Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-02T20:55:55.311Z Has data issue: false hasContentIssue false

Analysis of Bufo arenarum oviductal secretion during the sexual cycle

Published online by Cambridge University Press:  08 June 2009

Claudia A. Crespo
Affiliation:
Department of Developmental Biology, National Council for Scientific and Technical Research, National University of Tucumán, Chacabuco 461, Tucumán 4000, Argentina.
Inés Ramos
Affiliation:
Department of Developmental Biology, National Council for Scientific and Technical Research, National University of Tucumán, Chacabuco 461, Tucumán 4000, Argentina.
Marcela F. Medina
Affiliation:
Department of Developmental Biology, National Council for Scientific and Technical Research, National University of Tucumán, Chacabuco 461, Tucumán 4000, Argentina.
Silvia N. Fernández*
Affiliation:
Department of Developmental Biology, National University of Tucumán, Chacabuco 461, Tucumán 4000, Argentina. Department of Developmental Biology, National Council for Scientific and Technical Research, National University of Tucumán, Chacabuco 461, Tucumán 4000, Argentina.
*
All correspondence to: Silvia N. Fernández. Department of Developmental Biology, National University of Tucumán, Chacabuco 461, Tucumán 4000, Argentina. Tel: +54 0381 4247752 (7005). Fax: +54 0381 4107214. e-mail: [email protected]

