Oogenesis:A Collaborative Effort
How many cells does it take to make an oocyte?
The task of oogenesis is to construct a large cell containing a large and complex dowry of resources for construction of the embryo before it can either make them on its own or obtain them from its environment. Organization is critical: Components may be spatially restricted to facilitate establishment of distinct embryonic regions.
Review the timing of oogenesis and compare to that of the male. Remember: most of the events of oocyte differentiation occur during prophase I of meiosis. In the mammal, all oogonial decisions and transformation into oocytes are completed either before or shortly after birth. But, there is no oocyte growth until puberty. Then, cohorts of oocytes resume development during each cycle.
(See Browder et al., Fig. 3.2)
In some organisms, all stages of oogenesis can co-exist in the ovary (e.g. frogs).
Oocyte-Accessory Cell Interactions
Roles of accessory cells: production of steroid hormones, transportation of essential components to the oocyte, and formation of accessory layers surrounding the oocyte (later, the egg).
There are two categories of accessory cells: follicle cells and nurse cells. What is the major distinction between these two categories of cells? Nurse cells are found in a number of invertebrate species. We shall discuss insect nurse cells in some detail.
In the mammalian follicle, each oocyte is surrounded by a multilayered cohort of follicle cells, often referred to as granulosa cells. Between the oocyte and granulosa cells is the acellular zona pellucida, which is secreted by the oocyte. The zona is penetrated by many short microvilli from the surface of the oocyte and cytoplasmic processes from the follicle cells. Desmosomes and gap junctions form at the points where the cytoplasmic process contact the oocyte surface. The gap junctions function in transfer of nutrients and regulatory molecules into the oocyte.
Granulosa cells secrete the fluid that accumulates in the extracellular spaces and bathes the oocyte. The spaces coalesce to form the antrum (Fig. 1). Follicles with large antra are called Graafian follicles. In the Graafian follicle a cluster of granulosa cells surround the accentrically-located oocyte. They are collectively called the cumulus oophorus. The cumulus is shed along with the egg at ovulation.
Figure 1. Preovulatory mammalian follicle. Image courtesy of Dr. Douglas Kline, Kent State University.
The insect egg chamber is found in so-called meroistic insects (e.g., Drosophila). Incomplete cytokinesis of the terminal oogonial divisions results in a cluster of 16 cells interconnected by cytoplasmic bridges.
(See Browder et al., Fig. 3.6; Gilbert, Fig. 22.27; Kalthoff, Fig. 3.15)
One of these cells differentiates into the oocyte, and the rest become nurse cells. The nurse cells, which become highly polyploid (1024N), provide macromolecules and even organelles to the developing oocyte.
(See Browder et al., Fig. 3.8; Gilbert, Fig. 22.28; Kalthoff, Fig. 3.18; Shostak, Fig. 7.28)
Oocytes grow rapidly from the support they receive from these 15 polyploid cells. Drosophila oocyte volume increases 90,000 fold in just 3 days (Xue and Cooley, 1993)! At the end of oogenesis, residual nurse cell cytoplasm is transferred into the oocyte. Its volume doubles in just 30 minutes.
The entire nurse cell-oocyte complex is surrounded by follicle cells, which also play significant roles in oogenesis, as we shall discuss later.
(See Browder et al., Fig. 3.5; Gilbert, Fig. 22.27; Kalthoff, Fig. 3.14)
Oocyte Structure and Morphogenesis
Polarity is a salient feature of oocytes. Consider, for example, the yolk-rich amphibian oocyte. As we shall discuss later, not only are organelles localized in the egg, but macromolecules may also have specific domains.
(See Browder et al., Fig. 3.11)
As with sperm, mitochondria are significant oocyte organelles. They may be present in great abundance to fuel the events of early development, during which the embryo has no facility to produce new mitochondria of its own. (Remember that mitochondria are self-replicating.)
An example is the amphibian Xenopus laevis. In somatic cells, the ratio of nuclear DNA:mitochondrial DNA is 100:1. In the fully-grown oocyte, that ratio has reversed to a range from 1:1 to 1:100. During mitochondrial replication in early oogenesis, mitochondria cluster around the nucleus to form a structure called the mitochondrial cloud.
