NOTE Virology Molecular characterization of bovine foamy and its association with infection in Vietnamese cattle

Dung Thi LE1)#, Son Vu NGUYEN2,3)#, Mari OKAMOTO1), Nanako YAMASHITA-KAWANISHI1), Tung Duy DAO4,5), Vuong Nghia BUI4,5), Haruko OGAWA4), Kunitoshi IMAI4) and Takeshi HAGA1)*

1)Division of Infection Control and Disease Prevention, Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan 2)Department of Veterinary Pathology, Faculty of Veterinary Medicine, Vietnam National University of Agriculture, Hanoi 100000, Vietnam 3)Laboratory of Veterinary Pathology, Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan 4)Department of Veterinary Medicine, Obihiro University of Agriculture and Veterinary Medicine, 2-11 Inada, Obihiro, Hokkaido 080-8555, Japan 5)National Institute of Veterinary Research, 86 Truong Chinh, Dong Da, Hanoi 100000, Vietnam

ABSTRACT. The detection of (BFV) in Vietnamese cattle was performed using J. Vet. Med. Sci. conventional PCR targeting pol and gag genes. Out of 243 tested samples, ten (4.1%) and eight (3.3%) samples were positive for BFV gag and pol DNA, respectively. The prevalence of bovine 83(8): 1273–1277, 2021 leukemia virus (BLV) estimated by detection of proviral DNA using nested PCR targeting env gene doi: 10.1292/jvms.21-0190 was 26.7% (65/243). The results of nucleotide sequence alignment and the phylogenetic analysis suggested that Vietnamese BFV strains showed high homology to isolates belonging to either European or non-European clades. There was no significant correlation between BLV and BFV. This Received: 27 March 2021 study provides information regarding BFV infection and confirms the existence of two BFV clades Accepted: 10 June 2021 among Vietnamese cattle for the first time. Advanced Epub: KEY WORDS: bovine foamy virus (BFV), bovine leukemia virus (BLV), cattle, Vietnam 28 June 2021

Foamy (FVs) belong to the subfamily within the family Retroviridae. FVs are ubiquitous in a wide range of mammals, including nonhuman primates (Simian FV, or SFV), chimpanzees (Prototype FV, or PFV), bats (Chiropteran FV, or CFV), cats (feline FV, or FFV), horses (equine FV, or EFV), and cattle (bovine FV, or BFV). In their natural hosts, they establish a lifelong, persistent infection [21, 28]. Although FVs have been known to cause a pronounced cytopathic effect in many tissue culture cells in vitro [21, 31], these viruses have not been shown to be associated to a defined disease with obvious clinical signs. However, the pathogenic potential of FVs was suggested. A previous study demonstrated the transient depression of the cell- mediated immune response occurred in rabbits infected by SFV [10]. Another study showed that chronic progressive polyarthritis of cats has been associated with FFV [24]. In humans, among patients with subacute granulomatous thyroiditis (de Quervain) and autoimmune hyperthyroidism (Grave’s disease), PFV was commonly found [17, 32]. Besides, mice transgenic expressing the partial or complete genome of PFV were shown to develop progressive encephalopathy and myopathy [1, 4]. BFV was first isolated from lymphosarcomatous and apparently healthy cattle in 1969 [19]. Subsequently, BFV infection was confirmed in livestock cattle in different parts of the world [2, 3, 5, 11, 12, 14, 20, 23, 27, 33]. Moreover, the previous studies showed the concomitant infection of BFV with either bovine leukemia virus (BLV) or bovine immunodeficiency virus, and suggested the presence of BFV in the host may contribute to diseases caused by other pathogens [2, 12, 13]. The BFV genome is composed of gag, pol, and env structural genes flanked by the long terminal repeats (LTRs) and additional accessory genes designated as tas and bet [26]. The previous results of phylogenetic analysis suggested that BFV could be classified into two distinct clades, the European clade and the non-European clade [7, 9, 23]. The European clade comprised the two European isolates, including BFV Reims and BFV 100, and the non-European clade comprising the BFV isolates from China, USA, and Japan [7, 9, 23].

*Correspondence to: Haga, T.: [email protected] #These authors contributed equally to this work. (Supplementary material: refer to PMC https://www.ncbi.nlm.nih.gov/pmc/journals/2350/) ©2021 The Japanese Society of Veterinary Science This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial No Derivatives (by-nc-nd) License. (CC-BY-NC-ND 4.0: https://creativecommons.org/licenses/by-nc-nd/4.0/) 1273 D. T. LE ET AL.

