Zic1 controls placode progenitor formation non-cell autonomously by regulating retinoic acid production and transport

Jaurena, Maria Belen; Juraver-Geslin, Hugo; Devotta, Arun; Saint-Jeannet, Jean Pierre

doi:10.1038/ncomms8476

Cited by 29 publications

(64 citation statements)

References 61 publications

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“…3E, F). Consistent with reports that zic1 is required for placode gene expression (Hong and Saint-Jeannet, 2007; Jaurena et al, 2015), in no case was ectopic neural plate expression of six1 detected (Fig. 3G).…”

Section: Resultssupporting

confidence: 92%

Wbp2nl has a developmental role in establishing neural and non-neural ectodermal fates

Marchak

Grant

Neilson

et al. 2017

Developmental Biology

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In many animals, maternally synthesized mRNAs are critical for primary germ layer formation. In Xenopus, several maternal mRNAs are enriched in the animal blastomere progenitors of the embryonic ectoderm. We previously identified one of these, WW-domain binding protein 2 N-terminal like (wbp2nl), that others previously characterized as a sperm protein (PAWP) that promotes meiotic resumption. Herein we demonstrate that it has an additional developmental role in regionalizing the embryonic ectoderm. Knock-down of Wbp2nl in the dorsal ectoderm reduced cranial placode and neural crest gene expression domains and expanded neural plate domains; knock-down in ventral ectoderm reduced epidermal gene expression. Conversely, increasing levels of Wbp2nl in the neural plate induced ectopic epidermal and neural crest gene expression and repressed many neural plate and cranial placode genes. The effects in the neural plate appear to be mediated, at least in part, by down-regulating chd, a BMP antagonist. Because the cellular function of Wbp2nl is not known, we mutated several predicted motifs. Expressing mutated proteins in embryos showed that a putative phosphorylation site at Thr45 and an α-helix in the PH-G domain are required to ectopically induce epidermal and neural crest genes in the neural plate. An intact YAP-binding motif also is required for ectopic epidermal gene expression as well as for down-regulating chd. This work reveals novel developmental roles for a cytoplasmic protein that promotes epidermal and neural crest formation at the expense of neural ectoderm.

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Section: Resultssupporting

confidence: 92%

Wbp2nl has a developmental role in establishing neural and non-neural ectodermal fates

Marchak

Grant

Neilson

et al. 2017

Developmental Biology

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“…In Xenopus , both Raldh2 (enzyme catalyzing oxidation of retinaldehyde into retinoic acid) and lipocalin-type prostaglandin D2 synthase (LPDGS, regulator of RA transport) are expressed around the anterior neural plate and their expression is non-cell autonomously regulated by the zinc finger transcription factor Zic1 expressed at the anterior neural plate [90]. Another expression domain of Raldh2 identified in mice includes the POM adjacent to the temporal portion of the optic vesicle, which in this case acts in a paracrine mode towards the optic vesicle [91].…”

Section: The “Birth” Of “Visible” Lens Embryologymentioning

confidence: 99%

Signaling and Gene Regulatory Networks in Mammalian Lens Development

2017

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Ocular lens development represents an advantageous system to study regulatory mechanisms governing cell fate decisions, extracellular signaling, cell and tissue organization, and underlying gene regulatory networks. Spatiotemporaly regulated domains of BMP, FGF, and other signaling molecules in the late gastrula-early neurula stage embryos generate the border region between the neural plate and non-neural ectoderm from which multiple cell types, including lens progenitor cells, emerge and undergo initial tissue formation. Extracellular signaling and DNA-binding transcription factors govern lens and optic cup morphogenesis. Pax6, c-Maf, Hsf4, Prox1, Sox1, and a few additional factors regulate expression of the lens structural proteins, the crystallins. A multitude of cross-talks between a diverse array of signaling pathways control the complexity and order of the lens morphogenetic processes and its transparency.

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“…Anos1 was identified as a target of Pax3 and Zic1 [13,31], two important regulators of neural crest and cranial placode fates in the embryo [7–12]. anos1 is first detected at the early neurula stage at the lateral edges of the anterior neural plate, in the cranial neural crest forming region.…”

Section: Discussionmentioning

confidence: 99%

“…These growth factors in turn activate a unique repertoire of transcription factors that are responsible for initiating the differentiation program of each one of these cell populations [5,6]. Among these transcription factors, Pax3 and Zic1 are especially critical to promote neural crest and cranial placode fates [7–12]. To characterize the molecular events downstream of Pax3 and Zic1, several years ago we performed a microarray screen using Xenopus animal cap explants expressing varying combinations of these factors [13].…”

Section: Introductionmentioning

confidence: 99%

Anosmin-1 is essential for neural crest and cranial placodes formation in Xenopus

Bae

Hong

Saint-Jeannet

2018

Biochemical and Biophysical Research Communications

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During embryogenesis vertebrates develop a complex craniofacial skeleton associated with sensory organs. These structures are primarily derived from two embryonic cell populations the neural crest and cranial placodes, respectively. Neural crest cells and cranial placodes are specified through the integrated action of several families of signaling molecules, and the subsequent activation of a complex network of transcription factors. Here we describe the expression and function of Anosmin-1 (Anos1), an extracellular matrix protein, during neural crest and cranial placodes development in Xenopus laevis. Anos1 was identified as a target of Pax3 and Zic1, two transcription factors necessary and sufficient to generate neural crest and cranial placodes. Anos1 is expressed in cranial neural crest progenitors at early neurula stage and in cranial placode derivatives later in development. We show that Anos1 function is required for neural crest and sensory organs development in Xenopus, consistent with the defects observed in Kallmann syndrome patients carrying a mutation in ANOS1. These findings indicate that anos1 has a conserved function in the development of craniofacial structures, and indicate that anos1-depleted Xenopus embryos represent a useful model to analyze the pathogenesis of Kallmann syndrome.

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Zic1 controls placode progenitor formation non-cell autonomously by regulating retinoic acid production and transport

Cited by 29 publications

References 61 publications

Wbp2nl has a developmental role in establishing neural and non-neural ectodermal fates

Wbp2nl has a developmental role in establishing neural and non-neural ectodermal fates

Signaling and Gene Regulatory Networks in Mammalian Lens Development

Anosmin-1 is essential for neural crest and cranial placodes formation in Xenopus

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