Zinc protection of fertilized eggs is an ancient feature of sexual reproduction in animals

Abstract

One of the earliest and most prevalent barriers to successful reproduction is polyspermy, or fertilization of an egg by multiple sperm. To prevent these supernumerary fertilizations, eggs have evolved multiple mechanisms. It has recently been proposed that zinc released by mammalian eggs at fertilization may block additional sperm from entering. Here, we demonstrate that eggs from amphibia and teleost fish also release zinc. Using Xenopus laevis as a model, we document that zinc reversibly blocks fertilization. Finally, we demonstrate that extracellular zinc similarly disrupts early embryonic development in eggs from diverse phyla, including Cnidaria, Echinodermata, and Chordata. Our study reveals that a fundamental strategy protecting human eggs from fertilization by multiple sperm may have evolved more than 650 million years ago.

Zinc is a master-regulator of sperm function associated with binding, motility, and metabolic modulation during porcine sperm capacitation

“…Such rapid exocytosis of over 10 billion zinc ions 41 completely inhibits sperm binding to the ZP while sustaining sperm binding to oviductal glycans mimicking oviductal epithelium in an in vitro system 28 . Evolutionary conservation of this so-called oocyte zinc spark 42 corroborates our view that Zn 2+ can reversibly alter sperm motility and the ability to interact with the oviductal epithelial cells and the egg coat. Cytoskeletal proteins such as actin and tubulin were shown to be zinc-scavenging proteins, and Zn 2+ stimulates the assembly of tubulin protofilaments 43 and induces F-actin polymerization 44 .…”

Zn2+is Essential for Ca2+Oscillations in Mouse Eggs

“…Despite accruing Zn 2+ during oocyte maturation, fertilization witnesses a necessary Zn 2+ release into the external milieu, known as “Zn 2+ sparks” (Converse and Thomas, 2020; Kim et al, 2011; Mendoza et al, 2022; Que et al, 2019, 2015; Seeler et al, 2021). This release of Zn 2+ is a conserved event in fertilization across species and is associated with several biological functions, including those related to fending off polyspermy (Kim et al, 2011; Que et al, 2019; Wozniak et al, 2020). The concomitant decrease in Zn 2+ facilitates the resumption of the cell cycle and exit from the MII stage (Kim et al, 2011).…”

“…Remarkably, after fertilization, Zn 2+ levels need to decrease, as Emi2 is a Zn 2+ -associated molecule, and high Zn 2 levels prevent MII exit (Bernhardt et al, 2012; Shoji et al, 2014; Suzuki et al, 2010b). Following the initiation of Ca 2+ oscillations, approximately 10 to 20% of the Zn 2+ accrued during maturation is ejected during the Zn 2+ sparks, a conserved event in vertebrates and invertebrate species (Converse and Thomas, 2020; Kim et al, 2011; Mendoza et al, 2022; Que et al, 2019; Seeler et al, 2021; Tokuhiro and Dean, 2018; Wozniak et al, 2020; Zhang et al, 2016). The use of Zn 2+ chelators such as N,N,N,N-tetrakis (2-pyridinylmethyl)-1,2-ethylenediamine (TPEN) to create Zn 2+ -deficient conditions buttressed the importance of Zn 2+ during meiotic transitions (Kim et al, 2010; Suzuki et al, 2010b).…”

Zn2+ is Essential for Ca2+ Oscillations in Mouse Eggs

“…Despite accruing Zn 2+ during oocyte maturation, fertilization witnesses a necessary Zn 2+ release into the external milieu, known as "Zn 2+ sparks" (Kim et al, 2011;Que et al, 2019Que et al, , 2015. This release of Zn 2+ is a conserved event in fertilization across species and is associated with several biological functions, including those related to fending off polyspermy (Kim et al, 2011;Que et al, 2019;Wozniak et al, 2020). The concomitant decrease in Zn 2+ facilitates the resumption of the cell cycle and exit from the MII stage (Kim et al, 2011).…”