Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-10T16:20:07.645Z Has data issue: false hasContentIssue false
  • English
  • Français

The polysulphate binding domain of human proacrosin/acrosin is involved in both the enzyme activation and spermatozoa-zona pellucida interaction

Published online by Cambridge University Press:  15 January 2010

R. D. Moreno ,
M. S. Sepúlveda ,
A. de Ioannes  and
C. Barros
R. D. Moreno
Affiliation:
Embryology and Immunology Laboratory, Faculty of Biological Sciences, Pontifical Catholic University of Chile, Santiago, Chile
M. S. Sepúlveda
Affiliation:
Embryology and Immunology Laboratory, Faculty of Biological Sciences, Pontifical Catholic University of Chile, Santiago, Chile
C. Barros*
Affiliation:
Embryology and Immunology Laboratory, Faculty of Biological Sciences, Pontifical Catholic University of Chile, Santiago, Chile
*
Dr Claudio Barros, Laboratory of Embryology, PO Box 114-D, Santiago, Chile. Telephone + 56-2-686-2880. Fax: +56-2-222 5515. e-mail: cbarros@genes.bio.puc.cl
Get access Rights & Permissions [Opens in a new window]

Summary

Mammalian acrosin is a protease present as a zymogen in the acrosome of a non-reacted mammalian sperm, and in vitro is able to carry out limited hydrolysis of homologous and heterologous zonae pellucidae. On the other hand, sulphated polymers and zona pellcida glycoproteins bind to acrosin on a domain different from the active site, named the polysulphate binding domain (PSBD). Thus it is believed that acrosome-reacted spermatozoa bind to glycan chains of the zona pellucida through PSBD participating as secondary binding receptor. The aim of the present work was to study the role of PSBD during both human gamete interaction and acrosin activation. In this work we present evidence that the anti-human acrosin monoclonal antibody C5F10 is directed to an epitope located on or near the PSBD on human proacrosin/acrosin. Moreover, we show that this antibody is able to inhibit both proacrosin activation induced by fucoidan and the sperm binding to the zona pellucida. Our results suggest that the same PSBD is involved in both sperm secondary binding, during zona pellucida penetration, and proacrosin activation.

Keywords

AcrosinFucoidanProacrosinSpermatozoonZona pellucida
Type
Research Article
Information
Zygote , Volume 6 , Issue 1 , February 1998 , pp. 75 - 83
Copyright
Copyright © Cambridge University Press 1998

