Abstract
Protein-carbohydrate interaction regulates multiple important processes during fertilization, an essential biological event where individual gametes undergo intercellular recognition to fuse and generate a zygote. In the mammalian female reproductive tract, sperm temporarily adhere to the oviductal epithelium via the complementary interaction between carbohydrate-binding proteins on the sperm membrane and carbohydrates on the oviductal cells. After detachment from the oviductal epithelium at the appropriate time point following ovulation, sperm migrate and occasionally bind to the extracellular matrix, called the zona pellucida (ZP), which surrounds the egg, thereafter undergoing the exocytotic acrosomal reaction to penetrate the envelope and to reach the egg plasma membrane. This sperm-ZP interaction also involves the direct interaction between sperm carbohydrate-binding proteins and carbohydrates within the ZP, most of which have been conserved across divergent species from mammals to amphibians and echinoderms. This review focuses on the carbohydrate-mediated interaction of sperm with the female reproductive tract, mainly the interaction between sperm and the ZP, and introduces the fertilization-suppressive action of dicalcin, a Xenopus laevis ZP protein-associated protein. The action of dicalcin correlates significantly with a dicalcin-dependent change in the lectin-staining pattern within the ZP, suggesting a unique role of dicalcin as an inherent protein that is capable of regulating the affinity between the lectin and oligosaccharides attached on its target glycoprotein.
Highlights
Much attention has been paid to gaining greater understanding of the molecular mechanisms of the fertilization process whereby two gametes interact, achieve mutual recognition, and fuse to initiate the resumption of the cell cycle of eggs, which leads to development of a new individual
To consolidate the current knowledge on protein-carbohydrate interaction in the communication between sperm and cells of the female reproductive system, we briefly describe the fertilization process, sperm storage in the oviduct, sperm interaction with the egg-coating envelope, and the molecules involved with these sperm behaviors, followed by a review of the unique action of dicalcin
zona pellucida (ZP) proteins are mainly synthesized in growing oocytes during each reproductive cycle in mammalian and amphibian species, whereas fish and bird ZP proteins are synthesized in the ovary or liver or both
Summary
Much attention has been paid to gaining greater understanding of the molecular mechanisms of the fertilization process whereby two gametes (i.e., sperm and egg) interact, achieve mutual recognition, and fuse to initiate the resumption of the cell cycle of eggs, which leads to development of a new individual. Evidence has accumulated showing that, on the route of the sperm toward the egg, there are at least two regulatory steps that involve protein-oligosaccharide interactions: one is the sperm-oviductal epithelium interaction, and the other is the sperm-zona pellucida (ZP) interaction In both these interactions, sperm recognition of the target involves the binding of multiple carbohydrate receptor proteins on the sperm to the complementary oligosaccharide chains attached to the surface of the target cells. Many candidates and combinations of interacting proteins and carbohydrates have been reported across divergent species and have been discussed in numerous excellent reviews [3,4,5,6,7,8,9,10,11] In addition to these molecules, we have recently isolated and characterized dicalcin, a unique glycoprotein-associated protein, which regulates the affinity of interaction between a lectin and the carbohydrate moieties of glycoprotein, affecting fertilization success in Xenopus laevis [12]. To consolidate the current knowledge on protein-carbohydrate interaction in the communication between sperm and cells of the female reproductive system (i.e., oviductal epithelial cells, and eggs), we briefly describe the fertilization process, sperm storage in the oviduct, sperm interaction with the egg-coating envelope, and the molecules involved with these sperm behaviors, followed by a review of the unique action of dicalcin
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