The E glycoprotein plays an essential role in the high pathogenicity of European-Mediterranean IS98 strain of West Nile virus

Virology

Volumn 492, Issue , 2016, Pages 53-65

  Alsaleh, Khaled ^a   Khou, Cécile ^a   Frenkiel, Marie Pascale ^a   Lecollinet, Sylvie ^b   Vàzquez, Ana ^c   de Arellano, Eva Ramírez ^c   Després, Philippe ^d   Pardigon, Nathalie ^a  

^a INSTITUT PASTEUR   (France)

^b ECOLE NATIONALE VÉTÉRINAIRE D ALFORT   (France)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d UNIVERSITÉ DE LA RÉUNION   (France)

Author keywords

Chimeric virus; Flavivirus; Infectious clones; Kunjin virus; Mouse; Pathogenesis; Virulence factors; West Nile virus

Indexed keywords

GLYCOPROTEIN E; GLYCOPROTEIN E, FLAVIVIRUS; LIVE VACCINE; VIRUS ENVELOPE PROTEIN; VIRUS VACCINE;

5' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; GLYCOSYLATION; IN VITRO STUDY; IN VIVO STUDY; KUNJIN VIRUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; VIRUS PATHOGENESIS; VIRUS STRAIN; VIRUS VIRULENCE; WEST NILE VIRUS; ANIMAL; BAGG ALBINO MOUSE; CHEMISTRY; DISEASE MODEL; EUROPE; GENETIC REASSORTMENT; GENETICS; HUMAN; IMMUNIZATION; IMMUNOLOGY; MORTALITY; PATHOGENICITY; PROTEIN TERTIARY STRUCTURE; SOUTHERN EUROPE; SURVIVAL ANALYSIS; WEST NILE FEVER;

ANIMALS; DISEASE MODELS, ANIMAL; EUROPE; FEMALE; HUMANS; IMMUNIZATION; MEDITERRANEAN REGION; MICE; MICE, INBRED BALB C; PROTEIN STRUCTURE, TERTIARY; REASSORTANT VIRUSES; SURVIVAL ANALYSIS; VACCINES, ATTENUATED; VIRAL ENVELOPE PROTEINS; VIRAL VACCINES; WEST NILE FEVER; WEST NILE VIRUS;

EID: 84958280120     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2016.02.009     Document Type: Article

References (78)

