ECB-ART-49709
PLoS Biol
2020 Jul 01;187:e3000811. doi: 10.1371/journal.pbio.3000811.
Show Gene links
Show Anatomy links
Zinc protection of fertilized eggs is an ancient feature of sexual reproduction in animals.
Wozniak KL
,
Bainbridge RE
,
Summerville DW
,
Tembo M
,
Phelps WA
,
Sauer ML
,
Wisner BW
,
Czekalski ME
,
Pasumarthy S
,
Hanson ML
,
Linderman MB
,
Luu CH
,
Boehm ME
,
Sanders SM
,
Buckley KM
,
Bain DJ
,
Nicotra ML
,
Lee MT
,
Carlson AE
.
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.
PubMed ID: 32735558
PMC ID: PMC7423145
Article link: PLoS Biol
Grant support: [+]
Article Images: [+] show captions
References [+] :
Bernhardt,
A zinc-dependent mechanism regulates meiotic progression in mammalian oocytes.
2012, Pubmed
Bernhardt, A zinc-dependent mechanism regulates meiotic progression in mammalian oocytes. 2012, Pubmed
Bianchi, Juno is the egg Izumo receptor and is essential for mammalian fertilization. 2014, Pubmed
Bonnell, Egg jelly layers of Xenopus laevis are unique in ultrastructure and sugar distribution. 1996, Pubmed
Burkart, Ovastacin, a cortical granule protease, cleaves ZP2 in the zona pellucida to prevent polyspermy. 2012, Pubmed
Burnett, Xenopus tropicalis allurin: expression, purification, and characterization of a sperm chemoattractant that exhibits cross-species activity. 2008, Pubmed
Busa, An elevated free cytosolic Ca2+ wave follows fertilization in eggs of the frog, Xenopus laevis. 1985, Pubmed
Carlson, Identical phenotypes of CatSper1 and CatSper2 null sperm. 2005, Pubmed
Claw, Evolution of the egg: new findings and challenges. 2012, Pubmed
Duncan, The zinc spark is an inorganic signature of human egg activation. 2016, Pubmed
Elinson, Site of sperm entry and a cortical contraction associated with egg activation in the frog Rana pipiens. 1975, Pubmed
Feng, Evolution and multiple origins of zona pellucida genes in vertebrates. 2018, Pubmed
Guerardel, O-glycan variability of egg-jelly mucins from Xenopus laevis: characterization of four phenotypes that differ by the terminal glycosylation of their mucins. 2000, Pubmed
Heasman, Fertilization of cultured Xenopus oocytes and use in studies of maternally inherited molecules. 1991, Pubmed
Jaffe, Studies of the voltage-dependent polyspermy block using cross-species fertilization of amphibians. 1983, Pubmed
Jaffe, Fast block to polyspermy in sea urchin eggs is electrically mediated. 1976, Pubmed , Echinobase
Kim, Zinc sparks are triggered by fertilization and facilitate cell cycle resumption in mammalian eggs. 2011, Pubmed
Kong, The inorganic anatomy of the mammalian preimplantation embryo and the requirement of zinc during the first mitotic divisions. 2015, Pubmed
Kroeger, Production of haploid zebrafish embryos by in vitro fertilization. 2014, Pubmed
Kubo, Immunohistochemical localisation of gp69/64 molecules in Xenopus egg envelopes in relation to their sperm binding activity. 2002, Pubmed
Lee, A wave of free cytosolic calcium traverses zebrafish eggs on activation. 1999, Pubmed
Marszałek, Revised stability constant, spectroscopic properties and binding mode of Zn(II) to FluoZin-3, the most common zinc probe in life sciences. 2016, Pubmed
Medina, Role of cations as components of jelly coats in Bufo arenarum fertilization. 2010, Pubmed
Mir, How the mother can help: studying maternal Wnt signaling by anti-sense-mediated depletion of maternal mRNAs and the host transfer technique. 2008, Pubmed
Nomizu, Zinc, iron, and copper contents of Xenopus laevis oocytes and embryos. 1993, Pubmed
Que, Bovine eggs release zinc in response to parthenogenetic and sperm-induced egg activation. 2019, Pubmed
Que, Quantitative mapping of zinc fluxes in the mammalian egg reveals the origin of fertilization-induced zinc sparks. 2015, Pubmed
Que, Zinc sparks induce physiochemical changes in the egg zona pellucida that prevent polyspermy. 2017, Pubmed
Runft, Egg activation at fertilization: where it all begins. 2002, Pubmed
Sanders, CRISPR/Cas9-mediated gene knockin in the hydroid Hydractinia symbiolongicarpus. 2018, Pubmed
Sato, Polyspermy-preventing mechanisms in mouse eggs fertilized in vitro. 1979, Pubmed
Schneider, NIH Image to ImageJ: 25 years of image analysis. 2012, Pubmed
Shen, Sources of calcium in sea urchin eggs during the fertilization response. 1993, Pubmed , Echinobase
Shumaker, TPEN, a Zn2+/Fe2+ chelator with low affinity for Ca2+, inhibits lamin assembly, destabilizes nuclear architecture and may independently protect nuclei from apoptosis in vitro. 1998, Pubmed
Snow, Fertilization stimulates an increase in inositol trisphosphate and inositol lipid levels in Xenopus eggs. 1996, Pubmed
Stewart-Savage, A cell surface block to polyspermy occurs in golden hamster eggs. 1988, Pubmed
Sun, Zinc regulates the ability of Cdc25C to activate MPF/cdk1. 2007, Pubmed
Suzuki, Full-term mouse development by abolishing Zn2+-dependent metaphase II arrest without Ca2+ release. 2010, Pubmed
Tholl, Swimming of Xenopus laevis sperm exhibits multiple gears and its duration is extended by egg jelly constituents. 2011, Pubmed
Tokuhiro, Glycan-Independent Gamete Recognition Triggers Egg Zinc Sparks and ZP2 Cleavage to Prevent Polyspermy. 2018, Pubmed
Wallace, Protein incorporation by isolated amphibian oocytes. 3. Optimum incubation conditions. 1973, Pubmed
Webb, Ca(2+) signaling during activation and fertilization in the eggs of teleost fish. 2013, Pubmed
Wong, Defending the zygote: search for the ancestral animal block to polyspermy. 2006, Pubmed
Wozniak, Ion channels and signaling pathways used in the fast polyspermy block. 2020, Pubmed , Echinobase
Wozniak, Extracellular Ca2+ Is Required for Fertilization in the African Clawed Frog, Xenopus laevis. 2017, Pubmed
Wozniak, PLC and IP3-evoked Ca2+ release initiate the fast block to polyspermy in Xenopus laevis eggs. 2018, Pubmed
Xiang, Allurin, a 21 kD sperm chemoattractant, is rapidly released from the outermost jelly layer of the Xenopus egg by diffusion and medium convection. 2005, Pubmed