Immune response dynamics of recent and chronic small ruminant lentivirus infection in the male reproductive system
DOI:
https://doi.org/10.5433/1679-0359.2023v44n1p185Keywords:
Antibodies, SRLV, Small Ruminant, Breeder, Western Blot.Abstract
The objective of this study was to analyze the immune responses of bucks to small ruminant lentivirus (SRLV) with a focus on the reproductive system of males with recent and chronic infection. A total of 12 bucks were selected, six seronegative and six seropositive with chronic natural infection for more than 18 months (chronic infection group). After selecting the animals, the six seronegative males were intravenously inoculated with caprine arthritis-encephalitis virus (CAEV)-Co viral strain at a titer of 10-5,6 TCID50/mL. After viral inoculation, this group was called the recent infection group and was monitored weekly with the chronically infected group for 180 days with blood serum and seminal plasma Western Blot (WB) analysis. Of the animals with chronic SRLV infection, 18.94% (50/264) showed anti-SRLV antibodies in at least one of the samples, and 81.06% (214/264) were negative. Anti-SRLV antibodies were detected in 27.27% (36/132) of the blood serum samples from this group, while 10.60% (14/132) were reactive in the seminal plasma WB test. The animals inoculated with CAEV-Co became seropositive after the third week of viral inoculation. In this group, 31.06% (41/132) of seminal plasma samples had anti-SRLV antibodies, and of these, 70.73% (29/41) coincided with blood serum results. Of the remaining 29.27% (12/41), the seminal plasma sample of only three animals (RIA2, RIA3, and RIA5) had anti-SRLV antibodies. One of the animals with a recent infection presented anti-SRLV antibodies only in seminal plasma samples, possibly due to virus compartmentalization. Intermittent viral shedding was observed in both biological samples, regardless of the infection stage. The immune response in bucks with recent SRLV infection is more significant than in chronically infected animals. Regardless of the stage of infection, there is a fluctuation in antibody levels, therefore, this creates a risk of false-negative samples when performing the diagnosis.
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Araújo, J. F., Andrioli, A., Pinheiro, R. R., Sider, L. H., Sousa, A. L. M., Azevedo, D. A. A., Peixoto, R. M., Lima, A. M. C., Damasceno, E. M., Souza, S. C. R., & Teixeira, M. F. S. (2020). Vertical transmissibility of small ruminant lentivirus. Plos One, 15(11), e0239916. doi: 10.1371/journal.pone.0239916 DOI: https://doi.org/10.1371/journal.pone.0239916
Azevedo, D. A. A., Pinheiro, R. R., Santos, V. W. S., Damasceno, E. M., Sousa, A. L. M., Araújo, J. F., Andrioli, A., Sider, L. H., Peixoto, R. M., & Teixeira, M. F. S. (2019). Comparison of serological and molecular tests for diagnosis of caprine arthritis encephalitis and clinical evaluation of mammary glands of infected dairy goats. Acta Scientiae Veterinariae, 47(1), 1668e. doi: 10.22456/1679-9216.92281 DOI: https://doi.org/10.22456/1679-9216.92281
Azevedo, D. A. A., Santos, V. W. S., Sousa, A. L. M., Peixoto, R. M., Pinheiro, R. R., Andrioli, A., & Teixeira, M. F. S. (2017). Small ruminant lentiviruses: economic and productive losses, consequences of the disease. Arquivos do Instituto Biológico, 87(1-10), e0552016. doi: 10.1590/1808-1657000552016 DOI: https://doi.org/10.1590/1808-1657000552016
