The zona pellucida of mammalian oocytes plays an important role in binding and activation of sperm cells during the molecular events leading to fertilization. The genes coding for the three zona pellucida glycoproteins ZPA, ZPB, and ZPC of various species including mouse, dog, and human have been cloned and sequenced by several groups. However, it has remained a matter of debate as to whether the oocytes alone or in conjunction with the surrounding granulosa cells express and deposit these proteins to form the zona pellucida matrix. Addressing this unresolved issue, we assessed the expression and localization of all three zona pellucida proteins in ovaries of human, cynomolgus monkey and mice using immunohistochemical methods. In addition, oocyte-specific expression of ZPC from the primordial stage onward was confirmed by in situ hybridization. In sections of human ovaries, ZPA, ZPB, and ZPC proteins were immunohistochemically detected in the cytoplasms of primordial oocytes and during later stages of folliculogenesis in the zona pellucida matrices of oocytes. In sections fixed with formalin, a clear homogeneous ring was visible around the oocyte and no staining of granulosa cells was observed. In contrast, staining of ZP proteins was also observed between granulosa cells when Bouin's reagent had been used for tissue fixation. Thus, the original zona pellucida architecture was better preserved by formalin fixation. We further demonstrated that dissolution of the zona pellucida of isolated bovine oocytes occurred after they were exposed to Bouin's reagent. In summary, these results demonstrate that in mice, monkeys and humans, zona proteins are expressed and assembled exclusively by the oocyte and not by the granulosa cells. Previously observed results of ZP expression by an involvement of granulosa cells might therefore be the result of an improper fixation of the tissues leading to the disruption of the zona pellucida. Additionally this study highlights the importance of choosing the correct fixative for immunohistochemistry, not only for the usual reason of retaining antigenicity, but rather to retain the entire architectural structure.

Immunohistochemical localization of zona pellucida proteins ZPA, ZPB and ZPC in human; cynomolgus monkey; and mouse ovaries

The development of the mammalian oocyte and ovary serves as a focus for molecular genetic studies on cell lineage, tissue-specific gene expression, and organogenesis. The female germ cell populates the primitive gonad during the second trimester of mouse development, and their interactions with the support cells result in the formation of the ovary. After birth and during the reproductive life of the female, cohorts of oocytes grow, undergo meiotic maturation, and, following ovulation, are available for fertilization in the oviduct. The expression of the zona pellucida genes serves as a marker of germ cell growth and represents the set of oocyte-specific genes unique to mammals. These zona genes encode proteins that are secreted to form an extracellular matrix that surrounds the eggs and mediates the species-specific events of fertilization.

Developmental Genetics of the Zona Pellucida

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Developmental Genetics of the Zona Pellucida