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Archives of Virology

, Volume 163, Issue 3, pp 659–670 | Cite as

Molecular epidemiology and characterization of bovine leukemia virus in domestic yaks (Bos grunniens) on the Qinghai-Tibet Plateau, China

  • Meng Wang
  • Yun Wang
  • Abdul Rasheed Baloch
  • Yangyang Pan
  • Fang Xu
  • Lili Tian
  • Qiaoying Zeng
Original Article

Abstract

Bovine leukemia virus (BLV) is a member of the genus Deltaretrovirus of the family Retroviridae and cause a chronic lymphosarcoma, which is extensive in cattle. In yaks (Bos grunniens), the distribution, strains and genetic characteristics of BLV have rarely been studied. The aim of our study was to investigate BLV infections in domestic yaks and determine the genetic variability of BLV circulating in a region of the Qinghai Tibet Plateau, China. Blood samples were collected from 798 yaks, which were from different farms from Gansu, Qinghai and Sichuan provinces surrounding the Qinghai-Tibet Plateau. Nested PCR targeting BLV long terminal repeats was used to detect the BLV provirus. The highest prevalence of BLV infection was in Gansu province, where it was 18.93% (39/206) in white yaks from Tianzhu City and 19.14% (31/162) in black yaks from Gannan City. In Qinghai and Sichuan provinces, the prevalence of BLV in black yaks was 14.83% (35/236) and 14.94% (29/194), respectively. The prevalence of BLV was not significantly different in yaks up to one year old than in older animals. Phylogenetic analysis was performed using 16 different env-gp51 (497-bp) gene sequences from the three provinces and 71 known BLV strains, which revealed that in both Gansu and Qinghai provinces, genotypes 6 and 10 of the BLV strains were at high levels, whereas only genotype 10 was prevalent in Sichuan Province. Phylogenetic analysis and sequence comparisons revealed 95.7-99.8% sequence identity among the full-length env genes of 16 strains, nearly full-length genome sequences of six BLV strains, and those of the known genotypes 6 and 10 of BLV. This study provides comprehensive information is regarding the widespread infection of domestic yaks with BLV on the Qinghai-Tibet Plateau of China, and shows that at least two BLV genotypes (genotypes 6 and 10) are circulating in this population.

Notes

Compliance with ethical standards

Funding

This work was supported by a Grant from the National Natural Science Foundation of China (no. 31260616); Fuxi Foundation of Exceptional Talent at Gansu Agricultural University; Scientific Research Foundation for the New Scholars, Gansu Agricultural University (no. GSAU-RCZX201702) and the Innovation Foundation of the College of Veterinary Medicine, Gansu Agriculture University (no. JYCX-KX017).

Conflict of interest

The authors declare that there are no competing interests regarding the publication of this paper.

Ethical approval

All animals were handled with the assistance of veterinarians from the local veterinary institute and animal health and epidemiology centre. All procedures in this study were approved in strict accordance with good animal practice following the guidelines of the Animal Care and Use Committee of Gansu Agricultural University and performed in accordance with animal welfare and ethics.

