A virus-like particle system identifies the endonuclease domain of Crimean-Congo hemorrhagic fever virus

Journal of Virology

Volumn 89, Issue 11, 2015, Pages 5957-5967

  Devignot, Stephanie ^a   Bergeron, Eric ^b   Nichol, Stuart ^b   Mirazimi, Ali ^c,d,e   Weber, Friedemann ^a,f  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^c SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

^d NATIONAL VETERINARY INSTITUTE   (Sweden)

^e KAROLINSKA INSTITUTE   (Sweden)

^f JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ENDONUCLEASE; GLYCOPROTEIN; RNA DIRECTED RNA POLYMERASE; VIRUS ANTIBODY; DNA DIRECTED RNA POLYMERASE; NUCLEOCAPSID PROTEIN; VIRAL PROTEIN; VIROSOME;

AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; CRIMEAN CONGO HEMORRHAGIC FEVER VIRUS; GENE REPLICATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN STABILITY; REPORTER GENE; VIRUS ATTACHMENT; VIRUS ENTRY; VIRUS PARTICLE; VIRUS REPLICATION; CELL LINE; ENZYMOLOGY; GENE EXPRESSION; GENETICS; LIVER CELL; METABOLISM; NAIROVIRUS; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; VIROLOGY; VIRUS ASSEMBLY;

BUNYAVIRIDAE; CRIMEAN-CONGO HEMORRHAGIC FEVER VIRUS; NAIROVIRUS;

CELL LINE; DNA-DIRECTED RNA POLYMERASES; ENDONUCLEASES; GENE EXPRESSION; GENES, REPORTER; HEMORRHAGIC FEVER VIRUS, CRIMEAN-CONGO; HEPATOCYTES; HUMANS; NUCLEOCAPSID PROTEINS; PROTEIN STRUCTURE, TERTIARY; TRANSCRIPTION, GENETIC; VIRAL PROTEINS; VIROSOMES; VIRUS ASSEMBLY; VIRUS ATTACHMENT; VIRUS INTERNALIZATION;

EID: 84929627797     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03691-14     Document Type: Article

References (46)

