Structure, function, and evolution of the crimean-congo hemorrhagic fever virus nucleocapsid protein

Journal of Virology

Volumn 86, Issue 20, 2012, Pages 10914-10923

  Carter, Stephen D ^a   Surtees, Rebecca ^a,b   Walter, Cheryl T ^a   Ariza, Antonio ^a   Bergeron, Éric ^c   Nichol, Stuart T ^c   Hiscox, Julian A ^a   Edwards, Thomas A ^a   Barr, John N ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b PUBLIC HEALTH ENGLAND   (United Kingdom)

^c NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; NUCLEOCAPSID PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; EVOLUTION; NAIRO VIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STRUCTURE; RNA BINDING; RNA SYNTHESIS; RNA VIRUS; STRUCTURAL HOMOLOGY; VIRUS STRAIN;

AMINO ACID SEQUENCE; CASPASE 3; CRYSTALLOGRAPHY, X-RAY; EVOLUTION, MOLECULAR; HEMORRHAGIC FEVER VIRUS, CRIMEAN-CONGO; HEMORRHAGIC FEVER, CRIMEAN; NUCLEOCAPSID; NUCLEOCAPSID PROTEINS; PHYLOGENY; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RNA, VIRAL; RNA-BINDING PROTEINS; SEQUENCE ALIGNMENT;

ARENAVIRUS; BUNYAVIRIDAE; CRIMEAN-CONGO HEMORRHAGIC FEVER VIRUS; DHORI VIRUS; LASSA VIRUS; ORTHOBUNYAVIRUS; RNA VIRUSES;

EID: 84869031243     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01555-12     Document Type: Article

References (55)

