1887

Abstract

Previous studies have classified the sequences of bovine leukemia virus (BLV) provirus from different locations worldwide into between two and four genetic groupings. These different studies gave unique names to the identified groups and no study has yet integrated all the available sequences. Thus, we hypothesized that many of the different groups previously identified actually correspond to a limited group of genotypes that are unevenly distributed worldwide. To examine this hypothesis, we sequenced the gene from 28 BLV field strains and compared these sequences to 46 sequences that represent all the genetic groupings already identified. By using phylogenetic analyses, we recovered six clades, or genotypes, that we have called genotypes 1, 2, 3, 4, 5 and 6. Genotypes 1–5 have counterparts among the sequence groupings identified previously. One sequence did not cluster with any of the others and was highly divergent when compared with the six genotypes identified here. Thus, an extra genotype, which we named 7, may exist. Similarity comparisons were highly congruent with phylogenetic analyses. Furthermore, our analyses confirmed the existence of geographical clusters.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.011791-0
2009-11-01
2024-11-12
Loading full text...

Full text loading...

/deliver/fulltext/jgv/90/11/2788.html?itemId=/content/journal/jgv/10.1099/vir.0.011791-0&mimeType=html&fmt=ahah

References

  1. Asfaw Y., Tsuduku S., Konishi M., Murakami K., Tsuboi T., Wu D., Sentsui H. 2005; Distribution and superinfection of bovine leukemia virus genotypes in Japan. Arch Virol 150:493–505 [CrossRef]
    [Google Scholar]
  2. Ban J., Czene S., Altaner C., Callebaut I., Krchnak V., Merza M., Burny A., Kettmann R., Portetelle D. 1992; Mapping of sequential epitopes recognized by monoclonal antibodies on the bovine leukaemia virus external glycoproteins expressed in Escherichia coli by means of antipeptide antibodies. J Gen Virol 73:2457–2461 [CrossRef]
    [Google Scholar]
  3. Baule C., van Vuuren M., Lowings J. P., Belak S. 1997; Genetic heterogeneity of bovine viral diarrhoea viruses isolated in Southern Africa. Virus Res 52:205–220 [CrossRef]
    [Google Scholar]
  4. Baule C., Kulcsar G., Belak K., Albert M., Mittelholzer C., Soos T., Kucsera L., Belak S. 2001; Pathogenesis of primary respiratory disease induced by isolates from a new genetic cluster of bovine viral diarrhea virus type I. J Clin Microbiol 39:146–153 [CrossRef]
    [Google Scholar]
  5. Brillowska A., Dabrowski S., Rulka J., Kubis P., Buzala E., Kur J. 1999; Protection of cattle against bovine leukemia virus (BLV) infection could be attained by DNA vaccination. Acta Biochim Pol 46:971–976
    [Google Scholar]
  6. Bruck C., Mathot S., Portetelle D., Berte C., Franssen J. D., Herion P., Burny A. 1982a; Monoclonal antibodies define eight independent antigenic regions on the bovine leukemia virus (BLV) envelope glycoprotein gp51. Virology 122:342–352 [CrossRef]
    [Google Scholar]
  7. Bruck C., Portetelle D., Burny A., Zavada J. 1982b; Topographical analysis by monoclonal antibodies of BLV-gp51 epitopes involved in viral functions. Virology 122:353–362 [CrossRef]
    [Google Scholar]
  8. Bruck C., Portetelle D., Mammerickx M., Mathot S., Burny A. 1984a; Epitopes of bovine leukemia virus glycoprotein gp51 recognized by sera of infected cattle and sheep. Leuk Res 8:315–321 [CrossRef]
