Nucleocapsid protein structures from orthobunyaviruses reveal insight into ribonucleoprotein architecture and RNA polymerization

Nucleic Acids Research

Volumn 41, Issue 11, 2013, Pages 5912-5926

  Ariza, Antonio ^a   Tanner, Sian J ^a   Walter, Cheryl T ^a   Dent, Kyle C ^a   Shepherd, Dale A ^a   Wu, Weining ^a   Matthews, Susan V ^a   Hiscox, Julian A ^b   Green, Todd J ^c   Luo, Ming ^c   Elliott, Richard M ^d   Fooks, Anthony R ^b,e   Ashcroft, Alison E ^a   Stonehouse, Nicola J ^a   Ranson, Neil A ^a   Barr, John N ^a   Edwards, Thomas A ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c University of Alabama at Birmingham   (United States)

^d UNIVERSITY OF ST ANDREWS   (United Kingdom)

^e VETERINARY LABORATORIES AGENCY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOCAPSID PROTEIN; RIBONUCLEOPROTEIN; RNA; TETRAMER;

ANIMAL CELL; ARTICLE; BASE PAIRING; BUNYAMWERA VIRUS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOBUNYAVIRUS; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN RNA BINDING; PROTEIN STRUCTURE; SCHMALLENBERG VIRUS; STRUCTURAL HOMOLOGY; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEOCAPSID PROTEINS; ORTHOBUNYAVIRUS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; RIBONUCLEOPROTEINS; RNA; TRANSCRIPTION, GENETIC; VIRUS REPLICATION;

BUNYAMWERA VIRUS; ORTHOBUNYAVIRUS; RNA VIRUSES;

EID: 84878449321     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt268     Document Type: Article

References (66)