Although BFV has been detected worldwide, epidemiology and molecular characteristics of BFV remain to be the least analyzed among the . This study aimed to determine for the first time, the presence of BFV and its molecular characteristic in Vietnamese cattle. Additionally, we investigated the association between BFV and BLV infection. The present study will update and contribute to enriching the knowledge in the prevalence and molecular characteristics of BFV. In this study, 243 blood samples were collected from 67 beef and dairy cattle farms located in the three Vietnamese provinces, namely, Hanoi, Vinhphuc, and Bacninh, from February 2017 to June 2018. All investigated cattle did not show any symptoms at the time of sampling. Peripheral blood was obtained from the jugular vein and used for DNA extraction. The blood samples were collected following the guidelines of National technical regulation on Animal diseases–General requirements for sample collection, storage, and shipment (QCVN01-83:2011/BNNPTNT). Permission was obtained from the farm owners before collecting the samples. Total DNA was extracted from each EDTA-treated whole blood sample using QIAamp DNA Mini Kit (QIAGEN, Hilden, Germany) and High Pure PCR Template Preparation Kit (Roche Diagnostics GmbH, Mannheim, Germany) following the manufacturer’s instructions. DNA samples were used to confirm the existence of BFV proviral DNA by PCR assays targeting gag and pol genes. The partial sequence of pol and gag genes of the BFV provirus were amplified by PCR using the primer sets (Table 1). Simultaneously, we used the extracted DNA samples to screen the prevalence of BLV infection and the results were published [6, 18]. In the present study, additional primer sets suggested by Dao et al. [6] targeting to env-gp51 gene were used to confirm the results obtained in the previous studies (Table 1). Each PCR reaction mixture contained 10 µl of Buffer KOD FX Neo 2×, 4 µl of distilled water, 4 µl of dNTPs 2 mM, 0.8 µl of primers mixture, 0.4 µl of KOD FX Neo Polymerase (Toyobo, Osaka, Japan) and 0.8 µl of extracted DNA/the first round PCR product. Distilled water was used as a negative control for PCR. The thermal cycling conditions for both PCR reactions targeting BFV pol and gag genes were as follows: an initial denaturation at 94°C for 2 min; 40 cycles of denaturing at 98°C for 10 sec, annealing at 64.5°C for 30 sec, and extension at 68°C for 15 sec. The thermal cycle reactions for the first round PCR to amplify the BLV env gene were carried out in the following conditions: an initial denaturation at 94°C for 2 min; followed by 40 cycles of denaturing at 98°C for 10 sec, annealing at 57°C for 30 sec, and extension at 72°C for 1 min; an additional cycle was run at 72°C for 10 min. The reaction parameters for the second round PCR were 2 min at 94°C for initial denaturation, followed by 35 cycles consisting of denaturation at 98°C for 10 sec, annealing at 56°C for 30 sec, and extension at 72°C for 1 min; the last cycle was done at 72°C for 10 min. The amplification reactions were performed in a S1000TM Thermal Cycler (Bio Rad, Hercules, CA, USA). The PCR products were analyzed by electrophoresis on 2% agarose gel containing Gel Red (Biotium, Fremont, CA, USA). The BFV pol and gag positive PCR products were purified using NucleSpin Gel and PCR Clean up kit (Macherey-Nagel GmbH & Co., KG, Duren, Germany) following the manufacturer’s recommendations. The purified PCR products were subsequently sequenced using ABI 3730xl DNA Analyzer (Thermo Fisher Scientific, Waltham, MA, USA) and BigDye Terminator v3.1 Cycle Sequencing Kit (Thermo Fisher Scientific) in accordance with the manufacturer’s instructions. Vietnamese BFV sequences were obtained by MEGA 7.0 software [16]. The nucleotide sequences of Vietnamese strains were aligned together with BFV pol and gag sequences obtained from the GenBank of National Center for Biotechnology Information by BioEdit version 7.2.5 [8]. Phylogenetic analysis of the partial sequences of the pol and gag genes were performed using MEGA 7.0 software [16]. Phylogenetic trees were constructed using the maximum likelihood (ML) algorithm with the Kimura-2 parameter model (K2+G) of nucleotide substitution. The reliability of phylogenetic relationships was evaluated using bootstrap analysis with 1,000 replicates. The statistically significant association between BLV and BFV infection was determined by Pearson’s 2χ test. PCR test targeting BFV gag gene identified 10 out of 243 samples (4.1%) as positive, whereas PCR assay targeting pol gene identified eight (3.3%) (Table 2). Of 67 investigated herds, the existence of BFV was confirmed in ten herds (14.9%). BFV was prevalent among the cattle in the three investigated provinces. BFV-positive cattle were confirmed in seven out of 45 farms in Hanoi, in two out of 14 farms in Vinhphuc and in one out of eight farms in Bacninh. Simultaneously, BLV was detected in 65 out of 243 cattle (26.7%) in the same group of animals. The results of Pearson’s χ2 test (P>0.05) indicated that there was no significant association between BLV and BFV infections (Table 3). Selected positive samples, which were satisfied by both PCR assays targeting gag and pol gene, were further used for gene sequencing. Seven sequences of pol gene and eight sequences of the gag gene of BFV-positive samples were successfully obtained. Because some strains showed 100% identity to each other, only distinct sequences were aligned with the reference strains and included in the phylogenetic trees. The sequences of Vietnamese strains were deposited in GenBank under accession numbers LC580271 through LC580278. Subsequently, ML phylogenetic trees based on pol and gag genes were constructed under K2+G model. The result of phylogenetic analysis suggested that Vietnamese strains were high homologous to either the European or non-European clade isolates (Fig. 1A and 1B). The Vietnamese isolates, BN07 (LC580272 and LC580276), TM02-05 (LC580273 and LC580277), and VP02-25 (LC580274 and LC580278) were grouped into the same branch with BFV strains isolated in USA, Japan, and China. The Vietnamese strain P01-07 (LC580271 and LC580275) was significantly divergent from other Vietnamese strains, shown to be closer with strains named Reims (GenBank accession number: JX307862.1) and BFV 100 (GenBank accession number: JX307861.1), which were identified in Germany and Poland, respectively. By comparing the sequences of Vietnamese strains with those of the reference AY134750.1 strain, we identified 18 and 29 substitutions in our obtained pol and gag sequences, respectively (Supplementary Fig. 1 and Supplementary Fig. 2). Of 18 pol substitutions, 11 were silent substitutions, and seven were nonsynonymous. Among 29 gag substitutions, 25 were silent substitutions, and the others were nonsynonymous. The Vietnamese strains, P01-07 (LC580271), BN07 (LC580272), and VP02-25 (LC580274) exhibited six, three, and one unique substitution(s) in gag region, respectively.