    [Google Scholar]
  9. Bruck C., Rensonnet N., Portetelle D., Cleuter Y., Mammerickx M., Burny A., Mamoun R., Guillemain B., van der Maaten M. J., Ghysdael J. 1984b; Biologically active epitopes of bovine leukemia virus glycoprotein gp51: their dependence on protein glycosylation and genetic variability. Virology 136:20–31 [CrossRef]
    [Google Scholar]
  10. Burny A., Cleuter Y., Kettmann R., Mammerickx M., Marbaix G., Portetelle D., Van den Broeke A., Willems L., Thomas R. 1987; Bovine leukaemia: facts and hypotheses derived from the study of an infectious cancer. Cancer Surv 6:139–159
    [Google Scholar]
  11. Callebaut I., Burny A., Krchnak V., Gras-Masse H., Wathelet B., Portetelle D. 1991; Use of synthetic peptides to map sequential epitopes recognized by monoclonal antibodies on the bovine leukemia virus external glycoprotein. Virology 185:48–55 [CrossRef]
    [Google Scholar]
  12. Callebaut I., Voneche V., Mager A., Fumiere O., Krchnak V., Merza M., Zavada J., Mammerickx M., Burny A., Portetelle D. 1993; Mapping of B-neutralizing and T-helper cell epitopes on the bovine leukemia virus external glycoprotein gp51. J Virol 67:5321–5327
    [Google Scholar]
  13. Camargos M. F., Stancek D., Rocha M. A., Lessa L. M., Reis J. K., Leite R. C. 2002; Partial sequencing of env gene of bovine leukaemia virus from Brazilian samples and phylogenetic analysis. J Vet Med B Infect Dis Vet Public Health 49:325–331 [CrossRef]
    [Google Scholar]
  14. Camargos M. F., Pereda A., Stancek D., Rocha M. A., dos Reis J. K., Greiser-Wilke I., Leite R. C. 2007; Molecular characterization of the env gene from Brazilian field isolates of bovine leukemia virus. Virus Genes 34:343–350 [CrossRef]
    [Google Scholar]
  15. Camin J. H., Sokal R. R. 1965; A method for deducing branching sequences in phylogeny. Evolution 19:311–326 [CrossRef]
    [Google Scholar]
  16. Cassar O., Capuano C., Bassot S., Charavay F., Duprez R., Afonso P. V., Abel M., Walter H., Mera W. other authors 2007; Human T lymphotropic virus type 1 subtype C melanesian genetic variants of the Vanuatu Archipelago and Solomon Islands share a common ancestor. J Infect Dis 196:510–521 [CrossRef]
    [Google Scholar]
  17. Chor B., Hendy M. D., Holland B. R., Penny D. 2000; Multiple maxima of likelihood in phylogenetic trees: an analytic approach. Mol Biol Evol 17:1529–1541 [CrossRef]
    [Google Scholar]
  18. Coulston J., Naif H., Brandon R., Kumar S., Khan S., Daniel R. C., Lavin M. F. 1990; Molecular cloning and sequencing of an Australian isolate of proviral bovine leukaemia virus DNA: comparison with other isolates. J Gen Virol 71:1737–1746 [CrossRef]
    [Google Scholar]
  19. Dube D. K., Sherman M. P., Saksena N. K., Bryz-Gornia V., Mendelson J., Love J., Arnold C. B., Spicer T., Dube S. other authors 1993; Genetic heterogeneity in human T-cell leukemia/lymphoma virus type II. J Virol 67:1175–1184
    [Google Scholar]
  20. Dube S., Bachman S., Spicer T., Love J., Choi D., Esteban E., Ferrer J. F., Poiesz B. J. 1997; Degenerate and specific PCR assays for the detection of bovine leukaemia virus and primate T cell leukaemia/lymphoma virus pol DNA and RNA: phylogenetic comparisons of amplified sequences from cattle and primates from around the world. J Gen Virol 78:1389–1398
    [Google Scholar]