Bertoni, G., Zahno, M. L., Zanoni, R., Vogt, H. R., Peterhans, E., Ruff, G., Cheevers, W. P., Sonigo, P., & Pancino, G. (1994). Antibody reactivity to the immunodominant epitopes of the caprine arthritis-encephalitis virus gp38 transmembrane protein associates with development of arthritis. Journal of Virology, 68(11), 7139-7147. doi: 10.1128/JVI.68.11.7139-7147.1994 DOI: https://doi.org/10.1128/jvi.68.11.7139-7147.1994
Blacklaws, B. A., & Harkiss, G. D. (2010). Small ruminant lentiviruses and human immunodeficiency virus: cousins that take a long view. Current HIV Research, 8(1), 26-52. doi: 10.2174/157016210790416406 DOI: https://doi.org/10.2174/157016210790416406
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Analytical Biochemistry, 72(1-2), 248-254. doi: 10.1016/0003-2697(76)90527-3 DOI: https://doi.org/10.1016/0003-2697(76)90527-3
Burgener, A., Boutilier, J., Wachihi, C., Kimani, J., Carpenter, M., Westmacott, G., & Plummer, F. (2008). Identification of differentially expressed proteins in the cervical mucosa of HIV-1-resistant sex workers. Journal of Proteome Research, 7(10), 4446-4454. doi: 10.1021/pr800406r DOI: https://doi.org/10.1021/pr800406r
Cavalcante, F. R. A., Andrioli, A., Pinheiro, R. R., Souza, K. C., Veras, A. K. A., Lopes, T. A., Sousa, S. D., & Silva, P. A. F. (2013). Detecção do vírus da artrite encefalite caprina por nested PCR e nested RT-PCR em ovócitos e fluido uterino. Arquivos do Instituto Biológico, 80(4), 381-386. doi: 10.1590/S1808-16572013000400002 DOI: https://doi.org/10.1590/S1808-16572013000400002
Damasceno, E. M., Pinheiro, R. R., Andrioli, A., Alves, F. S. F., Lima, A. M. C., Peixoto, R. M., Araújo, J. F., Damasceno, M. S., & Brandão, I. S. (2020). Seroprevalence and associated risk factors of Mycoplasma agalactiae and investigation of coinfection with the caprine lentivirus in Rio Grande do Norte, Brazil. Tropical Animal Health and Production, 52(4), 2111-2117. doi: 10.1007/s11250-020-02234-5 DOI: https://doi.org/10.1007/s11250-020-02234-5
Dantas, T. V. M., Araújo, S. A. C., Pinheiro, R. R., Aragão, M. A. C., Silva, J. B. A., Ricarte, A. R. F., Ribeiro, A. L., & Teixeira, M. F. S. (2008). Development and standardization of an indirect ELISA for the diagnosis Maedi-Visnain sheep. Ciência Animal Brasileira, 9(1), 181-187. https://revistas.ufg.br/vet/article/view/3677/3445
Hasegawa, M. Y., Lara, M. C. C. S. H., Gaeta, N. C., Marques, J. A., Ribeiro, B. L. M., Rossi, R. S., Marques, E. C., & Gregory, L. (2017). Transmissibilidade de lentivírus de pequenos ruminantes para cabritos e cabras adultas por meio de sêmen infectado experimentalmente. Pesquisa Veterinária Brasileira, 37(8), 805-812. doi: 10.1590/S0100-736X2017000800005 DOI: https://doi.org/10.1590/s0100-736x2017000800005
Jarczak, J., Kaba, J., Reczynska, D., & Bagnicka, E. (2016). Impaired expression of cytokines as a result of viral infections with an emphasis on small ruminant lentivirus infection in goats. Viruses, 8(7), 186. doi: 10.3390/v8070186 DOI: https://doi.org/10.3390/v8070186
