Epidemiological evidence for early-onset of enzootic bovine leukosis by L233-Tax-carrying bovine leukemia virus in Japanese Black cattle

Bovine leukemia virus (BLV) is the causative agent of enzootic bovine leukosis (EBL), of which annual number has rapidly increased in Japan, and it can be divided into two categories based on the amino acid at position 233 in the Tax protein. Here, we conducted a nationwide surveillance of Japanese...

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Published inJournal of Veterinary Medical Science Vol. 84; no. 9; pp. 1216 - 1220
Main Authors TOMIYASU, Takafumi, MORI, Hiroshi, OKAZAKI, Katsunori
Format Journal Article
LanguageEnglish
Published Tokyo JAPANESE SOCIETY OF VETERINARY SCIENCE 2022
Japan Science and Technology Agency
The Japanese Society of Veterinary Science
Subjects
Age
Amino acids
bovine leukemia virus
Bovine leukosis
Embryo transfer
enzootic bovine leucosis
Epidemiology
Japanese Black cattle
Leukosis
Tax
Tax protein
Tumors
Virology
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Abstract Bovine leukemia virus (BLV) is the causative agent of enzootic bovine leukosis (EBL), of which annual number has rapidly increased in Japan, and it can be divided into two categories based on the amino acid at position 233 in the Tax protein. Here, we conducted a nationwide surveillance of Japanese Black cattle between 2008 and 2021 in Japan. Among 237 tumor samples, 131 (55.3%) and 101 (42.6%) were harbored L233- and P233-Tax, respectively. Onset of EBL under the age of 3 years by L233-Tax-carrying BLV was frequently observed, especially in the animals born via embryo transfer. We also found that L233-Tax-carrying BLV was more prevalent in dairy areas than non-dairy areas. These findings give insight into prevention of EBL.
AbstractList Bovine leukemia virus (BLV) is the causative agent of enzootic bovine leukosis (EBL), of which annual number has rapidly increased in Japan, and it can be divided into two categories based on the amino acid at position 233 in the Tax protein. Here, we conducted a nationwide surveillance of Japanese Black cattle between 2008 and 2021 in Japan. Among 237 tumor samples, 131 (55.3%) and 101 (42.6%) were harbored L233- and P233-Tax, respectively. Onset of EBL under the age of 3 years by L233-Tax-carrying BLV was frequently observed, especially in the animals born via embryo transfer. We also found that L233-Tax-carrying BLV was more prevalent in dairy areas than non-dairy areas. These findings give insight into prevention of EBL.
Bovine leukemia virus (BLV) is the causative agent of enzootic bovine leukosis (EBL), of which annual number has rapidly increased in Japan, and it can be divided into two categories based on the amino acid at position 233 in the Tax protein. Here, we conducted a nationwide surveillance of Japanese Black cattle between 2008 and 2021 in Japan. Among 237 tumor samples, 131 (55.3%) and 101 (42.6%) were harbored L233- and P233-Tax, respectively. Onset of EBL under the age of 3 years by L233-Tax-carrying BLV was frequently observed, especially in the animals born via embryo transfer. We also found that L233-Tax-carrying BLV was more prevalent in dairy areas than non-dairy areas. These findings give insight into prevention of EBL.
Bovine leukemia virus (BLV) is the causative agent of enzootic bovine leukosis (EBL), of which annual number has rapidly increased in Japan, and it can be divided into two categories based on the amino acid at position 233 in the Tax protein. Here, we conducted a nationwide surveillance of Japanese Black cattle between 2008 and 2021 in Japan. Among 237 tumor samples, 131 (55.3%) and 101 (42.6%) were harbored L233- and P233-Tax, respectively. Onset of EBL under the age of 3 years by L233-Tax-carrying BLV was frequently observed, especially in the animals born via embryo transfer. We also found that L233-Tax-carrying BLV was more prevalent in dairy areas than non-dairy areas. These findings give insight into prevention of EBL.Bovine leukemia virus (BLV) is the causative agent of enzootic bovine leukosis (EBL), of which annual number has rapidly increased in Japan, and it can be divided into two categories based on the amino acid at position 233 in the Tax protein. Here, we conducted a nationwide surveillance of Japanese Black cattle between 2008 and 2021 in Japan. Among 237 tumor samples, 131 (55.3%) and 101 (42.6%) were harbored L233- and P233-Tax, respectively. Onset of EBL under the age of 3 years by L233-Tax-carrying BLV was frequently observed, especially in the animals born via embryo transfer. We also found that L233-Tax-carrying BLV was more prevalent in dairy areas than non-dairy areas. These findings give insight into prevention of EBL.
