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Contribution of different Ca2+ channels to the acrosome reaction-mediated initiation of sperm motility in the newt Cynops pyrrhogaster

Published online by Cambridge University Press:  20 December 2013

Eriko Takayama-Watanabe
Affiliation:
Institute of Arts and Sciences, Yamagata University, 1-4-12 Kojirakawa, Yamagata 990-8560, Japan.
Hiroto Ochiai
Affiliation:
Department of Biology, Faculty of Science, Yamagata University, 1-4-12 Kojirakawa, Yamagata 990-8560, Japan.
Shunpei Tanino
Affiliation:
Department of Biology, Faculty of Science, Yamagata University, 1-4-12 Kojirakawa, Yamagata 990-8560, Japan.
Akihiko Watanabe*
Affiliation:
Department of Biology, Faculty of Science, Yamagata University, 1-4-12 Kojirakawa, Yamagata 990-8560, Japan. Department of Biology, Faculty of Science, Yamagata University, 1-4-12 Kojirakawa, Yamagata 990-8560, Japan.
*
All correspondence to: Akihiko Watanabe. Department of Biology, Faculty of Science, Yamagata University, 1-4-12 Kojirakawa, Yamagata 990-8560, Japan. e-mail: [email protected]

Summary

Initiation of sperm motility in urodeles, which is induced by a sperm motility-initiating substance (SMIS) in the sequestered granules on the surface of egg jelly, is mediated by the acrosome reaction (AR), which is triggered by an AR-inducing substance (ARIS) on a sheet-like structure. Details of the unique process of the interaction between egg jelly and sperm in these species is still unclear. The current study showed the fine structure of egg jelly in the newt Cynops pyrrhogaster, a urodele species, revealing that its outer surface was covered by a sheet-like structure of approximately 0.29 μm in thickness. Granules of approximately 2 μm in diameter with small particles of approximately 54 nm were attached to its surface and distributed inhomogeneously just beneath the sheet-like structure. Emission spectrometry revealed that the Ca2+ concentration was maintained at a high level compared with that of the blood plasma and the vas deferens fluid, suggesting that egg jelly is a reliable source of Ca2+ for the sperm–egg interaction. Blockers of the T-type voltage-dependent Ca2+ channel (VDCC), but not the L-type VDCC, inhibited both AR and initiation of sperm motility. Conversely, Ni+, which affects the α1 H subunit of T-type VDCC, only inhibited the initiation of sperm motility. These data suggest that, in response to ARIS and SMIS, sequential gating of distinct Ca2+ channels occurs in the AR, followed by the initiation of sperm motility on the surface of the egg jelly in C. pyrrhogaster at fertilization.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013 

