Differential distribution of competence for panplacodal and neural crest induction to non-neural and neural ectoderm

Pieper, Mareike; Ahrens, Katja; Rink, Elke; Peter, Annette; Schlosser, Gerhard

doi:10.1242/dev.074468

Cited by 89 publications

(176 citation statements)

References 72 publications

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“…Subsequently, Dlx3b/4b, which is able to initiate otic induction in the absence of Foxi1, represses neuronal and imposes sensory fate by the activation of atoh1b. Consistently, it has been shown that neuronal differentiation is repressed after overexpression of Dlx3 (Pieper et al, 2012). However, although sensory hair cell formation is completely abolished and neuronal fate is increased in Dlx3b/4b-depleted embryos, nonsensory epithelial cells are still present and give rise to a size-reduced otic vesicle.…”

Section: Research Articlesupporting

confidence: 53%

Zebrafish Foxi1 provides a neuronal ground state during inner ear induction preceding the Dlx3b/4b-regulated sensory lineage

2013

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SUMMARYVertebrate inner ear development is a complex process that involves the induction of a common territory for otic and epibranchial precursors and their subsequent segregation into otic and epibranchial cell fates. In zebrafish, the otic-epibranchial progenitor domain (OEPD) is induced by Fgf signaling in a Foxi1-and Dlx3b/4b-dependent manner, but the functional differences of Foxi1 and Dlx3b/4b in subsequent cell fate specifications within the developing inner ear are poorly understood. Based on pioneer tracking (PioTrack), a novel Cre-dependent genetic lineage tracing method, and genetic data, we show that the competence to embark on a neuronal or sensory fate is provided sequentially and very early during otic placode induction. Loss of Foxi1 prevents neuronal precursor formation without affecting hair cell specification, whereas loss of Dlx3b/4b inhibits hair cell but not neuronal precursor formation. Consistently, in Dlx3b/4b-and Sox9a-deficient b380 mutants almost all otic epithelial fates are absent, including sensory hair cells, and the remaining otic cells adopt a neuronal fate. Furthermore, the progenitors of the anterior lateral line ganglia also arise from the OEPD in a Foxi1-dependent manner but are unaffected in the absence of Dlx3b/4b or in b380 mutants. Thus, in addition to otic fate Foxi1 provides neuronal competence during OEPD induction prior to and independently of the Dlx3b/4b-mediated sensory fate of the developing inner ear.

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Section: Research Articlesupporting

confidence: 53%

Zebrafish Foxi1 provides a neuronal ground state during inner ear induction preceding the Dlx3b/4b-regulated sensory lineage

2013

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“…3j), suggesting that, like in vertebrates [33][34][35] , axin expression is dependent on Wnt/b-catenin pathway activity in Platynereis. This latter conclusion is reinforced by the observation of a very strong increase in the expression of Pduaxin in embryos treated with azakenpaullone, an inhibitor of glycogen synthase kinase-3 that constitutively activates the Wnt/ b-catenin pathway 31,36,37 ( Supplementary Fig. S7).…”

Section: Resultsmentioning

confidence: 85%

Involvement of the Wnt/β-catenin pathway in neurectoderm architecture in Platynereis dumerilii

et al. 2013

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Signalling pathways are essential for the correct development of the central nervous system (CNS) in bilaterian animals. Here we show that in the CNS of the annelid Platynereis dumerilii, neural progenitor cells (NPCs) are located close to the ventral midline and express axin, a negative regulator of the Wnt/b-catenin pathway. Using pharmacological inhibitors, we observe that Wnt/b-catenin is required for the transition between proliferating NPCs and differentiating neurons. We also show that the Rho-associated kinase (Rok) is necessary for neurectoderm morphogenesis and ventral midline formation, and indirectly affects the distribution of the NPCs and the development of axonal scaffolds. Moreover, seven genes belonging to the planar cell polarity (PCP) pathway are expressed in the developing Platynereis neurectoderm, suggesting an involvement in its morphogenesis. When compared with previous studies in vertebrates, our data suggest that the involvement of the Wnt/b-catenin pathway in the control of neural cell proliferation/differentiation is ancestral to bilaterians.

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“…3D,E; Leung et al, 2013) further supporting the idea that segregation of NC and cranial placode fates occurs very early in our cultures. It has been suggested that NC competence segregates with the neuralized domain of the ectoderm (Pieper et al, 2012;Schlosser, 2008). We have examined the expression dynamics of a number of neural-related transcripts, including LHX2, PAX6, SOX1, SOX2, OTX2 and HES5 (Greber et al, 2011;Hou et al, 2013;Zhang et al, 2010).…”

Section: Discussionmentioning

confidence: 99%

WNT/β-catenin signaling mediates human neural crest induction via a pre-neural border intermediate

et al. 2016

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Neural crest (NC) cells arise early in vertebrate development, migrate extensively and contribute to a diverse array of ectodermal and mesenchymal derivatives. Previous models of NC formation suggested derivation from neuralized ectoderm, via meso-ectodermal, or neural-non-neural ectoderm interactions. Recent studies using bird and amphibian embryos suggest an earlier origin of NC, independent of neural and mesodermal tissues. Here, we set out to generate a model in which to decipher signaling and tissue interactions involved in human NC induction. Our novel human embryonic stem cell (ESC)-based model yields high proportions of multipotent NC cells (expressing SOX10, PAX7 and TFAP2A) in 5 days. We demonstrate a crucial role for WNT/β-catenin signaling in launching NC development, while blocking placodal and surface ectoderm fates. We provide evidence of the delicate temporal effects of BMP and FGF signaling, and find that NC development is separable from neural and/ or mesodermal contributions. We further substantiate the notion of a neural-independent origin of NC through PAX6 expression and knockdown studies. Finally, we identify a novel pre-neural border state characterized by early WNT/β-catenin signaling targets that displays distinct responses to BMP and FGF signaling from the traditional neural border genes. In summary, our work provides a fast and efficient protocol for human NC differentiation under signaling constraints similar to those identified in vivo in model organisms, and strengthens a framework for neural crest ontogeny that is separable from neural and mesodermal fates.

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Differential distribution of competence for panplacodal and neural crest induction to non-neural and neural ectoderm

Cited by 89 publications

References 72 publications

Zebrafish Foxi1 provides a neuronal ground state during inner ear induction preceding the Dlx3b/4b-regulated sensory lineage

Zebrafish Foxi1 provides a neuronal ground state during inner ear induction preceding the Dlx3b/4b-regulated sensory lineage

Involvement of the Wnt/β-catenin pathway in neurectoderm architecture in Platynereis dumerilii

WNT/β-catenin signaling mediates human neural crest induction via a pre-neural border intermediate

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