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Structural analysis of toad oviductal mucosa in relation to jelly components secretion throughout the reproductive cycle

Published online by Cambridge University Press:  22 November 2012

Claudia Alejandra Crespo ,
Inés Ramos ,
Marcela Fátima Medina ,
Susana Beatriz Cisint ,
Ana Lucrecia Iruzubieta Villagra  and
Silvia Nélida Fernández
Claudia Alejandra Crespo
Affiliation:
Superior Institute of Biological Research, National Council for Scientific and Technical Research, National University of Tucumán, Chacabuco 461, Tucumán 4000, Argentina.
Inés Ramos
Affiliation:
Superior Institute of Biological Research, National Council for Scientific and Technical Research, National University of Tucumán, Chacabuco 461, Tucumán 4000, Argentina.
Marcela Fátima Medina
Affiliation:
Superior Institute of Biological Research, National Council for Scientific and Technical Research, National University of Tucumán, Chacabuco 461, Tucumán 4000, Argentina.
Susana Beatriz Cisint
Affiliation:
Superior Institute of Biological Research, National Council for Scientific and Technical Research, National University of Tucumán, Chacabuco 461, Tucumán 4000, Argentina.
Ana Lucrecia Iruzubieta Villagra
Affiliation:
Superior Institute of Biological Research, National Council for Scientific and Technical Research, National University of Tucumán, Chacabuco 461, Tucumán 4000, Argentina.
Silvia Nélida Fernández*
Affiliation:
Superior Institute of Biological Research, National University of Tucumán, Chacabuco 461, Tucumán 4000, Argentina.
*
All correspondence to: Silvia N. Fernández. Superior Institute of Biological Research, National University of Tucumán, Chacabuco 461, Tucumán 4000, Argentina. Tel: +54 0381 424 7752/7005. Fax: +54 0381 424 7752/7044. e-mail: sfernandez@fbqf.unt.edu.ar
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Summary

In amphibians, the components of the jelly coats that surround the oocytes at the time of fertilization and coordinate gamete interaction are secreted by the oviduct. We analysed the histological variations in the mucosa of the oviductal pars convoluta (PC) of Rhinella arenarum during the reproductive cycle and its relationship with secretion. During the preovulatory period, the mucosa reaches a high degree of morphological and functional development, with a large number of epithelial (ESC) and glandular secretory cells (GSC) loaded with contents that are secreted into the oviductal lumen. During the ovulatory period, the secretory cells (SC) of both layers present maximum secretory activity through apocrinia and merocrinia. While the ESC located at the tips of the folds release their content directly in contact with the oocytes, the GSC secrete material from the bottom of the epithelial folds that, by interaction with the secretion of the ESC in the lateral faces, form a product with a certain degree of organization. Secretion is a continuous process with formation of coats of increasing complexity from the intermediate proximal zone (IPZ) to the pars convoluta (pc) itself, and the passage of the oocyte is a requisite for the organization of the jelly coats around the gamete.

During the early postovulatory period, although there is a marked decrease in the number and volume of the SC, the ESC still release material into the oviductal lumen. In the late postovulatory period the morphological characteristics of the PC begin to recovery although there is no evidence of secretion.

Keywords

AmphibianFertilizationJelly coatsOviductal secretionReproductive cycle
Type
Research Article
Information
Zygote , Volume 22 , Issue 2 , May 2014 , pp. 229 - 238
Copyright
Copyright © Cambridge University Press 2012 

