Universality and Diversity of a Fast, Electrical Block to Polyspermy During Fertilization in Animals

Iwao, Yasuhiro; Izaki, Kenta

doi:10.1007/978-4-431-56609-0_24

Cited by 8 publications

(18 citation statements)

References 194 publications

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“…Later, it was demonstrated that the abrupt depolarization of the egg membrane's potential following the attachment of the first successful sperm renders the egg refractory to supernumerary fertilization [15]. While the latter hypothesis of fast voltage-dependent block to polyspermy has been widely supported by similar experiments in other animal models [16][17][18][19], controversy remains regarding whether or not the manifested positive-going 'fertilization potential' is the direct cause of the fast block to polyspermy [20][21][22].…”

Section: Introductionmentioning

confidence: 99%

Nicotine Induces Polyspermy in Sea Urchin Eggs through a Non-Cholinergic Pathway Modulating Actin Dynamics

Limatola

Vasilev

Santella

et al. 2019

Cells

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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.

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Section: Introductionmentioning

confidence: 99%

Nicotine Induces Polyspermy in Sea Urchin Eggs through a Non-Cholinergic Pathway Modulating Actin Dynamics

Limatola

Vasilev

Santella

et al. 2019

Cells

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“…Fertilization in anuran amphibians, frogs and toads, which usually lay eggs of less than 2 mm in diameter, is basically monospermic (Iwao, ; Iwao & Izaki, ). However, polyspermy can occasionally occur in some species, such as the Mediterranean painted a frog, Discoglossus pictus (Talevi, ) and the Puerto Rican terrestrial‐breeding frog, Eleutherodactylus coqui (Elinson, ) which lay large eggs of 1.6 and 3.6 mm in diameter, respectively.…”

Section: Physiological Polyspermy In Urodele Amphibiansmentioning

confidence: 99%

“…Interestingly, in the polyspermic B. ovata egg, each fertilizing sperm induces a short‐lived, positive fertilization potential, but fertilization is insensitive to a positive egg‐membrane potential (Goudeau & Goudeau, ), indicating a lack of an electrical polyspermy block. Eggs of many marine invertebrates, such as sea urchins, ensure monospermy by eliciting a positive fertilization potential (Iwao & Izaki, ); the smaller eggs of the ancestor of comb jellies might have exhibited monospermy ensured by the electrical polyspermy block. Physiological polyspermy in the comb jelly seems to be acquired, accompanied by an increase in the size of eggs and yolk content.…”

Section: Examples Of Physiological Polyspermy In Other Taxamentioning

confidence: 99%

“…When the membrane voltage of unfertilized eggs remains higher than 0 mV, fertilization is prevented, whereas maintenance of the membrane voltage at less than −10 mV causes polyspermy (Glahn & Nuccitelli, 2003;Watabe et al, 2019). Thus, monospermy is ensured by the positive fertilization potential operating as a fast electrical block to polyspermy at the egg plasma membrane (Iwao & Izaki, 2018). After the fast polyspermy block, the cortical granules are discharged to form a fertilization envelope, which prevents the approach of sperm at the egg surface for several minutes after fertilization (Grey, Working, & Hedrick, 1976;Hedrick, 2008;Wong & Wessel, 2006), which is referred to as the slow but permanent block to polyspermy.…”

Section: Introductionmentioning

confidence: 99%

“…The union of a male (sperm) nucleus and a female (egg) nucleus, known as syngamy, in the fertilized egg is necessary to mix genetic material derived from both parents and to create a new diploid genome for the next generation. In most animals, only one sperm is incorporated into the egg, which is referred to as monospermy (Figures a and a), and extra sperm is prevented from entering the fertilized egg by several blocks against polyspermy (Iwao & Izaki, ). In monospermic frogs such as the South African clawed frog, Xenopus laevis , and the western clawed frog, Xenopus tropicalis , the membrane potential of unfertilized eggs is negative (~−20 mV), and a positive fertilization potential of 7–27 mV is elicited at sperm entry (Watabe et al, ; Webb & Nuccitelli, ).…”

Section: Introductionmentioning

confidence: 99%

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Physiological polyspermy: Selection of a sperm nucleus for the development of diploid genomes in amphibians

Iwao

Kimoto

Fujimoto

et al. 2019

Molecular Reproduction Devel

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The union between a sperm and an egg nucleus in egg fertilization is necessary to mix genetic materials to create a new diploid genome for the next generation. In most animals, only one sperm is incorporated into the egg (monospermy), but several animals exhibit physiological polyspermy in which several sperms enter the egg during normal fertilization. However, only one sperm nucleus forms the zygote nucleus with the egg nucleus, even in a polyspermic egg. The cellular and molecular mechanisms involved in the selection of sperm nuclei in the egg cytoplasm have been well investigated in urodele amphibians. The principal sperm nucleus develops a larger sperm aster and contacts the egg nucleus to form a zygote nucleus, whereas other accessory sperm nuclei are unable to approach the egg nucleus. The diploid zygote nucleus induces cleavage and participates in embryonic development, whereas the accessory sperm nuclei undergo pyknosis and degenerate. We propose several models to account for the mechanisms of the selection of one sperm nucleus and the degeneration of accessory sperm nuclei. The roles of physiological polyspermy in animal reproduction are discussed by comparison with other polyspermic species.

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Cellular dynamics of double fertilization and early embryogenesis in flowering plants

et al. 2020

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Flowering plants (angiosperms) perform a unique double fertilization in which two sperm cells fuse with two female gamete cells in the embryo sac to develop a seed. Furthermore, during land plant evolution, the mode of sexual reproduction has been modified dramatically from motile sperm in the early-diverging land plants, such as mosses and ferns as well as some gymnosperms (Ginkgo and cycads) to non-motile sperm that are delivered to female gametes by the pollen tube in flowering plants. Recent studies have revealed the cellular dynamics and molecular mechanisms for the complex series of double fertilization processes and elucidated differences and similarities between animals and plants. Here, together with a brief comparison with animals, we review the current understanding of flowering plant zygote dynamics, covering from gamete nuclear migration, karyogamy and polyspermy block, to zygotic genome activation as well as asymmetrical division of the zygote. Further analyses of the detailed molecular and cellular mechanisms of flowering plant fertilization should shed light on the evolution of the unique sexual reproduction of flowering plants.

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Universality and Diversity of a Fast, Electrical Block to Polyspermy During Fertilization in Animals

Cited by 8 publications

References 194 publications

Nicotine Induces Polyspermy in Sea Urchin Eggs through a Non-Cholinergic Pathway Modulating Actin Dynamics

Nicotine Induces Polyspermy in Sea Urchin Eggs through a Non-Cholinergic Pathway Modulating Actin Dynamics

Physiological polyspermy: Selection of a sperm nucleus for the development of diploid genomes in amphibians

Cellular dynamics of double fertilization and early embryogenesis in flowering plants

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