Contribution of mouse egg zona pellucida glycoproteins to gamete recognition during fertilization

Wassarman, Paul M.

doi:10.1002/jcp.20389

Cited by 56 publications

(35 citation statements)

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“…The mouse ZP consists of 3 glycoproteins, however, only purified mZP3 from unfertilized eggs inhibits binding of mouse sperm to eggs at nanomolar concentrations (Bleil and Wassarman, 1980;Wassarman, 2005) and induces sperm to undergo the acrosome reaction (Bleil and Wassarman, 1983;Arnoult et al, 1996). Purified mZP1 and mZP2 have no effect on sperm binding or the acrosome reaction.…”

Section: Relevant Observations and Implicationsmentioning

confidence: 99%

“…It is of interest that ZP3 is among the 10% most divergent proteins in mammals, that the region of polypeptide encoded by mZP3 exon-7 has undergone a significant number of changes during evolution compared to other regions, and that exon-7 is a site of positive Darwinian selection (Swanson et al, 2001). These features may be related to the proposed role of ZP3 in species-restricted fertilization (Wassarman, 1990(Wassarman, , 1999(Wassarman, , 2005. mZP1-3 null mutant mice have been produced by homologous recombination in embryonic stem cells.…”

Section: Relevant Observations and Implicationsmentioning

confidence: 99%

“…A large body of evidence strongly suggests that capacitated mouse sperm recognize and bind to mZP3 during fertilization and, as a result, undergo the acrosome reaction, a form of cellular exocytosis that enables sperm to penetrate the ZP (Yanagimachi, 1994;Wassarman, 1999Wassarman, , 2005Wassarman et al, 2001;Florman and Ducibella, 2006;Wassarman and Litscher, 2008) (Fig. 2).…”

Section: Mammalian Fertilization and The Zona Pellucidamentioning

confidence: 99%

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Zona pellucida glycoprotein ZP3 and fertilization in mammals

Litscher

Williams

Wassarman

2009

Molecular Reproduction Devel

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SUMMARYAn early step in mammalian fertilization is species-restricted binding of sperm to the egg's zona pellucida (ZP), a thick extracellular coat that surrounds eggs. Sperm bind to the ZP of unfertilized eggs, but not to the ZP of fertilized eggs. Shortly after binding to the unfertilized egg ZP, sperm undergo the acrosome reaction, a form of cellular exocytosis that enables sperm to penetrate the ZP. Three glycoproteins, mZP1-3, constitute the mouse egg's ZP and participate in the process of fertilization. For example, sperm exposed to unfertilized egg mZP3 at nanomolar concentrations are inhibited from binding to eggs and undergo the acrosome reaction. Neither mZP1 nor mZP2 has an effect on sperm binding or the acrosome reaction. Furthermore, mZP3 from fertilized eggs has no effect on sperm binding and is unable to induce the acrosome reaction. These and other properties of mZP3 suggest that it is a receptor for sperm and inducer of the acrosome reaction. Mapping of the mZP3 combining-site for sperm suggests that it is located near the C-terminus of the polypeptide, just downstream of the ZP domain, in a region encoded by exon-7 of the mZP3 gene. This region of mZP3 is a site of positive Darwinian selection. When mZP3 exon-7 is fused to the Fc fragment of human IgG and sperm exposed to the chimeric protein, sperm are inhibited from binding to eggs. However, the chimeric protein does not induce the acrosome reaction. Therefore, polypeptide encoded by mZP3 exon-7 is necessary and sufficient for binding of mouse sperm.

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Section: Relevant Observations and Implicationsmentioning

confidence: 99%

Section: Relevant Observations and Implicationsmentioning

confidence: 99%

Section: Mammalian Fertilization and The Zona Pellucidamentioning

confidence: 99%

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Zona pellucida glycoprotein ZP3 and fertilization in mammals

Litscher

Williams

Wassarman

2009

Molecular Reproduction Devel

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“…It contains ligands for sperm binding and signaling molecules that affect acrosomal exocytosis (Dean, 2007, Wassarman, 2005. In addition, assays in vitro have implicated some of the carbohydrate residues in mediating sperm-zona interactions in mice (Bleil and Wassarman, 1988, Florman and Wassarman, 1985, Miller et al, 1992 although recent studies with genetically manipulated mice call into question the roles of terminal galactose or N-acetylglucosamine residues on the zona pellucida glycans (Williams et al, 2007).…”

Section: Role Of Zp In Acrosome Interactionsmentioning

confidence: 99%

The role of the acrosomal matrix in fertilization

Buffone

Foster²,

Gerton³

2008

Int. J. Dev. Biol.

