Induction of Zona Reaction in Golden Hamster Eggs by Cortical Granule Material

Barros, C.; Yanagimachi, Ryuzo

doi:10.1038/233268a0

Cited by 233 publications

(61 citation statements)

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“…Hence, the oviductal-acquired resistance of the ZP seems to be a relatively common event, not species specific, as shown in sheep, rabbit, cow, and pig oviducts (8,31). In mice or hamster, however, the ZP resistance to proteinases is not acquired in the oviduct (10,32), but the postfertilization increased resistance of the ZP to pronase arises from the cortical reaction (3,33,34). Moreover, we have shown that mouse eggs exposed to bOF do not acquire resistance to proteinase and, intriguingly, mouse is an exception for the OGP association with the ZP, despite its evidence in the perivitelline space (21).…”

Section: Discussionmentioning

confidence: 99%

“…The entrance of the spermatozoon into the oocyte's cytoplasm induces the release of cortical granule contents, which modify the vitelline membrane, the zona pellucida (ZP), or both, rendering the oocyte refractory to additional sperm binding and penetration (3) and ending in changes in the mechanical properties and resistance to protease throughout the ZP (4). Yet assuming strong similarities in fertilization mechanisms among rodents and ungulates, observations in ovulated unfertilized porcine and bovine oocytes, showing that ZP resistance to pronase lasts from hours to days (5)(6)(7)(8), contrast with the much shorter resistance (seconds to minutes) exhibited by ZP of mouse or hamster oviductal oocytes before fertilization (9,10).…”

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confidence: 99%

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Oviduct-specific glycoprotein and heparin modulate sperm–zona pellucida interaction during fertilization and contribute to the control of polyspermy

Coy

Cánovas

Mondéjar

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

193

177

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Polyspermy is an important anomaly of fertilization in placental mammals, causing premature death of the embryo. It is especially frequent under in vitro conditions, complicating the successful generation of viable embryos. A block to polyspermy develops as a result of changes after sperm entry (i.e., cortical granule exocytosis). However, additional factors may play an important role in regulating polyspermy by acting on gametes before sperm-oocyte interaction. Most studies have used rodents as models, but ungulates may differ in mechanisms preventing polyspermy. We hypothesize that zona pellucida (ZP) changes during transit of the oocyte along the oviductal ampulla modulate the interaction with spermatozoa, contributing to the regulation of polyspermy. We report here that periovulatory oviductal fluid (OF) from sows and heifers increases (both, con-and heterospecifically) ZP resistance to digestion with pronase (a parameter commonly used to measure the block to polyspermy), changing from digestion times of Ϸ1 min (pig) or 2 min (cattle) to 45 min (pig) or several hours (cattle). Exposure of oocytes to OF increases monospermy after in vitro fertilization in both species, and in pigs, sperm-ZP binding decreases. The resistance of OF-exposed oocytes to pronase was abolished by exposure to heparin-depleted medium; in a medium with heparin it was not altered. Proteomic analysis of the content released in the heparin-depleted medium after removal of OFexposed oocytes allowed the isolation and identification of oviduct-specific glycoprotein. Thus, an oviduct-specific glycoproteinheparin protein complex seems to be responsible for ZP changes in the oviduct before fertilization, affecting sperm binding and contributing to the regulation of polyspermy.sperm-oocyte interaction ͉ oviductal fluid ͉ ZP hardening P olyspermy (the penetration of the egg cytoplasm by more than one spermatozoa) is a pathologic condition in placental mammals, usually causing early death of the embryo (1). Although the prevalence of polyspermy under natural conditions is moderate, in in vitro fertilization (IVF) systems polyspermy remains a major obstacle to successful development of viable embryos in different species, including humans (2). Mechanisms underlying the block to polyspermy in mammals have been partially uncovered and characterized, mainly with use of rodents as animal models and usually related to events occurring after sperm entry into the oocyte.The entrance of the spermatozoon into the oocyte's cytoplasm induces the release of cortical granule contents, which modify the vitelline membrane, the zona pellucida (ZP), or both, rendering the oocyte refractory to additional sperm binding and penetration (3) and ending in changes in the mechanical properties and resistance to protease throughout the ZP (4). Yet assuming strong similarities in fertilization mechanisms among rodents and ungulates, observations in ovulated unfertilized porcine and bovine oocytes, showing that ZP resistance to pronase lasts from hours to days (5-8), contras...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Oviduct-specific glycoprotein and heparin modulate sperm–zona pellucida interaction during fertilization and contribute to the control of polyspermy

Coy

Cánovas

Mondéjar

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

193

177

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“…I also wish to thank Mrs. telline space (Verhage and Fazleabas, 19901, facilitates Frances Anderson for kindly typing the manuscript. either a more svnchronous exocvtosis of the cortical ACKNOWLEDGMENTS is that a glYcoProtein On the Agricultural Research Council (UK), for which grateful granule contents or expedites andaugments physiological responses of the zona substance to cortical granule material (Barros and Yanagimachi, 1971;Gwatkin et al, 1973), leading more efficiently to establishment of a functional block to polyspermy. Irrespective of which of these or indeed other possibilities, such as an influence on the sperm plasmalemma to stabilise and reduce the numbers becoming capacitated simultaneously, ultimately turns out to be correct, interpretation of the egg transplantation studies described earlier in this review may also need to take into account these putative influences of oviduct fluid glycoproteins rather than focussing simply on the number of competent sperm cells available at the site of fertilisation.…”