ArticleNumber 22-0169
Author OKAZAKI, Katsunori
MORI, Hiroshi
TOMIYASU, Takafumi
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  organization: Laboratory of Microbiology and Immunology, Faculty of Pharmaceutical Sciences, Health Sciences University of Hokkaido, Hokkaido, Japan
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  organization: Laboratory of Microbiology and Immunology, Faculty of Pharmaceutical Sciences, Health Sciences University of Hokkaido, Hokkaido, Japan
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crossref_primary_10_1016_j_rvsc_2022_12_008
crossref_primary_10_3390_metabo14110624
crossref_primary_10_1016_j_vetmic_2023_109829
crossref_primary_10_21897_rmvz_3411
Cites_doi 10.2460/javma.244.8.914
10.1016/0378-1135(88)90066-1
10.3389/fmicb.2013.00328
10.1016/j.vetmic.2021.109042
10.1016/j.coviro.2017.06.012
10.1292/jvms.13-0253
10.1016/j.vetmic.2013.09.026
10.1016/S0167-5877(03)00057-6
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10.1016/j.prevetmed.2007.05.010
10.1093/oxfordjournals.aje.a119397
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10.1136/vr.102464
10.4314/ovj.v9i1.6
10.1016/S0749-0720(15)30367-4
10.1016/j.virusres.2015.08.013
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References 9. Kahrs RF. 2001. Bovine leukemia virus and enzootic bovine leucosis. pp 103–112. In: Viral Diseases of Cattle, 2nd ed., Iowa State University Press, Ames.
18. Panei CJ, Larsen AE, Fuentealba NA, Metz GE, Echeverría MG, Galosi CM, Valera AR. 2019. Study of horn flies as vectors of bovine leukemia virus. Open Vet J 9: 33–37.
14. Mori H, Tomiyasu T, Nishiyama K, Matsumoto M, Osawa Y, Okazaki K. 2019. L233P mutation in the bovine leukemia virus Tax protein depresses endothelial cell recruitment and tumorigenesis in athymic nude mice. Arch Virol 164: 1343–1351.
22. Yuan Y, Kitamura-Muramatsu Y, Saito S, Ishizaki H, Nakano M, Haga S, Matoba K, Ohno A, Murakami H, Takeshima SN, Aida Y. 2015. 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 210: 248–254.
7. 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: 364–371.
12. MAFF. 2020. Annual statistics of livestock (in Japanese). Production, Marketing and Consumption Statistics Division, Ministry of Agriculture, Forestry and Fisheries. https://www.e-stat.go.jp/stat-search/files?page=1&layout=datalist&toukei=00500222&tstat=000001015614&cycle=7&tclass1=000001020206&tclass2=000001134566&tclass3val=0 [accessed on March 31, 2022].
4. Bartlett PC, Sordillo LM, Byrem TM, Norby B, Grooms DL, Swenson CL, Zalucha J, Erskine RJ. 2014. Options for the control of bovine leukemia virus in dairy cattle. J Am Vet Med Assoc 244: 914–922.
10. Kanno T, Ishihara R, Hatama S, Oue Y, Edamatsu H, Konno Y, Tachibana S, Murakami K. 2014. Effect of freezing treatment on colostrum to prevent the transmission of bovine leukemia virus. J Vet Med Sci 76: 255–257.
5. 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: 197–218.
19. Safari R, Hamaidia M, de Brogniez A, Gillet N, Willems L. 2017. Cis-drivers and trans-drivers of bovine leukemia virus oncogenesis. Curr Opin Virol 26: 15–19.
15. Murakami K, Kobayashi S, Konishi M, Kameyama K, Tsutsui T. 2013. Nationwide survey of bovine leukemia virus infection among dairy and beef breeding cattle in Japan from 2009–2011. J Vet Med Sci 75: 1123–1126.
1. Acaite J, Tamosiunas V, Lukauskas K, Milius J, Pieskus J. 2007. The eradication experience of enzootic bovine leukosis from Lithuania. Prev Vet Med 82: 83–89.
2. Aida Y, Murakami H, Takahashi M, Takeshima SN. 2013. Mechanisms of pathogenesis induced by bovine leukemia virus as a model for human T-cell leukemia virus. Front Microbiol 4: 328.
16. Nuotio L, Rusanen H, Sihvonen L, Neuvonen E. 2003. Eradication of enzootic bovine leukosis from Finland. Prev Vet Med 59: 43–49.
