Reverse genetics system for severe fever with thrombocytopenia syndrome virus

Journal of Virology

Volumn 89, Issue 6, 2015, Pages 3026-3037

  Brennan, Benjamin ^a   Li, Ping ^a   Zhang, Shuo ^b   Li, Aqian ^b   Liang, Mifang ^b   Li, Dexin ^b   Elliott, Richard M ^a  

^a MRC UNIVERSITY OF GLASGOW CENTRE FOR VIRUS RESEARCH   (United Kingdom)

^b Key Laboratory for Medical Virology NHFPC National Institute for Viral Disease Control and Prevention China CDC   (China)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; RNA POLYMERASE; VIRUS PROTEIN; VIRUS RNA; VIRAL PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; CELL CULTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE ACTIVITY; HOST CELL; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PHLEBOVIRUS; PRIORITY JOURNAL; PROCESS DEVELOPMENT; PROCESS OPTIMIZATION; PROTEIN SYNTHESIS INHIBITION; REVERSE GENETICS; SEVERE FEVER WITH THROMBOCYTOPENIA SYNDROME VIRUS; VIRAL GENETICS; VIROGENESIS; VIRUS CELL INTERACTION; VIRUS REPLICATION; AMINO ACID SEQUENCE; CHEMISTRY; CHINA; EVALUATION STUDY; FEMALE; GENETICS; HUMAN; METABOLISM; MIDDLE AGED; MOLECULAR GENETICS; PROCEDURES; SANDFLY FEVER; SEQUENCE ALIGNMENT; VIROLOGY; VIRUS GENOME;

BUNYAVIRIDAE; IXODIDA; PHLEBOVIRUS; UUKUNIEMI VIRUS;

AMINO ACID SEQUENCE; BASE SEQUENCE; CHINA; FEMALE; GENOME, VIRAL; HUMANS; MIDDLE AGED; MOLECULAR SEQUENCE DATA; PHLEBOTOMUS FEVER; PHLEBOVIRUS; REVERSE GENETICS; SEQUENCE ALIGNMENT; VIRAL PROTEINS;

EID: 84923172365     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03432-14     Document Type: Article

References (55)

