Association of BoLA-DRB3 Alleles with the Progression of Bovine Leukosis in the Lucerna Breed
Abstract
The bovine leukosis virus causes enzootic bovine leukosis (BLV) of the Retroviridae family and is the most significant neoplastic disease in cattle, leading to substantial economic losses globally. This study aimed to associate the progression of bovine leukosis with BoLA-DRB3 alleles in the Lucerna breed. A total of 104 animals were tested for the presence of BLV by nested PCR, the development of persistent lymphocytosis (PL) by peripheral blood smear, antibody titers (AT) to BLV by ELISA, and proviral load (PVL) by qPCR. Animals were genotyped for the BoLA-DRB3 gene by PCR-SBT. Allele frequencies of the DRB3 gene were estimated and associated using Fisher’s exact test and odds ratio. About 93.2% of the animals were virus positive, and 18.3% developed PL. Fifty percent of the animals had elevated AT with a value of 88.7 log2, and 43.3% had elevated PVL with 326871 copies/105 cells. In total, 17 BoLA-DRB3 alleles were found; the BoLA-DRB3*011:01 allele (12.1%) was the most frequent. Two alleles showed an association with susceptibility to viral infection (BoLA-DRB3*15:01 and *23:01), and only the BoLA-DRB3*38:01 allele was considered resistant. The BoLA-DRB3*11:01 and *15:01 alleles were not associated with LP, and neither allele was associated with high LP. Low AT was found in the BoLA-DRB3*13:01 and *20:01:02 alleles. The BoLA-DRB3*15:01 and *16:01 alleles were associated with high AT. Low PVL was associated with the BoLA-DRB3*11:01 and *23:01 alleles. BoLA-DRB3*15:01 allele was associated with high PVL. In conclusion, the Lucerne breed has a slow progression of enzootic bovine leukosis.
References
Bolaños, I., D. Y. Hernández, & L. A. Álvarez. 2017. Asociación de los alelos del gen BoLA-DRB3 con la infección natural de Babesia spp en el ganado criollo Hartón del Valle. Archivos Zootecnia 66:113-120. https://doi.org/10.21071/az.v66i253.2133
Chieh-Wen. L., L. Borjigin, S. Saito, K. Fukunaga, E. Saitou, K. Okazaki, T. Mizutani, S. Wada, S. Takeshima, & Y. Aida. 2020. BoLA-DRB3 Polymorphism is associated with differential susceptibility to bovine leukemia virus-induced lymphoma and proviral load. Viruses 12:352. https://doi.org/10.3390/v12030352
Chieh-Wen, L. & Y. Aida. 2022. Association of BoLA-DRB3 with bovine leukemia virus. Major Histocompatibility Complex 29:158-167. https://doi.org/10.12667/mhc.29.158
Corredor-Figueroa, A., S. Sandra, N. Olaya-Galán, J. Quintero, A. Fajardo, M. Soñora, P. Moreno, J. Cristina, A. Sánchez, J. Tobón, D. Ortiz, & M. Gutiérrez. 2020. Prevalence and molecular epidemiology of bovine leukemia virus in Colombian cattle. Infect. Genet. Evol. 80:104171. https://doi.org/10.1016/j.meegid.2020.104171
Giraldo, N., A. Viveros, J. C. Rincón, & L. González-Herrera. 2023. Curva de primera lactancia en ganado bovino con diferente proporción Lucerna y su relación con factores ambientales asociados a la producción de leche. Livestock Research for Rural Development 35:1.
Gutiérrez, S., C. Lützelschwab, C. Barrios, & M. Juliarena. 2020. Leucosis bovina: Una visión actualizada. Rev. Investig. Vet. Peru. 31:e16913. https://doi.org/10.15381/rivep.v31i3.16913
Hernández, D. Y., J. E. Muñoz, & L. A. Álvarez. 2014. Asociación del locus BoLA-DRB3.2 con el virus de la leucosis bovina en el ganado criollo colombiano. Rev. Colombiana Cienc. Anim Recia. 6:319-326. https://doi.org/10.24188/recia.v6.n2.2014.435
Hernández. D. Y., J. E. Muñoz, & L. A. Álvarez. 2015. Genetic diversity of BoLA-DRB3 gene in colombian creole Hartón del Valle cattle. CES. Arq. Bras. Med. Vet. Zootec. 10:18-30.
