Mouse early oocytes are transiently polar: Three-dimensional and ultrastructural analysis

Abstract

The oocytes of many invertebrate and non-mammalian vertebrate species are not only asymmetrical but also polar in the distribution of organelles, localized RNAs and proteins, and the oocyte polarity dictates the patterning of the future embryo. Polarily located within the oocytes of many species is the Balbiani body (Bb), which in Xenopus is known to be associated with the germinal granules responsible for the determination of germ cell fate. In contrast, in mammals, it is widely believed that the patterning of the embryo does not occur before implantation, and that oocytes are non-polar and symmetrical. Although the oocytes of many mammals, including mice and humans, contain Bbs, it remains unknown how and if the presence of Bbs relates to mouse oocyte and egg polarity. Using three-dimensional reconstruction of mouse neonatal oocytes, we showed that mouse early oocytes are both asymmetrical and transiently polar. In addition, the specifics of polarity in mouse oocytes are highly reminiscent of those in Xenopus early oocytes. Based on these findings, we conclude that the polarity of early oocytes imposed by the position of the centrioles at the cytoplasmic bridges is a fundamental and ancestral feature across the animal kingdom.

Premature ovarian failure in nobox-deficient mice is caused by defects in somatic cell invasion and germ cell cyst breakdown

“…However, in some oocytes, the centrosomes, normally positioned in the center of a Balbiani body (see Figs. 4, 5 and 8 in Kloc et al, [12]), were located outside of the Balbiani body, often in the vicinity of oocyte plasma membrane ( Fig. 3e and f).…”

“…Nobox deficiency in mice and perturbation of NOBOX homeodomain in women result in the premature ovarian failure (POF) syndrome characterized by postnatal oocyte loss and the replacement of follicles by fibrous tissue [1,2,6,8,10]. In mice, as in the majority of other animal species, mitotic divisions of primary oogonia, followed by incomplete cytokinesis, lead to the formation of germ cell cysts (nests, clusters) containing several oocytes connected by intercellular bridges [11][12][13]. Subsequently, the germ cell cysts break apart: somatic cells invade the cysts and separate and surround individual oocytes, resulting in the formation of individual ovarian follicles, which, in mammals, are called primordial follicles [11][12][13].…”

“…In mice, as in the majority of other animal species, mitotic divisions of primary oogonia, followed by incomplete cytokinesis, lead to the formation of germ cell cysts (nests, clusters) containing several oocytes connected by intercellular bridges [11][12][13]. Subsequently, the germ cell cysts break apart: somatic cells invade the cysts and separate and surround individual oocytes, resulting in the formation of individual ovarian follicles, which, in mammals, are called primordial follicles [11][12][13]. Histological studies of oocyte development in mice between the newborn stage and day 14 after birth showed that ovaries of Nobox +/− and Nobox −/− newborns have similar overall numbers of germ cell cysts and oocytes, indicating no overall germ cell loss [7].…”

Early oogenesis in the short‐tailed fruit bat Carollia perspicillata: Transient germ cell cysts and noncanonical intercellular bridges

“…In both species the asymmetry is related to the localization of the Golgi complexes. In mouse oocytes, the Golgi complexes are organized around a pair of centrioles (the centrosome) and constitute a specific structure called the Balbiani body (Pepling et al, 2007; Kloc et al, 2008). The 3D reconstruction of the distribution of organelles in mouse oocytes showed that the Balbiani body was always located near the intercellular bridge connecting sister oocytes.…”

Expression of Intermediate Filaments in the Balbiani Body and Ovarian Follicular Wall of the Japanese Quail <b><i>(Coturnix japonica)</i></b>

“…It has generally been thought that the primary role of the Balbiani body is to provide precursor yolk material and other metabolic requirements for the oocyte [Guraya, 1976]. It has also been hypothesised that the Balbiani body plays a role in the selection of the healthiest mitochondria for the future zygote [Cox and Spradling, 2003] and that it is a component of a vegetal pole RNA transport pathway [Kloc et al, 2008].…”