Jarczak, J., Stoniewska, D., Kaba, J., & Bagnicka, E. (2019). The expression of cytokines in the milk somatic cells, blood leukocytes and serum of goats infected with small ruminant lentivirus. BMC Veterinary Research, 15(1), 1-11. doi: 10.1186/s12917-019-2182-4 DOI: https://doi.org/10.1186/s12917-019-2182-4
Larruskain, A., & Jugo, B. M. (2013). Retroviral infections in sheep and goats: small ruminant lentiviruses and host interaction. Viruses, 5(8), 2043-2061. doi: 10.3390/v5082043 DOI: https://doi.org/10.3390/v5082043
Li, Y., Yang, D., Wang, J. Y., Yao, Y., Zhang, W. Z., Wang, L. J., Cheng, D. J., Yang, F. K., Zhang, F. M., Zhuang, M., & Ling, H. (2014). Critical amino acids within the human immunodeficiency virus type 1 envelope glycoprotein V4 N- and C-terminals contribute to virus entry. Plos One, 9(1), e86083. doi: 10.1371/journal.pone.0086083 DOI: https://doi.org/10.1371/journal.pone.0086083
Lorenzi, J. C. C., & Coelho-Castelo, A. A. M. (2011). Resposta imune contra infecções virais. Scire Salutis, 1(2), 35-44. doi: 10.6008/ESS2236-9600.2011.002.0004 DOI: https://doi.org/10.6008/ESS2236-9600.2011.002.0004
Marinho, R. C., Martins, G. R., Souza, K. C., Sousa, A. L. M., Silva, S. T. C., Nobre, J. A., & Teixeira, M. F. S. (2018). Duplex nested-PCR for detection of small ruminant lentiviruses. Brazilian Journal of Microbiology, 49(1), 83-92. doi: 10.1016/j.bjm.2018.04.013 DOI: https://doi.org/10.1016/j.bjm.2018.04.013
Minguijón, E., Reina, R., Pérez, M., Polledo, L., Villoria, M., Ramírez, H., Leginagoikoa, I., Badiola, J. J., García-Marín, J. F., Andrés, D., Luján, L., Amorena, B., & Juste, R. A. (2015). Small ruminant lentivirus infections and diseases. Veterinary Microbiology, 181(1-2), 75-78. doi: 10.1016/j.vetmic.2015.08.007 DOI: https://doi.org/10.1016/j.vetmic.2015.08.007
Mital, P., Hinton, B. T., & Dufour, J. M. (2011). The blood-testis and blood-epididymis barriers are more than just their tight junctions. Biology of Reproduction, 84(5), 851-858. doi: 10.1095/biolreprod.110.087452 DOI: https://doi.org/10.1095/biolreprod.110.087452
Paula, N. R. O., Andrioli, A., Cardoso, J. F. S., Pinheiro, R. R., Sousa, F. M. L., Souza, K. C., Alves, F. S. F., Campello, C. C., Ricarte, A. R. F., & Teixeira, M. F. S. (2009). Profile of the caprine arthritis-encephalitis virus (CAEV) in blood, semen from bucks naturally and experimentally infected in the semi-arid region of Brazil. Small Ruminant Research, 85(1), 27-33. doi: 10.1016/j.smallrumres.2009.06.018 DOI: https://doi.org/10.1016/j.smallrumres.2009.06.018
Peixoto, R. M., Andrioli, A., Pinheiro, R. R., Alves, F. S. F., Santos, V. W. S., Sousa, M. M., Azevedo, D. A. A., Damasceno, E. M., & Teixeira, M. F. S. (2018a). Mycoplasma agalactiae em rebanhos leiteiros no estado do Ceará em associação com o vírus da artrite encefalite caprina. Acta Scientiae Veterinariae, 46(1), 1533e. doi: 10.22456/1679-9216.86091 DOI: https://doi.org/10.22456/1679-9216.81885
Peixoto, R. M., Sousa, A. L. M., Araújo, J. F., & Pinheiro, R. R. (2021). Western Blot in immunodiagnosis of small ruminant lentivirus. Acta Scientiae Veterinariae, 49(1), 1781e. doi: 10.22456/1679-9216.109822 DOI: https://doi.org/10.22456/1679-9216.109822
Peixoto, R. M., Teixeira, M. F. S., Andrioli, A., Pinheiro, R. R., Silva, A. A. S., Aguiar, T. D. F., Azevedo, D. A. A., & Sousa, A. L. M. (2018b). Prospectives of herbal remedies in the treatment of caprine semen infected by caprine arthritis encephalitis virus. Medicina Veterinária, 12(3), 193-201. doi: 10.26605/medvet-v12n3-2395 DOI: https://doi.org/10.26605/medvet-v12n3-2395
