Drosophila melanogaster as a model organism for bluetongue virus replication and tropism

Journal of Virology

Volumn 86, Issue 17, 2012, Pages 9015-9024

  Shaw, Andrew E ^a   Veronesi, Eva ^b   Maurin, Guillemette ^c   Ftaich, Najate ^c   Guiguen, Francois ^c   Rixon, Frazer ^a   Ratinier, Maxime ^a   Mertens, Peter ^b   Carpenter, Simon ^b   Palmarini, Massimo ^a   Terzian, Christophe ^c   Arnaud, Frederick ^c  

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

^b INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^c University Lyon i   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORESCENT DYE; MCHERRY FLUORESCENT PROTEIN; NONSTRUCTURAL PROTEIN 3; NONSTRUCTURAL PROTEIN 3A; TETRACYCLINE; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS VECTOR;

ANIMAL EXPERIMENT; ARTICLE; BLUETONGUE ORBIVIRUS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DISEASE CARRIER; DROSOPHILA MELANOGASTER; FEASIBILITY STUDY; FEMALE; HOST PATHOGEN INTERACTION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVERSE GENETICS; TRANSGENIC ORGANISM; VIRAL TROPISM; VIRUS ENTRY; VIRUS GENOME; VIRUS PARTICLE; VIRUS PLAQUE; VIRUS REPLICATION; WESTERN BLOTTING; WILD TYPE; WOLBACHIA PIPIENTIS;

ANIMALS; BLUETONGUE; BLUETONGUE VIRUS; CATTLE; CATTLE DISEASES; CELL LINE; CERATOPOGONIDAE; DISEASE MODELS, ANIMAL; DROSOPHILA MELANOGASTER; INSECT VECTORS; VIRAL TROPISM; VIRUS REPLICATION;

ANIMALIA; ARBOVIRUS; BACTERIA (MICROORGANISMS); BLUETONGUE VIRUS; CERATOPOGONIDAE; DIPTERA; DROSOPHILA MELANOGASTER; HEXAPODA; WOLBACHIA PIPIENTIS;

EID: 84866146334     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00131-12     Document Type: Article

References (80)