1. Ergonul O. 2006. Crimean-Congo haemorrhagic fever. Lancet Infect Dis 6:203-214. http://dx.doi.org/10.1016/S1473-3099(06)70435-2.
2. Bente DA, Forrester NL, Watts DM, McAuley AJ, Whitehouse CA, Bray M. 2013. Crimean-Congo hemorrhagic fever: history, epidemiology, pathogenesis, clinical syndrome and genetic diversity. Antiviral Res 100: 159-189. http://dx.doi.org/10.1016/j.antiviral.2013.07.006.
3. Ascioglu S, Leblebicioglu H, Vahaboglu H, Chan KA. 2011. Ribavirin for patients with Crimean-Congo haemorrhagic fever: a systematic review and meta-analysis. J Antimicrob Chemother 66:1215-1222. http://dx.doi.org/10.1093/jac/dkr136.
4. Bereczky S, Lindegren G, Karlberg H, Akerstrom S, Klingstrom J, Mirazimi A. 2010. Crimean-Congo hemorrhagic fever virus infection is lethal for adult type I interferon receptor-knockout mice. J Gen Virol 91:1473-1477. http://dx.doi.org/10.1099/vir.0.019034-0.
5. Bente DA, Alimonti JB, Shieh WJ, Camus G, Stroher U, Zaki S, Jones SM. 2010. Pathogenesis and immune response of Crimean-Congo hemorrhagic fever virus in a STAT-1 knockout mouse model. J Virol 84: 11089-11100. http://dx.doi.org/10.1128/JVI.01383-10.
6. Flick R, Flick K, Feldmann H, Elgh F. 2003. Reverse genetics for Crimean-Congo hemorrhagic fever virus. J Virol 77:5997-6006. http://dx.doi.org/10.1128/JVI.77.10.5997-6006.2003.
7. Elliott RM, Weber F. 2009. Bunyaviruses and the type I interferon system. Viruses 1:1003-1021. http://dx.doi.org/10.3390/v1031003.
8. Hoenen T, Groseth A, de Kok-Mercado F, Kuhn JH, Wahl-Jensen V. 2011. Minigenomes, transcription and replication competent virus-like particles and beyond: reverse genetics systems for filoviruses and other negative stranded hemorrhagic fever viruses. Antiviral Res 91:195-208. http://dx.doi.org/10.1016/j.antiviral.2011.06.003.
9. Dunn EF, Pritlove DC, Jin H, Elliott RM. 1995. Transcription of a recombinant bunyavirus RNA template by transiently expressed bunyavirus proteins. Virology 211:133-143. http://dx.doi.org/10.1006/viro.1995.1386.
10. Flick R, Pettersson RF. 2001. Reverse genetics system for Uukuniemi virus (Bunyaviridae): RNA polymerase I-catalyzed expression of chimeric viral RNAs. J Virol 75:1643-1655. http://dx.doi.org/10.1128/JVI.75.4.1643-1655.2001.
11. Flick K, Hooper JW, Schmaljohn CS, Pettersson RF, Feldmann H, Flick R. 2003. Rescue of Hantaan virus minigenomes. Virology 306:219-224. http://dx.doi.org/10.1016/S0042-6822(02)00070-3.
12. Ikegami T, Peters CJ, Makino S. 2005. Rift Valley fever virus nonstructural protein NSs promotes viral RNA replication and transcription in a minigenome system. J Virol 79:5606-5615. http://dx.doi.org/10.1128/JVI.79.9.5606-5615.2005.
13. Blakqori G, Kochs G, Haller O, Weber F. 2003. Functional L polymerase of La Crosse virus allows in vivo reconstitution of recombinant nucleocapsids. J Gen Virol 84:1207-1214. http://dx.doi.org/10.1099/vir.0.18876-0.
14. 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. http://dx.doi.org/10.1128/JVI.01859-09.
15. Barr JN, Rodgers JW, Wertz GW. 2006. Identification of the Bunyamwera bunyavirus transcription termination signal. J Gen Virol 87:189-198. http://dx.doi.org/10.1099/vir.0.81355-0.
16. Flick K, Katz A, Overby A, Feldmann H, Pettersson RF, Flick R. 2004. Functional analysis of the noncoding regions of the Uukuniemi virus (Bunyaviridae) RNA segments. J Virol 78:11726-11738. http://dx.doi.org/10.1128/JVI.78.21.11726-11738.2004.
17. Kohl A, Dunn EF, Lowen AC, Elliott RM. 2004. Complementarity, sequence and structural elements within the 3' and 5' non-coding regions of the Bunyamwera orthobunyavirus S segment determine promoter strength. J Gen Virol 85:3269-3278. http://dx.doi.org/10.1099/vir.0.80407-0.
