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PKA activation in concert with ARIS and asterosap induces the acrosome reaction in starfish

Published online by Cambridge University Press:  01 November 2006

M. Sadiqul Islam ,
O. Kawase ,
S. Hase ,
M. Hoshi  and
M. Matsumoto
M. Sadiqul Islam
Affiliation:
Department of Biosciences and Informatics, Keio University 3–14–1, Hiyoshi, Kouhoku-ku, Yokohama, Japan.
O. Kawase
Affiliation:
Department of Biosciences and Informatics, Keio University 3–14–1, Hiyoshi, Kouhoku-ku, Yokohama, Japan.
S. Hase
Affiliation:
Department of Biology, Keio University 4–1–1, Hiyoshi, Kouhoku-ku, Yokohama, Japan.
M. Hoshi
Affiliation:
Department of Biosciences and Informatics, Keio University 3–14–1, Hiyoshi, Kouhoku-ku, Yokohama, Japan.
M. Matsumoto*
Affiliation:
Department of Biosciences and Informatics, Keio University 3–14–1, Hiyoshi, Kouhoku-ku, Yokohama, Japan.
*
All correspondence to: M. Matsumoto. Department of Biosciences and InformaticsKeio University 3–14–1, Hiyoshi, Kouhoku-ku, Yokohama 223–8522, Japan. Tel: +81 045 566 1774. Fax: +81 045 566 1448. e-mail: mmatsumo@bio.keio.ac.jp
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Summary

The acrosome reaction (AR) is a fundamental event for fertilization, which is induced in concert with acrosome reaction-inducing substance (ARIS) and asterosap, both of which are components of starfish egg jelly (EJ). During the AR, a spermatozoon undergoes a series of physiological changes, such as in intracellular cGMP concentration ([cGMP]i), pHi and intracellular Ca2+ concentration ([Ca2+]i). Affinity purification of cGMP-binding protein resulted in the isolation of a regulatory subunit of the cAMP-dependent protein kinase A (PKA), suggesting the involvement of a cAMP-dependent pathway in the AR. By using a cAMP enzyme immunoassay, [cAMP]i was found to increase in starfish spermatozoa when stimulated with ARIS and asterosap. ARIS could also increase the [cAMP]i in the presence of high pH seawater. Pretreatment of spermatozoa with two specific and cell-permeable PKA inhibitors, H89 and KT5720, prevented the induction of the AR in a concentration-dependent manner. These results suggest that PKA activity participates in the induction of the AR with ARIS and asterosap. To investigate this, we have cloned a gene that encodes a regulatory subunit of PKA that had been identified in starfish spermatozoa.

Keywords

Acrosome reactionCyclic AMPEgg jellyPKAStarfish
Type
Research Article
Information
Zygote , Volume 14 , Issue 4 , November 2006 , pp. 329 - 340
Copyright
Copyright © Cambridge University Press 2006

