The Role of Carbohydrates in the Induction of the Acrosome Reaction in Mouse Spermatozoa1

Loeser, Christoph R.; Tulsiani, D. R. P.

doi:10.1095/biolreprod60.1.94

Cited by 63 publications

(44 citation statements)

References 49 publications

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“…Again, this hypothesis needs to be thoroughly tested (12 Another very significant recent observation involves the induction of the acrosome reaction. Bovine serum albumin (BSA)-based neoglycoproteins terminated at multiple positions with a single monosaccharide (GalNAc-BSA, GlcNAc-BSA, or Man-BSA) induce the acrosome reaction in mice (53). The current study indicates that oligosaccharides with GalNAc, GlcNAc, or Man at the nonreducing ends are also present in the mZP.…”

Section: Discussionmentioning

confidence: 80%

Structural Analysis of Murine Zona Pellucida Glycans

Easton¹,

Patankar²,

Lattanzio³

et al. 2000

Journal of Biological Chemistry

104

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Murine sperm initiate fertilization by binding to specific oligosaccharides linked to the zona pellucida, the specialized matrix coating the egg. Biophysical analyses have revealed the presence of both high mannose and complex-type N-glycans in murine zona pellucida. The predominant high mannose-type glycan had the composition Man 5 GlcNAc 2 , but larger oligosaccharides of this type were also detected. Biantennary, triantennary, and tetraantennary complex-type N-glycans were found to be terminated with the following antennae: Gal␤1-4GlcNAc, NeuAc␣2-3Gal␤1-4GlcNAc, NeuGc␣2-3Gal␤1-4GlcNAc, the Sd a antigen (NeuAc␣2-3[GalNAc␤1-4]Gal-␤1-4GlcNAc, NeuGc␣2-3[GalNAc␤1-4]Gal␤1-4GlcNAc), and terminal GlcNAc. Polylactosamine-type sequence was also detected on a subset of the antennae. Analysis of the O-glycans indicated that the majority were core 2-type (Gal␤1-4GlcNAc␤1-6[Gal␤1-3]GalNAc). The ␤1-6-linked branches attached to these O-glycans were terminated with the same sequences as the N-glycans, except for terminal GlcNAc. Glycans bearing Gal␤1-4GlcNAc␤1-6 branches have previously been suggested to mediate initial murine gamete binding. Oligosaccharides terminated with GalNAc␤1-4Gal have been implicated in the secondary binding interaction that occurs following the acrosome reaction. The significant implications of these observations are discussed.The initial event in the life of all sexually reproducing metazoans is the fertilization of an individual egg by a single sperm. Murine sperm begin this process by binding to the specialized extracellular matrix of the egg known as the mZP 1 (1). This matrix has been shown to be composed of three major glycoproteins (designated mZP1, mZP2, and mZP3) (2). There is strong evidence to suggest that binding occurs via the interaction of mZP3-associated glycans with lectin-like proteins on the sperm surface (3, 4) that in turn induce a signal transduction event known as the acrosome reaction (5). During this reaction, the plasma membrane of the sperm fuses with the outer membrane of a lysosome-like organelle known as the acrosome lying just beneath the surface of the sperm. The resulting membrane complex then blebs off to expose the inner acrosomal membrane. In the mouse model, this inner acrosomal membrane then undergoes secondary binding to mZP2. Sperm move through the mZP and fuse with the egg, thus completing the process of fertilization.Initial studies performed by Wassarman and co-workers (3) indicate that either Pronase glycopeptides (3) or O-linked oligosaccharides (4) obtained from mZP3 block murine sperm-egg binding. Several major models for the initial murine gamete binding interaction have subsequently been proposed that are based upon specific carbohydrate recognition (6 -9). A recent study involving recombinant mZP3 synthesized in murine F9 embryonal carcinoma cells suggests that vicinal presentation of O-linked oligosaccharides within a specific region of mZP3 is necessary for initial sperm-egg binding (10). mZP2 has been proposed to be the glycoprotein that mediates...

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Section: Discussionmentioning

confidence: 80%

Structural Analysis of Murine Zona Pellucida Glycans

Easton¹,

Patankar²,

Lattanzio³

et al. 2000

Journal of Biological Chemistry

104

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“…There is additional confusion in the literature regarding the composition of the zona pellucida and the structure of the biologically active glycosides. In this regard, at least four different monosaccharide residues have been implicated as being critical for initial sperm binding (Amari et al, 2001;Bendahmane et al, 2001;Johnston et al, 1998;Loeser and Tulsiani, 1999). Many of these observations result from the ability of defined glycoconjugates to competitively inhibit sperm-egg binding, but their interpretation is questioned by two findings.…”

Section: Discussionmentioning

confidence: 99%

“…This binding enables GalT I-null sperm to penetrate the zona pellucida matrix, presumably via spontaneous acrosome reactions, and fertilize eggs (although at only 7% the efficiency of wild-type sperm when assayed in vitro). Similarly, well-defined oligosaccharides that are not predicted to be substrates for GalT I competitively inhibit sperm-egg binding (Amari et al, 2001;Bendahmane et al, 2001;Johnston et al, 1998;Loeser and Tulsiani, 1999). Even though these inhibitory oligosaccharides do not appear to be present within the zona pellucida (Aviles et al, 1999;Aviles et al, 2000b), their ability to inhibit binding speaks against a role for GalT I in initial gamete adhesion.…”