1. Acta Crystallographica. Section D. Biological Crystallography. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50:760-763.
2. Andersson I, et al. 2004. Human MxA protein inhibits the replication of Crimean-Congo hemorrhagic fever virus. J. Virol. 78:4323-4329.
3. Andersson I, et al. 2004. Role of actin filaments in targeting of Crimean Congo hemorrhagic fever virus nucleocapsid protein to perinuclear regions of mammalian cells. J. Med. Virol. 72:83-93.
4. Bergeron E, Albarino CG, Khristova ML, Nichol ST. 2010. Crimean-Congo hemorrhagic fever virus-encoded ovarian tumor protease activity is dispensable for virus RNA polymerase function. J. Virol. 84:216-226.
5. Bond CS, Schuttelkopf AW. 2009. ALINE: a WYSIWYG proteinsequence alignment editor for publication-quality alignments. Acta Crystallogr. D Biol. Crystallogr. 65:510-512.
6. Brunotte L, et al. 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.
7. Carter SD, Barr JN, Edwards TA. 2012. Expression, purification and crystallization of the Crimean-Congo hemorrhagic fever virus nucleocapsid protein. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 68:569-573.
8. Chen VB, et al. 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66: 12-21.
9. Cheng E, et al. 2011. Characterization of the interaction between hantavirus nucleocapsid protein (N) and ribosomal protein S19 (RPS19). J. Biol. Chem. 286:11814-11824.
10. Cowtan K. 2010. Recent developments in classical density modification. Acta Crystallogr. D Biol. Crystallogr. 66:470-478.
11. Denault JB, Salvesen GS. 2003. Expression, purification, and characterization of caspases. Curr. Protoc. Protein Sci. Chapter 21:Unit 21.13.
12. Deyde VM, Khristova ML, Rollin PE, Ksiazek TG, Nichol ST. 2006. Crimean-Congo hemorrhagic fever virus genomics and global diversity. J. Virol. 80:8834-8842.
13. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132.
14. Ergonul O, Tuncbilek S, Baykam N, Celikbas A, Dokuzoguz B. 2006. Evaluation of serum levels of interleukin (IL)-6, IL-10, and tumor necrosis factor-alpha in patients with Crimean-Congo hemorrhagic fever. J. Infect. Dis. 193:941-944.
15. Ferron F, 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. doi:10.1371/journal. ppat.1002030.
16. Guo Y, et al. 2012. Crimean-Congo hemorrhagic fever virus nucleoprotein reveals endonuclease activity in bunyaviruses. Proc. Natl. Acad. Sci. U. S. A. 109:5046-5051.
17. Hastie KM, Kimberlin CR, Zandonatti MA, MacRae IJ, Saphire EO. 2011. Structure of the Lassa virus nucleoprotein reveals a dsRNA-specific3= to 5= exonuclease activity essential for immune suppression. Proc. Natl. Acad. Sci. U. S. A. 108:2396-2401.
18. Hastie KM, et al. 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.
19. Hepojoki J, et al. 2010. Cytoplasmic tails of hantavirus glycoproteins interact with the nucleocapsid protein. J. Gen. Virol. 91:2341-2350.
20. Karlberg H, Tan YJ, Mirazimi A. 2011. Induction of caspase activation and cleavage of the viral nucleocapsid protein in different cell types during Crimean-Congo hemorrhagic fever virus infection. J. Biol. Chem. 286: 3227-3234.
21. Kochs G, Janzen C, Hohenberg H, Haller O. 2002. Antivirally active MxA protein sequesters La Crosse virus nucleocapsid protein into perinuclear complexes. Proc. Natl. Acad. Sci. U. S. A. 99:3153-3158.
22. Lamzin VS, Wilson KS. 1997. Automated refinement for protein crystallography. Methods Enzymol. 277:269-305.
23. Larkin MA, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
24. Lenz O, ter Meulen J, Klenk HD, Seidah NG, Garten W. 2001. The Lassa virus glycoprotein precursor GP-C is proteolytically processed by subtilase SKI-1/S1P. Proc. Natl. Acad. Sci. U. S. A. 98:12701-12705.
25. Maltezou HC, Papa A. 2010. Crimean-Congo hemorrhagic fever: risk for emergence of new endemic foci in Europe? Travel Med. Infect. Dis. 8:139-143.
26. Mild M, Simon M, Albert J, Mirazimi A. 2010. Towards an understanding of the migration of Crimean-Congo hemorrhagic fever virus. J. Gen. Virol. 91:199-207.
27. Mir MA, Duran WA, Hjelle BL, Ye C, Panganiban AT. 2008. Storage of cellular 5= mRNA caps in P bodies for viral cap-snatching. Proc. Natl. Acad. Sci. U. S. A. 105:19294-19299.
28. Mir MA, Panganiban AT. 2008. A protein that replaces the entire cellular eIF4F complex. EMBO J. 27:3129-3139.
29. Mir MA, Sheema S, Haseeb A, Haque A. 2010. Hantavirus nucleocapsid protein has distinct m7G cap- and RNA-binding sites. J. Biol. Chem. 285: 11357-11368.
30. Murshudov GN, Vagin AA, Dodson EJ. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53:240-255.
31. Ontiveros SJ, Li Q, Jonsson CB. 2010. Modulation of apoptosis and immune signaling pathways by the Hantaan virus nucleocapsid protein. Virology 401:165-178.
32. Overby AK, Pettersson RF, Neve EP. 2007. The glycoprotein cytoplasmic tail of Uukuniemi virus (Bunyaviridae) interacts with ribonucleoproteins and is critical for genome packaging. J. Virol. 81:3198-3205.
33. Page RD. 1996. TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12:357-358.
34. Painter J, Merritt EA. 2006. Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr. D Biol. Crystallogr. 62:439-450.
35. Qi X, et al. 2010. Cap binding and immune evasion revealed by Lassa nucleoprotein structure. Nature 468:779-783.
36. Ramanathan HN, et al. 2007. Dynein-dependent transport of the Hantaan virus nucleocapsid protein to the endoplasmic reticulum-Golgi intermediate compartment. J. Virol. 81:8634-8647.
37. Ramanathan HN, Jonsson CB. 2008. New and Old World hantaviruses differentially utilize host cytoskeletal components during their life cycles. Virology 374:138-150.
38. Ravkov EV, Nichol ST, Peters CJ, Compans RW. 1998. Role of actin microfilaments in Black Creek Canal virus morphogenesis. J. Virol. 72: 2865-2870.
39. Raymond DD, Piper ME, Gerrard SR, Smith JL. 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.
40. Ribeiro D, Borst JW, Goldbach R, Kormelink R. 2009. Tomato spotted wilt virus nucleocapsid protein interacts with both viral glycoproteins Gn and Gc in planta. Virology 383:121-130.
41. Rodrigues R, Paranhos-Baccala G, Vernet G, Peyrefitte CN. 2012. Crimean-Congo hemorrhagic fever virus-infected hepatocytes induce ER-stress and apoptosis crosstalk. PLoS One 7:e29712. doi:10.1371/ journal.pone.0029712.
42. Schmaljohn CS, Nichol ST. 2007. Bunyaviridae, p 1741-1789. In Knipe DM, et al (ed), Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
43. Shi X, Kohl A, Li P, Elliott RM. 2007. Role of the cytoplasmic tail domains of Bunyamwera orthobunyavirus glycoproteins Gn and Gc in virus assembly and morphogenesis. J. Virol. 81:10151-10160.
44. Simon M, Johansson C, Lundkvist A, Mirazimi A. 2009. Microtubuledependent and microtubule-independent steps in Crimean-Congo hemorrhagic fever virus replication cycle. Virology 385:313-322.
45. Snippe M, Willem Borst J, Goldbach R, Kormelink R. 2007. Tomato spotted wilt virus Gc and N proteins interact in vivo. Virology 357:115-123.
46. Soares-Weiser K, Thomas S, Thomson G, Garner P. 2010. Ribavirin for Crimean-Congo hemorrhagic fever: systematic review and meta-analysis. BMC Infect. Dis. 10:207.
47. Swanepoel R, et al. 1987. Epidemiologic and clinical features of Crimean-Congo hemorrhagic fever in southern Africa. Am. J. Trop. Med. Hyg. 36:120-132.
48. Thompson JD, Higgins DG, Gibson TJ. 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.
49. Unni S, et al. 2011. Web servers and services for electrostatics calculations with APBS and PDB2PQR. J. Comput. Chem. 32:1488-1491.
50. Vieth S, Torda AE, Asper M, Schmitz H, Gunther S. 2004. Sequence analysis of L RNA of Lassa virus. Virology 318:153-168.
51. Vincent MJ, et al. 2003. Crimean-Congo hemorrhagic fever virus glycoprotein proteolytic processing by subtilase SKI-1. J. Virol. 77:8640-8649.
52. Vonrhein C, Blanc E, Roversi P, Bricogne G. 2007. Automated structure solution with autoSHARP. Methods Mol. Biol. 364:215-230.
53. Zhirnov OP, Konakova TE, Garten W, Klenk H. 1999. Caspasedependent N-terminal cleavage of influenza virus nucleocapsid protein in infected cells. J. Virol. 73:10158-10163.
54. Zhirnov OP, Syrtzev VV. 2009. Influenza virus pathogenicity is determined by caspase cleavage motifs located in the viral proteins. J. Mol. Genet. Med. 3:124-132.
55. Zhou Q, et al. 1997. Target protease specificity of the viral serpin CrmA. Analysis of five caspases. J. Biol. Chem. 272:7797-7800.