Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-10T17:27:48.018Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  18 July 2012

Eriko Takayama-Watanabe ,
Chiara Campanella ,
Hideo Kubo  and
Akihiko Watanabe
Eriko Takayama-Watanabe
Affiliation:
Institute of Arts and Sciences, Yamagata University, 1-4-12 Kojirakawa, Yamagata 990-8560, Japan.
Chiara Campanella
Affiliation:
Dipartimento di Biologia Strutturale e Funzionale, Università di Napoli ‘Federico II’, I-80126 Napoli, Italy.
Hideo Kubo
Affiliation:
Department of Medical Biology, Tokyo Metropolitan Institute of Medical Science, 2-1-6 Kamikitazawa, Setagaya-ku, Tokyo 156-8506, Japan.
Akihiko Watanabe*
Affiliation:
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. Tel: +81 23 628 4619. e-mail: watan@sci.kj.yamagata-u.ac.jp
Get access Rights & Permissions [Opens in a new window]

Summary

The egg jelly of Discoglossus pictus contains sperm motility-activating activity, the molecular basis of which has not been studied. Discoglossus pictus sperm initiated motility immediately after immersion in egg-jelly extract, as well as after immersion in hyposmotic solution, which initiates sperm motility in the external fertilization of anuran amphibians. Sequential treatment of the D. pictus sperm with these two solutions revealed the predominant effect of hyposmolality in initiation of motility. The motility initiation induced by jelly extract was suppressed by a monoclonal antibody (mAb) that is specific for the 34 kDa sperm motility-initiating substance (SMIS) in the egg jelly of the newt, Cynops pyrrhogaster. Immunoblotting using the anti-SMIS mAb revealed several antigenic proteins that included major ones with sizes of 18- and 34-kDa in D. pictus jelly extract. Scanning electron microscopic observation revealed that granules of jelly matrix, in which SMIS localizes and which have a critical role in the internal fertilization of C. pyrrhogaster, were not observed near the surface of the D. pictus egg jelly. These results suggest that sperm motility-activating activity in egg jelly of D. pictus may be mediated by SMIS homologous proteins that act through a mechanism that is partially different from that of C. pyrrhogaster.

Keywords

CynopsDiscoglossusEgg jellyFertilizationSperm motility
Type
Research Article
Information
Zygote , Volume 20 , Issue 4 , November 2012 , pp. 417 - 422
Copyright
Copyright © Cambridge University Press 2012

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

Campanella, C. (1975). The site of spermatozoon entrance in the unfertilized egg of Discoglossus pictus (Anura): an electron microscope study. Biol. Reprod. 12, 439–47.CrossRefGoogle Scholar
Campanella, C. & Gabbiani, G. (1979). Motile properties and localization of contractile proteins in the spermatozoon of Discoglossus pictus. Gamete Res. 2, 163–75.CrossRefGoogle Scholar
Campanella, C., Carotenuto, R., Infante, V., Maturi, G. & Atripaldi, U. (1997). Sperm–egg interaction in the painted frog (Discoglossus pictus): an ultrastructural study. Mol. Reprod. Dev. 47, 323–33.3.0.CO;2-Z>CrossRefGoogle ScholarPubMed
Duellman, W.E. & Trueb, L. (1994). Biology of Amphibians. Baltimore, MD: Johns Hopkins University Press.CrossRefGoogle Scholar
Greven, H. (1998). Survey of the oviduct of salamandrids with special reference to the viviparous species. J. Exp. Zool. 282, 507–13.3.0.CO;2-0>CrossRefGoogle Scholar
Hardy, P.H. & Dent, J.N. (1986). Regulation of motility in sperm of the red-spotted newt. J. Exp. Zool. 240, 385–96.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Inoda, T. & Morisawa, M. (1987). Effect of osmolality on the initiation of sperm motility in Xenopus laevis. Comp. Biochem. Physiol. 88A, 539–42.CrossRefGoogle 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. 290, 314–22.CrossRefGoogle Scholar
Morisawa, M. (1994). Cell signaling mechanisms for sperm motility. Zool. Sci. 11, 647–62.Google ScholarPubMed
Ohta, M., Kubo, H., Nakauchi, Y. & Watanabe, A. (2010). Sperm motility-initiating activity in the egg jelly of the externally-fertilizing urodele amphibian, Hynobius lichenatus. Zool. Sci. 27, 875–9.CrossRefGoogle ScholarPubMed
Sasaki, M. (1924). On a Japanese salamander, in Lake Kuttarush, which propagates like the axolotl. J. Coll. Agric. Hokkaido Imperial University 15, 1–36.Google Scholar
Sasaki, T., Kamimura, S., Takai, H., Watanabe, A. & Onitake, K. (2002). The activity for the induction of the sperm acrosome reaction localizes in the outer layer and exists in the high-molecular-weight components of the egg-jelly of the newt, Cynops pyrrhogaster. Zygote 10, 1–9.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Takai, H. & Morisawa, M. (1995). Change in intracellular K+ concentration caused by external osmolality change regulates sperm motility of marine and freshwater teleosts. J. Cell Sci. 108, 1175–81.CrossRefGoogle ScholarPubMed
Talevi, R. & Campanella, C. (1988). Fertilization in Discoglossus pictus. I: Regionalization of sperm–egg interaction sites and occurrence of a late stage of sperm penetration. Dev. Biol. 130, 524–35.CrossRefGoogle Scholar
Towbin, H., Staehelin, T. & Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. PNAS USA 76, 4350–4.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, 793–802.CrossRefGoogle Scholar
van der Horst, G., Wilson, B. & Channing, A. (1995). Amphibian sperm: phylogeny and fertilization environment. In: Advances in Spermatozoal Phylogeny and Taxonomy, (eds Jamieson, B.G.M. & Ausio, J.), pp. 333–42. J-I Justine, Mém. Mus. natn. Hist. nat.Google Scholar
Watanabe, A. & Onitake, K. (2003). Sperm activation. In: Reproductive Biology and Phylogeny of Urodela (Amphibia), (ed. Sever, D.M.), Enfield, NH: Science Publishers. pp. 423–55.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.CrossRefGoogle ScholarPubMed
Watanabe, A., Fukutomi, K., Kubo, H., Ohta, M., Takayama-Watanabe, E. & Onitake, K. (2009). Identification of egg-jelly substances triggering sperm acrosome reaction in the newt, Cynops pyrrhogaster. Mol. Reprod. Dev. 79, 399–406.CrossRefGoogle 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, 591–97.CrossRefGoogle ScholarPubMed