Summary
Cattle are proposed to be reservoir hosts of bluetongue virus (BTV) because infected animals typically have a prolonged cell-associated viremia. Enriched populations of bovine monocytes, erythrocytes and lymphocytes were inoculated with BTV serotype 10 (BTV 10) and the infected cells then were examined by transmission electron microscopy to characterize the interaction of BTV with bovine blood cells. Replication of BTV 10 in monocytes and stimulated (replicating) lymphocytes was morphologically similar to that which occured in Vero cells, with formation of viral inclusion bodies and virus-specific tubules. In contrast, BTV 10 infection of unstimulated (non-replicating) lymphocytes and erythrocytes did not progress beyond adsorption, after which virus particles persisted in invaginations of the cell membrane. Studies with core particles and neutralizing monoclonal antibodies established that outer capsid protein VP2 is necessary for attachment of BTV 10 to erythrocytes. These in vitro virus-cell interactions provide a cogent explanation for the pathogenesis of BTV infection of cattle, especially the prolonged cell associated viremia that occurs in BTV-infected cattle.
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Barratt-Boyes SM, Rossitto PV, Stott JL, MacLachlan NJ (1992) Flow cytometric analysis of in-vitro bluetongue virus infection of bovine blood mononuclear cells. J Gen Virol 73: 1953–1960
Barratt-Boyes SM, MacLachlan NJ (1994) Dynamics of viral spread in bluetongue virus infected calves. Vet Microbiol (in press)
Bowne JG (1971) Bluetongue disease. Adv Vet Sci Comp Med 15: 1–46
Brewer AW, MacLachlan NJ (1992) Ultrastructural characterization of the interaction of bluetongue virus with bovine erythrocytes in-vitro. Vet Pathol 29: 356–359
Cheville NF (1983) Cell pathology. The lowa State University Press, Ames
Cowley JA, Gorman BM (1987) Genetic reassortants for identification of the genome segment coding for the bluetongue virus hemagglutinin. J Virol 61: 2304–2306
Cromack AS, Blue JL, Gratzek JB (1971) A quantitative ultrastructural study of the development of bluetongue virus in Madin-Darby bovine kidney cells. J Gen Virol 13: 229–224
Dangler CA, de la Concha-Bermejillo A, Stott JL, Osburn BI (1990) Limitations of in situ hybridization for the detection of bluetongue virus in blood mononuclear cells. J Vet Diagn Invest 2: 303–307
de la Concha-Bermejillo A, Schore CE, Dangler CA, de Mattos CC, de Mattos CA, Osburn BI (1992) Comparison of slot blot nucleic acid hybridization, immunofluorescence, and virus isolation techniques to detect bluetongue virus in blood mononuclear cells from cattle with experimentally induced infection. Am J Vet Res 53: 2245–2250
de la Concha-Bermejillo A, Odeon A, BonDurant RH, Osburn BI (1993) Experimental infection of pregnant cattle with bluetongue virus serotype 11 between postbreeding days 21 and 48. J Vet Diagn Invest 5: 329–335
DeMaula CD, Heidner HW, Rossitto PV, Pierce CM, MacLachlan NJ (1993) Neutralization determinants of United States bluetongue virus serotype 10. Virology 195: 292–296
Du Toit RM (1962) The role played by bovines in the transmission of bluetongue of sheep. J S Afr Vet Med Assoc 33: 483–490
Eaton BT, Crameri GS (1989) The site of bluetongue virus attachment to glycophorins from a number of animal erythrocytes. J Gen Virol 70: 3347–3353
Eaton BT, Hyatt AD, Brookes SM (1990) The replication of bluetongue viruses. Curr Topics Microbiol Immunol 162: 89–118
Ellis JA, Coen ML, MacLachlan NJ, Wilson WC, Williams ES, Luedke AJ (1993) Low prevalence of bluetongue virus expression in leukocytes from experimentally infected ruminants. Am J Vet Res 54: 1452–1456
