The vertebrate Balbiani body, germ plasm, and oocyte polarity

Jamieson-Lucy, Allison; Mullins, Mary C.

doi:10.1016/bs.ctdb.2019.04.003

Cited by 58 publications

(64 citation statements)

References 163 publications

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“…They are set aside early during embryo development to ensure that they develop into germ cells instead of activating somatic differentiation programs. In some species, the so-called germ granules comprising RNAs and RNA-associated proteins determine where the germ cells will form [1][2][3][4][5]. How germ granules are organized has long been unclear.…”

Section: When the Germline Meets Phase Separationmentioning

confidence: 99%

Phase Separation during Germline Development

Cheng

Schuh

2021

Trends in Cell Biology

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Many non-membrane-bound compartments in cells organize by phase separation. Recent research implicates phase separation in different steps during germline development. Phase separation drives the formation and partitioning of germ granules that determine germ cell identity during early embryogenesis. Phase separation promotes the interactions between ribonucleoprotein particles and membrane-bound organelles to form the Balbiani body in Xenopus and zebrafish oocytes. Phase separation mediates pairing and synapsis of homologous chromosomes during meiotic recombination in various species. Phase separation enriches microtubule regulatory proteins and promotes acentrosomal spindle assembly in mammalian oocytes.

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Section: When the Germline Meets Phase Separationmentioning

confidence: 99%

Phase Separation during Germline Development

Cheng

Schuh

2021

Trends in Cell Biology

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“…This is surprising, as humans and frogs are evolutionary more distant to each other than mouse is to either species. Balbiani bodies are enigmatic super-organelles; their only known function is to host healthy mitochondria and protect RNAs from degradation to be passed on to the new embryo in the form of germ plasm (Jamieson-Lucy and Mullins, 2019; Kloc et al, 2004; Marlow, 2017). Species that use inductive processes to specify their germline, such as mammals or axolotls, still contain a Balbiani body, indicating a conserved function for this super-organelle.…”

Section: Discussionmentioning

confidence: 99%

“…The Balbiani body is only present in early, non-growing oocytes and dissociates upon oocyte activation, thus is closely associated with oocyte dormancy. The function of the Balbiani body remains elusive, although it is proposed to protect mitochondria and RNA in the germline (Jamieson-Lucy and Mullins, 2019; Kloc et al, 2004). This enigmatic super-organelle has been observed in, among others, humans (Hertig and Adams, 1967), monkeys (Hope, 1965), cats (Amselgruber, 1983), frogs (Al-Mukhtar and Webb, 1971; Boke et al, 2016) and zebrafish (Marlow and Mullins, 2008).…”

Section: Introductionmentioning

confidence: 99%

Mouse oocytes do not contain a Balbiani body

Dhandapani

Salzer

Durán

et al. 2021

Preprint

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Poor oocyte quality accounts for majority of female fertility problems, however, we know little about how oocytes can remain healthy for many years or why they eventually decline with age. An oocyte spends majority of its lifetime in primordial state. Unlike many somatic cell types or mature oocytes, the cellular and molecular biology of primordial oocytes are largely unexplored. Yet, studying these aspects is necessary to understand the remarkable lifespan of oocytes and their eventual decline.A hallmark of primordial oocytes in many species is the Balbiani body, a non-membrane bound compartment that contains majority of mitochondria in oocyte cytoplasm. The Balbiani body was shown to be held together by an amyloid-like matrix in Xenopus oocytes. It has been proposed to be essential for maintaining mitochondria in a healthy state during long-lasting dormancy.Here, we develop enabling methods that allow live-imaging based comparative characterisation of Xenopus, mouse and human primordial oocytes. We show that human and Xenopus oocytes have a Balbiani body, characterised by an intense accumulation of mitochondria. Our results suggest that amyloid-like features of Balbiani bodies are conserved in humans and Xenopus. However, despite previous reports, we could not find a conventional Balbiani body in mouse oocytes. We demonstrate what was mistaken for a Balbiani body in mouse primordials is an unconventionally shaped Golgi apparatus. Our work provides the first insights into the organisation of the cytoplasm in mammalian primordial oocytes, and clarifies relative advantages and limitations of different model systems for studying female (in)fertility.Significance StatementWorld-wide data suggest that >25% of female fertility problems are undiagnosed, pointing to a huge gap in our understanding of female reproduction. Our findings help fill this gap by studying the cell biology of primordial oocytes. Having optimised methods for isolation and live-imaging of oocytes, we show that oocytes of evolutionary more distant species, Xenopus and human have a conserved super-organelle, a Balbiani body, in their cytoplasm whereas mouse oocytes do not have one. We propose that the shorter lifespan in mice obviates the need for a Balbiani body. Our results also suggest that primordial oocytes have active organelles, and thus call for a re-examination of the concept of dormancy in these long-lived cells.

