Oviductal estrogen receptor α signaling prevents protease-mediated embryo death

Winuthayanon, Wipawee; Bernhardt, Miranda L.; Padilla-Banks, Elizabeth; Myers, Page; Edin, Matthew L.; Lih, Fred B.; Hewitt, Sylvia C.; Korach, Kenneth S.; Williams, Carmen J.

doi:10.7554/elife.10453

Cited by 72 publications

(72 citation statements)

References 60 publications

(72 reference statements)

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“…Finally, it is also important to consider how ZP hardening influences further embryo development. It has already been reported that insufficient hardening leads to early embryonic loss (Gahlay et al, 2010; Winuthayanon et al, 2015), but whether there are any consequences of excessive hardening, especially in relation to embryo hatching, remains unclear. By creating a situation that is structurally very different from that of oocytes with an abnormally thicker ZP, a feature that does not appear to impair hatching (Syrkasheva et al, 2017), super‐hardening of the egg coat could potentially have a significant effect on the success rate of assisted reproduction in humans.…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, different knockout mouse models showed that impairment of ZP2 cleavage reduces fertility only partially, indicating that ZP2 processing is not essential to ensure monospermic fertilization and further successful development (Burkart et al, 2012; Gahlay et al, 2010; Rankin et al, 2003; Sachdev et al, 2012). The subfertility of these genetically modified female mice is likely to be caused by precocious ZP hatching and early embryonic loss (Burkart et al, 2012; Floehr, Dietzel, Schmitz, Chappell, & Jahnen‐Dechent, 2017; Winuthayanon et al, 2015) and there is no evidence of abnormal sperm accumulation in the perivitelline space of their oocytes (Gahlay et al, 2010; Rankin et al, 2003; Tokuhiro & Dean, 2018). The latter observation suggests the existence of a ZP2‐independent block to sperm penetration, which appears to depend on ovastacin's enzymatic activity based on the presence of supernumerary sperm in the perivitelline space of ovastacin‐deficient oocytes, as well as oocytes expressing ovastacin with an active‐site mutation (Tokuhiro & Dean, 2018).…”

Section: Cg Exocytosis Modifies the Zp After Fertilizationmentioning

confidence: 99%

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Mammalian egg coat modifications and the block to polyspermy

Fahrenkamp

Algarra

Jovine

2020

Molecular Reproduction Devel

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Fertilization by more than one sperm causes polyploidy, a condition that is generally lethal to the embryo in the majority of animal species. To prevent this occurrence, eggs have developed a series of mechanisms that block polyspermy at the level of the plasma membrane or their extracellular coat. In this review, we first introduce the mammalian egg coat, the zona pellucida (ZP), and summarize what is currently known about its composition, structure, and biological functions. We then describe how this specialized extracellular matrix is modified by the contents of cortical granules (CG), secretory organelles that are exocytosed by the egg after gamete fusion. This process releases proteases, glycosidases, lectins and zinc onto the ZP, resulting in a series of changes in the properties of the egg coat that are collectively referred to as hardening. By drawing parallels with comparable modifications of the vitelline envelope of nonmammalian eggs, we discuss how CG‐dependent modifications of the ZP are thought to contribute to the block to polyspermy. Moreover, we argue for the importance of obtaining more information on the architecture of the ZP, as well as systematically investigating the many facets of ZP hardening.

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Section: Discussionmentioning

confidence: 99%

Section: Cg Exocytosis Modifies the Zp After Fertilizationmentioning

confidence: 99%

Mammalian egg coat modifications and the block to polyspermy

Fahrenkamp

Algarra

Jovine

2020

Molecular Reproduction Devel

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“…Loss of ESR1 in the oviductal epithelial cells in female mice results in excess protease activity and increased expression of antimicrobial peptides such as defensins. These changes, due to a lack of ESR1 in the oviduct, dampen the plasma membrane integrity of the embryos and ultimately cause embryonic death before the 2-cell stage (Winuthayanon et al 2015). The study demonstrated that the epithelial ESR1 is required to suppress innate immune systems (Fig.…”

Section: Figurementioning

confidence: 97%

Oviduct: roles in fertilization and early embryo development

Winuthayanon

2017

Journal of Endocrinology

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202

191

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Animal oviducts and human Fallopian tubes are a part of the female reproductive tract that hosts fertilization and pre-implantation development of the embryo. With an increasing understanding of roles of the oviduct at the cellular and molecular levels, current research signifies the importance of the oviduct on naturally conceived fertilization and pre-implantation embryo development. This review highlights the physiological conditions within the oviduct during fertilization, environmental regulation, oviductal fluid composition and its role in protecting embryos and supplying nutrients. Finally, the review compares different aspects of naturally occurring fertilization and assisted reproductive technology (ART)-achieved fertilization and embryo development, giving insight into potential areas for improvement in this technology.

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“…This elevated protease activity caused premature degradation of the zona pellucida (ZP) and embryo lysis and wild-type embryos transferred into cKO oviduct failed to develop normally unless rescued by concomitant transfer of protease inhibitors. It was concluded that oestrogen-epithelial receptor α is necessary to suppress oviductal protease activity, which is required for a successful fertilization and preimplantation embryo development (Winuthayanon et al 2015). Epithelial cells also play a role in the transport of the oocyte to the site of fertilization; whereas, during early embryo development, they contribute to creating an optimal environment.…”

Section: Epithelial Cellsmentioning

confidence: 99%

Oviductal response to gametes and early embryos in mammals

Maillo¹,

Sánchez‐Calabuig²,

Lopera-Vásquez³

et al. 2016

Reproduction

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The oviduct is a complex and organized thin tubular structure connecting the ovary with the uterus. It is the site of final sperm capacitation, oocyte fertilization and, in most species, the first 3-4 days of early embryo development. The oviductal epithelium is made up of ciliary and secretory cells responsible for the secretion of proteins and other factors which contribute to the formation of the oviductal fluid. Despite significant research, most of the pathways and oviductal factors implicated in the crosstalk between gametes/early embryo and the oviduct remain unknown. Therefore, studying the oviductal environment is crucial to improve our understanding of the regulatory mechanisms controlling fertilization and embryo development. In vitro systems are a valuable tool to study in vivo pathways and mechanisms, particularly those in the oviducts which in livestock species are challenging to access. In studies of gamete and embryo interaction with the reproductive tract, oviductal epithelial cells, oviductal fluid and microvesicles co-cultured with gametes/embryos represent the most appropriate in vitro models to mimic the physiological conditions in vivo.Reproduction (2016) 152 R127-R141

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Oviductal estrogen receptor α signaling prevents protease-mediated embryo death

Cited by 72 publications

References 60 publications

Mammalian egg coat modifications and the block to polyspermy

Mammalian egg coat modifications and the block to polyspermy

Oviduct: roles in fertilization and early embryo development

Oviductal response to gametes and early embryos in mammals

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