From oogonia to mature oocytes: Inactivation of the maternal centrosome in humans

Abstract

The fine structure of human oogonia and growing oocytes has been reviewed in fetal and adult ovaries. Preovulatory maturation and the ultrastructure of stimulated oocytes from the germinal vesicle (GV) stage to metaphase II (MII) stage are also documented. Oogonia have large nuclei, scanty cytoplasm with complex mitochondria. During folliculogenesis, follicle cell processes establish desmosomes and deep gap junctions at the surface of growing oocytes, which are retracted during the final stages of maturation. The zona pellucida is secreted in secondary follicles. Growing oocytes have mitochondria, Golgi, rough endoplasmic reticulum (RER), ribosomes, lysosomes, and lipofuscin bodies, often associated with Balbiani bodies and have nuclei with reticulated nucleoli. Oocytes from antral follicles show numerous surface microvilli and cortical granules (CGs) separated from the oolemma by a band of microfilaments. The CGs are evidently secreted by Golgi membranes. The GV oocytes have peripheral Golgi complexes associated with a single layer of CGs close to the oolemma. They have many lysosomes, and nuclei with dense compact nucleoli. GV breakdown occurs by disorganization of the nuclear envelope and the oocyte enters a transient metaphase I followed by MII, when it is arrested and ovulated. Maturation of oocytes in vitro follows the same pattern of meiosis seen in preovulatory oocytes. The general organization of the human oocyte conforms to that of most other mammals but has some unique features. The MII oocyte has the basic cellular organelles such as mitochondria, smooth endoplasmic reticulum, microfilaments, and microtubules, while Golgi, RER, lysosomes, multivesicular, residual and lipofuscin bodies are very rare. It neither has yolk nor lipid inclusions. Its surface has few microvilli, and 1-3 layers of CGs, aligned beneath the oolemma. Special reference has been made to the reduction and inactivation of the maternal centrosome during oogenesis. The MII spindle, often oriented perpendicular to the oocyte surface, is barrel-shaped, anastral and lacks centrioles. Osmiophilic centrosomes are not demonstrable in human eggs, since the maternal centrosome is nonfunctional. However, oogonia and growing oocytes have typical centrioles, similar to those of somatic cells. The sperm centrosome activates the egg and organizes the sperm aster and mitotic spindles of the embryo, after fertilization.

Actin cytoskeleton in cell polarity and asymmetric division during mouse oocyte maturation

“…A common mechanism in positioning the spindle in mitotic cells is that the spindle moves to its expected location through a physical interaction between astral microtubules (MTs) and cell cortex [Cowan and Hyman, 2004;Siller and Doe, 2009]. However, spindle positioning during mouse oocyte meiosis must rely on other mechanisms since it is devoid of true centrosomes and largely of astral MTs [Szollosi et al, 1972;Brunet et al, 1999;Sathananthan et al, 2006]. Indeed, instead of MT, actin filaments (F-actin) are involved in spindle positioning in both MI and MII [Longo and Chen, 1985;Verlhac et al, 2000;Leader et al, 2002;Yi et al, 2011].…”

Analysis of centriole elimination duringC. elegansoogenesis

“…This could pose a threat to faithful chromosome segregation because the resulting spindle might be tetrapolar. In most metazoan species, including Caenorhabditis elegans and Homo sapiens, this problem is solved by the elimination of centrioles during oogenesis (reviewed by Schatten, 1994;Manandhar et al, 2005;Sathananthan et al, 2006). Electron microscopy (EM) analysis indicates that centrioles are absent in mouse and human oocytes (Hertig and Adams, 1967;Calarco et al, 1972;Szollosi et al, 1972;Szollosi et al, 1986;Sathananthan et al, 1996).…”

Centrosomes in fertilization, early embryonic development, stem cell division, and cancer

“…The centrosome during oogenesis and in oocytes Oogonia and oocytes up to the pachytene stage of hamsters, mice, rats, gerbils, and man contain centrioles, but in subsequent meiotic stages, centrioles are absent. At the time of germinal vesicle breakdown microtubule polymerization focuses on several electron-dense aggregates inside the ooplasm (Szöllösi et al, 1972;Sathananthan et al, 2006). Mature oocytes of rabbits, cows, and sheep are likewise devoid of centrioles Crozet et al, 2000).…”