Alterations of the cytoskeleton in all three embryonic lineages contribute to the epiboly defect of Pou5f1/Oct4 deficient MZspg zebrafish embryos

Lachnit, Martina; Kur, Esther; Driever, Wolfgang

doi:10.1016/j.ydbio.2007.10.008

Cited by 91 publications

(118 citation statements)

References 61 publications

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“…Interestingly, MZ zebrafish mutants of the atypical cadherin Dachsous 1b (Dchs1b) display similar voids in the YCL actin and microtubule cytoskeleton and slow epiboly progression (Li-Villarreal et al, 2015). A similar defect is observed in MZ pou5f3 zebrafish mutant embryos, where a loss of the YCL itself is associated with the microtubule gaps (Lachnit et al, 2008). We also observe abnormalities of the yolk cortex (e.g.…”

Section: Discussion Ctsba Endopeptidase Function In Developmentsupporting

confidence: 52%

Split top: A maternal cathepsin B that regulates dorsoventral patterning and morphogenesis

et al. 2016

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The vertebrate embryonic dorsoventral axis is established and patterned by Wnt and bone morphogenetic protein (BMP) signaling pathways, respectively. Whereas Wnt signaling establishes the dorsal side of the embryo and induces the dorsal organizer, a BMP signaling gradient patterns tissues along the dorsoventral axis. Early Wnt signaling is provided maternally, whereas BMP ligand expression in the zebrafish is zygotic, but regulated by maternal factors. Concomitant with BMP activity patterning dorsoventral axial tissues, the embryo also undergoes dramatic morphogenetic processes, including the cell movements of gastrulation, epiboly and dorsal convergence. Although the zygotic regulation of these cell migration processes is increasingly understood, far less is known of the maternal regulators of these processes. Similarly, the maternal regulation of dorsoventral patterning, and in particular the maternal control of ventral tissue specification, is poorly understood. We identified split top, a recessive maternal-effect zebrafish mutant that disrupts embryonic patterning upstream of endogenous BMP signaling. Embryos from split top mutant females exhibit a dorsalized embryonic axis, which can be rescued by BMP misexpression or by derepressing endogenous BMP signaling. In addition to dorsoventral patterning defects, split top mutants display morphogenesis defects that are both BMP dependent and independent. These morphogenesis defects include incomplete dorsal convergence, delayed epiboly progression and an early lysis phenotype during gastrula stages. The latter two morphogenesis defects are associated with disruption of the actin and microtubule cytoskeleton within the yolk cell and defects in the outer enveloping cell layer, which are both known mediators of epiboly movements. Through chromosomal mapping and RNA sequencing analysis, we identified the lysosomal endopeptidase cathepsin Ba (ctsba) as the gene deficient in split top embryos. Our results identify a novel role for Ctsba in morphogenesis and expand our understanding of the maternal regulation of dorsoventral patterning.

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Section: Discussion Ctsba Endopeptidase Function In Developmentsupporting

confidence: 52%

Split top: A maternal cathepsin B that regulates dorsoventral patterning and morphogenesis

et al. 2016

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“…Formation of the YSL is one of the earliest differentiation events in the embryo and plays a vital role in embryo development: The YSL is crucial in regulating dorso-anterior axis formation (2)(3)(4)(5)(6), epiboly movements involved in embryo patterning and morphogenesis (7)(8)(9)(10)(11)(12), and cardiac progenitor cell movements (13).…”

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confidence: 99%

Solute carrier family 3 member 2 (Slc3a2) controls yolk syncytial layer (YSL) formation by regulating microtubule networks in the zebrafish embryo

Takesono

Moger

Farooq

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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The yolk syncytial layer (YSL) in the zebrafish embryo is a multinucleated syncytium essential for embryo development, but the molecular mechanisms underlying YSL formation remain largely unknown. Here we show that zebrafish solute carrier family 3 member 2 (Slc3a2) is expressed specifically in the YSL and that slc3a2 knockdown causes severe YSL defects including clustering of the yolk syncytial nuclei and enhanced cell fusion, accompanied by disruption of microtubule networks. Expression of a constitutively active RhoA mimics the YSL phenotypes caused by slc3a2 knockdown, whereas attenuation of RhoA or ROCK activity rescues the slc3a2 -knockdown phenotypes. Furthermore, slc3a2 knockdown significantly reduces tyrosine phosphorylation of c-Src, and overexpression of a constitutively active Src restores the slc3a2 -knockdown phenotypes. Our data demonstrate a signaling pathway regulating YSL formation in which Slc3a2 inhibits the RhoA/ROCK pathway via phosphorylation of c-Src to modulate YSL microtubule dynamics. This work illuminates processes at a very early stage of zebrafish embryogenesis and more generally informs the mechanism of cell dynamics during syncytium formation.

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“…Epiboly movements, yolk syncytial layer formation and axonal transport are all processes that require an intact microtubule cytoskeleton (Du et al, 2012;Guzik and Goldstein, 2004;Hsu et al, 2006;Lachnit et al, 2008;Solnica-Krezel and Driever, 1994;Strahle and Jesuthasan, 1993;Takesono et al, 2012). Parallel microtubule arrays in early zebrafish embryos were first described by Jesuthasan and Strahle (Jesuthasan and Strahle, 1997), by Tubulin immunostaining in fixed embryos.…”

Section: Introductionmentioning

confidence: 99%

Dynamic microtubules at the vegetal cortex predict the embryonic axis in zebrafish

et al. 2012

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SUMMARYIn zebrafish, as in many animals, maternal dorsal determinants are vegetally localized in the egg and are transported after fertilization in a microtubule-dependent manner. However, the organization of early microtubules, their dynamics and their contribution to axis formation are not fully understood. Using live imaging, we identified two populations of microtubules, perpendicular bundles and parallel arrays, which are directionally oriented and detected exclusively at the vegetal cortex before the first cell division. Perpendicular bundles emanate from the vegetal cortex, extend towards the blastoderm, and orient along the animal-vegetal axis. Parallel arrays become asymmetric on the vegetal cortex, and orient towards dorsal. We show that the orientation of microtubules at 20 minutes post-fertilization can predict where the embryonic dorsal structures in zebrafish will form. Furthermore, we find that parallel microtubule arrays colocalize with wnt8a RNA, the candidate maternal dorsal factor. Vegetal cytoplasmic granules are displaced with parallel arrays by ~20°, providing in vivo evidence of a cortical rotation-like process in zebrafish. Cortical displacement requires parallel microtubule arrays, and probably contributes to asymmetric transport of maternal determinants. Formation of parallel arrays depends on Ca 2+ signaling. Thus, microtubule polarity and organization predicts the zebrafish embryonic axis. In addition, our results suggest that cortical rotation-like processes might be more common in early development than previously thought.

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Alterations of the cytoskeleton in all three embryonic lineages contribute to the epiboly defect of Pou5f1/Oct4 deficient MZspg zebrafish embryos

Cited by 91 publications

References 61 publications

Split top: A maternal cathepsin B that regulates dorsoventral patterning and morphogenesis

Split top: A maternal cathepsin B that regulates dorsoventral patterning and morphogenesis

Solute carrier family 3 member 2 (Slc3a2) controls yolk syncytial layer (YSL) formation by regulating microtubule networks in the zebrafish embryo

Dynamic microtubules at the vegetal cortex predict the embryonic axis in zebrafish

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