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Abstract

The family of segmented, negative-stranded RNA viruses includes over 350 members that infect a bewildering variety of animals and plants. Many of these bunyaviruses are the causative agents of serious disease in their respective hosts, and are classified as emerging viruses because of their increased incidence in new populations and geographical locations throughout the world. Emerging bunyaviruses, such as Crimean–Congo hemorrhagic fever virus, tomato spotted wilt virus and Rift Valley fever virus, are currently attracting great interest due to migration of their arthropod vectors, a situation possibly linked to climate change. These and other examples of continued emergence suggest that bunyaviruses will probably continue to pose a sustained global threat to agricultural productivity, animal welfare and human health. The threat of emergence is particularly acute in light of the lack of effective preventative or therapeutic treatments for any of these viruses, making their study an important priority. This review presents recent advances in the understanding of the bunyavirus life cycle, including aspects of their molecular, cellular and structural biology. Whilst special emphasis is placed upon the emerging bunyaviruses, we also describe the extensive body of work involving model bunyaviruses, which have been the subject of major contributions to our overall understanding of this important group of viruses.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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2011-11-01
2024-03-29
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References

  1. Acrani G. O., Gomes R., Proença-Módena J. L., da Silva A. F., Carminati P. O., Silva M. L., Santos R. I. M., Arruda E. 2010; Apoptosis induced by Oropouche virus infection in HeLa cells is dependent on virus protein expression. Virus Res 149:56–63 [View Article][PubMed]
    [Google Scholar]
  2. Adam I., Karsany M. S. 2008; Case report: Rift Valley Fever with vertical transmission in a pregnant Sudanese woman. J Med Virol 80:929 [View Article][PubMed]
    [Google Scholar]
  3. Alfadhli A., Love Z., Arvidson B., Seeds J., Willey J., Barklis E. 2001; Hantavirus nucleocapsid protein oligomerization. J Virol 75:2019–2023 [View Article][PubMed]
    [Google Scholar]
  4. Altamura L. A., Bertolotti-Ciarlet A., Teigler J., Paragas J., Schmaljohn C. S., Doms R. W. 2007; Identification of a novel C-terminal cleavage of Crimean–Congo hemorrhagic fever virus PreGN that leads to generation of an NSM protein. J Virol 81:6632–6642 [View Article][PubMed]
    [Google Scholar]
  5. Andersson A. M., Pettersson R. F. 1998; Targeting of a short peptide derived from the cytoplasmic tail of the G1 membrane glycoprotein of Uukuniemi virus (Bunyaviridae) to the Golgi complex. J Virol 72:9585–9596[PubMed]
    [Google Scholar]
  6. Andersson I., Simon M., Lundkvist A., Nilsson M., Holmström A., Elgh F., Mirazimi A. 2004a; Role of actin filaments in targeting of Crimean Congo hemorrhagic fever virus nucleocapsid protein to perinuclear regions of mammalian cells. J Med Virol 72:83–93 [View Article][PubMed]
    [Google Scholar]
  7. Andersson I., Bladh L., Mousavi-Jazi M., Magnusson K.-E., Lundkvist Å., Haller O., Mirazimi A. 2004b; Human MxA protein inhibits the replication of Crimean–Congo hemorrhagic fever virus. J Virol 78:4323–4329 [CrossRef]
    [Google Scholar]
  8. Barr J. N. 2007; Bunyavirus mRNA synthesis is coupled to translation to prevent premature transcription termination. RNA 13:731–736 [View Article][PubMed]
    [Google Scholar]
  9. Barr J. N., Wertz G. W. 2004; Bunyamwera bunyavirus RNA synthesis requires cooperation of 3′- and 5′-terminal sequences. J Virol 78:1129–1138 [View Article][PubMed]
    [Google Scholar]
  10. Barr J. N., Wertz G. W. 2005; Role of the conserved nucleotide mismatch within 3′- and 5′-terminal regions of Bunyamwera virus in signaling transcription. J Virol 79:3586–3594 [View Article][PubMed]
    [Google Scholar]
  11. Barr J. N., Elliott R. M., Dunn E. F., Wertz G. W. 2003; Segment-specific terminal sequences of Bunyamwera bunyavirus regulate genome replication. Virology 311:326–338 [View Article][PubMed]
    [Google Scholar]
  12. Barr J. N., Rodgers J. W., Wertz G. W. 2005; The Bunyamwera virus mRNA transcription signal resides within both the 3′ and the 5′ terminal regions and allows ambisense transcription from a model RNA segment. J Virol 79:12602–12607 [View Article][PubMed]
    [Google Scholar]
  13. Barr J. N., Rodgers J. W., Wertz G. W. 2006; Identification of the Bunyamwera bunyavirus transcription termination signal. J Gen Virol 87:189–198 [View Article][PubMed]
    [Google Scholar]
  14. Battisti A. J., Chu Y. K., Chipman P. R., Kaufmann B., Jonsson C. B., Rossmann M. G. 2011; Structural studies of Hantaan virus. J Virol 85:835–841 [View Article][PubMed]
