DsRNA binding characterization of full length recombinant wild type and mutants Zaire ebolavirus VP35

Antiviral Research

Volumn 93, Issue 3, 2012, Pages 354-363

  Zinzula, Luca ^a   Esposito, Francesca ^a   Pala, Daniela ^a   Tramontano, Enzo ^a  

^a UNIVERSITY OF CAGLIARI   (Italy)

Author keywords

Biochemical screening assay; DsRNA binding; Ebola virus; VP35

Indexed keywords

AURYNTRICARBOXYLIC ACID; CARBOXYLIC ACID; UNCLASSIFIED DRUG; VIRUS RNA;

ARTICLE; ASSAY; EBOLA VIRUS; IN VITRO STUDY; MAGNETIC PULL DOWN ASSAY; NONHUMAN; PRIORITY JOURNAL; RNA BINDING; SCREENING; TEMPERATURE; VIRUS CHARACTERIZATION; VIRUS ISOLATION; WILD TYPE; ZAIRE EBOLAVIRUS;

EBOLAVIRUS; HEMORRHAGIC FEVER, EBOLA; KINETICS; MUTATION; PROTEIN BINDING; RNA, DOUBLE-STRANDED; VIRAL REGULATORY AND ACCESSORY PROTEINS;

EBOLA VIRUS; ZAIRE EBOLAVIRUS;

EID: 84857948331     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2012.01.005     Document Type: Article

References (78)

