficient production of Rift Valley fever virus-like particles: The antiviral protein MxA can inhibit primary transcription of bunyaviruses. Virology, 385, 400-408.
26. Gasteiger, E., Gattiker, A., Hoogland, C., Ivanyi, I., Appel, R.D. and Bairoch, A. (2003) ExPASy: The proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res., 31, 3784-3788. (Pubitemid 37442246
27. Lundstrom, K. (2003) Semliki Forest virus vectors for large-scale production of recombinant proteins. Methods Mol. Med., 76, 525-543.
28. Kabsch, W. (2010) Xds. Acta Crystallogr. D Biol. Crystallogr., 66, 125-132.
29. Winn, M.D., Ballard, C.C., Cowtan, K.D., Dodson, E.J., Emsley, P., Evans, P.R., Keegan, R.M., Krissinel, E.B., Leslie, A.G., McCoy, A. et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr., 67, 235-242.
30. Kiefer, F., Arnold, K., Kunzli, M., Bordoli, L. and Schwede, T. (2009) The SWISS-MODEL Repository and associated resources. Nucleic Acids Res., 37, D387-D392.
31. Vagin, A. and Teplyakov, A. (2010) Molecular replacement with MOLREP. Acta Crystallogr. D Biol. Crystallogr., 66, 22-25.
32. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C. and Read, R.J. (2007) Phaser crystallographic software. J. Appl. Crystallogr., 40, 658-674.
33. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr., 60, 2126-2132.
34. Adams, P.D., Afonine, P.V., Bunkoczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W. et al. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr., 66, 213-221.
35. Davis, I.W., Leaver-Fay, A., Chen, V.B., Block, J.N., Kapral, G.J., Wang, X., Murray, L.W., Arendall, W.B. III, Snoeyink, J., Richardson, J.S. et al. (2007) MolProbity: All-Atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res., 35, W375-W383.
36. Steinkellner, G., Rader, R., Thallinger, G.G., Kratky, C. and Gruber, K. (2009) VASCo: Computation and visualization of annotated protein surface contacts. BMC Bioinformatics, 10, 32.
37. Englander, J.J., Del Mar, C., Li, W., Englander, S.W., Kim, J.S., Stranz, D.D., Hamuro, Y. and Woods, V.L. Jr (2003) Protein structure change studied by hydrogen-deuterium exchange, functional labeling, and mass spectrometry. Proc. Natl. Acad. Sci. U.S.A., 100, 7057-7062.
38. Klemm, C., Reguera, J., Cusack, S., Zielecki, F., Kochs, G. and Weber, F. (2013) Systems to establish bunyavirus genome replication in the absence of transcription. J. Virol., 87, 8205-8212.
39. Schmaljohn, C.S. and Patterson, J.L. (1990) Bunyaviridae and their replication. Part II: Replication of bunyaviridae. In: Fields, B.N. and and Knipe, D.M. (eds). Fields Virology, 2nd edn. Raven Press, New York, NY, pp. 1175-1194.
40. Zheng, W. and Tao, Y.J. (2013) Genome encapsidation by orthobunyavirus nucleoproteins. Proc. Natl. Acad. Sci. U.S.A., 110, 8769-8770.
41. Accardi, L., Prehaud, C., Di Bonito, P., Mochi, S., Bouloy, M. and Giorgi, C. (2001) Activity of Toscana and Rift Valley fever virus transcription complexes on heterologous templates. J. Gen. Virol., 82, 781-785.
42. Estabrook, E.M., Tsai, J. and Falk, B.W. (1998) In vivo transfer of barley stripe mosaic hordeivirus ribonucleotides to the 5-Terminus of maize stripe tenuivirus RNAs. Proc. Natl. Acad. Sci. U.S.A., 95, 8304-8309.
43. 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. (Pubitemid 44529927
44. Kelley, L.A. and Sternberg, M.J. (2009) Protein structure prediction on the Web: A case study using the Phyre server. Nat. Protocols, 4, 363-371.
45. Espinoza, A.M., Hernandez, M., Pereira, R., Falk, B. and Medina, V. (1992) In situ immunogold labeling analysis of the rice hoja blanca virus nucleoprotein and major noncapsid protein. Virology, 191, 619-627.