1. Arnaud F, Murcia PR, Palmarini M. 2007. Mechanisms of late restriction induced by an endogenous retrovirus. J. Virol. 81:11441-11451.
2. Bansal OB, Stokes A, Bansal A, Bishop D, Roy P. 1998. Membrane organization of bluetongue virus nonstructural glycoprotein NS3. J. Virol. 72:3362-3369.
3. Baylis M, Mellor PS, Wittmann EJ, Rogers DJ. 2001. Prediction of areas around the Mediterranean at risk of bluetongue by modelling the distribution of its vector using satellite imaging. Vet. Rec. 149:639-643.
4. Beaton AR, Rodriguez J, Reddy YK, Roy P. 2002. The membrane trafficking protein calpactin forms a complex with bluetongue virus protein NS3 and mediates virus release. Proc. Natl. Acad. Sci. U. S. A. 99:13154-13159.
5. Belhouchet M, et al. 2011. Detection of a fourth orbivirus non-structural protein. PLoS One 6:e25697. doi:10.1371/journal.pone.0025697.
6. Blagrove MS, Arias-Goeta C, Failloux AB, Sinkins SP. 2011. Wolbachia strain wMel induces cytoplasmic incompatibility and blocks dengue transmission in Aedes albopictus. Proc. Natl. Acad. Sci. U. S. A. [Epub ahead of print.] doi:10.1073/pnas.1112021108.
7. Boorman J. 1974. The maintenance of laboratory colonies of Culicoides variipennis (Coq.), C. nubeculosus (M.) and C. reithi (Keiff.). Bull. Entomol. Res. 64:371-377.
8. Boorman J. 1986. Presence of bluetongue virus vectors on Rhodes. Vet. Rec. 118:21.
9. Bowne JG, Jones RH. 1966. Observations on bluetongue virus in the salivary glands of an insect vector, Culicoides variipennis. Virology 30:127-133.
10. Boyce M, Celma CC, Roy P. 2008. Development of reverse genetics systems for bluetongue virus: recovery of infectious virus from synthetic RNA transcripts. J. Virol. 82:8339-8348.
11. Brookes SM, Hyatt AD, Eaton BT. 1993. Characterization of virus inclusion bodies in bluetongue virus-infected cells. J. Gen. Virol. 74(Pt 3):525-530.
12. Caporale M, et al. 2011. Determinants of bluetongue virus virulence in murine models of disease. J. Virol. 85:11479-11489.
13. Caracappa S, et al. 2003. Identification of a novel bluetongue virus vector species of Culicoides in Sicily. Vet. Rec. 153:71-74.
14. Carpenter S, Lunt HL, Arav D, Venter GJ, Mellor PS. 2006. Oral susceptibility to bluetongue virus of Culicoides (Diptera: Ceratopogonidae) from the United Kingdom. J. Med. Entomol. 43:73-78.
15. Carpenter S, Wilson A, Mellor PS. 2009. Culicoides and the emergence of bluetongue virus in northern Europe. Trends Microbiol. 17:172-178.
16. Celma CC, Roy P. 2009. A viral nonstructural protein regulates bluetongue virus trafficking and release. J. Virol. 83:6806-6816.
17. Cherry S, Silverman N. 2006. Host-pathogen interactions in drosophila: new tricks from an old friend. Nat. Immunol. 7:911-917.
18. Clark ME, Anderson CL, Cande J, Karr TL. 2005. Widespread prevalence of wolbachia in laboratory stocks and the implications for Drosophila research. Genetics 170:1667-1675.
19. Darpel KE, et al. 2007. Clinical signs and pathology shown by British sheep and cattle infected with bluetongue virus serotype 8 derived from the 2006 outbreak in northern Europe. Vet. Rec. 161:253-261.
20. De Liberato C, et al. 2005. Identification of Culicoides obsoletus (Diptera: Ceratopogonidae) as a vector of bluetongue virus in central Italy. Vet. Rec. 156:301-304.
21. DuToit RM. 1944. The transmission of blue-tongue and horse sickness by Culicoides. Onderstepoort J. Vet. Sci. Anim. Ind. 19:7-16.
22. Ferrandon D, Imler JL, Hetru C, Hoffmann JA. 2007. The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat. Rev. Immunol. 7:862-874.
23. Finney DJ. 1952. Statistical method in biological assay, p 524-531. Hafner Publishing Company, New York, NY.
24. Foster NM, Jones RH. 1979. Multiplication rate of bluetongue virus in the vector Culicoides variipennis (Diptera: Ceratopogonidae) infected orally. J. Med. Entomol. 15:302-303.
25. Fu H. 1995. Mechanisms controlling the infection of Culicoides biting midges with bluetongue virus. Ph.D. thesis. University of Hertfordshire, Hertfordshire, United Kingdom.
26. Fu H, Leake CJ, Mertens PP, Mellor PS. 1999. The barriers to bluetongue virus infection, dissemination and transmission in the vector, Culicoides variipennis (Diptera: Ceratopogonidae). Arch. Virol. 144:747-761.