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

Baba, T., Kashiwabara, S.I., Watanabe, K., Itoh, H., Michikawa, Y., Kimura, K., Takada, M., Fukamazu, A. & Arai, Y (1989 a). Activation and maturation mechanism of boar acrosin zymogen based on the deduced primary structure. J. Biol. Chem. 264, 11920–7.CrossRefGoogle ScholarPubMed
Baba, T., Michikawa, Y., Kawakura, K. & Arai, Y. (1989 b). Activation of boar proacrosin is effected by processing at both N- and C-terminal portions of the zymogen molecule. FEBS Lett. 244, 132–6.Google Scholar
Barros, C. & Jedlicki, A. (1985). Human sperm fertilizing ability: quality criteria. In Human In Vitro Fertilization, ed. Testart, J. & Frydman, R., pp. 79–91. New York: INSERM Symposium. Elsevier.Google Scholar
Barros, C., Gonzalez, J., Herrera, E. & Bustos-Obregón, E. (1979). Human sperm penetration into zona-free hamster oocyte as a test to evaluate the sperm fertilizing ability. Andrologia 11, 197–210.CrossRefGoogle ScholarPubMed
Barros, C., Jedlicki, A., Bize, I. & Aguirre, E. (1984). Relationship between the length of sperm preincubation and zona penetration in the golden hamster: a scanning electron microscopy study. Gamete Res. 9, 31–43.CrossRefGoogle Scholar
Barros, C., Crosby, J.A. & Moreno, R.D. (1996) Early steps of sperm-egg interactions during mammalian fertilisation. Cell Biol. Int. 20, 33–9.Google Scholar
Berger, T., Davis, A., Wardrip, N.J. & Hedrick, J.L. (1989). Sperm binding to the pig zona pellucida and inhibition of binding by solubilized components of the zona pellucida. j. Reprod. Fertil. 86, 559–65.Google Scholar
Berman, H.A., Becktel, W. & Taylor, P. (1981). Spectroscopie studies on acetylcholinesterase: influence of peripheral-site occupation on active-center conformation. Biochemistry 20, 4803–10.Google Scholar
Biggers, J., Whitten, W. & D, Whittingham (1971). The culture of mouse embryos in vitro. In Methods in Mammalian Embryology, ed. Daniel, J.C., pp. 86–116. San Francisco: W.H. Freeman.Google Scholar
Danishefky, L. & S, Klein (1977). Effect of heparin modification on its activity in enhancing the inhibition of thrombin by antithrombin III. Biochim. Biophys. Acta 498, 215–22.Google Scholar
de Ioannes, A.E., Becker, M.I., Perez, C., Capoté, C., Barros, C. (1990). Role of acrosin and antibodies to acrosin in gamete interactions. In Gamete Interactions: Prospects for Immunocontraception, ed. Alexander, N., Griffin, D., Spieler, J. & Waites, G., pp. 185–95. New York: Wiley-Liss.Google Scholar
Drahorad, J., Cechova, D. & Tesarik, J. (1988) Activation of proacrosin by a locally produced component of human follicular fluid, J. Reprod. Fertil. 83, 599–603.CrossRefGoogle ScholarPubMed
Drahorad, J., Tesarik, J., Cechova, D. & Vilim, V. (1991). Proteins and glycosaminoglycans in the intercellular matrix of the human cumulus-oophorus and their effect on conversion of proacrosin to acrosin. J. Reprod. Fertil. 93, 253–62.CrossRefGoogle ScholarPubMed
Dravland, J.E., Meizel, S. (1982). The effect of inhibitors of trypsin and phospholipase A2 on the penetration of zona pellucida-free hamster eggs by acrosome-reacted hamster sperm, j. Androl. 3, 388–95.Google Scholar
Dudkiewicz, A.B. (1983). Inhibition of fertilisation in the rabbit by anti-acrosin antibodies. Gamete Res. 8, 183–7.Google Scholar
Dumbar, B.S., Dudkiewicz, A.B. & Bundman, D.S. (1985). Proteolysis of specific porcine zona pellucida glycoproteins by boar acrosin. Biol. Repród. 32, 619–30.Google Scholar
Eberspaecher, U., Gerwien, J., Habenicht, U.-F., Schleuning, W.-D. & Donner, P. (1991). Activation and subsequent degradation of proacrosin is mediated by zona pellucida glycoproteins, negatively charged polysaccharides, and DNA. Mol. Reprod. Dev. 30, 164–70Google Scholar
Fock-Nüzel, R., Lottspeich, F., Henschen, A. & Müller-Esterl, W. (1984). Boar acrosin is a two chain molecule: isolation and primary structure of the light chain; homology with the propart of other serine proteases. Eur. J. Biochem. 141, 441–6.CrossRefGoogle Scholar
Green, D.P.L. (1978). The activation of proteolysis in the acrosome reaction of guinea-pig sperm, J. Cell Sci. 32, 153–64.Google Scholar
