Keywords
Trematode
Small ruminants
Immunomodulation. Cytokine.
Small ruminants
Immunomodulation. Cytokine.
How to Cite
Mendes, E. A., Pereira, C. A. de J., & Lima, W. dos S. (2021). Immune response in Santa Inês sheep during Fasciola hepatica infection. Semina: Ciências Agrárias, 42(6), 3289–3304. https://doi.org/10.5433/1679-0359.2021v42n6p3289
Abstract
In the present study, we describe the proliferative response and the IFN - y, IL-10, IL-4 cytokine expression profiles in peripheral blood, and IgG production, after the experimental infection of Santa Inês sheep with 250 Fasciola hepatica metacercariae that were evaluated at 60 and 210 days post-infection(dpi). The cytokine expression profile at 60 dpi was characterized by the production of IFN - y, and IL-10, which is indicative of an initial mixed Th1/Th2 response. The modulation of the response occurred at 210 dpi with a predominance of IL-10 and IL-4 over IFN - y. Mononuclear cells from peripheral blood stimulated with F. hepatica antigen exhibited proliferative capacity at 60 dpi, whereas the response was consistent with modulation from Th1 to Th2 in the chronic phase. The IgG antibody response was more marked at 60 days than at 210 dpi, confirming the mixed-response profile. The late modulation of the T lymphocyte response in association with the predominance of IL-10 and IL-4 at 210 dpi suggests the involvement of these cytokines after the establishment of the parasites in the bile ducts. The transition from a mixed to a regulatory response in the chronic phase was also accompanied by a reduced number of eggs per gram of feces.References
Aldridge, A., & O'Neill, S. M. (2016). Fasciola hepatica tegumental antigens induce anergic-like T cells via dendritic cells in a mannose receptor dependent manner. European Journal of Immunology, 46(5), 1180-1192. doi: 10.1002/eji.201545905
Beesley, N. J., Williams, D. J. L., Paterson, S., & Hodgkinson, J. (2017). Fasciola hepatica demonstrates high levels of genetic diversity, a lack of population structure and high gene flow: possible implications for drug resistance. International Journal for Parasitology, 47(1), 11-20. doi:10.1016/j.ijpara.2016.09.0 07
Boray, J. C. (1967). Studies on experimental infections with Fasciola hepatica, with particular reference to acute fascioliasis in sheep. Annals of Tropical Medicine & Parasitology, 61(4), 439-450. doi: 10.1080/0 0034983.1967.11686513
Chauvin, A., Bouvet, G., & Boulard, C. (1995). Humoral and cellular immune responses to Fasciola hepatica experimental primary and secondary infection in sheep. International Journal for Parasitology, 25(10), 1227-1241. doi: 10.1016/0020-7519(95)00039-5
Dalton, J. P., Robinson, M. W., Mulcahy, G., O'Neill, S. M., & Donnelly, S. (2013). Immunomodulatory molecules of Fasciola hepatica: candidates for both vaccine and immunotherapeutic development. Veterinary Parasitology, 195(3-4), 272-285. doi: 10.1016/j.vetpar.2013.04.