1. Barrette R.W., Metwally S.A., Rowland J.M., Xu L., Zaki S.R., Nichol S.T., Rollin P.E., Towner J.S., Shieh W.-J., Batten B., Sealy T.K., Carrillo C., Moran K.E., Bracht A.J., Mayr G.A., Sirios-Cruz M., Cathagan D.P., Lautner E.A., Ksiazek T.G., White W.R., McIntosh M.T. Discovery of Swine as a host for the Reston ebolavirus. Science 2009, 325:204-206.
2. Barrette, R.W., Xu, L., Rowland, J.M., McIntosh, M.T., in press. Current perspectives on the phylogeny of Filoviridae. Infect. Genet. Evol. doi: doi:10.1016/j.meegid.2011.06.017.
3. Basler C.F., Wuang X., Mühlberger E., Volchkov V., Paragas J., Klenk H.-D., Garcia-Sastre A., Palese P. The Ebola virus VP35 protein functions as a type I IFN antagonist. Proc. Natl. Acad. Sci. USA 2000, 97:12289-12294.
4. Basler C.F., Mikulasova A., Martinez-Sobrido L., Paragas J., Mühlberger E., Bray M., Klenk H.-D., Palese P., Garcia-Sastre A. The Ebola virus VP35 protein inhibits activation of interferon regulatory factor 3. J. Virol. 2003, 77:7945-7956.
5. Basler C.F., Amarasinghe G.K. Evasion of interferon responses by Ebola and Marburg viruses. J. Interferon Cytokine Res. 2009, 29:511-520.
6. Becquart P., Wauquier N., Mahlakõv T., Nkoghe D., Padilla C., Souris M., Ollomo B., Gonzales J.-P., De Lamballerie X., Kazanji M., Leroy E.M. High prevalence of both humoral and cellular immunity to Zaire ebolavirus among rural populations in Gabon. PLoS One 2010, 5:e9126.
7. Boehmann Y., Enterlein S., Randolf A., Mühlberger E. A reconstituted replication and transcription system for Ebola virus Reston and comparison with Ebola virus Zaire. Virology 2005, 332:406-417.
8. Bowie A.G., Unterholzner L. Viral evasion and subversion of pattern-recognition receptor signaling. Nat. Rev. Immunol. 2008, 8:911-922.
9. Bylund D.B., Murrin L.C. Radioligand saturation binding experiments over large concentration ranges. Life Sci. 2000, 67:2897-2911.
10. Cárdenas W.B., Loo Y.M., Gale M., Hartman A.L., Kimberlin C.R., Martinez-Sobrido L., Saphire E.O., Basler C.F. Ebola virus VP35 protein binds double-stranded RNA and inhibits alpha/beta interferon production induced by RIG-I signaling. J. Virol. 2006, 80:5168-5178.
11. Chang T.H., Kubota T., Matsuoka M., Jones S., Bradfute S.B., Bray M., Ozato K. Ebola Zaire virus blocks type I interferon production by exploiting the host SUMO modification machinery. PLoS Pathog. 2009, 5:e1000493.
12. Chen Y., Bopda-Waffo A., Basu A., Krishnan R., Silberstein E., Taylor D.R., Talele T.T., Arora P., Kaushik-Basu N. Characterization of aurintricarboxylic acid as a potent hepatitis C virus replicase inhibitor. Antivir. Chem. Chemother. 2009, 20:19-36.
13. Chien C., Xu Y., Xiao R., Aramini J.M., Sahasrabudhe P.V., Krug R.M., Montelione G.T. Biophysical characterization of the complex between double-stranded RNA and the N-terminal domain of the NS1 protein from influenza A virus: evidence for a novel RNA-binding mode. Biochemistry 2004, 43:1950-1962.
14. Chung S., Wendeler M., Rausch J.W., Beilhartz G., Gotte M., O'Keefe B.R., Bermingham A., Beutler J.A., Liu S., Zhuang X., Le Grice S.F. Structure-activity analysis of vinylogous urea inhibitors of human immunodeficiency virus-encoded ribonuclease H. Antimicrob. Agents Chemother. 2010, 54:3913-3921.
15. Conzelmann K.K. Transcriptional activation of alpha/beta interferon genes: interference by non segmented negative-stranded RNA viruses. J. Virol. 2005, 79:5241-5248.
16. Cushman M., Sherman P. Inhibition of HIV-1 integration protein by aurintricarboxylic acid monomers, monomer analogs, and polymer fractions. Biochim. Biophys. Res. Commun. 1992, 185:85-90.
17. Enterlein S., Warfield K.L., Swenson D.L., Stein D.A., Smith J.L., Gamble C.S., Kroeker A.D., Iversen P.L., Bavari S., Mühlberger E. VP35 knockdown inhibits Ebola virus amplification and protects against lethal infection in mice. Antimicrob. Agents Chemother. 2006, 50:984-993.
18. Fabozzi G., Nabel C.S., Dolan M.A., Sullivan N.J. Ebolavirus proteins suppress the effects of small interfering RNA by direct interaction with the mammalian RNA interference pathway. J. Virol. 2011, 85:2512-2523.