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Table 1. Primer used in this study Primer name Sequence (5′–3′) Position* Target band Reference 1. Conventional PCR targeting to bovine foamy virus (BFV) gag and pol genes BFV-pol-F GGGACTCTGGGGCTGAAATC 3056–3076 386 bp BFV-pol-R CTCAATACGCCGATGTCCGA 3422–3441 This present study BFV-gag-F GGCAACCCTTGCCTATTCCT 1573–1592 559 bp BFV-gag-R TGGACCGGGTAAACACCTTG 2112–2131 2. Nested PCR targeting bovine leukemia virus (BLV) env-gp51gene BLV Outer F TCAGAGGGCGGAGAAACAC 4650–4668 1558 bp BLV Outer R GGTCAAGCATTTTATCAGG 6190–6208 Dao et al. [6] BLV Inner F TGGGTTCCCTGGCGTTT 4794–4810 1375 bp BLV Inner R AAAAAGGGCTAATAGGAACAGG 6148–6169 *Nucleotide positions according to the GenBank accession numbers AY134750.1 (BFV) and LC164086 (BLV).

Table 2. Bovine foamy virus (BFV) detection in Vietnamese cattle by PCR targeting gag and pol No. of Number of BFV-positive samples No. of BFV-postive farms Sample Location tested (by PCR targeting gag) number farms PCR targeting gag PCR targeting pol Both Hanoi 45 7 (15.6%) 166 7 (4.2%) 5 (3.0%) 5 (3.0%) Vinhphuc 14 2 (14.3%) 47 2 (4.3%) 2 (4.3%) 2 (4.3%) Bacninh 8 1 (12.5%) 30 1 (3.3%) 1 (3.3%) 1 (3.3%) Total 67 10 (14.9%) 243 10 (4.1%) 8 (3.3%) 8 (3.3%)

Table 3. Detection of bovine foamy virus (BFV) and bovine leukemia virus (BLV) among Vietnamese cattle by PCR BLV Positive Negative Total BFV Positive 3 7 10 Negative 62 171 233 Total 65 178 243 Pearson χ2 P=0.812 (OR=1.182).