    [Google Scholar]
  15. Bellocq C., Kolakofsky D. 1987; Translational requirement for La Crosse virus S-mRNA synthesis: a possible mechanism. J Virol 61:3960–3967[PubMed]
    [Google Scholar]
  16. Bergeron E., Vincent M. J., Nichol S. T. 2007; Crimean–Congo hemorrhagic fever virus glycoprotein processing by the endoprotease SKI-1/S1P is critical for virus infectivity. J Virol 81:13271–13276 [View Article][PubMed]
    [Google Scholar]
  17. Bergeron E., Albariño C. G., Khristova M. L., Nichol S. T. 2010; Crimean–Congo hemorrhagic fever virus-encoded ovarian tumor protease activity is dispensable for virus RNA polymerase function. J Virol 84:216–226 [View Article][PubMed]
    [Google Scholar]
  18. Bertolotti-Ciarlet A., Smith J., Strecker K., Paragas J., Altamura L. A., McFalls J. M., Frias-Stäheli N., García-Sastre A., Schmaljohn C. S., Doms R. W. 2005; Cellular localization and antigenic characterization of Crimean–Congo hemorrhagic fever virus glycoproteins. J Virol 79:6152–6161 [View Article][PubMed]
    [Google Scholar]
  19. Blakqori G., Delhaye S., Habjan M., Blair C. D., Sánchez-Vargas I., Olson K. E., Attarzadeh-Yazdi G., Fragkoudis R., Kohl A. et al. 2007; La Crosse bunyavirus nonstructural protein NSs serves to suppress the type I interferon system of mammalian hosts. J Virol 81:4991–4999 [View Article][PubMed]
    [Google Scholar]
  20. Blakqori G., van Knippenberg I., Elliott R. M. 2009; Bunyamwera orthobunyavirus S-segment untranslated regions mediate poly(A) tail-independent translation. J Virol 83:3637–3646 [View Article][PubMed]
    [Google Scholar]
  21. Boudko S. P., Kuhn R. J., Rossmann M. G. 2007; The coiled-coil domain structure of the Sin Nombre virus nucleocapsid protein. J Mol Biol 366:1538–1544 [View Article][PubMed]
    [Google Scholar]
  22. 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 [View Article][PubMed]
    [Google Scholar]
  23. Bridgen A., Weber F., Fazakerley J. K., Elliott R. M. 2001; Bunyamwera bunyavirus nonstructural protein NSs is a nonessential gene product that contributes to viral pathogenesis. Proc Natl Acad Sci U S A 98:664–669 [View Article][PubMed]
    [Google Scholar]
  24. Bridgen A., Dalrymple D. A., Weber F., Elliott R. M. 2004; Inhibition of Dugbe nairovirus replication by human MxA protein. Virus Res 99:47–50 [View Article][PubMed]
    [Google Scholar]
  25. Capodagli G. C., McKercher M. A., Baker E. A., Masters E. M., Brunzelle J. S., Pegan S. D. 2011; Structural analysis of a viral ovarian tumor domain protease from the Crimean–Congo hemorrhagic fever virus in complex with covalently bonded ubiquitin. J Virol 85:3621–3630 [View Article][PubMed]
    [Google Scholar]
  26. Chattopadhyay S., Marques J. T., Yamashita M., Peters K. L., Smith K., Desai A., Williams B. R., Sen G. C. 2010; Viral apoptosis is induced by IRF-3-mediated activation of Bax. EMBO J 29:1762–1773 [View Article][PubMed]
    [Google Scholar]
  27. Cheng E., Haque A., Rimmer M. A., Hussein I. T., Sheema S., Little A., Mir M. A. 2011; Characterization of the interaction between hantavirus nucleocapsid protein (N) and ribosomal protein S19 (RPS19). J Biol Chem 286:11814–11824 [View Article][PubMed]
    [Google Scholar]
  28. Cifuentes-Muñoz N., Barriga G. P., Valenzuela P. D., Tischler N. D. 2011; Aromatic and polar residues spanning the candidate fusion peptide of the Andes virus Gc protein are essential for membrane fusion and infection. J Gen Virol 92:552–563 [View Article][PubMed]
    [Google Scholar]
  29. Colón-Ramos D. A., Irusta P. M., Gan E. C., Olson M. R., Song J., Morimoto R. I., Elliott R. M., Lombard M., Hollingsworth R. et al. 2003; Inhibition of translation and induction of apoptosis by bunyaviral nonstructural proteins bearing sequence similarity to reaper. Mol Biol Cell 14:4162–4172 [View Article][PubMed]
    [Google Scholar]
  30. de Haan P., Kormelink R., de Oliveira Resende R., van Poelwijk F., Peters D., Goldbach R. 1991; Tomato spotted wilt virus L RNA encodes a putative RNA polymerase. J Gen Virol 72:2207–2216 [View Article][PubMed]
    [Google Scholar]
  31. de Medeiros R. B., Figueiredo J., Resende R. O., De Avila A. C. 2005; Expression of a viral polymerase-bound host factor turns human cell lines permissive to a plant- and insect-infecting virus. Proc Natl Acad Sci U S A 102:1175–1180 [View Article][PubMed]
    [Google Scholar]
  32. Deyde V. M., Rizvanov A. A., Chase J., Otteson E. W., St Jeor S. C. 2005; Interactions and trafficking of Andes and Sin Nombre hantavirus glycoproteins G1 and G2. Virology 331:307–315 [View Article][PubMed]
    [Google Scholar]
  33. Dias A., Bouvier D., Crépin T., McCarthy A. A., Hart D. J., Baudin F., Cusack S., Ruigrok R. W. 2009; The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 458:914–918 [View Article][PubMed]
