Enhancement of protein expression by alphavirus replicons by designing self-replicating subgenomic RNAs

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 29, 2014, Pages 10708-10713

  Kim, Dal Young ^a   Atasheva, Svetlana ^a   McAuley, Alexander J ^b   Plante, Jessica A ^b,c   Frolova, Elena I ^a   Beasley, David W C ^b   Frolov, Ilya ^a  

^a University of Alabama at Birmingham   (United States)

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

^c University of North Carolina at Chapel Hill   (United States)

Author keywords

Expression vectors; Vaccines

Indexed keywords

GENOMIC RNA; GREEN FLUORESCENT PROTEIN; NEUTRALIZING ANTIBODY; VIRUS ENVELOPE PROTEIN;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ANTIBODY TITER; ARTICLE; GENE EXPRESSION SYSTEM; HETEROLOGOUS EXPRESSION; IMMUNIZATION; IN VITRO STUDY; INTERNAL RIBOSOME ENTRY SITE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REPLICON; RNA REPLICATION; RNA SYNTHESIS; VENEZUELAN EQUINE ENCEPHALITIS; VENEZUELAN EQUINE ENCEPHALOMYELITIS ALPHAVIRUS; VIRUS PARTICLE; WEST NILE FLAVIVIRUS;

EXPRESSION VECTORS; VACCINES;

ALPHAVIRUS; ANIMALS; ANTIBODIES, NEUTRALIZING; ENCEPHALITIS VIRUS, VENEZUELAN EQUINE; GENE EXPRESSION; GENETIC VECTORS; GENOME, VIRAL; GREEN FLUORESCENT PROTEINS; INTERFERON-BETA; INTRACELLULAR SPACE; MICE; PROTEIN BIOSYNTHESIS; REPLICON; RNA INTERFERENCE; RNA, VIRAL; VIRAL PROTEINS; VIRUS REPLICATION; WEST NILE VIRUS;

EID: 84904705802     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1408677111     Document Type: Article

References (42)

