• 1.

    Lanciotti RS, Roehrig JT, Deubel V, Smith J, Parker M, Steele K, Crise B, Volpe KE, Crabtree MB, Scherret JH, Hall RA, MacKenzie JS, Cropp CB, Panigrahy B, Ostlund E, Schmitt B, Malkinson M, Banet C, Weissman J, Komar N, Savage HM, Stone W, McNamara T, Gubler DJ, 1999. Origin of the West Nile virus responsible for an outbreak of encephalitis in the northeastern United States. Science 286: 23332337.

    • Search Google Scholar
    • Export Citation
  • 2.

    van Regenmortel MHV, 2000. Introduction to the species concept in virus taxonomy. van Regenmortel MH, Fauquet CM, Bishop DH, Carstens EB, Estes MK, Lemon SM, Maniloff J, Mayo MA, McGeogh DJ, Pringle CR, Wickner RB, eds. Virus Taxonomy. Classification and Nomenclature of Viruses. Seventh Report of the International Committee on Taxonomy of Viruses. San Diego: Academic Press, 316.

    • Search Google Scholar
    • Export Citation
  • 3.

    Malkinson M, Banet C, 2002. The role of birds in the ecology of West Nile virus in Europe and Africa. Curr Top Microbiol Immunol 267: 309322.

    • Search Google Scholar
    • Export Citation
  • 4.

    Steele KE, Linn MJ, Schoepp RJ, Komar N, Geisbert TW, Manduca RM, Calle PP, Raphael BL, Clippinger TL, Larsen T, Smith J, Lanciotti RS, Panella NA, McNamara TS, 2000. Pathology of fatal West Nile virus infections in native and exotic birds during the 1999 outbreak in New York City, New York. Vet Pathol 37: 208224.

    • Search Google Scholar
    • Export Citation
  • 5.

    Komar N, Langevin S, Hinten S, Nemeth N, Edwards E, Hettler D, Davis B, Bowen R, Bunning M, 2003. Experimental infection of North American birds with the New York 1999 strain of West Nile virus. Emerg Infect Dis 9: 311322.

    • Search Google Scholar
    • Export Citation
  • 6.

    Brault AC, Langevin SA, Bowen RA, Panella NA, Biggerstaff BJ, Miller BR, Komar N, 2004. Differential virulence of West Nile strains for American crows. Emerg Infect Dis 10: 21612168.

    • Search Google Scholar
    • Export Citation
  • 7.

    Kinney RM, Huang CY, Whiteman MC, Bowen RA, Langevin SA, Miller BR, Brault AC, 2006. Avian virulence and thermostable replication of the North American strain of West Nile virus. J Gen Virol 87: 36113622.

    • Search Google Scholar
    • Export Citation
  • 8.

    Brault AC, Huang CY, Langevin SA, Kinney RM, Bowen RA, Ramey WN, Panella NA, Holmes EC, Powers AM, Miller BR, 2007. A single positively selected West Nile viral mutation confers increased virogenesis in American crows. Nat Genet 39: 11621166.

    • Search Google Scholar
    • Export Citation
  • 9.

    Langevin SA, Brault AC, Panella NA, Bowen RA, Komar N, 2005. Variation in virulence of West Nile virus strains for house sparrows (Passer domesticus). Am J Trop Med Hyg 72: 99102.

    • Search Google Scholar
    • Export Citation
  • 10.

    Fernandez-Salas I, Contreras-Cordero JF, Blitvich BJ, Gonzalez-Rojas JI, Cavazos-Alvarez A, Marlenee NL, Elizondo-Quiroga A, Lorono-Pino MA, Gubler DJ, Cropp BC, Calisher CH, Beaty BJ, 2003. Serologic evidence of West Nile virus infection in birds, Tamaulipas State, Mexico. Vector Borne Zoonotic Dis 3: 209213.

    • Search Google Scholar
    • Export Citation
  • 11.

    Estrada-Franco JG, Navarro-Lopez R, Beasley DW, Coffey L, Carrara AS, Travassos da Rosa A, Clements T, Wang E, Ludwig GV, Cortes AC, Ramirez PP, Tesh RB, Barrett AD, Weaver SC, 2003. West Nile virus in Mexico: evidence of widespread circulation since July 2002. Emerg Infect Dis 9: 16041607.

