The C-terminal region of OVGP1 remodels the zona pellucida and modifies fertility parameters

Algarra, Blanca; Han, Ling; Soriano‐Úbeda, Cristina; Avilés, Manuel; Coy, Pilar; Jovine, Luca; Jiménez-Movilla, María

doi:10.1038/srep32556

Cited by 32 publications

(48 citation statements)

References 40 publications

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“…For example, prefertilization association of oviduct specific glycoprotein (OVGP1)/oviductin with the ZP was shown to modify its resistance to proteolysis and modulate its sperm‐binding activity, thus controlling polyspermy. Consistent with the observation that different homologues of OVGP1 have variable effects on fertilization, the C‐terminal region of OVGP1 differs among species and regulates the extent to which the protein can penetrate the ZP, in addition to being required for OVGP1 endocytosis into the egg (Algarra et al, 2016; Coy et al, 2008).…”

Section: Other Factors Associated With Zp Hardeningmentioning

confidence: 53%

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: Other Factors Associated With Zp Hardeningmentioning

confidence: 53%

Mammalian egg coat modifications and the block to polyspermy

Fahrenkamp

Algarra

Jovine

2020

Molecular Reproduction Devel

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“…Edn2 directly induces vascular endothelial growth factor in granulosa cells of the bovine ovary [35] and ovulation and CL formation are signi cantly impaired in Edn2-knockout mice [34]. Oviduct-speci c glycoprotein (OVGP1), also known as oviductin, is the major non-serum glycoprotein in the oviduct uid during fertilization and increases the number of fertilized eggs and promotes early embryonic development [36]. Furthermore, Edn2 and OVGP1 are primarily localized in the ovaries after N-eCG administration.…”

Section: Discussionmentioning

confidence: 99%

Comparative gene expression profiling of mouse ovaries upon stimulation with natural equine chorionic gonadotropin (N-eCG) and tethered recombinant-eCG (R-eCG)

Min

Park

Lee

et al. 2020

Preprint

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Background: Equine chorionic gonadotropin (eCG) induces super-ovulation in laboratory animals. Notwithstanding its extensive usage, limited information is available regarding the differences between the in vivo effects of natural eCG (N-eCG) and recombinant eCG (R-eCG). This study aimed to investigate the gene expression profiles of mouse ovaries upon stimulation with N-eCG and R-eCG produced from CHO-suspension (CHO-S) cells. R-eCG gene was constructed and transfected into CHO-S cells and quantified. Subsequently, we determined the metabolic clearance rate (MCR) of N-eCG and R-eCG up to 24 h after intravenous administration through the mice tail vein and identified differentially expressed genes in both ovarian tissues, via quantitative real-time PCR (qRT-PCR) and immunohistochemistry (IHC). Results: R-eCG was markedly expressed initially after transfection and maintained until recovery on day 9. Glycan chains were substantially modified in R-eCG protein produced from CHO-S cells and eliminated through PNGase F treatment. The MCR was slightly lower for R-eCG than for N-eCG, and no significant difference was observed after 60 min. Notwithstanding their low concentrations, R-eCG and N-eCG were detected in the blood at 24h post-injection. Microarray analysis of ovarian tissue revealed that 20 of 12,816 genes assessed therein were significantly up-regulated and 43 genes were down-regulated by >2-fold in the group that received R-eCG (63 [0.49%] differentially regulated genes in total). The microarray results were concurrent with and hence validated by those of RT-PCR, qRT-PCR, and IHC analyses. Conclusions: The present results indicate that R-eCG can be adequately produced through a cell-based expression system through post-translational modification of eCG and can induce ovulation in vivo. These results provide novel insights into the molecular mechanisms underlying the up- or down-regulation of specific ovarian genes and the production of R-eCG with enhanced biological activity in vivo.