Section: Insemination Into Oviductsmentioning

confidence: 99%

Oviduct function in pigs, with particular reference to the pathological condition of polyspermy

Hunter

1991

Molecular Reproduction Devel

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Because the exceptionally high incidence of polyspermic fertilisation has been emphasised as a major defect in systems of in vitro fertilisation in pigs, the aetiology of the condition has been analysed in a series of experiments in vivo in the search for a common underlying cause and possible means of mitigation. Whereas the defense mechanism against polyspermy in pig oocytes is classically viewed as a zona reaction, more recent evidence suggests a secondary block at the vitelline surface. Both blocks may be compromised in situations leading to polyspermy, although deleterious influences seem to be expressed principally in an inadequate zona block, as judged by the presence of perivitelline spermatozoa.Postovulatory aging of mammalian oocytes prior to sperm penetration leads to polyspermy, as can be demonstrated in pig eggs. The primary lesion may concern the cortical reaction, owing to a delayed and incomplete exocytosis of the vesicular contents. Eggs ovulated after gonadotrophin treatment during the luteal phase of the cycle show a high incidence of polyspermic penetration (60.6%), as do those shed at estrus in animals treated with progesterone systemically (40%) or by local microinjections in the oviduct wall (32.3%). Whereas progesterone may be modifying interactions of the gametes and responses of the egg organelles in all four above experimental situations, enhanced numbers of spermatozoa ascending a more patent isthmus appear to be the principal cause of polyspermy. Support for this hypothesis comes from isthmus resection with re-anastomosis of remaining portions of the oviduct (32.4% polyspermy), and surgical insemination directly into the oviducts (33.8% polyspermy). Recent experiments draw attention to a role for oviduct epithelial glycoproteins in modulating the extent of polyspermy in vitro. The role of such oviduct macromolecules in gamete interactions in vivo is considered.

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“…1). In rodents, the block to sperm binding can be mimicked by treatment of ovulated eggs with cortical granule exudates (Barros & Yanagimachi 1971) and recent genetic studies indicate that, irrespective of fertilization, it is the cleavage status of ZP2 that determines whether sperm bind to the zona pellucida (Rankin et al 2003). The zona block to penetration has been difficult to study separately from mechanisms that affect sperm binding (i.e.…”

Section: Post-fertilization Block To Polyspermymentioning

confidence: 99%

“…This has led to a model in which the zona pellucida composed, ad minimus, of ZP2 and ZP3 forms a three-dimensional matrix around ovulated eggs to which sperm will bind. Normally, after fertilization the cortical granules exocytose a protease that cleaves ZP2 (Barros & Yanagimachi 1971, Gwatkin et al 1973, Wolf & Hamada 1977. This cleavage modifies the supramolecular structure of the zona matrix rendering it unable to support sperm binding.…”

Section: Supramolecular Modelsmentioning

confidence: 99%

Insights into the molecular basis of sperm–egg recognition in mammals

Hoodbhoy¹,

Dean²

2004

Reproduction

126

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The zona pellucida surrounding the egg and pre-implantation embryo is required for in vivo fertility and early development. Explanatory models of sperm -egg recognition need to take into account the ability of sperm to bind to ovulated eggs, but not to two-cell embryos. For the last two decades, investigators have sought to identify an individual protein or carbohydrate side chain as the 'sperm receptor'. However, recent genetic data in mice are more consistent with the three-dimensional structure of the zona pellucida, rather than a single protein (or carbohydrate), determining sperm binding. The mouse and human zonae pellucidae contain three glycoproteins (ZP1, ZP2, ZP3) and, following fertilization, ZP2 is proteolytically cleaved. The replacement of endogenous mouse proteins with human ZP2, ZP3 or both does not alter taxon specificity of sperm binding or prevent fertility. Surprisingly, human ZP2 is not cleaved following fertilization and intact ZP2 correlates with persistent sperm binding to two-cell embryos. Taken together, these data support a model in which the cleavage status of ZP2 modulates the three-dimensional structure of the zona pellucida and determines whether sperm bind (uncleaved) or do not (cleaved).

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Induction of Zona Reaction in Golden Hamster Eggs by Cortical Granule Material

Cited by 233 publications

References 5 publications

Oviduct-specific glycoprotein and heparin modulate sperm–zona pellucida interaction during fertilization and contribute to the control of polyspermy

Oviduct-specific glycoprotein and heparin modulate sperm–zona pellucida interaction during fertilization and contribute to the control of polyspermy

Oviduct function in pigs, with particular reference to the pathological condition of polyspermy

Insights into the molecular basis of sperm–egg recognition in mammals

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