Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Virology Journal
Published in: Virology Journal 1/2017

Open Access 01-12-2017 | Review

Epidemiology and genetic diversity of bovine leukemia virus

Authors: Meripet Polat, Shin-nosuke Takeshima, Yoko Aida

Published in: Virology Journal | Issue 1/2017

Login to get access

Abstract

Bovine leukemia virus (BLV), an oncogenic member of the Deltaretrovirus genus, is closely related to human T-cell leukemia virus (HTLV-I and II). BLV infects cattle worldwide and causes important economic losses. In this review, we provide a summary of available information about commonly used diagnostic approaches for the detection of BLV infection, including both serological and viral genome-based methods. We also outline genotyping methods used for the phylogenetic analysis of BLV, including PCR restriction length polymorphism and modern DNA sequencing-based methods. In addition, detailed epidemiological information on the prevalence of BLV in cattle worldwide is presented. Finally, we summarize the various BLV genotypes identified by the phylogenetic analyses of the whole genome and env gp51 sequences of BLV strains in different countries and discuss the distribution of BLV genotypes worldwide.
Literature
1.
Kettmann R, Portetelle D, Mammerickx M, Cleuter Y, Dekegel D, Galoux M, Ghysdael J, Burny A, Chantrenne H. Bovine leukemia virus: an exogenous RNA oncogenic virus. Proc Natl Acad Sci U S A. 1976;73:1014–8.PubMedPubMedCentralCrossRef
2.
Aida Y, Murakami H, Takahashi M, Takeshima SN. Mechanisms of pathogenesis induced by bovine leukemia virus as a model for human T-cell leukemia virus. Front Microbiol. 2013;4:328.PubMedPubMedCentralCrossRef
3.
4.
Hajj HE, Nasr R, Kfoury Y, Dassouki Z, Nasser R, Kchour G, Hermine O, De The H, Bazarbachi A. Animal models on HTLV-1 and related viruses: what did we learn? Front Microbiol. 2012;3:333.PubMedPubMedCentralCrossRef
5.
Kirkland PD, Rodwell BJ. Enzootic Bovine Leukosis. Australia and New Zealand Standard Diagnostic Procedures. 2005:1–14.
6.
Williams DL, Barta O, Amborski GF. Molecular studies of T-lymphocytes from cattle infected with bovine leukemia virus. Vet Immunol Immunopathol. 1988;19:307–23.PubMedCrossRef
7.
Stott ML, Thurmond MC, Dunn SJ, Osburn BI, Stott JL. Integrated bovine leukosis proviral DNA in T helper and T cytotoxic/suppressor lymphocytes. J Gen Virol. 1991;72(Pt 2):307–15.PubMedCrossRef
8.
Schwartz I, Bensaid A, Polack B, Perrin B, Berthelemy M, Levy D. In vivo leukocyte tropism of bovine leukemia virus in sheep and cattle. J Virol. 1994;68:4589–96.PubMedPubMedCentral
9.
Mirsky ML, Olmstead CA, Da Y, Lewin HA. The prevalence of proviral bovine leukemia virus in peripheral blood mononuclear cells at two subclinical stages of infection. J Virol. 1996;70:2178–83.PubMedPubMedCentral
10.
Wu D, Takahashi K, Murakami K, Tani K, Koguchi A, Asahina M, Goryo M, Aida Y, Okada K. B-1a, B-1b and conventional B cell lymphoma from enzootic bovine leukosis. Vet Immunol Immunopathol. 1996;55:63–72.PubMedCrossRef
11.
Panei CJ, Takeshima SN, Omori T, Nunoya T, Davis WC, Ishizaki H, Matoba K, Aida Y. Estimation of bovine leukemia virus (BLV) proviral load harbored by lymphocyte subpopulations in BLV-infected cattle at the subclinical stage of enzootic bovine leucosis using BLV-CoCoMo-qPCR. BMC Vet Res. 2013;9:95.PubMedPubMedCentralCrossRef
12.
Aida Y, Okada K, Amanuma H. Phenotype and ontogeny of cells carrying a tumor-associated antigen that is expressed on bovine leukemia virus-induced lymphosarcoma. Cancer Res. 1993;53:429–37.PubMed
13.
Nekouei O, VanLeeuwen J, Stryhn H, Kelton D, Keefe G. Lifetime effects of infection with bovine leukemia virus on longevity and milk production of dairy cows. Prev Vet Med. 2016;133:1–9.PubMedCrossRef
14.
Sandev N, Koleva M, Binev R, Ilieva D. Influence of enzootic bovine leukosis virus upon the incidence of subclinical mastitis in cows at a different stage of infection. Veterinarski Archiv. 2004;76:411–6.
15.
Bartlett PC, Norby B, Byrem TM, Parmelee A, Ledergerber JT, Erskine RJ. Bovine leukemia virus and cow longevity in Michigan dairy herds. J Dairy Sci. 2013;96:1591–7.PubMedCrossRef
16.
Ferrer JF, Marshak RR, Abt DA, Kenyon SJ. Persistent lymphocytosis in cattle: its cause, nature and relation to lymphosarcoma. Ann Rech Vet. 1978;9:851–7.PubMed
17.
OIE. Manual of diagnostic tests and vaccines for terrestrial animals: chapter 2.4.11. Enzootic Bovine Leukosis. Seventh Edition edn. France: World organization for animal health; 2012.
