Virus and host factors affecting the clinical outcome of bluetongue virus infection

Journal of Virology

Volumn 88, Issue 18, 2014, Pages 10399-10411

  Caporale, Marco ^a,b   di Gialleonorado, Luigina ^a   Janowicz, Anna ^b   Wilkie, Gavin ^b   Shaw, Andrew ^b   Savini, Giovanni ^a   van Rijn, Piet A ^c,d   Mertens, Peter ^e   Di Ventura, Mauro ^a   Palmarini, Massimo ^b  

^a ISTITUTO ZOOPROFILATTICO SPERIMENTALE DELL ABRUZZO E DEL MOLISE G CAPORALE   (Italy)

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

^c WAGENINGEN UNIVERSITY   (Netherlands)

^d NORTH WEST UNIVERSITY   (South Africa)

^e INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS RNA;

ADULT; AGE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLUETONGUE; BLUETONGUE VIRUS 2; BLUETONGUE VIRUS 8; BREED DIFFERENCE; CONTROLLED STUDY; CULICOIDES; DISEASE PREDISPOSITION; DISEASE SEVERITY; FEMALE; GENETIC VARIABILITY; GOAT; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SEROTYPE; SHEEP; SPECIES DIFFERENCE; SYMPTOMATOLOGY; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS MUTATION; VIRUS REPLICATION; VIRUS STRAIN; VIRUS TRANSMISSION; VIRUS VIRULENCE; ANIMAL; BLUETONGUE ORBIVIRUS; CERATOPOGONIDAE; CLASSIFICATION; DISEASE CARRIER; GENETICS; GOAT DISEASE; HOST PATHOGEN INTERACTION; MOLECULAR GENETICS; PATHOGENICITY; PHYSIOLOGY; SHEEP DISEASE; VIROLOGY; VIRULENCE;

AGE FACTORS; ANIMALS; BLUETONGUE; BLUETONGUE VIRUS; CERATOPOGONIDAE; FEMALE; GENOME, VIRAL; GOAT DISEASES; GOATS; HOST-PATHOGEN INTERACTIONS; INSECT VECTORS; MALE; MICE; MOLECULAR SEQUENCE DATA; SHEEP; SHEEP DISEASES; VIRULENCE;

EID: 84906330886     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01641-14     Document Type: Article

References (86)

