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Participation of the 39-kDa glycoprotein (gp39) of the vitelline envelope of Bufo arenarum eggs in sperm–egg interaction

Published online by Cambridge University Press:  16 March 2011

Daniel Barrera ,
Ricardo J. Llanos  and
Dora C. Miceli
Daniel Barrera
Affiliation:
Departamento de Biología del Desarrollo, Instituto Superior de Investigaciones Biológicas (INSIBIO), Chacabuco 461, T4000ILI, San Miguel de Tucumán, Tucumán, República Argentina.
Ricardo J. Llanos
Affiliation:
Departamento de Biología del Desarrollo, Instituto Superior de Investigaciones Biológicas (INSIBIO), Chacabuco 461, T4000ILI, San Miguel de Tucumán, Tucumán, República Argentina.
Dora C. Miceli*
Affiliation:
Departamento de Biología del Desarrollo, Instituto Superior de Investigaciones Biológicas (INSIBIO), Chacabuco 461, T4000ILI, San Miguel de Tucumán, Tucumán, República Argentina. Departamento de Biología del Desarrollo, Instituto Superior de Investigaciones Biológicas (INSIBIO), Chacabuco 461, T4000ILI, San Miguel de Tucumán, Tucumán, República Argentina.
*
All correspondence to: Dora C. Miceli. Departamento de Biología del Desarrollo, Instituto Superior de Investigaciones Biológicas (INSIBIO), Chacabuco 461, T4000ILI, San Miguel de Tucumán, Tucumán, República Argentina. Tel: +54 381 4247752. Fax: +54 381 4247752. e-mail: [email protected]
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Summary

The acquisition of egg fertilizability in Bufo arenarum takes place during the oviductal transit and during this process the extracellular coelomic envelope (CE) of the eggs is converted into the vitelline envelope (VE). It has been stated that one of the necessary events leading to a fertilizable state is the proteolytic cleavage of CE glycoproteins in the oviductal pars recta by oviductin, a serine protease. Consequently, there is a marked increase in the relative quantity of glycoproteins with 39 (gp39) and 42 kDa (gp42) in the VE. In the present study, sperm–VE binding assays using heat-solubilized biotin-conjugated VE glycoproteins revealed that both gp39 and gp42 have sperm binding capacity. According to this result, our study was focused on gp39, a glycoprotein that we have previously reported as a homologue of mammalian ZPC. For this purpose, rabbit polyclonal antibodies against gp39 were generated at our laboratory. The specificity of the antibodies was confirmed with western blot of VE glycoproteins separated on SDS-PAGE. Immunohistochemical and immunoelectron studies showed gp39 distributed throughout the width of the VE. In addition, immunofluorescence assays probed that gp39 bound to the sperm head. Finally, as an approach to elucidate the possible involvement of gp39 in fertilization, inhibition assays showed that pretreatment of eggs with antibodies against gp39 generated a significant decrease in the fertilization rate. Therefore, our findings suggest that gp39, which is modified by oviductal action, participates as a VE glycoprotein ligand for sperm in Bufo arenarum fertilization.

Keywords

FertilizationOviductinSperm–egg interactionVitelline envelopeZPC
Type
Research Article
Information
Zygote , Volume 20 , Issue 2 , May 2012 , pp. 159 - 171
Copyright
Copyright © Cambridge University Press 2011

