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Epidemiology and Genetic Diversity of Bovine Leukemia Virus Meripet Polat1,2, Shin-Nosuke Takeshima1,2,3 and Yoko Aida1,2,3*

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Epidemiology and Genetic Diversity of Bovine Leukemia Virus Meripet Polat1,2, Shin-Nosuke Takeshima1,2,3 and Yoko Aida1,2,3* Polat et al. Virology Journal (2017) 14:209 DOI 10.1186/s12985-017-0876-4 REVIEW Open Access Epidemiology and genetic diversity of bovine leukemia virus Meripet Polat1,2, Shin-nosuke Takeshima1,2,3 and Yoko Aida1,2,3* 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 informationontheprevalenceofBLVincattleworldwideispresented. 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. Keywords: Bovine leukemia virus (BLV), BLV diagnostic approches, BLV genotyping methods, BLV epidemiology Background clinically normal cattle, CD5+ IgM+ B-cells were Bovine leukemia virus (BLV) is a retrovirus, an increased [11], and there is substantial evidence suggest- oncogenic member of the Deltaretrovirus genus, and the ing that BLV-infected but clinically normal cattle may causative agent of enzootic bovine leukosis (EBL) [1, 2]. exhibit a degree of immunological dysregulation leading The Deltaretrovirus genus also includes human T-cell to economic losses for various reasons including lymphotropic virus types I and II (HTLV-I and -II) and reduced milk production [13], a high incidence of infec- simian T-cell lymphotropic virus (STLV) [3, 4]. EBL is a tious disease [14], and reproductive inefficiency [15]. Ap- contagious lymphoproliferative disease of cattle, charac- proximately one-third of infected cattle develop a benign terized by B-cell lymphosarcoma, which occurs through- form of non-malignant proliferation of untransformed out the world [2, 5]. Although BLV can infect various B-lymphocytes, termed persistent lymphocytosis (PL). immune cell populations, including CD5+ IgM+ and PL is typically characterized by a permanent and stable − CD5 IgM+ B-cells; CD2+, CD3+, CD4+, CD8+, and γ/δ increase in the number of CD5+ IgM+ B-cells circulating T-cells; monocytes; and granulocytes in peripheral in the peripheral blood. Less than 5% of infected cattle blood and lymphoid tissues of cattle [6–11], BLV- develop malignant B-cell lymphoma originating from induced tumors usually arise from the CD5+ IgM+ B- mono- or oligo-clonal accumulation of CD5+ IgM+ B- cell subpopulation [12]. cells after a relatively long period of latency. This malig- BLV infection can result in a variety of clinical out- nant form of B-cell lymphoma is predominantly detected comes [2]. The majority of BLV-infected cattle are in cattle over 4–5 years old [16]. Such malignancies asymptomatic carriers of the virus, neither showing any induce disruption of the spleen and remarkable enlarge- clinical signs nor any changes in lymphocyte count; ment of the lymph nodes, which can be visible under however, a recent study showed that although lympho- the skin. BLV-induced neoplastic cells can penetrate into cyte counts were not elevated in BLV-infected but the abomasums, right auricle of the heart, intestine, kid- ney, lung, liver, and uterus. The clinical signs of BLV- * Correspondence: [email protected] induced tumors are varied and primarily involve digestive 1 Viral Infectious Diseases Unit, RIKEN, 2-1 Hirosawa, Wako, Saitama 351-0198, disturbance, weight loss, weakness, reduced milk produc- Japan 2Nano Medical Engineering Laboratory, RIKEN, 2-1 Hirosawa, Wako, Saitama tion, loss of appetite, and enlarged lymph nodes [17]. 351-0198, Japan Full list of author information is available at the end of the article © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Polat et al. Virology Journal (2017) 14:209 Page 2 of 16 BLV genome structure preleukemic and malignant cells, and may have roles in The BLV genome consists of 8714 nucleotides (nt) [18] tumor onset and progression [39, 40] through their including essential structural protein and enzyme coding effects on proviral load and consequently viral replica- genes and a pX region, flanked by two identical long ter- tion in the natural host [41]. Besides, Van Driessche et minal repeats (LTRs) (Fig. 1a). The structural protein al. revealed the recruitment of positive epigenetic marks and enzyme coding genes, namely, gag, pro, pol, and