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“…Two modes of germ cells specification and development occur in animals: induction mode and preformation mode. The induction mode has been well explained or predicted in species, such as mice and several mammals, turtles, salamander, skates, and sharks [ 2 ]. In the mice and humans, signals from extraembryonic tissues induce a unique gene regulatory network in germline-competent cells for PGC specification, and PGCs are established in perigastrulation-stage embryos [ 3 ].…”

Section: Introductionmentioning

confidence: 99%

“…In the mice and humans, signals from extraembryonic tissues induce a unique gene regulatory network in germline-competent cells for PGC specification, and PGCs are established in perigastrulation-stage embryos [ 3 ]. The preformation mode has been well explained or predicted in species, such as fruit flies, frogs, zebrafish, roundworm, sturgeon, and ascidians [ 2 , 4 ]. In the fruit flies, frogs, and zebrafish, the maternally stored germ plasm (containing RNAs, proteins, and energy-rich mitochondria) in the oocyte is inherited into the cells specifying precursor germ cells during early embryonic development [ 5 , 6 , 7 ].…”

Section: Introductionmentioning

confidence: 99%

Whole-Transcriptome Sequencing-Based Analysis of DAZL and Its Interacting Genes during Germ Cells Specification and Zygotic Genome Activation in Chickens

Rengaraj

Won

Han

et al. 2020

IJMS

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The deleted in azoospermia like (DAZL) is required for germ cells development and maintenance. In chickens, the mRNA and protein of DAZL, a representative maternally inherited germ plasm factor, are detected in the germ plasm of oocyte, zygote, and all stages of the intrauterine embryos. However, it is still insufficient to explain the origin and specification process of chicken germ cells, because the stage at which the zygotic transcription of DAZL occurs and the stage at which the maternal DAZL RNA/protein clears have not yet been fully identified. Moreover, a comprehensive understanding of the expression of DAZL interacting genes during the germ cells specification and development and zygotic genome activation (ZGA) is lacking in chickens. In this study, we identified a set of DAZL interacting genes in chickens using in silico prediction method. Then, we analyzed the whole-transcriptome sequencing (WTS)-based expression of DAZL and its interacting genes in the chicken oocyte, zygote, and Eyal-Giladi and Kochav (EGK) stage embryos (EGK.I to EGK.X). In the results, DAZL transcripts are increased in the zygote (onset of transcription), maintained the increased level until EGK.VI, and decreased from EGK.VIII (possible clearance of maternal RNAs). Among the DAZL interacting genes, most of them are increased either at 1st ZGA or 2nd ZGA, indicating their involvement in germ cells specification and development.

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The vertebrate Balbiani body, germ plasm, and oocyte polarity

Cited by 58 publications

References 163 publications

Phase Separation during Germline Development

Phase Separation during Germline Development

Mouse oocytes do not contain a Balbiani body

Whole-Transcriptome Sequencing-Based Analysis of DAZL and Its Interacting Genes during Germ Cells Specification and Zygotic Genome Activation in Chickens

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