1. Mellor PS, Baylis M, Mertens PP. 2009. Bluetongue. Academic Press, London, United Kingdom.
2. Roy P. 2008. Bluetongue virus: dissection of the polymerase complex. J. Gen. Virol. 89:1789-1804. http://dx.doi.org/10.1099/vir.0.2008/002089-0.
3. Ratinier M, Caporale M, Golder M, Franzoni G, Allan K, Nunes SF, Armezzani A, Bayoumy A, Rixon F, Shaw A, Palmarini M. 2011. Identification and characterization of a novel non-structural protein of bluetongue virus. PLoS Pathog. 7:e1002477. http://dx.doi.org/10.1371/journal.ppat.1002477.
4. Gouet P, Diprose JM, Grimes JM, Malby R, Burroughs JN, Zientara S, Stuart DI, Mertens PP. 1999. The highly ordered double-stranded RNA genome of bluetongue virus revealed by crystallography. Cell 97:481-490. http://dx.doi.org/10.1016/S0092-8674(00)80758-8.
5. Grimes JM, Burroughs JN, Gouet P, Diprose JM, Malby R, Zientara S, Mertens PP, Stuart DI. 1998. The atomic structure of the bluetongue virus core. Nature 395:470-478. http://dx.doi.org/10.1038/26694.
6. Roy P. 2008. Functional mapping of bluetongue virus proteins and their interactions with host proteins during virus replication. Cell Biochem. Biophys. 50:143-157. http://dx.doi.org/10.1007/s12013-008-9009-4.
7. Belhouchet M, Mohd Jaafar F, Firth AE, Grimes JM, Mertens PP, Attoui H. 2011. Detection of a fourth orbivirus non-structural protein. PLoS One 6:e25697. http://dx.doi.org/10.1371/journal.pone.0025697.
8. Kahlon J, Sugiyama K, Roy P. 1983. Molecular basis of bluetongue virus neutralization. J. Virol. 48:627-632.
9. Huismans H, Erasmus BJ. 1981. Identification of the serotype-specific and group-specific antigens of bluetongue virus. Onderstepoort J. Vet. Res. 48:51-58.
10. Hofmann MA, Renzullo S, Mader M, Chaignat V, Worwa G, Thuer B. 2008. Genetic characterization of toggenburg orbivirus, a new bluetongue virus, from goats, Switzerland. Emerg. Infect. Dis. 14:1855-1861. http://dx.doi.org/10.3201/eid1412.080818.
11. Maan S, Maan NS, Nomikou K, Veronesi E, Bachanek-Bankowska K, Belaganahalli MN, Attoui H, Mertens PP. 2011. Complete genome characterization of a novel 26th bluetongue virus serotype from Kuwait. PLoS One 6:e26147. http://dx.doi.org/10.1371/journal.pone.0026147.
12. Maan S, Maan NS, Samuel AR, Rao S, Attoui H, Mertens PP. 2007. Analysis and phylogenetic comparisons of full-length VP2 genes of the 24 bluetongue virus serotypes. J. Gen. Virol. 88:621-630. http://dx.doi.org/10.1099/vir.0.82456-0.
13. Shaw AE, Ratinier M, Nunes SF, Nomikou K, Caporale M, Golder M, Allan K, Hamers C, Hudelet P, Zientara S, Breard E, Mertens P, Palmarini M. 2013. Reassortment between two serologically unrelated bluetongue virus strains is flexible and can involve any genome segment. J. Virol. 87:543-557. http://dx.doi.org/10.1128/JVI.02266-12.
14. Purse BV, Brown HE, Harrup L, Mertens PP, Rogers DJ. 2008. Invasion of bluetongue and other orbivirus infections into Europe: the role of biological and climatic processes. Rev. Sci. Tech. 27:427-442.
15. Maclachlan NJ, Guthrie AJ. 2010. Re-emergence of bluetongue, African horse sickness, and other orbivirus diseases. Vet. Res. 41:35. http://dx.doi.org/10.1051/vetres/2010007.
