Crystal structure of Junin virus nucleoprotein

Journal of General Virology

Volumn 94, Issue PART10, 2013, Pages 2175-2183

  Zhang, Yinjie ^a,b   Li, Le ^a,b   Liu, Xiang ^b   Dong, Shishang ^a,b   Wang, Wenming ^a,b   Huo, Tong ^a,b   Guo, Yu ^a   Rao, Zihe ^a,b   Yang, Cheng ^a,b  

^a NANKAI UNIVERSITY   (China)

^b Tianjin Joint Academy of Biomedicine and Technology   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EXONUCLEASE; TRANSFER RNA; VIRUS NUCLEOPROTEIN;

ARTICLE; ATOMIC ABSORPTION SPECTROMETRY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ION EXCHANGE CHROMATOGRAPHY; JUNIN VIRUS; LASSA VIRUS; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; GENE EXPRESSION REGULATION, VIRAL; JUNIN VIRUS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEOPROTEINS; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT;

EID: 84884186043     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.055053-0     Document Type: Article

References (49)

1. Adams, P. D., Grosse-Kunstleve, R. W., Hung, L. W., Ioerger, T. R., McCoy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K. & Terwilliger, T. C. (2002). PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 58, 1948-1954.
2. Albertini, A. A., Wernimont, A. K., Muziol, T., Ravelli, R. B., Clapier, C. R., Schoehn, G., Weissenhorn, W. & Ruigrok, R. W. (2006). Crystal structure of the rabies virus nucleoprotein-RNA complex. Science 313, 360-363.
3. Albertini, A. A., Schoehn, G., Weissenhorn, W. & Ruigrok, R. W. (2008). Structural aspects of rabies virus replication. Cell Mol Life Sci 65, 282-294.
4. 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. & other authors (2013). Nucleocapsid protein structures from orthobunyaviruses reveal insight into ribonucleoprotein architecture and RNA polymerization. Nucleic Acids Res 41, 5912-5926.
5. Brunotte, L., Kerber, R., Shang, W., Hauer, F., Hass, M., Gabriel, M., Lelke, M., Busch, C., Stark, H. & other authors (2011). Structure of the Lassa virus nucleoprotein revealed by X-ray crystallography, small-angle X-ray scattering, and electron microscopy. J Biol Chem 286, 38748-38756.
6. Casabona, J. C., Levingston Macleod, J. M., Loureiro, M. E., Gomez, G. A. & Lopez, N. (2009). The RING domain and the L79 residue of Z protein are involved in both the rescue of nucleocapsids and the incorporation of glycoproteins into infectious chimeric arenaviruslike particles. J Virol 83, 7029-7039.
7. Cisneros, G. A., Perera, L., Schaaper, R. M., Pedersen, L. C., London, R. E., Pedersen, L. G. & Darden, T. A. (2009). Reaction mechanism of the epsilon subunit of E. coli DNA polymerase III: insights into active site metal coordination and catalytically significant residues. J Am Chem Soc 131, 1550-1556.
8. Cuevas, C. D., Lavanya, M., Wang, E. & Ross, S. R. (2011). Junin virus infects mouse cells and induces innate immune responses. J Virol 85, 11058-11068.
9. de Silva, U., Choudhury, S., Bailey, S. L., Harvey, S., Perrino, F. W. & Hollis, T. (2007). The crystal structure of TREX1 explains the 3′ nucleotide specificity and reveals a polyproline II helix for protein partnering. J Biol Chem 282, 10537-10543.
10. DeLano, W. L. (2002). The PyMOL Molecular Graphics System. San Carlos, CA: DeLano Scientific.
11. Eckerle, L. D., Becker, M. M., Halpin, R. A., Li, K., Venter, E., Lu, X., Scherbakova, S., Graham, R. L., Baric, R. S. & other authors (2010). Infidelity of SARS-CoV Nsp14-exonuclease mutant virus replication is revealed by complete genome sequencing. PLoS Pathog 6, e1000896.
12. Emsley, P. & Cowtan, K. (2004). Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60, 2126-2132.