  21. Dube S., Dolcini G., Abbott L., Mehta S., Dube D., Gutierrez S., Ceriani C., Esteban E., Ferrer J., Poiesz B. 2000; The complete genomic sequence of a BLV strain from a Holstein cow from Argentina. Virology 277:379–386 [CrossRef]
    [Google Scholar]
  22. Eirin M. E., Dilernia D. A., Berini C. A., Jones L. R., Pando M. A., Biglione M. M. 2008; Divergent strains of human T-lymphotropic virus type 1 (HTLV-1) within the Cosmopolitan subtype in Argentina. AIDS Res Hum Retroviruses 24:1237–1244 [CrossRef]
    [Google Scholar]
  23. Eisen J. A. 1997; The genetic data environment. A user modifiable and expandable multiple sequence analysis package. Methods Mol Biol 70:13–38
    [Google Scholar]
  24. Farris J. S. 1970; Methods for computing Wagner trees. Syst Zool 19:83–92 [CrossRef]
    [Google Scholar]
  25. Farris J. S. 1983; The logical basis of phylogenetic analysis. In Proceedings of the 2nd meeting of the Willi Hennig Society. Advances in Cladistics 2 pp 7–36Edited by Platnick N. F., Funk V. A. New York: Columbia University Press;
    [Google Scholar]
  26. Fechner H., Kurg A., Geue L., Blankenstein P., Mewes G., Ebner D., Beier D. 1996; Evaluation of polymerase chain reaction (PCR) application in diagnosis of bovine leukaemia virus (BLV) infection in naturally infected cattle. Zentralbl Veterinarmed B 43:621–630
    [Google Scholar]
  27. Fechner H., Blankenstein P., Looman A. C., Elwert J., Geue L., Albrecht C., Kurg A., Beier D., Marquardt O., Ebner D. 1997; Provirus variants of the bovine leukemia virus and their relation to the serological status of naturally infected cattle. Virology 237:261–269 [CrossRef]
    [Google Scholar]
  28. Felmer R., Munoz G., Zuniga J., Recabal M. 2005; Molecular analysis of a 444 bp fragment of the bovine leukaemia virus gp51 env gene reveals a high frequency of non-silent point mutations and suggests the presence of two subgroups of BLV in Chile. Vet Microbiol 108:39–47 [CrossRef]
    [Google Scholar]
  29. Felsenstein J. 1981; Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376 [CrossRef]
    [Google Scholar]
  30. Felsenstein J. 1985; Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791 [CrossRef]
    [Google Scholar]
  31. Gatei M. H., Good M. F., Daniel R. C., Lavin M. F. 1993; T-cell responses to highly conserved CD4 and CD8 epitopes on the outer membrane protein of bovine leukemia virus: relevance to vaccine development. J Virol 67:1796–1802
    [Google Scholar]
  32. Gillet N., Florins A., Boxus M., Burteau C., Nigro A., Vandermeers F., Balon H., Bouzar A. B., Defoiche J. other authors 2007; Mechanisms of leukemogenesis induced by bovine leukemia virus: prospects for novel anti-retroviral therapies in human. Retrovirology 4:18 [CrossRef]
    [Google Scholar]
  33. Giribet G. 2005; TNT: Tree analysis using new technology. Syst Biol 54:176–178 [CrossRef]
    [Google Scholar]
  34. Goloboff P. A. 1993; Estimating character weights during tree search. Cladistics 9:83–91 [CrossRef]
    [Google Scholar]
  35. Goloboff P. A. 1999; Analyzing large data sets in reasonable times: solutions for composite optima. Cladistics 15:415–428 [CrossRef]
    [Google Scholar]
  36. Goloboff P. A., Farris J. S. 2001; Methods for quick consensus estimations. Cladistics 17:S26–S34 [CrossRef]
    [Google Scholar]
  37. Goloboff P. A., Farris J. S., Nixon K. C. 2008; TNT, a free program for phylogenetic analysis. Cladistics 24:774–786 [CrossRef]
