Evolutionary patterns of eastern equine encephalitis virus in North versus South America suggest ecological differences and taxonomic revision

Journal of Virology

Volumn 84, Issue 2, 2010, Pages 1014-1025

  Arrigo, Nicole C ^a   Paige, Adams ^a   Weaver, Scott C ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POLYPROTEIN; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CLADISTICS; CONTROLLED STUDY; EASTERN EQUINE ENCEPHALOMYELITIS VIRUS; ECOLOGY; EMBRYO; GENE SEQUENCE; GENETIC CONSERVATION; GENETIC LINE; GENETIC VARIABILITY; GEOGRAPHY; MOLECULAR EVOLUTION; NONHUMAN; NORTH AMERICA; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PATHOGENICITY; PHYLOGENY; PRIORITY JOURNAL; RESERVOIR; SOUTH AMERICA; TAXONOMY; VENEZUELAN EQUINE ENCEPHALOMYELITIS ALPHAVIRUS; VIRUS GENOME;

ANIMALS; BAYES THEOREM; CRICETINAE; ENCEPHALITIS VIRUS, EASTERN EQUINE; ENCEPHALOMYELITIS, EASTERN EQUINE; EVOLUTION, MOLECULAR; GENETIC VARIATION; HORSE DISEASES; HORSES; HUMANS; NORTH AMERICA; OPEN READING FRAMES; PHYLOGENY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; SOUTH AMERICA; SPECIES SPECIFICITY; VIRAL STRUCTURAL PROTEINS;

EASTERN EQUINE ENCEPHALITIS VIRUS; EQUIDAE; MAMMALIA; VENEZUELAN EQUINE ENCEPHALITIS VIRUS;

EID: 73849139633     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01586-09     Document Type: Article

References (69)

1. Aguilar, P. V., A. P. Adams, E. Wang, W. Kang, A. Carrara, M. Anishchenko, I. Frolov, and S. C. Weaver. 2008. Structural and nonstructural protein genome regions of eastern equine encephalitis virus are determinants of interferon sensitivity and murine virulence. J. Virol. 82:4920-4930.
2. Aguilar, P. V., I. P. Greene, L. L. Coffey, G. Medina, A. C. Moncayo, M. Anishchenko, G. V. Ludwig, M. J. Turell, M. L. O'Guinn, J. Lee, R. B. Tesh, D. M. Watts, K. L. Russell, C. Hice, S. Yanoviak, A. C. Morrison, T. A. Klein, D. J. Dohm, H. Guzman, A. P. Travassos da Rosa, C. Guevara, T. Kochel, J. Olson, C. Cabezas, and S. C. Weaver. 2004. Endemic Venezuelan equine encephalitis in northern Peru. Emerg. Infect. Dis. 10:880-888.
3. Aguilar, P. V., S. Paessler, A. S. Carrara, S. Baron, J. Poast, E. Wang, A. C. Moncayo, M. Anishchenko, D. Watts, R. B. Tesh, and S. C. Weaver. 2005. Variation in interferon sensitivity and induction among strains of eastern equine encephalitis virus. J. Virol. 79:11300-11310.
4. Aguilar, P. V., R. M. Robich, M. J. Turell, M. L. O'Guinn, T. A. Klein, A. Huaman, C. Guevara, Z. Rios, R. B. Tesh, D. M. Watts, J. Olson, and S. C. Weaver. 2007. Endemic eastern equine encephalitis in the Amazon region of Peru. Am. J. Trop. Med. Hyg. 76:293-298.
5. Armstrong, P. M., T. G. Andreadis, J. F. Anderson, J. W. Stull, and C. N. Mores. 2008. Tracking eastern equine encephalitis virus perpetuation in the northeastern United States by phylogenetic analysis. Am. J. Trop. Med. Hyg. 79:291-296.
6. Auguste, A. J., S. M. Volk, N. C. Arrigo, R. Martinez, V. Ramkissoon, A. P. Adams, N. N. Thompson, A. A. Adesiyun, D. D. Chadee, J. E. Foster, A. P. A. Travassos da Rosa, R. B. Tesh, S. C. Weaver, and C. V. F. Carrington. 2009. Isolation and phylogenetic analysis of Mucambo virus (Venezuelan equine encephalitis complex subtype IIIA) in Trinidad. Virology 392:123-130.