1. Adams S.C., Broom A.K., Sammels L.M., Hartnett A.C., Howard M.J., Coelen R.J., Mackenzie J.S., Hall R.A. Glycosylation and antigenic variation among Kunjin virus isolates. Virology 1995, 206:49-56.
2. Audsley M., Edmonds J., Liu W., Mokhonov V., Mokhonova E., Melian E.B., Prow N., Hall R.A., Khromykh A.A. Virulence determinants between New York 99 and Kunjin strains of West Nile virus. Virology 2011, 414:63-73.
3. Bahuon C., Despres P., Pardigon N., Panthier J.J., Cordonnier N., Lowenski S., Richardson J., Zientara S., Lecollinet S. IS-98-ST1 West Nile virus derived from an infectious cDNA clone retains neuroinvasiveness and neurovirulence properties of the original virus. PLoS One 2012, 7:e47666.
4. Bakonyi T., Ivanics E., Erdelyi K., Ursu K., Ferenczi E., Weissenbock H., Nowotny N. Lineage 1 and 2 strains of encephalitic West Nile virus, central Europe. Emerg. Infect. Dis. 2006, 12:618-623.
5. Beasley D.W., Barrett A.D. Identification of neutralizing epitopes within structural domain III of the West Nile virus envelope protein. J. Virol. 2002, 76:13097-13100.
6. Beasley D.W., Davis C.T., Whiteman M., Granwehr B., Kinney R.M., Barrett A.D. Molecular determinants of virulence of West Nile virus in North America. Arch. Virol. Suppl. 2004, 35-41.
7. Beasley D.W., Li L., Suderman M.T., Barrett A.D. Mouse neuroinvasive phenotype of West Nile virus strains varies depending upon virus genotype. Virology 2002, 296:17-23.
8. Beasley D.W., Whiteman M.C., Zhang S., Huang C.Y., Schneider B.S., Smith D.R., Gromowski G.D., Higgs S., Kinney R.M., Barrett A.D. Envelope protein glycosylation status influences mouse neuroinvasion phenotype of genetic lineage 1 West Nile virus strains. J Virol. 2005, 79:8339-8347.
9. Berthet F.X., Zeller H.G., Drouet M.T., Rauzier J., Digoutte J.P., Deubel V. Extensive nucleotide changes and deletions within the envelope glycoprotein gene of Euro-African West Nile viruses. J. Gen. Virol. 1997, 78:2293-2297.
10. Borisevich V., Seregin A., Nistler R., Mutabazi D., Yamshchikov V. Biological properties of chimeric West Nile viruses. Virology 2006, 349:371-381.
11. Botha E.M., Markotter W., Wolfaardt M., Paweska J.T., Swanepoel R., Palacios G., Nel L.H., Venter M. Genetic determinants of virulence in pathogenic lineage 2 West Nile virus strains. Emerg. Infect. Dis. 2008, 14:222-230.
12. Brault A.C., Huang C.Y., Langevin S.A., Kinney R.M., Bowen R.A., Ramey W.N., Panella N.A., Holmes E.C., Powers A.M., Miller B.R. A single positively selected West Nile viral mutation confers increased virogenesis in American crows. Nat. Genet. 2007, 39:1162-1166.
13. Brault A.C., Langevin S.A., Bowen R.A., Panella N.A., Biggerstaff B.J., Miller B.R., Komar N. Differential virulence of West Nile strains for American crows. Emerg. Infect. Dis. 2004, 10:2161-2168.
14. Brinton M.A. Replication cycle and molecular biology of the West Nile virus. Viruses 2014, 6:13-53.
15. Calistri P., Giovannini A., Hubalek Z., Ionescu A., Monaco F., Savini G., Lelli R. Epidemiology of west nile in europe and in the mediterranean basin. Open. Virol. J. 2010, 4:29-37.
16. Chambers T.J., Halevy M., Nestorowicz A., Rice C.M., Lustig S. West Nile virus envelope proteins: nucleotide sequence analysis of strains differing in mouse neuroinvasiveness. J. Gen. Virol. 1998, 79:2375-2380.
17. Ching C.Y., Casals J., Bowen E.T., Simpson D.I., Platt G.S., Way H.J., Smith C.E. Arbovirus infections in Sarawak: the isolation of Kunjin virus from mosquitoes of the Culex pseudovishnui group. Ann. Trop. Med. Parasitol. 1970, 64:263-268.
