Ion channels and signaling pathways used in the fast polyspermy block

Abstract

Fertilization of an egg by multiple sperms, polyspermy, is lethal to most sexually reproducing species. To combat the entry of additional sperm into already fertilized eggs, organisms have developed various polyspermy blocks. One such barrier, the fast polyspermy block, uses a fertilization‐activated depolarization of the egg membrane to electrically inhibit supernumerary sperm from entering the egg. The fast block is commonly used by eggs of oviparous animals with external fertilization. In this review, we discuss the history of the fast block discovery, as well as general features shared by all organisms that use this polyspermy block. Given the diversity of habitats of external fertilizers, the fine details of the fast block‐signaling pathways differ drastically between species, including the identity of the depolarizing ions. We highlight the known molecular mediators of these signaling pathways in amphibians and echinoderms, with a fine focus on ion channels that signal these fertilization‐evoked depolarizations. We also discuss the investigation for a fast polyspermy block in mammals and teleost fish, and we outline potential fast block triggers. Since the first electrical recordings made on eggs in the 1950s, the fields of developmental biology and electrophysiology have substantially matured, and yet we are only now beginning to discern the intricate molecular mechanisms regulating the fast block to polyspermy.

Cellular and molecular aspects of oocyte maturation and fertilization: a perspective from the actin cytoskeleton

“…As for the significance of this earliest electrical event at fertilization, L.A. Jaffe [35] suggested that the activation potential going positive values was responsible for the establishment of a fast block to polyspermy. While such rapid polyspermy-preventing mechanism has been suggested to act in diverse organisms [121,122], other authors have ruled out the possibility that the fast electrical block ensures monospermy in sea urchin eggs [123,124]. In line with this, and at variance with the prevailing view that emphasises the depolarization of the egg plasma membrane as the fast mechanism to prevent polyspermy, our laboratory has recently provided evidence that sea urchin eggs remain mostly monospermic, instead of exhibiting the expected polyspermy, when fertilized at conditions that lower the fertilization potential, i.e., artificial seawater with reduced amount of Na + [125][126][127].…”

Perfect date—the review of current research into molecular bases of mammalian fertilization

“…Although commonly referred to as an evolutionarily conserved safeguard response, the contribution of an electrically mediated membrane block is virtually unfounded in mammals, including humans. It is likely that here, the fast membrane depolarization is less important than in invertebrates and amphibians because the female reproductive tract limits arrival of the sperm to the fertilization site and the sperm-to-egg ratio is thus much lower than during external fertilization [116,117]. Besides, the membrane potential overshot is only transient, lasting up to several minutes.…”

Preventing polyspermy in mammalian eggs—Contributions of the membrane block and other mechanisms

“…However, humans and other mammals do not appear to have precisely same blocks to polyspermy noted in this cartoon and commonly referenced in developmental biology textbooks—the fast block and the slow block . This classic terminology is based on discoveries that started in echinoderms with the work of Ernest Just and extended to a range of other water‐dwelling species with external fertilization (also addressed in Wozniak & Carlson, 2019). Summarized briefly, the fast block to polyspermy in these species involves a rapid and transient depolarization of the egg membrane, dubbed the fertilization potential (see Wozniak & Carlson, 2019 for more details).…”

“…This classic terminology is based on discoveries that started in echinoderms with the work of Ernest Just and extended to a range of other water‐dwelling species with external fertilization (also addressed in Wozniak & Carlson, 2019). Summarized briefly, the fast block to polyspermy in these species involves a rapid and transient depolarization of the egg membrane, dubbed the fertilization potential (see Wozniak & Carlson, 2019 for more details). This depolarization occurs very quickly, initiated within fractions of a second after sperm entry into the egg cytoplasm.…”