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Analysis of bovine leukemia virus integration sites in cattle under 3 years old with enzootic bovine leukosis

  • Masaki Maezawa
  • Hisashi InokumaEmail author
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Abstract

In the present study, we analyzed bovine leukemia virus (BLV) integration sites in under 3 years old with enzootic bovine leukosis (EBL) cattle and compared these to 30 cattle over 3 years old with EBL. BLV proviruses were integrated near CpG islands and into long interspersed nuclear elements more frequently in EBL cattle under 3 years old than in those over 3 years old. These results suggest that cattle under 3 years old with EBL have different BLV provirus integration sites from those of cattle over 3 years old with EBL, and the BLV provirus integration site may represent one factor contributing to early onset of EBL.

Notes

Acknowledgements

We thank the veterinarians of the Iwate and Tokachi Agriculture Mutual Aid Association and Tokachi and Hayakita Meat Hygiene Inspection Centers for sampling. This work was supported by JSPS KAKENHI grant number 16K15044.

Compliance with ethical standards

Conflict of interest

The authors have no conflicts of interest to declare.

Ethical approval

No ethical approval was necessary, as the present study had no human participants and the authors did not perform any of the procedures on the animals.

Supplementary material

705_2019_4431_MOESM1_ESM.docx (32 kb)
Supplementary material 1 (DOCX 32 kb)