    [Google Scholar]
  34. Eifan S. A., Elliott R. M. 2009; Mutational analysis of the Bunyamwera orthobunyavirus nucleocapsid protein gene. J Virol 83:11307–11317 [View Article][PubMed]
    [Google Scholar]
  35. Estrada D. F., De Guzman R. N. 2011; Structural characterization of the Crimean–Congo hemorrhagic fever virus Gn tail provides insight into virus assembly. J Biol Chem 286:21678–21686 [View Article][PubMed]
    [Google Scholar]
  36. Estrada D. F., Boudreaux D. M., Zhong D., St Jeor S. C., De Guzman R. N. 2009; The hantavirus glycoprotein G1 tail contains dual CCHC-type classical zinc fingers. J Biol Chem 284:8654–8660 [View Article][PubMed]
    [Google Scholar]
  37. Ferron F., Li Z., Danek E. I., Luo D., Wong Y., Coutard B., Lantez V., Charrel R., Canard B. et al. 2011; The hexamer structure of Rift Valley fever virus nucleoprotein suggests a mechanism for its assembly into ribonucleoprotein complexes. PLoS Pathog 7:e1002030 [View Article][PubMed]
    [Google Scholar]
  38. Flick K., Katz A., Overby A., Feldmann H., Pettersson R. F., Flick R. 2004; Functional analysis of the noncoding regions of the Uukuniemi virus (Bunyaviridae) RNA segments. J Virol 78:11726–11738 [View Article][PubMed]
    [Google Scholar]
  39. Fontana J., López-Montero N., Elliott R. M., Fernández J. J., Risco C. 2008; The unique architecture of Bunyamwera virus factories around the Golgi complex. Cell Microbiol 10:2012–2028 [View Article][PubMed]
    [Google Scholar]
  40. Freiberg A. N., Sherman M. B., Morais M. C., Holbrook M. R., Watowich S. J. 2008; Three-dimensional organization of Rift Valley fever virus revealed by cryoelectron tomography. J Virol 82:10341–10348 [View Article][PubMed]
    [Google Scholar]
  41. Frese M., Kochs G., Feldmann H., Hertkorn C., Haller O. 1996; Inhibition of bunyaviruses, phleboviruses, and hantaviruses by human MxA protein. J Virol 70:915–923[PubMed]
    [Google Scholar]
  42. Frias-Staheli N., Giannakopoulos N. V., Kikkert M., Taylor S. L., Bridgen A., Paragas J., Richt J. A., Rowland R. R., Schmaljohn C. S. et al. 2007; Ovarian tumor domain-containing viral proteases evade ubiquitin- and ISG15-dependent innate immune responses. Cell Host Microbe 2:404–416 [View Article][PubMed]
    [Google Scholar]
  43. Garcia S., Billecocq A., Crance J. M., Prins M., Garin D., Bouloy M. 2006; Viral suppressors of RNA interference impair RNA silencing induced by a Semliki Forest virus replicon in tick cells. J Gen Virol 87:1985–1989 [View Article][PubMed]
    [Google Scholar]
  44. Garcin D., Lezzi M., Dobbs M., Elliott R. M., Schmaljohn C., Kang C. Y., Kolakofsky D. 1995; The 5′ ends of Hantaan virus (Bunyaviridae) RNAs suggest a prime-and-realign mechanism for the initiation of RNA synthesis. J Virol 69:5754–5762[PubMed]
    [Google Scholar]
  45. Gauliard N., Billecocq A., Flick R., Bouloy M. 2006; Rift Valley fever virus noncoding regions of L, M and S segments regulate RNA synthesis. Virology 351:170–179 [View Article][PubMed]
    [Google Scholar]
  46. Gavrilovskaya I. N., Shepley M., Shaw R., Ginsberg M. H., Mackow E. R. 1998; β3 Integrins mediate the cellular entry of hantaviruses that cause respiratory failure. Proc Natl Acad Sci U S A 95:7074–7079 [View Article][PubMed]
    [Google Scholar]
  47. Gerrard S. R., Nichol S. T. 2002; Characterization of the Golgi retention motif of Rift Valley fever virus GN glycoprotein. J Virol 76:12200–12210 [View Article][PubMed]
    [Google Scholar]
  48. Gerrard S. R., Bird B. H., Albariño 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 [View Article][PubMed]
    [Google Scholar]
  49. Goldsmith C. S., Elliott L. H., Peters C. J., Zaki S. R. 1995; Ultrastructural characteristics of Sin Nombre virus, causative agent of hantavirus pulmonary syndrome. Arch Virol 140:2107–2122 [View Article][PubMed]
    [Google Scholar]
  50. Guelmino D. J., Jevtic M. 1955; An epidemiological and hematological study of sandfly fever in Serbia. Acta Trop 12:179–182[PubMed]
    [Google Scholar]
  51. Habjan M., Andersson I., Klingström J., Schümann M., Martin A., Zimmermann P., Wagner V., Pichlmair A., Schneider U. et al. 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 [View Article][PubMed]
    [Google Scholar]
  52. Habjan M., Pichlmair A., Elliott R. M., Overby A. K., 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 RNA-dependent protein kinase. J Virol 83:4365–4375 [View Article][PubMed]
    [Google Scholar]
  53. Haferkamp S., Fernando L., Schwarz T. F., Feldmann H., Flick R. 2005; Intracellular localization of Crimean–Congo hemorrhagic fever (CCHF) virus glycoproteins. Virol J 2:42 [View Article][PubMed]
    [Google Scholar]
  54. Hardestam J., Klingström J., Mattsson K., Lundkvist A. 2005; HFRS causing hantaviruses do not induce apoptosis in confluent Vero E6 and A-549 cells. J Med Virol 76:234–240 [View Article][PubMed]
