Structural and nonstructural protein genome regions of eastern equine encephalitis virus are determinants of interferon sensitivity and murine virulence

Journal of Virology

Volumn 82, Issue 10, 2008, Pages 4920-4930

  Aguilar, Patricia V ^a,b   Adams, A Paige ^a,b   Wang, Eryu ^a,b   Kang, Wenli ^a,b   Carrara, Anne Sophie ^a,b   Anishchenko, Michael ^a,b   Frolov, Ilya ^a,b   Weaver, Scott C ^a,b  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; GAMMA INTERFERON; NONSTRUCTURAL PROTEIN 1; STRUCTURAL PROTEIN; INTERFERON; VIRUS PROTEIN;

ARTICLE; BRAIN INFECTION; CHIMERA; CONTROLLED STUDY; EASTERN EQUINE ENCEPHALOMYELITIS VIRUS; FATALITY; GENOME; NONHUMAN; PLANT GROWTH; PRIORITY JOURNAL; STRAIN DIFFERENCE; VIREMIA; VIRUS REPLICATION; VIRUS RESISTANCE; VIRUS STRAIN; VIRUS VIRULENCE; ANIMAL; ENCEPHALOMYELITIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; LD 50; MOUSE; PATHOGENICITY; PHYSIOLOGY; SURVIVAL; VIROLOGY; VIRULENCE; VIRUS CULTURE;

EASTERN EQUINE ENCEPHALITIS VIRUS; EQUIDAE; MURINAE; MUS;

ANIMALS; ENCEPHALITIS VIRUS, EASTERN EQUINE; ENCEPHALOMYELITIS, EQUINE; INTERFERONS; LETHAL DOSE 50; MICE; PLAQUE ASSAY; SURVIVAL ANALYSIS; VIRAL NONSTRUCTURAL PROTEINS; VIRAL STRUCTURAL PROTEINS; VIREMIA; VIRULENCE;

EID: 43249104024     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02514-07     Document Type: Article

References (66)