Hernández. D. Y., J. E. Muñoz, & L. A. Álvarez. 2016. Dinámica de la leucosis bovina en el ganado criollo Hartón del Valle en infección natural. Arch. Zootec. 65:365-373. https://doi.org/10.21071/az.v65i251.698
Hernández, D. Y., D. E. Montes, & L. A. Álvarez. 2018. Association of BoLA-DRB3.2 alleles with enzootic bovine leukosis: Profiles BLV infection, persistent lymphocytosis and antibody production in Hartón Del Valle Cattle. Indian J. Sci. Technol. 11:1-14. https://doi.org/10.17485/ijst/2018/v11i24/128164
Juliarena, M., C. Barrios, C. Ceriani, & E. Esteban. 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. https://doi.org/10.3168/jds.2015-10480
Kohara, J., M. Takeuchi, Y. Hirano, Y. Sakurai, & T. Takahashi. 2018. Vector control efficacy of fly nets on preventing bovine leukemia virus transmission. J. Vet. Med. Sci. 80:1524-1527. https://doi.org/10.1292/jvms.18-0199
Konishi, M., H. Ishizaki, K. Kameyama, K. Murakami, & T. Yamamoto. 2018. The effectiveness of colostral antibodies for preventing bovine leukemia virus (BLV) infection in vitro. BMC Vet. Res. 14:419. https://doi.org/10.1186/s12917-018-1724-5
Kuczewski, A., H. Hogeveen, K. Orsel, R. Wolf, J. Thompson, E. Spackman, & F. van der Meer. 2019. Economic evaluation of 4 bovine leukemia virus control strategies for Alberta dairy farms. J. Dairy Sci. 102:2578-2592. https://doi.org/10.3168/jds.2018-15341
Kuczewski, A., K. Orsel, H. Barkema, S. Mason, R. Erskine, & F. van der Meer. 2021. Invited review: Bovine leukemia virus-transmission, control, and eradication. J. Dairy Sci. 104:6358-6375. https://doi.org/10.3168/jds.2020-18925
Longeri, M., V. Russo, M. Strillacci, A. Perillo, M. Carisetti, M. Cozzi, B. Neola, & S. Roperto. 2021. Association between BoLA-DRB3.2 polymorphism and bovine papillomavirus infection for bladder tumor risk in Podolica cattle. Front. Vet. Sci. 8:630089. https://doi.org/10.3389/fvets.2021.630089
Morales, J., A. López-Herrera, & J. Echeverri. 2020 Association of BoLA DRB3 gene polymorphisms with BoHV-1 infection and zootechnical traits. Open. Vet. J. 10:331-339. https://doi.org/10.4314/ovj.v10i3.12
Nakada, S., Y. Fujimoto, J. Kohara, & K. Makita. 2023. Economic losses associated with mastitis due to bovine leukemia virus infection. J. Dairy. Sci. 106:576-588. https://doi.org/10.3168/jds.2021-21722
Nakatsuchi, A., A. Bao, S. Watanuki, R. Matsuura, L. Borjigin, L. Bai, M. Kuroda, Y. Matsumoto, J. Kohara, & Y. Aida. 2022a. Anti-BLV antibodies in whey correlate with bovine leukemia virus disease progression and BoLA-DRB3 polymorphism. Front. Vet. Sc. 9:1038101. https://doi.org/10.3389/fvets.2022.1038101
Nakatsuchi, A., S. Watanuki, L. Borjigin, H. Sato, L. Bai, R. Matsuura, M. Kuroda, H. Murakami, R. Sato, S. Asaji, A. Ando, Y. Matsumoto, S. Takeshima, & Y. Aida. 2022b. BoLA-DRB3 polymorphism controls proviral load and infectivity of bovine leukemia virus (BLV) in milk. Pathogens 11:210. https://doi.org/10.3390/pathogens11020210