112

107

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Mammalian sperm must have properly formed acrosomes to be fully functional in the process of binding and penetrating the zona pellucida (ZP), the extracellular matrix surrounding the egg. There is much evidence to raise doubts about the old "bag of enzymes" paradigm of acrosomal function, although this is the model that seems to prevail. We concur with other scientists that acrosomal exocytosis is not an all or none event where the acrosome is either "intact" or "reacted". As determined by transmission electron microscopy of human sperm undergoing acrosomal exocytosis, six stages can be identified, with the intermediate ones involving loss of acrosomal matrix material. In the mouse, there is a temporal relationship among four stages of acrosomal exocytosis. Numerous evidences suggest a more complex role for the acrosome in fertilization in which the acrosomal matrix is a scaffold for sperm-ZP interactions that self-regulates by a controlled disassembly mechanism.

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“…The adhesion of sperm to the oviductal epithelium establishing the sperm reservoir in the caudal portion of the isthmus has been shown for several mammalian species to involve carbohydrates (reviewed by Suarez, 2002. The initial binding and recognition process (primary binding) between both gametes, which starts the fertilization cascade as well as the transient binding of the acrosome-reacted sperm to the zona pellucida (secondary binding), which is an essential step in the penetration process operate by utilizing the information potential of carbohydrates (Töpfer-Petersen, 1999;Wassarman 2005;Wassarman et al, 2005).…”

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confidence: 99%

Glycobiology of fertilization in the pig

Töpfer‐Petersen¹,

Ekhlasi-Hundrieser²,

Tsolova³

2008

Int. J. Dev. Biol.

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By adopting internal fertilization, the meeting of both gametes -the sperm and the egg -and thus the highly coordinated sequence of interactions leading to fertilization, occur in the female reproductive tract. In mammals, the oviduct has been shown to translate the requirements of the female, coordinating sperm activation (capacitation) and sperm transport with the arrival of the ovulated egg. A hierarchy of carbohydrate-based interactions accompanies these events ranging from the binding of uncapacitated sperm to the oviductal epithelium (establishment of the female sperm reservoir), to the primary and secondary binding processes contributing to gamete recognition and sperm penetration of the oocyte zona pellucida. The current perspective will focus on the carbohydrate-recognition systems in the binding events during fertilization in the pig. The roles of the major carbohydrate-binding proteins, the spermadhesins and the acrosomal serine proteinase, pro/acrosin are discussed under consideration of recent structural data. The glycans and the glycoproteins of the porcine oviduct with a focus on the candidate sperm receptors as well as the zona pellucida N-glycans of prepuberal pigs have been characterized by a mass spectrometric approach. Furthermore, some preliminary data supporting the hypothesis that the zona pellucida has to undergo a maturation process during oocyte development are presented. KEY WORDS: gamete interaction, spermadhesin, acrosin, zona pellucida, glycoprotein, glycan A short review of mammalian fertilizationThe fertilization of an egg by a sperm is the fundamental event in life, as it culminates in the creation of a new individual. In mammals, the meeting of the fertilizing competent sperm and the ovulated egg is the beginning of a highly coordinated sequence of cellular interactions between the haploid gametes, which leads to the formation of the diploid zygote and initiates embryonic development.The first contact between sperm and egg takes place at the outer surface of the surrounding extracellular matrix of the egg, the zona pellucida (ZP). By binding to distinct oligosaccharides of the ZP glycoproteins, the fertilizing sperm recognizes the egg. Upon anchoring the sperm to the egg through the ZP carbohydrates the signaling cascade leading to acrosomal exocytosis of the sperm is activated allowing the sperm to pass through the zona pellucida. The acrosome-reacted sperm in the end interacts and fuses with the egg plasma membrane, which in turn enables the egg to complete meiosis, to initiate the mechanisms to prevent Int.

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Contribution of mouse egg zona pellucida glycoproteins to gamete recognition during fertilization

Cited by 56 publications

References 35 publications

Zona pellucida glycoprotein ZP3 and fertilization in mammals

Zona pellucida glycoprotein ZP3 and fertilization in mammals

The role of the acrosomal matrix in fertilization

Glycobiology of fertilization in the pig

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