[en] Bovine herpesvirus 4 (BoHV-4) has been isolated from cattle throughout the world, but virological and serological studies have suggested that the African buffalo is also a natural host for this virus. It has previously been found that the Bo17 gene of BoHV-4 was acquired from an ancestor of the African buffalo, probably around 1.5 million years ago. Analysis of the variation of the Bo17 gene sequence among BoHV-4 strains suggested a relatively ancient transmission of BoHV-4 from the buffalo to the Bos primigenius lineage, followed by a host-dependent split between zebu and taurine BoHV-4 strains. In the present study, the evolutionary history of BoHV-4 was investigated by analysis of five gene sequences from each of nine strains representative of the viral species: three isolated from African buffalo in Kenya and six from cattle from Europe, North America and India. No two gene sequences had the same evolutionary tree, indicating that recombination has occurred between divergent lineages; six recombination events were delineated for these sequences. Nevertheless, exchange has been infrequent enough that a clonal evolutionary history of the strains could be discerned, upon which the recombination events were superimposed. The dates of divergence among BoHV-4 lineages were estimated from synonymous nucleotide-substitution rates. The inferred evolutionary history suggests that African buffalo were the original natural reservoir of BoHV-4 and that there have been at least three independent transmissions from buffalo to cattle, probably via intermediate hosts and - at least in the case of North American strains - within the last 500 years.
Bartha, A., Juhasz, M. & Liebermann, H. (1966). Isolation of a bovine herpesvirus from calves with respiratory disease and keratoconjunctivitis. A preliminary report. Acta Vet Acad Sci Hung 16, 357-358.
Borchers, K., Brackmann, J., Wolf, O., Rudolph, M., Glatzel, P., Krasinska, M., Krasinski, Z. A. & Frölich, K. (2002). Virologic investigations of free-living European bison (Bison bonasus) from the Bialowieza Primeval Forest, Poland. J Wildl Dis 38, 533-538.
Bradley, D. G., MacHugh, D. E., Cunningham, P. & Loftus, R. T. (1996). Mitochondrial diversity and the origins of African and European cattle. Proc Natl Acad Sci U S A 93, 5131-5135.
Bublot M., Van Bressem, M.-F., Thiry, E., Dubuisson, J. & Pastoret, P.-P. (1990). Bovine herpesvirus 4 genome: cloning, mapping and strain variation analysis. J Gen Virol 71, 133-142.
Bublot M., Wellemans, G., Van Bressem, M.-F., Dubuisson, J., Pastoret, P.-P. & Thiry, E. (1991). Genomic diversity among bovine herpesvirus 4 field isolates. Arch Virol 116, 1-18.
Burrows, J. M., Khanna, R., Sculley, T. B., Alpers, M. P., Moss, D. J. & Burrows, S. R. (1996). Identification of a naturally occurring recombinant Epstein-Barr virus isolate from New Guinea that encodes both type 1 and type 2 nuclear antigen sequences. J Virol 70, 4829-4833.
Davison, A. J. (2002). Evolution of the herpesviruses. Vet Microbiol 86, 69-88.
Dewals, B., Gillet L., Gerdes, T., Taracha, E. L. N., Thiry, E. & Vanderplasschen, A. (2005). Antibodies against bovine herpesvirus 4 are highly prevalent in wild African buffaloes throughout eastern and southern Africa. Vet Microbiol 110, 209-220.
Gillet, L., Minner, F., Detry, B. & 7 other authors (2004). Investigation of the susceptibility of human cell lines to bovine herpesvirus 4 infection: demonstration that human cells can support a non-permissive persistent infection which protects them against tumor necrosis factor alpha-induced apoptosis. J Virol 78, 2336-2347.
Hatwell, J. N. & Sharp, P. M. (2000). Evolution of human polyomavirus JC. J Gen Virol 81, 1191-1200.
