Ebolavirus VP35 coats the backbone of double-stranded RNA for interferon antagonism

Journal of Virology

Volumn 87, Issue 18, 2013, Pages 10385-10388

  Bale, Shridhar ^a   Julien, Jean Philippe ^a   Bornholdt, Zachary A ^a   Krois, Alexander S ^a   Wilson, Ian A ^a   Saphire, Erica Ollmann ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COAT PROTEIN; DOUBLE STRANDED RNA; INTERFERON; PATTERN RECOGNITION RECEPTOR; PROTEIN VP35; RETINOIC ACID INDUCIBLE PROTEIN I; UNCLASSIFIED DRUG; VIRUS RNA;

ARTICLE; BETA SHEET; BINDING AFFINITY; CRYSTAL STRUCTURE; EBOLA VIRUS; HOST CELL; INTERFERON PRODUCTION; MARBURG VIRUS; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; RESTON VIRUS; RNA BINDING; RNA CAPPING; RNA STRUCTURE; SIGNAL TRANSDUCTION; STRAIN DIFFERENCE; VIRUS ATTACHMENT; VIRUS MORPHOLOGY; VIRUS STRAIN;

CRYSTALLOGRAPHY, X-RAY; EBOLAVIRUS; INTERFERONS; MARBURGVIRUS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; RNA, DOUBLE-STRANDED; RNA, VIRAL; VIRAL REGULATORY AND ACCESSORY PROTEINS;

EID: 84883301490     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01452-13     Document Type: Article

References (29)