16. Wilson A, Carpenter S, Gloster J, Mellor P. 2007. Re-emergence of bluetongue in northern Europe in 2007. Vet. Rec. 161:487-489. http://dx.doi.org/10.1136/vr.161.14.487.
17. Guis H, Caminade C, Calvete C, Morse AP, Tran A, Baylis M. 2012. Modelling the effects of past and future climate on the risk of bluetongue emergence in Europe. J. R. Soc. Interface 9:339-350. http://dx.doi.org/10.1098/rsif.2011.0255.
18. Mehlhorn H, Walldorf V, Klimpel S, Jahn B, Jaeger F, Eschweiler J, Hoffmann B, Beer M. 2007. First occurrence of Culicoides obsoletustransmitted bluetongue virus epidemic in Central Europe. Parasitol. Res. 101:219-228. http://dx.doi.org/10.1007/s00436-007-0519-6.
19. Spreull J. 1905. Malarial catharral fever (bluetongue) of sheep in South Africa. J. Comp. Path. Ther. 18:321-337. http://dx.doi.org/10.1016/S0368-1742(05)80073-6.
20. MacLachlan NJ, Crafford JE, Vernau W, Gardner IA, Goddard A, Guthrie AJ, Venter EH. 2008. Experimental reproduction of severe bluetongue in sheep. Vet. Pathol. 45:310-315. http://dx.doi.org/10.1354/vp.45-3-310.
21. Maclachlan NJ, Drew CP, Darpel KE, Worwa G. 2009. The pathology and pathogenesis of bluetongue. J. Comp. Pathol. 141:1-16. http://dx.doi.org/10.1016/j.jcpa.2009.04.003.
22. Gibbs EP, Greiner EC. 1994. The epidemiology of bluetongue. Comp. Immunol. Microbiol. Infect. Dis. 17:207-220. http://dx.doi.org/10.1016/0147-9571(94)90044-2.
23. Parsonson IM. 1990. Pathology and pathogenesis of bluetongue infections. Curr. Top. Microbiol. Immunol. 162:119-141.
24. Erasmus BJ. 1975. Bluetongue in sheep and goats. Aust. Vet. J. 51:165. http://dx.doi.org/10.1111/j.1751-0813.1975.tb00048.x.
25. Henrich M, Reinacher M, Hamann HP. 2007. Lethal bluetongue virus infection in an alpaca. Vet. Rec. 161:764. http://dx.doi.org/10.1136/vr.161.22.764.
26. Mauroy A, Guyot H, De Clercq K, Cassart D, Thiry E, Saegerman C. 2008. Bluetongue in captive yaks. Emerg. Infect. Dis. 14:675-676. http://dx.doi.org/10.3201/eid1404.071416.
27. Barratt-Boyes SM, MacLachlan NJ. 1994. Dynamics of viral spread in bluetongue virus infected calves. Vet. Microbiol. 40:361-371. http://dx.doi.org/10.1016/0378-1135(94)90123-6.
28. Barratt-Boyes SM, MacLachlan NJ. 1995. Pathogenesis of bluetongue virus infection of cattle. J. Am. Vet. Med. Assoc. 206:1322-1329.
29. Falconi C, Lopez-Olvera JR, Gortazar C. 2011. BTV infection in wild ruminants, with emphasis on red deer: a review. Vet. Microbiol. 151:209. http://dx.doi.org/10.1016/j.vetmic.2011.02.011.
30. Meyer G, Lacroux C, Leger S, Top S, Goyeau K, Deplanche M, Lemaire M. 2009. Lethal bluetongue virus serotype 1 infection in llamas. Emerg. Infect. Dis. 15:608-610. http://dx.doi.org/10.3201/eid1504.081514.
31. Darpel KE, Batten CA, Veronesi E, Shaw AE, Anthony S, Bachanek-Bankowska K, Kgosana L, Abin-Tarif Carpenter S, Muller-Doblies UU, Takamatsu HH, Mellor PS, Mertens PP, Oura CA. 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. http://dx.doi.org/10.1136/vr.161.8.253.
32. Koumbati M, Mangana O, Nomikou K, Mellor PS, Papadopoulos O. 1999. Duration of bluetongue viraemia and serological responses in experimentally infected European breeds of sheep and goats. Vet. Microbiol. 64:277-285. http://dx.doi.org/10.1016/S0378-1135(98)00255-7.
33. Luedke AJ, Anakwenze EI. 1972. Bluetongue virus in goats. Am. J. Vet. Res. 33:1739-1745.
