Pseudoinfectious Venezuelan Equine Encephalitis Virus: A New Means of Alphavirus Attenuation

Journal of Virology

Volumn 87, Issue 4, 2013, Pages 2023-2035

  Atasheva, Svetlana ^a   Kim, Dal Young ^a   Akhrymuk, Maryna ^a   Morgan, David G ^b   Frolova, Elena I ^a   Frolov, Ilya ^a  

^a University of Alabama at Birmingham   (United States)

^b INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; VIRUS ANTIGEN; VIRUS DNA; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DNA MODIFICATION; DNA PACKAGING; GENE EXPRESSION; GENE MUTATION; HUMAN; HUMAN CELL; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PSEUDOINFECTION; SAFETY; VENEZUELAN EQUINE ENCEPHALITIS; VENEZUELAN EQUINE ENCEPHALOMYELITIS ALPHAVIRUS; VENEZUELAN EQUINE ENCEPHALOMYELITIS PSEUDOINFECTIOUS VIRUS; VIRION; VIRUS ATTENUATION; VIRUS CAPSID; VIRUS GENOME; VIRUS LIKE AGENT; VIRUS PARTICLE; VIRUS REPLICATION; VIRUS TRANSMISSION;

EID: 84873855544     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/jvi.02881-12     Document Type: Article

References (47)