18.
Sagata N, Yasunaga T, Tsuzuku-Kawamura J, Ohishi K, Ogawa Y, Ikawa Y. Complete nucleotide sequence of the genome of bovine leukemia virus: its evolutionary relationship to other retroviruses. Proc Natl Acad Sci U S A. 1985;82:677–81.PubMedPubMedCentralCrossRef
19.
Sagata N, Yasunaga T, Ohishi K, Tsuzuku-Kawamura J, Onuma M, Ikawa Y. Comparison of the entire genomes of bovine leukemia virus and human T-cell leukemia virus and characterization of their unidentified open reading frames. EMBO J. 1984;3:3231–7.PubMedPubMedCentral
20.
Callebaut I, Voneche V, Mager A, Fumiere O, Krchnak V, Merza M, Zavada J, Mammerickx M, Burny A, Portetelle D. Mapping of B-neutralizing and T-helper cell epitopes on the bovine leukemia virus external glycoprotein gp51. J Virol. 1993;67:5321–7.PubMedPubMedCentral
21.
Inabe K, Nishizawa M, Tajima S, Ikuta K, Aida Y. The YXXL sequences of a transmembrane protein of bovine leukemia virus are required for viral entry and incorporation of viral envelope protein into virions. J Virol. 1999;73:1293–301.PubMedPubMedCentral
22.
Jewell NA, Mansky LM. The beginning: genome recognition, RNA encapsidation and the initiation of complex retrovirus assembly. J Gen Virol. 2000;81:1889–99.PubMedCrossRef
23.
24.
Bai L, Otsuki H, Sato H, Kohara J, Isogai E, Takeshima SN, Aida Y. Identification and characterization of common B cell epitope in bovine leukemia virus via high-throughput peptide screening system in infected cattle. Retrovirology. 2015;12:106.PubMedPubMedCentralCrossRef
25.
Copeland TD, Morgan MA, Oroszlan S. Complete amino acid sequence of the nucleic acid-binding protein of bovine leukemia virus. FEBS Lett. 1983;156:37–40.PubMedCrossRef
26.
Mager A, Masengo R, Mammerickx M, Letesson JJ. T cell proliferative response to bovine leukaemia virus (BLV): identification of T cell epitopes on the major core protein (p24) in BLV-infected cattle with normal haematological values. J Gen Virol. 1994;75(Pt 9):2223–31.PubMedCrossRef
27.
Willems L, Kerkhofs P, Attenelle L, Burny A, Portetelle D, Kettmann R. The major homology region of bovine leukaemia virus p24gag is required for virus infectivity in vivo. J Gen Virol. 1997;78(Pt 3):637–40.PubMedCrossRef
28.
Katoh I, Yasunaga T, Yoshinaka Y. Bovine leukemia virus RNA sequences involved in dimerization and specific gag protein binding: close relation to the packaging sites of avian, murine, and human retroviruses. J Virol. 1993;67:1830–9.PubMedPubMedCentral
29.
Willems L, Heremans H, Chen G, Portetelle D, Billiau A, Burny A, Kettmann R. Cooperation between bovine leukaemia virus transactivator protein and ha-ras oncogene product in cellular transformation. EMBO J. 1990;9:1577–81.PubMedPubMedCentral
30.
Willems L, Grimonpont C, Heremans H, Rebeyrotte N, Chen G, Portetelle D, Burny A, Kettmann R. Mutations in the bovine leukemia-virus tax protein can abrogate the long terminal repeat-directed Transactivating activity without concomitant loss of transforming potential. Proc Natl Acad Sci U S A. 1992;89:3957–61.PubMedPubMedCentralCrossRef
31.
Tajima S, Aida Y. The region between amino acids 245 and 265 of the bovine leukemia virus (BLV) tax protein restricts transactivation not only via the BLV enhancer but also via other retrovirus enhancers. J Virol. 2000;74:10939–49.PubMedPubMedCentralCrossRef
32.
Felber BK, Derse D, Athanassopoulos A, Campbell M, Pavlakis GN. Cross-activation of the Rex proteins of HTLV-I and BLV and of the rev protein of HIV-1 and nonreciprocal interactions with their RNA responsive elements. New Biol. 1989;1:318–28.PubMed
33.
Tajima S, Takahashi M, Takeshima SN, Konnai S, Yin SA, Watarai S, Tanaka Y, Onuma M, Okada K, Aida Y. A mutant form of the tax protein of bovine leukemia virus (BLV), with enhanced transactivation activity, increases expression and propagation of BLV in vitro but not in vivo. J Virol. 2003;77:1894–903.PubMedPubMedCentralCrossRef
34.
Takahashi M, Tajima S, Takeshima SN, Konnai S, Yin SA, Okada K, Davis WC, Aida Y. Ex vivo survival of peripheral blood mononuclear cells in sheep induced by bovine leukemia virus (BLV) mainly occurs in CD5- B cells that express BLV. Microbes Infect. 2004;6:584–95.PubMedCrossRef
35.
Takahashi M, Tajima S, Okada K, Davis WC, Aida Y. Involvement of bovine leukemia virus in induction and inhibition of apoptosis. Microbes Infect. 2005;7:19–28.PubMedCrossRef