    • Search Google Scholar
    • Export Citation
  • 12.

    Beasley DW, Davis CT, Estrada-Franco J, Navarro-Lopez R, Campomanes-Cortes A, Tesh RB, Weaver SC, Barrett AD, 2004. Genome sequence and attenuating mutations in West Nile virus isolate from Mexico. Emerg Infect Dis 10: 22212224.

    • Search Google Scholar
    • Export Citation
  • 13.

    Davis CT, Ebel GD, Lanciotti RS, Brault AC, Guzman H, Siirin M, Lambert A, Parsons RE, Beasley DW, Novak RJ, Elizondo-Quiroga D, Green EN, Young DS, Stark LM, Drebot MA, Artsob H, Tesh RB, Kramer LD, Barrett AD, 2005. Phylogenetic analysis of North American West Nile virus isolates, 2001–2004: evidence for the emergence of a dominant genotype. Virology 342: 252265.

    • Search Google Scholar
    • Export Citation
  • 14.

    Beasley DW, Davis CT, Whiteman M, Granwehr B, Kinney RM, Barrett AD, 2004. Molecular determinants of virulence of West Nile virus in North America. Arch Virol Suppl: 3541.

    • Search Google Scholar
    • Export Citation
  • 15.

    Beasley DW, Whiteman MC, Zhang S, Huang CY, Schneider BS, Smith DR, Gromowski GD, Higgs S, Kinney RM, Barrett AD, 2005. Envelope protein glycosylation status influences mouse neuroinvasion phenotype of genetic lineage 1 West Nile virus strains. J Virol 79: 83398347.

    • Search Google Scholar
    • Export Citation
  • 16.

    Shirato K, Miyoshi H, Goto A, Ako Y, Ueki T, Kariwa H, Takashima I, 2004. Viral envelope protein glycosylation is a molecular determinant of the neuroinvasiveness of the New York strain of West Nile virus. J Gen Virol 85: 36373645.

    • Search Google Scholar
    • Export Citation
  • 17.

    Li J, Bhuvanakantham R, Howe J, Ng ML, 2006. The glycosylation site in the envelope protein of West Nile virus (Sarafend) plays an important role in replication and maturation processes. J Gen Virol 87: 613622.

    • Search Google Scholar
    • Export Citation
  • 18.

    Murata R, Eshita Y, Maeda A, Maeda J, Akita S, Tanaka T, Yoshii K, Kariwa H, Umemura T, Takashima I, 2010. Glycosylation of the West Nile virus envelope protein increases in vivo and in vitro viral multiplication in birds. Am J Trop Med Hyg 82: 696704.

    • Search Google Scholar
    • Export Citation
  • 19.

    Beasley DW, Li L, Suderman MT, Barrett AD, 2002. Mouse neuroinvasive phenotype of West Nile virus strains varies depending upon virus genotype. Virology 296: 1723.

    • Search Google Scholar
    • Export Citation
  • 20.

    Davis CT, Beasley DW, Guzman H, Siirin M, Parsons RE, Tesh RB, Barrett AD, 2004. Emergence of attenuated West Nile virus variants in Texas, 2003. Virology 330: 342350.

    • Search Google Scholar
    • Export Citation
  • 21.

    Reisen WK, Lothrop HD, Wheeler SS, Kennsington M, Gutierrez A, Fang Y, Garcia S, Lothrop B, 2008. Persistent West Nile virus transmission and the apparent displacement St. Louis encephalitis virus in southeastern California, 2003–2006. J Med Entomol 45: 494508.

    • Search Google Scholar
    • Export Citation
  • 22.

    Chambers TJ, Halevy M, Nestorowicz A, Rice CM, Lustig S, 1998. West Nile virus envelope proteins: nucleotide sequence analysis of strains differing in mouse neuroinvasiveness. J Gen Virol 79: 23752380.

    • Search Google Scholar
    • Export Citation
  • 23.