Section: Introductionmentioning

confidence: 99%

Characterization of a novel ZP3-independent sperm-binding ligand that facilitates sperm adhesion to the egg coat

Rodeheffer

Shur

2004

Development

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During mammalian fertilization, sperm adhere to the extracellular coat of the egg, or zona pellucida, in a species-specific manner. In mouse, evidence suggests that sperm recognize and bind to specific oligosaccharide ligands within the zona pellucida glycoprotein, ZP3, viaβ1,4-galactosyltransferase I (GalT I), a lectin-like receptor on the sperm surface. Although in vitro experiments using isolated gametes lend support to this model, recent in vivo studies of genetically altered mice question whether ZP3 and/or GalT I are solely responsible for sperm-egg binding. In this regard, sperm from GalT I-null mice bind poorly to ZP3 and fail to undergo a zona-induced acrosome reaction; however, they still bind to the ovulated egg coat in vitro. In this report, we characterize a novel ZP3- and GalT I-independent mechanism for sperm adhesion to the egg coat. Results show that the ovulated zona pellucida contains at least two distinct ligands for sperm binding: a ZP3-independent ligand that is peripherally associated with the egg coat and facilitates gamete adhesion; and a ZP3-dependent ligand that is present in the insoluble zona matrix and is recognized by sperm GalT I to facilitate acrosomal exocytosis. The ZP3-independent ligand is not a result of contamination by egg cortical granules, nor is it the mouse homolog of oviduct-specific glycoprotein. It behaves as a 250 kDa, WGA-reactive glycoprotein with a basic isoelectric point, distinguishing it from the acidic glycoproteins that form the insoluble matrix of the egg coat. When eluted from isoelectric focusing gels, the acidic matrix glycoproteins possess sperm-binding activity for wild-type sperm, but not for GalT I-null sperm,whereas the basic glycoprotein retains sperm-binding activity for both wild-type and GalT I-null sperm. Thus, GalT I-null sperm are able to resolve gamete recognition into at least two distinct binding events, leading to the characterization of a novel, peripherally associated, sperm-binding ligand on the ovulated zona pellucida.

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“…The role of the carbohydrate portion of glycoprotein is becoming increasingly recognized for its importance in mediating the adhesion between the mammalian spermatozoon and the zona pellucida (Loeser & Tulsiani 1999). The post-testicular modification of preformed glycosyl moieties is one of the mechanisms of sperm glycosylation during epididymal transit as demonstrated by CD52, a major maturationassociated sperm membrane antigen (Kirchhoff & Hale 1996, Kirchhoff et al 1998.…”

Section: Introductionmentioning

confidence: 99%

Partial characterization, sperm association and significance of N- and O-linked glycoproteins in epididymal fluid of rhesus monkeys (Macaca mulatta)

Srivastav

Singh²,

Chandra³

et al. 2004

Reproduction

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The present study investigated regional modifications of glycosylation status, sperm association and functional significance of N-and O-linked glycoproteins in epididymal luminal fluid of the rhesus monkey (Macaca mulatta). The predominant glycoproteins of the epididymal luminal fluid that increase in the extent of glycosylation or unmasking of exposed epitopes in a region-specific, maturation-dependent manner, included those of 150, 116, 68, 64, 58 (N-and O-linked) and 170 kDa (O-linked). The higher expression of 40 (N-linked), 38 (N-and O-linked) and 60, 56 and 33 kDa (O-linked) glycoproteins in the proximal caput epididymal fluid was followed by alteration or reorganization of 60, 38 and 33 kDa (O-linked) glycoproteins in the distal segments of the epididymis. The association of epididymal fluid glycoproteins with maturing spermatozoa was identified by generating polyclonal antiserum against monkey caudal sperm membrane in female albino rabbits. The antiserum crossreacted strongly with 58 and 33 kDa epididymal fluid glycoproteins of monkeys and also reacted with 116, 68, 58, 56 and 33 kDa glycoproteins from Triton X-100 extracts of human spermatozoa, indicating the presence of antigenically related components in both species. The functional significance of epididymal fluid glycoproteins in sperm functions was investigated by raising antiserum against a heavily glycosylated 58 kDa glycoprotein (MEF1) of caudal epididymal fluid, which crossreacted with the Triton X-100 extracts of epididymal spermatozoa of monkey and ejaculated human spermatozoa on immunoblots. In an in vitro micro-sperm agglutination assay, anti-MEF1 serum agglutinated both rat caudal epididymal spermatozoa and human spermatozoa. MEF1 seemed to be involved in fertilization as demonstrated by inhibition of fertility (100%) in female albino rabbits and rats immunized with this protein. A sperm-agglutinating 58 kDa glycoprotein of rhesus monkey epididymis with functional significance in fertility was identified, thus indicating that it is a potential candidate for contraceptive vaccine development.

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The Role of Carbohydrates in the Induction of the Acrosome Reaction in Mouse Spermatozoa1

Cited by 63 publications

References 49 publications

Structural Analysis of Murine Zona Pellucida Glycans

Structural Analysis of Murine Zona Pellucida Glycans

Characterization of a novel ZP3-independent sperm-binding ligand that facilitates sperm adhesion to the egg coat

Partial characterization, sperm association and significance of N- and O-linked glycoproteins in epididymal fluid of rhesus monkeys (Macaca mulatta)

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