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A Taenia crassiceps metacestode factor enhances ovarian follicle atresia and oocyte degeneration in female mice

Published online by Cambridge University Press:  20 August 2013

S. Solano ,
N. Zepeda ,
N. Copitin ,
A.M. Fernandez ,
P. Tato  and
J.L. Molinari
S. Solano
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México, 04510México, D.F., México
N. Zepeda
Affiliation:
Departamento de Bioquímica y Biología Estructural, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, 04510México D.F., México
N. Copitin
Affiliation:
Departamento de Bioquímica y Biología Estructural, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, 04510México D.F., México
A.M. Fernandez
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México, 04510México, D.F., México
P. Tato
Affiliation:
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México, 04510México, D.F., México
J.L. Molinari*
Affiliation:
Departamento de Bioquímica y Biología Estructural, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, 04510México D.F., México
*
*Fax: +52 55–56-22–56-30 E-mail: [email protected]
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Abstract

The histopathological effects of Taenia crassiceps infection or T. crassiceps metacestode factor inoculation on the mouse ovary were determined using six female mice in three groups: infected mice, mice inoculated with the metacestode factor and control mice. The control group was subcutaneously inoculated with healthy peritoneal fluid. The infected group was intraperitoneally inoculated with 40 T. crassiceps metacestodes, and the metacestode factor group was subcutaneously inoculated with T. crassiceps metacestode factor (MF). Light and electron microscopy and TUNEL (terminal deoxynucleotidyl transferase (TdT)-mediated dUTP nick end labelling) assays revealed a significant increase in ovarian follicular atresia (predominantly in antral/preovulatory stages of development), oocyte degeneration (P< 0.05), and a decrease in the amount of corpus luteum in follicles of mice infected and inoculated with MF compared with the control group. Significant abnormalities of the granulosa cells and oocytes of the primordial, primary and secondary ovarian follicles occurred in both treated mouse groups (P< 0.05) compared with no degeneration in the control group. These pathological changes in female mice either infected with T. crassiceps metacestodes or inoculated with T. crassiceps MF may have consequences for ovulation and fertility.

Type
Research Papers
Information
Journal of Helminthology , Volume 89 , Issue 1 , January 2015 , pp. 49 - 57
Copyright
Copyright © Cambridge University Press 2013 

