Eastern and Venezuelan equine encephalitis viruses differ in their ability to infect dendritic cells and macrophages: Impact of altered cell tropism on pathogenesis

Journal of Virology

Volumn 82, Issue 21, 2008, Pages 10634-10646

  Gardner, Christina L ^a   Burke, Crystal W ^a   Tesfay, Mulu Z ^a   Glass, Pamela J ^b   Klimstra, William B ^a   Ryman, Kate D ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b UNITED STATES ARMY MEDICAL RESEARCH INSTITUTE OF INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; PROTEIN KINASE R; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL GROWTH; CONTROLLED STUDY; DENDRITIC CELL; EASTERN EQUINE ENCEPHALOMYELITIS VIRUS; FIBROBLAST; MACROPHAGE; MOUSE; NONHUMAN; OSTEOBLAST; PATHOGENESIS; PRIORITY JOURNAL; RNA TRANSLATION; VENEZUELAN EQUINE ENCEPHALOMYELITIS ALPHAVIRUS; VIREMIA; VIRUS INFECTIVITY; VIRUS REPLICATION; VIRUS VIRULENCE; ANIMAL; BIOSYNTHESIS; BLOOD; CELL CULTURE; CELL LINE; COMPARATIVE STUDY; ENCEPHALOMYELITIS; GROWTH, DEVELOPMENT AND AGING; HAMSTER; PROTEIN SYNTHESIS; SURVIVAL; VIROLOGY;

MOSQUITO-BORNE VIRUSES; VENEZUELAN EQUINE ENCEPHALITIS VIRUS;

ANIMALS; CELL LINE; CELLS, CULTURED; CRICETINAE; DENDRITIC CELLS; ENCEPHALITIS VIRUS, EASTERN EQUINE; ENCEPHALITIS VIRUS, VENEZUELAN EQUINE; ENCEPHALOMYELITIS, EQUINE; ENCEPHALOMYELITIS, VENEZUELAN EQUINE; FIBROBLASTS; INTERFERON-ALPHA; INTERFERON-BETA; MACROPHAGES; MICE; OSTEOBLASTS; PROTEIN BIOSYNTHESIS; SURVIVAL ANALYSIS; VIRAL PROTEINS;

EID: 55249092120     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01323-08     Document Type: Article

References (57)