36.
37.
Willems L, Kerkhofs P, Dequiedt F, Portetelle D, Mammerickx M, Burny A, Kettmann R. Attenuation of bovine leukemia virus by deletion of R3 and G4 open reading frames. Proc Natl Acad Sci U S A. 1994;91:11532–6.PubMedPubMedCentralCrossRef
38.
Florins A, Gillet N, Boxus M, Kerkhofs P, Kettmann R, Willems L. Even attenuated bovine leukemia virus proviruses can be pathogenic in sheep. J Virol. 2007;81:10195–200.PubMedPubMedCentralCrossRef
39.
40.
Rosewick N, Momont M, Durkin K, Takeda H, Caiment F, Cleuter Y, Vernin C, Mortreux F, Wattel E, Burny A, et al. Deep sequencing reveals abundant noncanonical retroviral microRNAs in B-cell leukemia/lymphoma. Proc Natl Acad Sci U S A. 2013;110:2306–11.PubMedPubMedCentralCrossRef
41.
Gillet NA, Hamaidia M, de Brogniez A, Gutierrez G, Renotte N, Reichert M, Trono K, Willems L. Bovine leukemia virus small noncoding RNAs are functional elements that regulate replication and contribute to Oncogenesis in vivo. PLoS Pathog. 2016;12:e1005588.PubMedPubMedCentralCrossRef
42.
Van Driessche B, Rodari A, Delacourt N, Fauquenoy S, Vanhulle C, Burny A, Rohr O, Van Lint C. Characterization of new RNA polymerase III and RNA polymerase II transcriptional promoters in the bovine leukemia virus genome. Sci Rep. 2016;6:31125.PubMedPubMedCentralCrossRef
43.
Jimba M, Takeshima SN, Murakami H, Kohara J, Kobayashi N, Matsuhashi T, Ohmori T, Nunoya T, Aida Y. BLV-CoCoMo-qPCR: a useful tool for evaluating bovine leukemia virus infection status. BMC Vet Res. 2012;8:167.PubMedPubMedCentralCrossRef
44.
Walker PJ, Molloy JB, Rodwell BJ. A protein immunoblot test for detection of bovine leukemia virus p24 antibody in cattle and experimentally infected sheep. J Virol Methods. 1987;15:201–11.PubMedCrossRef
45.
Portetelle D, Bruck C, Mammerickx M, Burny A. In animals infected by bovine leukemia virus (BLV) antibodies to envelope glycoprotein gp51 are directed against the carbohydrate moiety. Virology. 1980;105:223–33.PubMedCrossRef
46.
Bai L, Takeshima SN, Isogai E, Kohara J, Aida Y. Novel CD8(+) cytotoxic T cell epitopes in bovine leukemia virus with cattle. Vaccine. 2015;33:7194–202.PubMedCrossRef
47.
Aida Y, Miyasaka M, Okada K, Onuma M, Kogure S, Suzuki M, Minoprio P, Levy D, Ikawa Y. Further phenotypic characterization of target cells for bovine leukemia virus experimental infection in sheep. Am J Vet Res. 1989;50:1946–51.PubMed
48.
Wang CT. Bovine leukemia virus infection in Taiwan: epidemiological study. J Vet Med Sci. 1991;53:395–8.PubMedCrossRef
49.
Monti GE, Frankena K, Engel B, Buist W, Tarabla HD, de Jong MC. Evaluation of a new antibody-based enzyme-linked immunosorbent assay for the detection of bovine leukemia virus infection in dairy cattle. J Vet Diagn Investig. 2005;17:451–7.CrossRef
50.
Kurdi A, Blankenstein P, Marquardt O, Ebner D. Serologic and virologic investigations on the presence of BLV infection in a dairy herd in Syria. Berl Munch Tierarztl Wochenschr. 1999;112:18–23.PubMed
51.
Fukai K, Sato M, Kawara M, Hoshi Z, Ueno S, Chyou N, Akashi H. A case of an embryo transfer calf infected with bovine leukemia virus from the recipient cow. Zentralbl Veterinarmed B. 1999;46:511–5.PubMed
52.
Zaghawa A, Beier D, Abd El-Rahim IH, Karim I, El-ballal S, Conraths FJ, Marquardt O. An outbreak of enzootic bovine leukosis in upper Egypt: clinical, laboratory and molecular-epidemiological studies. J Vet Med B Infect Dis Vet Public Health. 2002;49:123–9.PubMedCrossRef
53.
Schoepf KC, Kapaga AM, Msami HM, Hyera JM. Serological evidence of the occurrence of enzootic bovine leukosis (EBL) virus infection in cattle in Tanzania. Trop Anim Health Prod. 1997;29:15–9.PubMedCrossRef
54.
Levy D, Deshayes L, Parodi AL, Levy JP, Stephenson JR, Devare SG, Gilden RV. Bovine leukemia virus specific antibodies among French cattle. II. Radioimmunoassay with the major structural protein (BLV p24). Int J Cancer. 1977;20:543–50.PubMedCrossRef
55.
Naif HM, Brandon RB, Daniel RCW, Lavin MF. Bovine leukemia Proviral DNA detection in cattle using the polymerase chain-reaction. Vet Microbiol. 1990;25:117–29.PubMedCrossRef
56.
Burridge MJ, Thurmond MC, Miller JM, Schmerr MJ, Van Der Maaten MJ. Fall in antibody titer to bovine leukemia virus in the periparturient period. Can J Comp Med. 1982;46:270–1.PubMedPubMedCentral
57.
Nguyen VK, Maes RF. Evaluation of an enzyme-linked immunosorbent assay for detection of antibodies to bovine leukemia virus in serum and milk. J Clin Microbiol. 1993;31:979–81.PubMedPubMedCentral