(See Browder et al., Fig. 3.12)
The cloud also contain electron-dense material called granulofibrillar material (GFM). The mitochondrial cloud later disperses, forming large subcortical islands of mitochondria and GFM at one pole of the oocyte. These clusters resemble similar clusters in unfertilized eggs that are similar to the germ plasm, which is thought to function in germ cell determination
(See Browder et al., Fig. 3.14).
The amount and distribution of yolk varies considerably in the animal kingdom. You should be able to distinguish among oligolecithal, telolecithal and centrolecithal eggs and name examples of each. How is an amphibian egg classified?
Yolk is formed in one of two ways: It is either synthesized within the oocyte (autosynthesis) or exogenously and transported into the oocyte (heterosynthesis). Vertebrate vitellogenesis is predominantly heterosynthetic. The yolk precursor (vitellogenin), which is synthesized in the liver, is incorporated via receptor-mediated endocytosis. Study this process in your textbook. A similar process occurs in Drosophila. Yolk is synthesized in the fat body and ovaries.
(See Browder et al., Figures 3.17-3.20; Gilbert, Fig. 22.22; Kalthoff, Fig. 3.20; Shostak, Fig. 7.32)
Yolk is distributed in the amphibian oocyte in an asymmetrical pattern, with most platelets and the largest ones located in the vegetal hemisphere. The other hemisphere is the animal hemisphere. This polarity foreshadows the polarity of the embryo itself. The establishment of this polarity has been studied by monitoring the deposition of fluorescent-labeled vitellogenin.
(See Browder et al., Fig. 3.22)
Young oocytes have a centrally located germinal vesicle (what is a germinal vesicle?) and uniformly-distributed yolk platelets; the latter are localized in the subcortical cytoplasm. Asymmetry results from a displacement of the yolk platelets from the animal hemisphere to the vegetal hemisphere (at a rate of 50 µm/day). The displacement process presumably involves the cytoskeleton.
The cortex is a semi-rigid gel (as distinct from the endoplasm, which is fluid). The cortex resists centrifugation. The cortex may contain specialized organelles, such as cortical granules and/or pigment granules
(See Browder et al., Figs. 3.11 and 3.17)
Cortical granules are membrane-enclosed organelles that release their contents at fertilization. We shall discuss the roles of these components later. The cortical granules are formed in the endoplasm. Precursor molecules are apparently synthesized on the ribosomes of the rough endoplasmic reticulum and transported within the E.R. to the Golgi apparatus, where the granules are assembled
(See Browder et al., Fig. 3.24)
Oocyte Structure and Morphogenesis
Clegg, N. J., Frost, D. M., Larkin, M. K., Subrahmanyan, L., Bryant, Z. and Ruohola-Baker, H. maelstrom is required for an early step in the establishment of Drosophila oocyte polarity: posterior localization of grk mRNA.
Deng, W.-M. and Bownes, M. Two signalling pathways specify localised expression of the Broad-Complex in Drosophila eggshell patterning and morphogenesis.
Gosden, R., Krapez, J. and Briggs, D. 1997. Growth and development of the mammalian oocyte. BioEssays 19: 875-882.
Jackson, S.M. and Blochlinger, K. 1997. cut interacts with Notch and Protein kinase A to regulate egg chamber formation and to maintain germline cyst integrity during Drosophila oogenesis. Development 124: 3663-3672.
Ohlstein, B. and McKearin, D. 1997. Ectopic expression of the Drosophila Bam protein eliminates oogenic germline stem cells. Development 124: 3651-3662.
Browder, L.W., Erickson, C.A. and Jeffery, W.R. 1991. Developmental Biology. Third edition. Saunders College Pub. Philadelphia.
Gilbert, S.F. 1997. Developmental Biology. Fifth Edition. Sinauer. Sunderland, MA.
Kalthoff, K. 1996. Analysis of Biological Development. McGraw-Hill. New
Xue, F. and L. Cooley. 1993. kelch encodes a component of intercellular bridges in Drosophila egg chambers.Cell 72: 681-693
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Leon Browder & Laurie Iten (Ed.) Dynamic Development
Last revised Friday, June 12, 1998