Participation of the nonreducing terminal β‐galactosyl residues of the neutral N‐linked carbohydrate chains of porcine zona pellucida glycoproteins in sperm–egg binding

Yonezawa, Naoto; Amari, S.; Takahashi, Kazuya; Ikeda, Kikuko; Imai, Fabiana Lica; Kanai, Saeko; Kikuchi, Kazuhiro; Nakano, Minoru

doi:10.1002/mrd.20195

Cited by 41 publications

(31 citation statements)

References 26 publications

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“…A feasible role for oviductal b-D-galactosidase would concern remodeling the ZP since b-galactosyl residues in the ZP oligosaccharides are involved in porcine sperm-egg binding (Yonezawa et al 2005). These authors showed that treatment with b-D-galactosidase and endo-b-D-galactosidase of isolated porcine ZPs reduced the number of sperm bound and inhibited the sperm penetration in treated oocytes.…”

Section: Discussionmentioning

confidence: 99%

Determination of glycosidase activity in porcine oviductal fluid at the different phases of the estrous cycle

Carrasco

Romar

Sánchez³

et al. 2008

Reproduction

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Sperm-oocyte binding and gamete-oviductal epithelium interactions are carbohydrate-mediated events occurring in the oviductal fluid (OF). Thus, knowledge about the activities of glycosidases (enzymes catalyzing hydrolytic cleavage of terminal sugar residues) in this milieu would help us understand the molecular mechanisms involved in these events. This work was carried out to investigate the glycosidase activity, protein content, and volume of OF collected from gilts and sows. Oviducts were classified into four phases of the estrous cycle (early follicular, late follicular, early luteal, and late luteal) based on the appearance of the ovaries. OF was aspirated, centrifuged, measured for volume, and frozen until assay. Substrates conjugated to 4-methylumbelliferyl were used to screen the activities of seven different glycosidases at physiological pH (7.2). a-L-Fucosidase and b-N-acetyl-glucosaminidase activities increased at the late follicular phase to decrease after ovulation. b-D-Galactosidase, a-D-mannosidase, and b-N-acetyl-galactosaminidase showed higher activities at the early follicular phase, which decreased after ovulation. N-Acetyl-neuraminidase and a-D-galactosidase did not show activity at any phase of estrous cycle neither in sows nor in gilts at pH 7.2, although it did at acidic pH (4.4) in the follicular and luteal phase samples. Total protein also changed during the cycle showing the maximum secretion at the late follicular phase (2118.6G200.7 mg/oviduct). The highest volumes of OF were collected from the oviducts at the late follicular phase (50.7G1.3 ml/oviduct). These results indicate that OF from sows and gilts shows glycosidase activity varying throughout the estrous cycle suggesting a role of these enzymes in carbohydrate-mediated events. Reproduction (2008) 136 833-842

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Section: Discussionmentioning

confidence: 99%

Determination of glycosidase activity in porcine oviductal fluid at the different phases of the estrous cycle

Carrasco

Romar

Sánchez³

et al. 2008

Reproduction

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“…In both species, the biologically active carbohydrates are linked to the ZPB glycoprotein. The heteromultimeric complex of recombinant porcine ZPglycoproteins expressed in baculovirus-Sf9 insect cells carrying pauci-and high-mannose type glycans binds bovine but not porcine sperm (Yonezawa et al, 2005), indicating that in fact the binding event is dependent on the expression of specific carbohydrates. Despite the use of differing receptor-ligand systems, sperm are able to interact with the heterologous zona pellucida in vitro.…”

Section: Species-specificity Of Gamete-recognitionmentioning

confidence: 99%

“…The sperm-binding activity has been mapped to the neutral triand tetra-antennary complex N-glycans of ZPB expressing nonreducing terminal β-galactosyl residues (Kudo et al, 1998;Yonezawa et al, 2005). The request for polyvalency to achieve stable binding may be the reason that tri-and tetra-antennary glycans are shown to possess higher binding activity than the biantennary chains.…”

Section: Receptor-ligand Systems Involved In Primary Bindingmentioning

confidence: 99%

“…Gamete interaction in domestic animals has been best studied in pig and cattle. The polyvalent presentation of terminal α-mannosyl residues in high-mannose N-glycans has been found to determine bovine sperm-egg binding (Amari et al, 2001), whereas sperm recognition in the pig is mediated by terminal β-galactosyl residues in complex N-glycans (Yonezawa et al, 2005). In both species, the biologically active carbohydrates are linked to the ZPB glycoprotein.…”

Section: Species-specificity Of Gamete-recognitionmentioning

confidence: 99%

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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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“…Thus, sperm that suffer AA due to interaction with SBG in the lumen of the isthmus at post-ovulatory stages of oestrus would keep SBG bound at their altered acrosomal membrane. Considering that ZP3α (Mr 55 kDa) binds to the acrosome region of acrosome-damaged or partially acrosome-reacted spermatozoa (Yonezawa et al, 2005), that Mr 55 kDa zona pellucida component exhibits Galβ1-3GalNac, as does SBG (Marini and Cabada, 2003), and that deglycosylation of Mr 55 kDa makes ZP unable to trigger acrosomal reaction, it is possible that SBG bound to AA sperm would block their interaction with ZP3α. Reduction of the number of sperm bound to the zona may serve to reduce the incidence of polyspermy (Hunter, 1993;Killian, 2004).…”

Section: Cellular Distribution Of Tyrosine-phosphorylated Proteins Upmentioning

confidence: 99%

Porcine oviduct sperm binding glycoprotein and its deleterious effect on sperm: a mechanism for negative selection of sperm?

Teijeiro

Dapino²,

Marini

2011

Biol. Res.

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In their journey through the oviduct some subpopulations of sperm are preserved in a reservoir, while others are negatively selected. Sperm binding glycoprotein (SBG) is a pig oviductal epithelial cell glycoprotein that produces, under capacitating conditions, acrosome alteration, p97 tyrosine-phosphorylation and reduction of the motility of sperm. In this paper, we show that SBG is accessible at the extracellular surface of the oviductal epithelial cells, supporting a sperm interaction biological role in situ. We analyze the possible dependence of the tyrosine-phosphorylation of p97 on the PKA mechanism, fi nding that apparently it is not PKA dependent. Also, after SBG treatment the phosphorylated proteins locate mainly at the detached periacrosomal region and at the tail of sperm; the latter may be related to SBG's motility reduction effect. The study of the time course effect of SBG on sperm as detected by chlortetracycline (CTC) staining and of its binding to sperm by immunodetection in conjunction with CTC, shows results in agreement with the hypothesis that this glycoprotein is involved in the alteration of acrosomes in a specifi c sperm subpopulation. The results suggest that SBG may be part of a mechanism for negative selection of sperm.

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Participation of the nonreducing terminal β‐galactosyl residues of the neutral N‐linked carbohydrate chains of porcine zona pellucida glycoproteins in sperm–egg binding

Cited by 41 publications

References 26 publications

Determination of glycosidase activity in porcine oviductal fluid at the different phases of the estrous cycle

Determination of glycosidase activity in porcine oviductal fluid at the different phases of the estrous cycle

Glycobiology of fertilization in the pig

Porcine oviduct sperm binding glycoprotein and its deleterious effect on sperm: a mechanism for negative selection of sperm?

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