References

  1. 1.
    Kettmann R, Portetelle D, Mammerickx M, Cleuter Y, Dekegel D, Galoux M, Ghysdael J, Burny A, Chantrenne H (1976) Bovine leukemia virus: an exogenous RNA oncogenic virus? Modern trends in human leukemia II. Springer, Berlin, pp 375–389Google Scholar
  2. 2.
    Willems L, Burny A, Collete D, Dangoisse O, Dequiedt F, Gatot J-S, Kerkhofs P, Lefebvre L, Merezak C, Peremans T (2000) Genetic determinants of bovine leukemia virus pathogenesis. AIDS Res Hum Retroviruses 16(16):1787–1795CrossRefPubMedGoogle Scholar
  3. 3.
    Moratorio G, Obal G, Dubra A, Correa A, Bianchi S, Buschiazzo A, Cristina J, Pritsch O (2010) Phylogenetic analysis of bovine leukemia viruses isolated in South America reveals diversification in seven distinct genotypes. Arch Virol 155(4):481–489CrossRefPubMedGoogle Scholar
  4. 4.
    Burny A, Cleuter Y, Kettmann R, Mammerickx M, Marbaix G, Portetelle D, Van den Broeke A, Willems L, Thomas R (1988) Bovine leukaemia: facts and hypotheses derived from the study of an infectious cancer. Vet Microbiol 17(3):197–218CrossRefPubMedGoogle Scholar
  5. 5.
    Polat M, Ohno A, S-n Takeshima, Kim J, Kikuya M, Matsumoto Y, Mingala CN, Onuma M, Aida Y (2015) Detection and molecular characterization of bovine leukemia virus in Philippine cattle. Arch Virol 160(1):285–296CrossRefPubMedGoogle Scholar
  6. 6.
    Llames L, Goyache J, Domenech A, Arjona A, Suarez G, Gomez-Lucia E (2001) Evaluation of virus excretion by cells persistently infected with the bovine leukaemia virus (BLV) using monoclonal antibodies. J Clin Virol 22(1):31–39CrossRefPubMedGoogle Scholar
  7. 7.
    Polat M, Moe HH, Shimogiri T, Moe KK, S-n Takeshima, Aida Y (2017) The molecular epidemiological study of bovine leukemia virus infection in Myanmar cattle. Arch Virol 162(2):425–437CrossRefPubMedGoogle Scholar
  8. 8.
    Schwartz I, Levy D (1994) Pathobiology of bovine leukemia virus. Vet Res 25(6):521–536PubMedGoogle Scholar
  9. 9.
    Gutiérrez G, Alvarez I, Politzki R, Lomónaco M, Santos MJD, Rondelli F, Fondevila N, Trono K (2011) Natural progression of bovine leukemia virus infection in Argentinean dairy cattle. Vet Microbiol 151(3):255–263CrossRefPubMedGoogle Scholar
  10. 10.
    Aida Y, Murakami H, Takahashi M, Takeshima S-N (2013) Mechanisms of pathogenesis induced by bovine leukemia virus as a model for human T-cell leukemia virus. Front Microbiol 4:328CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Gillet N, Florins A, Boxus M, Burteau C, Nigro A, Vandermeers F, Balon H, Bouzar A-B, Defoiche J, Burny A (2007) Mechanisms of leukemogenesis induced by bovine leukemia virus: prospects for novel anti-retroviral therapies in human. Retrovirology 4(1):18CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Mamoun R, Astier T, Guillemain B, Duplan J (1983) Bovine lymphosarcoma: expression of BLV-related proteins in cultured cells. J Gen Virol 64(9):1895–1905CrossRefPubMedGoogle Scholar
  13. 13.
    Zarkik S, Decroly E, Wattiez R, Seidah NG, Burny A, Ruysschaert J-M (1997) Comparative processing of bovine leukemia virus envelope glycoprotein gp72 by subtilisin/kexin-like mammalian convertases. FEBS Lett 406(1–2):205–210CrossRefPubMedGoogle Scholar
  14. 14.
    Bai L, Otsuki H, Sato H, Kohara J, Isogai E, S-n Takeshima, Aida Y (2015) Identification and characterization of common B cell epitope in bovine leukemia virus via high-throughput peptide screening system in infected cattle. Retrovirology 12(1):106CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    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(9):5321–5327PubMedPubMedCentralGoogle Scholar
  16. 16.
    Johnston ER, Radke K (2000) The SU and TM envelope protein subunits of bovine leukemia virus are linked by disulfide bonds, both in cells and in virions. J Virol 74(6):2930–2935CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Mamoun R, Morisson M, Rebeyrotte N, Busetta B, Couez D, Kettmann R, 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(9):4180–4188PubMedPubMedCentralGoogle Scholar
  18. 18.
    Bruck C, Mathot S, Portetelle D, Berte C, Franssen J-D, Herion P, Burny A (1982) Monoclonal antibodies define eight independent antigenic regions on the bovine leukemia virus (BLV) envelope glycoprotein gp51. Virology 122(2):342–352CrossRefPubMedGoogle Scholar
  19. 19.
    Khudhair YI, Hasso SA, Yaseen NY, Al-Shammari AM (2016) Serological and molecular detection of bovine leukemia virus in cattle in Iraq. Emerg Microb Infect 5(6):e56CrossRefGoogle Scholar
  20. 20.
    Lee E, Kim E-J, Ratthanophart J, Vitoonpong R, Kim B-H, Cho I-S, Song J-Y, Lee K-K, Shin Y-K (2016) Molecular epidemiological and serological studies of bovine leukemia virus (BLV) infection in Thailand cattle. Infect Genet Evol 41:245–254CrossRefPubMedGoogle Scholar
  21. 21.