1. Aguilar, P. V., A. P. Adams, E. Wang, W. Kang, A.-S. 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., L. W. Leung, E. Wang, S. C. Weaver, and C. F. Basler. 2008. A five-amino-acid deletion of the eastern equine encephalitis virus capsid protein attenuates replication in mammalian systems but not in mosquito cells. J. Virol. 82:6972-6983.
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., 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.
5. 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.
6. Aronson, J. F., F. B. Grieder, N. L. Davis, P. C. Charles, T. Knott, K. Brown, and R. E. Johnston. 2000. A single-site mutant and revertants arising in vivo define early steps in the pathogenesis of Venezuelan equine encephalitis virus. Virology 270:111-123.
7. Bakker, A., and J. Klein-Nulend. 2003. Osteoblast isolation from murine calvariae and long bones. Methods Mol. Med. 80:19-28.
8. Berben-Bloemheuvel, G., M. A. Kasperaitis, H. van Heugten, A. A. Thomas, H. van Steeg, and H. O. Voorma. 1992. Interaction of initiation factors with the cap structure of chimaeric mRNA containing the 5′-untranslated regions of Semliki Forest virus RNA is related to translational efficiency. Eur. J. Biochem. 208:581-587.
9. 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.
10. 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.
11. Castello, A., M. A. Sanz, S. Molina, and L. Carrasco. 2006. Translation of Sindbis virus 26S mRNA does not require intact eukaryotic initiation factor 4G. J. Mol. Biol. 355:942-956.
12. Centers for Disease Control and Prevention. 2008. Confirmed and probable eastern equine encephalitis cases, human, United States, 1964-2007, by state. http://www.cdc.gov/ncidod/dvbid/Arbor/pdf/EEE_DOC.pdf.
13. Charles, P. C., J. Trgovcich, N. L. Davis, and R. E. Johnston. 2001. Immunopathogenesis and immune modulation of Venezuelan equine encephalitis virus-induced disease in the mouse. Virology 284:190-202.
14. 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.
15. Colina, R., M. Costa-Mattioli, R. J. Dowling, M. Jaramillo, L. H. Tai, C. J. Breitbach, Y. Martineau, O. Larsson, L. Rong, Y. V. Svitkin, A. P. Makrigiannis, J. C. Bell, and N. Sonenberg. 2008. Translational control of the innate immune response through IRF-7. Nature 452:323-328.
16. de la Monte, S., F. Castro, N. J. Bonilla, A. Gaskin de Urdaneta, and G. M. Hutchins. 1985. The systemic pathology of Venezuelan equine encephalitis virus infection in humans. Am. J. Trop. Med. Hyg. 34:194-202.
17. Deresiewicz, R. L., S. J. Thaler, L. Hsu, and A. A. Zamani. 1997. Clinical and neuroradiographic manifestations of eastern equine encephalitis. N. Engl. J. Med. 336:1867-1874.
18. Edgil, D., M. S. Diamond, K. L. Holden, S. M. Paranjape, and E. Harris. 2003. Translation efficiency determines differences in cellular infection among dengue virus type 2 strains. Virology 317:275-290.
19. Frolov, I., R. Hardy, and C. M. Rice. 2001. Cis-acting RNA elements at the 5′ end of Sindbis virus genome RNA regulate minus- and plus-strand RNA synthesis. RNA 7:1638-1651.
20. Gardner, J. P., I. Frolov, S. Perri, Y. Ji, M. L. MacKichan, J. zur Megede, M. Chen, B. A. Belli, D. A. Driver, S. Sherrill, C. E. Greer, G. R. Otten, S. W. Barnett, M. A. Liu, T. W. Dubensky, and J. M. Polo. 2000. Infection of human dendritic cells by a Sindbis virus replicon vector is determined by a single amino acid substitution in the E2 glycoprotein. J. Virol. 74:11849-11857.
21. Garmashova, N., S. Atasheva, W. Kang, S. C. Weaver, E. Frolova, and I. Frolov. 2007. Analysis of Venezuelan equine encephalitis virus capsid protein function in the inhibition of cellular transcription. J. Virol. 81:13552-13565.
22. 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 transcriptional shutoff. J. Virol. 81:2472-2484.
23. Grieder, F. B., B. K. Davis, X. D. Zhou, S. J. Chen, F. D. Finkelman, and W. C. Gause. 1997. Kinetics of cytokine expression and regulation of host protection following infection with molecularly cloned Venezuelan equine encephalitis virus. Virology 233:302-312.
24. 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.
25. Grieder, F. B., and S. N. Vogel. 1999. Role of interferon and interferon regulatory factors in early protection against Venezuelan equine encephalitis virus infection. Virology 257:106-118.
26. Griffin, D. E. 2001. Alphaviruses, p. 917-962. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology. Lippincott Williams & Wilkins, Philadelphia, PA.
27. Hurst, E. 1936. Infection of the rhesus monkey (Macaca mulatta) and the guinea-pig with the virus of equine encephalomyelitis. J. Pathol Bacteriol. 42:271-302.
28. Johnson, K. M., and D. H. Martin. 1974. Venezuelan equine encephalitis. Adv. Vet. Sci. Comp. Med. 18:79-116.
29. Klimstra, W. B., K. D. Ryman, 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.
30. Klimstra, W. B., J. C. Williams, K. D. Ryman, and H. W. Heidner. 2005. Targeting Sindbis virus-based vectors to Fc receptor-positive cell types. Virology 338:9-21.
31. Konopka, J. L., L. O. Penalva, J. M. Thompson, L. J. White, C. W. Beard, J. D. Keene, and R. E. Johnston. 2007. A two-phase innate host response to alphavirus infection identified by mRNP-tagging in vivo. PLoS Pathog. 3:e199.
