Abstract
To better define the molecular epidemiology of bluetongue virus (BTV) infection, the genetic characteristics and phylogenetic relationships of the S3 genes of the five U.S. prototype strains of BTV, the commercially available serotype 10 modified live virus vaccine, and 18 field isolates of BTV serotypes 10, 11, 13, and 17 obtained in California during 1980, 1981, 1989, and 1990 were determined. With the exception of the S3 gene of the U.S. prototype strain of BTV serotype 2 (BTV 2), these viruses had an overall sequence homology of between 95 and 100%. Phylogenetic analyses segregated the prototype U.S. BTV 2 strain to a unique branch (100% bootstrap value), whereas the rest of the viruses clustered in two main monophyletic groups that were not correlated with their serotype, year of isolation, or geographical origin. The lack of consistent association between S3 gene sequence and virus serotype likely is a consequence of reassortment of BTV gene segments during natural mixed infections of vertebrate and invertebrate hosts. The prototype strain of BTV 13, which is considered an introduction to the U.S. like BTV 2, presents an S3 gene which is highly homologous to those of some isolates of BTV 10 and especially to that of the vaccine strain. This finding strongly suggests that the U.S. prototype strain of BTV 13 is a natural reassortant. The different topologies of the phylogenetic trees of the L2 and S3 genes of the various viruses indicate that these two genome segments evolve independently. We conclude that the S3 gene segment of populations of BTV in California is formed by different consensus sequences which cocirculate and which cannot be grouped by serotype.
Full Text
The Full Text of this article is available as a PDF (165.9 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Akita G. Y., Chinsangaram J., Osburn B. I., Ianconescu M., Kaufman R. Detection of bluetongue virus serogroup by polymerase chain reaction. J Vet Diagn Invest. 1992 Oct;4(4):400–405. doi: 10.1177/104063879200400405. [DOI] [PubMed] [Google Scholar]
- Beaty B. J., Bishop D. H. Bunyavirus-vector interactions. Virus Res. 1988 Jun;10(4):289–301. doi: 10.1016/0168-1702(88)90071-8. [DOI] [PubMed] [Google Scholar]
- Buonagurio D. A., Nakada S., Fitch W. M., Palese P. Epidemiology of influenza C virus in man: multiple evolutionary lineages and low rate of change. Virology. 1986 Aug;153(1):12–21. doi: 10.1016/0042-6822(86)90003-6. [DOI] [PubMed] [Google Scholar]
- Chapell J. D., Goral M. I., Rodgers S. E., dePamphilis C. W., Dermody T. S. Sequence diversity within the reovirus S2 gene: reovirus genes reassort in nature, and their termini are predicted to form a panhandle motif. J Virol. 1994 Feb;68(2):750–756. doi: 10.1128/jvi.68.2.750-756.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Collisson E. W., Barber T. L. Isolation and identification of bluetongue virus: a serotype new to the U.S. Prog Clin Biol Res. 1985;178:319–327. [PubMed] [Google Scholar]
- Davies F. G., Mungai J. N., Pini A. A new bluetongue virus serotype isolated in Kenya. Vet Microbiol. 1992 Apr;31(1):25–32. doi: 10.1016/0378-1135(92)90138-j. [DOI] [PubMed] [Google Scholar]
- Fitch W. M., Margoliash E. Construction of phylogenetic trees. Science. 1967 Jan 20;155(3760):279–284. doi: 10.1126/science.155.3760.279. [DOI] [PubMed] [Google Scholar]
- Fukusho A., Yu Y., Yamaguchi S., Roy P. Completion of the sequence of bluetongue virus serotype 10 by the characterization of a structural protein, VP6, and a non-structural protein, NS2. J Gen Virol. 1989 Jul;70(Pt 7):1677–1689. doi: 10.1099/0022-1317-70-7-1677. [DOI] [PubMed] [Google Scholar]