1. Bale S, Julien JP, Bornholdt ZA, Kimberlin CR, Halfmann P, Zandonatti MA, Kunert J, Kroon GJ, Kawaoka Y, Macrae IJ, Wilson IA, Saphire EO. 2012. Marburg virus VP35 can both fully coat the backbone and cap the ends of dsRNA for interferon antagonism. PLoS Pathog. 8:e1002916. doi:10.1371/journal.ppat.1002916.
2. Chao JA, Lee JH, Chapados BR, Debler EW, Schneemann A, Williamson JR. 2005. Dual modes of RNA-silencing suppression by Flock House virus protein B2. Nat. Struct. Mol. Biol. 12:952-957.
3. Cheng A, Wong SM, Yuan YA. 2009. Structural basis for dsRNA recognition by NS1 protein of influenza A virus. Cell Res. 19:187-195.
4. Kimberlin CR, Bornholdt ZA, Li S, Woods VL, Jr, MacRae IJ, Saphire EO. 2010. Ebolavirus VP35 uses a bimodal strategy to bind dsRNA for innate immune suppression. Proc. Natl. Acad. Sci. U. S. A. 107:314-319.
5. Leung DW, Prins KC, Borek DM, Farahbakhsh M, Tufariello JM, Ramanan P, Nix JC, Helgeson LA, Otwinowski Z, Honzatko RB, Basler CF, Amarasinghe GK. 2010. Structural basis for dsRNA recognition and interferon antagonism by Ebola VP35. Nat. Struct. Mol. Biol. 17:165-172.
6. Masliah G, Barraud P, Allain FH. 2013. RNA recognition by doublestranded RNA binding domains: a matter of shape and sequence. Cell. Mol. Life Sci. 70:1875-1895.
7. Vargason JM, Szittya G, Burgyan J, Hall TM. 2003. Size selective recognition of siRNA by an RNA silencing suppressor. Cell 115:799-811.
8. Baize S, Leroy EM, Georges-Courbot MC, Capron M, Lansoud-Soukate J, Debre P, Fisher-Hoch SP, McCormick JB, Georges AJ. 1999. Defective humoral responses and extensive intravascular apoptosis are associated with fatal outcome in Ebola virus-infected patients. Nat. Med. 5:423-426.
9. Leroy EM, Baize S, Volchkov VE, Fisher-Hoch SP, Georges-Courbot MC, Lansoud-Soukate J, Capron M, Debre P, McCormick JB, Georges AJ. 2000. Human asymptomatic Ebola infection and strong inflammatory response. Lancet 355:2210-2215.
10. Mahanty S, Gupta M, Paragas J, Bray M, Ahmed R, Rollin PE. 2003. Protection from lethal infection is determined by innate immune responses in a mouse model of Ebola virus infection. Virology 312:415-424.
11. Kuhn JH, Bao Y, Bavari S, Becker S, Bradfute S, Brister JR, Bukreyev AA, Chandran K, Davey RA, Dolnik O, Dye JM, Enterlein S, Hensley LE, Honko AN, Jahrling PB, Johnson KM, Kobinger G, Leroy EM, Lever MS, Muhlberger E, Netesov SV, Olinger GG, Palacios G, Patterson JL, Paweska JT, Pitt L, Radoshitzky SR, Saphire EO, Smither SJ, Swanepoel R, Towner JS, van der Groen G, Volchkov VE, Wahl-Jensen V, Warren TK, Weidmann M, Nichol ST. 2013. Virus nomenclature below the species level: a standardized nomenclature for natural variants of viruses assigned to the family Filoviridae. Arch. Virol. 158:301-311.
12. Cárdenas WB, Loo YM, Gale M, Jr, Hartman AL, Kimberlin CR, Martinez-Sobrido L, Saphire EO, Basler CF. 2006. Ebola virus VP35 protein binds double-stranded RNA and inhibits alpha/beta interferon production induced by RIG-I signaling. J. Virol. 80:5168-5178.
13. Basler CF, Mikulasova A, Martinez-Sobrido L, Paragas J, Muhlberger E, Bray M, Klenk HD, Palese P, Garcia-Sastre A. 2003. The Ebola virus VP35 protein inhibits activation of interferon regulatory factor 3. J. Virol. 77:7945-7956.
14. Haasnoot J, de Vries W, Geutjes EJ, Prins M, de Haan P, Berkhout B. 2007. The Ebola virus VP35 protein is a suppressor ofRNAsilencing. PLoS Pathog. 3:e86. doi:10.1371/journal.ppat.0030086.
15. Johnson RF, McCarthy SE, Godlewski PJ, Harty RN. 2006. Ebola virus VP35-VP40 interaction is sufficient for packaging 3E-5E minigenome RNA into virus-like particles. J. Virol. 80:5135-5144.
16. Leung DW, Prins KC, Basler CF, Amarasinghe GK. 2010. Ebolavirus VP35 is a multifunctional virulence factor. Virulence 1:526-531.
17. Bale S, Dias JM, Fusco ML, Hashiguchi T, Wong AC, Liu T, Keuhne AI, Li S, Woods VL, Jr, Chandran K, Dye JM, Saphire EO. 2012. Structural basis for differential neutralization of ebolaviruses. Viruses 4:447-470.
18. Leung DW, Ginder ND, Fulton DB, Nix J, Basler CF, Honzatko RB, Amarasinghe GK. 2009. Structure of the Ebola VP35 interferon inhibitory domain. Proc. Natl. Acad. Sci. U. S. A. 106:411-416.
19. Leung DW, Shabman RS, Farahbakhsh M, Prins KC, Borek DM, Wang T, Muhlberger E, Basler CF, Amarasinghe GK. 2010. Structural and functional characterization of Reston Ebola virus VP35 interferon inhibitory domain. J. Mol. Biol. 399:347-357.
20. Ramanan P, Edwards MR, Shabman RS, Leung DW, Endlich-Frazier AC, Borek DM, Otwinowski Z, Liu G, Huh J, Basler CF, Amarasinghe GK. 2012. Structural basis for Marburg virus VP35-mediated immune evasion mechanisms. Proc. Natl. Acad. Sci. U. S. A. 109:20661-20666.
21. Berke IC, Li Y, Modis Y. 2013. Structural basis of innate immune recognition of viral RNA. Cell. Microbiol. 15:386-394.
22. Binder M, Eberle F, Seitz S, Mucke N, Huber CM, Kiani N, Kaderali L, Lohmann V, Dalpke A, Bartenschlager R. 2011. Molecular mechanism of signal perception and integration by the innate immune sensor retinoic acid-inducible gene-I (RIG-I). J. Biol. Chem. 286:27278-27287.
23. Peisley A, Lin C, Wu B, Orme-Johnson M, Liu M, Walz T, Hur S. 2011. Cooperative assembly and dynamic disassembly of MDA5 filaments for viral dsRNA recognition. Proc. Natl. Acad. Sci. U. S. A. 108:21010-21015.
24. Pflugrath JW. 1999. The finer things in X-ray diffraction data collection. Acta Crystallogr. D Biol. Crystallogr. 55:1718-1725.
25. Collaborative Computational Project, Number 4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. 50(Pt 5):760-763.
26. Vagin A, Teplyakov A. 1997. MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30:1022-1025.
27. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung L-W, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2010. PHENIX: a comprehensive Pythonbased system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66:213-221.
28. Emsley P, Cowtan K. 2004. COOT: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132.
29. de Azevedo WF, Jr, Dias R. 2008. Experimental approaches to evaluate the thermodynamics of protein-drug interactions. Curr. Drug Targets 9:1071-1076.