Reassessing the role of protein-carbohydrate complementarity during sperm-egg interactions in the mouse

Shur, Barry D.

doi:10.1387/ijdb.082571bs

Cited by 18 publications

(22 citation statements)

References 102 publications

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“…If spermatozoa of the mouse do indeed finally bind to the zona rather by way of the IAM, this has wider implications. It may explain the difficulty in using fertilization as the end point in this model species to identify an essential receptor on the sperm plasmalemma (see Shur (2008)) or among candidates (e.g. proacrosin, zonadhesin, P56 and arylsulfatase A) in the acrosomal matrix (see Tardif et al (2010) and Avelia et al (2013)).…”

Section: Zona Bindingmentioning

confidence: 99%

Singular features of fertilization and their impact on the male reproductive system in eutherian mammals

Bedford

2014

Reproduction

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Therian (marsupial and eutherian) mammals have evolved a suite of novel reproductive features -seen variously in their gametes, the steps of fertilization and the male reproductive tract -whose adaptive significance remains unclear. Present evidence for the betterunderstood eutherian mammals suggests that the 'prime mover' in their evolution has been the character of the egg coat, with other such features being adaptations to the consequences of this. Its elastic thickness allows the zona pellucida to stretch to a variable degree and yet remain around the blastocyst during much or all of its expansion before implantation, but its character represents an unusual challenge for spermatozoa. Novel aspects of the acrosome related to this challenge enable it to maintain a relatively prolonged binding after the onset of the acrosome reaction, and the structure, shape and behaviour of the sperm head point to physical thrust as a major element of zona penetration -with the unique configuration of gamete fusion as a sequela of this strategy. In the male, such adaptations are reflected in sperm head formation in the testis and in sperm maturation in the epididymis involving at least the sperm head's structure, plasmalemma and acrosome. This complexity allied to a slow epididymal sperm transport, a relatively modest sperm production and the brief life span of mature spermatozoa kept above the cauda epididymidis could account for the evolution of the sperm storage function -a development seemingly linked, in turn, to the need for sperm capacitation and scrotal evolution.Reproduction (2014) 147 R43-R52

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Section: Zona Bindingmentioning

confidence: 99%

Singular features of fertilization and their impact on the male reproductive system in eutherian mammals

Bedford

2014

Reproduction

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“…Moreover, ZP3 can stimulate the acrosome reaction on sperm in vitro [37,38], although recent data suggest that cumulus cells might be mainly responsible for inducing this process in vivo [39]. Nevertheless, significant disagreement remains over the precise functions of ZP3 and ZP2 [40,41], and whether sperm binding to ZP3 is mainly dependent on carbohydrates, the polypeptide, or requires both is unclear [1,41,42]. Structural biology could potentially contribute to the solution of this problem, but its application to egg coat subunits-as well as to ZP domain proteins in general-has been hindered by the difficulty of overproducing these molecules in properly folded form at the milligram scale, their very heavy and heterogeneous glycosylation, and their tendency to aggregate at high concentrations.…”

Section: Introductionmentioning

confidence: 99%

A Structural View of Egg Coat Architecture and Function in Fertilization1

Monné¹,

Jovine²

2011

Biology of Reproduction

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Species-restricted interaction between gametes at the beginning of fertilization is mediated by the extracellular coat of the egg, a matrix of cross-linked glycoprotein filaments called the zona pellucida (ZP) in mammals and the vitelline envelope in nonmammals. All egg coat subunits contain a conserved protein-protein interaction module-the "ZP domain"-that allows them to polymerize upon dissociation of a C-terminal propeptide containing an external hydrophobic patch (EHP). Recently, the first crystal structures of a ZP domain protein, sperm receptor ZP subunit zona pellucida glycoprotein 3 (ZP3), have been reported, giving a glimpse of the structural organization of the ZP at the atomic level and the molecular basis of gamete recognition in vertebrates. The ZP module is divided in two related immunoglobulin-like domains, ZP-N and ZP-C, that contain characteristic disulfide bond patterns and, in the case of ZP-C, also incorporate the EHP. This segment lies at the interface between the two domains, which are connected by a long loop carrying a conserved O-glycan important for binding to sperm in vitro. The structures explain several apparently contradictory observations by reconciling the variable disulfide bond patterns found in different homologues of ZP3 as well as the multiple ZP3 determinants alternatively involved in gamete interaction. These findings have implications for our understanding of ZP subunit biogenesis; egg coat assembly, architecture, and interaction with sperm; structural rearrangements leading to postfertilization hardening of the ZP and the block to sperm binding; and the evolutionary origin of egg coats.