Emmons RW, Oshiro LS, Johnson HN, Lennette EH (1972) Intraerythrocytic location of Colorado tick fever virus. J Gen Virol 17: 185–195
Heidner HW, MacLachlan NJ, Fuller FJ, Richards RG (1988) Bluetongue virus genome remains stable during prolonged infection of cattle. J Gen Virol 69: 2629–2636
Huismans H, Van der Walt NT, Cloete M, Erasmus BJ (1983) The biochemical and immunological characterization of bluetongue virus outer capsid polypeptides. In: Compans RW, Bishop DHL (eds) Double stranded RNA viruses. Elsevier, New York, pp 165–172
Jain NC (1986) The erythrocyte: its morphology, metabolism, and survival. In: Jain NC (ed) Veterinary hematology, 4th edn. Lea & Febiger, Philadelphia, pp 527–562
Lecatsas G (1968) Electron microscopic study of the formation of bluetongue virus. Onderstepoort J Vet Res 35: 139–149
Luedke AJ (1970) Distribution of virus in blood components during viremia of bluetongue. Proc US Anim Health Assoc 74: 9–21
MacLachlan NJ, Thompson J (1985) Bluetongue virus-induced interferon in cattle. Am J Vet Res 46: 1238–1241
MacLachlan NJ, Fuller FJ (1986) Genetic stability in calves of a single strain of bluetongue virus. Am J Vet Res 47: 762–764
MacLachlan NJ, Heidner HW, Fuller FJ (1987) Humoral immune response of calves to bluetongue virus infection. Am J Vet Res 48: 1031–1035
MacLachlan NJ, Jagels G, Rossitto PV, Moore PF, Heidner HW (1990) The pathogenesis of experimental bluetongue virus infection of calves. Vet Pathol 27: 223–229
MacLachlan NJ, Barratt-Boyes SM, Brewer AW, Stott JL (1992) Bluetongue virus infection of cattle. In: Walton TE, Osburn BI (eds) Bluetongue, African horse sickness, and related orbiviruses. CRC Press, Boca Raton, pp 527–536
MacLachlan NJ, Nunamaker RA, Katz JB, Sawyer MM, Akita GY, Osburn BI, Tabachnick WS (1994) Detection of bluetongue virus in the blood of inoculated calves: Comparison of virus isolation, PCR assay, and in-vitro feeding ofCulicoides variipennis. Arch Virol 136: 1–8
Mertens PPC, Burroughs JN, Anderson J (1987) Purification and properties of virus particles, infectious subviral particles, and cores of bluetongue virus serotypes 1 and 4. Virology 157: 375–386
Morrill JC, MacConnell S (1985) An electron microscopic study of blood cells from calves experimentally infected with bluetongue virus. In: Barber TL, Jochim MM (eds) Bluetongue and related orbiviruses. Alan Liss, New York, pp 279–287
Nevill EM (1971) Cattle and Culicoides biting midges as possible overwintering hosts of bluetongue virus. Onderstepoort J Vet Res 38: 65–72
Richards RG, MacLachlan NJ, Heidner HW, Fuller FJ (1988) Comparison of the virologic and serologic responses of lambs and calves infected with bluetongue virus serotype 10. Vet Microbiol 18: 233–242
Spreull J (1905) Malarial catarrhal fever (bluetongue) of sheep in South Africa. J Comp Pathol Therap 18: 233–242
Stott JL, Blanchard-Channell M, Scibienski RJ, Stott ML (1990) Interaction of bluetongue virus with bovine lymphocytes. J Gen Virol 71: 363–368
Verwoerd DW (1969) Purification and characterization of bluetongue virus. Virology 38: 203–212
Whetter LE, MacLachlan NJ, Gebhard DH, Heidner HW, Moore PF (1989) Bluetongue virus infection of bovine monocytes. J Gen Virol 70: 1663–1676
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Brewer, A.W., MacLachlan, N.J. The pathogenesis of bluetongue virus infection of bovine blood cells in vitro: ultrastructural characterization. Archives of Virology 136, 287–298 (1994). https://doi.org/10.1007/BF01321058
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DOI: https://doi.org/10.1007/BF01321058