    [Google Scholar]
  38. Guindon S., Gascuel O. 2003; A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704 [CrossRef]
    [Google Scholar]
  39. Hasegawa M., Kishino H., Yano T. 1985; Dating the human–ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174 [CrossRef]
    [Google Scholar]
  40. Hayward G. S., Zong J. C. 2007; Modern evolutionary history of the human KSHV genome. Curr Top Microbiol Immunol 312:1–42
    [Google Scholar]
  41. Hemmatzadeh F. 2007; Sequencing and phylogenetic analysis of gp51 gene of bovine leukaemia virus in Iranian isolates. Vet Res Commun 31:783–789 [CrossRef]
    [Google Scholar]
  42. Huelsenbeck J. P., Ronquist F. 2001; MrBayes: Bayesian inference of phylogeny. Bioinformatics 17:754–755 [CrossRef]
    [Google Scholar]
  43. Huelsenbeck J. P., Fredrik Ronquist F., Nielsen R., Bollback J. P. 2001; Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294:2310–2314 [CrossRef]
    [Google Scholar]
  44. Ibrahim K. M., Nichols R. A., Hewitt G. M. 1996; Spatial patterns of genetic variation generated by different forms of dispersal during range expansion. Heredity 77:282–291 [CrossRef]
    [Google Scholar]
  45. Jones L. R., Zandomeni R., Weber E. L. 2001; Genetic typing of bovine viral diarrhea virus isolates from Argentina. Vet Microbiol 81:367–375 [CrossRef]
    [Google Scholar]
  46. Jones L. R., Cigliano M. M., Zandomenni R. O., Weber E. L. 2004; Phylogenetic analysis of bovine pestiviruses: testing the evolution of clinical symptoms. Cladistics 20:443–453 [CrossRef]
    [Google Scholar]
  47. Katoh K., Misawa K., Kuma K., Miyata T. 2002; mafft: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066 [CrossRef]
    [Google Scholar]
  48. Katoh K., Kuma K., Toh H., Miyata T. 2005; mafft version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511–518 [CrossRef]
    [Google Scholar]
  49. Kerkhofs P., Gatot J. S., Knapen K., Mammerickx M., Burny A., Portetelle D., Willems L., Kettmann R. 2000; Long-term protection against bovine leukaemia virus replication in cattle and sheep. J Gen Virol 81:957–963
    [Google Scholar]
  50. Kettmann R., Couez D., Burny A. 1981; Restriction endonuclease mapping of linear unintegrated proviral DNA of bovine leukemia virus. J Virol 38:27–33
    [Google Scholar]
  51. Licursi M., Inoshima Y., Wu D., Yokoyama T., Gonzalez E. T., Sentsui H. 2002; Genetic heterogeneity among bovine leukemia virus genotypes and its relation to humoral responses in hosts. Virus Res 86:101–110 [CrossRef]
    [Google Scholar]
  52. Licursi M., Inoshima Y., Wu D., Yokoyama T., Gonzalez E. T., Sentsui H. 2003; Provirus variants of bovine leukemia virus in naturally infected cattle from Argentina and Japan. Vet Microbiol 96:17–23 [CrossRef]
    [Google Scholar]
  53. Makuwa M., Souquière S., Clifford S. L., Telfer P. T., Sallé B., Bourry O., Onanga R., Mouinga-Ondeme A., Wickings E. J. other authors 2004; Two distinct STLV-1 subtypes infecting Mandrillus sphinx follow the geographic distribution of their hosts. AIDS Res Hum Retroviruses 20:1137–1143 [CrossRef]
    [Google Scholar]
  54. Mamoun R. Z., Morisson M., Rebeyrotte N., Busetta B., Couez D., Kettmann R., Hospital M., Guillemain B. 1990; Sequence variability of bovine leukemia virus env gene and its relevance to the structure and antigenicity of the glycoproteins. J Virol 64:4180–4188
    [Google Scholar]