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“…At the center of the debate is whether sperm binding is carbohydratemediated, in which case sperm are thought to bind specific carbohydrate structures on the ZP, and many studies support this interpretation (Florman and Wassarman, 1985;Miller et al, 1992;Shur, 2008). Alternatively, it has been argued that sperm recognize the overall supramolecular structure of the ZP rather than specific carbohydrate determinants (Hoodbhoy and Dean, 2004).…”

Section: Introductionmentioning

confidence: 99%

“…The sperm-binding activity of ZP3 has been attributed to specific glycan chains because deglycosylated ZP3 does not possess sperm-binding activity (Bleil and Wassarman, 1988;Florman and Wassarman, 1985). A wide range of sperm surface components have been implicated as receptors for the ZP, but only one, -1,4-galactosyltransferase 1 (B4galt1, also known as GalT1), has been shown to selectively bind ZP3 glycans and trigger acrosomal exocytosis (Miller et al, 1992;Shi et al, 2001;Shur, 2008). Evidence consistent with sperm GalT1 functioning as a ZP3 receptor includes: (i) expression of GalT1 on Xenopus oocytes leads to selective ZP3 binding and GalT1-dependent signal transduction; (ii) overexpression of GalT1 on mouse sperm results in increased binding of soluble ZP3; whereas (iii) GalT1-null sperm do not bind ZP3 at significant levels and fail to undergo ZP-induced acrosomal exocytosis (Lu and Shur, 1997;Youakim et al, 1994;Shi et al, 2001).…”

Section: Introductionmentioning

confidence: 99%

Mouse oviduct-specific glycoprotein is an egg-associated ZP3-independent sperm-adhesion ligand

Lyng

Shur

2009

Journal of Cell Science

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Mouse sperm-egg binding requires a multiplicity of receptorligand interactions, including an oviduct-derived, high molecular weight, wheat germ agglutinin (WGA)-binding glycoprotein that associates with the egg coat at ovulation. Herein, we report the purification and identification of this sperm-binding ligand. WGA-binding, high molecular weight glycoproteins isolated from hormonally primed mouse oviduct lysates competitively inhibit sperm-egg binding in vitro. Within this heterogeneous glycoprotein preparation, a distinct 220 kDa protein selectively binds to sperm surfaces, and was identified by sequence analysis as oviduct-specific glycoprotein (OGP). The sperm-binding activity of OGP was confirmed by the loss of sperm-binding following immunodepletion of OGP from oviduct lysates, and by the ability of both immunoprecipitated OGP and natively purified OGP to competitively inhibit spermegg binding. As expected, OGP is expressed by the secretory cells of the fimbriae and infundibulum; however, in contrast to previous reports, OGP is also associated with both the zona pellucida and the perivitelline space of mouse oocytes. Western blot analysis and lectin affinity chromatography demonstrate that whereas the bulk of OGP remains soluble in the ampullar fluid, distinct glycoforms associate with the cumulus matrix, zona pellucida and perivitelline space. The sperm-binding activity of OGP is carbohydrate-dependent and restricted to a relatively minor peanut agglutinin (PNA)-binding glycoform that preferentially associates with the sperm surface, zona pellucida and perivitelline space, relative to other more abundant glycoforms. Finally, pretreatment of two-cell embryos, which do not normally bind sperm, with PNA-binding OGP stimulates sperm binding.

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Reassessing the role of protein-carbohydrate complementarity during sperm-egg interactions in the mouse

Cited by 18 publications

References 102 publications

Singular features of fertilization and their impact on the male reproductive system in eutherian mammals

Singular features of fertilization and their impact on the male reproductive system in eutherian mammals

A Structural View of Egg Coat Architecture and Function in Fertilization1

Mouse oviduct-specific glycoprotein is an egg-associated ZP3-independent sperm-adhesion ligand

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