7. Brault, A. C., A. M. Powers, C. L. Chavez, R. N. Lopez, M. F. Cachon, L. F. Gutierrez, W. Kang, R. B. Tesh, R. E. Shope, and S. C. Weaver. 1999. Genetic and antigenic diversity among eastern equine encephalitis viruses from North, Central, and South America. Am. J. Trop. Med. Hyg. 61:579-586.
8. Briese, T., J. T. Paweska, L. K. McMullan, S. K. Hutchison, C. Street, G. Palacios, M. L. Khristova, J. Weyer, R. Swanepoel, M. Egholm, S. T. Nichol, and W. I. Lipkin. 2009. Genetic detection and characterization of Lujo virus, a new hemorrhagic fever-associated arenavirus from southern Africa. PLoS Pathog. 5:e1000455.
9. Calisher, C. H., and N. Karabatsos. 1988. Arbovirus serogroups: definition and geographic distribution, p. 19-57. In T. P. Monath (ed.), The arboviruses: epidemiology and ecology, vol. I. CRC Press, Boca Raton, FL.
10. Calisher, C. H., R. E. Shope, W. Brandt, J. Casals, N. Karabatsos, F. A. Murphy, R. B. Tesh, and M. E. Wiebe. 1980. Proposed antigenic classification of registered arboviruses I. Togaviridae, Alphavirus. Intervirology 14: 229-232.
11. Casals, J. 1964. Antigenic variants of eastern equine encephalitis virus. J. Exp. Med. 119:547-565.
12. Causey, O. R., R. E. Shope, P. Sutmoller, and H. Laemmert. 1962. Epizootic eastern equine encephalitis in the Bratanca region of Para, Brazil. Rev. Servicio Especial Saude Publica 12:39-45.
13. Cilnis, M. J., W. Kang, and S. C. Weaver. 1996. Genetic conservation of Highlands J. viruses. Virology 218:343-351.
14. Cupp, E. W., K. Klingler, H. K. Hassan, L. M. Viguers, and T. R. Unnasch. 2003. Transmission of eastern equine encephalomyelitis virus in central Alabama. Am. J. Trop. Med. Hyg. 68:495-500.
15. Cupp, E. W., W. F. Scherer, and J. V. Ordonez. 1979. Transmission of Venezuelan encephalitis virus by naturally infected Culex (Melanoconion) opisthopus. Am. J. Trop. Med. Hyg. 28:1060-1063.
16. Cupp, E. W., D. Zhang, X. Yue, M. S. Cupp, C. Guyer, T. R. Sprenger, and T. R. Unnasch. 2004. Identification of reptilian and amphibian blood meals from mosquitoes in an eastern equine encephalomyelitis virus focus in central Alabama. Am. J. Trop. Med. Hyg. 71:272-276.
17. de Souza Lopes, O., and L. de Abreu Sacchetta. 1974. Epidemiological studies on Eastern equine encephalitis virus in Sao Paulo, Brazil. Rev. Inst. Med. Trop. Sao Paulo 16:253-258.
18. Dietz, W. H., Jr., P. Galindo, and K. M. Johnson. 1980. Eastern equine encephalomyelitis in Panama: the epidemiology of the 1973 epizootic. Am. J. Trop. Med. Hyg. 29:133-140.
19. Drummond, A. J., S. Y. Ho, M. J. Phillips, and A. Rambaut. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4:e88.
20. Drummond, A. J., and A. Rambaut. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7:214.
21. Drummond, A. J., A. Rambaut, B. Shapiro, and O. G. Pybus. 2005. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol. Biol. Evol. 22:1185-1192.
22. Elvinger, F., A. D. Liggett, K. N. Tang, L. R. Harrison, J. R. Cole, Jr., C. A. Baldwin, and W. B. Nessmith. 1994. Eastern equine encephalomyelitis virus infection in swine. J. Am. Vet. Med. Assoc. 205:1014-1016.
23. Farrar, M. D., D. L. Miller, C. A. Baldwin, S. L. Stiver, and C. L. Hall. 2005. Eastern equine encephalitis in dogs. J. Vet. Diagn. Invest. 17:614-617.