Peterson, K., Brinkhof, J., Houwers, D. J., Colenbrander, B., & Gadella, B. M. (2008). Presence of pro-lentiviral DNA in male sexual organs and ejaculates of small ruminants. Theriogenology, 69(4), 433-442. doi: 10.1016/j.theriogenology.2007.10.013 DOI: https://doi.org/10.1016/j.theriogenology.2007.10.013
Pisoni, G., Bertoni, G., Manarolla, G., Vogt, H. R., Scaccabarozzi, L., Locatelli, C., & Moroni, P. (2010). Genetic analysis of small ruminant lentiviruses following lactogenic transmission. Virology, 407(1), 91-99. doi: 10.1016/j.virol.2010.08.004 DOI: https://doi.org/10.1016/j.virol.2010.08.004
Qu, N., Ogawa, Y., Kuramasu, M., Negahori, K., Sakabe, K., & Itoh, M. (2019). Immunological microenvironment in the testis. Reproductive Medicine and Biology, 9(1), 24-31. doi: 10.1002/rmb2.12293 DOI: https://doi.org/10.1002/rmb2.12293
Rachid, A., Croisé, B., Russo, P., Vignoni, M., Lacerenza, D., Rosati, S., Kuzmak, J., & Valas, S. (2013). Diverse host-virus interactions following caprine arthritis-encephalitis virus infection in sheep and goats. Journal of General Virology, 94(3), 634-642. doi: 10.1099/vir.0.044768-0 DOI: https://doi.org/10.1099/vir.0.044768-0
Ramírez, H., Reina, R., Bertolotti, L., Cenoz, A., Hernández, M. M., San Román, B., & De Andrés, D. (2012). Study of compartmentalization in the visna clinical form of small ruminant lentivirus infection in sheep. BMC Veterinary Research, 8(8), 1-12. doi: 10.1186/1746-6148-8-8 DOI: https://doi.org/10.1186/1746-6148-8-8
Ramírez, H., San Román, B., Glaria, I., Reina, R., Hernández, M. M., Andrés, X., Cresco, H., Hichou, B., Cianca, S., Goni, C., Grandas, A., García-Pastor, L., Vijil, L. E., Quintín, F., Grilló, M. J., Andrés, D., & Amorena, B. (2009). Antibody based diagnosis of small ruminant lentivirus infection in seminal fluid. Theriogenology, 72(8), 1085-1096. doi: 10.1016/j.theriogenology.2009.06.028 DOI: https://doi.org/10.1016/j.theriogenology.2009.06.028
Ravazzolo, A. P., Nenci, C., Vogt, H. R., Waldvogel, A., Obexer-Ruff, G., Peterhans, E., & Bertoni, G. (2006). Viral load, organ distribution, histopathological lesions, and cytokine mRNA expression in goats infected with a molecular clone of the caprine arthritis encephalitis virus. Virology, 350(1), 116-127. doi: 10.1016/j.virol.2006.02.014 DOI: https://doi.org/10.1016/j.virol.2006.02.014
Rodrigues, A. S., Brito, R. L. L., Pinheiro, R. R., Dias, R. P., Alves, S. M., Souza, T. S., Souza, K. C., Azevedo, D. A. A., Andrioli, A., Magalhães, D. C. T., & Teixeira, M. F. S. (2014). Padronização do Elisa indireto e Western Blot para diagnóstico da artrite-encefalite caprina. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 66(2), 417-424. doi: 10.1590/1678-41626303 DOI: https://doi.org/10.1590/1678-41626303
Sabatte, J., Faigle, W., Caballos, A., Morelle, W., Rodríguez, C. R., Lenicov, F. R., Thépaut, M., Fieschi, F., Malchiodi, E., Férnandez, M., Arezana-Seisdedos, F., Lortat-Jacob, H., Michalski, J. C., Geffner, J., & Amigorema, S. (2011). Semen clusterin is a novel DC-SIGN ligand. The Journal of Immunology, 187(10), 5299-5309. doi: 10.4049/jimmunol.1101889 DOI: https://doi.org/10.4049/jimmunol.1101889