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References

Alcaide, M.A. & Cruz López, M.E. (2002). Histoquímica de los contenidos en oviducto de Bufo paracnemis. Acta Zool. Lilloana 46, 39–49.Google Scholar
Bakos, M.A., Korosky, A. & Hedrick, J.L. (1990). Enzymatic and envelope-converting activities of pars recta oviductal fluid from Xenopus laevis. Dev. Biol. 138, 169–76.CrossRefGoogle ScholarPubMed
Barbieri, F.D. & Budeguer de Atenor, M.S. (1973). Role of oviductal secretions in the fertilization of Bufo arenarum oocytes. Arch. Biol. (Bruxelles) 84, 501–11.Google Scholar
European Communities Council Directive. (1986). Guide for use and care of laboratory animals. Off. J. Eur. Commun. L358, 1–29.Google Scholar
Crespo, C.A., Ramos, I., Medina, M.F. & Fernández, S.N. (2009). Analysis of Bufo arenarum oviductal secretion during the sexual cycle. Zygote 18, 60–80.Google Scholar
Díaz-Paniagua, C. (1990). Temporary ponds as breeding sites of amphibians at a locally southwestern Spain. Herpetolog. J. 1, 447–453.Google Scholar
Elinson, R.P. (1971). Fertilization of partially jellied and jellyless oocyte of the frog Rana pipiens. J. Exp. Zool. 176, 415–28.CrossRefGoogle ScholarPubMed
Fernández, S.N. & Ramos, I. (2003). Endocrinology of reproduction. In Reproductive Biology and Phylogeny of Anura (ed. Jamieson, B.G.M.), pp. 73–117. Enfield, New Hampshire USA: Science Publishers, Inc.Google Scholar
Fernández, S.N., Mansilla, Z.C. & Miceli, D.C. (1984). Hormonal regulation of an oviducal protein involved in Bufo arenarum fertilization. Com. Biochem. Physiol. 78, 147–52.CrossRefGoogle Scholar
Fernández, S.N., Mansilla, Z.C. & Miceli, D.C. (1989a). Correlation between the sexual cycle and ultrastructure of Bufo arenarum oviducal pars recta epithelium. Micr. Electr. Biol. Cel. 13, 211–20.Google Scholar
Fernández, S.N., Mansilla, Z.C. & Miceli, D.C. (1989b). Effect of ovariectomy and subsequent hormonal replacement on the proliferation of secretory cells of Bufo arenarum oviducal pars recta epithelium. Micr. Electr. Biol. Cel. 13, 201–10.Google Scholar
Hardy, D.M. & Hedrick, J.L. (1992). Oviductin. Purification and properties of the oviductal protease that processes the molecular weight 43,000 glycoprotein of the Xenopus laevis egg envelope. Biochemistry 31, 4466–72.CrossRefGoogle Scholar
Hedrick, J.L. (2007). A comparative analysis of molecular mechanisms for blocking polyspermy: identification of a lectin-ligand binding reaction in mammalian eggs. Soc. Reprod. Fertil. Suppl. 63, 409–19.Google ScholarPubMed
Hedrick, J.L. & Nishihara, T. (1991). Structure and function of the extracellular matrix of anuran eggs. J. Electron. Microsc. Technique 17, 319–35.CrossRefGoogle ScholarPubMed
Houssay, B.A., Giusti, L.A. & Lascano González, J.N. (1929). Implantation d'hypophyse et stimulation des glandes et des fonctions sexuelles du crapraud. Séanc C R Soc. Biol. (Paris) 102, 864–66.Google Scholar
Katagiri, Ch. (1987). Role of oviductal secretions in mediating gamete fusion in anuran amphibians. Zool. Sci. 4, 348–59.Google Scholar
Katagiri, Ch., Iwao, Y. & Yoshizaki, N. (1982). Participation of oviducal pars recta secretions in inducing the acrosome reaction and release of vitelline coat lysin in fertilizing toad sperm. Dev. Biol. 94, 1–10.CrossRefGoogle ScholarPubMed
Killian, G.J. (2004). Evidence for the role of oviduct secretions in sperm function, fertilization and embryo development. Anim. Reprod. Sci. 82–83, 141–53.CrossRefGoogle ScholarPubMed