Hardy, D.M., Oda, M.N., Friend, D.S. & Huang, T.F. Jr (1991). A mechanism for differential release of acrosomal enzymes during the acrosome reaction. Biochem. J. 275, 759–66.Google Scholar
Harlow, E. & Lane, D. (1988). Antibodies: A Laboratory Manual, pp. 472–510. New York: Cold Spring Harbor Laboratory Press.Google Scholar
Huang, T.T.F. & Yanagimachi, R. (1982). Evidence suggesting that L-fucose is part of a recognition signal for sperm-zona pellucida attachment in mammals. Gamete Res. 5, 355–61.Google Scholar
Huang, T.T.F. & Yariagimachi, R. (1984). Fucoidan inhibits attachment of guinea pig spermatozoa to the zona pellucida through binding to the inner acrosomal membrane and equatorial domains. Exp. Cell Res. 153, 363–73.Google Scholar
Jansen, S., Quigley, M., Reik, W. & Jones, R. (1995). Analysis of polysulphate-binding domains in porcine proacrosin, a putative zona adhesion protein from mammalian spermatozoa. Int. J. Dev. Biol. 39, 501–510.Google Scholar
Jones, R. (1991). Interaction of zona pellucida glycoproteins, sulphated carbohydrates and synthetic polymers with proacrosin, the putative egg-binding proteins from mammalian spermatozoa. Development 11, 1155–63CrossRefGoogle Scholar
Jones, R., Brown, C.R. & Lancaster, R.T. (1988). Carbohydrate-binding properties of boar sperm proacrosin and assessment of its role in sperm-egg recognition and adhesion during fertilisation. Development. 102, 781–92.CrossRefGoogle Scholar
Kreienkamp, H.J., Weise, C., Raba, R., Aaviksaar, A. & Hucho, F. (1991). Anionic subsites of the catalytic center of acetylcholinesterase from Torpedo and from cobravenom. Proc. Natl. Acad. Sci. USA 88, 6117–21.Google Scholar
Laemmli, U.K. (1970). Cleavage of the structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–5.CrossRefGoogle ScholarPubMed
Leyton, L., De Ioannes, A., Croxatto, H., Graham, E. & Elce, J. (1986). Two satisfactory methods for purification of human acrosin. Biochem. Cell Biol. 64, 1020–4.Google Scholar
Lo Leggio, L., Williams, R.M. & Jones, R. (1994). Some effects of zona pellucida glycoproteins and sulphated polymers on the autoactivation of boar sperm proacrosin and activity of α-acrosin J. Reprod. Fertil. 100, 177–185.Google Scholar
Lui, C.W. & Meizel, S. (1979). Further evidence in support of a role for hamster sperm hydrolytic enzymes in the acrosome reaction, J. Exp. Zool. 207 173–85.Google Scholar
Meizel, S. & Lui, C.W. (1976). Evidence for a role of a trypsin-like enzyme in the hamster sperm acrosome reaction. j. Exp. Zool. 195, 137–44.Google Scholar
Moreno, R.D. & Barros, C. (1991). Effect of TEST-yolk upon human sperm acrosome reaction. Micr. Electr. Biol. Cel. 15, 107–18.Google ScholarPubMed
Nakano, M., Tanak, Y., Kimura, T., Hatanak, Y. & Tobita, T. (1989). Boar acrosin digestion of the porcine egg coat, zona pellucida, and rearrangement of the zona proteins. J. Biochem. 105, 138–142.Google Scholar
Olson, G.E., Winfrey, V.P. (1994). Structure of acrosomal matrix domains of rabbit sperm, J. Struct. Biol. 112, 41–8.Google Scholar
Ordentlich, A., Barak, D., Kronman, C., Ariel, N., Segali, Y., Velan, B. & Shaffemam, A. (1995). Contribution of aromatic moieties of tyrosine 133 of the anionie subsite tryptophan 86 to catalytic efficiency and allosteric modulation of acetylcholinesterase. J. Biol. Chem. 270, 2082–91.Google Scholar
Parrish, R., Wincek, T.J. & Polakoski, K.L. (1980). Glycosami-noglycan stimulation of the in vitro conversion of boar proacrosin into acrosin. j. Androl. 1, 89–95.Google Scholar
Polakoski, K.L. & Parrish, R.F. (1977). Boar proacrosin: purification and preliminary activation studies of proacrosin isolated from ejaculated boar sperm, J. Biol. Chem. 252, 1888–94.Google Scholar
Radie, Z., Reiner, E. & Taylor, P. (1991). Role of the peripheral anionie site on acetylcholinesterase: inhibition by substrate excess and coumarin derivates. Mol. Pharmacol. 39, 98–104.Google Scholar
Richardson, R.T. & O'Rand, M.G. (1996). Site-directed mutagenesis of rabbit proacrosin. J. Biol. Chem. 271, 24069–74.Google Scholar
Rosenberg, R.D., Oosta, G.M., Jordan, R.E. & Gardner, W.T. (1980). The interaction of heparin with thrombin and antithrombin. Biochem. Biophys. Res. Commun. 96, 1200–8.Google Scholar