    [Google Scholar]
  55. Hepojoki J., Strandin T., Wang H., Vapalahti O., Vaheri A., Lankinen H. 2010; Cytoplasmic tails of hantavirus glycoproteins interact with the nucleocapsid protein. J Gen Virol 91:2341–2350 [View Article][PubMed]
    [Google Scholar]
  56. Honig J. E., Osborne J. C., Nichol S. T. 2004; Crimean–Congo hemorrhagic fever virus genome L RNA segment and encoded protein. Virology 321:29–35 [View Article][PubMed]
    [Google Scholar]
  57. Huiskonen J. T., Hepojoki J., Laurinmäki P., Vaheri A., Lankinen H., Butcher S. J., Grünewald K. 2010; Electron cryotomography of Tula hantavirus suggests a unique assembly paradigm for enveloped viruses. J Virol 84:4889–4897 [View Article][PubMed]
    [Google Scholar]
  58. Ikegami T., Won S., Peters C. J., 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 [View Article][PubMed]
    [Google Scholar]
  59. Ikegami T., Won S., Peters C. J., Makino S. 2007; Characterization of Rift Valley fever virus transcriptional terminations. J Virol 81:8421–8438 [View Article][PubMed]
    [Google Scholar]
  60. Ikegami T., Narayanan K., Won S., Kamitani W., Peters C. J., 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 [View Article][PubMed]
    [Google Scholar]
  61. Jääskeläinen K. M., Kaukinen P., Minskaya E. S., Plyusnina A., Vapalahti O., Elliott R. M., Weber F., Vaheri A., Plyusnin A. 2007; Tula and Puumala hantavirus NSs ORFs are functional and the products inhibit activation of the interferon-beta promoter. J Med Virol 79:1527–1536 [View Article][PubMed]
    [Google Scholar]
  62. James T. W., Frias-Staheli N., Bacik J. P., Levingston Macleod J. M., Khajehpour M., García-Sastre A., Mark B. L. 2011; Structural basis for the removal of ubiquitin and interferon-stimulated gene 15 by a viral ovarian tumor domain-containing protease. Proc Natl Acad Sci U S A 108:2222–2227 [View Article][PubMed]
    [Google Scholar]
  63. Jin H., Elliott R. M. 1993; Characterization of Bunyamwera virus S RNA that is transcribed and replicated by the L protein expressed from recombinant vaccinia virus. J Virol 67:1396–1404[PubMed]
    [Google Scholar]
  64. Kainz M., Hilson P., Sweeney L., Derose E., German T. L. 2004; Interaction between Tomato spotted wilt virus N protein monomers involves nonelectrostatic forces governed by multiple distinct regions in the primary structure. Phytopathology 94:759–765 [View Article][PubMed]
    [Google Scholar]
  65. Kalveram B., Lihoradova O., Ikegami T. 2011; NSs protein of Rift Valley fever virus promotes posttranslational downregulation of the TFIIH subunit p62. J Virol 85:6234–6243 [View Article][PubMed]
    [Google Scholar]
  66. Kang J. I., Park S. H., Lee P. W., Ahn B. Y. 1999; Apoptosis is induced by hantaviruses in cultured cells. Virology 264:99–105 [View Article][PubMed]
    [Google Scholar]
  67. Katz A., Freiberg A. N., Backström V., Schulz A. R., Mateos A., Holm L., Pettersson R. F., Vaheri A., Flick R., Plyusnin A. 2010; Oligomerization of Uukuniemi virus nucleocapsid protein. Virol J 7:187 [View Article][PubMed]
    [Google Scholar]
  68. Kaukinen P., Vaheri A., Plyusnin A. 2003; Mapping of the regions involved in homotypic interactions of Tula hantavirus N protein. J Virol 77:10910–10916 [View Article][PubMed]
    [Google Scholar]
  69. Khan A. S., Khabbaz R. F., Armstrong L. R., Holman R. C., Bauer S. P., Graber J., Strine T., Miller G., Reef S. et al. 1996; Hantavirus pulmonary syndrome: the first 100 US cases. J Infect Dis 173:1297–1303 [View Article][PubMed]
    [Google Scholar]
  70. Kikkert M., Van Lent J., Storms M., Bodegom P., Kormelink R., Goldbach R. 1999; Tomato spotted wilt virus particle morphogenesis in plant cells. J Virol 73:2288–2297[PubMed]
    [Google Scholar]
  71. Kinsella E., Martin S. G., Grolla A., Czub M., Feldmann H., Flick R. 2004; Sequence determination of the Crimean–Congo hemorrhagic fever virus L segment. Virology 321:23–28 [View Article][PubMed]
    [Google Scholar]
  72. Klingström J., Hardestam J., Stoltz M., Zuber B., Lundkvist A., Linder S., Ahlm C. 2006; Loss of cell membrane integrity in Puumala hantavirus-infected patients correlates with levels of epithelial cell apoptosis and perforin. J Virol 80:8279–8282 [View Article][PubMed]
    [Google Scholar]
  73. Kohl A., Clayton R. F., Weber F., Bridgen A., Randall R. E., Elliott R. M. 2003; Bunyamwera virus nonstructural protein NSs counteracts interferon regulatory factor 3-mediated induction of early cell death. J Virol 77:7999–8008 [View Article][PubMed]
    [Google Scholar]
  74. Kohl A., Dunn E. F., Lowen A. C., Elliott R. M. 2004; Complementarity, sequence and structural elements within the 3′ and 5′ non-coding regions of the Bunyamwera orthobunyavirus S segment determine promoter strength. J Gen Virol 85:3269–3278 [View Article][PubMed]