  55. McMahon M. M., Sanderson M. J. 2006; Phylogenetic supermatrix analysis of GenBank sequences from 2228 papilionoid legumes. Syst Biol 55:818–836 [CrossRef]
    [Google Scholar]
  56. Mirsky M. L., Olmstead C. A., Da Y., Lewin H. A. 1996; The prevalence of proviral bovine leukemia virus in peripheral blood mononuclear cells at two subclinical stages of infection. J Virol 70:2178–2183
    [Google Scholar]
  57. Molteni E., Agresti A., Meneveri R., Marozzi A., Malcovati M., Bonizzi L., Poli G., Ginelli E. 1996; Molecular characterization of a variant of proviral bovine leukaemia virus (BLV). Zentralbl Veterinarmed B 43:201–211 [CrossRef]
    [Google Scholar]
  58. Monti G., Schrijver R., Beier D. 2005; Genetic diversity and spread of Bovine leukaemia virus isolates in Argentine dairy cattle. Arch Virol 150:443–458 [CrossRef]
    [Google Scholar]
  59. Nixon K. C. 1999; The parsimony ratchet, a new method for rapid parsimony analysis. Cladistics 15:407–414 [CrossRef]
    [Google Scholar]
  60. Nylander J. A. 2004 MrAIC.pl: Program distributed by the author Evolutionary Biology Centre, Uppsala University;
    [Google Scholar]
  61. Phillips A., Janies D., Wheeler W. 2000; Multiple sequence alignment in phylogenetic analysis. Mol Phylogenet Evol 16:317–330 [CrossRef]
    [Google Scholar]
  62. Portetelle D., Dandoy C., Burny A., Zavada J., Siakkou H., Gras-Masse H., Drobecq H., Tartar A. 1989; Synthetic peptides approach to identification of epitopes on bovine leukemia virus envelope glycoprotein gp51. Virology 169:34–41 [CrossRef]
    [Google Scholar]
  63. Rambaut A., Drummond A. J. 2007 Tracer v1.4: University of Oxford Oxford, UK: Available at http://beast.bio.ed.ac.uk/Tracer
    [Google Scholar]
  64. Rannala B., Yang Y. 1996; Probability distribution of molecular evolutionary trees: a new method of phylogenetic inference. J Mol Evol 43:304–311 [CrossRef]
    [Google Scholar]
  65. Reichel M. P., Tham K. M., Barnes S., Kittelberger R. 1998; Evaluation of alternative methods for the detection of bovine leukaemia virus in cattle. N Z Vet J 46:140–146 [CrossRef]
    [Google Scholar]
  66. Rice N. R., Stephens R. M., Couez D., Deschamps J., Kettmann R., Burny A., Gilden R. V. 1984; The nucleotide sequence of the env gene and post-env region of bovine leukemia virus. Virology 138:82–93 [CrossRef]
    [Google Scholar]
  67. Ronquist F., Huelsenbeck J. P. 2003; MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574 [CrossRef]
    [Google Scholar]
  68. Sagata N., Yasunaga T., Tsuzuku-Kawamura J., Ohishi K., Ogawa Y., Ikawa Y. 1985; Complete nucleotide sequence of the genome of bovine leukemia virus: its evolutionary relationship to other retroviruses. Proc Natl Acad Sci U S A 82:677–681 [CrossRef]
    [Google Scholar]
  69. Saitou N., Nei M. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
    [Google Scholar]
  70. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  71. Simmonds P. 2006; Recombination and selection in the evolution of picornaviruses and other mammalian positive-stranded RNA viruses. J Virol 80:11124–11140 [CrossRef]
    [Google Scholar]
  72. Smith S. A., Donoghue M. J. 2008; Rates of molecular evolution are linked to life history in flowering plants. Science 322:86–89 [CrossRef]
    [Google Scholar]
  73. Smith S. W., Overbeek R., Woese C. R., Gilbert W., Gillevet P. M. 1994; The genetic data environment an expandable GUI for multiple sequence analysis. Comput Appl Biosci 10:671–675