1. Plyusnin, A., Beaty, B.J., Elliott, R.M., Goldbach, R., Kormelink, R., Lundkvist, A., Schmaljohn, C.S. and Tesh, R.B. (2012) Bunyaviridae. In: King, A.M.Q., Adams, M.J., Carstens, E.B. and Lefkowitz, E.J. (eds), Virus Taxonomy: classification and nomenclature of viruses: Ninth report of the International Committee on Taxonomy of Viruses, pp. 725-741.
2. Parsonson, I.M., Della-Porta, A.J. and Snowdon, W.A. (1977) Congenital abnormalities in newborn lambs after infection of pregnant sheep with Akabane virus. Infect. Immun., 15, 254-262.
3. Pappu, H.R., Jones, R.A. and Jain, R.K. (2009) Global status of tospovirus epidemics in diverse cropping systems: successes achieved and challenges ahead. Virus Res., 141, 219-236.
4. Thompson, W.H., Kalfayan, B. and Anslow, R.O. (1965) Isolation of California Encephalitis Group Virus from a Fatal Human Illness. Am. J. Epidemiol., 81, 245-253.
5. Bardos, V., Medek, M., Kania, V. and Hubalek, Z. (1975) Isolation of Tahyna virus from the blood of sick children. Acta Virol., 19, 447.
6. Sexton, D.J., Rollin, P.E., Breitschwerdt, E.B., Corey, G.R., Myers, S.A., Dumais, M.R., Bowen, M.D., Goldsmith, C.S., Zaki, S.R., Nichol, S.T. et al. (1997) Life-threatening Cache Valley virus infection. N. Engl. J. Med., 336, 547-549.
7. Gerrard, S.R., Li, L., Barrett, A.D. and Nichol, S.T. (2004) Ngari virus is a Bunyamwera virus reassortant that can be associated with large outbreaks of hemorrhagic fever in Africa. J. Virol., 78, 8922-8926.
8. Hoffmann, B., Scheuch, M., Hoper, D., Jungblut, R., Holsteg, M., Schirrmeier, H., Eschbaumer, M., Goller, K.V., Wernike, K., Fischer, M. et al. (2012) Novel orthobunyavirus in Cattle, Europe, 2011. Emerg. Infect. Dis., 18, 469-472.
9. Goller, K.V., Hoper, D., Schirrmeier, H., Mettenleiter, T.C. and Beer, M. (2012) Schmallenberg virus as possible ancestor of Shamonda virus. Emerg. Infect. Dis., 18, 1644-1646.
10. 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.
11. Ribeiro, D., Borst, J.W., Goldbach, R. and Kormelink, R. (2009) Tomato spotted wilt virus nucleocapsid protein interacts with both viral glycoproteins Gn and Gc in planta. Virology, 383, 121-130.
12. Shi, X., Kohl, A., Li, P. and Elliott, R.M. (2007) Role of the cytoplasmic tail domains of Bunyamwera orthobunyavirus glycoproteins Gn and Gc in virus assembly and morphogenesis. J. Virol., 81, 10151-10160.
13. 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. USA, 107, 11769-11774.
14. 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 the rift valley Fever virus nucleoprotein suggests a mechanism for its assembly into ribonucleoprotein complexes. PLoS Pathog., 7, e1002030.
15. 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. USA, 109, 19208-19213.
16. Carter, S.D., Surtees, R., Walter, C.T., Ariza, A., Bergeron, E., Nichol, S.T., Hiscox, J.A., Edwards, T.A. and Barr, J.N. (2012) Structure, function, and evolution of the Crimean-Congo hemorrhagic fever virus nucleocapsid protein. J. Virol., 86, 10914-10923.
17. Walter, C.T. and Barr, J.N. (2011) Recent advances in the molecular and cellular biology of bunyaviruses. J. Gen. Virol., 92, 2467-2484.
18. Guo, Y., Wang, W., Ji, W., Deng, M., Sun, Y., Zhou, H., Yang, C., Deng, F., Wang, H., Hu, Z. et al. (2012) Crimean-Congo hemorrhagic fever virus nucleoprotein reveals endonuclease activity in bunyaviruses. Proc. Natl Acad. Sci. USA, 109, 5046-5051.
19. Wang, Y., Dutta, S., Karlberg, H., Devignot, S., Weber, F., Hao, Q., Tan, Y.J., Mirazimi, A. and Kotaka, M. (2012) Structure of Crimean-Congo hemorrhagic fever virus nucleoprotein: superhelical homo-oligomers and the role of caspase-3 cleavage. J. Virol., 86, 12294-12303.
20. Rodgers, J.W., Zhou, Q., Green, T.J., Barr, J.N. and Luo, M. (2006) Purification, crystallization and preliminary X-ray crystallographic analysis of the nucleocapsid protein of Bunyamwera virus. Acta Crystallograph. Sect. F Struct. Biol. Cryst. Commun., 62, 361-364.
21. Kabsch, W. (2010) Xds. Acta Crystallogr. D Biol. Crystallogr., 66, 125-132.
22. Battye, T.G., Kontogiannis, L., Johnson, O., Powell, H.R. and Leslie, A.G. (2011) iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr. D Biol. Crystallogr., 67, 271-281.
23. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr., 62, 72-82.
24. Terwilliger, T.C., Adams, P.D., Read, R.J., McCoy, A.J., Moriarty, N.W., Grosse-Kunstleve, R.W., Afonine, P.V., Zwart, P.H. and Hung, L.W. (2009) Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard. Acta Crystallogr. D Biol. Crystallogr., 65, 582-601.
25. Terwilliger, T.C. and Berendzen, J. (1999) Automated MAD and MIR structure solution. Acta Crystallogr. D Biol. Crystallogr., 55, 849-861.
26. Cowtan, K. (2006) The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr. D Biol. Crystallogr., 62, 1002-1011.
27. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr., 60, 2126-2132.
28. Murshudov, G.N., Vagin, A.A. and Dodson, E.J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr., 53, 240-255.
29. Storoni, L.C., McCoy, A.J. and Read, R.J. (2004) Likelihoodenhanced fast rotation functions. Acta Crystallogr. D Biol. Crystallogr., 60, 432-438.
30. Jenkins, H.T., Malkova, B. and Edwards, T.A. (2011) Kinked beta-strands mediate high-affinity recognition of mRNA targets by the germ-cell regulator DAZL. Proc. Natl Acad. Sci. USA, 108, 18266-18271.
31. Novoa, R.R., Calderita, G., Cabezas, P., Elliott, R.M. and Risco, C. (2005) Key Golgi factors for structural and functional maturation of bunyamwera virus. J. Virol., 79, 10852-10863.
32. Arstila, P. (1974) Characteristics of vesicular stomatitis virus envelopes released with saponin. J. Gen. Virol., 24, 319-326.
