Cortical granule translocation

Eggs of most animal species are fertilized by a single sperm and fusion of these two cells is essential for the activation of the developmental program of the zygote. Cases in which multiple sperm fertilize an egg, a condition known as polyspermy, the supernumerary paternal centrioles and chromosomes usually create aberrant cell divisions that result in death. Thus, eggs have evolved mechanisms to prevent polyspermy. The most conserved mechanism is a permanent modification of the extracellular matrix of the egg to separate physically and biochemically extraneous sperm from the egg. This change at the cell surface results from secretion of dense core vesicles called cortical granules, which are poised in the egg cortex prior to fertilization. The contents of cortical granules in frogs and sea urchins have been well studied and are found to contain a diverse repertoire of molecules that includes enzymes, structural proteins and glycosaminoglycans (Wessel et al., 2001). Once secreted, these molecules mix with the nascent vitelline layer of the egg and lift it from the cell surface to form a proteinaceous envelope. In mammals, the contents of cortical granules are not as well understood, but they too modify the oocyte extracellular matrix, the zona pellucida, making it nonreceptive to subsequent sperm. In general, cortical granules are synthesized throughout oogenesis, accumulating linearly, and are dispersed evenly throughout the cytoplasm of the cell. However, just prior to the resumption of meiosis, apparent by germinal vesicle (oocyte nucleus) breakdown, cortical granules translocate en masse to the cell surface where they dock to the plasma membrane (Berg and Wessel, 1997). While the stimulus for cortical granule translocation to the plasma membrane is not known in any animal, in sea urchins it does occur temporally coincident with the resumption of meiosis. A general indication of meiotic maturation is movement of the germinal vesicle to the oocyte surface, where it breaks down, and progresses through two rounds of meiotic reduction, resulting in two polar bodies and a haploid complement of chromosomes. Oocytes of most animals are halted at some point in meiosis (MII for frog and mouse, for example) and fertilization reinitiates the meiotic process and the exocytosis of cortical granules. In starfish, a close relative of sea urchins, oocytes are shed with an intact germinal vesicle and 1-methyladenine synthesized in the follicle cells reinitiates meiosis. These oocytes are usually fertilized in MII, and then complete meiosis. If these oocytes are not fertilized within 20 4315 Development 129, 4315-4325 (2002) Printed in Great Britain © The Company of Biologists Limited 2002 DEV5507