24. Fauquet, C. M., M. A. Mayo, J. Maniloff, U. Desselberger, and L. A. Ball (ed.). 2005. Virus taxonomy: eighth report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, San Diego, CA.
25. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791.
26. Gardner, C. L., J. Yin, C. W. Burke, W. B. Klimstra, and K. D. Ryman. 2009. Type I interferon induction is correlated with attenuation of a South American eastern equine encephalitis virus strain in mice. Virology 390:338-347.
27. Hayes, C. G., and R. C. Wallis. 1977. Ecology of Western equine encephalomyelitis in the eastern United States. Adv. Virus Res. 21:37-83.
28. Kondig, J. P., M. J. Turell, J. S. Lee, M. L. O'Guinn, and L. P. Wasieloski, Jr. 2007. Genetic analysis of South American eastern equine encephalomyelitis viruses isolated from mosquitoes collected in the Amazon Basin region of Peru. Am. J. Trop. Med. Hyg. 76:408-416.
29. Mendez, W., J. Liria, J. C. Navarro, C. Z. Garcia, J. E. Freier, R. Salas, S. C. Weaver, and R. Barrera. 2001. Spatial dispersion of adult mosquitoes (Diptera: Culicidae) in a sylvatic focus of Venezuelan equine encephalitis virus. J. Med. Entomol. 38:813-821.
30. Mitchell, C. J., C. D. Morris, G. C. Smith, N. Karabatsos, D. Vanlandingham, and E. Cody. 1996. Arboviruses associated with mosquitoes from nine Florida counties during 1993. J. Am. Mosq. Control Assoc. 12:255-262.
31. Monath, T. P., M. S. Sabattini, R. Pauli, J. F. Daffner, C. J. Mitchell, G. S. Bowen, and C. B. Cropp. 1985. Arbovirus investigations in Argentina, 1977-1980. IV. Serologic surveys and sentinel equine program. Am. J. Trop. Med. Hyg. 34:966-975.
32. Morris, C. D. 1988. Eastern equine encephalomyelitis, p. 1-36. In T. P. Monath (ed.), The arboviruses: epidemiology and ecology, vol. III. CRC Press, Boca Raton, FL.
33. O'Guinn, M. L., J. S. Lee, J. P. Kondig, R. Fernandez, and F. Carbajal. 2004. Field detection of eastern equine encephalitis virus in the Amazon Basin region of Peru using reverse transcription-polymerase chain reaction adapted for field identification of arthropod-borne pathogens. Am. J. Trop. Med. Hyg. 70:164-171.
34. Platteborze, P. L., J. P. Kondig, R. J. Schoepp, and L. P. Wasieloski. 2005. Comparative sequence analysis of the eastern equine encephalitis virus pathogenic strains FL91-4679 and GA97 to other North American strains. DNA Seq. 16:308-320.
35. Posada, D., and K. A. Crandall. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818.
36. Powers, A. M., P. V. Aguilar, L. J. Chandler, A. C. Brault, T. A. Meakins, D. Watts, K. L. Russell, J. Olson, P. F. Vasconcelos, A. T. Da Rosa, S. C. Weaver, and R. B. Tesh. 2006. Genetic relationships among Mayaro and Una viruses suggest distinct patterns of transmission. Am. J. Trop. Med. Hyg. 75:461-469.
37. Powers, A. M., A. C. Brault, Y. Shirako, E. G. Strauss, W. Kang, J. H. Strauss, and S. C. Weaver. 2001. Evolutionary relationships and systematics of the alphaviruses. J. Virol. 75:10118-10131.
38. Reisen, W. K., and T. P. Monath. 1988. Western equine encephalomyelitis, p. 89-137. In T. P. Monath (ed.), The arboviruses: epidemiology and ecology, vol. V. CRC Press, Boca Raton, FL.
39. Sabattini, M. S., G. Aviles, and T. P. Monath. 1998. Historical, epidemiological, and ecological aspects of arboviruses in Argentina: Togaviridae, Alphavirus, p. 140. In A. P. A. Travassos da Rosa, P. F. C. Vasconcelos, and J. F. S. Travassos da Rosa (ed.), An overview of arbovirology in Brazil and neighbouring countries. Instituto Evandro Chagas, Belem, Brazil.