- Gould A. R., Hyatt A. D. The orbivirus genus. Diversity, structure, replication and phylogenetic relationships. Comp Immunol Microbiol Infect Dis. 1994 Aug-Nov;17(3-4):163–188. doi: 10.1016/0147-9571(94)90041-8. [DOI] [PubMed] [Google Scholar]
- Gould A. R., Pritchard L. I. Relationships amongst bluetongue viruses revealed by comparisons of capsid and outer coat protein nucleotide sequences. Virus Res. 1990 Aug;17(1):31–52. doi: 10.1016/0168-1702(90)90078-p. [DOI] [PubMed] [Google Scholar]
- Heidner H. W., Iezzi L. G., Osburn B. I., MacLachlan N. J. Genetic variation and evolutionary relationships amongst bluetongue viruses endemic in the United States. Virus Res. 1991 Oct;21(2):91–109. doi: 10.1016/0168-1702(91)90001-c. [DOI] [PubMed] [Google Scholar]
- Hwang G. Y., Chiou J. F., Yang Y. Y., Li J. K. Comparative sequence analyses of the cognate structural protein VP6 genes of five US bluetongue viruses. Virus Res. 1992 Aug;24(3):315–323. doi: 10.1016/0168-1702(92)90126-t. [DOI] [PubMed] [Google Scholar]
- Hwang G. Y., Yang Y. Y., Chiou J. F., Li J. K. Sequence conservation among the cognate nonstructural NS3/3A protein genes of six bluetongue viruses. Virus Res. 1992 Apr;23(1-2):151–161. doi: 10.1016/0168-1702(92)90074-j. [DOI] [PubMed] [Google Scholar]
- Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980 Dec;16(2):111–120. doi: 10.1007/BF01731581. [DOI] [PubMed] [Google Scholar]
- Kowalik T. F., Li J. K. Bluetongue virus evolution: sequence analyses of the genomic S1 segments and major core protein VP7. Virology. 1991 Apr;181(2):749–755. doi: 10.1016/0042-6822(91)90911-t. [DOI] [PubMed] [Google Scholar]
- Kozak M. Structural features in eukaryotic mRNAs that modulate the initiation of translation. J Biol Chem. 1991 Oct 25;266(30):19867–19870. [PubMed] [Google Scholar]
- Lu W., Duhamel G. E., Benfield D. A., Grotelueschen D. M. Serological and genotypic characterization of group A rotavirus reassortants from diarrheic calves born to dams vaccinated against rotavirus. Vet Microbiol. 1994 Nov;42(2-3):159–170. doi: 10.1016/0378-1135(94)90015-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- MCKERCHER D. G., MCGOWAN B., Jr, CABASSO V. J., ROBERTS G. I., SAITO J. K. Studies on bluetongue. III. The development of a modified live virus vaccine employing American strains of bluetongue virus. Am J Vet Res. 1957 Apr;18(67):310–316. [PubMed] [Google Scholar]
- MacLachlan N. J., Rossitto P. V., Heidner H. W., Iezzi L. G., Yilma T. D., DeMaula C. D., Osburn B. I. Variation amongst the neutralizing epitopes of bluetongue viruses isolated in the United States in 1979-1981. Vet Microbiol. 1992 Jun 15;31(4):303–316. doi: 10.1016/0378-1135(92)90123-b. [DOI] [PubMed] [Google Scholar]
- Oberst R. D., Squire K. R., Stott J. L., Chuang R. Y., Osburn B. I. The coexistence of multiple bluetongue virus electropherotypes in individual cattle during natural infection. J Gen Virol. 1985 Sep;66(Pt 9):1901–1909. doi: 10.1099/0022-1317-66-9-1901. [DOI] [PubMed] [Google Scholar]
- Osburn B. I., McGowan B., Heron B., Loomis E., Bushnell R., Stott J., Utterback W. Epizootiologic study of bluetongue: virologic and serologic results. Am J Vet Res. 1981 May;42(5):884–887. [PubMed] [Google Scholar]
- Rossitto P. V., MacLachlan N. J. Neutralizing epitopes of the serotypes of bluetongue virus present in the United States. J Gen Virol. 1992 Aug;73(Pt 8):1947–1952. doi: 10.1099/0022-1317-73-8-1947. [DOI] [PubMed] [Google Scholar]
- Roy P. Bluetongue virus genetics and genome structure. Virus Res. 1989 Jul;13(3):179–206. doi: 10.1016/0168-1702(89)90015-4. [DOI] [PubMed] [Google Scholar]
- Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