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References

Altfelder, K. & Müller, U. (1991). Cyclic nucleotide dependent protein kinases in the neural tissues of the honeybee Apis mellifera. Insect Biochem. 21, 487–94.CrossRefGoogle Scholar
Bardales, J.R., Diaz-Enrich, M.J., Ibarguren, I. & Villamarin, J.A. (2004). Isoforms of cAMP-dependent protein kinase in the bivalve mollusk Mytilus galloprovincialis: activation by cyclic nucleotides and effect of temperature. Arch. Biochem. Biophys. 432, 71–78.CrossRefGoogle ScholarPubMed
Bohmer, M., Van, Q., Weyand, I., Hagen, V., Beyermann, M., Matsumoto, M., Hoshi, M., Hildebrand, E., & Kaupp, B. (2005). Ca2+ spikes in the flagellum control chemotactic behavior of sperm. EMBO J. 24, 2741–52.Google Scholar
Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–54.Google Scholar
Brandt, H. & Hoskins, D.D. (1980). A cAMP-dependent phosphorylated motility protein in bovine epididymal sperm. J. Biol. Chem. 255, 982–87.Google Scholar
Breitbart, H. (2002). Intracellular calcium regulation in sperm capacitation and acrosomal reaction. Mol. Cell Endocrinol. 22, 139–44.CrossRefGoogle Scholar
Byrne, M., Morrice, M.G. & Wolf, B. (1997). Introduction of the Northern Pacific asteroid Asterias amurensis to Tasmania – reproduction and current distribution. Marine Biol. 127, 673–85.CrossRefGoogle Scholar
Carninci, P. & Hayashizaki, Y. (1999). High-efficiency full-length cDNA cloning. J. Meth. Enzymol. 303, 19–44.CrossRefGoogle ScholarPubMed
Chomczynski, P. & Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction. Anal Biochem. 162, 156–59.CrossRefGoogle ScholarPubMed
Cytrinska, M., Wojda, I., Frajnt, M. & Jakubowicz, T. (1999). PKA from Saccharomyces cerevisiae can be activated by cyclic AMP and cyclic GMP. Can. J. Microbiol. 45, 31–37.Google Scholar
Darszon, A., Nishigaki, T., Wood, C., Trevino, C.L., Felix, R. & Beltran, C. (2005). Calcium channels and Ca2+ fluctuations in sperm physiology. Int. Rev. Cyto. 243, 79–172.CrossRefGoogle ScholarPubMed
Garbers, D.L. & Hardman, J.G. (1976). Effects of egg factors on cyclic nucleotide metabolism in sea urchin sperm. J. Cycl. Nuc. Res. 2, 59–70.Google Scholar
Garbers, D.L. & Kopf, G.S. (1980). The regulation of spermatozoa by calcium and cyclic nucleotides. Adv. Cyclic Nucleotide Res. 13, 251–306.Google Scholar
Garbers, D.L., Tubb, D.J. & Kopf, G.S. (1980). Regulation of sea urchin sperm cyclic AMP-dependent protein kinases by an egg associated factor. Biol. Reprod. 22, 526–32.Google Scholar
Gunaratne, H.M., Yamagaki, T., Matsumoto, M. & Hoshi, M. (2003). Biochemical characterization of inner sugar chains of acrosome reaction-inducing substance in jelly coat of starfish eggs. Glycobiology 13, 567–80.CrossRefGoogle ScholarPubMed
Harrison, R.A.P. (2004). Rapid PKA-catalysed phosphorylation of boar sperm proteins induced by the capacitating agent bicarbonate. Mol. Reprod. Dev. 67, 337–52.CrossRefGoogle ScholarPubMed
Hirohashi, N. & Vacquier, V.D. (2002a). Egg sialoglycans increase intracellular pH and potentiate the acrosome reaction of sea urchin sperm. J. Biol. Chem. 277, 8041–47.Google Scholar
Hirohashi, N. & Vacquier, V.D. (2002b). Egg fucose sulfate polymer, sialoglycan and speract all trigger the sea urchin sperm acrosome reaction. Biochem. Biophys. Res. Commun. 296, 833–39.Google Scholar
Hirohashi, N. & Vacquier, V.D. (2003). Store-operated calcium channels trigger exocytosis of the sea urchin sperm acrosomal vesicle. Biochem. Biophys. Res. Commun. 304, 285–92.CrossRefGoogle ScholarPubMed
Hoshi, M., Nishigaki, T., Ushiyama, A., Okinaga, T., Chiba, K. & Matsumoto, M. (1994). Egg-jelly signal molecules for triggering the acrosome reaction in starfish spermatozoa. Int. J. Dev. Biol. 38, 167–74.Google Scholar
Hoshino, K., Nomura, K. & Suzuki, N. (1997). Cyclic AMP-dependent activation of an inter-phylum hybrid histone-kinase complex reconstituted from sea urchin sperm-regulatory subunits and bovine heart catalytic subunits. Eur. J. Biochem. 243, 612–23.Google Scholar
Ikadai, H. & Hoshi, M. (1981). Biochemical studies on the acrosome reaction of the starfish, Asterias amurensis. I. Factors participating in the acrosome reaction. Dev. Growth Differ. 23, 73–80.CrossRefGoogle ScholarPubMed
Jahnsen, T., Hedin, L., Kidd, V.J., Beattie, W.G., Lohmann, S.M., Walter, U., Durica, J., Schulz, T.Z., Schiltz, E., Browner, M.F., Lawrence, C.B., Goldman, D., Ratoosh, S.L. & Richards, J.S. (1986). Molecular cloning, cDNA structure and regulation of the regulatory subunit of type II cAMP-dependent protein kinase from rat ovarian granulosa cells. J. Biol. Chem. 261, 12352–61.Google Scholar
Kawase, O., Minakata, H., Hoshi, M. & Matsumoto, M. (2005). Astersap-induced elevation in intracellular pH is indispensable for ARIS-induced sustained increase in intracellular Ca2+ and following acrosome reaction in starfish spermatozoa. Zygote 13, 63–71.CrossRefGoogle ScholarPubMed
