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Volume 89, Issue 9

T7 RNA polymerase-dependent and -independent systems for cDNA-based rescue of Rift Valley fever virus Free

Abstract

Rift Valley fever virus (RVFV) is responsible for large and recurrent outbreaks of acute febrile illness among humans and domesticated animals in Africa. It belongs to the family , genus , and its negative-stranded RNA genome consists of three segments. Here, we report the establishment and characterization of two different systems to rescue the RVFV wild-type strain ZH548. The first system is based on the BHK-21 cell clone BSR-T7/5, which stably expresses T7 RNA polymerase (T7 pol). Rescue of wild-type RVFV was achieved with three T7 pol-driven cDNA plasmids representing the viral RNA segments in the antigenomic sense. The second system involves 293T cells transfected with three RNA pol I-driven plasmids for the viral segments and two RNA pol II-driven support plasmids to express the viral polymerase components L and N. It is known that the 5′ triphosphate group of T7 pol transcripts strongly activates the antiviral interferon system via the intracellular RNA receptor RIG-I. Nonetheless, both the T7 pol and the pol I/II system were of similar efficiency. This was even true for the rescue of a RVFV mutant lacking the interferon antagonist nonstructural proteins. Further experiments demonstrated that the unresponsiveness of BHK-21 and BSR-T7/5 cells to T7 pol transcripts is most probably due to a deficiency in the RIG-I pathway. Our reverse genetics systems now enable us to manipulate the genome of RVFV and study its virulence mechanisms. Moreover, the finding that BHK-derived cell lines have a compromised RIG-I pathway may explain their suitability for propagating and rescuing a wide variety of viruses.

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2008-09-01
2024-04-19
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References