    [Google Scholar]
  75. Kormelink R., Storms M., Van Lent J., Peters D., Goldbach R. 1994; Expression and subcellular location of the NSM protein of tomato spotted wilt virus (TSWV), a putative viral movement protein. Virology 200:56–65 [View Article][PubMed]
    [Google Scholar]
  76. Kuismanen E., Hedman K., Saraste J., Pettersson R. F. 1982; Uukuniemi virus maturation: accumulation of virus particles and viral antigens in the Golgi complex. Mol Cell Biol 2:1444–1458[PubMed]
    [Google Scholar]
  77. Le May N., Gauliard N., Billecocq A., Bouloy M. 2005; The N terminus of Rift Valley fever virus nucleoprotein is essential for dimerization. J Virol 79:11974–11980 [View Article][PubMed]
    [Google Scholar]
  78. Le May N., Mansuroglu Z., Léger P., Josse T., Blot G., Billecocq A., Flick R., Jacob Y., Bonnefoy E., Bouloy M. 2008; A SAP30 complex inhibits IFN-β expression in Rift Valley fever virus infected cells. PLoS Pathog 4:e13 [View Article][PubMed]
    [Google Scholar]
  79. Leonard V. H. J., Kohl A., Osborne J. C., McLees A., Elliott R. M. 2005; Homotypic interaction of Bunyamwera virus nucleocapsid protein. J Virol 79:13166–13172 [View Article][PubMed]
    [Google Scholar]
  80. Léonard V. H. J., Kohl A., Hart T. J., Elliott R. M. 2006; Interaction of Bunyamwera orthobunyavirus NSs protein with mediator protein MED8: a mechanism for inhibiting the interferon response. J Virol 80:9667–9675 [View Article][PubMed]
    [Google Scholar]
  81. Li X. D., Kukkonen S., Vapalahti O., Plyusnin A., Lankinen H., Vaheri A. 2004; Tula hantavirus infection of Vero E6 cells induces apoptosis involving caspase 8 activation. J Gen Virol 85:3261–3268 [View Article][PubMed]
    [Google Scholar]
  82. López N., Franze-Fernández M. T. 2007; A single stem-loop structure in Tacaribe arenavirus intergenic region is essential for transcription termination but is not required for a correct initiation of transcription and replication. Virus Res 124:237–244 [View Article][PubMed]
    [Google Scholar]
  83. López-Montero N., Risco C. 2011; Self-protection and survival of arbovirus-infected mosquito cells. Cell Microbiol 13:300–315 [View Article][PubMed]
    [Google Scholar]
  84. Lowen A. C., Elliott R. M. 2005; Mutational analyses of the nonconserved sequences in the Bunyamwera orthobunyavirus S segment untranslated regions. J Virol 79:12861–12870 [View Article][PubMed]
    [Google Scholar]
  85. Lowen A. C., Boyd A., Fazakerley J. K., Elliott R. M. 2005; Attenuation of bunyavirus replication by rearrangement of viral coding and noncoding sequences. J Virol 79:6940–6946 [View Article][PubMed]
    [Google Scholar]
  86. Lozach P. Y., Mancini R., Bitto D., Meier R., Oestereich L., Overby A. K., Pettersson R. F., Helenius A. 2010; Entry of bunyaviruses into mammalian cells. Cell Host Microbe 7:488–499 [View Article][PubMed]
    [Google Scholar]
  87. Lozach P. Y., Kühbacher A., Meier R., Mancini R., Bitto D., Bouloy M., Helenius A. 2011; DC-SIGN as a receptor for phleboviruses. Cell Host Microbe 10:75–88 [View Article][PubMed]
    [Google Scholar]
  88. Maltezou H. C., Papa A. 2010; Crimean–Congo hemorrhagic fever: risk for emergence of new endemic foci in Europe?. Travel Med Infect Dis 8:139–143 [View Article][PubMed]
    [Google Scholar]
  89. Mardani M., Keshtkar-Jahromi M., Ataie B., Adibi P. 2009; Crimean–Congo hemorrhagic fever virus as a nosocomial pathogen in Iran. Am J Trop Med Hyg 81:675–678 [View Article][PubMed]
    [Google Scholar]
  90. Marriott A. C., Nuttall P. A. 1996; Large RNA segment of Dugbe nairovirus encodes the putative RNA polymerase. J Gen Virol 77:1775–1780 [View Article][PubMed]
    [Google Scholar]
  91. Matsuoka Y., Chen S. Y., Compans R. W. 1991; Bunyavirus protein transport and assembly. Curr Top Microbiol Immunol 169:161–179[PubMed]
    [Google Scholar]
  92. Matsuoka Y., Chen S. Y., Compans R. W. 1994; A signal for Golgi retention in the bunyavirus G1 glycoprotein. J Biol Chem 269:22565–22573[PubMed]
    [Google Scholar]
  93. Mir M. A., Panganiban A. T. 2004; Trimeric hantavirus nucleocapsid protein binds specifically to the viral RNA panhandle. J Virol 78:8281–8288 [View Article][PubMed]
    [Google Scholar]
  94. Mir M. A., Panganiban A. T. 2005; The hantavirus nucleocapsid protein recognizes specific features of the viral RNA panhandle and is altered in conformation upon RNA binding. J Virol 79:1824–1835 [View Article][PubMed]
    [Google Scholar]
  95. Mir M. A., Panganiban A. T. 2010; The triplet repeats of the Sin Nombre hantavirus 5′ untranslated region are sufficient in cis for nucleocapsid-mediated translation initiation. J Virol 84:8937–8944 [View Article][PubMed]
    [Google Scholar]
  96. Mir M. A., Duran W. A., Hjelle B. L., Ye C., Panganiban A. T. 2008; Storage of cellular 5′ mRNA caps in P bodies for viral cap-snatching. Proc Natl Acad Sci U S A 105:19294–19299 [View Article][PubMed]