    Polat M, S-n Takeshima, Hosomichi K, Kim J, Miyasaka T, Yamada K, Arainga M, Murakami T, Matsumoto Y, Diaz VB (2016) A new genotype of bovine leukemia virus in South America identified by NGS-based whole genome sequencing and molecular evolutionary genetic analysis. Retrovirology 13(1):4CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Rodriguez SM, Golemba MD, Campos RH, Trono K, Jones LR (2009) Bovine leukemia virus can be classified into seven genotypes: evidence for the existence of two novel clades. J Gen Virol 90(11):2788–2797CrossRefPubMedGoogle Scholar
  23. 23.
    Sun W-W, Lv W-F, Cong W, Meng Q-F, Wang C-F, Shan X-F, Qian A-D (2015) Mycobacterium avium subspecies paratuberculosis and bovine leukemia virus seroprevalence and associated risk factors in commercial dairy and beef cattle in northern and northeastern China. BioMed Res Int 2015:315173.  https://doi.org/10.1155/2015/315173
  24. 24.
    Ma J-G, Zheng W-B, Zhou D-H, Qin S-Y, Yin M-Y, Zhu X-Q, Hu G-X (2016) First report of bovine leukemia virus infection in yaks (Bos mutus) in China. BioMed Res Int 2016:9170167.  https://doi.org/10.1155/2016/9170167
  25. 25.
    Xu F, Pan Y, Wang M, Wu X, Tian L, Baloch AR, Zeng Q (2016) First detection of ungulate tetraparvovirus 1 (bovine hokovirus 1) in domestic yaks in northwestern China. Arch Virol 161(1):177–180CrossRefPubMedGoogle Scholar
  26. 26.
    Xu F, Pan Y, Baloch AR, Tian L, Wang M, Na W, Ding L, Zeng Q (2014) Hepatitis E virus genotype 4 in yak, northwestern China. Emerg Infect Dis 20(12):2182CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Zhu W, Dong J-B, Zhang J, Uchida K, K-i Watanabe, Goto Y, Haga T (2013) Bos grunniens papillomavirus type 1: a novel deltapapillomavirus associated with fibropapilloma in yak. J Gen Virol 94(1):159–165CrossRefPubMedGoogle Scholar
  28. 28.
    Tajima S, Ikawa Y, Aida Y (1998) Complete bovine leukemia virus (BLV) provirus is conserved in BLV-infected cattle throughout the course of B-cell lymphosarcoma development. J Virol 72(9):7569–7576PubMedPubMedCentralGoogle Scholar
  29. 29.
    Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425PubMedGoogle Scholar
  31. 31.
    Balić D, Lojkić I, Periškić M, Bedeković T, Jungić A, Lemo N, Roić B, Čač Ž, Barbić L, Madić J (2012) Identification of a new genotype of bovine leukemia virus. Arch Virol 157(7):1281–1290CrossRefPubMedGoogle Scholar
  32. 32.
    Matsumura K, Inoue E, Osawa Y, Okazaki K (2011) Molecular epidemiology of bovine leukemia virus associated with enzootic bovine leukosis in Japan. Virus Res 155(1):343–348CrossRefPubMedGoogle Scholar
  33. 33.
    Suh GH, Lee JC, Lee CY, Hur TY, Son DS, Ahn BS, Kim NC, Lee CG (2005) Establishment of a bovine leukemia virus-free dairy herd in Korea. J Vet Sci 6(3):227–230PubMedGoogle Scholar
  34. 34.
    Schoepf K, Kapaga A, Masami H, Hyera J (1997) Serological evidence of the occurrence of enzootic bovine leukosis (EBL) virus infection in cattle in Tanzania. Trop Anim Health Prod 29(1):15–19CrossRefPubMedGoogle Scholar
  35. 35.
    Licursi M, Inoshima Y, Wu D, Yokoyama T, González ET, Sentsui H (2002) Genetic heterogeneity among bovine leukemia virus genotypes and its relation to humoral responses in hosts. Virus Res 86(1):101–110CrossRefPubMedGoogle Scholar
  36. 36.
    Portetelle D, Couez D, Bruck C, Kettmann R, Mammerickx M, Van Der Maaten M, Brasseur R, Burny A (1989) Antigenic variants of bovine leukemia virus (BLV) are defined by amino acid substitutions in the NH2 part of the envelope glycoprotein gp51. Virology 169(1):27–33CrossRefPubMedGoogle Scholar
  37. 37.
    Zhao X, Buehring GC (2007) Natural genetic variations in bovine leukemia virus envelope gene: possible effects of selection and escape. Virology 366(1):150–165CrossRefPubMedGoogle Scholar
  38. 38.
    Gatot J-S, Callebaut I, Van Lint C, Demonté D, Kerkhofs P, Portetelle D, Burny A, Willems L, Kettmann R (2002) Bovine leukemia virus SU protein interacts with zinc, and mutations within two interacting regions differently affect viral fusion and infectivity in vivo. J Virol 76(16):7956–7967CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Bruck C, Portetelle D, Burny A, Zavada J (1982) Topographical analysis by monoclonal antibodies of BLV-gp51 epitopes involved in viral functions. Virology 122(2):353–362CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2017

Authors and Affiliations

  • Meng Wang
    • 1
  • Yun Wang
    • 2
  • Abdul Rasheed Baloch
    • 4
  • Yangyang Pan
    • 1
  • Fang Xu
    • 1
  • Lili Tian
    • 3
  • Qiaoying Zeng
    • 1
  1. 1.College of Veterinary MedicineGansu Agricultural UniversityLanzhouChina
  2. 2.Anning Branch Lanzhou General HospitalLanzhouChina
  3. 3.China Animal Health and Epidemiology CenterQingdaoChina
  4. 4.Faculty of Fisheries and Protection of Waters, South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses, Research Institute of Fish Culture and HydrobiologyUniversity of South Bohemia in České BudějoviceVodňanyCzech Republic

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