13. Mekata H, Sekiguchi S, Konnai S, Kirino Y, Honkawa K, Nonaka N, Horii Y, Norimine J. 2015. Evaluation of the natural perinatal transmission of bovine leukaemia virus. Vet Rec 176: 254.
20. Sartwell PE. 1950. The distribution of incubation periods of infectious disease. Am J Hyg 51: 310–318.
3. Barez PY, de Brogniez A, Carpentier A, Gazon H, Gillet N, Gutiérrez G, Hamaidia M, Jacques JR, Perike S, Neelature Sriramareddy S, Renotte N, Staumont B, Reichert M, Trono K, Willems L. 2015. Recent advances in BLV research. Viruses 7: 6080–6088.
8. Juliarena MA, Barrios CN, Ceriani MC, Esteban EN. 2016. Hot topic: bovine leukemia virus (BLV)-infected cows with low proviral load are not a source of infection for BLV-free cattle. J Dairy Sci 99: 4586–4589.
21. Tomiyasu T, Sato A, Mori H, Okazaki K. 2021. L233P mutation in the bovine leukemia virus Tax protein has impact on annexin A3 and type I collagen secretion by host cells. Vet Microbiol 256: 109042.
11. Knapen K, Kerkhofs P, Mammerickx M. 1993. Eradication of enzootic bovine leukosis in Belgium: Results of the mass detection on the national cattle population in 1989, 1990 and 1991. Ann Med Vet 137: 197–201.
6. Hopkins SG, DiGiacomo RF. 1997. Natural transmission of bovine leukemia virus in dairy and beef cattle. Vet Clin North Am Food Anim Pract 13: 107–128.
17. Ochiai C, Katagiri Y, Kobayashi S, Naitoh I, Yoneyama S, Tomita K, Dongze L, Hikono H, Murakami K. 2020. Development of a microchip electrophoresis-based, high-throughput PCR-RFLP method to type Tax 233 variants of bovine leukemia virus in Japan. Arch Virol 165: 2961–2966.
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References_xml – reference: 3. Barez PY, de Brogniez A, Carpentier A, Gazon H, Gillet N, Gutiérrez G, Hamaidia M, Jacques JR, Perike S, Neelature Sriramareddy S, Renotte N, Staumont B, Reichert M, Trono K, Willems L. 2015. Recent advances in BLV research. Viruses 7: 6080–6088.
– reference: 13. Mekata H, Sekiguchi S, Konnai S, Kirino Y, Honkawa K, Nonaka N, Horii Y, Norimine J. 2015. Evaluation of the natural perinatal transmission of bovine leukaemia virus. Vet Rec 176: 254.
– reference: 16. Nuotio L, Rusanen H, Sihvonen L, Neuvonen E. 2003. Eradication of enzootic bovine leukosis from Finland. Prev Vet Med 59: 43–49.
– reference: 21. Tomiyasu T, Sato A, Mori H, Okazaki K. 2021. L233P mutation in the bovine leukemia virus Tax protein has impact on annexin A3 and type I collagen secretion by host cells. Vet Microbiol 256: 109042.
– reference: 22. Yuan Y, Kitamura-Muramatsu Y, Saito S, Ishizaki H, Nakano M, Haga S, Matoba K, Ohno A, Murakami H, Takeshima SN, Aida Y. 2015. 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 210: 248–254.
– reference: 10. Kanno T, Ishihara R, Hatama S, Oue Y, Edamatsu H, Konno Y, Tachibana S, Murakami K. 2014. Effect of freezing treatment on colostrum to prevent the transmission of bovine leukemia virus. J Vet Med Sci 76: 255–257.
– reference: 8. Juliarena MA, Barrios CN, Ceriani MC, Esteban EN. 2016. Hot topic: bovine leukemia virus (BLV)-infected cows with low proviral load are not a source of infection for BLV-free cattle. J Dairy Sci 99: 4586–4589.
– reference: 9. Kahrs RF. 2001. Bovine leukemia virus and enzootic bovine leucosis. pp 103–112. In: Viral Diseases of Cattle, 2nd ed., Iowa State University Press, Ames.
– reference: 5. 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: 197–218.
– reference: 17. Ochiai C, Katagiri Y, Kobayashi S, Naitoh I, Yoneyama S, Tomita K, Dongze L, Hikono H, Murakami K. 2020. Development of a microchip electrophoresis-based, high-throughput PCR-RFLP method to type Tax 233 variants of bovine leukemia virus in Japan. Arch Virol 165: 2961–2966.