27. Fuss B, Josten F, Feix M, Hoch M. 2004. Cell movements controlled by the Notch signalling cascade during foregut development in Drosophila. Development 131:1587-1595.
28. Georgel P, et al. 2001. Drosophila immune deficiency (IMD) is a death domain protein that activates antibacterial defense and can promote apoptosis. Dev. Cell 1:503-514.
29. Girard YA, Klingler KA, Higgs S. 2004. West Nile virus dissemination and tissue tropisms in orally infected Culex pipiens quinquefasciatus. Vector Borne Zoonotic Dis. 4:109-122.
30. Glaser RL, Meola MA. 2010. The native Wolbachia endosymbionts of Drosophila melanogaster and Culex quinquefasciatus increase host resistance to West Nile virus infection. PLoS One 5:e11977. doi:10.1371/journal.pone.0011977.
31. Grimes JM, et al. 1998. The atomic structure of the bluetongue virus core. Nature 395:470-478.
32. Grimes JM, et al. 1997. An atomic model of the outer layer of the bluetongue virus core derived from X-ray crystallography and electron cryomicroscopy. Structure 5:885-893.
33. Gubbins S, Carpenter S, Baylis M, Wood JL, Mellor PS. 2008. Assessing the risk of bluetongue toUKlivestock: uncertainty and sensitivity analyses of a temperature-dependent model for the basic reproduction number. J. R. Soc. Interface 5:363-371.
34. Han Z, Harty RN. 2004. The NS3 protein of bluetongue virus exhibits viroporin-like properties. J. Biol. Chem. 279:43092-43097.
35. Hanna SL, et al. 2005. N-linked glycosylation of west nile virus envelope proteins influences particle assembly and infectivity. J. Virol. 79:13262-13274.
36. Hedges LM, Brownlie JC, O'Neill SL, Johnson KN. 2008. Wolbachia and virus protection in insects. Science 322:702.
37. Hoffmann AA, et al. 2011. Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476:454-457.
38. Holden PR, Jones P, Brookfield JF. 1993. Evidence for a Wolbachia symbiont in Drosophila melanogaster. Genet. Res. 62:23-29.
39. Hyatt AD, Zhao Y, Roy P. 1993. Release of bluetongue virus-like particles from insect cells is mediated by BTV nonstructural protein NS3/NS3A. Virology 193:592-603.
40. Jennings DM, Mellor PS. 1987. Variation in the responses of Culicoides variipennis (Diptera, Ceratopogonidae) to oral infection with bluetongue virus. Arch. Virol. 95:177-182.
41. Kim JM, et al. 2008. A single N-linked glycosylation site in the Japanese encephalitis virus prM protein is critical for cell type-specific prM protein biogenesis, virus particle release, and pathogenicity in mice. J. Virol. 82:7846-7862.
42. King DG. 1988. Cellular organization and peritrophic membrane formation in the cardia (proventriculus) of Drosophila melanogaster. J. Morphol. 196:253-282.
43. Lemaitre B, Hoffmann J. 2007. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25:697-743.
44. Mellor PS, Carpenter S, Baylis M, Mertens PPC. 2009. Bluetongue in Europe and the Mediterranean Basin, p 235-265. In Mellor PS, Baylis M, Mertens PPC (ed), Bluetongue monograph. Elsevier, Oxford, United Kingdom.
45. Mellor PS. 2004. Infection of the vectors and bluetongue epidemiology in Europe. Vet. Ital. 40:167-174.
46. Mellor PS. 1990. The replication of bluetongue virus in Culicoides vectors. Curr. Top. Microbiol. Immunol. 162:143-161.
47. Mellor PS, Carpenter S, Harrup L, Baylis M, Mertens PP. 2008. Bluetongue in Europe and the Mediterranean Basin: history of occurrence prior to 2006. Prev. Vet. Med. 87:4-20.
48. Mellor PS, Jennings M, Boorman JP. 1984. Culicoides from Greece in relation to the spread of bluetongue virus. Rev. Elev. Med. Vet. Pays Trop. 37:286-289.
49. Mellor PS, Wittmann EJ. 2002. Bluetongue virus in the Mediterranean Basin 1998-2001. Vet. J. 164:20-37.
50. Méroc E, et al. 2009. Bluetongue in Belgium: episode II. Transbound Emerg. Dis. 56:39-48.
51. Mertens PP, Brown F, Sangar DV. 1984. Assignment of the genome segments of bluetongue virus type 1 to the proteins which they encode. Virology 135:207-217.
52. Monastyrskaya K, Booth T, Nel L, Roy P. 1994. Mutation of either of two cysteine residues or deletion of the amino or carboxy terminus of nonstructural protein NS1 of bluetongue virus abrogates virus-specified tubule formation in insect cells. J. Virol. 68:2169-2178.