58.
Ohshima K, Morimoto N, Kagawa Y, Numakunai S, Hirano T, Kayano HA. Survey for maternal antibodies to bovine leukemia virus (BLV) in calves born to cows infected with BLV. Nihon Juigaku Zasshi. 1984;46:583–6.PubMedCrossRef
59.
Kettmann R, Meunier-Rotival M, Cortadas J, Cuny G, Ghysdael J, Mammerickx M, Burny A, Bernardi G. Integration of bovine leukemia virus DNA in the bovine genome. Proc Natl Acad Sci U S A. 1979;76:4822–6.PubMedPubMedCentralCrossRef
60.
Kettmann R, Deschamps J, Cleuter Y, Couez D, Burny A, Marbaix G. Leukemogenesis by bovine leukemia virus: proviral DNA integration and lack of RNA expression of viral long terminal repeat and 3′ proximate cellular sequences. Proc Natl Acad Sci U S A. 1982;79:2465–9.PubMedPubMedCentralCrossRef
61.
Tajima S, Tsukamoto M, Aida Y. Latency of viral expression in vivo is not related to CpG methylation in the U3 region and part of the R region of the long terminal repeat of bovine leukemia virus. J Virol. 2003;77:4423–30.PubMedPubMedCentralCrossRef
62.
Tajima S, Aida Y. Induction of expression of bovine leukemia virus (BLV) in blood taken from BLV-infected cows without removal of plasma. Microbes Infect. 2005;7:1211–6.PubMedCrossRef
63.
Kettmann R, Cleuter Y, Mammerickx M, Meunier-Rotival M, Bernardi G, Burny A, Chantrenne H. Genomic integration of bovine leukemia provirus: comparison of persistent lymphocytosis with lymph node tumor form of enzootic. Proc Natl Acad Sci U S A. 1980;77:2577–81.PubMedPubMedCentralCrossRef
64.
Tajima S, Ikawa Y, Aida Y. Complete bovine leukemia virus (BLV) provirus is conserved in BLV-infected cattle throughout the course of B-cell lymphosarcoma development. J Virol. 1998;72:7569–76.PubMedPubMedCentral
65.
Burny A, Cleuter Y, Kettmann R, Mammerickx M, Marbaix G, Portetelle D, Vandenbroeke A, Willems L, Thomas R. Bovine leukemia - facts and hypotheses derived from the study of an infectious cancer. Vet Microbiol. 1988;17:197–218.PubMedCrossRef
66.
Brym P, Rusc A, Kaminski S. Evaluation of reference genes for qRT-PCR gene expression studies in whole blood samples from healthy and leukemia-virus infected cattle. Vet Immunol Immunopathol. 2013;153:302–7.PubMedCrossRef
67.
Tawfeeq MM, Horiuchi N, Kobayashi Y, Furuoka H, Inokuma H. Evaluation of gene expression in peripheral blood cells as a potential biomarker for enzootic bovine Leukosis. J Vet Med Sci. 2013;75:1213–7.PubMedCrossRef
68.
Somura Y, Sugiyama E, Fujikawa H, Murakami K. Comparison of the copy numbers of bovine leukemia virus in the lymph nodes of cattle with enzootic bovine leukosis and cattle with latent infection. Arch Virol. 2014;159:2693–7.PubMedCrossRef
69.
Lew AE, Bock RE, Miles J, Cuttell LB, Steer P, Nadin-Davis SA. Sensitive and specific detection of bovine immunodeficiency virus and bovine syncytial virus by 5’Taq nuclease assays with fluorescent 3’minor groove binder-DNA probes. J Virol Methods. 2004;116:1–9.PubMedCrossRef
70.
Jimba M, Takeshima SN, Matoba K, Endoh D, Aida Y. BLV-CoCoMo-qPCR: Quantitation of bovine leukemia virus proviral load using the CoCoMo algorithm. Retrovirology. 2010;7:91.PubMedPubMedCentralCrossRef
71.
Takeshima SN, Kitamura-Muramatsu Y, Yuan Y, Polat M, Saito S, Aida Y. BLV-CoCoMo-qPCR-2: improvements to the BLV-CoCoMo-qPCR assay for bovine leukemia virus by reducing primer degeneracy and constructing an optimal standard curve. Arch Virol. 2015;160:1325–32.PubMedCrossRef
72.
Nishimori A, Konnai S, Ikebuchi R, Okagawa T, Nakahara A, Murata S, Ohashi K. Direct polymerase chain reaction from blood and tissue samples for rapid diagnosis of bovine leukemia virus infection. J Vet Med Sci. 2016;78:791–6.PubMedPubMedCentralCrossRef
73.
Takeshima SN, Watanuki S, Ishizaki H, Matoba K, Aida Y. Development of a direct blood-based PCR system to detect BLV provirus using CoCoMo primers. Arch Virol. 2016;161:1539–46.PubMedCrossRef
74.
Polat M, Ohno A, Takeshima SN, Kim J, Kikuya M, Matsumoto Y, Mingala CN, Onuma M, Aida Y. Detection and molecular characterization of bovine leukemia virus in Philippine cattle. Arch Virol. 2015;160:285–96.PubMedCrossRef
75.
Polat M, Takeshima SN, Hosomichi K, Kim J, Miyasaka T, Yamada K, Arainga M, Murakami T, Matsumoto Y, de la Barra Diaz V, et al. A new genotype of bovine leukemia virus in South America identified by NGS-based whole genome sequencing and molecular evolutionary genetic analysis. Retrovirology. 2016;13:4.PubMedPubMedCentralCrossRef
