Abstract
While alkaloids often exert unique pharmacological effects on animal cells, exposure of sea urchin eggs to nicotine causes polyspermy at fertilization in a dose-dependent manner. Here, we studied molecular mechanisms underlying the phenomenon. Although nicotine is an agonist of ionotropic acetylcholine receptors, we found that nicotine-induced polyspermy was neither mimicked by acetylcholine and carbachol nor inhibited by specific antagonists of nicotinic acetylcholine receptors. Unlike acetylcholine and carbachol, nicotine uniquely induced drastic rearrangement of egg cortical microfilaments in a dose-dependent way. Such cytoskeletal changes appeared to render the eggs more receptive to sperm, as judged by the significant alleviation of polyspermy by latrunculin-A and mycalolide-B. In addition, our fluorimetric assay provided the first evidence that nicotine directly accelerates polymerization kinetics of G-actin and attenuates depolymerization of preassembled F-actin. Furthermore, nicotine inhibited cofilin-induced disassembly of F-actin. Unexpectedly, our results suggest that effects of nicotine can also be mediated in some non-cholinergic pathways.
Highlights
The general scheme of sexual reproduction in animals is the union of male and female haploid gametes to produce a diploid zygote that develops into a new organism
For quantitative assessment of nicotine’s effect on polyspermy, sea urchin eggs were treated with increasing concentrations of nicotine (0−20 mM) prior to fertilization for 5 min
When the number of egg-incorporated sperm and the elevation of the fertilization envelope (FE) were examined 10 min after insemination (Figure 1), it was evident that both FE elevation and the egg-incorporated sperm counts were affected by nicotine pretreatment in a dose-dependent manner
Summary
The general scheme of sexual reproduction in animals is the union of male and female haploid gametes to produce a diploid zygote that develops into a new organism. In some species undergoing internal fertilization (e.g., arachnids, insects, urodeles, reptiles, and birds), multiple sperm may commonly enter the egg, but only one male pronucleus is eventually selected to fuse with the female pronucleus, in order to effect monospermy [4,5,6]. In the vast majority of species, incidental polyspermy has deleterious effects on the zygotes and leads to abortive development ( referred to as ‘pathological polyspermy’), but their eggs appear to have some preventive mechanisms to avoid polyspermy [7,8,9]
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