1. 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.
2. 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.
3. Aguilar, P. V., S. C. Weaver, and C. F. Basler. 2007. Capsid protein of Eastern equine encephalitis virus inhibits host cell gene expression. J. Virol. 81:3866-3876.
4. Anishchenko, M., S. Paessler, I. P. Greene, P. V. Aguilar, A. S. Carrara, and S. C. Weaver. 2004. Generation and characterization of closely related epizootic and enzootic infectious cDNA clones for studying interferon sensitivity and emergence mechanisms of Venezuelan equine encephalitis virus. J. Virol. 78:1-8.
5. Bear, J. S., A. P. Byrnes, and D. E. Griffin. 2006. Heparin-binding and patterns of virulence for two recombinant strains of Sindbis virus. Virology 347:183-190.
6. Berlanga, J. J., I. Ventoso, H. P. Harding, J. Deng, D. Ron, N. Sonenberg, L. Carrasco, and C. de Haro. 2006. Antiviral effect of the mammalian translation initiation factor 2alpha kinase GCN2 against RNA viruses. EMBO J. 25:1730-1740.
7. Bernard, K. A., W. B. Klimstra, and R. E. Johnston. 2000. Mutations in the E2 glycoprotein of Venezuelan equine encephalitis virus confer heparan sulfate interaction, low morbidity, and rapid clearance from blood of mice. Virology 276:93-103.
8. Bick, M. J., J. W. Carroll, G. Gao, S. P. Goff, C. M. Rice, and M. R. MacDonald. 2003. Expression of the zinc-finger antiviral protein inhibits alphavirus replication. J. Virol. 77:11555-11562.
9. 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.
10. Brault, A. C., A. M. Powers, E. C. Holmes, C. H. Woelk, and S. C. Weaver. 2002. Positively charged amino acid substitutions in the E2 envelope glycoprotein are associated with the emergence of Venezuelan equine encephalitis virus. J. Virol. 76:1718-1730.
11. Brault, A. C., A. M. Powers, D. Ortiz, J. G. Estrada-Franco, R. Navarro-Lopez, and S. C. Weaver. 2004. Venezuelan equine encephalitis emergence: enhanced vector infection from a single amino acid substitution in the envelope glycoprotein. Proc. Natl. Acad. Sci. USA 101:11344-11349.
12. Byrnes, A. P., and D. E. Griffin. 1998. Binding of Sindbis virus to cell surface heparan sulfate. J. Virol. 72:7349-7356.
13. Byrnes, A. P., and D. E. Griffin. 2000. Large-plaque mutants of Sindbis virus show reduced binding to heparan sulfate, heightened viremia, and slower clearance from the circulation. J. Virol. 74:644-651.
14. 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. Intervirology 14:229-232.
15. Casals, J. 1964. Antigenic variants of Eastern equine encephalitis virus. J. Exp. Med. 119:547-565.
16. Charles, P. C., E. Walters, F. Margolis, and R. E. Johnston. 1995. Mechanism of neuroinvasion of Venezuelan equine encephalitis virus in the mouse. Virology 208:662-671.
17. Davis, N. L., F. J. Fuller, W. G. Dougherty, R. A. Olmsted, and R. E. Johnston. 1986. A single nucleotide change in the E2 glycoprotein gene of Sindbis virus affects penetration rate in cell culture and virulence in neonatal mice. Proc. Natl. Acad. Sci. USA 83:6771-6775.
18. Davis, N. L., N. Powell, G. F. Greenwald, L. V. Willis, B. J. Johnson, J. F. Smith, and R. E. Johnston. 1991. Attenuating mutations in the E2 glycoprotein gene of Venezuelan equine encephalitis virus: construction of single and multiple mutants in a full-length cDNA clone. Virology 183:20-31.
19. Dropulic, L. K., J. M. Hardwick, and D. E. Griffin. 1997. A single amino acid change in the E2 glycoprotein of Sindbis virus confers neurovirulence by altering an early step of virus replication. J. Virol. 71:6100-6105.
20. Farber, S., A. Hill, M. L. Connerly, and J. H. Dingle. 1940. Encephalitis in infants and children caused by the virus of the Eastern variety of equine encephalitis. JAMA 114:1725-1731.
21. Feemster, R. F., and W. Haymaker. 1958. Eastern equine encephalitis. Neurology 8:882-883.
22. Fothergill, L. D., J. H. Dingle, and J. J. Fellow. 1938. A fatal disease of pigeons caused by the virus of the Eastern variety of equine encephalomyelitis. Science 88:549-550.
23. Frolova, E. I., R. Z. Fayzulin, S. H. Cook, D. E. Griffin, C. M. Rice, and I. Frolov. 2002. Roles of nonstructural protein nsP2 and alpha/beta interferons in determining the outcome of Sindbis virus infection. J. Virol. 76:11254-11264.
24. Garmashova, N., R. Gorchakov, E. Volkova, S. Paessler, E. Frolova, and I. Frolov. 2007. The Old World and New World alphaviruses use different virus-specific proteins for induction of the transcriptional shutoff. J. Virol. 81:2472-2484.