76.
Polat M, Moe HH, Shimogiri T, Moe KK, Takeshima SN, Aida Y. The molecular epidemiological study of bovine leukemia virus infection in Myanmar cattle. Arch Virol. 2016.
77.
Ochirkhuu N, Konnai S, Odbileg R, Nishimori A, Okagawa T, Murata S, Ohashi K. Detection of bovine leukemia virus and identification of its genotype in Mongolian cattle. Arch Virol. 2016;161:985–91.PubMedCrossRef
78.
Dus Santos MJ, Trono K, Lager I, Wigdorovitz A. Development of a PCR to diagnose BLV genome in frozen semen samples. Vet Microbiol. 2007;119:10–8.PubMedCrossRef
79.
Martin D, Arjona A, Soto I, Barquero N, Viana M, Gomez-Lucia E. Comparative study of PCR as a direct assay and ELISA and AGID as indirect assays for the detection of bovine leukaemia virus. J Vet Med B Infect Dis Vet Public Health. 2001;48:97–106.PubMedCrossRef
80.
Heenemann K, Lapp S, Teifke JP, Fichtner D, Mettenleiter TC, Vahlenkamp TW. Development of a bovine leukemia virus polymerase gene-based real-time polymerase chain reaction and comparison with an envelope gene-based assay. J Vet Diagn Investig. 2012;24:649–55.CrossRef
81.
Kelly EJ, Jackson MK, Marsolais G, Morrey JD, Callan RJ. Early detection of bovine leukemia virus in cattle by use of the polymerase chain reaction. Am J Vet Res. 1993;54:205–9.PubMed
82.
Miyasaka T, Takeshima SN, Jimba M, Matsumoto Y, Kobayashi N, Matsuhashi T, Sentsui H, Aida Y. Identification of bovine leukocyte antigen class II haplotypes associated with variations in bovine leukemia virus proviral load in Japanese black cattle. Tissue Antigens. 2013;81:72–82.PubMedCrossRef
83.
Ohno A, Takeshima SN, Matsumoto Y, Aida Y. Risk factors associated with increased bovine leukemia virus proviral load in infected cattle in Japan from 2012 to 2014. Virus Res. 2015;210:283–90.PubMedCrossRef
84.
Yuan Y, Kitamura-Muramatsu Y, Saito S, Ishizaki H, Nakano M, Haga S, Matoba K, Ohno A, Murakami H, Takeshima SN, Aida Y. Detection of the BLV provirus from nasal secretion and saliva samples using BLV-CoCoMo-qPCR-2: comparison with blood samples from the same cattle. Virus Res. 2015;210:248–54.PubMedCrossRef
85.
Inabe K, Ikuta K, Aida Y. Transmission and propagation in cell culture of virus produced by cells transfected with an infectious molecular clone of bovine leukemia virus. Virology. 1998;245:53–64.PubMedCrossRef
86.
Mamoun RZ, Morisson M, Rebeyrotte N, Busetta B, Couez D, Kettmann R, Hospital M, Guillemain B. Sequence variability of bovine leukemia virus env gene and its relevance to the structure and antigenicity of the glycoproteins. J Virol. 1990;64:4180–8.PubMedPubMedCentral
87.
Portetelle D, Couez D, Bruck C, Kettmann R, Mammerickx M, Van der Maaten M, Brasseur R, Burny A. Antigenic variants of bovine leukemia virus (BLV) are defined by amino acid substitutions in the NH2 part of the envelope glycoprotein gp51. Virology 1989; 169:27-33.
88.
Bruck C, Mathot S, Portetelle D, Berte C, Franssen JD, Herion P, Burny A. Monoclonal antibodies define eight independent antigenic regions on the bovine leukemia virus (BLV) envelope glycoprotein gp51. Virology. 1982;122:342–52.PubMedCrossRef
89.
Kettmann R, Couez D, Burny A. Restriction endonuclease mapping of linear unintegrated proviral DNA of bovine leukemia virus. J Virol. 1981;38:27–33.PubMedPubMedCentral
90.
Coulston J, Naif H, Brandon R, Kumar S, Khan S, Daniel RC, Lavin MF. Molecular cloning and sequencing of an Australian isolate of proviral bovine leukaemia virus DNA: comparison with other isolates. J Gen Virol. 1990;71:1737–46.PubMedCrossRef
91.
Fechner H, Blankenstein P, Looman AC, Elwert J, Geue L, Albrecht C, Kurg A, Beier D, Marquardt O, Ebner D. Provirus variants of the bovine leukemia virus and their relation to the serological status of naturally infected cattle. Virology. 1997;237:261–9.PubMedCrossRef
92.
Licursi M, Inoshima Y, Wu D, Yokoyama T, Gonzalez ET, Sentsui H. Genetic heterogeneity among bovine leukemia virus genotypes and its relation to humoral responses in hosts. Virus Res. 2002;86:101–10.PubMedCrossRef
93.
Licursi M, Inoshima Y, Wu D, Yokoyama T, Gonzalez ET, Sentsui H. Provirus variants of bovine leukemia virus in naturally infected cattle from Argentina and Japan. Vet Microbiol. 2003;96:17–23.PubMedCrossRef
94.
Felmer R, Munoz G, Zuniga J, Recabal M. 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. 2005;108:39–47.PubMedCrossRef
95.