Dracz, R. M., & Lima, W. S. (2014). Autochthonous infection of buffaloes and cattle by Fasciola hepatica in Minas Gerais, Brazil. Revista Brasileira de Parasitologia Veterinária, 23(3), 413-416. doi: 10.1590/S1 984-29612014054
Dracz, R. M., Ribeiro, V. M. A., Pereira, C. A. J., & Lima, W. S. (2016). Ocorrência de Fasciola hepatica (Linnaeus, 1758) em capivara (Hydrochoerus hydrochaeris) (Linnaeus, 1766) em Minas Gerais, Brasil. Revista Brasileira de Parasitologia Veterinária, 25(3), 364-367. doi: 10.1590/S1984-29612016021
Flynn, R. J., & Mulcahy, G. (2008). The roles of IL-10 and TGF-beta in controlling IL-4 and IFN-gamma production during experimental Fasciola hepatica infection. International Journal for Parasitology, 38(14), 1673-1680. doi: 10.1016/j.ijpara.2008.05.008
Flynn, R. J., & Musah-Eroje, M. (2020). Evasion of Host Immunity during Fasciola hepatica Infection. In M. Cancela, & G. Maggioli (Eds.), Fasciola hepatica: Methods and Protocols, Methods in Molecular Biology. (Vol. 2137, pp. 107-115). Recovered from https://doi.org/10.1007/978-1-0716-0475-5_1,© Springer Science Business Media, LLC, part of Springer Nature 2020
Furst, T., Duthaler, U., Sripa, B., Utzinger, J., & Keiser, J. (2012). Trematode infections: liver and lung flukes. Infectious disease clinics, 26(2), 399-419. doi: 10.1016/j.idc.2012.03.008
Hacariz, O., Sayers, G., Flynn, R. J., Lejeune, A., & Mulcahy, G. (2009). IL-10 and TGF-beta1 are associated with variations in fluke burdens following experimental fasciolosis in sheep. Parasite Immunology, 31(10), 613-622. doi: 10.1111/j.1365-3024.2009.01135.x
Lima, W. dos S., Soares, L. R., Barcante, T. A., Guimaraes, M. P., & Barcante, J. M. (2009) Occurrence of Fasciola hepatica (Linnaeus, 1758) infection in Brazilian cattle of Minas Gerais, Brazil. Revista Brasileira de Parasitologia Veterinária, 18(2), 27-30. doi: 10.4322/rbpv.01802006
Mendes, E. A., Mendes, T. A. O., Santos, S. L., Menezes-Souza, D., Bartholomeu, D. C., Martins, I. V. F., Silva, L.M., Lima, W. S. (2013). Expression of IL-4, IL-10 and IFN-gamma in the liver tissue of cattle that are naturally infected with Fasciola hepatica. Veterinary Parasitology, 195(1-2), 177-182. doi: 10. 1016/j.vetpar.2013.03.035
Moreau, E., & Chauvin, A. (2010). Immunity against helminths: interactions with the host and the intercurrent infections. Journal of Biomedicine and Biotechnology, 2010 (428593), 1-10. doi: 10.1155/ 2010/428593
Moreau, E., Herve, S., Yu, Z. W., & Alain, C. (2002). Modulation of sheep lymphocyte responses by Fasciola hepatica excretory-secretory products. Veterinary Parasitology, 108(3), 207-215. doi: 10. 1016/S0304-4017(02)00196-6
Moxon, J. V., Flynn, R. J., Golden, O., Hamilton, J. V., Mulcahy, G., & Brophy, P. M. (2010). Immune responses directed at egg proteins during experimental infection with the liver fluke Fasciola hepatica. Parasite Immunology, 32(2), 111-124. doi: 10.1111/j.1365-3024.2009.01171.x
Pereira, C. A. J., Oliveira, L. L. S., Coaglio, A. L., Santos, F. S. O., Cezar, R. S. M., Mendes, T., Oliveira F. L. P., Consenza, G. Lima, W. S. (2016). Anti-helminthic activity of Momordica charantia L. against Fasciola hepatica eggs after twelve days of incubation in vitro. Veterinary Parasitology, 228(15), 160-166. doi: 10.1016/j.vetpar.2016.08.025
Pleasance, J., Wiedosari, E., Raadsma, H. W., Meeusen, E., & Piedrafita, D. (2011). Resistance to liver fluke infection in the natural sheep host is correlated with a type-1 cytokine response. Parasite Immunology, 33(9), 495-505. doi: 10.1111/j.1365-3024.2011.01305.x
Ravida, A., Aldridge, A. M., Driessen, N. N., Heus, F. A., Hokke, C. H., & O'Neill, S. M. (2016). Fasciola hepatica surface coat glycoproteins contain Mannosylated and phosphorylated N-glycans and exhibit immune modulatory properties independent of the mannose receptor. PLOS Neglected Tropical Diseases, 10(4), e0004601. doi: 10.1371/journal.pntd.0004601
