EGG molecules couple the oocyte-to-embryo transition with cell cycle progression

Abstract

The oocyte-to-embryo transition is a precisely coordinated process in which an oocyte becomes fertilized and transitions to an embryonic program of events. The molecules involved in this process have not been well studied. Recently, a group of interacting molecules in C. elegans have been described as coordinating the oocyte-to-embryo transition with the advancement of the cell cycle. Genes egg-3, egg-4, and egg-5 represent a small class of regulatory molecules known as protein-tyrosine phosphase-like proteins, which can bind phosphorylated substrates and act as scaffolding molecules or inhibitors. These genes are responsible for coupling the movements and activities of regulatory kinase mbk-2 with advancement of the cell cycle during the oocyte-to-embryo transition.

Figure 1

A. N2 wild-type population with worms in various stages of development. B. An adult sterile hermaphrodite.

Figure 2

A. Adult male, wild-type N2 worm. B. Adult hermaphrodite, wild-type N2 worm. C. Close-up of adult hermaphrodite proximal germline. At left are proximal most oocytes, at center the spermatheca containing mature spermatozoa, at left fertilized and developing embryos. D. Inactive spermatids dissected from a wild-type N2 male. E. Activated spermatozoa dissected from a wild-type N2 male, and activated with pronase.

Figure 3

A. The events of the oocyte-to-embryo transition 1. The proximal most (−1) oocyte. 2. As the proximal most oocyte approaches the spermatheca it undergoes NEBD and cytoskeletal rearrangment. The chromosomes condense. 3. Contractions of the somatic gonad sheath and spermatheca dilation lead to ovulation of the oocyte. After spermathecal entry, the egg is rapidly fertilized by a single sperm. 4. Metaphase I of meiosis I. The chromosomes are arranged in a characteristic pentagonal array. The sperm DNA marks the presumptive posterior of the embryo. 5. Anaphase I of meiosis I. The chromosomes separate and a single polar body is extruded. 6. Metaphase II of meiosis II. 7. Anaphase II of meiosis II. By this stage a robust chitin rich eggshell has been extruded. 8. The male and female DNA decondense and form pronuclei. 9. Cytoskeletal rearrangements bring the pronuclei together, they fuse. 10. The one cell embryo contains a single nucleus. 11. The beginning of mitotic divisions.

Figure 4

A. The EGG-4 and EGG-5 proteins rings the oocyte cortex. Again, the heaviest confluorescence occurs as the oocyte undergoes nuclear envelope breakdown. The protein remains at the cortex until the transition between metaphase I and anaphase I of meiosis I. At that point the protein washes across the cell in a distinct wave, becoming diffusely cytoplasmic. B. The EGG-3, CHS-1, and MBK-2 proteins rings the oocyte cortex. The heaviest confluorescence occurs as the oocyte undergoes nuclear envelope breakdown. The protein remains at the cortex until the transition between metaphase I and anaphase I of meiosis I. At that point the protein forms discrete cortical puncta. C. The hermaphrodite reproductive tract centered on the proximal most oocytes, spermatheca, and newest embryos. The animal contains a RFP:EGG-3 fusion protein.