    [Google Scholar]
  74. Swofford D. L. 1998 paup*: Phylogenetic analysis using parsimony (and other methods) Sunderland, MA: Sinauer;
    [Google Scholar]
  75. Swofford D. L., Olsen G. J., Wadell P. J., Hillis D. M. 1996; Phylogenetic inference. In Molecular Systematics, 2nd edn.Edited by Hillis D. M., Moriz C., Mable. Sunderland, MA: Sinauer;
    [Google Scholar]
  76. Tartaglia M., Saulle E., Pestalozza S., Morelli L., Antonucci G., Battaglia P. A. 1998; Detection of bovine mitochondrial DNA in ruminant feeds: a molecular approach to test for the presence of bovine-derived materials. J Food Prot 61:513–518
    [Google Scholar]
  77. Thompson J. D., Gibson T. J., Higgins D. G. 2002; Multiple sequence alignment using clustal_w and clustal_x. Curr Protoc Bioinformatics Chapter 2, Unit 2.3
    [Google Scholar]
  78. Tomaszewski E. K., Kaleta E. F., Phalen D. N. 2003; Molecular phylogeny of the psittacid herpesviruses causing Pacheco's disease: correlation of genotype with phenotypic expression. J Virol 77:11260–11267 [CrossRef]
    [Google Scholar]
  79. Trono K. G., Perez-Filgueira D. M., Duffy S., Borca M. V., Carrillo C. 2001; Seroprevalence of bovine leukemia virus in dairy cattle in Argentina: comparison of sensitivity and specificity of different detection methods. Vet Microbiol 83:235–248 [CrossRef]
    [Google Scholar]
  80. Van den Broeke A., Cleuter Y., Chen G., Portetelle D., Mammerickx M., Zagury D., Fouchard M., Coulombel L., Kettmann R., Burny A. 1988; Even transcriptionally competent proviruses are silent in bovine leukemia virus-induced sheep tumor cells. Proc Natl Acad Sci U S A 85:9263–9267 [CrossRef]
    [Google Scholar]
  81. Vidal A. U., Gessain A., Yoshida M., Tekaia F., Garin B., Guillemain B., Schulz T., Farid R., De Thé G. 1994; Phylogenetic classification of human T cell leukaemia/lymphoma virus type I genotypes in five major molecular and geographical subtypes. J Gen Virol 75:3655–3666 [CrossRef]
    [Google Scholar]
  82. Wiens J. J. 2006; Missing data and the design of phylogenetic analyses. J Biomed Inform 39:34–42 [CrossRef]
    [Google Scholar]
  83. Willems L., Thienpont E., Kerkhofs P., Burny A., Mammerickx M., Kettmann R. 1993; Bovine leukemia virus, an animal model for the study of intrastrain variability. J Virol 67:1086–1089
    [Google Scholar]
  84. Willems L., Burny A., Collete D., Dangoisse O., Dequiedt F., Gatot J. S., Kerkhofs P., Lefèbvre L., Merezak C. other authors 2000; Genetic determinants of bovine leukemia virus pathogenesis. AIDS Res Hum Retroviruses 16:1787–1795 [CrossRef]
    [Google Scholar]
  85. Zhao X., Buehring G. C. 2007; Natural genetic variations in bovine leukemia virus envelope gene: possible effects of selection and escape. Virology 366:150–165 [CrossRef]
    [Google Scholar]
  86. Zong J. C., Ciufo D. M., Alcendor D. J., Wan X., Nicholas J., Browning P. J., Rady P. L., Tyring S. K., Orenstein J. M., & other authors B. K. 1999; High-level variability in the ORF-K1 membrane protein gene at the left end of the Kaposi's sarcoma-associated herpesvirus genome defines four major virus subtypes and multiple variants or clades in different human populations. J Virol 73:4156–4170
    [Google Scholar]
/content/journal/jgv/10.1099/vir.0.011791-0
Loading
/content/journal/jgv/10.1099/vir.0.011791-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error