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Behaviour of the vitelline envelope in Bufo arenarum oocytes matured in vitro in blockade to polyspermy

Published online by Cambridge University Press:  01 May 2006

J. Oterino ,
G. Sánchez Toranzo ,
L. Zelarayán ,
M.T. Ajmat ,
F. Bonilla  and
M.I. Bühler
J. Oterino
Affiliation:
Departamento de Biología del Desarrollo, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina
G. Sánchez Toranzo
Affiliation:
Departamento de Biología del Desarrollo, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina
L. Zelarayán
Affiliation:
Departamento de Biología del Desarrollo, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina
M.T. Ajmat
Affiliation:
Departamento de Biología del Desarrollo, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina
F. Bonilla
Affiliation:
Departamento de Biología del Desarrollo, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina
M.I. Bühler*
Affiliation:
Departamento de Biología del Desarrollo, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina
*
All correspondence to: Dra. Marta I. Bühler, Departamento de Biología del Desarrollo, Chacabuco 461, 4000 – San Miguel de Tucumán, Argentina. Fax: +54 81 248025. e-mail: mbuhler@fbqf.unt.edu.ar
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Summary

During activation of amphibian eggs, cortical granule exocytosis causes elaborate ultrastructural changes in the vitelline envelope. These changes involve modifications in the structure of the vitelline envelope and formation of a fertilization envelope (FE) that can no longer be penetrated by sperm. In Bufo arenarum, as the egg traverses the oviduct, the vitelline envelope is altered by a trypsin-like protease secreted by the oviduct, which induces an increased susceptibility of the vitelline envelope to sperm lysins. Full-grown oocytes of B. arenarum, matured in vitro by progesterone, are polyspermic, although cortical granule exocytosis seems to occur within a normal chronological sequence. These oocytes can be fertilized with or without trypsin treatment, suggesting that the vitelline envelope is totally sperm-permeable. Vitelline envelopes without trypsin treatment cannot retain either gp90 or gp96. This suggests that these glycoproteins are involved in the block to polyspermy and that trypsin treatment of matured in vitro oocytes before insemination is necessary to enable vitelline envelopes to block polyspermy. The loss of the binding capacity in vitelline envelopes isolated from B. arenarum oocytes matured in vitro with trypsin treatment and activated by electric shock suggests that previous trypsin treatment is a necessary step for sperm block to occur. When in vitro matured oocytes were incubated with the product of cortical granules obtained from in vitro matured oocytes (vCGP), vitelline envelopes with trypsin treatment were able to block sperm entry. These oocytes exhibited the characteristic signs of activation. These results support the idea that B. arenarum oocytes can be activated by external stimuli and suggest the presence of unknown oocyte surface receptors linked to the activation machinery in response to fertilization. Electrophoretic profiles obtained by SDS-PAGE of solubilized vitelline envelopes from oocytes matured in vitro revealed the conversion of gp40 (in vitro matured oocytes, without trypsin treatment) to gp38 (ascribable to trypsin activity or cortical granule product activity, CGP) and the conversion of gp70 to gp68 (ascribable to trypsin activity plus CGP activity). Taking into account that only the vitelline envelopes of in vitro matured oocytes with trypsin treatment and activated can block sperm entry, we may suggest that the conversion of gp70 to gp68 is related to the changes associated with sperm binding.

Keywords

Bufo arenarumOocytesPolyspermyVitelline envelope
Type
Research Article
Information
Zygote , Volume 14 , Issue 2 , May 2006 , pp. 97 - 106
Copyright
Copyright © Cambridge University Press 2006