Rojo-Vazquez, F. A., Meana, A., Valcarcel, F., & Martinez-Valladares, M. (2012). Update on trematode infections in sheep. Veterinary Parasitology, 189(1), 15-38. doi: 10.1016/j.vetpar.2012.03.029
Ruiz-Campillo, M. T., Hernandez, V. M., Escamilla, A., Stevenson, M., Perez, J., Martinez-Moreno, Donnelly, S., Dalton, J. P. & Cwiklinski, K. (2017). Immune signatures of pathogenesis in the peritoneal compartment during early infection of sheep with Fasciola hepatica. Scientific Reports, 7(2782), 1-14. doi: 10.1038/s41598-017-03094-0
Vukman, K. V., Adams, P. N., & O'Neill, S. M. (2013b). Fasciola hepatica tegumental coat antigen suppresses MAPK signalling in dendritic cells and up-regulates the expression of SOCS3. Parasite Immunology, 35(7-8), 234-238. doi: 10.1111/pim.12033
Vukman, K. V., Adams, P. N., Metz, M., Maurer, M., & O'Neill, S. M. (2013a). Fasciola hepatica tegumental coat impairs mast cells' ability to drive Th1 immune responses. The Journal of Immunology, 190(6), 2873-2879. doi: 10.4049/jimmunol.1203011
Zhang, W. Y., Moreau, E., Hope, J. C., Howard, C. J., Huang, W. Y., & Chauvin, A. (2005). Fasciola hepatica and Fasciola gigantica: comparison of cellular response to experimental infection in sheep. Experimental Parasitology, 111(3), 154-159. doi: 10.1016/j.exppara.2005.06.005
Beesley, N. J., Williams, D. J. L., Paterson, S., & Hodgkinson, J. (2017). Fasciola hepatica demonstrates high levels of genetic diversity, a lack of population structure and high gene flow: possible implications for drug resistance. International Journal for Parasitology, 47(1), 11-20. doi:10.1016/j.ijpara.2016.09.0 07
Boray, J. C. (1967). Studies on experimental infections with Fasciola hepatica, with particular reference to acute fascioliasis in sheep. Annals of Tropical Medicine & Parasitology, 61(4), 439-450. doi: 10.1080/0 0034983.1967.11686513
Chauvin, A., Bouvet, G., & Boulard, C. (1995). Humoral and cellular immune responses to Fasciola hepatica experimental primary and secondary infection in sheep. International Journal for Parasitology, 25(10), 1227-1241. doi: 10.1016/0020-7519(95)00039-5
Dalton, J. P., Robinson, M. W., Mulcahy, G., O'Neill, S. M., & Donnelly, S. (2013). Immunomodulatory molecules of Fasciola hepatica: candidates for both vaccine and immunotherapeutic development. Veterinary Parasitology, 195(3-4), 272-285. doi: 10.1016/j.vetpar.2013.04.
Dracz, R. M., & Lima, W. S. (2014). Autochthonous infection of buffaloes and cattle by Fasciola hepatica in Minas Gerais, Brazil. Revista Brasileira de Parasitologia Veterinária, 23(3), 413-416. doi: 10.1590/S1 984-29612014054
Dracz, R. M., Ribeiro, V. M. A., Pereira, C. A. J., & Lima, W. S. (2016). Ocorrência de Fasciola hepatica (Linnaeus, 1758) em capivara (Hydrochoerus hydrochaeris) (Linnaeus, 1766) em Minas Gerais, Brasil. Revista Brasileira de Parasitologia Veterinária, 25(3), 364-367. doi: 10.1590/S1984-29612016021
Flynn, R. J., & Mulcahy, G. (2008). The roles of IL-10 and TGF-beta in controlling IL-4 and IFN-gamma production during experimental Fasciola hepatica infection. International Journal for Parasitology, 38(14), 1673-1680. doi: 10.1016/j.ijpara.2008.05.008
Flynn, R. J., & Musah-Eroje, M. (2020). Evasion of Host Immunity during Fasciola hepatica Infection. In M. Cancela, & G. Maggioli (Eds.), Fasciola hepatica: Methods and Protocols, Methods in Molecular Biology. (Vol. 2137, pp. 107-115). Recovered from https://doi.org/10.1007/978-1-0716-0475-5_1,© Springer Science Business Media, LLC, part of Springer Nature 2020
Furst, T., Duthaler, U., Sripa, B., Utzinger, J., & Keiser, J. (2012). Trematode infections: liver and lung flukes. Infectious disease clinics, 26(2), 399-419. doi: 10.1016/j.idc.2012.03.008
