Progesterone modulates microtubule dynamics and epiboly progression during zebrafish gastrulation

Eckerle, Stephanie; Ringler, Mario; Lecaudey, Virginie; Nitschke, Roland; Driever, Wolfgang

doi:10.1016/j.ydbio.2017.12.016

Cited by 13 publications

(13 citation statements)

References 63 publications

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“…Examination of EB3-GFP comets along the animal-vegetal axis revealed large numbers of EB3-GFP comets throughout the yolk cell at sphere stage, which indicates extensive microtubule growth, similar to a recent report ( Fig. 4A and Movie 5) (Eckerle et al, 2017). EB3-GFP comets spread downwards towards the vegetal pole, which is consistent with the network having uniform polarity, with microtubule plus ends extending vegetally (Solnica- Krezel and Driever, 1994).…”

Section: E-ysn Move Away From Isolated Microtubule Organizing Centerssupporting

confidence: 89%

“…As Clip1a is maternally expressed it might be involved in the establishment of the network, but this remains to be tested (Ikegami and Setou, 2010;Hsu et al, 2006). Eckerle et al (2017) examined microtubule dynamics in the yolk cell and found that progesterone stimulates microtubule growth during epiboly initiation. They proposed that progesterone and pregnenolone could function to establish the microtubule dynamics and stability that are required for the different phases of epiboly and that the progression phase of epiboly, when the e-YSN migrate, may necessitate microtubule stability over dynamics (Eckerle et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

“…To test this prediction, we examined e-YSN migration in embryos in which the yolk cell microtubules were stabilized and bundled. Stabilization of yolk microtubules, for example by taxol treatment, produces regions of bundled microtubules as well as regions of the yolk cell that are depleted of microtubules (Eckerle et al, 2017;Solnica-Krezel and Driever, 1994). To specifically affect the yolk cell microtubule network, we took a targeted approach by overexpressing the microtubulestabilizing protein Ras association domain family 1 (Rassf1) in the yolk cell.…”

Section: E-ysn Take Abnormal Trajectories When Yolk Microtubules Are mentioning

confidence: 99%

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A cargo model of yolk syncytial nuclear migration during zebrafish epiboly

et al. 2018

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In teleost fish, the multinucleate yolk syncytial layer functions as an extra-embryonic signaling center to pattern mesendoderm, coordinate morphogenesis and supply nutrients to the embryo. External yolk syncytial nuclei (e-YSN) undergo microtubule-dependent movements that distribute the nuclei over the large yolk mass. How e-YSN migration proceeds, and the role of the yolk microtubules, is not understood, but it is proposed that e-YSN are pulled vegetally as the microtubule network shortens from the vegetal pole. Live imaging revealed that nuclei migrate along microtubules, consistent with a cargo model in which e-YSN are moved down the microtubules by direct association with motor proteins. We found that blocking the plus-end directed microtubule motor kinesin significantly attenuated yolk nuclear movement. Blocking the outer nuclear membrane LINC complex protein Syne2a also slowed e-YSN movement. We propose that e-YSN movement is mediated by the LINC complex, which functions as the adaptor between yolk nuclei and motor proteins. Our work provides new insights into the role of microtubules in morphogenesis of an extraembryonic tissue and further contributes to the understanding of nuclear migration mechanisms during development.

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Section: E-ysn Move Away From Isolated Microtubule Organizing Centerssupporting

confidence: 89%

Section: Discussionmentioning

confidence: 99%

Section: E-ysn Take Abnormal Trajectories When Yolk Microtubules Are mentioning

confidence: 99%

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A cargo model of yolk syncytial nuclear migration during zebrafish epiboly

et al. 2018

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“…Cholesterol has an important role as substrate for the synthesis of pregnenolone, the first steroid hormone within the steroid hormone biosynthesis pathway. Pregnenolone and other steroids have been implicated in the regulation of zebrafish epiboly ( Eckerle et al, 2018 ; Hsu et al, 2006 ; Schwend et al, 2011 ; Weng et al, 2013 ). Therefore, we hypothesized that mondoa knockdown might affect epiboly by interfering with Nsdhl-dependent cholesterol and steroid hormone biogenesis.…”