– reference: 1. Acaite J, Tamosiunas V, Lukauskas K, Milius J, Pieskus J. 2007. The eradication experience of enzootic bovine leukosis from Lithuania. Prev Vet Med 82: 83–89.
– reference: 7. 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: 364–371.
– reference: 14. Mori H, Tomiyasu T, Nishiyama K, Matsumoto M, Osawa Y, Okazaki K. 2019. L233P mutation in the bovine leukemia virus Tax protein depresses endothelial cell recruitment and tumorigenesis in athymic nude mice. Arch Virol 164: 1343–1351.
– reference: 15. Murakami K, Kobayashi S, Konishi M, Kameyama K, Tsutsui T. 2013. Nationwide survey of bovine leukemia virus infection among dairy and beef breeding cattle in Japan from 2009–2011. J Vet Med Sci 75: 1123–1126.
– reference: 20. Sartwell PE. 1950. The distribution of incubation periods of infectious disease. Am J Hyg 51: 310–318.
– reference: 19. Safari R, Hamaidia M, de Brogniez A, Gillet N, Willems L. 2017. Cis-drivers and trans-drivers of bovine leukemia virus oncogenesis. Curr Opin Virol 26: 15–19.
– reference: 2. Aida Y, Murakami H, Takahashi M, Takeshima SN. 2013. Mechanisms of pathogenesis induced by bovine leukemia virus as a model for human T-cell leukemia virus. Front Microbiol 4: 328.
– reference: 6. Hopkins SG, DiGiacomo RF. 1997. Natural transmission of bovine leukemia virus in dairy and beef cattle. Vet Clin North Am Food Anim Pract 13: 107–128.
– reference: 12. MAFF. 2020. Annual statistics of livestock (in Japanese). Production, Marketing and Consumption Statistics Division, Ministry of Agriculture, Forestry and Fisheries. https://www.e-stat.go.jp/stat-search/files?page=1&layout=datalist&toukei=00500222&tstat=000001015614&cycle=7&tclass1=000001020206&tclass2=000001134566&tclass3val=0 [accessed on March 31, 2022].
– reference: 4. Bartlett PC, Sordillo LM, Byrem TM, Norby B, Grooms DL, Swenson CL, Zalucha J, Erskine RJ. 2014. Options for the control of bovine leukemia virus in dairy cattle. J Am Vet Med Assoc 244: 914–922.
– reference: 18. Panei CJ, Larsen AE, Fuentealba NA, Metz GE, Echeverría MG, Galosi CM, Valera AR. 2019. Study of horn flies as vectors of bovine leukemia virus. Open Vet J 9: 33–37.
– reference: 11. Knapen K, Kerkhofs P, Mammerickx M. 1993. Eradication of enzootic bovine leukosis in Belgium: Results of the mass detection on the national cattle population in 1989, 1990 and 1991. Ann Med Vet 137: 197–201.
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  doi: 10.1016/j.vetmic.2021.109042
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  doi: 10.1016/j.coviro.2017.06.012
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  doi: 10.1292/jvms.13-0253
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  doi: 10.1016/j.vetmic.2013.09.026
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  doi: 10.1292/jvms.12-0374
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  doi: 10.1016/j.prevetmed.2007.05.010
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  doi: 10.1093/oxfordjournals.aje.a119397
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  doi: 10.1007/s00705-020-04842-w
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  doi: 10.1007/s00705-019-04191-3
– ident: 9
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  doi: 10.3390/v7112929
– ident: 8
  doi: 10.3168/jds.2015-10480
– ident: 13
  doi: 10.1136/vr.102464
– ident: 18
  doi: 10.4314/ovj.v9i1.6
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  doi: 10.1016/S0749-0720(15)30367-4
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  doi: 10.1016/j.virusres.2015.08.013
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Snippet Bovine leukemia virus (BLV) is the causative agent of enzootic bovine leukosis (EBL), of which annual number has rapidly increased in Japan, and it can be...
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SubjectTerms Age
Amino acids
bovine leukemia virus
Bovine leukosis
Embryo transfer
enzootic bovine leucosis
Epidemiology
Japanese Black cattle
Leukosis
Tax
Tax protein
Tumors
Virology
Title Epidemiological evidence for early-onset of enzootic bovine leukosis by L233-Tax-carrying bovine leukemia virus in Japanese Black cattle
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ispartofPNX Journal of Veterinary Medical Science, 2022, Vol.84(9), pp.1216-1220
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