18. Habjan M, Penski N, Wagner V, Spiegel M, Overby AK, Kochs G, Huiskonen JT, 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. http://dx.doi.org/10.1016/j.virol.2008.12.011.
19. 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. J Virol 77:10700-10705. http://dx.doi.org/10.1128/JVI.77.19.10700-10705.2003.
20. Watanabe S, Watanabe T, Noda T, Takada A, Feldmann H, Jasenosky LD, Kawaoka Y. 2004. Production of novel Ebola virus-like particles from cDNAs: an alternative to Ebola virus generation by reverse genetics. J Virol 78:999-1005. http://dx.doi.org/10.1128/JVI.78.2.999-1005.2004.
21. Morin B, Coutard B, Lelke M, Ferron F, Kerber R, Jamal S, Frangeul A, Baronti C, Charrel R, de Lamballerie X, Vonrhein C, Lescar J, Bricogne G, Gunther S, Canard B. 2010. The N-terminal domain of the arenavirus L protein is an RNA endonuclease essential in mRNA transcription. PLoS Pathog 6:e1001038. http://dx.doi.org/10.1371/journal.ppat.1001038.
22. Klemm C, Reguera J, Cusack S, Zielecki F, Kochs G, Weber F. 2013. Systems to establish bunyavirus genome replication in the absence of transcription. J Virol 87:8205-8212. http://dx.doi.org/10.1128/JVI.00371-13.
23. Sanchez AJ, Vincent MJ, Nichol ST. 2002. Characterization of the glycoproteins of Crimean-Congo hemorrhagic fever virus. J Virol 76:7263-7275. http://dx.doi.org/10.1128/JVI.76.14.7263-7275.2002.
24. Habjan M, Penski N, Spiegel M, Weber F. 2008. T7 RNA polymerasedependent and-independent systems for cDNA-based rescue of Rift Valley fever virus. J Gen Virol 89:2157-2166. http://dx.doi.org/10.1099/vir.0.2008/002097-0.
25. Simon M, Falk KI, Lundkvist A, Mirazimi A. 2006. Exogenous nitric oxide inhibits Crimean Congo hemorrhagic fever virus. Virus Res 120: 184-190. http://dx.doi.org/10.1016/j.virusres.2006.03.005.
26. Bergeron E, Vincent MJ, Nichol ST. 2007. Crimean-Congo hemorrhagic fever virus glycoprotein processing by the endoprotease SKI-1/S1P is critical for virus infectivity. J Virol 81:13271-13276. http://dx.doi.org/10.1128/JVI.01647-07.
27. Kortekaas J, Oreshkova N, Cobos-Jimenez V, Vloet RP, Potgieter CA, Moormann RJ. 2011. Creation of a nonspreading Rift Valley fever virus. J Virol 85:12622-12630. http://dx.doi.org/10.1128/JVI.00841-11.
28. Howell CL, Miller MJ. 1983. Effect of sucrose phosphate and sorbitol on infectivity of enveloped viruses during storage. J Clin Microbiol 18:658-662.
29. Kissmann J, Joshi SB, Haynes JR, Dokken L, Richardson C, Middaugh CR. 2011. H1N1 influenza virus-like particles: physical degradation pathways and identification of stabilizers. J Pharm Sci 100:634-645. http://dx.doi.org/10.1002/jps.22304.
30. Dias A, Bouvier D, Crepin T, McCarthy AA, Hart DJ, Baudin F, Cusack S, Ruigrok RW. 2009. The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 458:914-918. http://dx.doi.org/10.1038/nature07745.
31. Yuan P, Bartlam M, Lou Z, Chen S, Zhou J, He X, Lv Z, Ge R, Li X, Deng T, Fodor E, Rao Z, Liu Y. 2009. Crystal structure of an avian influenza polymerase PA(N) reveals an endonuclease active site. Nature 458:909-913. http://dx.doi.org/10.1038/nature07720.
32. Reguera J, Weber F, 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. http://dx.doi.org/10.1371/journal.ppat.1001101.
33. Frias-Staheli N, Giannakopoulos NV, Kikkert M, Taylor SL, Bridgen A, Paragas J, Richt JA, Rowland RR, Schmaljohn CS, Lenschow DJ, Snijder EJ, Garcia-Sastre A, Virgin HWt. 2007. Ovarian tumor domaincontaining viral proteases evade ubiquitin-and ISG15-dependent innate immune responses. Cell Host Microbe 2:404-416. http://dx.doi.org/10.1016/j.chom.2007.09.014.
