Elsevier

Developmental Biology

Volume 134, Issue 2, August 1989, Pages 446-451
Developmental Biology

Full paper
Evidence that the voltage-dependent component in the fertilization process is contributed by the sperm

We dedicate this paper to the memory of the late Dr. Susumu Hagiwara.
https://doi.org/10.1016/0012-1606(89)90117-6Get rights and content

Abstract

To investigate the mechanisms that account for the voltage dependence of fertilization and provide an electrical block to polyspermy, we studied cross-fertilizations between three species of amphibians having different degrees of voltage dependence. Anurans, such as the toad Bufo japonicus, as well as the primitive urodele Hynobius nebulosus, have voltage-dependent fertilization; other urodeles, such as Cynops pyrrhogaster, have voltage-independent fertilization (Y. Iwao, 1989, Dev. Biol. 134, 438–445). Entry of Hynobius sperm into Cynops eggs was blocked by clamping the egg's membrane potential at +40 mV, as is the case for fertilization of Hynobius eggs with Hynobius sperm, but not for fertilization of Cynops eggs with Cynops sperm. Therefore, fertilization was voltage dependent in an experimental condition where only the sperm could be contributing this characteristic. The voltage-dependent properties of fertilization between Bufo eggs and Hynobius sperm were also characteristic of the sperm species; fertilization was blocked at +50 mV as in Hynobius fertilization, but not at +20 mV as in Bufo fertilization. These results support the conclusion that the voltage dependence of fertilization results from a component contributed by the sperm.

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    We previously proposed that a positive molecule on the sperm membrane is involved in sensing the voltage of the egg membrane at fertilization (Iwao and Jaffe, 1989). The level of voltage to prevent fertilization is dependent on the sperm species in the fertilization of amphibians (Iwao and Jaffe, 1989; Jaffe et al., 1983) and in marine invertebrates (Jaffe et al., 1982). In the present study, we showed that pre-treatment of the sperm membrane with negatively charged GM1 or the antibody against the positively charged HPX domain allows for sperm to fertilize eggs clamped at 0 mV, at which level fertilization never occurs in insemination with untreated sperm.

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    Voltage‐clamp studies of other anuran eggs, which do not exhibit such specializations for fusion, have shown that the efficacy of depolarization is instead dependent on its maximum amplitude. For example, the peak Vm achieved by one species is optimized to block supernumerary fusion of only conspecific sperm, and is not sufficient to repel less sensitive heterospecific sperm who require a higher voltage potential to be deterred or who are simply insensitive to membrane voltage potentials (Iwao and Jaffe, 1989; Jaffe et al., 1983a). To establish a timely fast electrical block requires a rapid signaling cascade that likely originates from the sperm itself (Iwao and Jaffe, 1989).

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    This membrane potential is believed to be involved in the fast block to polyspermy, since sperm cannot fertilize eggs when the egg membrane voltage is maintained at larger than 0 mV (Iwao and Jaffe, 1989). It has been shown that this may be due to the presence of voltage-sensitive component in Xenopus sperm which may be responsible for egg-binding (Iwao and Jaffe, 1989). The ‘receptor-mediated’ theory seems to be conclusive in Xenopus because extracellular application of a sperm-mimetic ligand leads to successful egg activation.

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This work was supported by a grant-in-aid for Scientific Research from the Japanese Ministry of Education, Science and Culture to Y.I., by the Stuart F. Wilson Award from the University of Connecticut Health Center to L.A.J., and by NIH Grant HD 14939 to L.A.J.

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Present address: Department of Physiology, University of Connecticut Health Center, Farmington, CT 06032.

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