19. Falzarano D., Geisbert T.W., Feldmann H. Progress in filovirus vaccine development: evaluating the potential for clinical use. Expert. Rev. Vaccines 2011, 10:63-77.
20. Feldmann H., Geisbert T.W. Ebola hemorrhagic fever. Lancet 2011, 377:849-862.
21. Feng Z., Cerveny M., Yan Z., He B. The VP35 protein of Ebola virus inhibits the antiviral effect mediated by double-stranded RNA-dependent protein kinase PKR. J. Virol. 2007, 81:182-192.
22. Geisbert T.W., Lee A.C.H., Robbins M., Geisbert J.B., Honko A.N., Sood V., Johnson J.C., de Jong S., Tavakoli I., Judge A., Hensley L.E., Mac Lachlan I. Post exposure protection of non-human primates against a lethal Ebola virus challenge with RNA interference: a proof of concept study. Lancet 2010, 375:1896-1905.
23. Ghosh U., Giri K., Bhattacharyya N.P. Interaction of auryntricarboxylic acid (ATA) with four nucleic acid proteins DNase I, RNase A, reverse transcriptase and Taq polymerase. Spectrochim. Acta, Part A 2009, 74:1145-1151.
24. Gonzáles R.G., Haxo R.S., Schleich T. Mechanism of action of polymeric auryntricarboxylic acid, a potent inhibitor of protein-nucleic acid interactions. Biochemistry 1980, 19:4299-4303.
25. Haasnoot J., de Vries W., Geutjes E.-J., Prins M., de Haan P., Berkhout P. The Ebola virus VP35 protein is a suppressor of RNA silencing. PLoS Pathog. 2007, 3:e86.
26. Hartman A.L., Towner J.S., Nichol S.T. A C-terminal basic amino acid motif of Zaire ebolavirus VP35 is essential for type I interferon antagonism and displays high identity with the RNA-binding domain of another interferon antagonist, the NS1 protein of influenza A virus. Virology 2004, 328:177-184.
27. Hartman A.L., Dover J.E., Towner J.S., Nichol S.T. Reverse genetic generation of recombinant Zaire Ebola Viruses containing disrupted IRF-3 inhibitory domains results in attenuated virus growth in vitro and higher levels of IRF-3 activation without inhibiting viral transcription or replication. J. Virol. 2006, 80:6430-6440.
28. Hartman A.L., Bird B.H., Towner J.S., Antoniadou Z.-A., Zaki S.R., Nichol S.T. Inhibition of IRF-3 activation by VP35 is critical for the high level of virulence of Ebola virus. J. Virol. 2008, 82:2699-2704.
29. Hartman A.L., Ling L., Nichol S.T., Hibberd M.L. Whole-genome expression profiling reveals that inhibition of host innate immune response pathways by Ebola virus can be reversed by a single amino acid change in the VP35 protein. J. Virol. 2008, 82:5348-5358.
30. Hartman A.L., Towner J.S., Nichol S.T. Ebola and Marburg hemorrhagic fever. Clin. Lab. Med. 2010, 30:161-177.
31. He R., Adonov A., Traykova-Adonova M., Cao J., Cutts T., Grudesky E., Deschambaul Y., Berry J., Drebot M., Li X. Potent and selective inhibition of SARS coronavirus replication by aurintricarboxylic acid. Biochem. Biophys. Res. Commun. 2004, 320:1199-1203.
32. Huang Y., Xu L., Sun Y., Nabel G.J. The assembly of Ebola virus nucleocapsid requires virion-associated proteins 35 and 24 and posttranslational modification of nucleoprotein. Mol. Cell. 2002, 10:307-316.
33. Jin H., Yan Z., Prabakhar B.S., Feng Z., Ma Y., Verpooten D., Ganesh B., He B. The VP35 protein of Ebola virus impairs dendritic cell maturation induced by virus and lipopolysaccharide. J. Gen. Virol. 2010, 91:352-361.
34. John S.P., Wang T., Steffen S., Longhi S., Schmaljohn C.S., Jonsson C.B. VP30 is an RNA binding protein. J. Virol. 2007, 81:8967-8976.
35. Johnson R.F., McCarthy S.E., Godlewski P.J., Harty R.N. Ebola virus VP35-VP40 interaction is sufficient for packaging 3E-5E minigenome RNA into virus-like particles. J. Virol. 2006, 80:5135-5144.
36. Katze M.G., Fornek J.L., Palermo R.E., Walters K.-A., Korth M.J. Innate immune modulation by RNA viruses: emerging insights from functional genomics. Nat. Rev. Immunol. 2008, 8:644-654.
37. Kimberlin C.R., Bornholdt Z.A., Li S., Woods V.L., MacRae I.J., Saphire E.O. Ebolavirus VP35 uses a bimodal strategy to bind dsRNA for innate immune suppression. Proc. Natl. Acad. Sci. USA 2010, 107:314-319.