18. Chu J.J., Rajamanonmani R., Li J., Bhuvanakantham R., Lescar J., Ng M.L. Inhibition of West Nile virus entry by using a recombinant domain III from the envelope glycoprotein. J. Gen. Virol. 2005, 86:405-412.
19. Ciccozzi M., Peletto S., Cella E., Giovanetti M., Lai A., Gabanelli E., Acutis P.L., Modesto P., Rezza G., Platonov A.E., Lo Presti A., Zehender G. Epidemiological history and phylogeography of West Nile virus lineage 2. Infect. Genet. Evol. 2013, 17:46-50.
20. Davis C.T., Galbraith S.E., Zhang S., Whiteman M.C., Li L., Kinney R.M., Barrett A.D. A combination of naturally occurring mutations in North American West Nile virus nonstructural protein genes and in the 3' untranslated region alters virus phenotype. J. Virol. 2007, 81:6111-6116.
21. Davis C.W., Nguyen H.Y., Hanna S.L., Sanchez M.D., Doms R.W., Pierson T.C. West Nile virus discriminates between DC-SIGN and DC-SIGNR for cellular attachment and infection. J. Virol. 2006, 80:1290-1301.
22. Donadieu E., Bahuon C., Lowenski S., Zientara S., Coulpier M., Lecollinet S. Differential virulence and pathogenesis of West Nile viruses. Viruses 2013, 5:2856-2880.
23. Dridi M., Rauw F., Muylkens B., Lecollinet S., van den Berg T., Lambrecht B. Setting up a SPF chicken model for the pathotyping of West Nile virus (WNV) strains. Transbound. Emerg. Dis. 2013, 60(Suppl 2):S51-S62.
24. Dridi M., Vangeluwe D., Lecollinet S., van den Berg T., Lambrecht B. Experimental infection of Carrion crows (Corvus corone) with two European West Nile virus (WNV) strains. Vet. Microbiol. 2013, 165:160-166.
25. Frost M.J., Zhang J., Edmonds J.H., Prow N.A., Gu X., Davis R., Hornitzky C., Arzey K.E., Finlaison D., Hick P., Read A., Hobson-Peters J., May F.J., Doggett S.L., Haniotis J., Russell R.C., Hall R.A., Khromykh A.A., Kirkland P.D. Characterization of virulent West Nile virus Kunjin strain, Australia, 2011. Emerg. Infect. Dis. 2012, 18:792-800.
26. Funk A., Truong K., Nagasaki T., Torres S., Floden N., Balmori Melian E., Edmonds J., Dong H., Shi P.Y., Khromykh A.A. RNA structures required for production of subgenomic flavivirus RNA. J. Virol. 2010, 84:11407-11417.
27. Hall R.A., Broom A.K., Smith D.W., Mackenzie J.S. The ecology and epidemiology of Kunjin virus. Curr. Top. Microbiol. Immunol. 2002, 267:253-269.
28. Hall R.A., Nisbet D.J., Pham K.B., Pyke A.T., Smith G.A., Khromykh A.A. DNA vaccine coding for the full-length infectious Kunjin virus RNA protects mice against the New York strain of West Nile virus. Proc. Natl. Acad. Sci. USA 2003, 100:10460-10464.
29. Hanna S.L., Pierson T.C., Sanchez M.D., Ahmed A.A., Murtadha M.M., Doms R.W. N-linked glycosylation of west nile virus envelope proteins influences particle assembly and infectivity. J. Virol. 2005, 79:13262-13274.
30. Hussmann K.L., Vandergaast R., Ochsner S.P., Huang A.C., Gale M., Fredericksen B.L. In vitro and in vivo characterization of a West Nile virus MAD78 infectious clone. Arch. Virol. 2014, 159:3113-3118.
31. Kajaste-Rudnitski A., Mashimo T., Frenkiel M.P., Guenet J.L., Lucas M., Despres P. The 2',5'-oligoadenylate synthetase 1b is a potent inhibitor of West Nile virus replication inside infected cells. J. Biol. Chem. 2006, 281:4624-4637.
32. Kanai R., Kar K., Anthony K., Gould L.H., Ledizet M., Fikrig E., Marasco W.A., Koski R.A., Modis Y. Crystal structure of west nile virus envelope glycoprotein reveals viral surface epitopes. J. Virol. 2006, 80:11000-11008.
33. Kariwa H., Murata R., Totani M., Yoshii K., Takashima I. Increased pathogenicity of West Nile virus (WNV) by glycosylation of envelope protein and seroprevalence of WNV in wild birds in Far Eastern Russia. Int. Journal. Environ. Res. Public Health 2013, 10:7144-7164.