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“…Their expression changes with stages of the oestrous cycle (Lamy et al 2016; Soleilhavoup et al 2016), presence of gametes (Georgiou et al 2005), or presence of embryos (Smits et al 2017). Some of these proteins are involved in crucial steps for fertilization, such as binding between sperm and oviduct (Ignotz et al 2007; Teijeiro et al 2011), zona pellucida–sperm interaction (Algarra et al 2016; Coy et al 2012a; Goncalves et al 2008a; Hao et al 2006; Lachance et al 2007; Mondejar et al 2013; Zumoffen et al 2013), sperm viability (Elliott et al 2009; Lloyd et al 2009; Moein-Vaziri et al 2014), acrosome reaction (Chiu et al 2010; Zhang et al 2006), dispersion of cumulus cells (Griffiths et al 2008), and sperm selection (Hanaue et al 2011). The present work suggests that the high diversity of proteins present in the OF of mammals is associated with a species-specific evolutionary pattern of the corresponding genes by fairly frequent pseudogenization.…”

Section: Discussionmentioning

confidence: 99%

“…For instance, annexins and DMBT1 participate in the binding between the sperm and the oviduct (Ignotz et al 2007; Teijeiro et al 2011). Progestagen-associated endometrial protein (PAEP) also known as glycodelin (Gd), lactotransferrin (LTF), heat shock 70 kDa protein 5 (HSPA5), OVGP1, prostaglandin D2 synthase (PTGDS), plasminogen (PLG), and SPP1 participate in the zona pellucida–sperm interaction controlling polyspermy (Algarra et al 2016; Chiu et al 2007; Coy et al 2008, 2012b; Goncalves et al 2008a; Hao et al 2006; Lachance et al 2007; Marin-Briggiler et al 2010; Mondejar et al 2013; Zumoffen et al 2013). Heat shock 70 kDa protein 8 (HSPA8) has a beneficial effect on sperm viability (Elliott et al 2009; Lloyd et al 2009; Moein-Vaziri et al 2014).…”

Section: Introductionmentioning

confidence: 99%

Genes Encoding Mammalian Oviductal Proteins Involved in Fertilization are Subjected to Gene Death and Positive Selection

Moros-Nicolás¹,

Fouchécourt²,

Goudet³

et al. 2018

J Mol Evol

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Oviductal proteins play an important role in mammalian fertilization, as proteins from seminal fluid. However, in contrast with the latter, their phylogenetic evolution has been poorly studied. Our objective was to study in 16 mammals the evolution of 16 genes that encode oviductal proteins involved in at least one of the following steps: (1) sperm–oviduct interaction, (2) acrosome reaction, and/or (3) sperm–zona pellucida interaction. Most genes were present in all studied mammals. However, some genes were lost along the evolution of mammals and found as pseudogenes: annexin A5 (ANXA5) and deleted in malignant brain tumor 1 (DMBT1) in tarsier; oviductin (OVGP1) in megabat; and probably progestagen-associated endometrial protein (PAEP) in tarsier, mouse, rat, rabbit, dolphin, and megabat; prostaglandin D2 synthase (PTGDS) in microbat; and plasminogen (PLG) in megabat. Four genes [ANXA1, ANXA4, ANXA5, and heat shock 70 kDa protein 5 (HSPA5)] showed branch-site positive selection, whereas for seven genes [ANXA2, lactotransferrin (LTF), OVGP1, PLG, S100 calcium-binding protein A11 (S100A11), Sperm adhesion molecule 1 (SPAM1), and osteopontin (SPP1)] branch-site model and model-site positive selection were observed. These results strongly suggest that genes encoding oviductal proteins that are known to be important for gamete fertilization are subjected to positive selection during evolution, as numerous genes encoding proteins from mammalian seminal fluid. This suggests that such a rapid evolution may have as a consequence that two isolated populations become separate species more rapidly.

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The C-terminal region of OVGP1 remodels the zona pellucida and modifies fertility parameters

Cited by 32 publications

References 40 publications

Mammalian egg coat modifications and the block to polyspermy

Mammalian egg coat modifications and the block to polyspermy

Comparative gene expression profiling of mouse ovaries upon stimulation with natural equine chorionic gonadotropin (N-eCG) and tethered recombinant-eCG (R-eCG)

Genes Encoding Mammalian Oviductal Proteins Involved in Fertilization are Subjected to Gene Death and Positive Selection

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