53. Mousson L, et al. 2010. Wolbachia modulates Chikungunya replication in Aedes albopictus. Mol. Ecol. 19:1953-1964.
54. Murcia PR, Arnaud F, Palmarini M. 2007. The transdominant endogenous retrovirus enJS56A1 associates with and blocks intracellular trafficking of Jaagsiekte sheep retrovirus Gag. J. Virol. 81:1762-1772.
55. Neil SJ, Eastman SW, Jouvenet N, Bieniasz PD. 2006. HIV-1 Vpu promotes release and prevents endocytosis of nascent retrovirus particles from the plasma membrane. PLoS Pathog. 2:e39. doi:10.1371/journal.ppat.0020039.
56. O'Neill SL, Giordano R, Colbert AM, Karr TL, Robertson HM. 1992. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc. Natl. Acad. Sci. U. S. A. 89:2699-2702.
57. Owens RJ, Limn C, Roy P. 2004. Role of an arbovirus nonstructural protein in cellular pathogenesis and virus release. J. Virol. 78:6649-6656.
58. Papadopoulos O, Mellor PS, Mertens PPC. 2009. Bluetongue control strategies. Bluetongue, p 429-452. In Mellor PS, Baylis M, Mertens PPC (ed), Bluetongue monograph. Elsevier, Oxford, United Kingdom.
59. Purse BV, et al. 2005. Climate change and the recent emergence of bluetongue in Europe. Nat. Rev. Microbiol. 3:171-181.
60. Ratinier M, et al. 2011. Identification and characterization of a novel non-structural protein of bluetongue virus. PLoS Pathog. 7:e1002477. doi:10.1371/journal.ppat.1002477.
61. Roy P. 2008. Bluetongue virus: dissection of the polymerase complex. J. Gen. Virol. 89:1789-1804.
62. Roy P. 2008. Functional mapping of bluetongue virus proteins and their interactions with host proteins during virus replication. Cell Biochem. Biophys. 50:143-157.
63. Roy P, Marshall JJ, French TJ. 1990. Structure of the bluetongue virus genome and its encoded proteins. Curr. Top. Microbiol. Immunol. 162:43-87.
64. Rubin GM. 1988. Drosophila melanogaster as an experimental organism. Science 240:1453-1459.
65. Sabin LR, Hanna SL, Cherry S. 2010. Innate antiviral immunity in Drosophila. Curr. Opin. Immunol. 22:4-9.
66. Savini G, et al. 2005. Bluetongue virus isolations from midges belonging to the Obsoletus complex (Culicoides, Diptera: Ceratopogonidae) in Italy. Vet. Rec. 157:133-139.
67. Schwartz-Cornil I, et al. 2008. Bluetongue virus: virology, pathogenesis and immunity. Vet. Res. 39:46.
68. Smith DR, Arrigo NC, Leal G, Muehlberger LE, Weaver SC. 2007. Infection and dissemination of Venezuelan equine encephalitis virus in the epidemic mosquito vector, Aedes taeniorhynchus. Am. J. Trop. Med. Hyg. 77:176-187.
69. Teixeira L, Ferreira A, Ashburner M. 2008. The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol. 6:e1000002. doi:10.1371/journal.pbio.1000002.
70. Thomas CP, Booth TF, Roy P. 1990. Synthesis of bluetongue virusencoded phosphoprotein and formation of inclusion bodies by recombinant baculovirus in insect cells: it binds the single-stranded RNA species. J. Gen. Virol. 71(Pt 9):2073-2083.
71. Toussaint JF, et al. 2006. Bluetongue in northern Europe. Vet. Rec. 159:327.
72. Vallet-Gely I, Lemaitre B, Boccard F. 2008. Bacterial strategies to overcome insect defences. Nat. Rev. Microbiol. 6:302-313.
73. Vassalos M. 1980. Cas de fièvre catarrhale du mouton dans l'ile de Lesbos (Greece). Bull. Off. Int. Epizoot. 92:547-555.
74. Velthuis AG, Saatkamp HW, Mourits MC, de Koeijer AA, Elbers AR. 2010. Financial consequences of the Dutch bluetongue serotype 8 epidemics of and 2007. Prev. Vet. Med. 93:294-304.
75. Veronesi E, et al. 2008. Quantifying bluetongue virus in adult Culicoides biting midges (Diptera: Ceratopogonidae). J. Med. Entomol. 45:129-132.
76. Walker T, et al. 2011. The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 476:450-453.
77. Wechsler SJ, McHolland LE, Tabachnick WJ. 1989. Cell lines from Culicoides variipennis (Diptera: Ceratopogonidae) support replication of bluetongue virus. J. Invertebr. Pathol. 54:385-393.
78. Wilson AJ, Mellor PS. 2009. Bluetongue in Europe: past, present and future. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364:2669-2681.
79. Wu X, Chen SY, Iwata H, Compans RW, Roy P. 1992. Multiple glycoproteins synthesized by the smallest RNA segment (S10) of bluetongue virus. J. Virol. 66:7104-7112.
80. Zhou W, Rousset F, O'Neil S. 1998. Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc. Biol. Sci. 265:509-515.