    Hanna SL, Pierson TC, Sanchez MD, Ahmed AA, Murtadha MM, Doms RW, 2005. N-linked glycosylation of West Nile virus envelope proteins influences particle assembly and infectivity. J Virol 79: 1326213274.

    • Search Google Scholar
    • Export Citation
  • 24.

    Scherret JH, Mackenzie JS, Khromykh AA, Hall RA, 2001. Biological significance of glycosylation of the envelope protein of Kunjin virus. Ann NY Acad Sci 951: 361363.

    • Search Google Scholar
    • Export Citation
  • 25.

    L'Vov DN, Shchelkanov M, Dzharkenov AF, Galkina IV, Kolobukhina LV, Aristova VA, Al'khovskii SV, Prilipov AG, Samokhvalov EI, Deriabin PG, Voronina AG, Vasil'ev AV, Bezzhonova OV, L'Vov DK, 2009. Population interactions of West Nile virus (Flaviviridae, Flavivirus) with arthropod vectors, vertebrates, humans in the middle and low belts of Volga delta in 2001–2006 [in Russian]. Vopr Virusol 54: 3643.

    • Search Google Scholar
    • Export Citation
  • 26.

    Adams SC, Broom AK, Sammels LM, Hartnett AC, Howard MJ, Coelen RJ, Mackenzie JS, Hall RA, 1995. Glycosylation and antigenic variation among Kunjin virus isolates. Virology 206: 4956.

    • Search Google Scholar
    • Export Citation
  • 27.

    Davis CT, Galbraith SE, Zhang S, Whiteman MC, Li L, Kinney RM, Barrett AD, 2007. A combination of naturally occurring mutations in North American West Nile virus nonstructural protein genes and the 3′ untranslated region alter virus phenotype. J Virol 81: 61116116.

    • Search Google Scholar
    • Export Citation
  • 28.

    Miller BR, Nasci RS, Godsey MS, Savage HM, Lutwama JJ, Lanciotti RS, Peters CJ, 2000. First field evidence for natural vertical transmission of West Nile virus in Culex univittatus complex mosquitoes from Rift Valley Province, Kenya. Am J Trop Med Hyg 62: 240246.

    • Search Google Scholar
    • Export Citation
  • 29.

    Charrel RN, Brault AC, Gallian P, Lemasson JJ, Murgue B, Murri S, Pastorino B, Zeller H, de Chesse R, de Micco P, de Lamballerie X, 2003. Evolutionary relationship between Old World West Nile virus strains. Evidence for viral gene flow between Africa, the Middle East, and Europe. Virology 315: 381388.

    • Search Google Scholar
    • Export Citation
  • 30.

    Brault AC, Langevin SA, Bowen RA, Panella NA, Biggerstaff BJ, Miller BR, Nicholas K, 2004. Differential virulence of West Nile strains for American crows. Emerg Infect Dis 10: 21612168.

    • Search Google Scholar
    • Export Citation
  • 31.

    Wheeler SS, Barker CM, Fang Y, Armijos MV, Carroll BD, Husted S, Johnson WO, Reisen WK, 2009. Differential impact of West Nile virus on California birds. Condor 111: 120.

    • Search Google Scholar
    • Export Citation
  • 32.

    Blitvich BJ, Fernandez-Salas I, Contreras-Cordero JF, Marlenee NL, Gonzalez-Rojas JI, Komar N, Gubler DJ, Calisher CH, Beaty BJ, 2003. Serologic evidence of West Nile virus infection in horses, Coahuila State, Mexico. Emerg Infect Dis 9: 853856.

    • Search Google Scholar
    • Export Citation
  • 33.

    Dupuis AP II, Marra PP, Kramer LD, 2003. Serologic evidence of West Nile virus transmission, Jamaica, West Indies. Emerg Infect Dis 9: 860863.

    • Search Google Scholar
    • Export Citation
  • 34.

    Lorono-Pino MA, Blitvich BJ, Farfan-Ale JA, Puerto FI, Blanco JM, Marlenee NL, Rosado-Paredes EP, Garcia-Rejon JE, Gubler DJ, Calisher CH, Beaty BJ, 2003. Serologic evidence of West Nile virus infection in horses, Yucatan State, Mexico. Emerg Infect Dis 9: 857859.