Monti G, Schrijver R, Beier D. Genetic diversity and spread of bovine leukaemia virus isolates in argentine dairy cattle. Arch Virol. 2005;150:443–58.PubMedCrossRef
96.
Asfaw Y, Tsuduku S, Konishi M, Murakami K, Tsuboi T, Wu D, Sentsui H. Distribution and superinfection of bovine leukemia virus genotypes in Japan. Arch Virol. 2005;150:493–505.PubMedCrossRef
97.
Rodriguez SM, Golemba MD, Campos RH, Trono K, Jones LR. Bovine leukemia virus can be classified into seven genotypes: evidence for the existence of two novel clades. J Gen Virol. 2009;90:2788–97.PubMedCrossRef
98.
Balic D, Lojkic I, Periskic M, Bedekovic T, Jungic A, Lemo N, Roic B, Cac Z, Barbic L, Madic J. Identification of a new genotype of bovine leukemia virus. Arch Virol. 2012;157:1281–90.PubMedCrossRef
99.
Matsumura K, Inoue E, Osawa Y, Okazaki K. Molecular epidemiology of bovine leukemia virus associated with enzootic bovine leukosis in Japan. Virus Res. 2011;155:343–8.PubMedCrossRef
100.
Rola-Luszczak M, Pluta A, Olech M, Donnik I, Petropavlovskiy M, Gerilovych A, Vinogradova I, Choudhury B, Kuzmak J. The molecular characterization of bovine leukaemia virus isolates from Eastern Europe and Siberia and its impact on phylogeny. PLoS One. 2013;8:e58705.PubMedPubMedCentralCrossRef
101.
Lee E, Kim EJ, Joung HK, Kim BH, Song JY, Cho IS, Lee KK, Shin YK. Sequencing and phylogenetic analysis of the gp51 gene from Korean bovine leukemia virus isolates. Virol J. 2015;12:64.PubMedPubMedCentralCrossRef
102.
Lee E, Kim EJ, Ratthanophart J, Vitoonpong R, Kim BH, Cho IS, Song JY, Lee KK, Shin YK. Molecular epidemiological and serological studies of bovine leukemia virus (BLV) infection in Thailand cattle. Infect Genet Evol. 2016;41:245–54.PubMedCrossRef
103.
OIE. World animal health infromation database-version: 1.4. Paris France: World organisation for animal Health; 2009.
104.
Nuotio L, Rusanen H, Sihvonen L, Neuvonen E. Eradication of enzootic bovine leukosis from Finland. Prev Vet Med. 2003;59:43–9.PubMedCrossRef
105.
Acaite J, Tamosiunas V, Lukauskas K, Milius J, Pieskus J. The eradication experience of enzootic bovine leukosis from Lithuania. Prev Vet Med. 2007;82:83–9.PubMedCrossRef
106.
Kautzsch S, Schluter H. Prognosis and economic-aspects relating to control of enzootic bovine Leukosis. Monatsh Veterinarmed 1990; 45:41-45.
107.
Maresca C, Costarelli S, Dettori A, Felici A, Iscaro C, Feliziani F. Enzootic bovine leukosis: report of eradication and surveillance measures in Italy over an 8-year period (2005-2012). Prev Vet Med. 2015;119:222–6.PubMedCrossRef
108.
Gottschau A, Willeberg P, Franti CE, Flensburg JC. The effect of a control program for enzootic bovine leukosis. Changes in herd prevalence in Denmark, 1969-1978. Am J Epidemiol. 1990;131:356–64.PubMedCrossRef
109.
110.
EFSA Panel on Animal Health and Welfare, More SJ, Bøtner A, Butterworth A, Calistri P, Depner K, Bicout D. Assessment of listing and categorisation of animal diseases within the framework of the Animal Health Law (Regulation (EU) No 2016/429): enzootic bovine leukosis (EBL). EFSA J. 2017;15(8):1–28.
111.
Zhao XR, Jimenez C, Sentsui H, Buehring GC. Sequence polymorphisms in the long terminal repeat of bovine leukemia virus: evidence for selection pressures in regulatory sequences. Virus Res 2007; 124:113–124.
112.
Sandev N, Illieva D, Rusenova N, Marasheva V. Prevalence of enzootic Bobivne Leukosis in Bulgaria. Bulletin UASVM Veterinary Medicine. 2015;72:43–6.
113.
European Panal on Animal Health and Welfare (EPAHW). Scientific opinion on enzootic bovine leukosis. EFSA J. 2015;13:63.
114.
Chethanond U-S. The epidemiology of enzootic bovine leukosis in diary cattle in New Zealand. Massey University; 1999.
115.
APHIS. Bovine Leukosis Virus (BLV) on U.S.Dairy Operations, 2007. United states department of agriculture; 2008.
116.
VanLeeuwen JA, Keefe GP, Tremblay R, Power C, Wichtel JJ. Seroprevalence of infection with Mycobacterium Avium subspecies paratuberculosis, bovine leukemia virus, and bovine viral diarrhea virus in maritime Canada dairy cattle. Can Vet J. 2001;42:193–8.PubMedPubMedCentral
117.
VanLeeuwen JA, Forsythe L, Tiwari A, Chartier R. Seroprevalence of antibodies against bovine leukemia virus, bovine viral diarrhea virus, Mycobacterium Avium subspecies paratuberculosis, and Neospora caninum in dairy cattle in Saskatchewan. Can Vet J. 2005;46:56–8.PubMedPubMedCentral
118.