32. Levitt, N. H., H. V. Miller, and R. Edelman. 1979. Interaction of alphaviruses with human peripheral leukocytes: in vitro replication of Venezuelan equine encephalomyelitis virus in monocyte cultures. Infect. Immun. 24:642-646.
33. Liu, C., D. W. Voth, P. Rodina, L. R. Shauf, and G. Gonzalez. 1970. A comparative study of the pathogenesis of western equine and eastern equine encephalomyelitis viral infections in mice by intracerebral and subcutaneous inoculations. J. Infect. Dis. 122:53-63.
34. MacDonald, G. H., and R. E. Johnston. 2000. Role of dendritic cell targeting in Venezuelan equine encephalitis virus pathogenesis. J. Virol. 74:914-922.
35. Mitchell, C. J., M. L. Niebylski, G. C. Smith, N. Karabatsos, D. Martin, J. P. Mutebi, G. B. Craig, Jr., and M. J. Mahler. 1992. Isolation of eastern equine encephalitis virus from Aedes albopictus in Florida. Science 257:526-527.
36. Moran, T. P., M. Collier, K. P. McKinnon, N. L. Davis, R. E. Johnston, and J. S. Serody. 2005. A novel viral system for generating antigen-specific T cells. J. Immunol. 175:3431-3438.
37. Paessler, S., P. Aguilar, M. Anishchenko, H. Q. Wang, J. Aronson, G. Campbell, A. S. Cararra, and S. C. Weaver. 2004. The hamster as an animal model for eastern equine encephalitis - and its use in studies of virus entrance into the brain. J. Infect. Dis. 189:2072-2076.
38. Perri, S., C. E. Greer, K. Thudium, B. Doe, H. Legg, H. Liu, R. E. Romero, Z. Tang, Q. Bin, T. W. Dubensky, Jr., M. Vajdy, G. R. Otten, and J. M. Polo. 2003. An alphavirus replicon particle chimera derived from Venezuelan equine encephalitis and Sindbis viruses is a potent gene-based vaccine delivery vector. J. Virol. 77:10394-10403.
39. Pushko, P., M. Parker, G. V. Ludwig, N. L. Davis, R. E. Johnston, and J. F. Smith. 1997. Replicon-helper systems from attenuated Venezuelan equine encephalitis virus: expression of heterologous genes in vitro and immunization against heterologous pathogens in vivo. Virology 239:389-401.
40. Ryman, K. D., C. L. Gardner, K. C. Meier, C. A. Biron, R. E. Johnston, and W. B. Klimstra. 2007. Early restriction of alphavirus replication and dissemination contributes to age-dependent attenuation of systemic hyperinflammatory disease. J. Gen. Virol. 88:518-529.
41. Ryman, K. D., C. L. Gardner, C. L. Wyza, 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.
42. Ryman, K. D., W. B. Klimstra, K. B. Nguyen, C. A. Biron, and R. E. Johnston. 2000. Alpha/beta interferon protects adult mice from fatal Sindbis virus infection and is an important determinant of cell and tissue tropism. J. Virol. 74:3366-3378.
43. Ryman, K. D., K. C. Meier, E. M. Nangle, S. L. Ragsdale, N. L. Korneeva, R. E. Rhoads, M. R. Macdonald, and W. B. Klimstra. 2005. Sindbis virus translation is inhibited by a PKR/RNase L-independent effector induced by alpha/beta interferon priming of dendritic cells. J. Virol. 79:1487-1499.
44. 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.
45. Ryzhikov, A. B., E. I. Ryabchikova, A. N. Sergeev, and N. V. Tkacheva. 1995. Spread of Venezuelan equine encephalitis virus in mice olfactory tract. Arch. Virol. 140:2243-2254.
46. Schoepp, R. J., J. F. Smith, and M. D. Parker. 2002. Recombinant chimeric western and eastern equine encephalitis viruses as potential vaccine candidates. Virology 302:299-309.
47. Smit, J. M., B. L. Waarts, K. Kimata, W. B. Klimstra, R. Bittman, and J. Wilschut. 2002. Adaptation of alphaviruses to heparan sulfate: interaction of Sindbis and Semliki Forest viruses with liposomes containing lipid-conjugated heparin. J. Virol. 76:10128-10137.
48. Strauss, J. H., and E. G. Strauss. 1994. The alphaviruses: gene expression, replication, and evolution. Microbiol. Rev. 58:491-562.
49. Tesfay, M. Z., J. Yin, C. L. Gardner, M. V. Khoretonenko, N. L. Korneeva, R. E. Rhoads, K. D. Ryman, and W. B. Klimstra. 2008. Alpha/beta interferon inhibits cap-dependent translation of viral but not cellular mRNA by a PKR-independent mechanism. J. Virol. 82:2620-2630.
50. Trgovcich, J., J. F. Aronson, and R. E. Johnston. 1996. Fatal Sindbis virus infection of neonatal mice in the absence of encephalitis. Virology 224:73-83.
51. 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.
52. Wacher, C., M. Muller, M. J. Hofer, D. R. Getts, R. Zabaras, S. S. Ousman, F. Terenzi, G. C. Sen, N. J. King, and I. L. Campbell. 2007. Coordinated regulation and widespread cellular expression of interferon-stimulated genes (ISG) ISG-49, ISG-54, and ISG-56 in the central nervous system after infection with distinct viruses. J. Virol. 81:860-871.
53. Walton, T. E., and M. A. Grayson. 1989. Venezuelan equine encephalomyelitis, p. 203-231. In T. P. Monath (ed.), The arboviruses: epidemiology and ecology, vol. 4. CRC Press, Boca Raton, FL.
54. 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.
55. 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.
56. 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.
57. Zuker, M. 2000. Calculating nucleic acid secondary structure. Curr. Opin. Struct. Biol. 10:303-310.