33. Frank, J., Radermacher, M., Penczek, P., Zhu, J., Li, Y., Ladjadj, M. and Leith, A. (1996) SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol., 116, 190-199.
34. van Heel, M., Harauz, G., Orlova, E.V., Schmidt, R. and Schatz, M. (1996) A new generation of the IMAGIC image processing system. J. Struct. Biol., 116, 17-24.
35. Barr, J.N., Elliott, R.M., Dunn, E.F. and Wertz, G.W. (2003) Segment-specific terminal sequences of Bunyamwera bunyavirus regulate genome replication. Virology, 311, 326-338.
36. Dunn, E.F., Pritlove, D.C., Jin, H. and Elliott, R.M. (1995) Transcription of a recombinant bunyavirus RNA template by transiently expressed bunyavirus proteins. Virology, 211, 133-143.
37. Iroegbu, C.U. and Pringle, C.R. (1981) Genetic interactions among viruses of the Bunyamwera complex. J. Virol., 37, 383-394.
38. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R. et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947-2948.
39. Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res., 22, 4673-4680.
40. Page, R.D. (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci., 12, 357-358.
41. Bond, C.S. and Schuttelkopf, A.W. (2009) ALINE: a WYSIWYG protein-sequence alignment editor for publication-quality alignments. Acta Crystallogr. D Biol. Crystallogr., 65, 510-512.
42. Krissinel, E. and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol., 372, 774-797.
43. Mohl, B.P. and Barr, J.N. (2009) Investigating the specificity and stoichiometry of RNA binding by the nucleocapsid protein of Bunyamwera virus. RNA, 15, 391-399.
44. Holm, L. and Rosenstrom, P. (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res., 38, W545-W549.
45. Eifan, S.A. and Elliott, R.M. (2009) Mutational analysis of the Bunyamwera orthobunyavirus nucleocapsid protein gene. J. Virol., 83, 11307-11317.
46. Walter, C.T., Bento, D.F., Alonso, A.G. and Barr, J.N. (2011) Amino acid changes within the Bunyamwera virus nucleocapsid protein differentially affect the mRNA transcription and RNA replication activities of assembled ribonucleoprotein templates. J. Gen. Virol., 92, 80-84.
47. Hewlett, M.J., Pettersson, R.F. and Baltimore, D. (1977) Circular forms of Uukuniemi virion RNA: an electron microscopic study. J. Virol., 21, 1085-1093.
48. Pardigon, N., Vialat, P., Girard, M. and Bouloy, M. (1982) Panhandles and hairpin structures at the termini of germiston virus RNAs (Bunyavirus). Virology, 122, 191-197.
49. Pettersson, R.F. and von Bonsdorff, C.H. (1975) Ribonucleoproteins of Uukuniemi virus are circular. J. Virol., 15, 386-392.
50. Raju, R. and Kolakofsky, D. (1989) The ends of La Crosse virus genome and antigenome RNAs within nucleocapsids are base paired. J. Virol., 63, 122-128.
51. Samso, A., Bouloy, M. and Hannoun, C. (1975) Circular ribonucleoproteins in the virus Lumbo (Bunyavirus). C. R. Acad. Sci., 280, 779-782.
52. Obijeski, J.F., Bishop, D.H., Palmer, E.L. and Murphy, F.A. (1976) Segmented genome and nucleocapsid of La Crosse virus. J. Virol., 20, 664-675.
53. Barr, J.N. and Wertz, G.W. (2004) Bunyamwera bunyavirus RNA synthesis requires cooperation of 3'-and 5'-terminal sequences. J. Virol., 78, 1129-1138.
54. Walter, C.T. and Barr, J.N. (2010) Bunyamwera virus can repair both insertions and deletions during RNA replication. RNA, 16, 1138-1145.
55. Fodor, E., Seong, B.L. and Brownlee, G.G. (1993) Photochemical cross-linking of influenza A polymerase to its virion RNA promoter defines a polymerase binding site at residues 9 to 12 of the promoter. J. Gen. Virol., 74(Pt. 7), 1327-1333.
56. Klumpp, K., Ruigrok, R.W. and Baudin, F. (1997) Roles of the influenza virus polymerase and nucleoprotein in forming a functional RNP structure. EMBO J., 16, 1248-1257.
57. Martin-Benito, J., Area, E., Ortega, J., Llorca, O., Valpuesta, J.M., Carrascosa, J.L. and Ortin, J. (2001) Three-dimensional reconstruction of a recombinant influenza virus ribonucleoprotein particle. EMBO Rep., 2, 313-317.
58. Cheong, H.K., Cheong, C. and Choi, B.S. (1996) Secondary structure of the panhandle RNA of influenza virus A studied by NMR spectroscopy. Nucleic Acids Res., 24, 4197-4201.
59. Flick, R. and Hobom, G. (1999) Interaction of influenza virus polymerase with viral RNA in the 'corkscrew' conformation. J. Gen. Virol., 80(Pt. 10), 2565-2572.
60. Fodor, E., Pritlove, D.C. and Brownlee, G.G. (1994) The influenza virus panhandle is involved in the initiation of transcription. J. Virol., 68, 4092-4096.
61. Hsu, M.T., Parvin, J.D., Gupta, S., Krystal, M. and Palese, P. (1987) Genomic RNAs of influenza viruses are held in a circular conformation in virions and in infected cells by a terminal panhandle. Proc. Natl Acad. Sci. USA, 84, 8140-8144.
62. Baudin, F., Bach, C., Cusack, S. and Ruigrok, R.W. (1994) Structure of influenza virus RNP. I. Influenza virus nucleoprotein melts secondary structure in panhandle RNA and exposes the bases to the solvent. EMBO J., 13, 3158-3165.
63. Garcin, D., Lezzi, M., Dobbs, M., Elliott, R.M., Schmaljohn, C., Kang, C.Y. and Kolakofsky, D. (1995) The 5' ends of Hantaan virus (Bunyaviridae) RNAs suggest a prime-and-realign mechanism for the initiation of RNA synthesis. J. Virol., 69, 5754-5762.
64. Jin, H. and Elliott, R.M. (1993) Non-viral sequences at the 5' ends of Dugbe nairovirus S mRNAs. J. Gen. Virol., 74, 2293-2297.
65. Arranz, R., Coloma, R., Chichon, F.J., Conesa, J.J., Carrascosa, J.L., Valpuesta, J.M., Ortin, J. and Martin-Benito, J. (2012) The structure of native influenza virion ribonucleoproteins. Science, 338, 1634-1637.
66. Moeller, A., Kirchdoerfer, R.N., Potter, C.S., Carragher, B. and Wilson, I.A. (2012) Organization of the influenza virus replication machinery. Science, 338, 1631-1634.