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References

Bakos, M.A., Kurosky, 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., del Pino, E.J. (1975). Jelly coats and diffusible factor in anuran fertilization. Arch. Biol. 86, 311–21.Google Scholar
Barisone, G.A., Hedrick, J.L. & Cabada, M.O. (2002). Vitelline envelope of Bufo arenarum: biochemical and biological characterization. Biol. Reprod. 66, 1203–209.CrossRefGoogle ScholarPubMed
Barisone, G.A., Krapf, D., Correa-Fiz, F., Arranz, S.E. and Cabada, M.O. (2007). Glycoproteins of the vitelline envelope of amphibian oocyte: biological and molecular characterization of ZPC component (gp41) in Bufo arenarum. Mol. Reprod. Dev. 74, 629–40.CrossRefGoogle ScholarPubMed
Barrera, D., Valdecantos, P.A., García, E.V. & Miceli, D.C. (2010). Cloning and sequence analysis of Bufo arenarum oviductin cDNA and detection of its orthologous gene expression in the mouse female reproductive tract. Zygote Epub ahead of print doi: 10.1017/S0967199410000468.CrossRefGoogle Scholar
Bayer, E.A. & Wilchek, M. (1980). The use of avidin–biotin complex as a tool in molecular biology. Methods Biochem. Anal. 26, 1–45.CrossRefGoogle ScholarPubMed
Cabada, M.O., Sánchez Riera, A.N., Genta, H.D., Sánchez, S.S. & Barisone, G.A. (1996). Vitelline envelope formation during oogenesis in Bufo arenarum. Biocell 20, 77–86.Google ScholarPubMed
Dunbar, B.S. (1987). Antibody preparation, detection and characterization techniques. In: Two Dimensional Electrophoresis and Immunological Techniques. Plenum Press, New York, pp. 303–33.CrossRefGoogle Scholar
European Communities Council Directive (1986). Council Directive 86/609/EEC on the approximation of laws, regulations and administrative provisions of the Member States regarding the protection of animals used for experimental and other scientific purposes. EEC Direct. Off. J. 358, 1–28.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.CrossRefGoogle ScholarPubMed
Hardy, D.M. & Hedrick, J.L. (1992). Oviductin: purification and properties of the oviductal protease that processed the molecular weight 43,000 glycoprotein of the Xenopus laevis egg envelope. Biochemistry 31, 4466–72.CrossRefGoogle Scholar
Harlow, E. & Lane, D. (1988). Storing and purifying antibodies. In: Antibodies: A Laboratory Manual (eds. Harlow, E. & Lane, D.) pp. 283–318. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory.Google Scholar
Hasegawa, A., Koyama, K. & Isojima, S. (1991). Isolation of four major glycoprotein families (ZP1, ZP2, ZP3, ZP4) of porcine zona pellucida and characterization of antisera raised to each glycoprotein family. Nippon Sanka Fujinka Gakkai Zasshi 43, 221–26.Google ScholarPubMed
Hedrick, J.L. & Hardy, D.M. (1991). Isolation of extracellular-matrix structures from Xenopus laevis oocytes, eggs and embryos. Methods Cell Biol. 36, 231–47.CrossRefGoogle ScholarPubMed
Hedrick, J.L. & Nishihara, T. (1991). Structure and function of the extracellular matrix of anuran eggs. J. Electron. Microsc. Tech. 17, 319–35.CrossRefGoogle ScholarPubMed
Hedrick, J.L. (2008). Anuran and pig egg zona pellucida glycoproteins in fertilization and early development. Int. J. Dev. Biol. 52, 683–701.CrossRefGoogle ScholarPubMed
Hiyoshi, M., Takamune, K., Mita, K., Kubo, H., Sugimoto, Y. & Katagiri, Ch. (2002). Oviductin, the oviductal protease that mediates gamete interaction by affecting the vitelline coat in Bufo japonicus: its molecular cloning and analyses of expression and posttranslational activation. Dev. Biol. 243, 176–84.CrossRefGoogle ScholarPubMed
Hoodbhoy, T. & Dean, J. (2004). Insights into the molecular basis of sperm–egg recognition in mammals. Reproduction 127, 417–22.CrossRefGoogle ScholarPubMed
Infante, V., Caputo, M., Riccio, S., De Filippis, A., Carotenuto, R., Vaccaro, M.C. & Campanella, C. (2004). Vitelline envelope gps 63 and 75 specifically bind sperm in “in vitro” assays in Discoglossus pictus. Mol. Reprod. Dev. 68, 213–22.CrossRefGoogle ScholarPubMed
Katagiri, C.H., Yoshizaki, N., Kotani, M. & Kubo, H. (1999). Analyses of oviductal pars recta-induced fertilizability of coelomic eggs in Xenopus laevis. Dev. Biol. 210, 269–76.CrossRefGoogle ScholarPubMed
