Animal Female Meiosis: The Challenges of Eliminating Centrosomes

Abstract

Sexual reproduction requires the generation of gametes, which are highly specialised for fertilisation. Female reproductive cells, oocytes, grow up to large sizes when they accumulate energy stocks and store proteins as well as mRNAs to enable rapid cell divisions after fertilisation. At the same time, metazoan oocytes eliminate their centrosomes, i.e., major microtubule-organizing centres (MTOCs), during or right after the long growth phases. Centrosome elimination poses two key questions: first, how can the centrosome be re-established after fertilisation? In general, metazoan oocytes exploit sperm components, i.e., the basal body of the sperm flagellum, as a platform to reinitiate centrosome production. Second, how do most metazoan oocytes manage to build up meiotic spindles without centrosomes? Oocytes have evolved mechanisms to assemble bipolar spindles solely around their chromosomes without the guidance of pre-formed MTOCs. Female animal meiosis involves microtubule nucleation and organisation into bipolar microtubule arrays in regulated self-assembly under the control of the Ran system and nuclear transport receptors. This review summarises our current understanding of the molecular mechanism underlying self-assembly of meiotic spindles, its spatio-temporal regulation, and the key players governing this process in animal oocytes.

How Essential Kinesin-5 Becomes Non-Essential: Force Balance and Microtubule Dynamics Matter

“…In higher eukaryotes and plants, the bipolar spindle is formed independent of the centrosome through the pathway referred to as the acentrosomal pathway [99][100][101]. Historically, the acentrosomal pathway is extensively characterised in vitro using extracts prepared from Xenopus oocytes, where the Ran GTPase acts as a master regulator [102,103]. This pathway is functional in vivo in several cell types which are naturally devoid of centrosomes (eg.…”

A pseudo-meiotic centrosomal function of TEX12 in cancer

“…The pathological effect of TEX12 on centrosome function in cancer cells raises the possibility that its physiological function during meiosis might also include a centrosome function, in addition to its well-established role in chromosome synapsis. While it is generally thought that centrosomes dissipate in gametogenesis, with the loss of centrioles and formation of asymmetric microtubule organising centres, recent studies have reported the retention of centriole remnants in mature oocytes [26][27][28][29][30] . In mice it has been extensively demonstrated that oocytes contribute the centrosomes while centrosomal proteins and centrioles was reported to come from the sperm 31 .…”

Comparative Biology of Centrosomal Structures in Eukaryotes

“…Boveri also first postulated that the first centrosome within a zygote originates from the fertilizing sperm cell, while the unfertilized egg lacks a centrosome [ 7 ]. This holds true for many animal species and is discussed in detail in the both the reviews of Avidor–Reiss and Gruss in this issue of Cells [ 10 , 11 ]. After these groundbreaking works of the late nineteenth century centrosome research became stuck in its descriptive character and poked along until the late 80s of the twentieth century with a relatively low number of key papers, despite the centrosome’s central importance for cellular function.…”

“…Here, the small GTPase Ran is rendered into its GTP form through the chromatin-associated GTP/GDP exchange factor Rcc1, which together with Aurora A activates several spindle assembly factors [ 52 , 53 , 54 , 55 ]. The latter organize γ-tubulin complexes to nucleate microtubules, which become arranged in a bipolar spindle through the activity of motor proteins including dynein, a bipolar Eg5-like kinesin and a chromokinesin [ 11 ]. Further examples for non-centrosomal microtubule organization also in interphase have been especially well-investigated in Drosophila .…”