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References

Balinsky, B.I. (1966). Changes in the ultrastructure of amphibian eggs following fertilization. Acta Embryol. Morphol. Exp. 9, 132–54.Google Scholar
Barbieri, F.D. & Oterino, J. (1972). A study of the diffusible factor released by the jelly of the egg of the toad Bufo arenarum. Dev. Growth Differ. 14, 107–17.CrossRefGoogle ScholarPubMed
Barisone, G.A., Albertali, I.E., Sánchez, M. & Cabada, M.O. (2003). The envelopes of amphibian oocytes: physiological modifications in Bufo arenarum. Reprod. Biol. Endocrinol. 1, 1–18.Google Scholar
Benoff, S. (1997). Carbohydrates and fertilization: an overview. Mol. Hum. Reprod. 3, 599–637.Google Scholar
Bühler, M.I., Petrino, T. & Legname, A. (1987). Sperm nuclear transformation and aster formation related to metabolic behaviour in amphibian eggs. Dev. Growth Differ. 29, 177–84.Google Scholar
Cabada, M.O., Mariano, M.I. & Raisman, J.S. (1978). Effect of trypsin inhibitors and concanavalin A on the fertilization of Bufo arenarum coelomic oocytes. J. Exp. Zool. 204, 409–16.Google Scholar
CabadaM.O., M.O.,Mariano, M.I. & Gómez, M.I. (1987). Cortical granule products and fertility prevention in Bufo arenarum oocytes. J. Exp. Zool. 241, 359.Google Scholar
Cross, N.L. & Elinson, R.P. (1980). A fast block to polyspermy in frogs mediated by changes in the membrane potential Dev. Biol. 75, 187–98.CrossRefGoogle ScholarPubMed
Elinson, R.P. (1973). Fertilization of frog body cavity eggs enhanced by treatments affecting the vitelline coat. J. Exp. Zool. 183, 291–302.CrossRefGoogle Scholar
Elinson, R.P. (1977). Fertilization of immature frog eggs: cleavage and development following subsequent activation. J. Embryol. Exp. Morphol. 37, 187–201.Google Scholar
Elinson, R.P. (1986). Fertilization in amphibians: the ancestry of the block to polyspermy. Int. Rev. Cytol. 101, 59–100.Google Scholar
Gerton, G.L. & Hedrick, J.L. (1986). The coelomic envelope to vitelline envelope conversion in eggs of Xenopus laevis. J. Cell Biochem. 30, 341–50.Google Scholar
Gómez, M.I. (1992). Estructuras involucradas en el bloqueo de la polispermia en ovocitos de Bufo arenarum. Doctoral thesis, Facultad de Bioquimica, Quimica y Farmacia, UNT.Google Scholar
Gómez, M.I., Santolaya, R.C. & Cabada, M.O. (1984). Exocytosis of cortical granules from activated oocytes of the toad Bufo arenarum. Cell Tissue Res. 237,191–4.CrossRefGoogle ScholarPubMed
Greve, L.C. & Hedrick, J.L. (1978). An immunocytochemical localization of the cortical granule lectin in fertilized and unfertilized egg of Xenopus laevis. Gamete Res. 1, 13–18.CrossRefGoogle Scholar
Grey, R.D., Wolf, D.P. & Hedrick, J.L. (1974). Formation and structure of the fertilization envelope in Xenopus laevis. Dev. Biol. 36, 44–61.CrossRefGoogle Scholar
Grey, R.D., Working, P.K. & Hedrick, J.L. (1976). Evidence that the fertilization envelope blocks sperm entry in eggs of Xenopus laevis: interaction of sperm with isolated envelopes. Dev. Biol. 54, 52–60.Google Scholar
Grey, R.D., Working, P.K. & Hedrick, J.L. (1977). Alteration of structure and penetrability of the vitelline envelope after passage of eggs from coelom to oviduct in Xenopus laevis. J. Exp. Zool. 201, 73–83.CrossRefGoogle ScholarPubMed
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.Google Scholar
Hedrick, J.L. & Nishihara, T. (1991). Structure and function of the extracellular matrix of anuran eggs. J. Electron Microsc. Tech. 17, 319–35.Google Scholar
Iwao, Y. & Katagiri, Ch. (1982). Properties of the vitelline coat Iysin from toad sperm. J. Exp. Zool. 219, 87–95.Google Scholar
Katagiri, C. (1959). Cortical change at fertilization in the egg of the grass frog, Rana temporaria. J. Fac. Sci. Hokkaido Univ. Ser. VI Zool. 14, 166–74.Google Scholar
Katagiri, Ch. (1974). A high frequency of fertilization in premature and mature coelomic toad eggs after enzymic removal of vitelline membrane. J. Embryol. Exp. Morphol. 31, 573–87.Google Scholar
Katagiri, Ch. (1987). Role of oviducal secretions in mediating gamete fusion in anuran amphibians. Zool. Sci. 4, 1–14.Google Scholar
KatagiriCh., 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.Google Scholar
Laemmeli, U.K. (1970). Cleavege of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–5.CrossRefGoogle Scholar
Larabell, C.A. & Chandler, D.E. (1991). Fertilization-induced changes in the vitelline envelope of echinoderm and amphibian eggs: self-assembly of an extracellular matrix. J. Electron Microsc. Tech. 17, 194–318.Google Scholar
Lin, Y.P. & Schuetz, A.W. (1985). Spontaneous oocyte maturation in Rana pipiens: estrogen and follicle wall involvement. Gamete Res. 12, 11–28.Google Scholar
Lindsay, L.L. & Hedrick, J.L. (1989). Proteases released from Xenopus laevis eggs at activation and their role in envelope conversion. Dev. Biol. 135, 202–11.CrossRefGoogle ScholarPubMed