Kubo, H., Kawano, T., Tsubuki, S., Kawashima, S., Katagiri, C. & Suzuki, A. (1997). A major glycoprotein of Xenopus egg vitelline envelope, gp41, is a frog homolog of mammalian ZP3. Dev. Growth Differ. 39, 405–17.CrossRefGoogle Scholar
Kubo, H., Matsushita, M., Kotani, M., Kawasaki, H., Saido, T.C., Kawashima, S., Katagiri, C. & Suzuki, A. (1999). Molecular basis for oviductin-mediated processing from gp43 to gp41, the predominant glycoproteins of Xenopus egg envelopes. Dev. Genet. 25, 123–29.3.0.CO;2-3>CrossRefGoogle ScholarPubMed
Laemmli, U.K. (1970). Cleavage of structural protein during assembly of the head of bacteriophage T4. Nature 227, 680–85.CrossRefGoogle ScholarPubMed
Lindsay, L.L., Matthew, J.W. & 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
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. 305, 872–82.CrossRefGoogle ScholarPubMed
Maresh, G.A. & Dunbar, B.S. (1987). Antigenic comparison of five species of mammalian zonae pellucidae. J. Exp. Zool. 244, 299–307.CrossRefGoogle ScholarPubMed
Mariano, M.I., de Martin, M.G. & Pisano, 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. & Cabada, M.O. (1998). Amphibian fertilization. Trends Comp. Biochem. Physiol. 5, 249–65.Google Scholar
Miceli, D.C., Fernández, S.N., Raisman, J.S. & Barbieri, F.D. (1978). 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. & Morero, R.D. (1980). Effect of oviducal proteinase upon Bufo arenarum vitelline envelope. A fluorescence approach. Dev. Growth Differ. 22, 639–43.CrossRefGoogle ScholarPubMed
Omata, S. & Katagiri, C. (1996). Involvement of carbohydrate moieties of the toad egg vitelline coat in binding with fertilizing sperm. Dev. Growth Differ. 38, 663–72.CrossRefGoogle ScholarPubMed
Spargo, S.C. & Hope, R.M. (2003). Evolution and nomenclature of the zona pellucida gene family. Biol. Reprod. 68, 58–62.CrossRefGoogle ScholarPubMed
Takamune, K., Yoshizaki, N. & Katagiri, C. (1986). Oviducal pars recta induced degradation of vitelline coat proteins in relation to acquisition of fertilizability of toad eggs. Gamete Res. 14, 215–24.CrossRefGoogle Scholar
Takamune, K. & Katagiri, C. (1987). The properties of the oviductal pars recta protease which mediates gamete interaction by affecting the vitelline coat of a toad egg. Dev. Growth Differ. 29, 193–203.CrossRefGoogle ScholarPubMed
Takamune, K., Lindsay, L.L., Hedrick, J.L. & Katagiri, Ch. (1987). Comparative studies of Bufo and Xenopus vitelline coat molecular transformations induced by homologous and heterologous oviducal pars recta proteases. J. Exp. Zool. 244, 145–50CrossRefGoogle Scholar
Tian, J.D., Gong, H., Thomsen, G.H. & Lennarz, W.J. (1997). Gamete interaction in Xenopus laevis: identification of sperm binding glycoproteins in the egg vitelline envelope. J. Cell Biol. 136, 1099–108.CrossRefGoogle ScholarPubMed
Timmons, T.M., Maresh, G.A., Bundman, D.S. & Dunbar, B.S. (1987). Use of specific monoclonal and polyclonal antibodies to define distinct antigens of the porcine zonae pellucidae. Biol. Reprod. 36, 1275–287.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.CrossRefGoogle ScholarPubMed
Vo, L.H. & Hedrick, J.L. (2000). Independent and hetero-oligomeric-dependent sperm binding to egg envelope glycoprotein ZPC in Xenopus laevis. Biol. Reprod. 62, 766–74.CrossRefGoogle ScholarPubMed
Vo, L.H., Yen, T.Y., Macher, B.A. & Hedrick, J.L. (2003). Identification of the ZPC oligosaccharide ligand involved in sperm binding and the glycan structures of Xenopus laevis vitelline envelope glycoproteins. Biol. Reprod. 69, 1822–30.CrossRefGoogle ScholarPubMed
Wassarman, P.M. & Litscher, E.S. (2008). Mammalian fertilization: the egg's multifunctional zona pellucida. Int. J. Dev. Biol. 52, 665–76.CrossRefGoogle ScholarPubMed
Yamaguchi, S., Hedrick, J.L. & Katagiri, Ch. (1989). The synthesis and localization of envelope glycoproteins in oocytes of Xenopus laevis using immunocytochemical methods. Dev. Growth Differ. 31, 85–94.CrossRefGoogle ScholarPubMed
Yang, J.C. & Hedrick, J.L. (1997). cDNA cloning and sequence analysis of the Xenopus laevis egg envelope glycoprotein gp43. Dev. Growth Differ. 39, 457–67.CrossRefGoogle ScholarPubMed