Nekouei OA. Study of prevalence, risk factors, and lifetime impacts of infection with bovine keukemia virus in the Canadian dairy industry. University of Prince Edward Island, Atlanti veterinary college, department of. Health Management. 2015;
119.
Suzan VM, Onuma M, Aguilar RE, Murakami Y. Prevalence of bovine Herpesvirus-1, Para-Influenza-3, bovine rotavirus, bovine viral diarrhea, bovine Adenovirus-7, bovine leukemia-virus and bluetongue virus-antibodies in cattle in Mexico. Jap J Vet Res. 1983;31:125–32.
120.
Samara SI, Lima EG, Nascimento AA. Monitoring of enzootic bovine leukosis in dairy cattle from the Pitangueiras region in São Paulo, Brazil. Braz J Vet Res Anim Sci. 1997;34:349–51.CrossRef
121.
D'Angelino JL, Garcia M, Birgel EH. Epidemiological study of enzootic bovine leukosis in Brazil. Trop Anim Health Prod. 1998;30:13–5.PubMedCrossRef
122.
Camargos MF, Stancek D, Rocha MA, Lessa LM, Reis JK, Leite RC. Partial sequencing of env gene of bovine leukaemia virus from Brazilian samples and phylogenetic analysis. J Vet Med B Infect Dis Vet Public Health. 2002;49:325–31.PubMedCrossRef
123.
Camargos MF, Pereda A, Stancek D, Rocha MA, dos Reis JK, Greiser-Wilke I, Leite RC. Molecular characterization of the env gene from Brazilian field isolates of bovine leukemia virus. Virus Genes. 2007;34:343–50.PubMedCrossRef
124.
Trono KG, Perez-Filgueira DM, Duffy S, Borca MV, Carrillo C. Seroprevalence of bovine leukemia virus in dairy cattle in Argentina: comparison of sensitivity and specificity of different detection methods. Vet Microbiol. 2001;83:235–48.PubMedCrossRef
125.
Bovine CAH. Leukaemia virus infection in Peru. Trop Anim Health Prod. 1983;15:61.CrossRef
126.
Marín C, de López NM, Alvarez L, Lozano O, España W, Castaños H, León A. Epidemiology of bovine leukemia in Venezuela. Ann Rech Vet. 1978;9:4.
127.
Moratorio G, Obal G, Dubra A, Correa A, Bianchi S, Buschiazzo A, Cristina J, Pritsch O. Phylogenetic analysis of bovine leukemia viruses isolated in South America reveals diversification in seven distinct genotypes. Arch Virol. 2010;155:481–9.PubMedCrossRef
128.
Rama G, Moratorio G, Greif G, Obal G, Bianchi S, Tomé L, Carrion F, Meikle A, Pritsch O. Development of a real time PCR assay using SYBR Green chemistry for bovine leukemia virus detection. Retrovirology. 2011: 8.
129.
Alfonso R, Almansa JE, Barrera JD. Serological prevalence and evaluation of risk factors of enzootic bovine leukosis in the Sabana de Bogota region and the Ubate and Chiquinquira valleys of Colombia. Revue Scientifique Et Technique De L Office International Des Epizooties. 1998;17:723–32.CrossRef
130.
Hernández-Herrera DY, Posso-Terranova A, Benavides J, Muñoz-Flórez J, Giovambattista G, Álvarez-Franco L. Bovine leukosis virus detection in Creole Colombian breeds using nested-PCR. ACTA AGRONÓMICA. 2011;60:311–7.
131.
Benavides B, Quevedo D, Cruz M. Epidemiological study of bovine leukemia virus in dairy cows in six herds in the municipality of Pasto Nariño. Revista Lasallista de Investigación. 2013;10:18–26.
132.
Yang Y, Fan W, Mao Y, Yang Z, Lu G, Zhang R, Zhang H, Szeto C, Wang C. Bovine leukemia virus infection in cattle of China: association with reduced milk production and increased somatic cell score. J Dairy Sci. 2016;99:3688–97.PubMedCrossRef
133.
Ma JG, Zheng WB, Zhou DH, Qin SY, Yin MY, Zhu XQ, Hu GX. First Report of Bovine Leukemia Virus Infection in Yaks (Bos mutus) in China. Biomed Res Int. 2016:9170167.
134.
Kobayashi S, Tsutsui T, Yamamoto T, Hayama Y, Kameyama K, Konishi M, Murakami K. Risk factors associated with within-herd transmission of bovine leukemia virus on dairy farms in Japan. BMC Vet Res. 2010;6:1.PubMedPubMedCentralCrossRef
135.
Murakami K, Kobayashi S, Konishi M, Kameyama K, Yamamoto T, Tsutsui T. The recent prevalence of bovine leukemia virus (BLV) infection among Japanese cattle. Vet Microbiol. 2011;148:84–8.PubMedCrossRef
136.
Murakami K, Kobayashi S, Konishi M, Kameyama K, Tsutsui T. Nationwide survey of bovine leukemia virus infection among dairy and beef breeding cattle in Japan from 2009-2011. J Vet Med Sci. 2013;75:1123–6.PubMedCrossRef
137.
Meas S, Ohashi K, Tum S, Chhin M, Te K, Miura K, Sugimoto C, Onuma M. Seroprevalence of bovine immunodeficiency virus and bovine leukemia virus in draught animals in Cambodia. J Vet Med Sci. 2000;62:779–81.PubMedCrossRef
138.
Nekoei S, Hafshejani TT, Doosti A, Khamesipour F. Molecular detection of bovine leukemia virus in peripheral blood of Iranian cattle, camel and sheep. Pol J Vet Sci. 2015;18:703–7.PubMed
