Dazl determines primordial follicle formation through the translational regulation of Tex14

Rosario, Roseanne; Crichton, James H; Stewart, Hazel L.; Childs, Andrew J.; Adams, Ian R.; Anderson, Richard A.

doi:10.1096/fj.201901247r

Cited by 13 publications

(18 citation statements)

References 54 publications

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“…5, B and C ). Considering the role of Dazl in licensing for meiosis ( 20 ) and its function in translational regulation of TEX14 in cultured mouse embryonic ovaries ( 21 ), we compared Dazl expression and confirmed that levels were comparable between Tex14 +/− and Tex14 −/− (fig. S5A).…”

Section: Resultsmentioning

confidence: 72%

Intercellular bridges coordinate the transition from pluripotency to meiosis in mouse fetal oocytes

et al. 2021

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Meiosis is critical to generating oocytes and ensuring female fertility; however, the mechanisms regulating the switch from mitotic primordial germ cells to meiotic germ cells are poorly understood. Here, we implicate intercellular bridges (ICBs) in this state transition. We used three-dimensional in toto imaging to map meiotic initiation in the mouse fetal ovary and revealed a radial geometry of this transition that precedes the established anterior-posterior wave. Our studies reveal that appropriate timing of meiotic entry across the ovary and coordination of mitotic-meiotic transition within a cyst depend on the ICB component Tex14, which we show is required for functional cytoplasmic sharing. We find that Tex14 mutants more rapidly attenuate the pluripotency transcript Dppa3 upon meiotic initiation, and Dppa3 mutants undergo premature meiosis similar to Tex14. Together, these results lead to a model that ICBs coordinate and buffer the transition from pluripotency to meiosis through dilution of regulatory factors.

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Section: Resultsmentioning

confidence: 72%

Intercellular bridges coordinate the transition from pluripotency to meiosis in mouse fetal oocytes

et al. 2021

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“…Our study examines the earliest stages of gonadogenesis and provides evidence that the conserved RBP, Dazl, is required for germline cyst formation and plays critical roles in germ cell amplification, and acts upstream of meiosis and establishment of germline stem cells to promote fertility. Immunoaffinity screens for Dazl targets have identified regulators of incomplete cytokinesis (Kim et al, 2015;Reynolds et al, 2005;Rosario et al, 2019;Rosario et al, 2017;Zagore et al, 2018). This work provides genetic evidence that Dazl is required to form germline cysts interconnected by ring canals.…”

Section: Discussionmentioning

confidence: 79%

“…Although Dazl has not been shown to be required for cyst formation, we reasoned that Dazl was a compelling candidate regulator of this conserved process, since in mouse and human fetal ovary it interacts with Tex14, a regulator of ring canal formation (Greenbaum et al, 2006;Reynolds et al, 2005;Rosario et al, 2017;Zagore et al, 2018). In zebrafish dazl is expressed at all stages of GC development, but its function at this particular stage of germline development is unknown (Hashimoto et al, 2004;Howley and Ho, 2000;Kosaka et al, 2007;Maegawa et al, 1999).…”

Section: Dazl Mutantsmentioning

confidence: 99%

“…Failure to generate a cyst in dazl mutants could be due to abnormal cyst architecture or cytokinesis such as failure to arrest the cytokinetic furrow, particularly given that Dazl interacts with cytokinesis and ring canal factors (Reynolds et al, 2005;Rosario et al, 2019;Rosario et al, 2017;Zagore et al, 2018). Actin is a prominent marker of intercellular connections and subcellular structures of GC cysts in other species, including the spectrosome of GSCs, and the branched fusome that connects germline cyst cells (de Cuevas et al, 1997;Kloc et al, 2004;Lin and Spradling, 1995;Snapp et al, 2004;Spradling et al, 1997).…”

Section: Dazl Is Required For Cystogenesismentioning

confidence: 99%

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Zebrafishdazlregulates cystogenesis upstream of the meiotic transition and germline stem cell specification and independent of meiotic checkpoints

Bertho

Clapp

Banisch

et al. 2019

Preprint

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StatementWe show that zebrafish dazl is required for incomplete cytokinesis to generate germline cysts during cystogenesis, acts upstream of germline stem cell establishment, and is required for meiosis, and fertility. AbstractFertility and gamete reserves are maintained by asymmetric divisions of the germline stem cells to produce new stem cells or daughters that differentiate as gametes. Before entering meiosis, differentiating germ cells (GCs) of sexual animals typically undergo cystogenesis. This evolutionary conserved process involves synchronous and incomplete mitotic divisions of a germ cell daughter (cystoblast) to generate sister cells connected by stable intercellular bridges that facilitate exchange of materials to support a large synchronous population of gamete progenitors. Here we investigate cystogenesis in zebrafish and identified Deleted in azoospermia (Dazl), a conserved vertebrate RNA binding protein as a regulator of this process. Analysis of dazl mutants revealed an essential role for Dazl in regulating incomplete cytokinesis and germline cyst formation before the meiotic transition. Accordingly, dazl mutant GCs form defective ring canals, and ultimately remain as individual cells that fail to differentiate as meiocytes. In addition

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“…We have used the compound WIN 18,446 to inhibit retinoic acid synthesis in a fetal mouse ovary culture system that supports germ cell survival and progression through prophase I of meiosis up to diplotene arrest, followed by primordial follicle formation and subsequent growth initiation ( Stefansdottir et al . 2016 , Rosario et al 2019 ). Fetal ovaries are cultured from e13.5, a stage when germ cells are committed to oocyte development and enter the first stages of meiosis ( Adams & McLaren 2002 ); thus, in this study we are investigating the role of retinoic acid on meiotic progression, distinct from its initiation.…”

Section: Discussionmentioning

confidence: 99%

Reduced retinoic acid synthesis accelerates prophase I and follicle activation

et al. 2020

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In female mammals, reproductive potential is determined during fetal life by the formation of a non-renewable pool of primordial follicles. Initiation of meiosis is one of the defining features of germ cell differentiation, and is well established to commence in response to retinoic acid. WIN 18,446 inhibits the conversion of retinol to retinoic acid, therefore was used to explore the impact of reduced retinoic acid synthesis on meiotic progression and thus germ cell development and subsequent primordial follicle formation. e13.5 mouse fetal ovaries were cultured in vitro and treated with WIN 18,446 for the first 3 days of a total of up to 12 days. Doses as low as 0.01µM reduced transcript levels of the retinoic acid response genes Stra8 and Rarβ without affecting germ cell number. Higher doses resulted in germ cell loss, rescued with the addition of retinoic acid. WIN 18,446 significantly accelerated the progression of prophase I; this was seen as early as 48 hours post treatment using meiotic chromosome spreads, and was still evident after 12 days of culture using Tra98/Msy2 immunostaining. Furthermore, ovaries treated with WIN 18,446 at e13.5 but not at P0 had a higher proportion of growing follicles compared to vehicle controls, thus showing evidence of increased follicle activation. These data therefore indicate that retinoic acid is not necessary for meiotic progression but may have a role in the regulation of its progression and germ cell survival at that time, and provide evidence for a link between meiotic arrest and follicle growth initiation.

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Dazl determines primordial follicle formation through the translational regulation of Tex14

Cited by 13 publications

References 54 publications

Intercellular bridges coordinate the transition from pluripotency to meiosis in mouse fetal oocytes

Intercellular bridges coordinate the transition from pluripotency to meiosis in mouse fetal oocytes

Zebrafishdazlregulates cystogenesis upstream of the meiotic transition and germline stem cell specification and independent of meiotic checkpoints

Reduced retinoic acid synthesis accelerates prophase I and follicle activation

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