25. Giltner, L. T., and M. S. Shahan. 1933. The 1933 outbreak of infectious equine encephalomyelitis in the Eastern states. North Am. Vet. 14:25-27.
26. Glasgow, G. M., H. M. Killen, P. Liljestrom, B. J. Sheahan, and G. J. Atkins. 1994. A single amino acid change in the E2 spike protein of a virulent strain of Semliki Forest virus attenuates pathogenicity. J. Gen. Virol. 75:663-668.
27. Greene, I. P., S. Paessler, M. Anishchenko, D. R. Smith, A. C. Brault, I. Frolov, and S. C. Weaver. 2005. Venezuelan equine encephalitis virus in the guinea pig model: evidence for epizootic virulence determinants outside the E2 envelope glycoprotein gene. Am. J. Trop. Med. Hyg. 72:330-338.
28. Greene, I. P., S. Paessler, L. Austgen, M. Anishchenko, A. C. Brault, R. A. Bowen, and S. C. Weaver. 2005. Envelope glycoprotein mutations mediate equine amplification and virulence of epizootic Venezuelan equine encephalitis virus. J. Virol. 79:9128-9133.
29. Grieder, F. B., N. L. Davis, J. F. Aronson, P. C. Charles, D. C. Sellon, K. Suzuki, and R. E. Johnston. 1995. Specific restrictions in the progression of Venezuelan equine encephalitis virus-induced disease resulting from single amino acid changes in the glycoproteins. Virology 206:994-1006.
30. Guo, X., J. W. Carroll, M. R. Macdonald, S. P. Goff, and G. Gao. 2004. The zinc finger antiviral protein directly binds to specific viral mRNAs through the CCCH zinc finger motifs. J. Virol. 78:12781-12787.
31. Heil, M. L., A. Albee, J. H. Strauss, and R. J. Kuhn. 2001. An amino acid substitution in the coding region of the E2 glycoprotein adapts Ross River virus to utilize heparan sulfate as an attachment moiety. J. Virol. 75:6303-6309.
32. Jackson, A. C., S. K. SenGupta, and J. F. Smith. 1991. Pathogenesis of Venezuelan equine encephalitis virus infection in mice and hamsters. Vet. Pathol. 28:410-418.
33. Johnston, R. E., and C. J. Peters. 1996. Alphaviruses, p. 843-898. In B. N. Fields, D. M. Knipe, and P. Howley (ed.), Fields virology, 3rd ed. Lippincott-Raven Publishers, Philadelphia, PA.
34. Klimstra, W. B., Ryman, K. D., and R. E. Johnston. 1998. Adaptation of Sindbis virus to BHK cells selects for use of heparan sulfate as an attachment receptor. J. Virol. 72:7357-7366.
35. Kobiler, D., C. M. Rice, C. Brodie, A. Shahar, J. Dubuisson, M. Halevy, and S. Lustig. 1999. A single nucleotide change in the 5′ noncoding region of Sindbis virus confers neurovirulence in rats. J. Virol. 73:10440-10446.
36. Lennette, E. H., D. Lennette, and E. T. Lennette. 1995. Diagnostic procedures for viral, rickettsial, and chlamydial infections. American Public Health Association, Washington, DC.
37. Lenschow, D. J., C. Lai, N. Frias-Staheli, N. V. Giannakopoulos, A. Lutz, T. Wolff, A. Osiak, B. Levine, R. E. Schmidt, A. Garcia-Sastre, D. A. Leib, A. Pekosz, K.-P. Knobeloch, I. Horak, and H. W. Virgin. 2007. IFN-stimulated gene 15 functions as a critical antiviral molecule against influenza, herpes, and Sindbis viruses. Proc. Natl. Acad. Sci. USA 104:1371-1376.
38. Lustig, S., A. C. Jackson, C. S. Hahn, D. E. Griffin, E. G. Strauss, and J. H. Strauss. 1988. Molecular basis of Sindbis virus neurovirulence in mice. J. Virol. 62:2329-2336.
39. Morris, C. 1988. Eastern equine encephalomyelitis, p. 1-36. In T. P. Monath (ed.), The arboviruses: epidemiology and ecology, vol. III. CRC Press, Boca Raton, FL.
40. Polo, J. M., and R. E. Johnston. 1990. Attenuating mutations in glycoproteins E1 and E2 of Sindbis virus produce a highly attenuated strain when combined in vitro. J. Virol. 64:4438-4444.
41. Powers, A. M., A. C. Brault, R. M. Kinney, and S. C. Weaver. 2000. The use of chimeric Venezuelan equine encephalitis viruses as an approach for the molecular identification of natural virulence determinants. J. Virol. 74:4258-4263.
42. Powers, A. M., K. I. Kamrud, K. E. Olson, S. Higgs, J. O. Carlson, and B. J. Beaty. 1996. Molecularly engineered resistance to California serogroup virus replication in mosquito cells and mosquitoes. Proc. Natl. Acad. Sci. USA 93:4187-4191.
43. Reed, L. J., and H. Muench. 1938. A simple method of estimating fifty percent endpoints. Am. J. Hyg. 27:493-497.
44. Roehrig, J. T., A. R. Hunt, G. J. Chang, B. Sheik, R. A. Bolin, T. F. Tsai, and D. W. Trent. 1990. Identification of monoclonal antibodies capable of differentiating antigenic varieties of Eastern equine encephalitis viruses. Am. J. Trop. Med. Hyg. 42:394-398.