139.
Mousavi S, Haghparast A, Mohammadi G, Tabatabaeizadeh SE. Prevalence of bovine leukemia virus (BLV) infection in the northeast of Iran. Vet Res Forum. 2014;5:135–9.PubMedPubMedCentral
140.
Trainin Z, Brenner J. The direct and indirect economic impacts of bovine leukemia virus infection on dairy cattle. Israel Journal of Veterinary Medicine. 2005;60:90–105.
141.
Hafez SM, Sharif M, Al-Sukayran A, Dela-Cruz D. Preliminary studies on enzootic bovine leukosis in Saudi dairy farms. Dtsch Tierarztl Wochenschr. 1990;97:61–3.PubMed
142.
Burgu I, Alkan F, Karaoglu T, Bilge-Dagalp S, Can-Sahna K, Gungor B, Demir B. Control and eradication programme of enzootic bovine leucosis (EBL) from selected dairy herds in Turkey. Dtsch Tierarztl Wochenschr. 2005;112:271–4.PubMed
143.
Zhao X, Buehring GC. Natural genetic variations in bovine leukemia virus envelope gene: possible effects of selection and escape. Virology. 2007;366:150–65.PubMedCrossRef
144.
Molteni E, Agresti A, Meneveri R, Marozzi A, Malcovati M, Bonizzi L, Poli G, Ginelli E. Molecular characterization of a variant of proviral bovine leukaemia virus (BLV). Zentralbl Veterinarmed B. 1996;43:201–11.PubMedCrossRef
145.
Derse D, Diniak AJ, Casey JW, Deininger PL. Nucleotide sequence and structure of integrated bovine leukemia virus long terminal repeats. Virology. 1985;141:162–6.PubMedCrossRef
146.
Yang Y, Kelly PJ, Bai J, Zhang R, Wang C. First molecular characterization of bovine leukemia virus infections in the Caribbean. PLoS One. 2016;11:e0168379.PubMedPubMedCentralCrossRef
147.
Dube S, Dolcini G, Abbott L, Mehta S, Dube D, Gutierrez S, Ceriani C, Esteban E, Ferrer J, Poiesz B. The complete genomic sequence of a BLV strain from a Holstein cow from Argentina. Virology. 2000;277:379–86.PubMedCrossRef
148.
Dube S, Abbott L, Dube DK, Dolcini G, Gutierrez S, Ceriani C, Juliarena M, Ferrer J, Perzova R, Poiesz BJ. The complete genomic sequence of an in vivo low replicating BLV strain. Virol J. 2009;6:120.PubMedPubMedCentralCrossRef
149.
Lim SI, Jeong W, Tark DS, Yang DK, Kweon CH. Agar gel immunodiffusion analysis using baculovirus-expressed recombinant bovine leukemia virus envelope glycoprotein (gp51/gp30(T-)). J Vet Sci. 2009;10:331–6.PubMedPubMedCentralCrossRef
150.
Inoue E, Matsumura K, Maekawa K, Nagatsuka K, Nobuta M, Hirata M, Minagawa A, Osawa Y, Okazaki K. Genetic heterogeneity among bovine leukemia viruses in Japan and their relationship to leukemogenicity. Arch Virol. 2011;156:1137–41.PubMedCrossRef
151.
Ababneh MM, Al-Rukibat RK, Hananeh WM, Nasar AT, Al-Zghoul MB. Detection and molecular characterization of bovine leukemia viruses from Jordan. Arch Virol. 2012;157:2343–8.PubMedCrossRef
152.
Rodriguez SM, Florins A, Gillet N, de Brogniez A, Sanchez-Alcaraz MT, Boxus M, Boulanger F, Gutierrez G, Trono K, Alvarez I, et al. Preventive and therapeutic strategies for bovine leukemia virus: lessons for HTLV. Viruses. 2011;3:1210–48.PubMedPubMedCentralCrossRef
153.
Inoue E, Matsumura K, Soma N, Hirasawa S, Wakimoto M, Arakaki Y, Yoshida T, Osawa Y, Okazaki K. L233P mutation of the tax protein strongly correlated with leukemogenicity of bovine leukemia virus. Vet Microbiol. 2013;167:364–71.PubMedCrossRef
154.
Murakami H, Asano S, Uchiyama J, Sato R, Sakaguchi M, Tsukamoto K. Bovine leukemia virus G4 enhances virus production. Virus Res. 2017;238:213–7.PubMedCrossRef
Metadata
Title
Epidemiology and genetic diversity of bovine leukemia virus
Authors
Meripet Polat
Shin-nosuke Takeshima
Yoko Aida
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2017
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-017-0876-4

Other articles of this Issue 1/2017

Virology Journal 1/2017 Go to the issue

Research

The genetic structure of Turnip mosaic virus population reveals the rapid expansion of a new emergent lineage in China

Research

Lytic viral replication and immunopathology in a cytomegalovirus-induced mouse model of secondary hemophagocytic lymphohistiocytosis

Research

Detection and epidemic dynamic of ToCV and CCYV with Bemisia tabaci and weed in Hainan of China

Review

Bacteriophage therapy to combat bacterial infections in poultry

Short report

Prevalence of plasma autoantibody against cancer testis antigen NY-ESO-1 in HTLV-1 infected individuals with different clinical status

Research

Cyclophilin B facilitates the replication of Orf virus
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits