Separation and Loss of Centrioles From Primordidal Germ Cells To Mature Oocytes In The Mouse

Abstract

Oocytes, including from mammals, lack centrioles, but neither the mechanism by which mature eggs lose their centrioles nor the exact stage at which centrioles are destroyed during oogenesis is known. To answer questions raised by centriole disappearance during oogenesis, using a transgenic mouse expressing GFP-centrin-2 (GFP CETN2), we traced their presence from e11.5 primordial germ cells (PGCs) through oogenesis and their ultimate dissolution in mature oocytes. We show tightly coupled CETN2 doublets in PGCs, oogonia, and pre-pubertal oocytes. Beginning with follicular recruitment of incompetent germinal vesicle (GV) oocytes, through full oocyte maturation, the CETN2 doublets separate within the pericentriolar material (PCM) and a rise in single CETN2 pairs is identified, mostly at meiotic metaphase-I and -II spindle poles. Partial CETN2 foci dissolution occurs even as other centriole markers, like Cep135, a protein necessary for centriole duplication, are maintained at the PCM. Furthermore, live imaging demonstrates that the link between the two centrioles breaks as meiosis resumes and that centriole association with the PCM is progressively lost. Microtubule inhibition shows that centriole dissolution is uncoupled from microtubule dynamics. Thus, centriole doublets, present in early G2-arrested meiotic prophase oocytes, begin partial reduction during follicular recruitment and meiotic resumption, later than previously thought.

The Centriole’s Role in Miscarriages

“…Like other cell types, early mammalian egg cells (pre-pubertal oocytes) have two centrioles, but they degenerate, and disappear during egg maturation ( Simerly et al, 2018 ). Ultimately, meiotic cell division is mediated without recognizable centrioles ( Manandhar et al, 2005 ; Simerly et al, 2018 ). The fate of the centrioles is different in sperm.…”

Biophysical and Quantitative Principles of Centrosome Biogenesis and Structure

“…Intriguingly, in starfish, daughter centrioles are kept in the oocyte, whereas mother centrioles are extruded along with the polar bodies (Borrego-Pinto et al 2016). In addition, centriole loss during mouse oogenesis seems to occur despite PCM persistence (Simerly et al 2018). These examples raise questions as to the mechanisms employed to regulate centriole loss in different species.…”

Meiosis initiation: a story of two sexes in all creatures great and small

“…Consequently, the oocyte requires a longer maturation period compared with the process of spermatogenesis. During oogenesis, the centrosomes are eliminated [ 46 ] and centrioles within the future zygote are provided by mature spermatids [ 47 ]. Therefore, meiosis is regulated differently in the context of meiotic entry, timing, hormonal changes and outcomes during oogenesis and spermatogenesis in order to produce high quality gametes that have contrasting roles prior to fertilisation.…”