Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-26T06:09:53.087Z Has data issue: false hasContentIssue false

Specific binding of acrosome-reaction-inducing substance to the head of starfish spermatozoa

Published online by Cambridge University Press:  26 September 2008

Akira Ushiyama
Affiliation:
Department of Life Science, Tokyo Institute of Technology, Japan.
Takeo Araki
Affiliation:
Department of Life Science, Tokyo Institute of Technology, Japan.
Kazuyoshi Chiba
Affiliation:
Department of Life Science, Tokyo Institute of Technology, Japan.
Motonori Hoshi*
Affiliation:
Department of Life Science, Tokyo Institute of Technology, Japan.
*
Motonori Hoshi, Department of Life Science, Tokyo Institute of Technology, 4259 Nagatsuta, Midori-ku, Yokohama 227, Japan. Telephone/Fax: 81-45-923-0368.

Extract

In the starfish, spermatozoa undergo the acrosome reaction upon encountering the jelly coat of eggs. A highly sulphated glycoprotein in the jelly coat is called acrosome-reaction-inducing substance (ARIS) because it is the key signal molecule to trigger the acrosome reaction. The activity of ARIS is mainly attributed to its sulphate and saccharide residues. The extremely large molecular size and speciesspecific action of ARIS suggest the presence of a specific ARIS receptor on the sperm surface, but no experimental evidence for the receptor has been presented. We therefore measured specific binding of ARIS and its pronase digest (P-ARIS), which retains the full activity of ARIS, to homologous spermatozoa by using fluorescien-isothiocyanate-labelled ARIS and125 I-labelled P-ARIS, respectively. The spermatozoa had the ability to bind ARIS, as well as P-ARIS, specifically. The binding was species-specific, and mostly localised to the head region of spermatozoa. Scatchard plot analysis indicated the presence of one class of ARIS receptor on the surface of acrosome-intact speramatozoa. Furthermore, the specific binding of P-ARIS to the anterior region of sperm heads was microscopically confirmed by using P-ARIS conjugated to polystyrene latex beads with intense fluorescence. It is concluded that starfish spermatozoa have a specific receptor for ARIS on the surface of the anterior region of heads.

