Nonstructural Protein NSs of Schmallenberg Virus Is Targeted to the Nucleolus and Induces Nucleolar Disorganization

Overview

Journal J Virol

Publisher American Society for Microbiology

Date 2016 Nov 1

PMID 27795408

Citations 17

Authors

Julie Gouzil

Aurore Fablet

Estelle Lara

Gregory Caignard

Marielle Cochet

Cindy Kundlacz

Massimo Palmarini

Mariana Varela

Emmanuel Breard

Corinne Sailleau

Cyril Viarouge

Muriel Coulpier

Stephan Zientara

Damien Vitour

Affiliations

Soon will be listed here.

Abstract

Importance: Schmallenberg virus (SBV) is an emerging arbovirus of ruminants that spread in Europe between 2011 and 2013. SBV induces fetal abnormalities during gestation, with the central nervous system being one of the most affected organs. The virus-encoded NSs protein acts as a virulence factor by impairing host cell transcription. Here, we show that NSs contains a nucleolar localization signal (NoLS) and induces disorganization of the nucleolus. The NoLS motif in the SBV NSs is absolutely necessary for virus-induced inhibition of cellular transcription. To our knowledge, this is the first report of nucleolar functions for NSs within the Bunyaviridae family.

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References

Doceul V, Lara E, Sailleau C, Belbis G, Richardson J, Breard E . Epidemiology, molecular virology and diagnostics of Schmallenberg virus, an emerging orthobunyavirus in Europe. Vet Res. 2013; 44:31. PMC: 3663787. DOI: 10.1186/1297-9716-44-31. View

Blakqori G, Delhaye S, Habjan M, Blair C, Sanchez-Vargas I, Olson K . La Crosse bunyavirus nonstructural protein NSs serves to suppress the type I interferon system of mammalian hosts. J Virol. 2007; 81(10):4991-9. PMC: 1900204. DOI: 10.1128/JVI.01933-06. View

De Regge N, Deblauwe I, De Deken R, Vantieghem P, Madder M, Geysen D . Detection of Schmallenberg virus in different Culicoides spp. by real-time RT-PCR. Transbound Emerg Dis. 2012; 59(6):471-5. DOI: 10.1111/tbed.12000. View

Kraatz F, Wernike K, Hechinger S, Konig P, Granzow H, Reimann I . Deletion mutants of Schmallenberg virus are avirulent and protect from virus challenge. J Virol. 2014; 89(3):1825-37. PMC: 4300748. DOI: 10.1128/JVI.02729-14. View

Weber F, Bridgen A, Fazakerley J, Streitenfeld H, Kessler N, Randall R . Bunyamwera bunyavirus nonstructural protein NSs counteracts the induction of alpha/beta interferon. J Virol. 2002; 76(16):7949-55. PMC: 155133. DOI: 10.1128/jvi.76.16.7949-7955.2002. View

Vitour D, Dabo S, Ahmadi Pour M, Vilasco M, Vidalain P, Jacob Y . Polo-like kinase 1 (PLK1) regulates interferon (IFN) induction by MAVS. J Biol Chem. 2009; 284(33):21797-21809. PMC: 2755906. DOI: 10.1074/jbc.M109.018275. View

Verbruggen P, Ruf M, Blakqori G, Overby A, Heidemann M, Eick D . Interferon antagonist NSs of La Crosse virus triggers a DNA damage response-like degradation of transcribing RNA polymerase II. J Biol Chem. 2010; 286(5):3681-92. PMC: 3030371. DOI: 10.1074/jbc.M110.154799. View

Marquez-Lona E, Tan Z, Schreiber S . Nucleolar stress characterized by downregulation of nucleophosmin: a novel cause of neuronal degeneration. Biochem Biophys Res Commun. 2011; 417(1):514-20. PMC: 3259220. DOI: 10.1016/j.bbrc.2011.11.152. View

Hoffmann B, Scheuch M, Hoper D, Jungblut R, Holsteg M, Schirrmeier H . Novel orthobunyavirus in Cattle, Europe, 2011. Emerg Infect Dis. 2012; 18(3):469-72. PMC: 3309600. DOI: 10.3201/eid1803.111905. View

10.

Rasmussen L, Kristensen B, Kirkeby C, Rasmussen T, Belsham G, Bodker R . Culicoids as vectors of Schmallenberg virus. Emerg Infect Dis. 2012; 18(7):1204-6. PMC: 3376822. DOI: 10.3201/eid1807.120385. View

11.

Brnic D, Stevanovic V, Cochet M, Agier C, Richardson J, Montero-Menei C . Borna disease virus infects human neural progenitor cells and impairs neurogenesis. J Virol. 2011; 86(5):2512-22. PMC: 3302287. DOI: 10.1128/JVI.05663-11. View

12.

Varela M, Pinto R, Caporale M, Piras I, Taggart A, Seehusen F . Mutations in the Schmallenberg Virus Gc Glycoprotein Facilitate Cellular Protein Synthesis Shutoff and Restore Pathogenicity of NSs Deletion Mutants in Mice. J Virol. 2016; 90(11):5440-5450. PMC: 4934738. DOI: 10.1128/JVI.00424-16. View

13.

Scott M, Troshin P, Barton G . NoD: a Nucleolar localization sequence detector for eukaryotic and viral proteins. BMC Bioinformatics. 2011; 12:317. PMC: 3166288. DOI: 10.1186/1471-2105-12-317. View

14.

Banerjee R, Weidman M, Navarro S, Comai L, Dasgupta A . Modifications of both selectivity factor and upstream binding factor contribute to poliovirus-mediated inhibition of RNA polymerase I transcription. J Gen Virol. 2005; 86(Pt 8):2315-2322. DOI: 10.1099/vir.0.80817-0. View

15.

Cautain B, Hill R, de Pedro N, Link W . Components and regulation of nuclear transport processes. FEBS J. 2014; 282(3):445-62. PMC: 7163960. DOI: 10.1111/febs.13163. View

16.

Chase A, Semler B . Viral subversion of host functions for picornavirus translation and RNA replication. Future Virol. 2013; 7(2):179-191. PMC: 3535308. DOI: 10.2217/fvl.12.2. View

17.

Hetman M, Pietrzak M . Emerging roles of the neuronal nucleolus. Trends Neurosci. 2012; 35(5):305-14. PMC: 3348388. DOI: 10.1016/j.tins.2012.01.002. View

18.

Kitani H, Yamakawa M, Ikeda H . Preferential infection of neuronal and astroglia cells by Akabane virus in primary cultures of fetal bovine brain. Vet Microbiol. 2000; 73(4):269-79. DOI: 10.1016/s0378-1135(00)00158-9. View

19.

Aminev A, Amineva S, Palmenberg A . Encephalomyocarditis virus (EMCV) proteins 2A and 3BCD localize to nuclei and inhibit cellular mRNA transcription but not rRNA transcription. Virus Res. 2003; 95(1-2):59-73. DOI: 10.1016/s0168-1702(03)00163-1. View

20.

Rikkonen M, Peranen J, Kaariainen L . Nuclear and nucleolar targeting signals of Semliki Forest virus nonstructural protein nsP2. Virology. 1992; 189(2):462-73. DOI: 10.1016/0042-6822(92)90570-f. View