Sepúlveda, M.S., Becker, M.I., Barros, C. & de Ioannes, A. (1993). Interference of gamete interactions by monoclonal antibodies to acrosin. In Reproductive Immunology, ed. Dondero, F. & Johnson, P.M., pp. 335–8. Serono Symposia.Google Scholar
Shafferman, A., Velan, M., Ordentlich, A., Kronman, C., Grosfeld, H., Leitner, M., Flashner, Y., Cohen, S., Barav, D. & Ariel, N. (1992). Substrate inhibition of acetylcholinesterase: residues affecting signal transduction from the surface to the catalytic center. EMBO j. 11, 3561–68.Google Scholar
Sillerico, T., Valdivia, M., de Ioannes, A. & Barros, C. (1996). Proacrosin and acrosin determination during capacitation and acrosome reaction in rabbit spermatozoa. Bioceli 20, 133–42.Google ScholarPubMed
Stambaugh, R. & Mastroianni, L. Jr (1980). Stimulation of rhesus monkey (Macaca mulatta) proacrosin activation by oviduct fluid, J. Reprod. Fertil. 59, 479–84.CrossRefGoogle ScholarPubMed
Takano, H., Yanagimachi, R. & Urch, U.A. (1993). Evidence that acrosin activity is important for the development of fusibility of mammalian spermatozoa with the oolemma: inhibitor studies using the golden hamster. Zygote 1, 79–91.Google Scholar
Töpfer-Petersen, E. & Cechova, D. (1990). Zona pellucida induces conversion of proacrosin to acrosin. Int. j. Androl. 13, 190–6.Google Scholar
Töpfer-Petersen, E. & Henschen, A. (1988). Zona pellucida-binding and fucose-binding of boar sperm acrosin is not correlated with proteolytic activity. Biol. Chem. Hoppe-Seyler 369, 69–76.CrossRefGoogle Scholar
Töpfer-Petersen, E., Calvete, J., Schäfer, W. & Henschen, A. (1990a). Complete localization of the disulphide bridges and glycosylation sites in boar sperm acrosin. FEBS Lett. 275, 139–142.Google Scholar
Töpfer-Petersen, E., Steinberg, M., von Eschenbach, C. & Zucker, C. (1990 b). Zona pellucida-binding of boar sperm acrosin is associated with the N-terminal peptide of the acrosin B-chain (heavy chain). FEBS Lett. 265, 51–4.Google Scholar
Towbin, H., Stachelin, T. & Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedures and some applications. Proc. Nati. Acad. Sci. USA 76, 4350–4.Google Scholar
Urch, U.A., Hedrick, J.L. (1988). The inhibition of boar acrosin amidase activity by sulphated polysaccharides. Biol. Chem. Hoppe-Seyler 369, 727–32.Google Scholar
Urch, U.A. & Patel, H. (1991). The interaction of boar sperm proacrosin with its natural substrate, the zona pellucida and with polysulphated polysaccharides. Development 11, 1165–72.Google Scholar
Urch, U.A., Wardrip, N.J. & Hedrick, J.L. (1985). Limited and specific proteolysis of the zona pellucida by acrosin. J. Exp. Zool. 233, 479–83.Google Scholar
Valdivia, M., Yunes, R., Melendez, J., de Ioannes, A.E., Leyton, L., Becker, M.I. & Barros, C. (1994). Immunolocali-zation of proacrosin/acrosin in rabbit sperm during acro-some reaction and in spermatozoa recovered from the perivitelline space. Mol. Reprod. Dev. 37, 216–22.Google Scholar
Williams, R.M. & Jones, R. (1990). Specific binding of sulphated polymers to ram sperm acrosin. FEBS Lett. 270, 168–72.Google Scholar
Wincek, T., Parrish, R. & Polakoski, K. (1979). Fertilization: a uterine glycosaminoglycan stimulates the conversion of sperm proacrosin to acrosin. Science 203, 553–4.CrossRefGoogle ScholarPubMed
Windt, M.-L., Franken, D.R., de Beer, P.M., Bouic, P.J.D. & Kruger, T.F. (1991). The hemizona assay (HZA) as an experimental model to evaluate the inhibition of sperm binding to the murine zona pellucida by isolated zona pellucida protein. Andrologia 23, 209–12.Google Scholar
Wolf, D.P. (1977). Involvement of a trypsin-like activity in sperm penetration of zone-free mouse ova. J Exp. Zool. 199, 149–55.Google Scholar
Yanagimachi, R. (1994). Mammalian fertilisation. In Physiology of Reproduction, ed. Knobil, E. & Neill, J.D., pp. 189–317. New York: Raven Press.Google Scholar
Yurewicz, E.C., Pack, B.A. & Sacco, A.G. (1991). Isolation, composition, and biological activity of sugar of porcine oocyte zona pellucida 55K glycoproteins. Mol. Reprod. Dev. 30, 126–34.Google Scholar