References

  1. 1.
    Schwartz I, Lévy D (1994) Pathobiology of bovine leukemia virus. Vet Res 25:521–536PubMedGoogle Scholar
  2. 2.
    Florins A, Boxus M, Vandermeers F, Verlaeten O, Bouzar AB, Defoiche J, Hubaux R, Burny A, Kettmann R, Willems L (2008) Emphasis on cell turnover in two hosts infected by bovine leukemia virus: a rationale for host susceptibility to disease. Vet Immunol Immunopathol 125:1–7CrossRefGoogle Scholar
  3. 3.
    Gutiérrez G, Alvarez I, Merlini R, Rondell F, Trono K (2014) Dynamics of perinatal bovine leukemia virus infection. BMC Vet Res 10:2416–2427CrossRefGoogle Scholar
  4. 4.
    Nishimori A, Konnai S, Okagawa T, Maekawa N, Goto S, Ikebuchi R, Nakahara A, Chiba Y, Ikeda M, Murata S, Ohashi K (2017) Identification of an atypical enzootic bovine leukosis in Japan by using a novel classification of bovine leukemia based on immunophenotypic analysis. Clin Vac Immunol 24:e00067-17CrossRefGoogle Scholar
  5. 5.
    Oguma K, Suzuki M, Sentsui H (2017) Enzootic bovine leukosis in a two-month-old calf. Virus Res 233:120–124CrossRefGoogle Scholar
  6. 6.
    Maezawa M, Watanabe K, Horiuchi N, Matsumoto K, Kobayashi Y, Inokuma H (2018) A clinical case of enzootic bovine leucosis in a 13-month-old Holstein heifer. Jpn J Vet Res 66:150–209Google Scholar
  7. 7.
    Doi K, Wu X, Taniguchi Y, Yasunaga J, Satou Y, Okayama A, Nosaka K, Matsuoka M (2005) Preferential selection of human T-cell leukemia virus type I provirus integration sites in leukemic versus carrier states. Blood 106:1048–1053.Google Scholar
  8. 8.
    Mitchell RD, Beitzel BF, Schroder ARW, Shinn P, Chen H, Berry CC, Ecker JR, Bushman FD (2004) Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLoS Biol 2:e234CrossRefGoogle Scholar
  9. 9.
    Gillet NA, Malani N, Melamed A, Gormley N, Carter R, Bently D, Berry C, Bushman FD, Taylor GP, Bangham CR (2011) The host genomic environment of the provirus determines the abundance of HTLV-1-infected T-cell clones. Blood 117:3113–3122CrossRefGoogle Scholar
  10. 10.
    Gillet NA, Gutiérrez G, Rodriguez SM, Brogniez AD, Renotte N, Alvarez I, Trono K, Willems L (2013) Massive depletion of bovine leukemia virus proviral clones located in genomic transcriptionally active sites during primary infection. PLos Path 9:e1003687CrossRefGoogle Scholar
  11. 11.
    Rosewick N, Durkin K, Artesi M, Marcais A, Hahaut V, Griebel P, Arsic N, Avettand-Fenoel V, Burny A, Charlier C, Hermine O, Georges M, Broeke AV (2017) Cis-perturbation of cancer drivers by the HTLV-1/BLV proviruses is an early determinant of leukemogenesis. Nta Commun 8:15264CrossRefGoogle Scholar
  12. 12.
    Murakami H, Yamada T, Suzuki M, Nakahara Y, Suzuki K, Sentsui H (2011) Bovine leukemia virus integration site selection in cattle that develop leukemia. Virus Res 156:107–112CrossRefGoogle Scholar
  13. 13.
    Miyasaka T, Oguma K, Sentsui H (2015) Distribution and characteristics of bovine leukemia virus integration sites in the host genome at three different clinical stages of infection. Arch Virol 160:39–46CrossRefGoogle Scholar
  14. 14.
    Inoue E, Matsumura K, Soma N, Hirasawa S, Wakimoto M, Arakaki Y, Yoshida T, Osawa Y, Okazaki K (2013) L233P mutation of the Tax protein strongly correlated with leukemogenicity of bovine leukemia virus. Vet Microbiol 167:364–371CrossRefGoogle Scholar
  15. 15.
    Sajiki Y, Konnai S, Nishimori A, Okagawa T, Maekawa N, Goto S, Nagano M, Kohara J, Kitano N, Takahashi T, Takahashi T, Mekata H, Horii Y, Murata S, Ohashi K (2017) Intrauterine infection with bovine leukemia virus in pregnant dam with high viral load. J Vet Med Sci 79:2036–2039CrossRefGoogle Scholar
  16. 16.
    Kettmann R, Cleuter Y, Mammerickx M, Meunier-Rotival M, Bernardi G, Burny A, Chantrenne H (1980) Genomic integration of bovine leukemia provirus: Comparison of persistent lymphocytosis with lymph node tumor form of enzootic bovine leukosis. Proc Natl Acad Sci USA 77:2577–2581CrossRefGoogle Scholar
  17. 17.
    Miura S, Horiuchi N, Matsumoto K, Kobayashi Y, Kawazu S, Inokuma H (2015) Detection of monoclonal integration of bovine leukemia virus proviral DNA as a malignant marker in two enzootic bovine leukosis cases with difficult clinical diagnosis. J Vet Med Sci 77:883–887CrossRefGoogle Scholar
  18. 18.
    Jordan A, Defechereux P, Verdin E (2001) The site of HIV-1 integration in the human genome determines basal transcriptional activity and response to Tat transactivation. Eur Mol Biol Organ 20:1726–1738CrossRefGoogle Scholar
  19. 19.
    Wu X, Li Y, Crise B, Burgess SM (2003) Transcription start regions in the human genome are favored targets for MLV integration. Science 300:1749–1751CrossRefGoogle Scholar
  20. 20.
    Finnegan DJ (2012) Retrotransposons. Curr Biolo 22:435–437Google Scholar
  21. 21.
    Heffron F, McCarthy BJ, Ohtsubo H, Ohtsubo E (1979) DNA sequence analysis of the transposon Tn3: three genes and three sites involved in transposition of Tn3. Cell 18:1153–1163CrossRefGoogle Scholar
  22. 22.
    Bradshaw AB, McEntee K (1989) DNA damage activates transcription and transposition of yeast Ty retrotransposons. Mol Gen Genet 218:465–474CrossRefGoogle Scholar
  23. 23.
    Wessler SR (1996) Plant retrotransposons: turned on by stress. Curr Biol 6:959–961CrossRefGoogle Scholar
  24. 24.
    Grandbastien MA (1998) Activation of plant retrotransposons under stress conditions. Trends Plant Sci 3:181–187CrossRefGoogle Scholar
  25. 25.
    Capy P, Gasperi G, Biemont C, Bazin C (2000) Stress and transposable elements: co-evolution or useful parasites. Heredity 85:101–106CrossRefGoogle Scholar
  26. 26.
    Belancio VP, Hedges DJ, Deininger P (2008) Mammalian non-LTR retrotransposons: for better or worse, insickness and in health. Genome res 18:343–358CrossRefGoogle Scholar
  27. 27.
    Carnell AN, Coodman JI (2003) The long (LINEs) and the short (SINEs) of It: altered methylation as a precursor to toxicity. Toxicol Sci 75:229–235CrossRefGoogle Scholar
  28. 28.
    Baba Y, Huttenhower C, Nosho K, Tanaka N, Shima K, Hazra A, Schernhammer ES, Hunter JD, Giovannucci LE, Fuchs SC, Ogino S (2010) Epigenomic diversity of colorectal cancer indicated by LINE-1 methylation in a database of 869 tumors. Mol Cancer 9:125CrossRefGoogle Scholar
  29. 29.
    Igarashi S, Suzuki H, Niinuma T, Shimizu H, Nojima M, Iwaki H, Nobuoka T, Nishida T, Miyazaki Y, Takamaru H, Yamamoto E, Yamamoto H, Tokino T, Hasegawa T, Hirata K, Imai K, Toyota M, Shinomura Y (2010) A novel correlation between LINE-1 hypomethylation and the malignancy of gastrointestinal stromal tumor. Clin Cancer Res 16:5114–5123CrossRefGoogle Scholar
  30. 30.
    Florl AR, Löwer R, Schmitz-Dräger BJ, Schulz WA (1999) DNA methylation and expression of LINE-1 and HERV-K provirus sequences in urothelial and renal cell carcinomas. British J Cancer 80:1312–1321CrossRefGoogle Scholar
  31. 31.
    Kang HG, Lee S, Kim HW, Lee HW, Kim CJ, Rhyu M, Ro YJ (2002) Epstein–Barr virus-positive gastric carcinoma demonstrates frequent aberrant methylation of multiple genes and constitutes CpG Island Methylator phenotype-positive gastric carcinoma. Am J Path 16:787–794CrossRefGoogle Scholar
  32. 32.
    Narimatsu T, Tamori A, Koh N, Kubo S, Hirohashi K, Yano Y, Arakawa T, Otani S, Nishiguchi S (2004) p16 promoter hypermethylation in human hepatocellular carcinoma with or without hepatitis virus infection. Intervirology 47:26–31CrossRefGoogle Scholar
  33. 33.
    Osawa T, Chong J, Sudo M, Sakuma K, Uozaki H, Shibahara J, Nagai H, Funata N, Fukayama M (2002) Reduced expression and promoter methylation of p16 gene in epstein-barr virus-associated gastric carcinoma. Jpn J Cancer Res 93:1195–1200CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Veterinary MedicineObihiro University of Agriculture and Veterinary MedicineObihiroJapan
  2. 2.United Graduate School of Veterinary SciencesGifu UniversityGifuJapan
  3. 3.Veterinary Medical CenterThe University of TokyoTokyoJapan

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