  1. Andzhaparidze O. G., Bogomolova N. N., Boriskin Y. S., Bektemirova M. S., Drynov I. D. 1981; Comparative study of rabies virus persistence in human and hamster cell lines. J Virol 37:1–6
     [Google Scholar]
  2. Balkhy H. H., Memish Z. A. 2003; Rift Valley fever: an uninvited zoonosis in the Arabian peninsula. Int J Antimicrob Agents 21:153–157 [CrossRef]
     [Google Scholar]
  3. Billecocq A., Spiegel M., Vialat P., Kohl A., Weber F., Bouloy M., Haller O. 2004; NSs protein of Rift Valley fever virus blocks interferon production by inhibiting host gene transcription. J Virol 78:9798–9806 [CrossRef]
     [Google Scholar]
  4. Binder M., Kochs G., Bartenschlager R., Lohmann V. 2007; Hepatitis C virus escape from the interferon regulatory factor 3 pathway by a passive and active evasion strategy. Hepatology 46:1365–1374 [CrossRef]
     [Google Scholar]
  5. Bird B. H., Albarino C. G., Nichol S. T. 2007; Rift Valley fever virus lacking NSm proteins retains high virulence in vivo and may provide a model of human delayed onset neurologic disease. Virology 362:10–15 [CrossRef]
     [Google Scholar]
  6. Blakqori G., Weber F. 2005; Efficient cDNA-based rescue of La Crosse bunyaviruses expressing or lacking the nonstructural protein NSs. J Virol 79:10420–10428 [CrossRef]
     [Google Scholar]
  7. Blakqori G., Kochs G., Haller O., Weber F. 2003; Functional L polymerase of La Crosse virus allows in vivo reconstitution of recombinant nucleocapsids. J Gen Virol 84:1207–1214 [CrossRef]
     [Google Scholar]
  8. Blakqori G., Delhaye S., Habjan M., Blair C. D., Sanchez-Vargas I., Olson K. E., Attarzadeh-Yazdi G., Fragkoudis R., Kohl A. other authors 2007; La Crosse bunyavirus nonstructural protein NSs serves to suppress the type I interferon system of mammalian hosts. J Virol 81:4991–4999 [CrossRef]
     [Google Scholar]
  9. Blight K. J., McKeating J. A., Rice C. M. 2002; Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J Virol 76:13001–13014 [CrossRef]
     [Google Scholar]
  10. Bluyssen H. A., Levy D. E. 1997; Stat2 is a transcriptional activator that requires sequence-specific contacts provided by Stat1 and p48 for stable interaction with DNA. J Biol Chem 272:4600–4605 [CrossRef]
     [Google Scholar]
  11. Borio L., Inglesby T., Peters C. J., Schmaljohn A. L., Hughes J. M., Jahrling P. B., Ksiazek T., Johnson K. M., Meyerhoff A. other authors 2002; Hemorrhagic fever viruses as biological weapons: medical and public health management. JAMA 287:2391–2405 [CrossRef]
     [Google Scholar]
  12. Bouloy M., Janzen C., Vialat P., Khun H., Pavlovic J., Huerre M., Haller O. 2001; Genetic evidence for an interferon-antagonistic function of rift valley fever virus nonstructural protein NSs. J Virol 75:1371–1377 [CrossRef]
     [Google Scholar]
  13. Bridgen A., Elliott R. M. 1996; Rescue of a segmented negative-strand RNA virus entirely from cloned complementary DNAs. Proc Natl Acad Sci U S A 93:15400–15404 [CrossRef]
     [Google Scholar]
  14. Brzozka K., Finke S., Conzelmann K. K. 2006; Inhibition of interferon signaling by rabies virus phosphoprotein P: activation-dependent binding of STAT1 and STAT2. J Virol 80:2675–2683 [CrossRef]
     [Google Scholar]
  15. Buchholz U. J., Finke S., Conzelmann K. K. 1999; Generation of bovine respiratory syncytial virus (BRSV) from cDNA: BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. J Virol 73:251–259
     [Google Scholar]
  16. Conzelmann K. K. 2004; Reverse genetics of mononegavirales. Curr Top Microbiol Immunol 283:1–41
     [Google Scholar]
  17. de Wit E., Spronken M. I., Vervaet G., Rimmelzwaan G. F., Osterhaus A. D., Fouchier R. A. 2007; A reverse-genetics system for influenza A virus using T7 RNA polymerase. J Gen Virol 88:1281–1287 [CrossRef]
     [Google Scholar]
  18. Elliott R. M. 1996 The Bunyaviridae New York: Plenum Press;
     [Google Scholar]
  19. Elliott R. M. 1997; Emerging viruses: the Bunyaviridae. Mol Med 3:572–577
     [Google Scholar]
  20. Ferran M. C., Lucas-Lenard J. M. 1997; The vesicular stomatitis virus matrix protein inhibits transcription from the human beta interferon promoter. J Virol 71:371–377
     [Google Scholar]
  21. Flatz L., Bergthaler A., de la Torre J. C., Pinschewer D. D. 2006; Recovery of an arenavirus entirely from RNA polymerase I/II-driven cDNA. Proc Natl Acad Sci U S A 103:4663–4668 [CrossRef]
     [Google Scholar]
  22. Fromont-Racine M., Senger B., Saveanu C., Fasiolo F. 2003; Ribosome assembly in eukaryotes. Gene 313:17–42 [CrossRef]
     [Google Scholar]
  23. Gerrard S. R., Bird B. H., Albarino C. G., Nichol S. T. 2007; The NSm proteins of Rift Valley fever virus are dispensable for maturation, replication and infection. Virology 359:459–465 [CrossRef]
     [Google Scholar]
  24. Groseth A., Feldmann H., Theriault S., Mehmetoglu G., Flick R. 2005; RNA polymerase I-driven minigenome system for Ebola viruses. J Virol 79:4425–4433 [CrossRef]
     [Google Scholar]
  25. Habjan M., Andersson I., Klingstrom J., Schumann M., Martin A., Zimmermann P., Wagner V., Pichlmair A., Schneider U. other authors 2008; Processing of genome 5′ termini as a strategy of negative-strand RNA viruses to avoid RIG-I-dependent interferon induction. PLoS ONE 3:e2032 [CrossRef]
     [Google Scholar]
  26. Hoffmann E., Neumann G., Kawaoka Y., Hobom G., Webster R. G. 2000; A DNA transfection system for generation of influenza A virus from eight plasmids. Proc Natl Acad Sci U S A 97:6108–6113 [CrossRef]
     [Google Scholar]
  27. Hornung V., Ellegast J., Kim S., Brzozka K., Jung A., Kato H., Poeck H., Akira S., Conzelmann K. K. other authors 2006; 5′-Triphosphate RNA is the ligand for RIG-I. Science 314:994–997 [CrossRef]
     [Google Scholar]
  28. Ikegami T., Peters C. J., Makino S. 2005; Rift valley fever virus nonstructural protein NSs promotes viral RNA replication and transcription in a minigenome system. J Virol 79:5606–5615 [CrossRef]
     [Google Scholar]
  29. Ikegami T., Won S., Peters C. J., Makino S. 2006; Rescue of infectious Rift Valley fever virus entirely from cDNA, analysis of virus lacking the NSs gene, and expression of a foreign gene. J Virol 80:2933–2940 [CrossRef]
     [Google Scholar]
  30. Karabatsos N., Buckley S. M. 1967; Susceptibility of the baby-hamster kidney-cell line (BHK-21) to infection with arboviruses. Am J Trop Med Hyg 16:99–105
     [Google Scholar]
  31. Kim D. H., Longo M., Han Y., Lundberg P., Cantin E., Rossi J. J. 2004; Interferon induction by siRNAs and ssRNAs synthesized by phage polymerase. Nat Biotechnol 22:321–325 [CrossRef]
     [Google Scholar]
  32. Le May N., Dubaele S., De Santis L. P., Billecocq A., Bouloy M., Egly J. M. 2004; TFIIH transcription factor, a target for the Rift Valley hemorrhagic fever virus. Cell 116:541–550 [CrossRef]
     [Google Scholar]
  33. Le May N., Mansuroglu Z., Leger P., Josse T., Blot G., Billecocq A., Flick R., Jacob Y., Bonnefoy E., Bouloy M. 2008; A SAP30 complex inhibits IFN-beta expression in Rift Valley fever virus infected cells. PLoS Pathog 4:e13 [CrossRef]
     [Google Scholar]
  34. Lowen A. C., Noonan C., McLees A., Elliott R. M. 2004; Efficient bunyavirus rescue from cloned cDNA. Virology 330:493–500 [CrossRef]
     [Google Scholar]
  35. MacDonald M. R., Machlin E. S., Albin O. R., Levy D. E. 2007; The zinc finger antiviral protein acts synergistically with an interferon-induced factor for maximal activity against alphaviruses. J Virol 81:13509–13518 [CrossRef]
     [Google Scholar]
  36. Meegan J. M., Hoogstraal H., Moussa M. I. 1979; An epizootic of Rift Valley fever in Egypt in 1977. Vet Rec 105:124–125 [CrossRef]
     [Google Scholar]
  37. Neumann G., Watanabe T., Ito H., Watanabe S., Goto H., Gao P., Hughes M., Perez D. R., Donis R. other authors 1999; Generation of influenza A viruses entirely from cloned cDNAs. Proc Natl Acad Sci U S A 96:9345–9350 [CrossRef]
     [Google Scholar]
  38. Ogawa Y., Sugiura K., Kato K., Tohya Y., Akashi H. 2007; Rescue of Akabane virus (family Bunyaviridae ) entirely from cloned cDNAs by using RNA polymerase I. J Gen Virol 88:3385–3390 [CrossRef]
     [Google Scholar]
  39. Otsuki K., Maeda J., Yamamoto H., Tsubokura M. 1979; Studies on avian infectious bronchitis virus (IBV). III. Interferon induction by and sensitivity to interferon of IBV. Arch Virol 60:249–255 [CrossRef]
     [Google Scholar]
  40. Pichlmair A., Schulz O., Tan C. P., Naslund T. I., Liljestrom P., Weber F., Reis. e Sousa C. 2006; RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science 314:997–1001 [CrossRef]
     [Google Scholar]
  41. Plumet S., Herschke F., Bourhis J. M., Valentin H., Longhi S., Gerlier D. 2007; Cytosolic 5′-triphosphate ended viral leader transcript of measles virus as activator of the RIG I-mediated interferon response. PLoS ONE 2:e279 [CrossRef]
     [Google Scholar]
  42. Sanchez A. B., de la Torre J. C. 2006; Rescue of the prototypic Arenavirus LCMV entirely from plasmid. Virology 350:370–380 [CrossRef]
     [Google Scholar]
  43. Shatkin A. J., Manley J. L. 2000; The ends of the affair: capping and polyadenylation. Nat Struct Biol 7:838–842 [CrossRef]
     [Google Scholar]
  44. Stanwick T. L., Hallum J. V. 1974; Role of interferon in six cell lines persistently infected with rubella virus. Infect Immun 10:810–815
     [Google Scholar]
  45. Struthers J. K., Swanepoel R., Shepherd S. P. 1984; Protein synthesis in Rift Valley fever virus-infected cells. Virology 134:118–124 [CrossRef]
     [Google Scholar]
  46. Sumpter R. Jr, Loo Y. M., Foy E., Li K., Yoneyama M., Fujita T., Lemon S. M., Gale M. Jr 2005; Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J Virol 79:2689–2699 [CrossRef]
     [Google Scholar]
  47. Vialat P., Billecocq A., Kohl A., Bouloy M. 2000; The S segment of rift valley fever phlebovirus ( Bunyaviridae ) carries determinants for attenuation and virulence in mice. J Virol 74:1538–1543 [CrossRef]
     [Google Scholar]
  48. Won S., Ikegami T., Peters C. J., Makino S. 2006; NSm and 78-kilodalton proteins of Rift Valley fever virus are nonessential for viral replication in cell culture. J Virol 80:8274–8278 [CrossRef]
     [Google Scholar]
  49. Zhong J., Gastaminza P., Cheng G., Kapadia S., Kato T., Burton D. R., Wieland S. F., Uprichard S. L., Wakita T., Chisari F. V. 2005; Robust hepatitis C virus infection in vitro . Proc Natl Acad Sci U S A 102:9294–9299 [CrossRef]
     [Google Scholar]
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T7 RNA polymerase-dependent and -independent systems for cDNA-based rescue of Rift Valley fever virus
J. Gen. Virol. 89, 2157 (2008); https://doi.org/10.1099/vir.0.2008/002097-0
/content/journal/jgv/10.1099/vir.0.2008/002097-0
/content/journal/jgv/10.1099/vir.0.2008/002097-0
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