40. Sabattini, M. S., J. F. Daffner, T. P. Monath, T. I. Bianchi, C. B. Cropp, C. J. Mitchell, and G. Aviles. 1991. Localized eastern equine encephalitis in Santiago del Estero Province, Argentina, without human infection. Medicina 51:3-8.
41. Sabattini, M. S., T. P. Monath, C. J. Mitchell, J. F. Daffner, G. S. Bowen, R. Pauli, and M. S. Contigiani. 1985. Arbovirus investigations in Argentina, 1977-1980. I. Historical aspects and description of study sites. Am. J. Trop. Med. Hyg. 34:937-944.
42. Scherer, W. F., S. C. Weaver, C. A. Taylor, E. W. Cupp, R. W. Dickerman, and H. H. Rubino. 1987. Vector competence of Culex (Melanoconion) taeniopus for allopatric and epizootic Venezuelan equine encephalomyelitis viruses. Am. J. Trop. Med. Hyg. 36:194-197.
43. Scott, T. W., and S. C. Weaver. 1989. Eastern equine encephalomyelitis virus: epidemiology and evolution of mosquito transmission. Adv. Virus Res. 37: 277-328.
44. Shapiro, B., A. Rambaut, and A. J. Drummond. 2006. Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol. Biol. Evol. 23:7-9.
45. Shope, R. E., A. H. D. Andrade, G. Bensabath, O. R. Causey, and P. S. Humphrey. 1966. The epidemiology of EEE WEE, SLE and Turlock viruses, with special reference to birds, in a tropical rain forest near Belem, Brazil. Am. J. Epidemiol. 84:467-477.
46. Strauss, E. G., and J. H. Strauss. 1986. Structure and replication of the alphavirus genome, p. 35-90. In S. Schlesinger and M. Schlesinger (ed.), The togaviruses and flaviviruses. Plenum Press, New York, NY.
47. Swofford, D. L. 1998. PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods), version 4. Sinauer Associates, Sunderland, MA.
48. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
49. Towner, J. S., T. K. Sealy, M. L. Khristova, C. G. Albarino, S. Conlan, S. A. Reeder, P. L. Quan, W. I. Lipkin, R. Downing, J. W. Tappero, S. Okware, J. Lutwama, B. Bakamutumaho, J. Kayiwa, J. A. Comer, P. E. Rollin, T. G. Ksiazek, and S. T. Nichol. 2008. Newly discovered Ebola virus associated with hemorrhagic fever outbreak in Uganda. PLoS Pathog. 4:e1000212.
50. Tully, T. N., Jr., S. M. Shane, R. P. Poston, J. J. England, C. C. Vice, D. Y. Cho, and B. Panigrahy. 1992. Eastern equine encephalitis in a flock of emus (Dromaius novaehollandiae). Avian Dis. 36:808-812.
51. Turell, M. J., J. Barth, and R. E. Coleman. 1999. Potential for Central American mosquitoes to transmit epizootic and enzootic strains of Venezuelan equine encephalitis virus. J. Am. Mosq. Control Assoc. 15:295-298.
52. Turell, M. J., J. W. Jones, M. R. Sardelis, D. J. Dohm, R. E. Coleman, D. M. Watts, R. Fernandez, C. Calampa, and T. A. Klein. 2000. Vector competence of Peruvian mosquitoes (Diptera: Culicidae) for epizootic and enzootic strains of Venezuelan equine encephalomyelitis virus. J. Med. Entomol. 37:835-839.
53. Turell, M. J., M. L. O'Guinn, D. Dohm, M. Zyzak, D. Watts, R. Fernandez, C. Calampa, T. A. Klein, and J. W. Jones. 2008. Susceptibility of Peruvian mosquitoes to eastern equine encephalitis virus. J. Med. Entomol. 45:720-725.
54. van Regenmortel, M. H. V. 2000. Introduction to the species concept in virus taxonomy, p. 3-16. In M. H. V. van Regenmortel, C. M. Fauquet, D. H. L. Bishop, E. B. Carstens, M. K. Estes, S. M. Lemon, J. Maniloff, M. A. Mayo, D. J. McGeogh, C. R. Pringle, and R. B. Wickner (ed.), Virus taxonomy. Classification and nomenclature of viruses, seventh report of the International Committee on Taxonomy of Viruses. Academic Press, San Diego, CA.