38. Kobinger G.P., Leung A., Neufeld J., Richardson J.S., Falzarano D., Smith G., Tierney K., Patel A., Weingartl H.M. Replication, pathogenicity, shedding and transmission of Zaire ebolavirus in pigs. J. Infect. Dis. 2011, 204:200-208.
39. Koyama S., Ishii K.J., Coban C., Akira S. Innate immune response to viral infection. Cytokine 2008, 43:336-341.
40. Kuhn J.H., Becker S., Ebihara H., Geisbert T.W., Johnson K.M., Kawaoka Y., Lipkin W.I., Negredo A.I., Netesov S.V., Nichol S.T., Palacios G., Peters C.J., Tenorio A., Volchkov V.E., Jahrling P.B. Proposal for a revised taxonomy of the family Filoviridae: classification, names of taxa and viruses, and virus abbreviations. Arch. Virol. 2010, 155:2083-2103.
41. Lemaire P.A., Anderson E., Lary J., Cole J.L. Mechanism of PKR activation by dsRNA. J. Mol. Biol. 2008, 381:351-360.
42. Leroy E.M., Gonzales J.-P., Baize S. Ebola and Marburg hemorrhagic fever viruses: major scientific advances, but a relatively minor public health threat for Africa. Clin. Microbiol. Infect. 2011, 17:964-976.
43. Leung D.W., Ginder N.D., Fulton D.B., Nix J., Basler C.F., Honzatko R.B., Amarasinghe G.K. Structure of the Ebola VP35 interferon inhibitory domain. Proc. Natl. Acad. Sci. USA 2009, 106:441-446.
44. Leung D.W., Borek D., Farahbakhsh M., Ramanan P., Nix J.C., Wang T., Prins K.C., Otwinowski Z., Honzatko R.B., Helgeson L.A., Basler C.F., Amarasinghe G.K. Crystallization and preliminary X-ray analysis of Ebola VP35 interferon inhibitory domain mutant proteins. Acta Crystallogr. Sect. F: Struct. Biol. Cryst. Commun. 2010, 66:689-692.
45. Leung D.W., Prins K.C., Basler C.F., Amarasinghe G.K. Ebolavirus VP35 is a multifunctional virulence factor. Virulence 2010, 6:526-531.
46. Leung D.W., Prins K.C., Borek D.M., Farahbakhsh M., Tufariello J.M., Ramaman P., Nix J.C., Helgeson L.A., Otwinowski Z., Honzatko R.B., Basler C.F., Amarasinghe G.K. Structural basis for dsRNA recognition and interferon antagonism by Ebola VP35. Nat. Struct. Mol. Biol. 2010, 17:165-172.
47. Leung D.W., Shabman R.S., Farahbakhsh M., Prins K.C., Borek D.M., Wang T., Mühlberger E., Basler C.F., Amarasinghe G.K. Structural and functional characterization of Reston Ebola virus VP35 interferon inhibitory domain. J. Mol. Biol. 2010, 3:347-357.
48. Loo Y.-M., Gale M. Immune signaling by RIG-I-like receptors. Immunity 2011, 34:680-692.
49. Lu C., Ranjith-Kumar C.T., Hao L., ChengKao C., Li P. Crystal structure of RIG-I C-terminal domain bound to blunt-ended double-strand RNA without 5'triphosphate. Nucleic Acids Res. 2010, 39:1565-1575.
50. Mahanty S., Bray M. Pathogenesis of filoviral hemorrhagic fevers. Lancet Infect. Dis. 2004, 4:487-498.
51. Maroto M., Fernandez Y., Ortin J., Pelaez F., Cabello M.A. Development of an HTS assay for the search of anti-influenza agents targeting the interaction of viral RNA with the NS1 protein. J. Biomol. Screen. 2008, 13:581-590.
52. Mohamadzadeh M., Chen L., Schmaljohn A.L. How Ebola and Marburg viruses battle the immune system. Nat. Rev. Immunol. 2007, 7:556-567.
53. Mohamadzadeh M. Potential factors induced by filoviruses that lead to immune suppression. Curr. Mol. Med. 2009, 9:174-185.
54. Möller P., Pariente N., Klenk H.-D., Becker S. Homo-oligomerization of Marburgvirus VP35 is essential for its function in replication and transcription. J. Virol. 2005, 79:14876-14886.
55. Motulsky H.J., Neubig R.R. Analyzing binding data. Curr. Protoc. Neurosci. 2010, 52:751-7565. 10.1002/0471142301.ns0705s52.
56. Mühlberger E., Löftering B., Klenk H.-D., Becker S. Three of the four nucleocapsid proteins of Marburg virus, NP, VP35, and L, are sufficient to mediate replication and transcription of Marburg virus-specific monocistronic minigenomes. J. Virol. 1998, 72:8756-8764.
57. Mühlberger E., Weik M., Volchkov V.E., Klenk H.-D., Becker S. Comparison of the transcription and replication strategies of Marburg virus and Ebola virus by using artificial replication systems. J. Virol. 1999, 73:2333-2342.
58. Prins K.C., Cárdenas W.B., Basler C.F. Ebola virus protein VP35 impairs the function of interferon regulatory factor-activating kinases IKK epsilon and TBK-1. J. Virol. 2009, 83:3069-3077.