    • Search Google Scholar
    • Export Citation
  • 35.

    Mattar S, Edwards E, Laguado J, Gonzalez M, Alvarez J, Komar N, 2005. West Nile virus antibodies in Colombian horses. Emerg Infect Dis 11: 14971498.

  • 36.

    Cruz L, Cardenas VM, Abarca M, Rodriguez T, Reyna RF, Serpas MV, Fontaine RE, Beasley DW, Da Rosa AP, Weaver SC, Tesh RB, Powers AM, Suarez-Rangel G, 2005. Short report: serological evidence of West Nile virus activity in El Salvador. Am J Trop Med Hyg 72: 612615.

    • Search Google Scholar
    • Export Citation
  • 37.

    Komar O, Robbins MB, Klenk K, Blitvich BJ, Marlenee NL, Burkhalter KL, Gubler DJ, Gonzalvez G, Pena CJ, Peterson AT, Komar N, 2003. West Nile virus transmission in resident birds, Dominican Republic. Emerg Infect Dis 9: 12991302.

    • Search Google Scholar
    • Export Citation
  • 38.

    Komar O, Robbins MB, Contreras GG, Benz BW, Klenk K, Blitvich BJ, Marlenee NL, Burkhalter KL, Beckett S, Gonzalvez G, Pena CJ, Peterson AT, Komar N, 2005. West Nile virus survey of birds and mosquitoes in the Dominican Republic. Vector Borne Zoonotic Dis 5: 120126.

    • Search Google Scholar
    • Export Citation
  • 39.

    Deardorff E, Estrada-Franco J, Brault AC, Navarro-Lopez R, Campomanes-Cortes A, Paz-Ramirez P, Solis-Hernandez M, Ramey WN, Davis CT, Beasley DW, Tesh RB, Barrett AD, Weaver SC, 2006. Introductions of West Nile virus strains to Mexico. Emerg Infect Dis 12: 314318.

    • Search Google Scholar
    • Export Citation
  • 40.

    Phoutrides E, Jusino-Mendez T, Perez-Medina T, Seda-Lozada R, Garcia-Negron M, Davila-Toro F, Hunsperger E, 2011. The utility of animal surveillance in the detection of West Nile virus activity in Puerto Rico, 2007. Vector Borne Zoonotic Dis 11: 447450.

    • Search Google Scholar
    • Export Citation
  • 41.

    Morales-Betoulle ME, Morales H, Blitvich BJ, Powers AM, Davis EA, Klein R, Cordon-Rosales C, 2006. West Nile virus in horses, Guatemala. Emerg Infect Dis 12: 10381039.

    • Search Google Scholar
    • Export Citation
  • 42.

    Pupo M, Guzman MG, Fernandez R, Llop A, Dickinson FO, Perez D, Cruz R, Gonzalez T, Estevez G, Gonzalez H, Santos P, Kouri G, Andonova M, Lindsay R, Artsob H, Drebot M, 2006. West Nile virus infection in humans and horses, Cuba. Emerg Infect Dis 12: 10221024.

    • Search Google Scholar
    • Export Citation
  • 43.

    Morales MA, Barrandeguy M, Fabbri C, Garcia JB, Vissani A, Trono K, Gutierrez G, Pigretti S, Menchaca H, Garrido N, Taylor N, Fernandez F, Levis S, Enria D, 2006. West Nile virus isolation from equines in Argentina, 2006. Emerg Infect Dis 12: 15591561.

    • Search Google Scholar
    • Export Citation
  • 44.

    Farfan-Ale JA, Lorono-Pino MA, Garcia-Rejon JE, Hovav E, Powers AM, Lin M, Dorman KS, Platt KB, Bartholomay LC, Soto V, Beaty BJ, Lanciotti RS, Blitvich BJ, 2009. Detection of RNA from a novel West Nile-like virus and high prevalence of an insect-specific flavivirus in mosquitoes in the Yucatan Peninsula of Mexico. Am J Trop Med Hyg 80: 8595.

    • Search Google Scholar
    • Export Citation
  • 45.