Hacariz, O., Sayers, G., Flynn, R. J., Lejeune, A., & Mulcahy, G. (2009). IL-10 and TGF-beta1 are associated with variations in fluke burdens following experimental fasciolosis in sheep. Parasite Immunology, 31(10), 613-622. doi: 10.1111/j.1365-3024.2009.01135.x
Lima, W. dos S., Soares, L. R., Barcante, T. A., Guimaraes, M. P., & Barcante, J. M. (2009) Occurrence of Fasciola hepatica (Linnaeus, 1758) infection in Brazilian cattle of Minas Gerais, Brazil. Revista Brasileira de Parasitologia Veterinária, 18(2), 27-30. doi: 10.4322/rbpv.01802006
Mendes, E. A., Mendes, T. A. O., Santos, S. L., Menezes-Souza, D., Bartholomeu, D. C., Martins, I. V. F., Silva, L.M., Lima, W. S. (2013). Expression of IL-4, IL-10 and IFN-gamma in the liver tissue of cattle that are naturally infected with Fasciola hepatica. Veterinary Parasitology, 195(1-2), 177-182. doi: 10. 1016/j.vetpar.2013.03.035
Moreau, E., & Chauvin, A. (2010). Immunity against helminths: interactions with the host and the intercurrent infections. Journal of Biomedicine and Biotechnology, 2010 (428593), 1-10. doi: 10.1155/ 2010/428593
Moreau, E., Herve, S., Yu, Z. W., & Alain, C. (2002). Modulation of sheep lymphocyte responses by Fasciola hepatica excretory-secretory products. Veterinary Parasitology, 108(3), 207-215. doi: 10. 1016/S0304-4017(02)00196-6
Moxon, J. V., Flynn, R. J., Golden, O., Hamilton, J. V., Mulcahy, G., & Brophy, P. M. (2010). Immune responses directed at egg proteins during experimental infection with the liver fluke Fasciola hepatica. Parasite Immunology, 32(2), 111-124. doi: 10.1111/j.1365-3024.2009.01171.x
Pereira, C. A. J., Oliveira, L. L. S., Coaglio, A. L., Santos, F. S. O., Cezar, R. S. M., Mendes, T., Oliveira F. L. P., Consenza, G. Lima, W. S. (2016). Anti-helminthic activity of Momordica charantia L. against Fasciola hepatica eggs after twelve days of incubation in vitro. Veterinary Parasitology, 228(15), 160-166. doi: 10.1016/j.vetpar.2016.08.025
Pleasance, J., Wiedosari, E., Raadsma, H. W., Meeusen, E., & Piedrafita, D. (2011). Resistance to liver fluke infection in the natural sheep host is correlated with a type-1 cytokine response. Parasite Immunology, 33(9), 495-505. doi: 10.1111/j.1365-3024.2011.01305.x
Ravida, A., Aldridge, A. M., Driessen, N. N., Heus, F. A., Hokke, C. H., & O'Neill, S. M. (2016). Fasciola hepatica surface coat glycoproteins contain Mannosylated and phosphorylated N-glycans and exhibit immune modulatory properties independent of the mannose receptor. PLOS Neglected Tropical Diseases, 10(4), e0004601. doi: 10.1371/journal.pntd.0004601
Rojo-Vazquez, F. A., Meana, A., Valcarcel, F., & Martinez-Valladares, M. (2012). Update on trematode infections in sheep. Veterinary Parasitology, 189(1), 15-38. doi: 10.1016/j.vetpar.2012.03.029
Ruiz-Campillo, M. T., Hernandez, V. M., Escamilla, A., Stevenson, M., Perez, J., Martinez-Moreno, Donnelly, S., Dalton, J. P. & Cwiklinski, K. (2017). Immune signatures of pathogenesis in the peritoneal compartment during early infection of sheep with Fasciola hepatica. Scientific Reports, 7(2782), 1-14. doi: 10.1038/s41598-017-03094-0
Vukman, K. V., Adams, P. N., & O'Neill, S. M. (2013b). Fasciola hepatica tegumental coat antigen suppresses MAPK signalling in dendritic cells and up-regulates the expression of SOCS3. Parasite Immunology, 35(7-8), 234-238. doi: 10.1111/pim.12033
Vukman, K. V., Adams, P. N., Metz, M., Maurer, M., & O'Neill, S. M. (2013a). Fasciola hepatica tegumental coat impairs mast cells' ability to drive Th1 immune responses. The Journal of Immunology, 190(6), 2873-2879. doi: 10.4049/jimmunol.1203011
Zhang, W. Y., Moreau, E., Hope, J. C., Howard, C. J., Huang, W. Y., & Chauvin, A. (2005). Fasciola hepatica and Fasciola gigantica: comparison of cellular response to experimental infection in sheep. Experimental Parasitology, 111(3), 154-159. doi: 10.1016/j.exppara.2005.06.005
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