Sperm Oocyte Fusion and Oocyte Activation

After sperm penetration through the zona pellucida, the sperm plasma membrane fuses with the oocyte plasma membrane in a narrow equatorial region of the head, followed by incorporation of the whole spermatozoon to the oocyte by a phagocytosis-like process (1). All components of the spermatozoon, with the exception of nuclear DNA, are subsequently dismantled in the oocyte cytoplasm.

An immediate consequence of sperm-oocyte fusion is oocyte activation (2). Shortly after the fusion, a particular type of calcium signal is generated in mammalian oocytes. These signals were first described in the mouse (3), but similar signals were later observed in oocytes of all mammalian species, including the human (4,5). The temporal pattern of these signals is characterized by periodically repeated sharp increases (spikes) in free cytoplasmic calcium ion concentration, also referred to as calcium oscillations (Fig. 1). The spatial propagation of these signals takes the form of calcium waves of which the first is triggered at the sperm-fusion site (Fig. 2A). These phenomena are mediated by fluxes of calcium ions which enter the cytosolic compartment along the pre-existing concentration gradients, both from the extracellular space and from the intracellular calcium

Figure 1 Calcium oscillations, visualized with the use of the intracellular calcium indicator Fluo3, in a living human oocyte fertilized by subzonal insemination. Source: From Ref. 5.
Calcium Ions Fertilization

Figure 2 Confocal microscopy images of sperm-induced intracellular free calcium concentration increases, and the effects of protein kinase C(PKC) activation and inhibition. Calcium was visualized by fluorescence microscopy after loading oocytes with intracellular calcium indicator Fluo-3. Differences in fluorescence intensity were converted to color according to the scale bar where the lowest values are coded black. (A) The first sperm-induced calcium increase in a control, without any PKC modulation. (B) The first sperm-induced calcium increase in an oocyte pretreated with the PKC activator 4P-phorbol 12-myristate 13-acetate before the exposure to spermatozoa. (C) The first sperm-induced calcium increase in an oocyte pretreated with the PKC inhibitor chelerythrine before the exposure to spermatozoa. (D) One of the ongoing series of calcium increases in an oocyte exposed to the PKC inhibitor chelerythrine after sperm penetration. Source: From Ref. 6.

Figure 2 Confocal microscopy images of sperm-induced intracellular free calcium concentration increases, and the effects of protein kinase C(PKC) activation and inhibition. Calcium was visualized by fluorescence microscopy after loading oocytes with intracellular calcium indicator Fluo-3. Differences in fluorescence intensity were converted to color according to the scale bar where the lowest values are coded black. (A) The first sperm-induced calcium increase in a control, without any PKC modulation. (B) The first sperm-induced calcium increase in an oocyte pretreated with the PKC activator 4P-phorbol 12-myristate 13-acetate before the exposure to spermatozoa. (C) The first sperm-induced calcium increase in an oocyte pretreated with the PKC inhibitor chelerythrine before the exposure to spermatozoa. (D) One of the ongoing series of calcium increases in an oocyte exposed to the PKC inhibitor chelerythrine after sperm penetration. Source: From Ref. 6.

organelles rich in calcium stores, mainly the endoplasmic reticulum (6). The movements of calcium ions between different intracellular calcium-storing organelles and the cytosol are mediated by two types of receptor-gated calcium channels—the inositol-trisphosphate-gated one and the ryanodine-gated one (7)—whose sensitivity to calcium-induced calcium release is modified by an yet poorly defined sperm-borne factor (8) so as to promote the ability of the oocyte calcium homeostasis machinery (the complex of calcium channels and calcium pumps) to generate calcium waves and calcium oscillations. The steady state required for the maintenance of calcium waves and calcium oscillations is likely to depend on a fine tuning of the phosphor-ylation status of components of the receptor-gated calcium channels, as these phenomena are disturbed by both activators (Fig. 2B) and inhibitors (Fig. 2C and D) of protein kinase C (PKC) (6).

Oocyte activation triggers the cortical reaction which modifies the properties of the zona pellucida by rendering it resistant to penetration of supernumerary spermatozoa (1). Moreover, it reactivates the cell cycle of the fertilized oocyte by removing substances which maintain the temporary arrest at metaphase of the second meiotic division; this event launches the beginning of the mitotic cell cycle of the newly formed embryo (1).

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