Type
Article
Copyright
Copyright © Cambridge University Press 1993

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

Bleil, J.D. & Wasserman, P.M. (1983). Sperm-egg interaction in the mouse: sequence of events and induction of the acrosome reaction by a zona pellucida glycoprotein. Dev.Biol. 95, 317–24CrossRefGoogle ScholarPubMed
Bleil, J.D. & Wasserman, P.M. (1986). Autoradiographic visualization of the mouse egg's sperm receptor bound to sperm. J. Cell Biol. 102, 1363–71CrossRefGoogle ScholarPubMed
Bleil, J.D. & Wasserman, P.M. (1990). Identification of a ZP3-binding protein on acrosome-intact mouse sperm by photoaffinity crosslinking. Proc. Natl. Acad. Sci. USA 87, 5563–7CrossRefGoogle ScholarPubMed
Darszon, A.Guerrero, A.Lievano, A.Gonzalez-Martinez, M. & Morales, M. (1988). Ionic channels in sea urchin sperm physiology. News Physiol. Sci. 3, 181–5Google Scholar
Dubois, M.Gilles, K.A.Hamilton, J.K.Rebers, P.A.Smith, F. (1956). Colorimetric method for determination of sugars and related substances. Anal. Chem. 28, 350–6CrossRefGoogle Scholar
Garbers, D.J. (1989). Molecular bases of fertilization. Annu.Rev. Biochem. 58, 719–42CrossRefGoogle Scholar
Hoshi, M.Amano, T.Okita, Y.Okinaga, T. & Matsui, T. (1990). Egg signals for triggering the acrosome reaction in starfish spermatozoa. J. Reprod. Fert. (Suppl.) 42, 23–31Google ScholarPubMed
Hoshi, M.Okinaga, T.Kontani, K.Araki, T. & Chiba, K. (1991). Acrosome reaction-inducing glycoconjugate in the jelly coat of starfish eggs. In Comparative Spermatology 20 Years After ed. Baccetti, B. pp. 175–80.New York: Raven Press.Google Scholar
Hunter, W.H. & Greenwood, F.C. (1962). Preparation of iodine-131 labelled human growth hormone of high specific activity. Nature 194 495–6CrossRefGoogle ScholarPubMed
Ikadai, H. & Hoshi, M. (1981 a). Biochemical studies on the acrosome reaction of the starfish, asterias amurensis factors participating in the acrosome reaction. Dev. Growth Differ. 23, 7380.CrossRefGoogle ScholarPubMed
Ikadai, H. & Hoshi, M. (1981 b). Biochemical studies on the acrosome reaction of the strafish, Asterias amurensis: purification and characterization of acrosome reactioninducing substance. Dev. Growth Differ. 23, 81–8.CrossRefGoogle ScholarPubMed
Lowry, O.H., 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
Maeda, H., Ishida, H., Kawauchi, H. & Tsuziumura, K. (1969). Reaction of fluorescein-isothiocyanate with proteins an amino acids. J. Biochem. 65, 777–83.CrossRefGoogle ScholarPubMed
Matsui, T., Nishiyama, I., Hino, A., & Hoshi, M. (1986 a) Induction of the acrosome reaction in starfish. Dev. Growth Differ. 28 339–48.CrossRefGoogle ScholarPubMed
Matsui, T., Nishiyama, I., Hino, A., & Hoshi, M. (1986 b). Acrosome-inducing substance purified from the egg jelly inhibits jelly-induced acrosome reaction in starfish: an apparent contradiction. Dev. Growth Differ. 28, 349–57.CrossRefGoogle Scholar
Mortillo, S. & Wasserman, P.M., (1991). Differential binding of gold-labelled zona pellucida glycoproteins mZP2 and mZP3 to mouse sperm membrane compartments. Development 113, 141–9.CrossRefGoogle Scholar
Nishiyama, I., Matsui, T. & Hoshi, M. (1987 a). Purification of Co-ARIS, a cofactor for acrosome reaction-inducing substance, from the egg jelly of starfish. Dev. Growth Differ. 29, 161–9CrossRefGoogle ScholarPubMed
Nishiyama, I., Matsui, T., Fujimoto, Y., Ikekawa, N. & Hoshi, M. (1987 b). Correlation between the molecular structure and the biological activity of Co-ARIS, a co-factor for acrosome reaction-inducing substance. Dev. Growth Differ. 29, 171–6CrossRefGoogle Scholar
Okinaga, T., Ohashi, Y. & Hoshi, M. (1992). A novel saccharide structure, , is present in acrosome reaction-inducing substance of the starfish, Asterias amurensis. Biochem. Biophys. Res.Commun 186, 405–10.CrossRefGoogle ScholarPubMed
Podell, S.B. & Vacqueir, V.D. (1985). Purification of the Mr 80000 and Mr 210000 proteins of the sea urchin sperm plasma membrane. J. Biol. Chem. 260, 2715–18.CrossRefGoogle Scholar
Podell, S.B., Moy, G.W. & Vacquier, V.D. (1984). Isolation and characterization of a plasma membrane fraction from sea urchin sperm exhibiting species specific recognition of the egg surface. Biochim. Biophys. Acta 778, 2537.CrossRefGoogle ScholarPubMed
Scatchard, G. (1949). The attractions of proteins for small molecules and ions. Ann. N.Y. Acad. Sci. 51, 660–72.CrossRefGoogle Scholar
SeGall, G.K., & Lennarz, W.J. (1979). Chemical characterization of the component of the jelly coat from sea urchin eggs responsible for induction of the acrosome reaction. Dev. Biol. 71, 3348CrossRefGoogle ScholarPubMed
Suzuki, N. (1990). Structure and function of sea urchin egg jelly molecules. Zool. Sci. 7, 335–70.Google Scholar
Tilney, L.G. (1985). The acrosomal reaction In Biology of Fertilization, ed. Metz, C.B. & Monroy, A., vol. 2, pp. 157213. Orlando: Academic Press.CrossRefGoogle Scholar
Trimmer, J.S. & Vacquier, V.D. (1986). Activation of sea urchin gametes. Annu. Rev. Cell Boil. 2, 126.CrossRefGoogle ScholarPubMed
Timmer, J.S., Trowbridge, I.S. & Vacquier, V.D. (1985). Monoclonal antibody to a membrane glycoprotein inhibits te acrosome reaction and associated Ca2+ and H+ fluxes of sea urchin sperm. Cell 40, 697703.CrossRefGoogle Scholar
Timmer, J.S., Schackmann, R.W. & Vacquier, V.D. (1986). Monoclonal antibodies increase inracellular Ca2+ in sea urchin spermatozoa. Proc. Natl. Acad. Sci. USA 83, 9055–9.CrossRefGoogle Scholar
Wasserman, P.M. (1990). Profile of a mammalian sperm receptor. Development 108, 117.CrossRefGoogle Scholar