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A Taenia crassiceps factor induces apoptosis of spleen CD4+T cells and TFG-β and Foxp3 gene expression in mice

Published online by Cambridge University Press:  08 April 2015

N. Zepeda ,
R. Tirado ,
N. Copitin ,
S. Solano ,
A.M. Fernández ,
P. Tato  and
J.L. Molinari
N. Zepeda
Affiliation:
Departamento de Bioquímica y Biología Estructural, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, México, D.F.
R. Tirado
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México, México, D.F.
N. Copitin
Affiliation:
Departamento de Bioquímica y Biología Estructural, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, México, D.F.
S. Solano
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México, México, D.F.
A.M. Fernández
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México, México, D.F.
P. Tato
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México, México, D.F.
J.L. Molinari*
Affiliation:
Departamento de Bioquímica y Biología Estructural, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, México, D.F.
*
*E-mail: [email protected]
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Abstract

This study was undertaken to determine whether a parasite substance produces structural pathology in the mouse spleen. A low-molecular-weight Taenia crassiceps metacestode factor (MF) isolated from the peritoneal fluid of female mice infected with T. crassiceps metacestodes induced pathological and immunological changes in mouse spleen cells in vivo. Electron microscopy and confocal microscopy revealed severe changes in the spleen histoarchitecture of T. crassiceps-infected and MF-treated mice. Apoptotic degenerated spleen cells were observed in the white and red pulps and were more conspicuous in the white pulp of the spleen from the T. crassiceps-infected mice than in that of the MF-treated mice. Flow cytometry analysis revealed that the numbers of spleen CD4+T cells were significantly lower in both experimental groups than in control mice. The ex vivo expression of transforming growth factor (TGF)-β and factor Foxp3 were significantly higher in splenocytes of the experimental mice than the basal expression observed in the control cells. These findings may have potential applications for a better understanding of the host–parasite relationship in human neurocysticercosis.

Type
Research Papers
Information
Journal of Helminthology , Volume 90 , Issue 2 , March 2016 , pp. 223 - 231
Copyright
Copyright © Cambridge University Press 2015 