Henry, B. E., II, Ota, R. & Evermann, J. F. (1986). Genetic relatedness of disease-associated field isolates of bovid herpesvirus type 4. Am J Vet Res 47, 2242-2246.
Hughes, A. L. (2002). Origin and evolution of viral interleukin-10 and other DNA virus genes with vertebrate homologues. J Mol Evol 54, 90-101.
Li, W. H. (1993). Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J Mol Evol 36, 96-99.
Li, H., Gailbreath, K., Flach, E. J. & 9 other authors (2005). A novel subgroup of rhadinoviruses in ruminants. J Gen Virol 86, 3021-3026.
Mack, R. (1970). The great African cattle plague epidemic of the 1890s. Trop Anim Health Prod 2, 210-219.
Markine-Goriaynoff, N., Georgin, J.-P., Goltz, M., Zimmermann, W., Broll, H., Wamwayi, H. M., Pastoret P.-P., Sharp, P. M. & Vanderplasschen, A. (2003a). The core 2 β-1,6-N-acetylglucosaminyltransferase-mucin encoded by bovine herpesvirus 4 was acquired from an ancestor of the African buffalo. J Virol 77, 1784-1792.
Markine-Gorlaynoff, N., Minner, F., de Fays, K., Gillet L., Thiry, E., Pastoret, P. P. & Vanderplasschen, A. (2003b). L'herpèsvirus bovin 4. Ann Méd Vét 147, 215-247 (in French).
McGeoch, D. J. (2001). Molecular evolution of the y-Herpesvirinae. Philos Trans R Soc Lond B Biol Sci 356, 421-435.
McGeoch, D. J., Cook, S., Dolan, A., Jamieson, F. E. & Telford, E. A. R. (1995). Molecular phylogeny and evolutionary timescale for the family of mammalian herpesviruses. J Mol Biol 247, 443-458.
Mohanty, S. B., Hammond, R. C. & Lillie, M. G. (1971). A new bovine herpesvirus and its effect on experimentally infected calves. Brief report. Arch Gesamte Virusforsch 33, 394-395.
Moreno-Lopez, J., Goltz, M., Rehbinder, C., Valsala, K. V. & Ludwig, H. (1989). A bovine herpesvirus (BHV-4) as passenger virus in ethmoidal tumours in Indian cattle. Zentralbl Veterinarmed B 36, 481-486.
Norberg, P., Bergström, T., Rekabdar, E., Lindh, M. & Liljeqvist, J.-Å. (2004). Phylogenetic analysis of clinical herpes simplex virus type 1 isolates identified three genetic groups and recombinant viruses. J Virol 78, 10755-10764.
Poole, L. J., Zong, J.-C., Ciufo, D. M., Alcendor, D. J., Cannon, J. S., Ambinder, R., Orenstein, J. M., Reitz, M. S. & Hayward, G. S. (1999). Comparison of genetic variability at multiple loci across the genomes of the major subtypes of Kaposi's sarcoma-associated herpesvirus reveals evidence for recombination and for two distinct types of open reading frame K15 alleles at the right-hand end. J Virol 73, 6646-6660.
Rossiter, P. B., Gumm, I. D., Stagg, D. A., Conrad, P. A., Mukolwe, S., Davies, F. G. & White, H. (1989). Isolation of bovine herpesvirus-3 from African buffaloes (Syncerus caffer). Res Vet Sci 46, 337-343.
Saitou, N. & Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406-425.
Shackelton, L. A. & Holmes, E. C. (2004). The evolution of large DNA viruses: combining genomic information of viruses and their hosts. Trends Microbiol 12, 458-465.
Shapiro, B., Drummond, A. J., Rambaut, A. & 24 other authors (2004). Rise and fall of the Beringian steppe bison. Science 306, 1561-1565.
Sharp, P. M. (2002). Origins of human virus diversity. Cell 108, 305-312.