34. Backx A, Heutink CG, van Rooij EM, van Rijn PA. 2007. Clinical signs of bluetongue virus serotype 8 infection in sheep and goats. Vet. Rec. 161:591-592. http://dx.doi.org/10.1136/vr.161.17.591.
35. Dercksen D, Groot Nibbelink N, Paauwe R, Backx A, van Rijn P, Vellema P. 2007. First outbreak of bluetongue in goats in The Netherlands. Tijdschr. Diergeneeskd. 132:786-790.
36. Coetzee P, Stokstad M, Myrmel M, Mutowembwa P, Loken T, Venter EH, Van Vuuren M. 2013. Transplacental infection in goats experimentally infected with a European strain of bluetongue virus serotype 8. Vet. J. 197:335-341. http://dx.doi.org/10.1016/j.tvjl.2013.01.005.
37. Schwartz-Cornil I, Mertens PP, Contreras V, Hemati B, Pascale F, Breard E, Mellor PS, MacLachlan NJ, Zientara S. 2008. Bluetongue virus: virology, pathogenesis and immunity. Vet. Res. 39:46. http://dx.doi.org/10.1051/vetres:2008023.
38. Neitz WO, Riemerschmid G. 1944. The influence of sunlight on the course of bluetongue. Onderterpoort J. Vet. Sci. Anim. Industry 19:69-70.
39. Verwoerd DW, Erasmus BJ. 2004. Bluetongue, p 1201-1220. In Coetzer J, Tustin R (ed), Infectious diseases of livestock, 2nd ed. Oxford Press, Cape Town, South Africa.
40. Jeggo MJ, Corteyn AH, Taylor WP, Davidson WL, Gorman BM. 1987. Virulence of bluetongue virus for British sheep. Res. Vet. Sci. 42:24-28.
41. Worwa G, Hilbe M, Chaignat V, Hofmann MA, Griot C, Ehrensperger F, Doherr MG, Thur B. 2010. Virological and pathological findings in bluetongue virus serotype 8 infected sheep. Vet. Microbiol. 144:264-273. http://dx.doi.org/10.1016/j.vetmic.2010.01.011.
42. Veronesi E, Hamblin C, Mellor PS. 2005. Live attenuated bluetongue vaccine viruses in Dorset poll sheep, before and after passage in vector midges (Diptera: Ceratopogonidae). Vaccine 23:5509-5516. http://dx.doi.org/10.1016/j.vaccine.2005.07.039.
43. Veronesi E, Darpel KE, Hamblin C, Carpenter S, Takamatsu HH, Anthony SJ, Elliott H, Mertens PP, Mellor PS. 2010. Viraemia and clinical disease in Dorset poll sheep following vaccination with live attenuated bluetongue virus vaccines serotypes 16 and 4. Vaccine 28:1397-1403. http://dx.doi.org/10.1016/j.vaccine.2009.10.107.
44. Daniels PW, Sendow I, Pritchard LI, Sukarsih Eaton BT. 2004. Regional overview of bluetongue viruses in South-East Asia: viruses, vectors and surveillance. Vet. Ital. 40:94-100.
45. Davies FG, Walker AR. 1974. The distribution in Kenya of bluetongue virus and antibody, and the Culicoides vector. J. Hyg. (Lond.) 72:265-272. http://dx.doi.org/10.1017/S0022172400023470.
46. Howell PG, Verwoerd DW. 1971. Bluetongue virus. Virol. Monogr. 9:35-74.
47. Chessa B, Pereira F, Arnaud F, Amorim A, Goyache F, Mainland I, Kao RR, Pemberton JM, Beraldi D, Stear MJ, Alberti A, Pittau M, Iannuzzi L, Banabazi MH, Kazwala RR, Zhang YP, Arranz JJ, Ali BA, Wang Z, Uzun M, Dione MM, Olsaker I, Holm LE, Saarma U, Ahmad S, Marzanov N, Eythorsdottir E, Holland MJ, Ajmone-Marsan P, Bruford MW, Kantanen J, Spencer TE, Palmarini M. 2009. Revealing the history of sheep domestication using retrovirus integrations. Science 324:532. http://dx.doi.org/10.1126/science.1170587.