In the present study, BFV detection was confirmed for the first time in the blood samples of Vietnamese cattle and the genetic variability of the Vietnamese BFV strains was demonstrated. The prevalence of BFV infection varies widely among countries [2, 3, 5, 11, 12, 14, 20, 23, 27, 33]. In the present study, out of 243 DNA samples from 67 cattle farms, only eight were positive for BFV provirus by PCR targeting to pol gene, whereas PCR targeting gag gene identified ten as positive. The difference could be caused by the sensitivity of the two primer sets. While PCR targeting to gag was able to detect one copy/µl, PCR targeting to pol gene showed lower sensitivity with a limit of detection of ten copies/µl (data not shown). The prevalence of BFV infection in Vietnamese cattle was lower than that of the ratio mentioned in other countries [2, 3, 5, 11, 12, 14, 20, 23, 27, 33]. However, the prevalence of BFV infection among countries is incomparable because the detection Fig. 1. Maximum likelihood (ML) phylogenetic trees built methods are divergent. To compare the infection prevalence of based on the nucleotide sequences of the partial BFV (bovine BFV in different areas, it would be necessary to have a standard foamy virus) pol gene (346 bp) (A) and gag gene (519 bp) (B) diagnostic method. from Vietnamese strains (indicated by filled circles/triangles) FVs establish persistent infection in susceptible animals, and and reference strains (shown by GenBank accession number, shedding of BFV can occur via various routes [21]. The extended country name, and strain name). The numbers at the branches period of infection and diverse transmission routes suggested show ML bootstrap support values. The bar at the bottom of the that BFV infection seems to become prevalent among cattle figure denotes the distance.

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populations. However, only a few cattle in the present study were found to be positive. The reason for this low prevalence in the present study remains unclear. Although a limited number of positive samples were detected, BFV infection was confirmed to be prevalent among cattle in the three provinces investigated in this study. Even though a small number of the samples examined herein were BFV-positive, we cannot exclude the risk of wider dissemination among cattle population. Pathogenicity of BFV has not been clearly demonstrated, and the previous studies suggested the presence of BFV in the host may contribute to diseases caused by other pathogens [2, 12, 13]. In the study presented here, BFV infection prevalence was lower than the observed prevalence of BLV (26.7%) in the same cattle group. We found no significant association between increased BLV detection and BFV infection. The same result was also obtained in the previous studies [11, 23]. The infection rate of BFV was found to be greater than those of BLV in the previous studies [12, 13]. In contrast, the findings in the other studies and in the present study demonstrated the lower infection rates of BFV [2, 11, 23]. Comparing to BLV, the potential for transmission from BFV positive cattle via physical contact between infected and uninfected cattle or hematophagous insects is less probable [11]. The weaker ability of transmission may contribute to the lower infection rate of BFV. The phylogenetic analysis of full-length genomic sequences from the previous study revealed two BFV clades, the European and non-European clades [7, 9, 23]. The European clade comprised the two European isolates, BFV-Riems from East Germany and BFV-100 from Poland. The non-European clade comprising the BFV isolates from China and the United States. Subsequently, the results from the recent studies suggested that most Japanese BFV isolates belonged to the non-European clade, and only one isolate was found to belong to the European clade [7, 23]. Therefore, BFV strains circulating in Asia countries primarily belonged to the non-European clade [7, 9, 23]. Interestingly, the Vietnamese strains were located on separate branches supported by bootstrap value of 100 (Fig. 1A and 1B), confirming the presence of both the non-European and the European clades in Vietnamese cattle. Considering the trade of cattle among countries, crossbreeding between native cattle and imported cattle may be the factors that caused the genetic diversification of BFV in Vietnam [22, 30]. Besides, the studies related to the molecular characterization of BFV are still limited. Hence, we hypothesized that if the greater samples are collected from different countries, more genotypes of BFV may be identified. In this study, we identified 18 and 29 substitutions in pol and gag sequences, respectively. Remarkably, each Vietnamese strain P01-07 (LC580271), BN07 (LC580272), and VP02-25 (LC580274) showed several single substitutions in gag sequences. However, the biological functions of these substitutions were unraveled. So far, studies related to phylogenetic analyses of FVs have primarily focused on the env and whole genome sequences. Besides, the partial of pol or gag sequences also were utilized [25, 29]. Following the published review, the pol and env gene sequences can be used for FVs classification [15]. A recent study indicated that BFV phylogenetic analysis based on pol sequence was consistent with the classification based on env and whole genome sequences and can be used to reflect the BFV evolutionary relationship [23]. In the present study, we did not perform sequence for env region and whole genome because of the limitation of DNA quantity and quality. However, our results of phylogenetic analyses based on both pol and gag region sequences confirmed the classification of BFV strains into two separate clades, being consistent with the previous study [7, 9, 23]. In conclusion, the present study provides evidence of the relatively low prevalence of BFV infection among Vietnamese cattle. Phylogenetic analysis based on partial pol and gag sequences revealed that Vietnamese BFV strains were closely similar to European and non-European clades isolates. The results of the present study provide additional insight into the evolution of BFV.

POTENTIAL CONFLICTS OF INTEREST. The authors have nothing to disclose.

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