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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.

SUBMITTER: Wozniak KL

PROVIDER: S-EPMC7423145 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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

Wozniak Katherine L KL Bainbridge Rachel E RE Summerville Dominique W DW Tembo Maiwase M Phelps Wesley A WA Sauer Monica L ML Wisner Bennett W BW Czekalski Madelyn E ME Pasumarthy Srikavya S Hanson Meghan L ML Linderman Melania B MB Luu Catherine H CH Boehm Madison E ME Sanders Steven M SM Buckley Katherine M KM Bain Daniel J DJ Nicotra Matthew L ML Lee Miler T MT Carlson Anne E AE

PLoS biology 20200731 7

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 block ...[more]

PMID: 32735558

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Project description:The Ca2+ oscillations initiated by the fertilizing sperm (but terminating concomitant with pronucleus formation) apparently ensure that the events constituting egg activation occur in the correct temporal order; early events (e.g., cortical granule exocytosis) require fewer oscillations than later events (e.g., recruitment of maternal mRNA). Whether the Ca2+ signaling events impact long-term development, in particular development to term, is unknown. Using fertilized eggs that have undergone the first few Ca2+ oscillations, we developed procedures that result either in inhibiting or stimulating the natural pattern of Ca2+ signaling of inseminated eggs. Although the incidence of development to the blastocyst stage is unaltered by these procedures, fewer offspring are born following embryo transfer, indicating that developmental competence of the blastocysts is reduced. Interestingly, embryo transfer experiments reveal that when the natural regime of Ca2+ oscillations is precociously interrupted, the incidence of implantation is compromised whereas hyper-stimulation of Ca2+ signaling events compromises post-implantation development. Moreover, although there was no major difference in the overall growth rates of the offspring, those obtained following hyper-stimulation exhibited a far greater variability in their weight. Analysis of global patterns of gene expression by microarray analysis revealed that approximately 20% of the transcripts are mis-regulated when too few oscillations are experienced by the embryo and EASE analysis indicates that genes preferentially involved in RNA processing and polymerase II transcription are differentially affected. In addition, a set of genes involved in cell adhesion is also mis-expressed and could thus be mechanistically linked to the observed reduced implantation. Only about 3% of the transcripts were mis-regulated following hyper-stimulation, and EASE analysis indicates that genes preferentially involved in metabolism are differentially affected. In toto, these results indicate that a range Ca2+ signaling events following fertilization (an excess or reduction) has long-term effects on both gene expression and development to term. Experiment Overall Design: We profiled the global gene expression in the blastocysts by treatment of Ca2+ oscillations, and identified the genes differentially expressed.

Dataset Information

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

Publications

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

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