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References

Arechavaleta, F., Molinari, J.L. & Tato, P. (1998) A Taenia solium metacestode factor nonspecifically inhibits cytokine production. Parasitology Research 84, 117–122.Google Scholar
Ashwell, G. (1957) Colorimetric analysis of sugars. pp. 73–84 in Colowick, S.P. & Kaplan, N.O. (Eds) Methods in enzymology, Vol. III . New York, Academic Press.Google Scholar
Bettelli, E., Carrier, Y., Gao, W., Korn, T., Strom, T.B., Oukka, M., Weiner, H.L. & Kuchroo, V.K. (2006) Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441, 235–238.Google Scholar
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, 248–254.Google Scholar
Bueno, E.C., Vaz, A.J., Machado, L.R., Livramento, J.A., Avila, S.L. & Ferreira, A.W. (2001) Antigen-specific suppression of cultured lymphocytes from patients with neurocysticercosis. Clinical and Experimental Immunology 126, 304–310.CrossRefGoogle ScholarPubMed
Chen, W., Jin, W., Hardegen, N., Leim, K.J., Li, L., Marinos, N., McGrady, G. & Wahl, S.M. (2003) Conversion of peripheral CD4+CD25 −  naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. Journal of Experimental Medicine 198, 1875–1886.Google Scholar
Escobar, A. (1983) The pathology of neurocysticercosis. pp. 27–54 in Palacios, E., Rodriguez, J. & Taveras, J.M. (Eds) Cysticercosis of the central nervous system. Springfield, Charles C. Thomas.Google Scholar
Everhart, M.E., Kuhn, R.E. & Zelmer, D.A. (2004) Infrapopulation dynamics of a wild strain of Taenia crassiceps (WFU) (Cestoda: Taeniidae) in BALB/cJ mice. Journal of Parasitology 90, 79–84.Google Scholar
Finney, C.A.M., Taylor, M.D., Wilson, M.S. & Maizels, R.M. (2007) Expansion and activation of CD4(+)CD25(+) regulatory T cells in Heligmosomoides polygyrus infection. European Journal of Immunology 37, 1874–1886.Google Scholar
Fontana, A., Frei, K., Bodmer, S., Hofer, E., Schreier, M.H., Palladino, M.A. Jr & Zinkernagel, R.M. (1989) Transforming growth factor-beta inhibits the generation of cytotoxic T cells in virus-infected mice. Journal of Immunology 143, 3230–3234.CrossRefGoogle ScholarPubMed
Gómez-García, L., Rivera-Montoya, I., Rodríguez-Sosa, M. & Terrazas, L.I. (2006) Carbohydrate components of Taenia crassiceps metacestodes display Th2-adjuvant and anti-inflammatory properties when co-injected with bystander antigen. Parasitology Research 99, 440–448.Google Scholar
Grainger, J.R., Smith, K.A., Hewitson, J.P., McSorley, H.J., Harcus, Y., Filbey, K.J., Finney, C.A., Greenwood, E.J., Knox, D.P., Wilson, M.S., Belkaid, Y., Rudensky, A.Y. & Maizels, R.M. (2010) Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-β pathway. Journal of Experimental Medicine 207, 2331–2341.CrossRefGoogle ScholarPubMed
Kehri, J.H., Wakefield, L.M., Roberts, A.B., Jakowlew, S., Alvarez-Mon, M., Derynck, R., Sporn, M.B. & Fauci, A.S. (1986) Production of transforming growth factor beta by human T lymphocytes and its potential role in the regulation of T cell growth. Journal of Experimental Medicine 163, 1037–1050.Google Scholar
Kehri, J.H., Thevenin, C., Rieckmann, P. & Fauci, A.S. (1991) Transforming growth factor-beta suppresses human B lymphocyte Ig production by inhibiting synthesis and the switch from the membrane form to the secreted form of Ig mRNA. Journal of Immunology 146, 4016–4023.Google Scholar
Molinari, J.L., Tato, P., Reynoso, O.A. & Cázares, J.M. (1990) Depressive effect of a Taenia solium cysticercus factor on cultured human lymphocytes stimulated with phytohemagglutinin. Annals of Tropical Medicine and Parasitology 84, 205–208.Google Scholar
Molinari, J.L., Soto, R., Tato, P., Rodriguez, D., Retana, A., Sepulveda, J. & Palet, A. (1993) Immunization against porcine cysticercosis in an endemic area in Mexico: a field and laboratory study. American Journal of Tropical Medicine and Hygiene 49, 502–512.Google Scholar
Molinari, J.L., Tato, P., Rodriguez, D., Solano, S., Rubio, M. & Sepulveda, J. (1998) Impairment of the inflammatory reaction on implanted Taenia solium metacestodes in mice by a T. solium RNA-peptide: a scanning microscopy study. Parasitology Research 84, 173–180.CrossRefGoogle Scholar
Peón, A.N., Espinosa-Jiménez, A. & Terrazas, L.I. (2013) Immunoregulation by Taenia crassiceps and its antigens. Biomed Research International 2013, Article ID 49858, doi 10.1155/2013/498583.Google Scholar
Rodríguez-Sosa, M., Rivera-Montoya, I., Espinosa, A., Romero-Grijalva, M., López-Flores, R., González, J. & Terrazas, L.I. (2006) Acute cysticercosis favours rapid and more severe lesions caused by Leishmania major and Leishmania mexicana infection, a role for alternatively activated macrophages. Cellular Immunology 242, 61–71.Google Scholar
Rubio, M., Tato, P., Govezensky, T. & Molinari, J.L. (1998) Depressed immunity to a Salmonella typhimurium vaccine in mice experimentally parasitized by Taenia crassiceps . Veterinary Parasitology 74, 179–189.Google Scholar
Sanz, C.R. (1987) Host response in childhood neurocysticercosis. Some pathological aspects. Child's Nervous System 3, 206–207.CrossRefGoogle ScholarPubMed
Sciutto, E., Fragoso, G., Baca, M., De la Cruz, V., Lemus, L. & Lamoyi, E. (1995) Depressed T-cell proliferation associated with susceptibility to experimental Taenia crassiceps infection. Infection and Immunity 63, 2277–2281.Google Scholar
Shabaana, A.K., Venkatasubramani, R., Narayan, N.S., Hoessli, D.C. & Dharmanlingam, K. (2001) Cytokine profiles in paraffin-embedded biopsy samples of lepromatous leprosy patients: semi-quantitative measure of cytokine mRNA using RT-PCR. International Journal of Leprosy and Other Mycobacterial Diseases 3, 204–214.Google Scholar
Solano, S., Zepeda, N., Copitin, N., Fernandez, A.M., Tato, P. & Molinari, J.L. (2015) A Taenia crassiceps metacestode factor enhances ovarian follicle atresia and oocyte degeneration in female mice. Journal of Helminthology 89, 49–57.Google Scholar
Spolski, R.J., Corson, J., Thomas, P.G. & Kuhn, R.E. (2000) Parasite-secreted products regulate the host response to larval Taenia crassiceps . Parasite Immunology 22, 297–305.CrossRefGoogle ScholarPubMed
Sun, Y., Li, Y., Luo, D. & Liao, D.J. (2012) Pseudogenes as weaknesses of ACTB (Actb) and GAPDH (Gapdh) used as reference genes in reverse transcription and polymerase chain reactions. PloS One 7, e41659.Google Scholar
Tato, P., Castro, A.M., Rodríguez, D., Soto, R., Arechavaleta, F. & Molinari, J.L. (1995) Suppression of murine lymphocyte proliferation induced by a small RNA purified from the Taenia solium metacestode. Parasitology Research 81, 181–187.Google Scholar
Tato, P., White, A.C. Jr, Willms, K., Rodríguez, D., Solano, S., Sepulveda, J. & Molinari, J.L. (1996) Immunosuppression and inhibition of inflammation in mice induced by a small Taenia solium RNA-peptide to implanted T. solium metacestodes. Parasitology Research 82, 590–597.Google Scholar
Yang, M., Yang, C. & Mine, Y. (2010) Multiple T cell epitope peptides suppress allergic responses in an egg allergy mouse model by the elicitation of forkhead box transcription factor 3- and transforming growth factor-beta-associated mechanisms. Clinical and Experimental Allergy 40, 668–678.Google Scholar
Zepeda, N., Copitin, N., Solano, S., González, M., Fernández, A.M., Tato, P. & Molinari, J.L. (2011a) Taenia crassiceps: infections of male mice lead to severe disruption of seminiferous tubule cells and increased apoptosis. Experimental Parasitology 127, 153–159.CrossRefGoogle ScholarPubMed
Zepeda, N., Copitin, N., Solano, S., Fernández, A.M., Tato, P. & Molinari, J.L. (2011b) Taenia crassiceps: a secretion-substance of low molecular weight leads to disruption and apoptosis of seminiferous epithelium cells in male mice. Experimental Parasitology 128, 184–191.Google Scholar