1. Griffin DE (2001) Alphaviruses. Fields' Virology, eds Knipe DM, Howley PM (Lippincott, Williams and Wilkins, New York), 4th Ed, pp 917-962.
2. Weaver SC, Frolov I (2005) Togaviruses. Virology, eds Mahy BWJ, Meulen VT (ASM Press, Salisbury, UK), Vol 2, pp 1010-1024.
3. Strauss EG, Strauss JH (1986) Structure and replication of the alphavirus genome. The Togaviridae and Flaviviridae, The Viruses, eds Schlesinger S, Schlesinger MJ (Plenum, New York), pp 35-90.
4. Frolov I, et al. (1996) Alphavirus-based expression vectors: Strategies and applications. Proc Natl Acad Sci USA 93(21):11371-11377. (Pubitemid 26347128)
5. Frolov I, Hardy R, Rice CM (2001) Cis-acting RNA elements at the 5′ end of Sindbis virus genome RNA regulate minus- and plus-strand RNA synthesis. RNA 7(11):1638-1651. (Pubitemid 33078938)
6. Fayzulin R, Frolov I (2004) Changes of the secondary structure of the 5′ end of the Sindbis virus genome inhibit virus growth in mosquito cells and lead to accumulation of adaptive mutations. J Virol 78(10):4953-4964. (Pubitemid 38581445)
7. Gorchakov R, Hardy R, Rice CM, Frolov I (2004) Selection of functional 5′ cis-acting elements promoting efficient sindbis virus genome replication. J Virol 78(1):61-75. (Pubitemid 37549720)
8. Michel G, Petrakova O, Atasheva S, Frolov I (2007) Adaptation of Venezuelan equine encephalitis virus lacking 51-nt conserved sequence element to replication in mammalian and mosquito cells. Virology 362(2):475-487. (Pubitemid 46678158)
9. Strauss JH, Kuhn RJ, Niesters HGM, Strauss EG (1990) Functions of the 5′-terminal and 3′-terminal sequences of the Sindbis virus genome in replication. New Aspects of Positive-Strand RNA Viruses, eds Brinton MA, Heinz FX (American Society of Microbiology, Washington, DC), pp 61-66.
10. 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(9):4158-4171.
11. Garmashova N, et al. (2007) Analysis of Venezuelan equine encephalitis virus capsid protein function in the inhibition of cellular transcription. J Virol 81(24):13552-13565. (Pubitemid 350247849)
12. Garmashova N, et al. (2007) The Old World and New World alphaviruses use different virus-specific proteins for induction of transcriptional shutoff. J Virol 81(5):2472-2484.
13. Kulasegaran-Shylini R, Atasheva S, Gorenstein DG, Frolov I (2009) Structural and functional elements of the promoter encoded by the 5′ untranslated region of the Venezuelan equine encephalitis virus genome. J Virol 83(17):8327-8339.
14. Kulasegaran-Shylini R, Thiviyanathan V, Gorenstein DG, Frolov I (2009) The 5′UTR-specific mutation in VEEV TC-83 genome has a strong effect on RNA replication and subgenomic RNA synthesis, but not on translation of the encoded proteins. Virology 387(1):211-221.
15. Gorchakov R, Garmashova N, Frolova E, Frolov I (2008) Different types of nsP3-containing protein complexes in Sindbis virus-infected cells. J Virol 82(20):10088-10101.
16. Frolova EI, Gorchakov R, Pereboeva L, Atasheva S, Frolov I (2010) Functional Sindbis virus replicative complexes are formed at the plasma membrane. J Virol 84(22):11679-11695.
17. Gorchakov R, et al. (2008) A new role for ns polyprotein cleavage in Sindbis virus replication. J Virol 82(13):6218-6231. (Pubitemid 351875103)
18. Strauss JH, Strauss EG (1994) The alphaviruses: Gene expression, replication, and evolution. Microbiol Rev 58(3):491-562.
19. Atasheva S, et al. (2013) Pseudoinfectious Venezuelan equine encephalitis virus: A new means of alphavirus attenuation. J Virol 87(4):2023-2035.
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(8):4028-4041. (Pubitemid 351521238)
21. Levis R, Weiss BG, Tsiang M, Huang H, Schlesinger S (1986) Deletion mapping of Sindbis virus DI RNAs derived from cDNAs defines the sequences essential for replication and packaging. Cell 44(1):137-145. (Pubitemid 16036721)
22. Lehtovaara P, Söderlund H, Keränen S, Pettersson RF, Kääriäinen L (1981) 18S defective interfering RNA of Semliki Forest virus contains a triplicated linear repeat. Proc Natl Acad Sci USA 78(9):5353-5357. (Pubitemid 12248584)
23. Lehtovaara P, Söderlund H, Keränen S, Pettersson RF, Kääriäinen L (1982) Extreme ends of the genome are conserved and rearranged in the defective interfering RNAs of Semliki Forest virus. J Mol Biol 156(4):731-748.
24. Petrakova O, et al. (2005) Noncytopathic replication of Venezuelan equine encephalitis virus and eastern equine encephalitis virus replicons in Mammalian cells. J Virol 79(12):7597-7608. (Pubitemid 40756793)
25. 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(2):315-327. (Pubitemid 43049620)
26. 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(23):12432-12442.
27. Zhang S, et al. (2006) A mutation in the envelope protein fusion loop attenuates mouse neuroinvasiveness of the NY99 strain of West Nile virus. Virology 353(1):35-40. (Pubitemid 44308491)
28. Kim DY, et al. (2011) Design of chimeric alphaviruses with a programmed, attenuated, cell type-restricted phenotype. J Virol 85(9):4363-4376.
29. Griffin DE (1986) Alphavirus pathogenesis and immunity. The Togaviridae and Flaviviridae, The Viruses, eds Schlesinger S, Schlesinger MJ (Plenum, New York), pp 209-250.
30. Weaver SC, Tesh RB, Shope RE (1998) Alphaviruses (VEE). Tropical Infectious Diseases: Principles, Pathogens and Practice, eds Guerrant RL, Krogstad DJ, Maguire JH, Walker DH, Weller PF (Churchill Livingstone, New York), Vol 2, pp 1281-1287.
31. Frolov I, et al. (1999) Selection of RNA replicons capable of persistent noncytopathic replication in mammalian cells. J Virol 73(5):3854-3865. (Pubitemid 29189829)
32. Baric RS, et al. (2002) Expression and self-assembly of Norwalk virus capsid protein from Venezuelan equine encephalitis virus replicons. J Virol 76(6):3023-3030. (Pubitemid 34184887)
33. Johnston RE, et al. (2005) Vaccination of macaques with SIV immunogens delivered by Venezuelan equine encephalitis virus replicon particle vectors followed by a mucosal challenge with SIVsmE660. Vaccine 23(42):4969-4979. (Pubitemid 41267025)
34. Mok H, et al. (2007) Venezuelan equine encephalitis virus replicon particles encoding respiratory syncytial virus surface glycoproteins induce protective mucosal responses in mice and cotton rats. J Virol 81(24):13710-13722. (Pubitemid 350247864)
35. Thomas CE, et al. (2006) Vaccination of mice with gonococcal TbpB expressed in vivo from Venezuelan equine encephalitis viral replicon particles. Infect Immun 74(3):1612-1620. (Pubitemid 43346794)
36. Zhu W, et al. (2005) Comparison of immune responses to gonococcal PorB delivered as outer membrane vesicles, recombinant protein, or Venezuelan equine encephalitis virus replicon particles. Infect Immun 73(11):7558-7568. (Pubitemid 41587662)
37. Thompson JM, et al. (2006) Mucosal and systemic adjuvant activity of alphavirus replicon particles. Proc Natl Acad Sci USA 103(10):3722-3727. (Pubitemid 43376622)
38. Thompson JM, Whitmore AC, Staats HF, Johnston RE (2008) Alphavirus replicon particles acting as adjuvants promote CD8+ T cell responses to co-delivered antigen. Vaccine 26(33):4267-4275.
39. Tzeng WP, Matthews JD, Frey TK (2006) Analysis of rubella virus capsid protein-mediated enhancement of replicon replication and mutant rescue. J Virol 80(8):3966-3974.
40. Kim DY, Firth AE, Atasheva S, Frolova EI, Frolov I (2011) Conservation of a packaging signal and the viral genome RNA packaging mechanism in alphavirus evolution. J Virol 85(16):8022-8036.
41. Mason PW, Shustov AV, Frolov I (2006) Production and characterization of vaccines based on flaviviruses defective in replication. Virology 351(2):432-443. (Pubitemid 44108076)
42. Lulla V, Kim DY, Frolova EI, Frolov I (2013) The amino-terminal domain of alphavirus capsid protein is dispensable for viral particle assembly but regulates RNA encapsidation through cooperative functions of its subdomains. J Virol 87(22):12003-12019.