34. Kaufmann B., Rossmann M.G. Molecular mechanisms involved in the early steps of flavivirus cell entry. Microbes Infect. 2011, 13:1-9.
35. Khromykh A.A., Varnavski A.N., Sedlak P.L., Westaway E.G. Coupling between replication and packaging of flavivirus RNA: evidence derived from the use of DNA-based full-length cDNA clones of Kunjin virus. J. Virol. 2001, 75:4633-4640.
36. Khromykh A.A., Westaway E.G. Subgenomic replicons of the flavivirus Kunjin: construction and applications. J. Virol. 1997, 71:1497-1505.
37. Kinney R.M., Huang C.Y., Whiteman M.C., Bowen R.A., Langevin S.A., Miller B.R., Brault A.C. Avian virulence and thermostable replication of the North American strain of West Nile virus. J. Gen. Virol. 2006, 87:3611-3622.
38. Kramer L.D., Styer L.M., Ebel G.D. A global perspective on the epidemiology of West Nile virus. Annu. Rev. Eỳntomol. 2008, 53:61-81.
39. Lanciotti R.S., Ebel G.D., Deubel V., Kerst A.J., Murri S., Meyer R., Bowen M., McKinney N., Morrill W.E., Crabtree M.B., Kramer L.D., Roehrig J.T. Complete genome sequences and phylogenetic analysis of West Nile virus strains isolated from the United States, Europe, and the Middle East. Virology 2002, 298:96-105.
40. Lanciotti R.S., Roehrig J.T., Deubel V., Smith J., Parker M., Steele K., Crise B., Volpe K.E., Crabtree M.B., Scherret J.H., Hall R.A., MacKenzie J.S., Cropp C.B., Panigrahy B., Ostlund E., Schmitt B., Malkinson M., Banet C., Weissman J., Komar N., Savage H.M., Stone W., McNamara T., Gubler D.J. Origin of the West Nile virus responsible for an outbreak of encephalitis in the northeastern United States. Science 1999, 286:2333-2337.
41. Langevin S.A., Bowen R.A., Ramey W.N., Sanders T.A., Maharaj P.D., Fang Y., Cornelius J., Barker C.M., Reisen W.K., Beasley D.W., Barrett A.D., Kinney R.M., Huang C.Y., Brault A.C. Envelope and pre-membrane protein structural amino acid mutations mediate diminished avian growth and virulence of a Mexican West Nile virus isolate. J. Gen. Virol. 2011, 92:2810-2820.
42. Laurent-Rolle M., Boer E.F., Lubick K.J., Wolfinbarger J.B., Carmody A.B., Rockx B., Liu W., Ashour J., Shupert W.L., Holbrook M.R., Barrett A.D., Mason P.W., Bloom M.E., Garcia-Sastre A., Khromykh A.A., Best S.M. The NS5 protein of the virulent West Nile virus NY99 strain is a potent antagonist of type I interferon-mediated JAK-STAT signaling. J. Virol. 2010, 84:3503-3515.
43. Lee J.W., Chu J.J., Ng M.L. Quantifying the specific binding between West Nile virus envelope domain III protein and the cellular receptor alphaVbeta3 integrin. J. Biol. Chem. 2006, 281:1352-1360.
44. Li L., Barrett A.D., Beasley D.W. Differential expression of domain III neutralizing epitopes on the envelope proteins of West Nile virus strains. Virology 2005, 335:99-105.
45. Lim S.M., Brault A.C., van Amerongen G., Bosco-Lauth A.M., Romo H., Sewbalaksing V.D., Bowen R.A., Osterhaus A.D., Koraka P., Martina B.E. Susceptibility of Carrion Crows to Experimental Infection with Lineage 1 and 2 West Nile Viruses. Emerg. Infect. Dis. 2015, 21:1357-1365.
46. Lim S.M., Koraka P., van Boheemen S., Roose J.M., Jaarsma D., van de Vijver D.A., Osterhaus A.D., Martina B.E. Characterization of the mouse neuroinvasiveness of selected European strains of West Nile virus. PLoS One 2013, 8:e74575.
47. Lo M.K., Tilgner M., Bernard K.A., Shi P.Y. Functional analysis of mosquito-borne flavivirus conserved sequence elements within 3' untranslated region of West Nile virus by use of a reporting replicon that differentiates between viral translation and RNA replication. J. Virol. 2003, 77:10004-10014.
