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Riddle DL, Blumenthal T, Meyer BJ, et al., editors. C. elegans II. 2nd edition. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 1997.

Cover of C. elegans II

C. elegans II. 2nd edition.

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Section IXOocyte Development, Maturation, and Ovulation

A. Oocyte Development

Late stages of oogenesis occur during diakinesis of meiotic prophase I. As distal germ-line nuclei progress around the loop and through the proximal gonad, they become more fully enclosed by membrane, cell and nuclear volumes increase, and chromosomes become increasingly condensed. Oocyte surface/membrane-associated antigens appear at this time (Strome 1986a; Guo and Kemphues 1995). Approximately five of the most mature oocytes accumulate large amounts of yolk proteins (S. Strome, pers. comm.), which are synthesized in the intestine (Kimble and Sharrock 1983).

Time-lapse Nomarski microscopy (Ward and Carrel 1979) has been used to define a pathway of landmark events in late oocyte development, meiotic maturation, and ovulation (Fig. 5) (J. McCarter and T. Schedl, unpubl.). In hermaphrodites, the oocyte nucleolus disappears about 70 minutes before ovulation. Subsequently, the nucleus migrates to the distal surface of the cell. The distal surface can also invaginate toward the nucleus, suggesting a physical connection that is under tension. With the exception of the acentrically placed nucleus (the importance of which is not currently known), the oocyte does not show an obvious polarization; no symmetry is observed in the cytoskeleton or the distribution of P granules (Strome 1986a) or PAR-1 (Guo and Kemphues 1995). Thus, unlike the Drosophila oocyte, which exhibits asymmetries that reflect a “prepattern” of the embryonic body axes (see, e.g., Roth et al. 1995), asymmetries in the C. elegans embryo appear to be established de novo at fertilization or during early zygotic development (see Kemphues and Stone, this volume).

Figure 5. Landmark morphological events in late oocyte development, meiotic maturation, and ovulation.

Figure 5

Landmark morphological events in late oocyte development, meiotic maturation, and ovulation. Events are shown for a single oocyte, as deduced by time-lapse Nomarski microscopy. Time is relative to (more...)

B. Oocyte Maturation

Meiotic maturation describes the transition from diakinesis to metaphase of meiosis I. The first indication of maturation is nuclear envelope breakdown (NEBD) which begins at 5.7 minutes before ovulation. At 3.0 minutes before ovulation, the oocyte begins to change shape from a cube to a sphere (oocyte cortical rearrangement). Vigorous sheath contractions occur at the same time. Analysis of sheath-ablated animals and mutants defective in sheath activity indicates that NEBD and oocyte cortical rearrangement do not depend on myoepithelial sheath contractile activity (Myers et al. 1996; J. McCarter and T. Schedl, unpubl.).

C. Ovulation

Ovulation, the exit of the most proximal oocyte from the gonad arm into the spermatheca, requires contraction of the eight proximal sheath cells (which are myoepithelial) and dilation of the distal spermatheca (oviduct valve). The rate of sheath contractions increases prior to NEBD and peaks at ovulation when the sheath appears to contract tonically as it pulls the dilating distal spermatheca over the oocyte. As the distal spermatheca closes, cytoplasmic streaming is visible in the oocyte, possibly indicating fertilization. The divisions of meiosis I and II occur in the uterus.

D. Meiotic Prophase Arrest

In unmated females, oocytes arrest in diakinesis, failing to undergo meiotic maturation and ovulation. Numerous oocytes accumulate, each with an enlarged, distally placed nucleus without a nucleolus. Sheath contractile activity in females is lower than the background level observed between ovulations in hermaphrodites. (At a low rate, oocytes in females stochastically exit from arrest and are ovulated.) It is unclear whether arrest is an active inhibition of progression or a failure to provide a positive signal that is necessary for progression.

In hermaphrodites with abundant sperm, oocyte development, maturation, and ovulation occur in an assembly-line-like fashion, with the time between successive ovulations averaging about 25 minutes. In this situation, the time an oocyte spends in diakinesis may reflect a developmental requirement for the execution of certain events and thus might not be a true “arrest” of the meiotic cell cycle.

E. Mutants with Endomitotic Oocytes

Mutants with polyploid oocytes in the gonad arm due to endomitosis (Emo) arise frequently in recessive sterile screens and are beginning to be characterized. Mutants with an Emo phenotype include ceh-18(mg57) (Greenstein et al. 1994) and certain non-null alleles of emo-1 (Iwasaki et al. 1996), lin-3 , let-23 (Aroian and Sternberg 1991), and mup-2 (Myers et al. 1996). Most Emo mutants examined to date by time-lapse microscopy show ovulation defects (J. McCarter and T. Schedl, unpubl.). Both lin-3(n1058) and let-23(sy10), for instance, show an additional 20-minute delay between NEBD and ovulation. The distal spermatheca fails to dilate during this time and the oocyte is damaged upon ovulation, with contents relapsing into the gonad arm.

The Emo phenotype can arise from germ-line or somatic defects. Mosaic analysis of emo-1 indicates a germ-line focus of action (Iwasaki et al. 1996). CEH-18 is found in sheath cell nuclei (Greenstein et al. 1994) and laser ablation of sheath, distal spermatheca, or their precursors can also result in an Emo phenotype (J. McCarter and T. Schedl, unpubl.). A current hypothesis is that the maturing oocyte signals the surrounding sheath and distal spermatheca cells to trigger ovulation, and failure of this process traps the mature oocyte in the gonad where it begins mitotic cycling. Karyokinesis and cytokinesis do not occur because unfertilized oocytes lack mitotic centrioles (Albertson 1984b).

Copyright © 1997, Cold Spring Harbor Laboratory Press.
Bookshelf ID: NBK20108


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