On the Control of Oocyte Meiotic Maturation and Ovulation inCaenorhabditis elegans

Abstract

Prior to fertilization, oocytes undergo meiotic maturation (cell cycle progression) and ovulation (expulsion from the ovary). To begin the study of these processes in Caenorhabditis elegans, we have defined a time line of germline and somatic events by video microscopy. As the oocyte matures, its nuclear envelope breaks down and its cell cortex rearranges. Immediately thereafter, the oocyte is ovulated by increasing contraction of the myoepithelial gonadal sheath and relaxation of the distal spermatheca. By systematically altering the germ cell contents of the hermaphrodite using mutant strains, we have uncovered evidence of four cell-cell interactions that regulate maturation and ovulation. (1) Both spermatids and spermatozoa induce oocyte maturation. In animals with a feminized germline, maturation is inhibited and oocytes arrest in diakinesis. The introduction of sperm by mating restores maturation. (2) Sperm also directly promote sheath contraction. In animals with a feminized or tumorous germline, contractions are infrequent, whereas in animals with a masculinized germline or with sperm introduced by mating, contractions are frequent. (3 and 4) The maturing oocyte both induces spermathecal dilation and modulates sheath contractions at ovulation; dilation of the distal spermatheca and sharp increases in sheath contraction rates are only observed in the presence of a maturing oocyte.

Structural components of the nonstriated contractile apparatuses in the Caenorhabditis elegans gonadal myoepithelial sheath and their essential roles for ovulation

“…When ovulation fails, a mature oocyte remains in the proximal ovary, repeats DNA synthesis without cell division, and becomes endomitotic (Iwasaki et al, 1996;McCarter et al, 1997McCarter et al, , 1999. This phenotype is designated as Emo (endomytotic oocytes in the proximal ovary) and is characterized by intense staining by 4Ј6-diamidino-2-phenylindole, dihydrochloride (DAPI) of overly amplified nuclear DNA in endomitotic oocytes ( Fig.…”

“…1). The germline and oocytes are surrounded by 10 sheath cells (pairs 1-5), and ovulation requires a signal from sperm that induces ovarian contraction and oocyte maturation, which are then followed by dilation of the spermatheca and fertilization (Ward and Carrel, 1979;McCarter et al, 1997McCarter et al, , 1999Hubbard and Greenstein, 2000;Yamamoto et al, 2006). The proximal sheath cells (pairs 3-5; Fig.…”

“…1) are smooth musclelike cells with distinct thin and thick filaments and designated as the myoepithelial sheath (Hirsh et al, 1976;Strome, 1986;Ardizzi and Epstein, 1987;Hall et al, 1999). Contraction of the myoepithelial sheath is periodically enhanced upon maturation of the most proximal oocytes (McCarter et al, 1997(McCarter et al, , 1999. Sheath contraction is negatively regulated by ceh-18 encoding a POU-class homeoprotein (Rose et al, 1997;Miller et al, 2003) and gap junctions that are formed between the myoepithelial sheath and maturing oocytes (Whitten and Miller, 2006).…”

Caenorhabditis elegans germ line: A model for stem cell biology

“…Given the rate of oocyte maturation (McCarter et al, 1999) and the new cell death estimate from JaramilloLambert et al, a rough calculation can be made regarding the required number of doublings that must occur in the proliferative zone to account for germ cell loss to programmed cell death and oogenesis. An adult hermaphrodite with a reserve of sperm ovulates approximately once every 23 min per gonad arm (McCarter et al, 1999), thereby producing ϳ60 oocytes in 24 Figure 2B,C of Maciejowski et al, 2006), with permission.…”

“…An adult hermaphrodite with a reserve of sperm ovulates approximately once every 23 min per gonad arm (McCarter et al, 1999), thereby producing ϳ60 oocytes in 24 Figure 2B,C of Maciejowski et al, 2006), with permission. The blue and red lines were intensified for clarity.…”