13. Enria, D. A., Briggiler, A. M. & Sánchez, Z. (2008). Treatment of Argentine hemorrhagic fever. Antiviral Res 78, 132-139.
14. Ge, P., Tsao, J., Schein, S., Green, T. J., Luo, M. & Zhou, Z. H. (2010). Cryo-EM model of the bullet-shaped vesicular stomatitis virus. Science 327, 689-693.
15. Grant, A., Seregin, A., Huang, C., Kolokoltsova, O., Brasier, A., Peters, C. & Paessler, S. (2012). Junín virus pathogenesis and virus replication. Viruses 4, 2317-2339.
16. Green, T. J., Zhang, X., Wertz, G. W. & Luo, M. (2006). Structure of the vesicular stomatitis virus nucleoprotein-RNA complex. Science 313, 357-360.
17. Guo, Y., Wang, W., Ji, W., Deng, M., Sun, Y., Zhou, H., Yang, C., Deng, F., Wang, H. & other authors (2012). Crimean-Congo hemorrhagic fever virus nucleoprotein reveals endonuclease activity in bunyaviruses. Proc Natl Acad Sci U S A 109, 5046-5051.
18. Hastie, K. M., Kimberlin, C. R., Zandonatti, M. A., MacRae, I. J. & Saphire, E. O. (2011a). 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.
19. Hastie, K. M., Liu, T., Li, S., King, L. B., Ngo, N., Zandonatti, M. A., Woods, V. L., Jr, de la Torre, J. C. & Saphire, E. O. (2011b). 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.
20. Holm, L. & Rosenström, P. (2010). Dali server: conservation mapping in 3D. Nucleic Acids Res 38 (Web Server issue), W545-W549.
21. Jiang, X., Huang, Q., Wang, W., Dong, H., Ly, H., Liang, Y. & Dong, C. (2013). Structures of arenaviral nucleoproteins with triphosphate dsRNA reveal a unique mechanism of immune suppression. J Biol Chem 288, 16949-16959.
22. Kranzusch, P. J. & Whelan, S. P. (2012). Architecture and regulation of negative-strand viral enzymatic machinery. RNA Biol 9, 941-948.
23. Laskowski, R., MacArthur, M. W., Moss, D. S. & Thornton, J. M. (1993). PROCHECK: A program to check the stereochemical quality of protein structures. J Appl Cryst 26, 283-291.
24. Levingston Macleod, J. M., D'Antuono, A., Loureiro, M. E., Casabona, J. C., Gomez, G. A. & Lopez, N. (2011). Identification of two functional domains within the arenavirus nucleoprotein. J Virol 85, 2012-2023.
25. Li, B., Wang, Q., Pan, X., Fernández de Castro, I., Sun, Y., Guo, Y., Tao, X., Risco, C., Sui, S. F. & Lou, Z. (2013). Bunyamwera virus possesses a distinct nucleocapsid protein to facilitate genome encapsidation. Proc Natl Acad Sci U S A 110, 9048-9053.
26. Martínez-Sobrido, L., Giannakas, P., Cubitt, B., García-Sastre, A. & de la Torre, J. C. (2007). Differential inhibition of type I interferon induction by arenavirus nucleoproteins. J Virol 81, 12696-12703.
27. Mills, J. N., Ellis, B. A., Childs, J. E., McKee, K. T., Jr, Maiztegui, J. I., Peters, C. J., Ksiazek, T. G. & Jahrling, P. B. (1994). Prevalence of infection with Junin virus in rodent populations in the epidemic area of Argentine hemorrhagic fever. Am J Trop Med Hyg 51, 554-562.
28. Minskaia, E., Hertzig, T., Gorbalenya, A. E., Campanacci, V., Cambillau, C., Canard, B. & Ziebuhr, J. (2006). Discovery of an RNA virus 3′ A5′ exoribonuclease that is critically involved in coronavirus RNA synthesis. Proc Natl Acad Sci U S A 103, 5108-5113.
29. Ng, A. K., Zhang, H., Tan, K., Li, Z., Liu, J. H., Chan, P. K., Li, S. M., Chan, W. Y., Au, S. W. & other authors (2008). Structure of the influenza virus A H5N1 nucleoprotein: implications for RNA binding, oligomerization, and vaccine design. FASEB J 22, 3638-3647.
30. Ng, A. K., Lam, M. K., Zhang, H., Liu, J., Au, S. W., Chan, P. K., Wang, J. & Shaw, P. C. (2012). Structural basis for RNA binding and homooligomer formation by influenza B virus nucleoprotein. J Virol 86, 6758-6767.