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References

Arnoult, C., Villaz, M. & Florman, H.M. (1998). Pharmacological properties of the T-type Ca2+ current of mouse spermatogenic cells. Mol. Pharmacol. 53, 1104–11.Google Scholar
Bezprozvanny, I. & Tsien, R.W. (1995). Voltage-dependent blockade of diverse types of voltage-gated Ca2+ channels expressed in Xenopus oocytes by the Ca2+ channel antagonist mibefradil (Ro 40-5967). Mol. Pharmacol. 48, 540–9.Google Scholar
Cai, X. & Clapham, D.E. (2008). Evolutionary genomics reveals lineage-specific gene loss and rapid evolution of a sperm-specific ion channel complex: CatSpers and CatSperβ. PLoS One 3, e3569. Google Scholar
Darszon, A., Acevedo, J.J., Galindo, B.E., Hernández-González, E.O., Nishigaki, T., Trevinõ, C.L., Wood, C. & Beltrán, C. (2006). Sperm channel diversity and functional multiplicity. Reproduction 131, 977–88.Google Scholar
Díaz, D., Bartolo, R., Delgadillo, D.M., Higueldo, F. & Gomora, J.C. (2005). Contrasting effects of Cd2+ and Co2+ on the blocking/unblocking of human Cav3 channels. J. Membr. Biol. 207, 91105.Google Scholar
Furukawa, T., Nukada, T., Namiki, Y., Miyashita, Y., Hatsuno, K., Ueno, Y., Yamakawa, T. & Isshiki, T. (2009). Five different profiles of dihydropyridines in blocking T-type Ca2+ channel subtypes (Cav3.1 (α1G), Cav3.2 (α1 H), and Cav3.3 (α1I)) expressed in Xenopus oocytes. Eur. J. Pharmacol. 613, 100–7.Google Scholar
Greven, H. (1998). Survey of the oviduct of salamandrids with special reference to the viviparous species. J. Exp. Zool. 282, 507–25.3.0.CO;2-0>CrossRefGoogle Scholar
Hiyoshi, W., Sasaki, T., Takayama-Watanabe, E., Takai, H., Watanabe, A. & Onitake, K. (2007). Egg jelly of the newt, Cynops pyrrhogaster contains a factor essential for sperm binding to the vitelline envelope. J. Exp. Zool. 307A, 301–11.Google Scholar
Itoh, T., Kamimura, S., Watanabe, A. & Onitake, K. (2002). Egg-jelly structure promotes efficiency of internal fertilization in the newt, Cynops pyrrhogaster . J. Exp. Zool. 292, 314–22.CrossRefGoogle ScholarPubMed
Jaiswal, B.S. & Eisenbach, M. (2002). Capacitation. In Fertilization (ed. Hardy, D.M.), pp. 57117. San Diego, CA, USA: Academic Press.CrossRefGoogle Scholar
Jiménez, C., Bourinet, E., Leuranguer, V., Richard, S., Snutch, T.P. & Nargeot, J. (2000). Determinants of voltage-dependent inactivation affect mibefradil block of calcium channels. Neuropharmacology 39, 110.Google Scholar
Katagiri, Ch. (1987). Role of oviductal secretions in mediating gamete fusion in anuran amphibians. Zool. Sci. 4, 114.Google Scholar
Lee, J.H., Gomora, J.C., Cribbs, L.L. & Perez-Reyes, E. (1999). Nickel block of three cloned calcium channels: low concentrations selectively block α1 H . Biophys J. 77, 3034–42.Google Scholar
Lopin, K.V., Obejero-Paz, C.A. & Jones, S.W. (2010). Evaluation of a two-site, three-barrier model for permeation in CaV3.1 (α1G) T-type calcium channels: Ca2+, Ba2+, Mg2+, and Na+ . J. Membr. Biol. 235, 131–43.Google Scholar
Matsuda, M. & Onitake, K. (1984). Fertilization of the eggs of Cynops pyrrhogaster (Japanese newt) after immersion in water. Roux's Arch. Dev. Biol. 193, 61–3.CrossRefGoogle ScholarPubMed
Mishra, S.K. & Hermsmeyer, K. (1994). Selective inhibition of T-type Ca2+ channels by Ro 40–5967. Circ. Res. 75, 144–8.CrossRefGoogle ScholarPubMed
Mizuno, J., Watanabe, A. & Onitake, K. (1999). Initiation of sperm motility in the newt, Cynops pyrrhogaster, is induced by a heat-stable component of egg-jelly. Zygote 7, 329–34.Google Scholar