Nakatsuchi, A., Y. Matsumoto, & Y. Aida. 2023. Influence of BoLA-DRB3 polymorphism and bovine leukemia virus (BLV) infection on dairy cattle productivity. Vet. Sci. 10:250. https://doi.org/10.3390/vetsci10040250
Norby, B., P. Bartlett, T. Byrem, & R. Erskine. 2016. Effect of infection with bovine leukemia virus on milk production in michigan dairy cows. J. Dairy Sci. 99:2043-2052. https://doi.org/10.3168/jds.2015-10089
Ohno, A., S. Takeshima, Y. Matsumoto, & Y. Aida. 2015. Risk factors associated with increased bovine leukemia virus proviral load in infected cattle in Japan from 2012 to 2014. Virus Res. 210:283-290. https://doi.org/10.1016/j.virusres.2015.08.020
Peakall, R. & P. Smouse. 2012. GenAlEx 6.5: Genetic analysis in excel. population genetic software for teaching and research--an update. Bioinformatics 28:2537-2539. https://doi.org/10.1093/bioinformatics/bts460
Rodríguez-Habibe, I., C. Celis-Giraldo, M. Patarroyo, C. Avendaño, & M. E. Patarroyo. 2020. A comprehensive review of the immunological response against foot-and-mouth disease virus infection and its evasion mechanisms. Vaccines 8:764. https://doi.org/10.3390/vaccines8040764
Ruiz, V., N. Porta, M. Lomónaco, K. Trono, & I. Alvarez. 2018. Bovine leukemia virus infection in neonatal calves. risk factors and control measures. Front. Vet. Sci. 5:267. https://doi.org/10.3389/fvets.2018.00267
Suprovych, T., M. Suprovych, R. Kylinchuk, T. Karchevska, I. Chornyi, & V. Kolodiy. 2020. Association of BoLA-DRB3.2 alleles with fusobacteriosis in cows. Regul. Mech. Biosyst. 11:249-254. https://doi.org/10.15421/022037
Takeshima, S., Y. Kitamura-Muramatsu, Y. Yuan, M. Polat, Y. Saito, & Y. Aida. 2015. BLV-CoCoMo-qPCR-2: Improvements to the BLV-CoCoMo-qPCR assay for bovine leukemia virus by reducing primer degeneracy and constructing an optimal standard curve. Arch. Virol. 160:1325-1332. https://doi.org/10.1007/s00705-015-2377-3
Tayeng, K., S. Tomar, S. Nanavat, R. Aich, S. Ignetious, & S. Nagoriya. 2021. BoLA-DRB3 gene polymorphism and its association with lactation yield and milk constituents in crossbred cattle. Indian Journal Veterinary Sciences Biotechnology 17:71-75. https://doi.org/10.21887/ijvsbt.17.1.18
The Jamovi Project. 2022. Jamovi. Computer Software. R. https://www.jamovi.org. [December 10, 2023].
Úsuga-Monroy, C., F. Díaz, L. G. González-Herrera, J. Echeverry-Zuluaga, & A. López-Herrera. 2023. Phylogenetic analysis of the partial sequences of the env and tax BLV genes reveals the presence of genotypes 1 and 3 in dairy herds of Antioquia, Colombia. Virus Disease 34:483-497. https://doi.org/10.1007/s13337-023-00836-9
Watanuki, S., S. Takeshima, L. Borjigin, H. Sato, L. Bai, H. Murakami, R. Sato, H. Ishizaki, Y. Matsumoto, & Y. Aida. 2019. Visualizing bovine leukemia virus (BLV)-Infected cells and measuring blv proviral loads in the milk of BLV seropositive dams. Vet. Res. 50:102. https://doi.org/10.1186/s13567-019-0724-1
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