    [Google Scholar]
  97. Mohamed M., McLees A., Elliott R. M. 2009; Viruses in the Anopheles A, Anopheles B, and Tete serogroups in the Orthobunyavirus genus (family Bunyaviridae) do not encode an NSs protein. J Virol 83:7612–7618 [View Article][PubMed]
    [Google Scholar]
  98. Mohl B. P., Barr J. N. 2009; Investigating the specificity and stoichiometry of RNA binding by the nucleocapsid protein of Bunyamwera virus. RNA 15:391–399 [View Article][PubMed]
    [Google Scholar]
  99. Müller R., Poch O., Delarue M., Bishop D. H., Bouloy M. 1994; Rift Valley fever virus L segment: correction of the sequence and possible functional role of newly identified regions conserved in RNA-dependent polymerases. J Gen Virol 75:1345–1352 [View Article][PubMed]
    [Google Scholar]
  100. Murphy F. A., Harrison A. K., Whitfield S. G. 1973; Bunyaviridae: morphologic and morphogenetic similarities of Bunyamwera serologic supergroup viruses and several other arthropod-borne viruses. Intervirology 1:297–316 [View Article][PubMed]
    [Google Scholar]
  101. Novoa R. R., Calderita G., Cabezas P., Elliott R. M., Risco C. 2005; Key Golgi factors for structural and functional maturation of Bunyamwera virus. J Virol 79:10852–10863 [View Article][PubMed]
    [Google Scholar]
  102. Ontiveros S. J., Li Q., Jonsson C. B. 2010; Modulation of apoptosis and immune signaling pathways by the Hantaan virus nucleocapsid protein. Virology 401:165–178 [View Article][PubMed]
    [Google Scholar]
  103. Osborne J. C., Elliott R. M. 2000; RNA binding properties of Bunyamwera virus nucleocapsid protein and selective binding to an element in the 5′ terminus of the negative-sense S segment. J Virol 74:9946–9952 [View Article][PubMed]
    [Google Scholar]
  104. Overby A. K., Pettersson R. F., Neve E. P. 2007; The glycoprotein cytoplasmic tail of Uukuniemi virus (Bunyaviridae) interacts with ribonucleoproteins and is critical for genome packaging. J Virol 81:3198–3205 [View Article][PubMed]
    [Google Scholar]
  105. Overby A. K., Pettersson R. F., Grünewald K., Huiskonen J. T. 2008; Insights into bunyavirus architecture from electron cryotomography of Uukuniemi virus. Proc Natl Acad Sci U S A 105:2375–2379 [View Article][PubMed]
    [Google Scholar]
  106. Padula P. J., Edelstein A., Miguel S. D., López N. M., Rossi C. M., Rabinovich R. D. 1998; Hantavirus pulmonary syndrome outbreak in Argentina: molecular evidence for person-to-person transmission of Andes virus. Virology 241:323–330 [View Article][PubMed]
    [Google Scholar]
  107. Pappu H. R., Jones R. A., Jain R. K. 2009; Global status of tospovirus epidemics in diverse cropping systems: successes achieved and challenges ahead. Virus Res 141:219–236 [View Article][PubMed]
    [Google Scholar]
  108. Pekosz A., Phillips J., Pleasure D., Merry D., Gonzalez-Scarano F. 1996; Induction of apoptosis by La Crosse virus infection and role of neuronal differentiation and human bcl-2 expression in its prevention. J Virol 70:5329–5335[PubMed]
    [Google Scholar]
  109. Pettersson R. F., von Bonsdorff C. H. 1975; Ribonucleoproteins of Uukuniemi virus are circular. J Virol 15:386–392[PubMed]
    [Google Scholar]
  110. Pinheiro F. P., Travassos da Rosa A. P., Gomes M. L., LeDuc J. W., Hoch A. L. 1982; Transmission of Oropouche virus from man to hamster by the midge Culicoides paraensis . Science 215:1251–1253 [View Article][PubMed]
    [Google Scholar]
  111. Pinschewer D. D., Perez M., de la Torre J. C. 2005; Dual role of the lymphocytic choriomeningitis virus intergenic region in transcription termination and virus propagation. J Virol 79:4519–4526 [View Article][PubMed]
    [Google Scholar]
  112. Piper M. E., Sorenson D. R., Gerrard S. R. 2011; Efficient cellular release of Rift Valley fever virus requires genomic RNA. PLoS One 6:e18070 [View Article][PubMed]
    [Google Scholar]
  113. Plyusnin A. 2002; Genetics of hantaviruses: implications to taxonomy. Arch Virol 147:665–682 [View Article][PubMed]
    [Google Scholar]
  114. Poch O., Blumberg B. M., Bougueleret L., Tordo N. 1990; Sequence comparison of five polymerases (L proteins) of unsegmented negative-strand RNA viruses: theoretical assignment of functional domains. J Gen Virol 71:1153–1162 [View Article][PubMed]
    [Google Scholar]
  115. Raju R., Kolakofsky D. 1989; The ends of La Crosse virus genome and antigenome RNAs within nucleocapsids are base paired. J Virol 63:122–128[PubMed]
    [Google Scholar]
  116. Raju R., Raju L., Kolakofsky D. 1989; The translational requirement for complete La Crosse virus mRNA synthesis is cell-type dependent. J Virol 63:5159–5165[PubMed]
    [Google Scholar]