1. Brown DT, Condreay LD. 1986. Replication of alphaviruses in mosquito cells, In Schlesinger S, Schlesinger MJ (ed), The Togaviridae and Flaviviridae. Plenum Press, New York, NY. p 171-207.
2. Paessler S, Fayzulin RZ, Anishchenko M, Greene IP, Weaver SC, Frolov I. 2003. Recombinant Sindbis/Venezuelan equine encephalitis virus is highly attenuated and immunogenic. J. Virol. 77:9278-9286.
3. Strauss JH, Strauss EG. 1994. The alphaviruses: gene expression, replication, and evolution. Microbiol. Rev. 58:491-562.
4. Dal Canto MC, Rabinowitz SG. 1981. Central nervous system demyelination in Venezuelan equine encephalomyelitis infection. J. Neurol. Sci. 49:397-418.
5. Alevizatos AC, McKinney RW, Feigin RD. 1967. Live, attenuated Ven-ezuelan equine encephalomyelitis virus vaccine. I. Clinical effects in man. Am. J. Trop. Med. Hyg. 16:762-768.
6. Burke DS, Ramsburg HH, Edelman R. 1977. Persistence in humans of antibody to subtypes of Venezuelan equine encephalomyelitis (VEE) virus after immunization with attenuated (TC-83) VEE virus vaccine. J. Infect. Dis. 136:354-359.
7. Pittman PR, Makuch RS, Mangiafico JA, Cannon TL, Gibbs PH, Peters CJ. 1996. Long-term duration of detectable neutralizing antibodies after administration of live-attenuated VEE vaccine and following booster vaccination with inactivated VEE vaccine. Vaccine 14:337-343.
8. Ludwig GV, Turell MJ, Vogel P, Kondig JP, Kell WK, Smith JF, Pratt WD. 2001. Comparative neurovirulence of attenuated and nonattenuated strains of Venezuelan equine encephalitis virus in mice. Am. J. Trop. Med. Hyg. 64:49-55.
9. Kinney RM, Johnson BJB, Welch JB, Tsuchiya KR, Trent DW. 1989. The full-length nucleotide sequences of the virulent Trinidad donkey strain of Venezuelan equine encephalitis virus and its attenuated vaccine derivative, strain TC-83. Virology 170:19-30.
10. Pedersen CE, Jr, Robinson DM, Cole FE, Jr. 1972. Isolation of the vaccine strain of Venezuelan equine encephalomyelitis virus from mosquitoes in Louisiana. Am. J. Epidemiol. 95:490-496.
11. Davis NL, Powell N, Greenwald GF, Willis LV, Johnson BJ, Smith JF, Johnston RE. 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.
12. Wang E, Petrakova O, Adams AP, Aguilar PV, Kang W, Paessler S, Volk SM, Frolov I, Weaver SC. 2007. Chimeric Sindbis/eastern equine encephalitis vaccine candidates are highly attenuated and immunogenic in mice. Vaccine 25:7573-7581.
13. Akahata W, Yang ZY, Andersen H, Sun S, Holdaway HA, Kong WP, Lewis MG, Higgs S, Rossmann MG, Rao S, Nabel GJ. 2010. A virus-like particle vaccine for epidemic Chikungunya virus protects nonhuman primates against infection. Nat. Med. 16:334-338.
14. Mason PW, Shustov AV, Frolov I. 2006. Production and characterization of vaccines based on flaviviruses defective in replication. Virology 351:432-443.
15. Rumyantsev AA, Giel-Moloney M, Liu Y, Gao QS, Zhang ZX, Catalan J, Frolov I, Almond J, Kleanthous H, Pugachev KV. 2011. Characterization of the RepliVax platform for replication-defective flavivirus vaccines. Vaccine 29:5184-5194.
16. Shustov AV, Frolov I. 2010. Efficient, trans-complementing packaging systems for chimeric, pseudoinfectious dengue 2/yellow fever viruses. Virology 400:8-17.
17. Shustov AV, Mason PW, Frolov I. 2007. Production of pseudoinfectious yellow fever virus with a two-component genome. J. Virol. 81:11737-11748.
18. Atasheva S, Krendelchtchikova V, Liopo A, Frolova E, Frolov I. 2010. Interplay of acute and persistent infections caused by Venezuelan equine encephalitis virus encoding mutated capsid protein. J. Virol. 84:10004-10015.
19. Volkova E, Gorchakov R, Frolov I. 2006. The efficient packaging of Venezuelan equine encephalitis virus-specific RNAs into viral particles is determined by nsP1-3 synthesis. Virology 344:315-327.
20. Atasheva S, Garmashova N, Frolov I, Frolova E. 2008. Venezuelan equine encephalitis virus capsid protein inhibits nuclear import in mammalian but not in mosquito cells. J. Virol. 82:4028-4041.
21. Garmashova N, Atasheva S, Kang W, Weaver SC, Frolova E, Frolov I. 2007. Analysis of Venezuelan equine encephalitis virus capsid protein function in the inhibition of cellular transcription. J. Virol. 81:13552-13565.
22. Liljeström P, Lusa S, Huylebroeck D, Garoff H. 1991. In vitro mutagenesis of a full-length cDNA clone of Semliki Forest virus: the small 6,000- molecular-weight membrane protein modulates virus release. J. Virol. 65: 4107-4113.
23. Lemm JA, Durbin RK, Stollar V, Rice CM. 1990. Mutations which alter the level or structure of nsP4 can affect the efficiency of Sindbis virus replication in a host-dependent manner. J. Virol. 64:3001-3011.
