Coordination of cellular differentiation, polarity, mitosis and meiosis – New findings from early vertebrate oogenesis

Abstract

A mechanistic dissection of early oocyte differentiation in vertebrates is key to advancing our knowledge of germline development, reproductive biology, the regulation of meiosis, and all of their associated disorders. Recent advances in the field include breakthroughs in the identification of germline stem cells in Medaka, in the cellular architecture of the germline cyst in mice, in a mechanistic dissection of chromosomal pairing and bouquet formation in meiosis in mice, in tracing oocyte symmetry breaking to the chromosomal bouquet of meiosis in zebrafish, and in the biology of the Balbiani body, a universal oocyte granule. Many of the major events in early oogenesis are universally conserved, and some are co-opted for species-specific needs. The chromosomal events of meiosis are of tremendous consequence to gamete formation and have been extensively studied. New light is now being shed on other aspects of early oocyte differentiation, which were traditionally considered outside the scope of meiosis, and their coordination with meiotic events. The emerging theme is of meiosis as a common groundwork for coordinating multifaceted processes of oocyte differentiation. In an accompanying manuscript we describe methods that allowed for investigations in the zebrafish ovary to contribute to these breakthroughs. Here, we review these advances mostly from the zebrafish and mouse. We discuss oogenesis concepts across established model organisms, and construct an inclusive paradigm for early oocyte differentiation in vertebrates.

Previtellogenic oocytes of South African largemouth bass Micropterus salmoides Lacépède 1802 (Actinopterygii, Perciformes) ‐ the Balbiani body, cortical alveoli and developing eggshell

“…In many cases, the cystoblasts continue mitotic division (karyokineses), however, cytokinesis is not complete, and the female germline cysts composed of cystocytes are formed. In the ovaries of teleost fish, and also of other vertebrates and of invertebrates, some cystocytes are eliminated by cell death, the remaining begin meiosis and continue the development as the oocytes (Bilinski, Kloc, & Tworzydlo, ; Elkouby, ; Elkouby, Jamieson‐Lucy, & Mullins, ; Elkouby & Mullins, ; Ikami, Nuzhat, & Lei, ; Kloc, Bilinski, Dougherty, Brey, & Etkin, ; Lei & Spradling, ; Marlow & Mullins, ; Mazzoni, Grier, & Quagio‐Grassiotto, ; Nakamura et al, ; Żelazowska & Fopp‐Bayat, ). The karyokineses of cystoblasts that lead to the formation of cysts are sometimes stopped in the ovaries and the cystoblasts enter meiosis without producing the cysts (Grier, Porak, Carroll, & Parenti, ).…”

“…The Balbiani body has been thoroughly examined in the African clawed frog, Xenopus laevis (Kloc et al, , ; Kloc & Etkin, ), and the house mouse, Mus musculus (Ikami et al, ; Kloc et al, ; Lei & Spradling, ). It has also been investigated in teleost fish, for example, in zebrafish Danio rerio (Elkouby, ; Elkouby et al, ; Elkouby & Mullins, ; Lyman‐Gingerich & Pelegri, ; Marlow & Mullins, ), rainbow trout Salmo gairdneri (Beams & Kessel, ), golden grey mullet Mugil (Liza) auratus (Bruslé, ), medaka Oryzias latipes (Iwamatsu & Nakashima, ; Kobayashi & Iwamatsu, ; Nakamura et al, ), and in the Atlantic salmon Salmo salar (Škugor, Tveiten, Johnsen, & Andersen, ). It is also present in oocytes of several species of sturgeons and paddlefish (Chondrostei, Acipenseriformes); for example, in the Russian sturgeon, Acipenser gueldenstaedtii (Zelazowska et al, ; Żelazowska, Jankowska, Plewniak, & Rajek, ), Siberian sturgeon, A. baerii (Żelazowska & Fopp‐Bayat, , ), Chinese, A. sinensis , Dabry's, A. dabryanus sturgeons (Yang, Yue, Ye, Li, & Wei, ; Ye et al, ; Ye, Li, Yue, Yang, & Wei, ; Ye, Yue, Yang, Li, & Wei, ; Yue et al, ), the North American paddlefish, Polyodon spathula (Żelazowska et al, ; Żelazowska & Kilarski, ) as well as in numerous species of invertebrates (e.g., Bilinski et al, ; Kloc, Jedrzejowska, Tworzydlo, & Bilinski, ).…”

“…remaining begin meiosis and continue the development as the oocytes (Bilinski, Kloc, & Tworzydlo, 2017;Elkouby, 2017;Elkouby, Jamieson-Lucy, & Mullins, 2016;Elkouby & Mullins, 2017;Ikami, Nuzhat, & Lei, 2017;Kloc, Bilinski, Dougherty, Brey, & Etkin, 2004;Lei & Spradling, 2016;Marlow & Mullins, 2008;Mazzoni, Grier, & Quagio-Grassiotto, 2010;Nakamura et al, 2011;Żelazowska & Fopp-Bayat, 2017b). The karyokineses of cystoblasts that lead to the formation of cysts are sometimes stopped in the ovaries and the cystoblasts enter meiosis without producing the cysts (Grier, Porak, Carroll, & Parenti, 2018).…”

Cystic proliferation of embryonic germ stem cells is necessary to reproductive success and normal mating behavior in medaka

“…Cystic division is a highly conserved mechanism that precedes gametogenesis in both invertebrates and vertebrates (Amini et al, 2014;Hansen and Schedl, 2006;Hinnant et al, 2017;Quagio-Grassiotto et al, 2011). It has been well established in vertebrates that female germ cells enter meiosis earlier, while male germ cells are arrested and undergo meiosis at the onset of the prepubertal period (Elkouby and Mullins, 2017;Koubova et al, 2006;Pepling, 2006). In medaka, this type of cystic cell division is known as proliferation type II, by which in females, the number of EGSCs increases dramatically during embryonic stages; whereas in males, this exponential proliferation to form cysts begins later, in the juvenile stage (Satoh and Egami, 1972;Tanaka, 2019).…”

Collective cell sorting requires contractile cortical waves in germline cells

“…in Drosophila (Elkouby and Mullins, 2017). In mammals, pre-granulosa cells invade in 39 between germ cells and each cyst eventually breaks down (CBD) into single cells encased by 40 granulosa cells, forming primordial follicles (PFs) ( In Drosophila, these early steps of oogenesis take place in a specialized structure 51 called the germarium at the anterior tip of the ovary (Figure 1a) (Huynh and St Johnston, 52 detachment from the plasma membrane (Charras and Paluch, 2008;Diz-Muñoz et al, 2013).…”