55. van Regenmortel, M. H. V., C. M. Fauquet, D. H. L. Bishop, E. B. Carstens, M. K. Estes, S. M. Lemon, J. Maniloff, M. A. Mayo, D. J. McGeogh, C. R. Pringle, and R. B. Wickner (ed.). 2000. Virus taxonomy. Classification and nomenclature of viruses, seventh report of the International Committee on Taxonomy of Viruses. Academic Press, San Diego, CA.
56. Walder, R., and O. M. Suarez. 1976. Studies of arboviruses in southwestern Venezuela. I. Isolations of Venezuelan and eastern equine encephalitis viruses from sentinel hamsters in the Catatumbo region. Int. J. Epidemiol. 5:375-384.
57. Walder, R., O. M. Suarez, and C. H. Calisher. 1984. Arbovirus studies in southwestern Venezuela during 1973-1981. II. Isolations and further studies of Venezuelan and eastern equine encephalitis, Una, Itaqui, and Moju viruses. Am. J. Trop. Med. Hyg. 33:483-491.
58. Walder, R., O. M. Suarez, and C. H. Calisher. 1984. Arbovirus studies in the Guajira region of Venezuela: activities of eastern equine encephalitis and Venezuelan equine encephalitis viruses during an interepizootic period. Am. J. Trop. Med. Hyg. 33:699-707.
59. Weaver, S. C. 2001. Venezuelan equine encephalitis, p. 539-548. In M. W. Service (ed.), The encyclopedia of arthropod-transmitted infections. CAB International, Wallingford, United Kingdom.
60. Weaver, S. C., L. A. Bellew, and R. Rico-Hesse. 1992. Phylogenetic analysis of alphaviruses in the Venezuelan equine encephalitis complex and identification of the source of epizootic viruses. Virology 191:282-290.
61. Weaver, S. C., A. C. Brault, W. Kang, and J. J. Holland. 1999. Genetic and fitness changes accompanying adaptation of an arbovirus to vertebrate and invertebrate cells. J. Virol. 73:4316-4326.
62. Weaver, S. C., C. Ferro, R. Barrera, J. Boshell, and J. C. Navarro. 2004. Venezuelan equine encephalitis. Annu. Rev. Entomol. 49:141-174.
63. Weaver, S. C., A. Hagenbaugh, L. Bellew, and C. H. Calisher. 1992. Genetic characterization of an antigenic subtype of eastern equine encephalomyelitis virus. Arch. Virol. 127:305-314.
64. Weaver, S. C., A. Hagenbaugh, L. A. Bellew, L. Gousset, V. Mallampalli, J. J. Holland, and T. W. Scott. 1994. Evolution of alphaviruses in the eastern equine encephalomyelitis complex. J. Virol. 68:158-169.
65. Weaver, S. C., A. M. Powers, A. C. Brault, and A. D. Barrett. 1999. Molecular epidemiological studies of veterinary arboviral encephalitides. Vet. J. 157: 123-138.
66. Weaver, S. C., R. Rico-Hesse, and T. W. Scott. 1992. Genetic diversity and slow rates of evolution in New World alphaviruses. Curr. Top. Microbiol. Immunol. 176:99-117.
67. Weaver, S. C., W. F. Scherer, C. A. Taylor, D. A. Castello, and E. W. Cupp. 1986. Laboratory vector competence of Culex (Melanoconion) cedecei for sympatric and allopatric Venezuelan equine encephalomyelitis viruses. Am. J. Trop. Med. Hyg. 35:619-623.
68. Weaver, S. C., T. W. Scott, and R. Rico-Hesse. 1991. Molecular evolution of eastern equine encephalomyelitis virus in North America. Virology 182:774-784.
69. Young, D. S., L. D. Kramer, J. G. Maffei, R. J. Dusek, P. B. Backenson, C. N. Mores, K. A. Bernard, and G. D. Ebel. 2008. Molecular epidemiology of eastern equine encephalitis virus, New York. Emerg. Infect. Dis. 14:454-460.