48. Lobigs M., Diamond M.S. Feasibility of cross-protective vaccination against flaviviruses of the Japanese encephalitis serocomplex. Expert. Rev. Vaccines 2012, 11:177-187.
49. Lucas M., Frenkiel M.P., Mashimo T., Guenet J.L., Deubel V., Despres P., Ceccaldi P.E. The Israeli strain IS-98-ST1 of West Nile virus as viral model for West Nile encephalitis in the Old World. Virol. J. 2004, 1:9.
50. Malkinson M., Banet C., Weisman Y., Pokamunski S., King R., Drouet M.T., Deubel V. Introduction of West Nile virus in the Middle East by migrating white storks. Emerg. Infect. Dis. 2002, 8:392-397.
51. Mashimo T., Lucas M., Simon-Chazottes D., Frenkiel M.P., Montagutelli X., Ceccaldi P.E., Deubel V., Guenet J.L., Despres P. A nonsense mutation in the gene encoding 2'-5'-oligoadenylate synthetase/L1 isoform is associated with West Nile virus susceptibility in laboratory mice. Proc. Natl. Acad. Sci. USA 2002, 99:11311-11316.
52. May F.J., Davis C.T., Tesh R.B., Barrett A.D. Phylogeography of West Nile virus: from the cradle of evolution in Africa to Eurasia, Australia, and the Americas. J. Virol. 2011, 85:2964-2974.
53. Mertens E., Kajaste-Rudnitski A., Torres S., Funk A., Frenkiel M.P., Iteman I., Khromykh A.A., Despres P. Viral determinants in the NS3 helicase and 2K peptide that promote West Nile virus resistance to antiviral action of 2',5'-oligoadenylate synthetase 1b. Virology 2010, 399:176-185.
54. Mukhopadhyay S., Kim B.S., Chipman P.R., Rossmann M.G., Kuhn R.J. Structure of West Nile virus. Science 2003, 302:248.
55. Murata R., Eshita Y., Maeda A., Maeda J., Akita S., Tanaka T., Yoshii K., Kariwa H., Umemura T., Takashima I. Glycosylation of the West Nile Virus envelope protein increases in vivo and in vitro viral multiplication in birds. Am. Journal. Trop. Med. Hyg. 2010, 82:696-704.
56. Nybakken G.E., Nelson C.A., Chen B.R., Diamond M.S., Fremont D.H. Crystal structure of the West Nile virus envelope glycoprotein. J. Virol. 2006, 80:11467-11474.
57. Pijlman G.P., Funk A., Kondratieva N., Leung J., Torres S., van der Aa L., Liu W.J., Palmenberg A.C., Shi P.Y., Hall R.A., Khromykh A.A. A highly structured, nuclease-resistant, noncoding RNA produced by flaviviruses is required for pathogenicity. Cell Host Microbe 2008, 4:579-591.
58. Platonov A.E., Shipulin G.A., Shipulina O.Y., Tyutyunnik E.N., Frolochkina T.I., Lanciotti R.S., Yazyshina S., Platonova O.V., Obukhov I.L., Zhukov A.N., Vengerov Y.Y., Pokrovskii V.I. Outbreak of West Nile virus infection, Volgograd Region, Russia, 1999. Emerg. Infect. Dis. 2001, 7:128-132.
59. Poidinger M., Hall R.A., Mackenzie J.S. Molecular characterization of the Japanese encephalitis serocomplex of the flavivirus genus. Virology 1996, 218:417-421.
60. Prow N.A. The changing epidemiology of Kunjin virus in Australia. Int. J. Environ. Res. Public Health 2013, 10:6255-6272.
61. Prow N.A., Setoh Y.X., Biron R.M., Sester D.P., Kim K.S., Hobson-Peters J., Hall R.A., Bielefeldt-Ohmann H. The West Nile virus-like flavivirus Koutango is highly virulent in mice due to delayed viral clearance and the induction of a poor neutralizing antibody response. J. Virol. 2014, 88:9947-9962.
62. Rizzo C., Salcuni P., Nicoletti L., Ciufolini M.G., Russo F., Masala R., Frongia O., Finarelli A.C., Gramegna M., Gallo L., Pompa M.G., Rezza G., Salmaso S., Declich S. Epidemiological surveillance of West Nile neuroinvasive diseases in Italy, 2008 to 2011. Euro Surveill.: Bull. Eur. Sur Les. Mal. Transm.=Eur. Commun. Dis. Bull. 2012, 17.
