Bookshelf

Regulation of Oocyte Meiosis

Vertebrate oocytes (developing eggs) have been particularly useful models for research on the cell cycle, in part because of their large size and ease of manipulation in the laboratory. A notable example, discussed earlier in this chapter, is provided by the discovery and subsequent purification of MPF from frog oocytes. Meiosis of these oocytes, like those of other species, is regulated at two unique points in the cell cycle, and studies of oocyte meiosis have illuminated novel mechanisms of cell cycle control.

The first regulatory point in oocyte meiosis is in the diplotene stage of the first meiotic division (Figure 14.37). Oocytes can remain arrested at this stage for long periods of time—up to 40 to 50 years in humans. During this diplotene arrest, the oocyte chromosomes decondense and are actively transcribed. This transcriptional activity is reflected in the tremendous growth of oocytes during this period. Human oocytes, for example, are about 100 μm in diameter (more than a hundred times the volume of a typical somatic cell). Frog oocytes are even larger, with diameters of approximately 1 mm. During this period of cell growth, the oocytes accumulate stockpiles of materials, including RNAs and proteins, that are needed to support early development of the embryo. As noted earlier in this chapter, early embryonic cell cycles then occur in the absence of cell growth, rapidly dividing the fertilized egg into smaller cells (see Figure 14.2).

Oocytes of different species vary as to when meiosis resumes and fertilization takes place. In some animals, oocytes remain arrested at the diplotene stage until they are fertilized, only then proceeding to complete meiosis. However, the oocytes of most vertebrates (including frogs, mice, and humans) resume meiosis in response to hormonal stimulation and proceed through meiosis I prior to fertilization. Cell division following meiosis I is asymmetric, resulting in the production of a small polar body and an oocyte that retains its large size. The oocyte then proceeds to enter meiosis II without having re-formed a nucleus or decondensed its chromosomes. Most vertebrate oocytes are then arrested again at metaphase II, where they remain until fertilization.

Like the M phase of somatic cells, the meiosis of oocytes is controlled by MPF. The regulation of MPF during oocyte meiosis, however, displays unique features that are responsible for metaphase II arrest (Figure 14.38). Hormonal stimulation of diplotene-arrested oocytes initially triggers the resumption of meiosis by activating MPF, as at the G2 to M transition of somatic cells. As in mitosis, MPF then induces chromosome condensation, nuclear envelope breakdown, and formation of the spindle. Activation of the anaphase-promoting complex B then leads to the metaphase to anaphase transition of meiosis I, accompanied by a decrease in the activity of MPF. Following cytokinesis, however, MPF activity again rises and remains high while the egg is arrested at metaphase II. A regulatory mechanism unique to oocytes thus acts to maintain MPF activity during metaphase II arrest, preventing the metaphase to anaphase transition of meiosis II and the inactivation of MPF that would result from cyclin B proteolysis during a normal M phase.

The factor responsible for metaphase II arrest was first identified by Yoshio Masui and Clement Markert in 1971, in the same series of experiments that led to the discovery of MPF. In this case, however, cytoplasm from an egg arrested at metaphase II was injected into an early embryo cell that was undergoing mitotic cell cycles (Figure 14.39). This injection of egg cytoplasm caused the embryonic cell to arrest at metaphase, indicating that metaphase arrest was induced by a cytoplasmic factor present in the egg. Because this factor acted to arrest mitosis, it was called cytostatic factor (CSF).

More recent experiments have identified a protein-serine/threonine kinase known as Mos as an essential component of CSF. Mos is specifically synthesized in oocytes around the time of completion of meiosis I and is then required both for the increase in MPF activity during meiosis II and for the maintenance of MPF activity during metaphase II arrest. The action of Mos results from activation of the ERK MAP kinase, which plays a central role in the cell signaling pathways discussed in the previous chapter. In oocytes, however, ERK plays a different role; it activates another protein kinase called Rsk, which inhibits action of the anaphase-promoting complex and arrests meiosis at metaphase II (Figure 14.40). Oocytes can remain arrested at this point in the meiotic cell cycle for several days, awaiting fertilization.