48. Elbers AR, Backx A, Meroc E, Gerbier G, Staubach C, Hendrickx G, van der Spek A, Mintiens K. 2008. Field observations during the bluetongue serotype 8 epidemic in 2006. I. Detection of first outbreaks and clinical signs in sheep and cattle in Belgium, France and the Netherlands. Prev. Vet. Med. 87:21-30. http://dx.doi.org/10.1016/j.prevetmed.2008.06.004.
49. Elbers AR, Backx A, Mintiens K, Gerbier G, Staubach C, Hendrickx G, van der Spek A. 2008. Field observations during the bluetongue serotype 8 epidemic in 2006. II. Morbidity and mortality rate, case fatality and clinical recovery in sheep and cattle in the Netherlands. Prev. Vet. Med. 87:31-40. http://dx.doi.org/10.1016/j.prevetmed.2008.06.003.
50. Perrin JB, Ducrot C, Vinard JL, Morignat E, Gauffier A, Calavas D, Hendrikx P. 2010. Using the National Cattle Register to estimate the excess mortality during an epidemic: application to an outbreak of bluetongue serotype 8. Epidemics 2:207-214. http://dx.doi.org/10.1016/j.epidem.2010.10.002.
51. Meroc E, Herr C, Verheyden B, Hooyberghs J, Houdart P, Raemaekers M, Vandenbussche F, De Clercq K, Mintiens K. 2009. Bluetongue in Belgium: episode II. Transbound. Emerg. Dis. 56:39-48. http://dx.doi.org/10.1111/j.1865-1682.2008.01063.x.
52. Maan S, Maan NS, van Rijn PA, van Gennip RG, Sanders A, Wright IM, Batten C, Hoffmann B, Eschbaumer M, Oura CA, Potgieter AC, Nomikou K, Mertens PP. 2010. Full genome characterisation of bluetongue virus serotype 6 from the Netherlands 2008 and comparison to other field and vaccine strains. PLoS One 5:e10323. http://dx.doi.org/10.1371/journal.pone.0010323.
53. van Rijn PA, Geurts Y, van der Spek AN, Veldman D, van Gennip RG. 2012. Bluetongue virus serotype 6 in Europe in 2008-emergence and disappearance of an unexpected non-virulent BTV. Vet. Microbiol. 158: 23-32. http://dx.doi.org/10.1016/j.vetmic.2012.01.022.
54. De Clercq K, Mertens P, De Leeuw I, Oura C, Houdart P, Potgieter AC, Maan S, Hooyberghs J, Batten C, Vandemeulebroucke E, Wright IM, Maan N, Riocreux F, Sanders A, Vanderstede Y, Nomikou K, Raemaekers M, Bin-Tarif A, Shaw A, Henstock M, Breard E, Dubois E, Gastaldi-Thiery C, Zientara S, Verheyden B, Vandenbussche F. 2009. Emergence of bluetongue serotypes in Europe, part 2: the occurrence of a BTV-11 strain in Belgium. Transbound. Emerg. Dis. 56:355-361. http://dx.doi.org/10.1111/j.1865-1682.2009.01092.x.
55. Coetzee P, van Vuuren M, Venter EH, Stokstad M. 2014. A review of experimental infections with bluetongue virus in the mammalian host. Virus Res. 182:21-34. http://dx.doi.org/10.1016/j.virusres.2013.12.044.
56. Umeshappa CS, Singh KP, Channappanavar R, Sharma K, Nanjundappa RH, Saxena M, Singh R, Sharma AK. 2011. A comparison of intradermal and intravenous inoculation of bluetongue virus serotype 23 in sheep for clinico-pathology, and viral and immune responses. Vet. Immunol. Immunopathol. 141:230-238. http://dx.doi.org/10.1016/j.vetimm.2011.03.005.
57. Caporale M, Wash R, Pini A, Savini G, Franchi P, Golder M, Patterson-Kane J, Mertens P, Di Gialleonardo L, Armillotta G, Lelli R, Kellam P, Palmarini M. 2011. Determinants of bluetongue virus virulence in murine models of disease. J. Virol. 85:11479-11489. http://dx.doi.org/10.1128/JVI.05226-11.