31. Niu, F., Shaw, N., Wang, Y. E., Jiao, L., Ding, W., Li, X., Zhu, P., Upur, H., Ouyang, S. & other authors (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.
32. Otwinowski, Z. & Minor, W. (1997). Processing of X-ray diffraction data collected in oscillation mode. In Methods in Enzymology, vol. 276. Macromolecular Crystallography, Part A, pp. 307-326. Edited by C. W., Jr & R. M. Sweet. New York: Academic Press.
33. Parodi, A. S., Coto, C. E., Boxaca, M., Lajmanovich, S. & González, S. (1966). Characteristics of Junin virus. Arch Gesamte Virusforsch 19, 393-402.
34. Perez, M., Craven, R. C. & de la Torre, J. C. (2003). The small RING finger protein Z drives arenavirus budding: implications for antiviral strategies. Proc Natl Acad Sci U S A 100, 12978-12983.
35. Qi, X., Lan, S., Wang, W., Schelde, L. M., Dong, H., Wallat, G. D., Ly, H., Liang, Y. & Dong, C. (2010). Cap binding and immune evasion revealed by Lassa nucleoprotein structure. Nature 468, 779-783.
36. Reguera, J., Malet, H., Weber, F. & 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.
37. Rudolph, M. G., Kraus, I., Dickmanns, A., Eickmann, M., Garten, W. & Ficner, R. (2003). Crystal structure of the Borna disease virus nucleoprotein. Structure 11, 1219-1226.
38. Ruigrok, R. W., Crépin, T. & Kolakofsky, D. (2011). Nucleoproteins and nucleocapsids of negative-strand RNA viruses. Curr Opin Microbiol 14, 504-510.
39. Steitz, T. A. & Steitz, J. A. (1993). A general two-metal-ion mechanism for catalytic RNA. Proc Natl Acad Sci U S A 90, 6498-6502.
40. Strecker, T., Eichler, R., Meulen, J., Weissenhorn, W., Dieter Klenk, H., Garten, W. & Lenz, O. (2003). Lassa virus Z protein is a matrix protein and sufficient for the release of virus-like particles [corrected]. J Virol 77, 10700-10705.
41. Sun, Y., Guo, Y. & Lou, Z. (2012). A versatile building block: the structures and functions of negative-sense single-stranded RNA virus nucleocapsid proteins. Protein Cell 3, 893-902.
42. Tawar, R. G., Duquerroy, S., Vonrhein, C., Varela, P. F., Damier-Piolle, L., Castagné, N., MacLellan, K., Bedouelle, H., Bricogne, G. & other authors (2009). Crystal structure of a nucleocapsid-like nucleoprotein-RNA complex of respiratory syncytial virus. Science 326, 1279-1283.
43. Terwilliger, T. C. (2000). Maximum-likelihood density modification. Acta Crystallogr D Biol Crystallogr 56, 965-972.
44. Terwilliger, T. C. & Berendzen, J. (1999). Automated MAD and MIR structure solution. Acta Crystallogr D Biol Crystallogr 55, 849-861.
45. Urata, S., Noda, T., Kawaoka, Y., Yokosawa, H. & Yasuda, J. (2006). Cellular factors required for Lassa virus budding. J Virol 80, 4191-4195.
46. Urata, S., Yasuda, J. & de la Torre, J. C. (2009). The Z protein of the New World arenavirus Tacaribe virus has bona fide budding activity that does not depend on known late domain motifs. J Virol 83, 12651-12655.
47. Yan, N., Regalado-Magdos, A. D., Stiggelbout, B., Lee-Kirsch, M. A. & Lieberman, J. (2010). The cytosolic exonuclease TREX1 inhibits the innate immune response to human immunodeficiency virus type 1. Nat Immunol 11, 1005-1013.
48. Ye, Q., Krug, R. M. & Tao, Y. J. (2006). The mechanism by which influenza A virus nucleoprotein forms oligomers and binds RNA. Nature 444, 1078-1082.
49. Zuo, Y., Zheng, H., Wang, Y., Chruszcz, M., Cymborowski, M., Skarina, T., Savchenko, A., Malhotra, A. & Minor, W. (2007). Crystal structure of RNase T, an exoribonuclease involved in tRNA maturation and end turnover. Structure 15, 417-428.