24. Perera R, Navaratnarajah C, Kuhn RJ. 2003. A heterologous coiled coil can substitute for helix I of the Sindbis virus capsid protein. J. Virol. 77:8345-8353.
25. Perera R, Owen KE, Tellinghuisen TL, Gorbalenya AE, Kuhn RJ. 2001. Alphavirus nucleocapsid protein contains a putative coiled coil alphahelix important for core assembly. J. Virol. 75:1-10.
26. Atasheva S, Fish A, Fornerod M, Frolova EI. 2010. Venezuelan equine encephalitis virus capsid protein forms a tetrameric complex with CRM1 and importin alpha/beta that obstructs nuclear pore complex function. J. Virol. 84:4158-4171.
27. Weiss B, Nitschko H, Ghattas I, Wright R, Schlesinger S. 1989. Evidence for specificity in the encapsidation of Sindbis RNAs. J. Virol. 63:5310-5318.
28. Zhang R, Hryc CF, Cong Y, Liu X, Jakana J, Gorchakov R, Baker ML, Weaver SC, Chiu W. 2011. A cryo-EM structure of an enveloped alphavirus Venezuelan equine encephalitis virus. EMBO J. 30:3854-3863.
29. Thompson JM, Whitmore AC, Konopka JL, Collier ML, Richmond EM, Davis NL, Staats HF, Johnston RE. 2006. Mucosal and systemic adjuvant activity of alphavirus replicon particles. Proc. Natl. Acad. Sci. USA. 103:3722-3727.
30. Konopka JL, Thompson JM, Whitmore AC, Webb DL, Johnston RE. 2009. Acute infection with Venezuelan equine encephalitis virus replicon particles catalyzes a systemic antiviral state and protects from lethal virus challenge. J. Virol. 83:12432-12442.
31. Frolov I, Schlesinger S. 1996. Translation of Sindbis virus mRNA: analysis of sequences downstream of the initiating AUG codon that enhance translation. J. Virol. 70:1182-1190.
32. Barry G, Fragkoudis R, Ferguson MC, Lulla A, Merits A, Kohl A, Fazakerley JK. 2010. Semliki Forest virus-induced endoplasmic reticulum stress accelerates apoptotic death of mammalian cells. J. Virol. 84:7369-7377.
33. Kamrud KI, Alterson K, Custer M, Dudek J, Goodman C, Owens G, Smith JF. 2010. Development and characterization of promoterless helper RNAs for the production of alphavirus replicon particle. J. Gen. Virol. 91:1723-1727.
34. Weiss BG, Schlesinger S. 1991. Recombination between Sindbis virus RNAs. J. Virol. 65:4017-4025.
35. Forsell K, Xing L, Kozlovska T, Cheng RH, Garoff H. 2000. Membrane proteins organize a symmetrical virus. EMBO J. 19:5081-5091.
36. Frolov I, Frolova E, Schlesinger S. 1997. Sindbis virus replicons and Sindbis virus: assembly of chimeras and of particles deficient in virus RNA. J. Virol. 71:2819-2829.
37. Smerdou C, Liljestrom P. 1999. Two-helper RNA system for production of recombinant Semliki Forest virus particles. J. Virol. 73:1092-1098.
38. Elliott MB, Chen T, Terio NB, Chong SY, Abdullah R, Luckay A, Egan MA, Boutilier LA, Melville K, Lerch RA, Long D, Eldridge JH, Parks CL, Udem SA, Hancock GE. 2007. Alphavirus replicon particles encoding the fusion or attachment glycoproteins of respiratory syncytial virus elicit protective immune responses in BALB/c mice and functional serum antibodies in rhesus macaques. Vaccine 25:7132-7144.
39. Foy BD, Olson KE. 2008. Alphavirus transducing systems. Adv. Exp. Med. Biol. 627:19-34.
40. Gorchakov R, Volkova E, Yun N, Petrakova O, Linde NS, Paessler S, Frolova E, Frolov I. 2007. Comparative analysis of the alphavirus-based vectors expressing Rift Valley fever virus glycoproteins. Virology 366:212-225.
41. Liljestrom P. 1994. Alphavirus expression systems. Curr. Opin. Biotechnol. 5:495-500.
42. Phillips A, Mossel E, Sanchez-Vargas I, Foy B, Olson K. 2010. Alphavirus transducing system: tools for visualizing infection in mosquito vectors. J. Vis. Exp. 2010:2363. doi:10.3791/2363.
43. Frolov I, Hoffman TA, Prágai BM, Dryga SA, Huang HV, Schlesinger S, Rice CM. 1996. Alphavirus-based expression systems: strategies and applications. Proc. Natl. Acad. Sci. USA. 93:11371-11377.
44. Donnelly JJ, Wahren B, Liu MA. 2005. DNA vaccines: progress and challenges. J. Immunol. 175:633-639.
45. Hariharan MJ, Driver DA, Townsend K, Brumm D, Polo JM, Belli BA, Catton DJ, Hsu D, Mittelstaedt D, McCormack JE, Karavodin L, Dubensky TW, Jr, Chang SM, Banks TA. 1998. DNA immunization against herpes simplex virus: enhanced efficacy using a Sindbis virusbased vector. J. Virol. 72:950-958.
46. Leitner WW, Ying H, Driver DA, Dubensky TW, Restifo NP. 2000. Enhancement of tumor-specific immune response with plasmid DNA replicon vectors. Cancer Res. 60:51-55.
47. Thompson JM, Whitmore AC, Staats HF, Johnston RE. 2008. Alphavirus replicon particles acting as adjuvants promote CD8T cell responses to co-delivered antigen. Vaccine 26:4267-4275.