Shen, D. T., Burger, D., Tong, G. Z. & Gorham, J. R. (1992). Molecular cloning and physical mapping of bovine herpesvirus 4 strain DN 599 and comparison with two American field-isolates. Arch Virol 127, 75-87.
Simonsen, B. T., Siegismund, H. R. & Arctander, P. (1998). Population structure of African buffalo inferred from mtDNA sequences and microsatellite loci: high variation but low differentiation. Mol Ecol 7, 225-237.
Storz, J. (1968). Comments on malignant catarrhal fever. J Am Vet Med Assoc 152, 804-806.
Thiry, E., Pastoret, P.-P., Dessy-Doize, C., Hanzen, C., Calberg-Bacq, C. M. & other authors (1981). Reactivation of a herpesvirus in cells cultured from a testicle of a bull showing orchitis and azoospermia. Ann Méd Vét 125, 207-214 (in French).
Thiry, E., Bublot, M., Dubuisson, J., Van Bressem, M.-F., Lequarre, A.-S., Lomonte, P., Vanderplasschen, A. & Pastoret, P.-P. (1992). Molecular biology of bovine herpesvirus type 4. Vet Microbiol 33, 79-92.
Thiry, E., Meurens, F., Muylkens, B. & 7 other authors (2005). Recombination in alphaherpesviruses. Rev Med Virol 15, 89-103.
Thompson, J. D., Higgins, D. G. & Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673-4680.
Todd, W. J. & Storz, J. (1983). Morphogenesis of a cytomegalovirus; from an American bison affected with malignant catarrhal fever. J Gen Virol 64, 1025-1030.
Troy, C. S., MacHugh, D. E., Bailey, J. F., Magee, D. A., Loftus, R. T., Cunningham, P., Chamberlain, A. T., Sykes, B. C. & Bradley, D. G. (2001). Genetic evidence for Near-Eastern origins of European cattle. Nature 410, 1088-1091.
Vanderplasschen, A., Markine-Goriaynoff, N., Lomonte, P. & 8 other authors (2000). A multipotential β-1,6-N-acetylglucosaminyl-transferase is encoded by bovine herpesvirus type 4. Proc Natl Acad Sci U S A 97, 5756-5761.
Van Hooft, W. F., Groen, A. F. & Prins, H. H. T. (2002). Phylo-geography of the African buffalo based on mitochondrial and Y-chromosomal loci: Pleistocene origin and population expansion of the Cape buffalo subspecies. Mol Ecol 11, 267-279.
Van Opdenbosch, E., Wellemans, G. & Oudewater, J. (1986). Toevallige isolatie van het boviene herpesvirus 4 uit de long van een schaap. Vlaams Diergeneesk Tijdschr 55, 432 (in Dutch).
Walling, D. M. & Raab-Traub, N. (1994). Epstein-Barr virus intra-strain recombination in oral hairy leukoplakia. J Virol 68, 7909-7917.
Wellemans, G., Antoine, H., Broes, A., Charlier, G. & Van Opdenbosch, E. (1983). Isolation of a herpesvirus from cows affected with post partural metritis. Ann Méd Vét 127, 481-482 (in French).
Wellenberg, G. J., van Rooij, E. M. A., Maissan, J. & Van Oirschot, J. T. (1999). Evaluation of newly developed immunoperoxidase monolayer assays for detection of antibodies against bovine herpesvirus 4. Clin Diagn Lab Immunol 6, 447-451.
Wenink, P. W., Groen, A. F., Roelke-Parker, M. E. & Prins, H. H. T. (1998). African buffalo maintain high genetic diversity in the major histocompatibility complex in spite of historically known population bottlenecks. Mol Ecol 7, 1315-1322.
Zimmermann, W., Broll, H., Ehlers, B., Buhk, H.-J., Rosenthal, A. & Goltz, M. (2001). Genome sequence of bovine herpesvirus 4, a bovine Rhadinovirus, and identification of an origin of DNA replication. J Virol 75, 1186-1194.