Section: Resultsmentioning

confidence: 99%

MondoA regulates gene expression in cholesterol biosynthesis-associated pathways required for zebrafish epiboly

Weger

Schink

et al. 2020

eLife

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The glucose-sensing Mondo pathway regulates expression of metabolic genes in mammals. Here, we characterized its function in the zebrafish and revealed an unexpected role of this pathway in vertebrate embryonic development. We showed that knockdown of mondoa impaired the early morphogenetic movement of epiboly in zebrafish embryos and caused microtubule defects. Expression of genes in the terpenoid backbone and sterol biosynthesis pathways upstream of pregnenolone synthesis was coordinately downregulated in these embryos, including the most downregulated gene nsdhl. Loss of Nsdhl function likewise impaired epiboly, similar to MondoA loss of function. Both epiboly and microtubule defects were partially restored by pregnenolone treatment. Maternal-zygotic mutants of mondoa showed perturbed epiboly with low penetrance and compensatory changes in the expression of terpenoid/sterol/steroid metabolism genes. Collectively, our results show a novel role for MondoA in the regulation of early vertebrate development, connecting glucose, cholesterol and steroid hormone metabolism with early embryonic cell movements.

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“…To take into account the interactions of maternal Sox19b with Pou5f3, we obtained a double mutant by crossing MZsox19b to Pou5f3 mutant MZspg m793 (Lunde et al, 2004). MZspg mutants develop severe epiboly defects which lead to gastrulation arrest (Eckerle et al, 2018;Song et al, 2013) and are weakly dorsalized (Belting et al, 2011;Reim and Brand, 2006). Epiboly defects in double MZsox19bspg mutants were similar to MZspg (Fig.…”

Section: Genetic Ablation Of Maternal Sox19b Delays Embryo Developmenmentioning

confidence: 99%

Pluripotency factors determine gene expression repertoire at zygotic genome activation

Gao

Veil

Rosenblatt

et al. 2020

Preprint

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PouV and SoxB1 family transcription factors (TFs) have emerged as master regulators of cell fate transitions. To investigate the genetic interactions between Pou5f3 and Sox19b in zebrafish embryos passing through Zygotic Genome Activation (ZGA), we combined time-resolved mutant transcription analysis using the novel tool RNA-sense, chromatin state and phenotypic assays. We distinguish four types of embryonic enhancers, differentially regulated by the two TFs. Pou5f3 is critical for activation of enhancer types 1 and 2, which are responsible for transcription of genes involved in gastrulation and ventral genes. Pou5f3 or Sox19b prevent premature activation of type 3 and 4 enhancers, which are responsible for transcription of organogenesis regulators, differentiation factors and dorsal genes. We also show that the balance between Sox19b and Pou5f3 is important for bulk ZGA timing. Our results uncover how independent activities of maternal Pou5f3 and Sox19b add up or antagonize to determine the early gene expression repertoire. Bullet points:• Pou5f3 and Sox19b bind independently to DNA • Disbalance between maternal Pou5f3 and Sox19b delays ZGA • Pou5f3 suppresses premature transcription of neural patterning genes, activated by SoxB1 factors • Pou5f3 and Sox19b synergistically suppress premature transcription of a wide range of differentiation genes • Pou5f3 and Sox19b restrict the dorsal organizer

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Progesterone modulates microtubule dynamics and epiboly progression during zebrafish gastrulation

Cited by 13 publications

References 63 publications

A cargo model of yolk syncytial nuclear migration during zebrafish epiboly

A cargo model of yolk syncytial nuclear migration during zebrafish epiboly

MondoA regulates gene expression in cholesterol biosynthesis-associated pathways required for zebrafish epiboly

Pluripotency factors determine gene expression repertoire at zygotic genome activation

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