45. Russell, D. L., J. M. Dalrymple, and R. E. Johnston. 1989. Sindbis virus mutations which coordinately affect glycoprotein processing, penetration, and virulence in mice. J. Virol. 63:1619-1629.
46. Ryman, K. D., C. L. Gardner, C. W. Burke, K. C. Meier, J. M. Thompson, and W. B. Klimstra. 2007. Heparan sulfate binding can contribute to the neurovirulence of neuroadapted and nonneuroadapted Sindbis viruses. J. Virol. 81:3563-3573.
47. Ryman, K. D., L. J. White, R. E. Johnston, and W. B. Klimstra. 2002. Effects of PKR/RNase L-dependent and alternative antiviral pathways on alphavirus replication and pathogenesis. Viral Immunol. 15:53-76.
48. Santagati, M. G., J. A. Maatta, P. V. Itaranta, A. A. Salmi, and A. E. Hinkkanen. 1995. The Semliki Forest virus E2 gene as a virulence determinant. J. Gen. Virol. 76:47-52.
49. Schlesinger, S., and M. J. Schlesinger. 1996. Togaviridae: the viruses and their replication, p. 523-539. In B. N. Fields, D. M. Knipe, and P. Howley (ed.), Fundamental virology. Lippincott-Raven, Philadelphia, PA.
50. Schoepp, R. J., and R. E. Johnston. 1993. Directed mutagenesis of a Sindbis virus pathogenesis site. Virology 193:149-159.
51. Scott, T. W., and S. C. Weaver. 1989. Eastern equine encephalitides virus: epidemiology and evolution of mosquito transmission. Adv. Virus Res. 37: 277-328.
52. Spotts, D. R., R. M. Reich, M. A. Kalkhan, R. M. Kinney, and J. T. Roehrig. 1998. Resistance to alpha/beta interferons correlates with the epizootic and virulence potential of Venezuelan equine encephalitis viruses and is determined by the 5′ noncoding region and glycoproteins. J. Virol. 72:10286-10291.
53. Strauss, J. H., and E. G. Strauss. 1994. The alphaviruses: gene expression, replication, and evolution. Microbiol. Rev. 58:491-562.
54. TenBroeck, C., and M. H. Merrill. 1933. A serological difference between Eastern and Western equine encephalomyelitis virus. Proc. Soc. Exp. Biol Med. 31:217-220.
55. Tucker, P. C., and D. E. Griffin. 1991. Mechanism of altered Sindbis virus neurovirulence associated with a single-amino-acid change in the E2 glycoprotein. J. Virol. 65:1551-1557.
56. Tucker, P. C., E. G. Strauss, R. J. Kuhn, J. H. Strauss, and D. E. Griffin. 1993. Viral determinants of age-dependent virulence of Sindbis virus for mice. J. Virol. 67:4605-4610.
57. Tuittila, M., and A. E. Hinkkanen. 2003. Amino acid mutations in the replicase protein nsP3 of Semliki Forest virus cumulatively affect neurovirulence. J. Gen. Virol. 84:1525-1533.
58. Tuittila, M. T., M. G. Santagati, M. Roytta, J. A. Maatta, and A. E. Hinkkanen. 2000. Replicase complex genes of Semliki Forest virus confer lethal neurovirulence. J. Virol. 74:4579-4589.
59. Vogel, P., W. M. Kell, D. L. Fritz, M. D. Parker, and R. J. Schoepp. 2005. Early events in the pathogenesis of Eastern equine encephalitis virus in mice. Am. J. Pathol. 166:159-171.
60. Walder, R., P. B. Jahrling, and G. A. Eddy. 1980. Differentiation markers of eastern equine encephalitis (EEE) viruses and virulence, p. 237-250. In J. Vesenjak-Hirjan (ed.), Arboviruses in the Mediterranean countries. Fisher, Stuttgart, Germany.
61. Wang, E., O. Petrakova, A. P. Adams, P. V. Aguilar, W. Kang, S. Paessler, S. M. Volk, I. Frolov, and S. C. Weaver. 2007. Chimeric Sindbis/Eastern equine encephalitis vaccine candidates are highly attenuated and immunogenic in mice. Vaccine 25:7573-7581.
62. Weaver, S. C. 2001. Eastern equine encephalitis. In M. W. Service (ed.), The encyclopedia of arthropod-transmitted infections. CAB International, Wallingford, United Kingdom.
63. Weaver, S. C., M. Anishchenko, R. Bowen, A. C. Brault, J. G. Estrada-Franco, Z. Fernandez, I. Greene, D. Ortiz, S. Paessler, and A. M. Powers. 2004. Genetic determinants of Venezuelan equine encephalitis emergence. Arch. Virol. Suppl. 18:43-64.
64. Weaver, S. C., M. Pfeffer, K. Marriot, W. Kang, and R. M. Kinney. 1999. Genetic evidence for the origins of Venezuelan equine encephalitis virus subtype IAB outbreaks. Am. J. Trop. Med. Hyg. 60:441-448.
65. White, L. J., J. G. Wang, N. L. Davis, and R. E. Johnston. 2001. Role of alpha/beta interferon in Venezuelan equine encephalitis virus pathogenesis: effect of an attenuating mutation in the 5′ untranslated region. J. Virol. 75:3706-3718.
66. Zhang, Y., C. W. Burke, K. D. Ryman, and W. B. Klimstra. 2007. Identification and characterization of interferon-induced proteins that inhibit alphavirus replication. J. Virol. 81:11246-11255.