Summary

Bufo arenarum oocytes are oviposited surrounded by jelly coats, one component of the extracellular matrix required for fertilization. The secretion, released to the oviductal lumen, was analysed by SDS-PAGE. The coomassie blue staining evidenced an electrophoretic pattern with molecules ranging between 300 and 19 kDa that showed variations in their secretion profiles during the sexual cycle. In the preovulatory period the densitometric analysis showed the presence of nine peaks with marked predominance of the 74 kDa molecule. Once ovulation has occurred, the jelly coats become arranged around the oocytes during their transit throughout the oviductal pars convoluta (PC), revealing the addition of three proteins only observed during this period, which suggests a differential secretion. Some of these proteins could not diffuse under any extraction treatment, indicating for them a structural or in situ function. Proteins of low molecular mass diffused totally while others showed a partial diffusing capacity. After ovulation a marked decrease in the relative amount of all the proteins released to the lumen, especially the 74 kDa protein, could be detected. During this period, unlike the other stages of the sexual cycle, a differential secretion pattern was observed along the PC. The histochemical analysis performed during the ovulatory period showed the presence of glycoconjugates including both acidic and neutral groups. The present results are in agreement with previous ultrastructural and histochemical studies that describe the role of Bufo arenarum jelly coats in fertilization.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Al-Anzi, B. & Chandler, D.E. (1998). A sperm chemoattractant is released from Xenopus egg jelly during spawning. Dev. Biol. 198, 366–75.Google Scholar
Alcaide, M.A. & Cruz López, M.E. (2002). Histoquímica de los contenidos en oviducto de Bufo paracnemis. Acta Zool. Lilloana 46, 3949.Google Scholar
Arranz, S.E. & Cabada, M.O. (2000). Diffusible highly glycosylated protein from Bufo arenarum egg-jelly coat: biological activity. Mol. Reprod. Devel. 56, 392400.Google Scholar
Arranz, S.E., Albertali, I.E. & Cabada, M.O. (1997). Bufo arenarum egg jelly coat: purification and characterization of two glycosylated proteins. Biochem. J. 323, 307–12.CrossRefGoogle ScholarPubMed
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.Google Scholar
Barbieri, F.D. (1976). Diffusible factor in anuran fertilization. Acta Physiol. Lat. Am. 26, 513.Google Scholar
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
Barbieri, F.D. & del Pino, E. (1975). Jelly coats and diffusible factor in anuran fertilization. Arch. Biol. (Bruxelles) 86, 311–21.Google Scholar
Barbieri, F.D & Oterino, J.M. (1972). A study of the diffusible factor released by the jelly of the egg of the toad Bufo arenarum. Develop. Growth Differ. 14, 107–17.CrossRefGoogle ScholarPubMed
Bonell, B.S., Reinhart, D. & Chandler, D.E. (1996). Xenopus laevis egg jelly coats consist of small diffusible proteins bound to a complex system of structurally stable networks composed of high-molecular-weight glycoconjugates. Dev. Biol. 174, 3242.CrossRefGoogle Scholar
Diaz Fontdevila, M.F., Bloj, B. & Cabada, M.O. (1991). Effect of egg water from Bufo arenarum on the fertilizing capacity of homologous spermatozoa. J. Exp. Zool. 257, 408–14.Google Scholar
Fernández, S.N. & Ramos, I. (2003). Endocrinology of reproduction. In Reproductive Biology and Phylogeny of Anura (ed. Jamieson, B.G.M.), pp. 73–11. Enfield, New Hampshire USA: Science Publishers, Inc.Google Scholar
Frazier, B.A., Pfeifer, J.D., Russell, D.G., Flak, P., Olsen, A.N., Hammar, M., Westblom, T.U. & Normark, S.J. (1993). Paracrystalline inclusions of a novel ferritin containing nonheme iron, produced by human gastric pathogen Helicobacter pylori: evidence for a third class of ferritins. J. Bacteriol. 175, 966–72.Google Scholar
Grey, R.D., Working, P.K. & Hedrick, J.L. (1977). Alteration of structure and penetrability of vitelline envelope after passage of eggs from coelom to oviduct in Xenopus laevis. J. Exp. Zool. 201, 7384.Google Scholar
Hedrick, J.L. & Hishihara, T. (1991). Structure and function of the extracellular matrix of anuran eggs. J. Electron. Microsc. Technique 17, 319–35.Google Scholar
Houssay, B.A., Giusti, L.A. & Lascano González, J.N. (1929). Implantation d'hypophyse et stimulation des glandes et des fonctions sexuelles du crapraud. C r Soc. Biol. (Paris) 102, 864–6.Google Scholar
Ishihara, K., Honoso, S., Kanatani, H. & Katagiri, Ch. (1984). Toad egg-jelly as a source of divalent cations essential for fertilization. Dev. Biol. 105, 435–42.Google Scholar
Katagiri, Ch. (1973). Chemical analysis of toad egg-jelly in relation to its sperm-capacitating activity. Develop. Growth Differ. 15, 8192.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 oviductal pars recta secretions in inducing the acrosome reaction and release of vitelline coat lysin in fertilizing toad sperm. Dev. Biol. 94, 110.Google Scholar
Krapf, D., Vidal, M., Arranz, S.E. & Cabada, M.O. (2006). Characterization and biological properties of L-HGP, a glycoprotein from the amphibian oviduct with acrosome-stabilizing effects. Biol. Cell 98, 403–13.Google Scholar
Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–5.CrossRefGoogle ScholarPubMed
Lowry, D.M., Rosebrough, N.J., Farr, A.L. & Randall, R.J. (1951). Protein measurement with the folin phenol reagent. J. Biol. Chem. 193, 265–75.CrossRefGoogle ScholarPubMed
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.Google Scholar
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 oviductal proteinase involved in Bufo arenarum fertilization. J. Embryol. Exp. Morphol. 48, 7991.Google Scholar
Miceli, D.C., Fernández, S.N. & del Pino, E.J. (1978b). A trypsin-like oviductal proteinase acting upon the vitelline envelope of Bufo arenarum coelomics oocytes. Isolation by affinity chromatography. Biochem. Biophys. Acta 526, 289–92.Google Scholar
Moreno, A.R. (1972). Histomorfología del oviducto de Bufo arenarum (Hensel). Rev. NO Argentino 9, 585602.Google Scholar
Noll, F. (1984). L +-Lactate. In Methods of Enzymic Analysis (eds Bergmeyer, J. & Grassl, M.), pp. 582–8. Weinheim: Verlag Chemie.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.Google Scholar
Omata, S. (1993). Relative roles of jelly layers in successful fertilization of Bufo japonicus. J. Exp. Zool. 265, 329–35.Google 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. Biochemistry 42, 12761–9.Google Scholar
Pisanó, A. (1956). Método para mantener la hipófisis de anfibio fisiológicamente in vitro. Arch. Bioq. Quim. Farm. Tucumán 7, 387–92.Google Scholar
Shimoda, Y., Kitajima, K., Inoue, S. & Inoue, Y. (1994). Isolation, structural determination and calcium-binding properties of the major glycoprotein present in Bufo japonicus japonicus egg jelly. Eur. J. Biochem. 223, 223–31.Google Scholar
Theil, E.C. (1987). Ferritin: structure, gene regulation and cellular function animals, plants and microorganisms. Annu. Rev. Biochem. 56, 289315.CrossRefGoogle ScholarPubMed
Wardi, A.H. & Michos, G.A. (1972). Alcian blue staining of glycoproteins in acrylamide disc electrophoresis. Anal. Biochem. 49, 607–9.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, 6173.Google Scholar
Yoshizaki, N. & Katagiri, Ch. (1981). Oviductal contribution to alteration of the vitelline coat in the frog, Rana japonica. An electron microscopic study. Develop. Growth Differ. 23, 495506.Google Scholar
Yurewicz, E.C., Oliphant, G. & Hedrick, J.L. (1975). The macromolecular composition of Xenopus laevis egg jelly coat. Biochemistry 14, 3101–7.Google Scholar
Zacharius, R.M., Zell, T.E., Morrison, J.H. & Woodlock, J.J. (1969). Glycoprotein staining following electrophoresis on acrylamide gels. Anal. Biochem. 30, 148–52.Google Scholar