58. Moulin V, Noordegraaf CV, Makoschey B, van der Sluijs M, Veronesi E, Darpel K, Mertens PP, de Smit H. 2012. Clinical disease in sheep caused by bluetongue virus serotype 8, and prevention by an inactivated vaccine. Vaccine 30:2228-2235. http://dx.doi.org/10.1016/j.vaccine.2011.11.100.
59. Bonneau KR, DeMaula CD, Mullens BA, MacLachlan NJ. 2002. Duration of viraemia infectious to Culicoides sonorensis in bluetongue virusinfected cattle and sheep. Vet. Microbiol. 88:115-125. http://dx.doi.org/10.1016/S0378-1135(02)00106-2.
60. DeMaula CD, Leutenegger CM, Jutila MA, MacLachlan NJ. 2002. Bluetongue virus-induced activation of primary bovine lung microvascular endothelial cells. Vet. Immunol. Immunopathol. 86:147-157. http://dx.doi.org/10.1016/S0165-2427(02)00012-0.
61. Eschbaumer M, Wackerlin R, Rudolf M, Keller M, Konig P, Zemke J, Hoffmann B, Beer M. 2010. Infectious blood or culture-grown virus: a comparison of bluetongue virus challenge models. Vet. Microbiol. 146: 150-154. http://dx.doi.org/10.1016/j.vetmic.2010.05.004.
62. Hamers C, Galleau S, Chery R, Blanchet M, Besancon L, Cariou C, Werle-Lapostolle B, Hudelet P, Goutebroze S. 2009. Use of inactivated bluetongue virus serotype 8 vaccine against virulent challenge in sheep and cattle. Vet. Rec. 165:369-373. http://dx.doi.org/10.1136/vr.165.13.369.
63. Escarmis C, Lazaro E, Manrubia SC. 2006. Population bottlenecks in quasispecies dynamics. Curr. Top. Microbiol. Immunol. 299:141-170.
64. Arnaud F, Black SG, Murphy L, Griffiths DJ, Neil SJ, Spencer TE, Palmarini M. 2010. Interplay between ovine bone marrow stromal cell antigen 2/tetherin and endogenous retroviruses. J. Virol. 84:4415-4425. http://dx.doi.org/10.1128/JVI.00029-10.
65. 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. http://dx.doi.org/10.1016/0022-2011(89)90123-7.
66. van Gennip RG, van de Water SG, Maris-Veldhuis M, van Rijn PA. 2012. Bluetongue viruses based on modified-live vaccine serotype 6 with exchanged outer shell proteins confer full protection in sheep against virulent BTV8. PLoS One 7:e44619. http://dx.doi.org/10.1371/journal.pone.0044619.
67. Dulbecco R, Vogt M. 1953. Some problems of animal virology as studied by the plaque technique. Cold Spring Harb. Symp. Quant. Biol. 18:273. http://dx.doi.org/10.1101/SQB.1953.018.01.039.
68. Lelli R, Di Ventura M, Mercante MT, Tittarelli M, Mangana-Vougiouka O, Nomikou K, Conte A, Di Emidio B, Portanti O, Giovannucci G, Bonfini B, Zaghini M, Caporale V. 2004. Bluetongue laboratory diagnosis: a ring test to evaluate serological results using a competitive ELISA kit. Vet. Ital. 40:577-580.
69. Polci A, Camma C, Serini S, Di Gialleonardo L, Monaco F, Savini G. 2007. Real-time polymerase chain reaction to detect bluetongue virus in blood samples. Vet. Ital. 43:77-88.
70. Reed LJ, Muench HA. 1938. A simple method for estimating fifty percent endpoints. Am. J. Hygiene 27:493-497.
71. Toussaint JF, Sailleau C, Breard E, Zientara S, De Clercq K. 2007. Bluetongue virus detection by two real-time RT-qPCRs targeting two different genomic segments. J. Virol. Methods 140:115-123. http://dx.doi.org/10.1016/j.jviromet.2006.11.007.
72. Calvo-Pinilla E, Rodriguez-Calvo T, Anguita J, Sevilla N, Ortego J. 2009. Establishment of a bluetongue virus infection model in mice that are deficient in the alpha/beta interferon receptor. PLoS One 4:e5171. http://dx.doi.org/10.1371/journal.pone.0005171.