Lindsay, L.L., Wieduwilt, M.J. & Hedrick, J.L. (1999). Oviductin, the Xenopus laevis oviductal protease that processes egg envelope glycoprotein gp43, increases 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
Mariano, M.I., Gómez de, Martin M. & Pisanó, A. (1984). Morphological modifications of oocyte vitelline envelope from Bufo arenarum during different functional states. Dev. Growth Differ. 26, 33–42.CrossRefGoogle ScholarPubMed
Miceli, D.C & Fernández, S.N. (1982). Properties of an oviducal protein involved in amphibian oocyte fertilization. J. Exp. Zool. 221, 520–7.CrossRefGoogle ScholarPubMed
Miceli, D.C., Fernández, S.N., Raisman, J.S. & Barbieri, F.D. (1978 a). A trypsin-like oviductal proteinase involved in Bufo arenarum fertilization. J. Embryol. Exp. Morphol. 48, 79–91.Google Scholar
Miceli, D.C, Fernández, S.N. & Del Pino, E.J. (1978 b). An oviducal enzime isolated by affinity chromatography which acts upon the vitelline envelope of Bufo arenarum coelomic oocytes. Biochim. Biophys. Acta 526, 289–92.Google Scholar
Nishihara, T. & Hedrick, J.L (1977). A molecular mechanism for envelope elevation at fertilization. Fed. Proc. 36, 811.Google Scholar
Omata, S. & Katagiri, Ch. (1996). Involvement of carbohydrate moieties of the toad vitelline coat in binding with fertilizing sperm. Dev. Growth Differ. 38, 663–72.CrossRefGoogle ScholarPubMed
Nishihara, T. & Hedrick, J.L. (1977). A molecular mechanism for envelope elevation at fertilization. Fed. Proc. 36, 811.Google Scholar
Oterino, J., Sánchez Toranzo, G., Zelarayán, L. & Bühler, M.I. (1997). Polyspermy in Bufo arenarum oocytes matured in vitro. Zygote 5, 267–71.CrossRefGoogle ScholarPubMed
Oterino, J., Sánchez Toranzo, G., Zelarayán, L., Valz-Gianinet, J.N. & Bühler, M.I. (2001). Cortical granule exocytosis in Bufo arenarum oocytes matured in vitro. Zygote 9, 251–9.Google Scholar
Petrino, T., Bühler, M. & Legname, A. (1984). Metabolic behaviour and activation capacity in the amphibian eggs. Comp. Biol. 3, 231–40.Google Scholar
Raisman, J.S & Barbieri, F.D (1969). Lytic effects of sperm suspensions on the vitelline membrane of Bufo arenarum oocytes. Acta Embryol. Exp. (Palermo) 1, 17–26.Google Scholar
Shivers, C.A. & James, J.M. (1970). Capacitation of frog sperm. Nature 227, 183–4.Google Scholar
Snell, W. & White, J.M. (1996). The molecules in mammalian fertilization. Cell 85, 629–37.Google Scholar
Subtelny, S. & Bradt, C. (1961). Transplantations of blastula nuclei into activated eggs from the body cavity and from the uterus of Rana pipiens. II. Development of the recipient body cavity eggs. Dev. Biol. 3, 96–114.Google Scholar
Takamune, K. & Katagiri, Ch. (1987). The properties of the oviducal pars recta protease which mediates gamete interaction by affecting vitelline coat of a toad egg. Dev. Growth Differ. 29, 193–203.CrossRefGoogle ScholarPubMed
Takamune, K., Yoshizaki, N. & Katagiri, Ch. (1986). Oviducal pars recta induced degradation of vitelline coat proteins in relation to acquisition of fertilizability of toad eggs. Gamete Res. 14, 215–24.Google Scholar
Tian, J., Gong, H., Thomsen, G.H. & Lennarz, W.J. (1997). Xenopus laevis sperm–egg adhesion is regulated by modifications in the sperm receptor and the egg vitelline envelope. Dev. Biol. 187, 143–53.Google Scholar
Tulsiani, D.R., Yoshida-Komiya, H. & Araki, Y. (1997). Mammalian fertilization: a carbohydrate-mediated event. Biol. Reprod. 57, 487–94.CrossRefGoogle ScholarPubMed
Valz-Gianinet, J.N., Del Pino, E.J. & Cabada, M. O. (1991). Glycoproteins from Bufo arenarum vitelline envelope with fertility-impairing effect on homologous spermatozoa. Dev. Biol. 146, 416–22.Google Scholar
Wassarman, P.M. (1988). Zona pellucida glycoproteins. Annu. Rev. Biochem. 57, 415–42.Google Scholar
Wassarman, P.M. (1990). Profile of a mammalian sperm receptor. Development 108, 1–17.Google Scholar
Wassarman, P.M. (1999). Mammalian fertilization: molecular aspects of gamete adhesion, exocytosis, and fusion. Cell 96, 175–83.Google Scholar
Wolf, D.P. (1974). On the contents of the cortical granules from Xenopus laevis eggs. Dev. Biol. 38, 14–29.Google Scholar
Yamasaki, H. & Katagiri, C. (1991). Egg exudate-induced reduction of sperm lysin sensitivity in the vitelline coat after fertilization of Bufo japonicus and its participation in polyspermy block. J. Exp. Zool. 258, 403–13.Google Scholar
Yanagimachi, R. (1994). Mammalian fertilization. In The Physiology of Reproduction (ed. Knobil, E. & Neill, J.D.), vol. 1, pp. 189–317. New York: Raven Press.Google Scholar
Yoshizaki, N. & Katagiri, Ch. (1981). Oviducal contribution to alteration of the vitelline coat in the frog. Rana japonica: an electron microscopic study. Dev. Growth Differ. 23, 495–506.Google Scholar
Zelarayán, L., Oterino, J. & Bühler, M.I. (1995). Spontaneous maturation in Bufo arenarum oocytes: follicle wall involvement, respiratory activity, and seasonal influences. J. Exp. Zool. 272, 356–63.Google Scholar