Immune response in Santa Inês sheep during Fasciola hepatica infection

Eveline Albuquerque Mendes, Cíntia Aparecida de Jesus Pereira, Walter dos Santos Lima

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.

Keywords


Trematode; Small ruminants; Immunomodulation. Cytokine.

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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




DOI: http://dx.doi.org/10.5433/1679-0359.2021v42n6p3289

Semina: Ciênc. Agrár.
Londrina - PR
E-ISSN 1679-0359
DOI: 10.5433/1679-0359
E-mail: semina.agrarias@uel.br
Este obra está licenciado com uma Licença Creative Commons Atribuição-NãoComercial 4.0 Internacional