  117. Ramanathan H. N., Chung D. H., Plane S. J., Sztul E., Chu Y. K., Guttieri M. C., McDowell M., Ali G., Jonsson C. B. 2007; Dynein-dependent transport of the Hantaan virus nucleocapsid protein to the endoplasmic reticulum–Golgi intermediate compartment. J Virol 81:8634–8647 [View Article][PubMed]
    [Google Scholar]
  118. Ravkov E. V., Nichol S. T., Compans R. W. 1997; Polarized entry and release in epithelial cells of Black Creek Canal virus, a New World hantavirus. J Virol 71:1147–1154[PubMed]
    [Google Scholar]
  119. Ravkov E. V., Nichol S. T., Peters C. J., Compans R. W. 1998; Role of actin microfilaments in Black Creek Canal virus morphogenesis. J Virol 72:2865–2870[PubMed]
    [Google Scholar]
  120. Raymond D. D., Piper M. E., Gerrard S. R., Smith J. L. 2010; Structure of the Rift Valley fever virus nucleocapsid protein reveals another architecture for RNA encapsidation. Proc Natl Acad Sci U S A 107:11769–11774 [View Article][PubMed]
    [Google Scholar]
  121. Reguera J., Weber F., Cusack S. 2010; Bunyaviridae RNA polymerases (L-protein) have an N-terminal, influenza-like endonuclease domain, essential for viral cap-dependent transcription. PLoS Pathog 6:e1001101 [View Article][PubMed]
    [Google Scholar]
  122. Ribeiro D., Borst J. W., Goldbach R., Kormelink R. 2009; Tomato spotted wilt virus nucleocapsid protein interacts with both viral glycoproteins Gn and Gc in planta . Virology 383:121–130 [View Article][PubMed]
    [Google Scholar]
  123. Salanueva I. J., Novoa R. R., Cabezas P., López-Iglesias C., Carrascosa J. L., Elliott R. M., Risco C. 2003; Polymorphism and structural maturation of bunyamwera virus in Golgi and post-Golgi compartments. J Virol 77:1368–1381 [View Article][PubMed]
    [Google Scholar]
  124. Schmaljohn C. S., Nichol S. T. 2006; Bunyaviridae . In Fields Virology, 5th edn. vol. 2 pp. 1741–1789 Edited by Knipe D. M., Howley P. M. Philadelphia, PA: Lippincott Williams & Wilkins;
    [Google Scholar]
  125. Schnettler E., Hemmes H., Huismann R., Goldbach R., Prins M., Kormelink R. 2010; Diverging affinity of tospovirus RNA silencing suppressor proteins, NSs, for various RNA duplex molecules. J Virol 84:11542–11554 [View Article][PubMed]
    [Google Scholar]
  126. Scholten O. E., Paul H., Peters D., Van Lent J. W., Goldbach R. W. 1994; In situ localisation of beet necrotic yellow vein virus (BNYVV) in rootlets of susceptible and resistant beet plants. Arch Virol 136:349–361 [View Article][PubMed]
    [Google Scholar]
  127. Sherman M. B., Freiberg A. N., Holbrook M. R., Watowich S. J. 2009; Single-particle cryo-electron microscopy of Rift Valley fever virus. Virology 387:11–15 [View Article][PubMed]
    [Google Scholar]
  128. Shi X., Elliott R. M. 2002; Golgi localization of Hantaan virus glycoproteins requires coexpression of G1 and G2. Virology 300:31–38 [View Article][PubMed]
    [Google Scholar]
  129. Shi X., Elliott R. M. 2004; Analysis of N-linked glycosylation of hantaan virus glycoproteins and the role of oligosaccharide side chains in protein folding and intracellular trafficking. J Virol 78:5414–5422 [View Article][PubMed]
    [Google Scholar]
  130. Shi X., Elliott R. M. 2009; Generation and analysis of recombinant Bunyamwera orthobunyaviruses expressing V5 epitope-tagged L proteins. J Gen Virol 90:297–306 [View Article][PubMed]
    [Google Scholar]
  131. Shi X., Kohl A., Léonard V. H., Li P., McLees A., Elliott R. M. 2006; Requirement of the N-terminal region of orthobunyavirus nonstructural protein NSm for virus assembly and morphogenesis. J Virol 80:8089–8099 [View Article][PubMed]
    [Google Scholar]
  132. Shi X., Kohl A., Li P., Elliott R. M. 2007; Role of the cytoplasmic tail domains of Bunyamwera orthobunyavirus glycoproteins Gn and Gc in virus assembly and morphogenesis. J Virol 81:10151–10160 [View Article][PubMed]
    [Google Scholar]
  133. Shi X., van Mierlo J. T., French A., Elliott R. M. 2010; Visualizing the replication cycle of Bunyamwera orthobunyavirus expressing fluorescent protein-tagged Gc glycoprotein. J Virol 84:8460–8469 [View Article][PubMed]
    [Google Scholar]
  134. Sin S. H., McNulty B. C., Kennedy G. G., Moyer J. W. 2005; Viral genetic determinants for thrips transmission of tomato spotted wilt virus. Proc Natl Acad Sci U S A 102:5168–5173 [View Article][PubMed]
    [Google Scholar]
  135. Smith J. F., Pifat D. Y. 1982; Morphogenesis of sandfly fever viruses (Bunyaviridae family). Virology 121:61–81 [View Article][PubMed]
    [Google Scholar]
  136. Snippe M., Smeenk L., Goldbach R., Kormelink R. 2007a; The cytoplasmic domain of tomato spotted wilt virus Gn glycoprotein is required for Golgi localisation and interaction with Gc. Virology 363:272–279 [View Article][PubMed]
    [Google Scholar]
  137. Snippe M., Willem Borst J., Goldbach R., Kormelink R. 2007b; Tomato spotted wilt virus Gc and N proteins interact in vivo . Virology 357:115–123 [View Article][PubMed]
    [Google Scholar]