59. Prins K.C., Delpeut S., Leung D.W., Reynard O., Volchkova V.A., Reid S.P., Ramanan P., Cárdenas W.B., Amarasinghe G.K., Volchkov V.E., Basler C.F. Mutations abrogating VP35 interactions with double-stranded RNA render Ebola virus avirulent in guinea pigs. J. Virol. 2010, 84:3004-3015.
60. Randall R.E., Goodbourn S. Interferons and viruses: an interplay between induction, signaling, antiviral responses and virus countermeasures. J. Gen. Virol. 2008, 89:1-47.
61. Reed D.S., Lackemeyer M.G., Garza N.L., Sullivan L.J., Nichols D.K. Aerosol exposure to Zaire ebola virus in three non human primate species: differences in disease course and clinical pathology. Microbes Infect. 2011, 13:930-936.
62. Reid S.P., Cárdenas W.B., Basler C.F. Homo-oligomerization facilitates the interferon-antagonist activity of the ebolavirus VP35 protein. Virology 2005, 341:179-189.
63. Sadler A.J., Williams B.R. Interferon-inducible antiviral effectors. Nat. Rev. Immunol. 2008, 8:559-568.
64. Schümann M., Gantke T., Mühlberger E. Ebola virus VP35 antagonizes PKR activity through its C-terminal interferon inhibitory domain. J. Virol. 2009, 83:8993-8997.
65. Severson W., Xu X., Kuhn M., Senutovitch N., Thokala M., Ferron F., Longhi S., Canard B., Jonsson C.B. Essential amino acids of the Hantaan virus N protein in its interaction with RNA. J. Virol. 2005, 79:10032-10039.
66. Shi W., Huang Y., Sutton-Smith M., Tissot B., Panico M., Morris H.R., Dell A., Haslam S.M., Boyington J., Graham B.S., Yang Z.-Y., Nabel G.J. A filovirus-unique region of Ebola virus nucleoprotein confers aberrant migration and mediates its incorporation into virions. J. Virol. 2008, 82:6190-6199.
67. Slice L.W., Codner E., Antelman D., Holly M., Wegrzynski B., Wang J., Toome V., Hsu M.C., Nalin C.M. Characterization of recombinant HIV-1 Tat and its interaction with TAR RNA. Biochemistry 1992, 31:12062-12068.
68. Spiropoulou C.F., Ranjan P., Pearce M.B., Sealy T.K., Albariño C.G., Gangappa S., Fujita T., Rollin P.E., Nichol S.T., Ksiazek T.G., Sambhara S. RIG-I activation inhibits ebola virus replication. Virology 2009, 392:11-15.
69. Tramontano E., La Colla P., Cheng Y.-C. Biochemical characterization of the HIV-1 integrase 3'-processing activity and its inhibition by phosphorothioate oligonucleotides. Biochemistry 1998, 37:7237-7243.
70. Wang Y., Ludwig J., Schuberth C., Goldeck M., Schlee M., Li H., Juranek S., Sheng G., Micura R., Tuschl T., Hartmannand G., Patel D.J. Structural and functional insights into 5'-ppp RNA pattern recognition by the innate immune receptor RIG-I. Nat. Struct. Mol. Biol. 2010, 17:781-787.
71. Warfield K.L., Swenson D.L., Olinger G.G., Nichols D.K., Pratt W.D., Blouch R., Stein D.A., Aman M.J., Iversen P.I., Bavari S. Gene-specific countermeasures against Ebola virus based on antisense phosphorodiamidate morpholino oligomers. PLoS Pathog. 2006, 2:e1.
72. Wauquier N., Becquart P., Gasquet C., Leroy E.M. Immunoglobulin G in Ebola outbreak survivors. Gabon. Emerg. Infect. Dis. 2009, 15:1136-1137.
73. Wauquier N., Becquart P., Padilla C., Baize S., Leroy E.M. Human fatal Zaire Ebola virus infection is associated with an aberrant innate immunity and with massive lymphocyte apoptosis. PLoS Negl. Trop. Dis. 2010, 5:e837.
74. Yap Y., Zhang X., Andonov A., He R. Structural analysis of inhibition mechanisms of aurintricarboxylic acid on SARS-CoV polymerase and other proteins. Comput. Biol. Chem. 2005, 29:212-219.
75. Yoneyama M., Fujita T. Recognition of viral nucleic acids in innate immunity. Rev. Med. Virol. 2010, 20:4-22.
76. Zampieri C.A., Sullivan N.J., Nabel G.J. Immunopathology of highly virulent pathogens: insights from Ebola virus. Nat. Immunol. 2007, 8:1159-1164.
77. Zheng X., Bevilacqua P.C. Straightening of bulged RNA by the double-stranded RNA-binding domain from the protein kinase PKR. Proc. Natl. Acad. Sci. USA 2000, 97:14162-14167.
78. Zinzula L., Esposito F., Mühlberger E., Trunschke M., Conrad D., Piano D., Tramontano E. Purification and functional characterization of the full length recombinant Ebola virus VP35 protein expressed in E. coli. Protein Expr. Purif. 2009, 66:113-119.