Neubaum, D.M. & Wolfner, M. (1999). Wise, winsome, or weird? Mechanisms of sperm storage in female animals. Curr. Topics Dev. Biol. 41, 6797.Google Scholar
Okimura, M., Watanabe, A. & Onitake, K. (2001). Organization of carbohydrate components in the egg-jelly layers of the newt, Cynops pyrrhogaster . Zool. Sci. 18, 909–18.Google Scholar
Omata, S. (1993). Relative roles of jelly layers in successful fertilization of Bufo japonicus . J. Exp. Zool. 265, 329–35.Google Scholar
Podlaha, O. & Zhang, J. (2003). Positive selection on protein-length in the evolution of a primate sperm ion channel. Proc. Natl. Acad. Sci. USA 100, 12241–6.Google Scholar
Ren, D. & Xia, J. (2010). Calcium signaling through CatSper channels in mammalian fertilization. Physiology 25, 165–75.CrossRefGoogle ScholarPubMed
Ren, D., Navarro, B., Perez, G., Jackson, A.C., Hsu, S., Shi, Q., Tilly, J.L. & Clapham, D.E. (2001). A sperm ion channel required for sperm motility and male fertility. Nature 413, 603–9.Google Scholar
Son, W.Y., Lee, J.H., Lee, J.H. & Han, C.T. (2000). Acrosome reaction of human spermatozoa is mainly mediated by α1 H T-type calcium channels. Mol. Hum. Reprod. 6, 893–7.Google Scholar
Strünker, T., Goodwin, N., Brenker, C., Kashikar, N.D., Weyand, I., Seifert, R. & Kaupp, U.B. (2011). The CatSper channel mediates progesterone-induced Ca2+ influx in human sperm. Nature 471, 382–6.Google Scholar
Takahashi, S., Nakazawa, H., Watanabe, A. & Onitake, K. (2006). The outermost layer of egg-jelly is crucial to successful fertilization in the newt, Cynops pyrrhogaster . J. Exp. Zool. 305A, 1010–7.Google Scholar
Takahashi, T., Kutsuzawa, M., Shiba, K., Takayama-Watanabe, E., Inaba, K. & Watanabe, A. (2013). Distinct Ca2+ channels maintain a high motility state of the sperm that may be needed for penetration of egg jelly of the newt, Cynops pyrrhogaster . Dev. Growth Differ. 55, 657–67.Google Scholar
Takayama-Watanabe, E., Campanella, C., Kubo, H. & Watanabe, A. (2012). Sperm motility initiation by egg jelly of the anuran, Discoglossus pictus may be mediated by sperm motility-initiating substance of the internally-fertilizing newt, Cynops pyrrhogaster . Zygote 20, 417–22.CrossRefGoogle ScholarPubMed
Ukita, M., Itoh, T., Watanabe, A. & Onitake, K. (1999). Substances for the initiation of sperm motility in egg-jelly of the Japanese newt, Cynops pyrrhogaster . Zool. Sci. 16, 793802.CrossRefGoogle Scholar
Watanabe, A. & Onitake, K. (2003). Sperm activation. In Reproductive Biology and Phylogeny of Urodele (Amphibian) (ed. Sever, D.M.), pp. 423–55. Enfield, NH, USA: Science Publisher.Google Scholar
Watanabe, T., Ito, T., Watanabe, A. & Onitake, K. (2003). Characteristics of sperm motility induced on the egg-jelly in the internal fertilization of the newt, Cynops pyrrhogaster . Zool. Sci. 20, 345–52.Google Scholar
Watanabe, T., Kubo, H., Takeshima, S., Nakagawa, M., Ohta, M., Kamimura, S., Takayama-Watanabe, E., Watanabe, A. & Onitake, K. (2010). Identification of the sperm motility-initiating substance in the newt, Cynops pyrrhogaster, and its possible relationship with the acrosome reaction during internal fertilization. Int. J. Dev. Biol. 54, 591–7.Google Scholar
Watanabe, A., Takayama-Watanabe, E., Vines, C.A. & Cherr, G.N. (2011). Sperm motility-initiating substance in newt egg-jelly induces differential initiation of sperm motility based on sperm intracellular calcium levels. Dev. Growth Differ. 53, 917.Google Scholar
Xia, J. & Ren, D. (2009). Egg-coat proteins activate calcium entry into mouse sperm via CATSPER channels. Biol. Reprod. 80, 1092–8.Google Scholar