63. Rizzoli A., Jimenez-Clavero M.A., Barzon L., Cordioli P., Figuerola J., Koraka P., Martina B., Moreno A., Nowotny N., Pardigon N., Sanders N., Ulbert S., Tenorio A. The challenge of West Nile virus in Europe: knowledge gaps and research priorities. Euro Surveill.: Bull. Eur. Sur Les. Mal. Transm.=Eur. Commun. Dis. Bull. 2015, 20.
64. Sanchez M.D., Pierson T.C., McAllister D., Hanna S.L., Puffer B.A., Valentine L.E., Murtadha M.M., Hoxie J.A., Doms R.W. Characterization of neutralizing antibodies to West Nile virus. Virology 2005, 336:70-82.
65. Scherret J.H., Poidinger M., Mackenzie J.S., Broom A.K., Deubel V., Lipkin W.I., Briese T., Gould E.A., Hall R.A. The relationships between West Nile and Kunjin viruses. Emerg. Infect. Dis. 2001, 7:697-705.
66. Setoh Y.X., Prow N.A., Rawle D.J., Tan C.S., Edmonds J.H., Hall R.A., Khromykh A.A. Systematic analysis of viral genes responsible for differential virulence between American and Australian West Nile virus strains. J. Gen. Virol. 2015, 96:1297-1308.
67. Shi P.Y., Tilgner M., Lo M.K. Construction and characterization of subgenomic replicons of New York strain of West Nile virus. Virology 2002, 296:219-233.
68. Shirato K., Miyoshi H., Goto A., Ako Y., Ueki T., Kariwa H., Takashima I. Viral envelope protein glycosylation is a molecular determinant of the neuroinvasiveness of the New York strain of West Nile virus. J. Gen. Virol. 2004, 85:3637-3645.
69. Sotelo E., Fernandez-Pinero J., Llorente F., Aguero M., Hoefle U., Blanco J.M., Jimenez-Clavero M.A. Characterization of West Nile virus isolates from Spain: new insights into the distinct West Nile virus eco-epidemiology in the Western Mediterranean. Virology 2009, 395:289-297.
70. Sotelo E., Gutierrez-Guzman A.V., del Amo J., Llorente F., El-Harrak M., Perez-Ramirez E., Blanco J.M., Hofle U., Jimenez-Clavero M.A. Pathogenicity of two recent Western Mediterranean West Nile virus isolates in a wild bird species indigenous to Southern Europe: the red-legged partridge. Veter. Res. 2011, 42:11.
71. Suen W.W., Prow N.A., Hall R.A., Bielefeldt-Ohmann H. Mechanism of West Nile virus neuroinvasion: a critical appraisal. Viruses 2014, 6:2796-2825.
72. Totani M., Yoshii K., Kariwa H., Takashima I. Glycosylation of the envelope protein of West Nile Virus affects its replication in chicks. Avian Dis. 2011, 55:561-568.
73. Vazquez A., Sanchez-Seco M.P., Ruiz S., Molero F., Hernandez L., Moreno J., Magallanes A., Tejedor C.G., Tenorio A. Putative new lineage of west nile virus, Spain. Emerg. Infect. Dis. 2010, 16:549-552.
74. Villordo S.M., Gamarnik A.V. Genome cyclization as strategy for flavivirus RNA replication. Virus Res. 2009, 139:230-239.
75. Volk D.E., Beasley D.W., Kallick D.A., Holbrook M.R., Barrett A.D., Gorenstein D.G. Solution structure and antibody binding studies of the envelope protein domain III from the New York strain of West Nile virus. J. Biol. Chem. 2004, 279:38755-38761.
76. Wright P.J. Envelope protein of the flavivirus Kunjin is apparently not glycosylated. J. Gen. Virol. 1982, 59:29-38.
77. Yamshchikov G., Borisevich V., Seregin A., Chaporgina E., Mishina M., Mishin V., Kwok C.W., Yamshchikov V. An attenuated West Nile prototype virus is highly immunogenic and protects against the deadly NY99 strain: a candidate for live WN vaccine development. Virology 2004, 330:304-312.
78. Zhang B., Dong H., Stein D.A., Iversen P.L., Shi P.Y. West Nile virus genome cyclization and RNA replication require two pairs of long-distance RNA interactions. Virology 2008, 373:1-13.