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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
Arteaga-Silva, M., Vargas-Villavicencio, J.A., Vigueras-Villaseñor, R.M., Rodríguez-Dorantes, M. & Morales-Montor, J. (2009) Taenia crassiceps infection disrupts estrous cycle and reproductive behavior in BALB/c mice. Acta Tropica 109, 141–145.Google Scholar
Ashwell, G. (1957) Methods in enzymology III. 73 pp. New York, Academic Press.Google Scholar
Bothelo, M.C., Soares, R., Vale, N., Ribeiro, R., Camilo, V., Almeida, R., Medeiros, R., Gomes, P., Machado, J.C. & Correia da Costa, J.M. (2010) Schistosoma haematobium: Identification of new estrogenic molecules with estradiol antagonist activity and ability to inactivate receptor in mammalian cells. Experimental Parasitology 126, 526–535.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.CrossRefGoogle ScholarPubMed
Cardenas, G., Valdez, R., Saenz, B., Bottasso, O., Fragoso, G., Sciutto, E., Romano, M.C. & Fleury, A. (2012) Impact of Taenia solium neurocysticercosis upon endocrine status and its relation with immuno-inflammatory parameters. International Journal for Parasitology 42, 171–176.Google Scholar
Chen, L., Russell, P.T. & Larsen, W.J. (1993) Functional significance of cumulus expansion in the mouse: roles for the preovulatory synthesis of hyaluronic acid within the cumulus mass. Molecular Reproduction & Development 34, 87–93.Google Scholar
Dennis, R.D., Baumeister, S., Geyer, R., Peter-Katalinic, J., Hartmann, R., Egge, H., Geyer, E. & Weigandt, H. (1992) Glycosphingolipids in cestodes. Chemical structures of ceramide monosaccharide, disaccharide, trisaccharide and tetrasaccharide from metacestodes of the fox tapeworm, Taenia crassiceps (Cestoda: Cyclophyllidea). European Journal of Biochemistry 207, 1053–1062.Google Scholar
Dharma, S.J., Kelkar, R.L. & Nandedkar, T.D. (2003) Fas and Fas ligand protein and mRNA in normal and atretic mouse ovarian follicles. Reproduction 126, 783–789.CrossRefGoogle ScholarPubMed
Elvin, J.A., Changning, Y. & Matzuk, M.M. (2000) Oocyte-expressed TGF-β superfamily members in female fertility. Molecular and Cellular Endocrinology 159, 1–5.Google Scholar
Everhart, M.E., Kuhn, R.E. & Zelmer, D.A. (2004) Intrapopulation dynamics of a wild strain of Taenia crassiceps (WFU) (Cestoda: Taeniidae) in Balb/ccj mice. Journal of Parasitology 90, 79–84.Google Scholar
Herrera, L.A., Tato, P., Molinari, J.L., Perez, E., Dominguez, H. & Ostrosky-Wegman, P. (2003) Induction of DNA damage in human lymphocytes treated with a soluble factor secretion by Taenia solium metacestodes. Teratogenesis Carcinogenesis and Mutagenesis Supplement 1, 79–83.CrossRefGoogle Scholar
Hirchfield, A.N. (1988) Size-frequency analysis of atresia in cycling rats. Biology of Reproduction 38, 1181–1188.Google Scholar
Hirchfield, A.N. (1991) Development of follicles in the mammalian ovary. International Review of Cytology 124, 43–101.Google Scholar
Hsueh, A.J.W., Billig, H. & Safriri, A. (1994) Ovarian follicle atresia: a hormonally controlled apoptotic process. Endocrine Reviews 15, 707–724.Google Scholar
Kaipia, A. & Hsueh, A.J.W. (1997) Regulation of ovarian follicle atresia. Annual Review of Physiology 59, 349–363.Google Scholar
Keer, J.F., Wyllie, A.H. & Currie, A.R. (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. British Journal of Cancer 26, 239–257.CrossRefGoogle Scholar
Kroemer, G., Galluzzi, L., Vandenabeele, P., Abrams, J., Alnemri, E.S., Baehrecke, E.H., Blagosklonny, M.V., El-Deiry, W.S., Goldstein, P. & Green, D.R.et al. (2009) Classification of cell death: Recommendations of the nomenclature committee on cell death. Cell Death and Differentiation 16, 3–11.Google Scholar
Lin, Y.C., Rikihisa, Y., Kono, H. & Gu, Y. (1990) Effects of larval tapeworm (Taenia taeniaeformis) infection on reproductive functions in male and female host rats. Experimental Parasitolology 70, 344–352.CrossRefGoogle ScholarPubMed
Mizushima, N., Koike, R., Kohsaka, H., Kushi, Y., Handa, S., Yagita, H. & Miyasaka, N. (1996) Ceramide induces apoptosis via CPP32 activation. FEBS Letters 395, 267–271.CrossRefGoogle ScholarPubMed
Molinari, J.L., Tato, P., Reynoso, O.A. & Cazares, J.M.L. (1990) Depressive effect of a Taenia solium cysticercus factor on cultured human lymphocytes stimulated with phytohemagglutinin. Pathogens and Global Health 84, 205–208.Google Scholar
Rikihisa, Y., Lin, Y.C. & Fukaya, T. (1985) Taenia taeniaeformis: Inhibition of rat testosterone production by excretory–secretory product of the cultured metacestode. Experimental Parasitology 58, 147–155.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
Spolski, R.J., Corson, J., Thomas, P.G. & Kuhn, R.E. (2000) Parasite-secretion products regulate the host response to larval Taenia crassiceps. Parasite Immunology 22, 297–305.Google Scholar
Su, Y.Q., Sugiura, K., Li, Q., Wigglesworth, K., Matzuc, M.M. & Eppig, J.J. (2010) Mouse oocytes enable LH-induced maturation of the cumulus–oocyte complex via promoting EGF receptor-dependent signaling. Molecular Endocrinology 24, 1230–1239.Google Scholar
Tato, P., Castro, A.M., Rodriguez, 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
Teilmann, S.C. (2005) Differential expression and localization of connexin-37 and connexin-43 in follicles of different stages in the 4-week-old mouse ovary. Molecular and Cellular Endocrinology 234, 27–35.Google Scholar
Tilly, J.L. (1996) Apoptosis and ovarian function. Reviews of Reproduction 1, 162–172.Google Scholar
van der Hoek, K.H., Maddocks, S., Woodhouse, C.M., van Rooijen, N., Robertson, S.A. & Norman, R.J. (2000) Intrabursal injection of clodronate liposomes causes macrophages depletion and inhibits ovulation in the mouse ovary. Biology of Reproduction 62, 1059–1066.CrossRefGoogle ScholarPubMed
Wu, R., van der Hoek, K.H., Ryan, N.K., Norman, R.J. & Robker, R.L. (2004) Macrophage contribution to ovarian function. Human Reproduction Update 10, 119–133.Google Scholar
Zepeda, N., Solano, S., Copitin, N., Fernández, A.M., Hernández, L., Tato, P. & Molinari, J.L. (2010) Decrease of peritoneal inflammatory CD4, CD8, CD19 lymphocytes and apoptosis of eosinophils in a murine Taenia crassiceps infection. Parasitology Research 107, 1129–1135.Google Scholar
Zepeda, N., Copitin, N., Solano, S., González, M., Fernandez, A.M., Tato, P. & Molinari, J.L. (2011a) Taenia crassiceps: Infections of male mice lead to severe disruption of seminiferous tubules cells and increased apoptosis. Experimental Parasitology 127, 153–159.Google Scholar
Zepeda, N., Copitin, N., Solano, S., Fernandez, 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