34. Hoenen T, Groseth A, Kolesnikova L, Theriault S, Ebihara H, Hartlieb B, Bamberg S, Feldmann H, Stroher U, Becker S. 2006. Infection of naive target cells with virus-like particles: implications for the function of Ebola virus VP24. J Virol 80:7260-7264. http://dx.doi.org/10.1128/JVI.00051-06.
35. Wenigenrath J, Kolesnikova L, Hoenen T, Mittler E, Becker S. 2010. Establishment and application of an infectious virus-like particle system for Marburg virus. J Gen Virol 91:1325-1334. http://dx.doi.org/10.1099/vir.0.018226-0.
36. Kohl A, Lowen AC, Leonard VH, Elliott RM. 2006. Genetic elements regulating packaging of the Bunyamwera orthobunyavirus genome. J Gen Virol 87:177-187. http://dx.doi.org/10.1099/vir.0.81227-0.
37. Zhao J, Xia H, Zhang Y, Yin S, Zhang Z, Tang S, Kou Z, Yu J, Fan Z, Li T. 2013. Mini-genome rescue of Crimean-Congo hemorrhagic fever virus and research into the evolutionary patterns of its untranslated regions. Virus Res 177:22-34. http://dx.doi.org/10.1016/j.virusres.2013.07.005.
38. Weber M, Gawanbacht A, Habjan M, Rang A, Borner C, Schmidt AM, Veitinger S, Jacob R, Devignot S, Kochs G, Garcia-Sastre A, Weber F. 2013. Incoming RNA virus nucleocapsids containing a 5'-triphosphorylated genome activate RIG-I and antiviral signaling. Cell Host Microbe 13:336-346. http://dx.doi.org/10.1016/j.chom.2013.01.012.
39. Habjan M, Andersson I, Klingstrom J, Schumann M, Martin A, Zimmermann P, Wagner V, Pichlmair A, Schneider U, Muhlberger E, Mirazimi A, Weber F. 2008. Processing of genome 5' termini as a strategy of negative-strand RNA viruses to avoid RIG-I-dependent interferon induction. PLoS One 3:e2032. http://dx.doi.org/10.1371/journal.pone.0002032.
40. Andersson I, Bladh L, Mousavi-Jazi M, Magnusson KE, Lundkvist A, Haller O, Mirazimi A. 2004. Human MxA protein inhibits the replication of Crimean-Congo hemorrhagic fever virus. J Virol 78:4323-4329. http://dx.doi.org/10.1128/JVI.78.8.4323-4329.2004.
41. Ke RQ, Zorzet A, Goransson J, Lindegren G, Sharifi-Mood B, Chinikar S, Mardani M, Mirazimi A, Nilsson M. 2011. Colorimetric nucleic acid testing assay for RNA virus detection based on circle-to-circle amplification of padlock probes. J Clin Microbiol 49:4279-4285. http://dx.doi.org/10.1128/JCM.00713-11.
42. Drosten C, Kummerer BM, Schmitz H, Gunther S. 2003. Molecular diagnostics of viral hemorrhagic fevers. Antiviral Res 57:61-87. http://dx.doi.org/10.1016/S0166-3542(02)00201-2.
43. Burt FJ, Leman PA, Smith JF, Swanepoel R. 1998. The use of a reverse transcription-polymerase chain reaction for the detection of viral nucleic acid in the diagnosis of Crimean-Congo haemorrhagic fever. J Virol Methods 70:129-137. http://dx.doi.org/10.1016/S0166-0934(97)00182-1.
44. Ibrahim SM, Aitichou M, Hardick J, Blow J, O'Guinn ML, Schmaljohn C. 2011. Detection of Crimean-Congo hemorrhagic fever, Hanta, and sandfly fever viruses by real-time RT-PCR. Methods Mol Biol 665:357-368. http://dx.doi.org/10.1007/978-1-60761-817-1_19.
45. Duh D, Saksida A, Petrovec M, Dedushaj I, Avsic-Zupanc T. 2006. Novel one-step real-time RT-PCR assay for rapid and specific diagnosis of Crimean-Congo hemorrhagic fever encountered in the Balkans. J Virol Methods 133:175-179. http://dx.doi.org/10.1016/j.jviromet.2005.11.006.
46. Shepherd AJ, Swanepoel R, Leman PA. 1989. Antibody response in Crimean-Congo hemorrhagic fever. Rev Infect Dis 11(Suppl 4):S801-S806. http://dx.doi.org/10.1093/clinids/11.Supplement_4.S801.