Kawase, O., Ueno, S., Minakata, H., Hoshi, M. & Matsumoto, M. (2004). Guanylyl cyclase and cGMP-specific phosphodiesterase participate in the acrosome reaction of starfish sperm. Zygote 12, 345–55.Google Scholar
Kopf, G.S. & Garbers, D.L. (1980). Calcium and fucose-sulfate-rich polymer regulate sperm cyclic nucleotide metabolism and the acrosome reaction. Biol. Reprod. 22, 118–26.Google Scholar
Koyota, S., Wimalasiri, K.M.S. & Hoshi, M. (1997). Structure of the main saccharide chain in acrosome reaction-inducing substance of starfish, Asterias amurensis, J. Biol. Chem. 272, 10372–76.Google Scholar
Leboulle, G. & Müller, U. (2004). Synergistic activation of insect cAMP-dependent protein kinase A (type II) by cyclic AMP and cyclic GMP. FEBS Lett. 576, 216–20.CrossRefGoogle Scholar
Levy, F.O., Oyen, O., Sandberg, M., Tasken, K., Eskild, W., Hansson, V. & Jahnsen, T. (1988). Molecular cloning, complementary deoxyribonucleic acid structure and predicted full-length amino acid sequence of the hormone-inducible regulatory subunit of 3′-5′-cyclic adenosine monophosphate-dependent protein kinase from human testis, Mol. Endocrinol. 2, 1364–73.Google Scholar
Locatelli, F., LaFourcade, C., Maldonado, H. & Romano, A. (2001). Characterization of cAMP-dependent protein kinase isoforms in the brain of the crab Chasmagnathus J. Comp. Physiol. [B] 171, 33–40.CrossRefGoogle ScholarPubMed
Luo, Z., Shafit-Zagardo, B. & Erlichman, J. (1990). Identification of the MAP2- and P75-binding domain in the regulatory subunit (RII beta) of type II cAMP-dependent protein kinase. Cloning and expression of the cDNA for bovine brain RII beta. J. Biol. Chem. 265, 21804–10.Google Scholar
Matsui, T., Nishiyama, I., Hino, A. & Hoshi, M. (1986). Induction of the acrosome reaction in starfish. Dev. Growth Differ. 28, 339–48.CrossRefGoogle ScholarPubMed
Matsumoto, M., Solzin, Z., Helbig, A., Hagen, V., Ueno, S., Kawase, O., Maruyama, Y., Ogiso, M., Godde, M., Minakata, H., Kaupp, U.B., Hoshi, M. & Weyand, I. (2003). A sperm-activating peptide controls a cGMP-signaling pathway in starfish sperm. Dev. Biol. 260, 314–24.Google Scholar
Nishigaki, T., Chiba, K., Miki, W. & Hoshi, M. (1996). Structure and function of asterosaps, sperm-activating peptides from the jelly coat of starfish eggs. Zygote 4, 237–45.Google Scholar
Nishiyama, I., Matsui, T., Fujimoto, Y., Ikekawa, N. & Hoshi, M. (1987). Correlation between the molecular structure and biological activity of Co-ARIS, a cofactor for acrosome reaction-inducing substance. Dev. Growth Differ. 29, 171–76.Google Scholar
O'Flaherty, C., de Lamirande, E. & Gagnon, C. (2004). Phosphorylation of the arginine–X–X–(serine/threonine) motif in human sperm proteins during capacitation: modulation and protein kinase A dependency. Mol. Hum. Reprod. 10, 355–63.CrossRefGoogle ScholarPubMed
Reed, R.B., Sandberg, M., Jahnsen, T., Lohmann, S.M., Francis, S.H. & Corbin, J.D. (1996). Fast and slow cyclic nucleotide-dissociation sites in cAMP-dependent protein kinase are transposed in type Iβ cGMP-dependent protein kinase. J. Biol. Chem. 271, 17570–75.CrossRefGoogle ScholarPubMed
Rodriguez, J.L., Barcia, R., Ramos-Martinez, J.I. & Villamarin, J.A. (1998). Purification of a novel isoform of the regulatory subunit of cAMP-dependent protein kinase from the bivalve mollusk Mytilus galloprovincialis. Arch. Biochem. Biophys. 359, 57–62.Google Scholar
Schackmann, R.W. (1989). Ionic regulation of the sea urchin sperm acrosome reaction and stimulation by egg-derived peptides. In The Cell Biology of Fertilization, (eds Schatten, H. & Schatten, G.), San Diego: Academic Press.Google Scholar
Spungin, B. & Breitbart, H. (1996). Calcium mobilization and influx during sperm exocytosis. J. Cell Sci. 109, 1947–55.CrossRefGoogle ScholarPubMed
Su, Y.H., Chen, S.H., Zhou, H. & Vacquier, V.D. (2005). Tandem mass spectrometry identifies proteins phosphorylated by cyclic AMP-dependent protein kinase when sea urchin sperm undergo the acrosome reaction. Dev. Biol. 285, 116–25.Google Scholar
Sundberg, L. & Porath, J. (1974). Preparation of adsorbents for biospecific affinity chromatography. Attachment of group-containing ligands to insoluble polymers by means of bifunctional oxiranes. J. Chromatogr. 90, 87–98.Google Scholar
Tash, J.S. & Means, A.R. (1983). Cyclic adenosine 3′,5′ monophosphate, calcium and protein phosphorylation in flagellar motility. Biol. Reprod. 28, 75–104.CrossRefGoogle ScholarPubMed
Taylor, S.S., Buechler, J.A. & Yonemoto, W. (1990). cAMP-dependent protein kinase: framework for a diverse family of regulatory enzymes. Annu. Rev. Biochem. 59, 971–1005.Google Scholar
Vardanis, A. (1980). A unique cyclic nucleotide-dependent protein kinase. J. Biol. Chem. 255, 7238–43.Google Scholar
Ward, C.R. & Kopf, G.S. (1993). Molecular events mediating sperm activation. Dev. Biol. 158, 9–34.CrossRefGoogle ScholarPubMed
Watkins, H.D., Kopf, G.S. & Garbers, D.L. (1978). Activation of sperm adenylate cyclase by factors associated with eggs. Biol. Reprod. 19, 890–94.Google Scholar