    Ostfeld RS, 2009. Biodiversity loss and the rise of zoonotic pathogens. Clin Microbiol Infect 15 (Suppl 1): 4043.

  • 46.

    Swaddle JP, Calos SE, 2008. Increased avian diversity is associated with lower incidence of human West Nile infection: observation of the dilution effect. PLoS ONE 3: e2488.

    • Search Google Scholar
    • Export Citation
  • 47.

    Reisen WK, Fang Y, Martinez VM, 2005. Avian host and mosquito (Diptera: Culicidae) vector competence determine the efficiency of West Nile and St. Louis encephalitis virus transmission. J Med Entomol 42: 367375.

    • Search Google Scholar
    • Export Citation
 
 
 

 

 

 

 

 

 

Reduced Avian Virulence and Viremia of West Nile Virus Isolates from Mexico and Texas

View More View Less
  • Division of Vector-borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado; Center for Vector-borne Diseases and Department of Pathology, Microbiology and Immunology, School of Veterinary Medicine, University of California, Davis, California; Departments of Pathology and Microbiology and Immunology, Center for Emerging Infectious Diseases and Biodefense, Institute for Human Infections and Immunity, University of Texas Medical Branch, Galveston, Texas; U.S. Fish and Wildlife Service, Portland, Oregon; Department of Biomedical Sciences, Colorado State University, Fort Collins, Colorado

A West Nile virus (WNV) isolate from Mexico (TM171-03) and BIRD1153, a unique genotype from Texas, have exhibited reduced murine neuroinvasive phenotypes. To determine if murine neuroinvasive capacity equates to avian virulence potential, American crow (Corvus brachyrhynchos) and house sparrows (Passer domesticus) were experimentally inoculated with representative murine neuroinvasive/non-neuroinvasive strains. In both avian species, a plaque variant from Mexico that was E-glycosylation competent produced higher viremias than an E-glycosylation–incompetent variant, indicating the potential importance of E-glycosylation for avian replication. The murine non-neuroinvasive BIRD1153 strain was significantly attenuated in American crows but not house sparrows when compared with the murine neuroinvasive Texas strain. Despite the loss of murine neuroinvasive properties of nonglycosylated variants from Mexico, our data indicate avian replication potential of these strains and that unique WNV virulence characteristics exist between murine and avian models. The implications of reduced avian replication of variants from Mexico for restricted WNV transmission in Latin America is discussed.

Author Notes

*Address correspondence to Aaron C. Brault, Division of Vector-borne Infectious Diseases, Centers for Disease Control and Prevention, 3150 Rampart Road, Fort Collins, CO 80521. E-mail: abrault@cdc.gov

Financial support: This study was supported by National Institutes of Health grants AI061822, AI055607, and AI67847; Pacific Southwest Regional Center for Excellence (PSWRCE) U54 AI065359; and Centers for Disease Control and Prevention grant CI000235.

Authors' addresses: Aaron C. Brault, Division of Vector-borne Diseases, Centers for Disease Control and Prevention, Fort Collins, CO, E-mail: abrault@cdc.gov. Stanley A. Langevin, Wanichaya N. Ramey, Ying Fang, Christopher M. Barker, and William K. Reisen, Center for Vector-borne Diseases and Department of Pathology, Microbiology and Immunology, School of Veterinary Medicine, University of California, Davis, CA, E-mails: salangevin1@gmail.com, wramey@berkeley.edu, ylfang@ucdavis.edu, cmbarker@ucdavis.edu, and arbo123@pacbell.net. David W. C. Beasley and Alan D. T. Barrett, Departments of Pathology and Microbiology and Immunology, Center for Emerging Infectious Diseases and Biodefense, Institute for Human Infections and Immunity, University of Texas Medical Branch, Galveston, TX, E-mails: dwbeasle@utmb.edu and abarrett@utmb.edu. Todd A. Sanders, U.S. Fish and Wildlife Service–Division of Migratory Bird Management, Portland, OR, E-mail: todd_sanders@fws.gov. Richard A. Bowen, Department of Biomedical Sciences, Colorado State University, Fort Collins, CO, E-mail: rbowen@colostate.edu.

Save