Santos, K. F., Eloy, A. M. X., Matos, M. N. C., Peixoto, R. M., Aragão, P. T. T. D., Pinheiro, R. R., & Cunha, R. M. S. (2019). Use of proteomics in the study of the acute phase of caprine arthritis encephalitis in seminal plasma. Small Ruminant Research, 181(2019), 39-44. doi: 10.1016/j.smallrumres.2019.10.004 DOI: https://doi.org/10.1016/j.smallrumres.2019.10.004
Soares, R., Armindo, R. D., & Rocha, G. A. (2014). Imunodeficiência e o sistema imunitário: o comportamento em portadores de HIV. Arquivos de Medicina, 28(2), 113-121. http://bibliobase.sermais.pt:8008/ BiblioNET/Upload/PDF16/013116%20ARQ%20MEDICINA%202014%20v28%20n4%20p113-22.pdf
Sousa, M. M., Andrioli, A., Pinheiro, R. R., Alves, F. S. F., Santos, V. W. S., Damasceno, E. M., Araújo, J. F., Sousa, A. L. M., & Vieira, L. S. (2019). An epidemiological study of caprine arthritis encephalitis virus (CAEV) in breeder goats from Northeastern Brazil. Semina: Ciências Agrárias, 40(5), 1857-1866. doi: 10.5433/1679-0359.2019v40n5p1857 DOI: https://doi.org/10.5433/1679-0359.2019v40n5p1857
Souza, K. C., Pinheiro, R. R., Santos, D. O., Brito, R. L. L., Rodrigues, A. S., Sider, L. H., Paula, N. R. O., Avila, A. A., Cardoso, J. F. S., & Andrioli, A. (2013). Transmission of the caprine arthritis-encephalitis vírus through artificial insemination. Small Ruminant Research, 109(2-3), 193-198. doi: 10.1016/j.smallrumres.2012.07.031 DOI: https://doi.org/10.1016/j.smallrumres.2012.07.031
Souza, T. S., Costa, J. N., Martinez, P. M., Costa, A. O., Neto, & Pinheiro, R. R. (2010). Anticorpos contra o vírus da língua azul em rebanhos ovinos da Microrregião de Juazeiro, Bahia. Arquivos do Instituto Biológico, 77(3), 419-427. doi: 10.1590/1808-1657v77p4192010 DOI: https://doi.org/10.1590/1808-1657v77p4192010
Stonos, N., Wootton, S. K., & Karraow, N. (2014). Immunogenetics of small ruminant lentiviral infections. Viruses, 6(8), 3311-3333. doi: 10.3390/v6083311 DOI: https://doi.org/10.3390/v6083311
Trujillo, J. D., Hötzel, K. J., Snekvik, K. R., & Cheevers, W. P. (2004). Antibody response to the surface envelope of caprine arthritis-encephalitis lentivirus: disease status is predicted by SU antibody isotype. Virology, 325(1), 129-136. doi: 10.1016/j.virol.2004.03.048 DOI: https://doi.org/10.1016/j.virol.2004.03.048
Turchetti, A. P., Paniago, J. J., Costa, L. F., Cruz, J. C., Braz, G. F., Gouveia, A. M., Paixão, T. A., Santos, R. L., & Heinemann, M. B. (2013). Distribution of caprine arthritis encephalitis vírus provirus, RNA, and antigen in the reproductive tract of one naturally and seven experimentally infected bucks. Theriogenology, 80(8), 933-939. doi: 10.1016/j.theriogenology.2013.07.021 DOI: https://doi.org/10.1016/j.theriogenology.2013.07.021
Winnall, W. R., Muir, J. A., & Hedger, M. P. (2011). Rat resident testicular macrophages have an alternatively activated phenotype and constitutively produce interleukin-10 in vitro. Journal of Leukocyte Biology, 90(1), 133-143. doi: 10.1189/jlb.1010557 DOI: https://doi.org/10.1189/jlb.1010557
World Organization of Animal Health - OIE (2008). Terrestrial manual. Caprine arthritis/encephalitis & Maedi-visna. (6th ed.). Paris, France: Office International des Epizooties, 2008. http://www.oie.int/doc/ged/D7710.pdf.
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