73. Coetzee P, Van Vuuren M, Stokstad M, Myrmel M, Venter EH. 2012. Bluetongue virus genetic and phenotypic diversity: towards identifying the molecular determinants that influence virulence and transmission potential. Vet. Microbiol. 161:1-12. http://dx.doi.org/10.1016/j.vetmic.2012.07.007.
74. Borderia AV, Stapleford KA, Vignuzzi M. 2011. RNA virus population diversity: implications for inter-species transmission. Curr. Opin. Virol. 1:643-648. http://dx.doi.org/10.1016/j.coviro.2011.09.012.
75. Biebricher CK, Eigen M. 2006. What is a quasispecies? Curr. Top. Microbiol. Immunol. 299:1-31.
76. Suarez DL. 2010. Avian influenza: our current understanding. Anim. Health Res. Rev. 11:19-33. http://dx.doi.org/10.1017/S1466252310000095.
77. Verwoerd DW. 2012. History of orbivirus research in South Africa. J. S. Afr. Vet. Assoc. 83:532. http://dx.doi.org/10.4102/jsava.v83i1.532.
78. Sanchez-Cordon PJ, Pleguezuelos FJ, Perez de Diego AC, Gomez-Villamandos JC, Sanchez-Vizcaino JM, Ceron JJ, Tecles F, Garfia B, Pedrera M. 2013. Comparative study of clinical courses, gross lesions, acute phase response and coagulation disorders in sheep inoculated with bluetongue virus serotype 1 and 8. Vet. Microbiol. 166:184-194. http://dx.doi.org/10.1016/j.vetmic.2013.05.032.
79. Lauring AS, Frydman J, Andino R. 2013. The role of mutational robustness in RNA virus evolution. Nat. Rev. Microbiol. 11:327-336. http://dx.doi.org/10.1038/nrmicro3003.
80. Jamburuthugoda VK, Eickbush TH. 2011. The reverse transcriptase encoded by the non-LTR retrotransposon R2 is as error-prone as that encoded by HIV-1. J. Mol. Biol. 407:661-672. http://dx.doi.org/10.1016/j.jmb.2011.02.015.
81. Vignuzzi M, Stone JK, Arnold JJ, Cameron CE, Andino R. 2006. Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439:344-348. http://dx.doi.org/10.1038/nature04388.
82. Pfeiffer JK, Kirkegaard K. 2005. Increased fidelity reduces poliovirus fitness and virulence under selective pressure in mice. PLoS Pathog. 1:e11. http://dx.doi.org/10.1371/journal.ppat.0010011.
83. Meng T, Kwang J. 2014. Attenuation of human enterovirus 71 highreplication-fidelity variants in AG129 mice. J. Virol. 88:5803-5815. http://dx.doi.org/10.1128/JVI.00289-14.
84. Gould AR, Eaton BT. 1990. The amino acid sequence of the outer coat protein VP2 of neutralizing monoclonal antibody-resistant, virulent and attenuated bluetongue viruses. Virus Res. 17:161-172. http://dx.doi.org/10.1016/0168-1702(90)90062-G.
85. Bonneau KR, Mullens BA, MacLachlan NJ. 2001. Occurrence of genetic drift and founder effect during quasispecies evolution of the VP2 and NS3/NS3A genes of bluetongue virus upon passage between sheep, cattle, and Culicoides sonorensis. J. Virol. 75:8298-8305. http://dx.doi.org/10.1128/JVI.75.17.8298-8305.2001.
86. Pages N, Breard E, Urien C, Talavera S, Viarouge C, Lorca-Oro C, Jouneau L, Charley B, Zientara S, Bensaid A, Solanes D, Pujols J, Schwartz-Cornil I. 2014. Culicoides midge bites modulate the host response and impact on bluetongue virus infection in sheep. PLoS One 9:e83683. http://dx.doi.org/10.1371/journal.pone.0083683.