- Samal S. K., Livingston C. W., Jr, McConnell S., Ramig R. F. Analysis of mixed infection of sheep with bluetongue virus serotypes 10 and 17: evidence for genetic reassortment in the vertebrate host. J Virol. 1987 Apr;61(4):1086–1091. doi: 10.1128/jvi.61.4.1086-1091.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Samal S. K., el-Hussein A., Holbrook F. R., Beaty B. J., Ramig R. F. Mixed infection of Culicoides variipennis with bluetongue virus serotypes 10 and 17: evidence for high frequency reassortment in the vector. J Gen Virol. 1987 Sep;68(Pt 9):2319–2329. doi: 10.1099/0022-1317-68-9-2319. [DOI] [PubMed] [Google Scholar]
- Stott J. L., Oberst R. D., Channell M. B., Osburn B. I. Genome segment reassortment between two serotypes of bluetongue virus in a natural host. J Virol. 1987 Sep;61(9):2670–2674. doi: 10.1128/jvi.61.9.2670-2674.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sugiyama K., Bishop D. H., Roy P. Analyses of the genomes of bluetongue viruses recovered in the United States. I. Oligonucleotide fingerprint studies that indicate the existence of naturally occurring reassortant BTV isolates. Virology. 1981 Oct 15;114(1):210–217. doi: 10.1016/0042-6822(81)90266-x. [DOI] [PubMed] [Google Scholar]
- Wade-Evans A. M., Mertens P. P., Belsham G. J. Sequence of genome segment 9 of bluetongue virus (serotype 1, South Africa) and expression analysis demonstrating that different forms of VP6 are derived from initiation of protein synthesis at two distinct sites. J Gen Virol. 1992 Nov;73(Pt 11):3023–3026. doi: 10.1099/0022-1317-73-11-3023. [DOI] [PubMed] [Google Scholar]
- Waldvogel A. S., Anderson C. A., Higgins R. J., Osburn B. I. Neurovirulence of the UC-2 and UC-8 strains of bluetongue virus serotype 11 in newborn mice. Vet Pathol. 1987 Sep;24(5):404–410. doi: 10.1177/030098588702400507. [DOI] [PubMed] [Google Scholar]
- Weaver S. C., Rico-Hesse R., Scott T. W. Genetic diversity and slow rates of evolution in New World alphaviruses. Curr Top Microbiol Immunol. 1992;176:99–117. doi: 10.1007/978-3-642-77011-1_7. [DOI] [PubMed] [Google Scholar]
- Webster R. G., Bean W. J., Gorman O. T., Chambers T. M., Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev. 1992 Mar;56(1):152–179. doi: 10.1128/mr.56.1.152-179.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yamashita M., Krystal M., Fitch W. M., Palese P. Influenza B virus evolution: co-circulating lineages and comparison of evolutionary pattern with those of influenza A and C viruses. Virology. 1988 Mar;163(1):112–122. doi: 10.1016/0042-6822(88)90238-3. [DOI] [PubMed] [Google Scholar]
- Yang Y. Y., Chiou J. F., Hwang G. Y., Huang I. J., Li J. K. Evolutionary analyses of five US bluetongue viruses using the cognate S2 genes. Virus Res. 1992 Sep 15;25(3):241–249. doi: 10.1016/0168-1702(92)90137-x. [DOI] [PubMed] [Google Scholar]
- de Mattos C. A., de Mattos C. C., Osburn B. I., MacLachlan N. J. Heterogeneity of the L2 gene of field isolates of bluetongue virus serotype 17 from the San Joaquin Valley of California. Virus Res. 1994 Jan;31(1):67–87. doi: 10.1016/0168-1702(94)90072-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- de Mattos C. A., de de Mattos C. C., Dangler C. A., Osburn B. I., Ianconescu M., Kaufmann R. Hybridization relatedness of Israeli and U.S. bluetongue (BLU) serotypes using cDNA probes from BLU virus strain 11-UC8. Arch Virol. 1992;122(1-2):23–33. doi: 10.1007/BF01321115. [DOI] [PubMed] [Google Scholar]
- de Mattos C. C., de Mattos C. A., Osburn B. I., Dangler C. A., Chuang R. Y., Doi R. H. Recombinant DNA probe for serotype-specific identification of bluetongue virus 17. Am J Vet Res. 1989 Apr;50(4):536–541. [PubMed] [Google Scholar]
- de Mattos C. C., de Mattos C. A., Osburn B. I., MacLachlan N. J. Evolution of the L2 gene of strains of bluetongue virus serotype 10 isolated in California. Virology. 1994 May 15;201(1):173–177. doi: 10.1006/viro.1994.1281. [DOI] [PubMed] [Google Scholar]