Lindsay, LL., Wieduwilt, M.Y. & Hedrick, J.L. (1999). Oviductin, the Xenopus laevis oviductal protease that processes egg envelope glycoprotein gp43, increase sperm binding to envelopes, and is translated as part of an unusual mosaic protein composed of two protease and several CUB domains. Biol. Reprod. 60, 989–95.CrossRefGoogle ScholarPubMed
Llanos, R.J., Barrera, D., Valz-Gianinet, J.N. & Miceli, D.C. (2006). Oviductal protease and trypsin treatment enhance sperm–envelope interaction in Bufo arenarum coelomic eggs. J. Exp. Zool. 305A, 872–82.CrossRefGoogle Scholar
Medina, M.F., Winik, B.C., Crespo, C.A., Ramos, I. & Fernández, S.N. (2000). Subcellular localization of Ca2+-ATPase and calcium in Bufo arenarum oviducts. Acta Histochem. Cytochem. 33, 49–58.CrossRefGoogle Scholar
Medina, M.F., Ramos, I., Crespo, C.A., González-Calvar, S. & Fernández, S.N. (2004). Changes in serum sex steroid levels throughout the reproductive cycle of Bufo arenarum females. Gen. Comp. Endocrinol. 136, 143–51.CrossRefGoogle ScholarPubMed
Medina, M.F., Crespo, C.A., Ramos, I., Cisint, S.B. & Fernández, S.N. (2007). Effect of steroid hormones on Bufo arenarum oviduct. Ultrastructural study. J. Exp. Zool. 307A, 312–23.CrossRefGoogle Scholar
Medina, M.F., Crespo, C.A., Ramos, I. & Fernández, S.N. (2009). Role of cations as components of jelly coats in Bufo arenarum fertilization. Zygote 18, 69–80.CrossRefGoogle ScholarPubMed
Miceli, D.C. & Fernández, S.N. (1982). Properties of an oviductal protein involved in amphibian oocytes fertilization. J. Exp. Zool. 221, 357–64.CrossRefGoogle Scholar
Miceli, D.C, Fernández, S.N., Raisman, J.S. & Barbieri, F.D. (1978a). A trypsin-like oviducal proteinase involved in Bufo arenarum fertilization. J. Embryol. Exp. Morphol. 48, 79–91.Google ScholarPubMed
Miceli, D.C., Fernández, S.N. & del Pino, E.J. (1978b). A trypsin-like oviducal proteinase acting upon the vitelline envelope of Bufo arenarum coelomics oocytes. Isolation by affinity chromatography. Biochem. Biophys. Acta 526, 289–92.Google ScholarPubMed
Miceli, D.C., Fernández, S.N., Mansilla, Z.C. & Cabada, M.O. (1987). New evidence of anuran oviductal pars recta involvement on gamete interaction. J. Exp. Zool. 244, 125–32.CrossRefGoogle Scholar
Moreno, A.R. (1972). Histomorfología del oviducto de Bufo arenarum (Hensel). Rev. NO Argentino 9, 585–602.Google Scholar
Olson, J.H. & Chandler, D.E. (1999). Xenopus laevis egg jelly contains small proteins that are essential to fertilization. Dev. Biol. 210, 401–10.CrossRefGoogle ScholarPubMed
Omata, S. (1993). Relative roles of jelly layers in successful fertilization of Bufo japonicus. J. Exp. Zool. 265, 329–35.CrossRefGoogle Scholar
Peavy, T.R., Hernandez, C. & Carroll, E.J. Jr. (2003). Jeltraxin, a frog egg jelly glycoprotein, has calcium-dependent lectin properties and is related to human serum pentraxins CRP and SAP. Biochem. 42, 12761–69.CrossRefGoogle ScholarPubMed
Pisanó, A. (1956). Método para mantener la hipófisis de anfibio fisiológicamente in vitro. Arch. Bioq. Quim. Farm. Tucumán 7, 387–92.Google Scholar
Ramos, I., Cisint, S., Crespo, C., Medina, M.F. & Fernández, S. (2001). Nuclear maturation inducers in Bufo arenarum oocytes. Zygote 9, 353–59.CrossRefGoogle ScholarPubMed
Valdez Toledo, C.L. & Pisanó, A. (1980). Fáses ovogénicas en el Bufo arenarum. Reproducción 4, 315–30.Google Scholar
Winik, B.C., Alcaide, M.F., Crespo, C.A., Medina, M.F., Ramos, I. & Fernández, S.N. (1999). Ultrastructural changes in the oviductal mucosa throughout the sexual cycle in Bufo arenarum. J. Morphol. 239, 61–73.3.0.CO;2-N>CrossRefGoogle Scholar
Takamune, K., Yoshizaki, N. & Katagiri, K. (1986). Oviductal pars recta-induced degradation of vitelline coat proteins in relation to acquisition of fertilizability of toad eggs. Gamete Res. 14, 215–24.CrossRefGoogle Scholar