  138. Soldan S. S., Plassmeyer M. L., Matukonis M. K., González-Scarano F. 2005; La Crosse virus nonstructural protein NSs counteracts the effects of short interfering RNA. J Virol 79:234–244 [View Article][PubMed]
    [Google Scholar]
  139. Song J.-W., Baek L. J., Schmaljohn C. S., Yanagihara R. 2007; Thottapalayam virus, a prototype shrewborne hantavirus. Emerg Infect Dis 13:980–985[PubMed] [CrossRef]
    [Google Scholar]
  140. Takeda A., Sugiyama K., Nagano H., Mori M., Kaido M., Mise K., Tsuda S., Okuno T. 2002; Identification of a novel RNA silencing suppressor, NSs protein of tomato spotted wilt virus. FEBS Lett 532:75–79 [View Article][PubMed]
    [Google Scholar]
  141. Taylor S. L., Frias-Staheli N., García-Sastre A., Schmaljohn C. S. 2009; Hantaan virus nucleocapsid protein binds to importin alpha proteins and inhibits tumor necrosis factor alpha-induced activation of nuclear factor kappa B. J Virol 83:1271–1279 [View Article][PubMed]
    [Google Scholar]
  142. Terasaki K., Murakami S., Lokugamage K. G., Makino S. 2011; Mechanism of tripartite RNA genome packaging in Rift Valley fever virus. Proc Natl Acad Sci U S A 108:804–809 [View Article][PubMed]
    [Google Scholar]
  143. Tesh R. B., Modi G. B. 1987; Maintenance of Toscana virus in Phlebotomus perniciosus by vertical transmission. Am J Trop Med Hyg 36:189–193[PubMed]
    [Google Scholar]
  144. Thomas D., Blakqori G., Wagner V., Banholzer M., Kessler N., Elliott R. M., Haller O., Weber F. 2004; Inhibition of RNA polymerase II phosphorylation by a viral interferon antagonist. J Biol Chem 279:31471–31477 [View Article][PubMed]
    [Google Scholar]
  145. Thompson W. H., Beaty B. J. 1977; Venereal transmission of La Crosse (California encephalitis) arbovirus in Aedes triseriatus mosquitoes. Science 196:530–531 [View Article][PubMed]
    [Google Scholar]
  146. Uhrig J. F., Soellick T. R., Minke C. J., Philipp C., Kellmann J. W., Schreier P. H. 1999; Homotypic interaction and multimerization of nucleocapsid protein of tomato spotted wilt tospovirus: identification and characterization of two interacting domains. Proc Natl Acad Sci U S A 96:55–60 [View Article][PubMed]
    [Google Scholar]
  147. van Knippenberg I., Goldbach R., Kormelink R. 2004; In vitro transcription of tomato spotted wilt virus is independent of translation. J Gen Virol 85:1335–1338 [View Article][PubMed]
    [Google Scholar]
  148. van Knippenberg I., Goldbach R., Kormelink R. 2005; Tomato spotted wilt virus S-segment mRNAs have overlapping 3′-ends containing a predicted stem-loop structure and conserved sequence motif. Virus Res 110:125–131 [View Article][PubMed]
    [Google Scholar]
  149. van Knippenberg I., Carlton-Smith C., Elliott R. M. 2010; The N-terminus of Bunyamwera orthobunyavirus NSs protein is essential for interferon antagonism. J Gen Virol 91:2002–2006 [View Article][PubMed]
    [Google Scholar]
  150. van Poelwijk F., Prins M., Goldbach R. 1997; Completion of the impatiens necrotic spot virus genome sequence and genetic comparison of the L proteins within the family Bunyaviridae . J Gen Virol 78:543–546[PubMed]
    [Google Scholar]
  151. Vera-Otarola J., Soto-Rifo R., Ricci E. P., Ohlmann T., Darlix J. L., López-Lastra M. 2010; The 3′ untranslated region of the Andes hantavirus small mRNA functionally replaces the poly(A) tail and stimulates cap-dependent translation initiation from the viral mRNA. J Virol 84:10420–10424 [View Article][PubMed]
    [Google Scholar]
  152. Verbruggen P., Ruf M., Blakqori G., Överby A. K., Heidemann M., Eick D., Weber F. 2011; Interferon antagonist NSs of La Crosse virus triggers a DNA damage response-like degradation of transcribing RNA polymerase II. J Biol Chem 286:3681–3692 [View Article][PubMed]
    [Google Scholar]
  153. Walter C. T., Costa Bento D. F., Alonso A. G., Barr J. N. 2011; Amino acid changes within the Bunyamwera virus nucleocapsid protein differentially affect the mRNA transcription and RNA replication activities of assembled ribonucleoprotein templates. J Gen Virol 92:80–84 [View Article][PubMed]
    [Google Scholar]
  154. Wang Y., Boudreaux D. M., Estrada D. F., Egan C. W., St Jeor S. C., De Guzman R. N. 2008; NMR structure of the N-terminal coiled coil domain of the Andes hantavirus nucleocapsid protein. J Biol Chem 283:28297–28304 [View Article][PubMed]
    [Google Scholar]
  155. Watts D. M., Pantuwatana S., DeFoliart G. R., Yuill T. M., Thompson W. H. 1973; Transovarial transmission of La Crosse virus (California encephalitis group) in the mosquito, Aedes triseriatus . Science 182:1140–1141 [View Article][PubMed]
    [Google Scholar]
  156. Won S., Ikegami T., Peters C. J., Makino S. 2007; NSm protein of Rift Valley fever virus suppresses virus-induced apoptosis. J Virol 81:13335–13345 [View Article][PubMed]
    [Google Scholar]
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