env, on BLV miRNA cluster, inducing strong antisense pro- have essential and indispensable roles in the viral life- moter activity [42]. They also identified cis-acting cycle, viral infectivity, and the production of infectious elements of an RNAPII-dependent promoter [42]. virions [19–24]. The gag gene of BLV is translated as the precursor, Pr45 Gag, and processed to generate three BLV diagnosis mature proteins [19, 23]: the matrix protein, p15, which A variety of techniques have been developed for diagno- binds viral genomic RNA and interacts with the lipid bi- sis of BLV and implemented worldwide. These diagnostic layer of the viral membrane [25]; the capsid protein, methods can be assigned into two main groups, consist- p24, which is the major target of the host immune ing of antibody-based serological tests and detection of response, with high antibody titers against this molecule the proviral genome by nucleic acid-based polymerase found in the serum of infected animals [26, 27]; and the chain reaction (PCR) assays (summarized in Table 1). nucleocapsid protein, p12, which binds to packaged gen- omic RNA [28] (Fig. 1b). The env gene encodes the ma- Serological tests ture extracellular protein, gp51, and a transmembrane For indirect BLV diagnostic methods, particularly protein, gp30 [19]. The pX region, which is located be- antibody-based tests, antibodies recognizing the p24 capsid tween env and the 3′ LTR [2], encodes the regulatory protein encoded by the gag gene and the extracellular gp51 proteins Tax and Rex, and the accessory proteins R3 and protein encoded by env-gp51 are targeted. This is because G4 (Fig. 1a). The regulatory proteins are important for antibodies against these proteins are produced shortly after regulation of viral transcription, transformation of BLV- BLV infection, can be detected 2–3 weeks post-infection, induced leukemogenesis, and nuclear export of viral and remain detectable for the life of the host animal [43]. RNA into the cytoplasm [29–36]. The R3 and G4 In addition, the p24 capsid protein is a major target for accessory proteins contribute to the maintenance of high host immune responses, inducing high antibody titers [44], viral loads [37, 38]. In addition to the genes described and gp51 invokes the expression of massive amounts of above, the BLV genome also contains RNA polymerase- specific antibodies in infected animals [24, 45, 46]. There- III-encoded viral microRNAs (miRNAs) between the env fore, antibodies against these proteins are targeted for BLV and pX regions. Viral miRNAs are strongly expressed in diagnostics using conventional serological techniques such Fig. 1 Schematic representations of the BLV genome structure (a) and viral particle (b). The structural and enzymatic genes, gag, pro, pol,andenv; regulatory genes, tax and rex; accessory genes R3 and G4; and microRNA (miRNA) are indicated in (a). Proteins encoded by structural and enzymatic genes, including the Env glycoproteins (gp51 and gp30) encoded by the env gene, the Gag proteins (p12, p24, and p15) encoded by the gag gene, reverse transcriptase and integrase (RT-IN) encoded by the pol gene, and protease (Pro) encoded by the pro gene are indicated in (b) Polat et al. Virology Journal (2017) 14:209 Page 3 of 16 Table 1 Summary of common techniques used for diagnosis of BLV prevalence Diagnostic assay Sample Target Advantages Disadvantages References Type Assay Serological AGID Serum Antibodies Specific, simple, and easy to perform Less sensitive and inconclusive Aida et al., 1989 test (p24, gp51) Large scale screening Less expensive Cannot evaluate disease states [47] Rapid of infected cattle Wang et al., 1991 [48] Monti et al., 2005 [49] Kurdi et al., 1999 [50] Jimba et al., 2012 [43] Naif et al., 1990 [55] ELISA Serum Milk Antibodies Specific and sensitive Large scale False negatives (cattle in early Naif et al., 1990 Bulk milk (p24, gp51) screening Time saving infection phase) False positive [55] (maternally derived antibodies) Cannot evaluate disease states of Burridge et al., infected cattle A number of 1982 [56] controls and a plate reader required Schoepf et al., Results require interpretation 1997 [53] Kurdi et al., 1999 [50] Monti et al., 2005 [49] Jimba et al., 2012 [43] Zaghawa et al., 2002 [52] PHA Virus particle
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