1. Plyusnin A, Beaty BJ, Elliott RM, Goldbach R, Kormelink R, Lundkvist Å, Schmaljohn CS, Tesh RB. 2012. Bunyaviridae, p 725-741. In King AMQ, Adams MJ, Carstens EB, Lefkowits EJ (ed), Virus taxonomy: ninth report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, London, United Kingdom.
2. Plyusnin A, Elliott RM (ed). 2011. Bunyaviridae: molecular and cellular biology. Caister Academic Press, Norfolk, United Kingdom.
3. Walter CT, Barr JN. 2011. Recent advances in the molecular and cellular biology of bunyaviruses. J Gen Virol 92:2467-2484. http://dx.doi.org/10 .1099/vir.0.035105-0.
4. Elliott RM, Schmaljohn CS. 2013. Bunyaviridae, p 1244-1282. In Knipe DM, Howley PM (ed), Fields virology, 6th ed. Wolters Kluwer, Philadelphia, PA.
5. Bouloy M. 2011. Molecular biology of phleboviruses, p 95-128. In Plyusnin A, ElliottRM(ed), Bunyaviridae: molecular and cellular biology. Caister Academic Press, Norfolk, United Kingdom.
6. Hubalek Z, Rudolf I. 2012. Tick-borne viruses in Europe. Parasitol Res 111:9-36. http://dx.doi.org/10.1007/s00436-012-2910-1.
7. Chevalier V. 2013. Relevance of Rift Valley fever to public health in the European Union. Clin Microbiol Infect 19:705-708. http://dx.doi.org/10 .1111/1469-0691.12163.
8. Ikegami T, Makino S. 2011. The pathogenesis of Rift Valley fever. Viruses 3:493-519. http://dx.doi.org/10.3390/v3050493.
9. Ikegami T. 2012. Molecular biology and genetic diversity of Rift Valley fever virus. Antiviral Res 95:293-310. http://dx.doi.org/10.1016/j.antiviral .2012.06.001.
10. Yu XJ, Liang MF, Zhang SY, Liu Y, Li JD, Sun YL, DLM, Zhang QF, Popov VL, Li C, Qu J, Li Q, Zhang YP, Hai R, Wu W, Wang Q, Zhan FX, Wang XJ, Kan B, Wang SW, Wan KL, Jing HQ, Lu JX, Yin WW, Zhou H, Guan XH, Liu JF, Bi ZQ, Liu GH, Ren J, Wang H, Zhao Z, Song JD, He JR, Wan T, Zhang JS, Fu XP, Sun LN, Dong XP, Feng ZJ, Yang WZ, Hong T, Zhang Y, Walker DH, Wang Y, Li DX. 2011. Fever with thrombocytopenia associated with a novel bunyavirus in China. N Engl J Med 364:1523-1532. http://dx.doi.org/10.1056/NEJMoa1010095.
11. Liu S, Chai C, Wang C, Amer S, Lv H, He H, Sun J, Lin J. 2014. Systematic review of severe fever with thrombocytopenia syndrome: virology, epidemiology, and clinical characteristics. Rev Med Virol 24:90-102. http://dx.doi.org/10.1002/rmv.1776
12. Liu Q, He B, Huang SY, Wei F, Zhu XQ. 2014. Severe fever with thrombocytopenia syndrome, an emerging tick-borne zoonosis. Lancet Infect Dis 14:763-772. http://dx.doi.org/10.1016/S1473-3099(14)70718-2.
13. Palacios G, Savji N, Travassos da Rosa A, Guzman H, Yu X, Desai A, Rosen GE, Hutchison S, Lipkin WI, Tesh R. 2013. Characterization of the Uukuniemi virus group (Phlebovirus: Bunyaviridae): evidence for seven distinct species. J Virol 87:3187-3195. http://dx.doi.org/10.1128/JVI.02719-12.
14. Stone R. 2010. Rival teams identify a virus behind deaths in Central China. Science 330:20-21. http://dx.doi.org/10.1126/science.330.6000.20.
15. Xu B, Liu L, Huang X, Ma H, Zhang Y, Du Y, Wang P, Tang X, Wang H, Kang K, Zhang S, Zhao G, Wu W, Yang Y, Chen H, Mu F, Chen W. 2011. Metagenomic analysis of fever, thrombocytopenia and leukopenia syndrome (FTLS) in Henan Province, China: discovery of a new bunyavirus. PLoS Pathog 7:e1002369. http://dx.doi.org/10.1371/journal.ppat .1002369.
16. Zhang Y-Z, Zhou D-J, Qin X-C, Tian J-H, Xiong Y, Wang J-B, Chen X-P, Gao D-Y, He Y-W, Jin D, Sun Q, Guo W-P, Wang W, Yu B, Li J, Dai Y-A, Li W, Peng J-S, Zhang, G-B, Zhang S, Chen X-M, Wang Y, Li M-H, Lu X, Ye C, de Jong MD, Xu J. 2012. The ecology, genetic diversity, and phylogeny of Huaiyangshan virus in China. J Virol 86:2864-2868. http://dx.doi.org/10.1128/JVI.06192-11.
17. Lohmeyer KH, Pound JM, May MA, Kammlah DM, Davey RB. 2011. Distribution of Rhipicephalus (Boophilus) microplus and Rhipicephalus (Boophilus) annulatus (Acari: Ixodidae) infestations detected in the United States along the Texas/Mexico border. J Med Entomol 48:770-774. http://dx.doi.org/10.1603/ME10209.
18. Kim KH, Yi J, Kim G, Choi SJ, Jun KI, Kim NH, Choe PG, Kim NJ, Lee JK, Oh MD. 2013. Severe fever with thrombocytopenia syndrome, South Korea, 2012. Emerg Infect Dis 19:1892-1894. http://dx.doi.org/10.3201/eid1911.130792.
19. Park SW, Song BG, Shin EH, Yun SM, Han MG, Park MY, Park C, Ryou J. 2014. Prevalence of severe fever with thrombocytopenia syndrome virus in Haemaphysalis longicornis ticks in South Korea. Ticks Tick Borne Dis 5:975-977. http://dx.doi.org/10.1016/j.ttbdis.2014.07.020.
20. Takahashi T, Maeda K, Suzuki T, Ishido A, Shigeoka T, Tominaga T, Kamei T, Honda M, Ninomiya D, Sakai T, Senba T, Kaneyuki S, Sakaguchi S, Satoh A, Hosokawa T, Kawabe Y, Kurihara S, Izumikawa K, Kohno S, Azuma T, Suemori K, Yasukawa M, Mizutani T, Omatsu T, Katayama Y, Miyahara M, Ijuin M, Doi K, Okuda M, Umeki K, Saito T, Fukushima K, Nakajima K, Yoshikawa T, Tani H, Fukushi S, Fukuma A, Ogata M, Shimojima M, Nakajima N, Nagata N, Katano H, Fukumoto H, Sato Y, Hasegawa H, Yamagishi T, Oishi K, Kurane I, Morikawa S, Saijo M. 2014. The first identification and retrospective study of severe fever with thrombocytopenia syndrome in Japan. J Infect Dis 209:816-827. http://dx.doi.org/10.1093/infdis/jit603.
21. Elliott RM, Brennan B. 2014. Emerging phleboviruses. Curr Opin Virol 5:50-57. http://dx.doi.org/10.1016/j.coviro.2014.01.011.
22. McMullan LK, Folk SM, Kelly AJ, MacNeil A, Goldsmith CS, Metcalfe MG, Batten BC, Albarino CG, Zaki SR, Rollin PE, Nicholson WL, Nichol ST. 2012. A new phlebovirus associated with severe febrile illness in Missouri. N Engl J Med 367:834-841. http://dx.doi.org/10.1056/NEJMoa1203378.
23. Savage HM, Godsey MS, Jr, Lambert A, Panella NA, Burkhalter KL, Harmon JR, Lash RR, Ashley DC, Nicholson WL. 2013. First detection of Heartland virus (Bunyaviridae: Phlebovirus) from field collected arthropods. Am J Trop Med Hyg 89:445-452. http://dx.doi.org/10.4269/ajtmh.13-0209.
24. Pastula DM, Turabelidze G, Yates KF, Jones TF, Lambert AJ, Panella AJ, Kosoy OI, Velez JO, Fisher M, Staples E. 2014. Notes from the field: Heartland virus disease-United States, 2012-2013. MMWR Morb Mortal Wkly Rep 63:270-271.
25. Punda V, Ropac D, Vesenjak-Hirjan J. 1987. Incidence of hemagglutination-inhibiting antibodies for Bhanja virus in humans along the northwest border of Yugoslavia. Zentralbl Bakteriol Mikrobiol Hyg A 265:227-234.
26. Dilcher M, Alves MJ, Finkeisen D, Hufert F, Weidmann M. 2012. Genetic characterization of Bhanja virus and Palma virus, two tick-borne phleboviruses. Virus Genes 45:311-315. http://dx.doi.org/10.1007/s11262-012-0785-y.
27. Matsuno K, Weisend C, Travassos da Rosa AP, Anzick SL, Dahlstrom E, Porcella SF, Dorward DW, Yu XJ, Tesh RB, Ebihara H. 2013. Characterization of the Bhanja serogroup viruses (Bunyaviridae): a novel species of the genus Phlebovirus and its relationship with other emerging tick-borne phleboviruses. J Virol 87:3719-3728. http://dx.doi.org/10 .1128/JVI.02845-12.
28. Kokernot RH, Calisher CH, Stannard LJ, Hayes J. 1969. Arbovirus studies in the Ohio-Mississippi Basin, 1964-1967. VII. Lone Star virus, a hitherto unknown agent isolated from the tick Amblyomma americanum (Linn). Am J Trop Med Hyg 18:789-795.
29. Swei A, Russell BJ, Naccache SN, Kabre B, Veeraraghavan N, Pilgard MA, Johnson BJ, Chiu CY. 2013. The genome sequence of Lone Star virus, a highly divergent bunyavirus found in the Amblyomma americanum tick. PLoS One 8:e62083. http://dx.doi.org/10.1371/journal.pone .0062083.
30. Mourya DT, Yadav PD, Basu A, Shete A, Patil DY, Zawar D, Majumdar TD, Kokate P, Sarkale P, Raut CG, Jadhav SM. 2014. Malsoor virus, a novel bat phlebovirus, is closely related to severe fever with thrombocytopenia syndrome virus and heartland virus. J Virol 88:3605-3609. http://dx .doi.org/10.1128/JVI.02617-13.
31. Wang J, Selleck P, Yu M, Ha W, Rootes C, Gales R, Wise T, Crameri S, Chen H, Broz I, Hyatt A, Woods R, Meehan B, McCullough S, Wang LF. 2014. Novel phlebovirus with zoonotic potential isolated from ticks, Australia. Emerg Infect Dis 20:1040-1043. http://dx.doi.org/10.3201/eid2006.140003.
32. Bridgen AE. 2013. Reverse genetics of RNA viruses: applications and perspectives. Wiley-Blackwell, Chichester, United Kingdom.
33. Buchholz UJ, Finke S, Conzelmann KK. 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.
34. Kaul A, Woerz I, Meuleman P, Leroux-Roels G, Bartenschlager R. 2007. Cell culture adaptation of hepatitis C virus and in vivo viability of an adapted variant. J Virol 81:13168-13179. http://dx.doi.org/10.1128/JVI .01362-07.
35. Billecocq A, Gauliard N, Le May N, Elliott RM, Flick R, Bouloy M. 2008. RNA polymerase I-mediated expression of viral RNA for the rescue of infectious virulent and avirulent Rift Valley fever viruses. Virology 378: 377-384. http://dx.doi.org/10.1016/j.virol.2008.05.033.
36. Johnson KN, Zeddam JL, Ball LA. 2000. Characterization and construction of functional cDNA clones of Pariacoto virus, the first Alphanodavirus isolated outside Australasia. J Virol 74:5123-5132. http://dx.doi.org/10.1128/JVI.74.11.5123-5132.2000.
37. Brennan B, Li P, Elliott RM. 2011. Generation and characterisation of a recombinant Rift Valley fever virus expressing a V5 epitope-tagged RNABrennan dependent RNA polymerase. J Gen Virol 92:2906-2913. http://dx.doi.org/10.1099/vir.0.036749-0.
38. Gauliard N, Billecocq A, Flick R, Bouloy M. 2006. Rift Valley fever virus noncoding regions of L,Mand S segments regulate RNA synthesis. Virology 351:170-179. http://dx.doi.org/10.1016/j.virol.2006.03.018.
39. Habjan M, Penski N, Wagner V, Spiegel M, Overby AK, Kochs G, Huiskonen JT, Weber F. 2009. Efficient production of Rift Valley fever virus-like particles: the antiviral protein MxA can inhibit primary transcription of bunyaviruses. Virology 385:400-408. http://dx.doi.org/10 .1016/j.virol.2008.12.011.
40. Weber F, Dunn EF, Bridgen A, Elliott RM. 2001. The Bunyamwera virus nonstructural protein NSs inhibits viral RNA synthesis in a minireplicon system. Virology 281:67-74. http://dx.doi.org/10.1006/viro.2000.0774.
41. Elliott RM. 2012. Bunyavirus reverse genetics and applications to studying interactions with host cells, p 200-223. In Bridgen A (ed), Reverse genetics of RNA viruses: applications and perspectives. Wiley-Blackwell, Chichester, United Kingdom.
42. Simons JF, Hellman U, Pettersson RF. 1990. Uukuniemi virus S RNA segment: ambisense coding strategy, packaging of complementary strands into virions, and homology to members of the genus Phlebovirus. J Virol 64:247-255.
43. Ikegami T, Won S, Peters CJ, Makino S. 2005. Rift Valley fever virus NSs mRNA is transcribed from an incoming anti-viral-sense S RNA segment. J Virol 79:12106-12111. http://dx.doi.org/10.1128/JVI.79.18 .12106-12111.2005.
44. Brennan B, Welch SR, Elliott RM. 2014. The consequences of reconfiguring the ambisense S genome segment of Rift Valley fever virus on viral replication in mammalian and mosquito cells and for genome packaging. PLoS Pathog 10:e1003922. http://dx.doi.org/10.1371/journal.ppat.1003922.
45. Santiago FW, Covaleda LM, Sanchez-Aparicio MT, Silvas JA, Diaz-Vizarreta AC, Patel JR, Popov V, Yu XJ, Garcia-Sastre A, Aguilar PV. 2014. Hijacking of RIG-I signaling proteins into virus-induced cytoplasmic structures correlates with the inhibition of type I interferon responses. J Virol 88:4572-4585. http://dx.doi.org/10.1128/JVI.03021-13.
46. Ning YJ, Wang M, Deng M, Shen S, Liu W, Cao WC, Deng F, Wang YY, Hu Z, Wang H. 2014. Viral suppression of innate immunity via spatial isolation of TBK1/IKKepsilon from mitochondrial antiviral platform. J Mol Cell Biol 6:324-337. http://dx.doi.org/10.1093/jmcb/mju015.
47. Wu X, Qi X, Liang M, Li C, Cardona CJ, Li D, Xing Z. 2014. Roles of viroplasm-like structures formed by nonstructural protein NSs in infection with severe fever with thrombocytopenia syndrome virus. FASEB J 28:2504-2516. http://dx.doi.org/10.1096/fj.13-243857.
48. Wu X, Qi X, Qu B, Zhang Z, Liang M, Li C, Cardona CJ, Li D, Xing Z. 2014. Evasion of antiviral immunity through sequestering of TBK1/IKKepsilon/IRF3 into viral inclusion bodies. J Virol 88:3067-3076. http://dx.doi.org/10.1128/JVI.03510-13.
49. Habjan M, Pichlmair A, Elliott RM, Overby AK, Glatter T, Gstaiger M, Superti-Furga G, Unger H, Weber F. 2009. NSs protein of Rift Valley fever virus induces the specific degradation of the double-stranded RNAdependent protein kinase. J Virol 83:4365-4375. http://dx.doi.org/10 .1128/JVI.02148-08.
50. Ikegami T, Narayanan K, Won S, Kamitani W, Peters CJ, Makino S. 2009. Rift Valley fever virus NSs protein promotes post-transcriptional downregulation of protein kinase PKR and inhibits eIF2alpha phosphorylation. PLoS Pathog 5:e1000287. http://dx.doi.org/10.1371/journal.ppat .1000287.
51. Pettersson RF. 1974. Effect of Uukuniemi virus infection on host cell macromolecule synthesis. Med Biol 52:90-97.
52. Acrani GO, Tilston-Lunel NL, Spiegel M, Weidmann M, Dilcher M, da Silva DEA, Nunes MRT, Elliott RM. 2014. Establishment of a minigenome system for Oropouche orthobunyavirus reveals the S genome segment to be significantly longer than previously reported. J Gen Virol http://dx.doi.org/10.1099/jgv.0.000005.
53. Eifan S, Schnettler E, Dietrich I, Kohl A, Blomstrom AL. 2013. Nonstructural proteins of arthropod-borne bunyaviruses: roles and functions. Viruses 5:2447-2468. http://dx.doi.org/10.3390/v5102447.
54. Qu B, Qi X, Wu X, Liang M, Li C, Cardona CJ, Xu W, Tang F, Li Z, Wu B, Powell K, Wegner M, Li D, Xing Z. 2012. Suppression of the interferon and NF-kappaB responses by severe fever with thrombocytopenia syndrome virus. J Virol 86:8388-8401. http://dx.doi.org/10 .1128/JVI.00612-12.
55. 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. http://dx.doi.org/10.1099/vir.0.18876-0.