Cooperative Wnt-Nodal Signals Regulate the Patterning of Anterior Neuroectoderm

Yaguchi, Junko; Takeda, Noriyo; Inaba, Kazuo; Yaguchi, Shunsuke

doi:10.1371/journal.pgen.1006001

Cited by 37 publications

(59 citation statements)

References 62 publications

(120 reference statements)

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“…Therefore, to focus on the specific function of Nodal, we used a morpholino oligonucleotide against nodal (Nodal‐MO) to block its translation and then determined the expression of the four genes. Several works have reported on the radialized morphology, significant decrease of ventrally expressed TGF‐β family genes, and radially distributed serotonergic neurons in Nodal morphants in other species, such as in H. pulcherrimus (Figure b,d,h,j,l) (Yaguchi et al., ), and a similar radialized phenotype, lack of gene expressions (Figure Y–f), and serotonergic neural patterns (Figure a,c,g,i,k) were obtained in T. reevesii by injecting Nodal‐MO; thus, the morpholino used in this experiment was supposed to be sufficiently specific to block translation of nodal , which showed that the Nodal‐deficient effect was conserved beyond species. In Nodal morphants, nodal and the other three TGF‐β genes were not expressed in blastula stages (Figure Y–f), which indicated that the expression of all four genes depended on Alk4/5/7 activity and the ligand was likely Nodal.…”

Section: Resultssupporting

confidence: 54%

“…Based on previous works using four different sea urchin species, Strongylocentrotus purpuratus , Paracentrotus lividus , Lytechinus variegatus , and H. pulcherrimus , the dorsal–ventral axis formation is regulated by the combinational functions of Nodal, Lefty, BMP2/4, and Chordin, which are all expressed at the ventral ectoderm during early embryogenesis of sea urchins (Bradham et al., ; Coffman, McCarthy, Dickey‐Sims, & Robertson, ; Duboc, Röttinger, Besnardeau, & Lepage, ; Flowers, Courteau, Poustka, Weng, & Venuti, ; Nam et al., ; Yaguchi et al., ). This observation suggests that embryos of T. reevesii also use the same system to establish the dorsal–ventral polarity because of the similar shapes of the embryonic/larval body.…”

Section: Resultsmentioning

confidence: 99%

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Transforming growth factor‐β signal regulates gut bending in the sea urchin embryo

Suzuki

Yaguchi

2018

Dev Growth Differ

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During gastrulation, one of the most important morphogenetic events in sea urchin embryogenesis, the gut bends toward the ventral side to form an open mouth. Although the involvement of transforming growth factor-β (TGF-β) signals in the cell-fate specification of the ectoderm and endoderm along the dorsal-ventral axis has been well reported, it remains unclear what controls the morphogenetic behavior of gut bending. Here, using two sea urchin species, Hemicentrotus pulcherrimus and Temnopleurus reevesii, we show that TGF-β signals are required for gut bending toward the ventral side. To search for the common morphogenetic cue in these two species, we initially confirmed the expression patterns of the dorsal-ventral regulatory TGF-β members, nodal, lefty, bmp2/4, and chordin, in T. reevesii because these factors are appropriate candidates to investigate the cue that starts gut bending, although genetic information about the body axes is entirely lacking in this species. Based on their expression patterns and a functional analysis of Nodal, the dorsal-ventral axis formation of T. reevesii is likely regulated by these TGF-β members, as in other sea urchins. When the Alk4/5/7 signal was inhibited by its specific inhibitor, SB431542, before the late gastrula stage of T. reevesii, the gut was extended straight toward the anterior tip region, although the ectodermal dorsal-ventral polarity was normal. By contrast, H. pulcherrimus gut bending was sensitive to SB431542 until the prism stage. These data clearly indicate that gut bending is commonly dependent on a TGF-β signal in sea urchins, but the timing of the response varies in different species.

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Section: Resultssupporting

confidence: 54%

Section: Resultsmentioning

confidence: 99%

Transforming growth factor‐β signal regulates gut bending in the sea urchin embryo

Suzuki

Yaguchi

2018

Dev Growth Differ

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“…We confirmed that NANOG was sustained by GSK3β inhibition at early stage of differentiation via WNT signaling ( Figure 4E). Wnt signaling is also important to regulate neural patterning through forming morphogen gradients with other signal factors (7,(51)(52)(53). Our data then extend the role of NANOG in patterning the regional specified neural precursors at early stage of differentiation.…”

supporting

confidence: 69%

Antagonism between the transcription factors NANOG and OTX2 specifies rostral or caudal cell fate during neural patterning transition

Zhang

Liao

et al. 2018

Journal of Biological Chemistry

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During neurogenesis, neural patterning is a critical step during which neural progenitor cells (NPCs) differentiate into neurons with distinct functions. However, the molecular determinants that regulate neural patterning remain poorly understood. Here, we optimized the "dual-SMAD inhibition" method to specifically promote differentiation of human pluripotent stem cells (hPSCs) into forebrain and hindbrain NPCs along the rostral-caudal (R-C) axes. We report that neural patterning determination occurs at the very early stage in this differentiation. Undifferentiated hPSCs expressed basal levels of the transcription factor orthodenticle homeobox 2 (OTX2) that dominantly drove hPSCs into the "default" rostral fate at the beginning of differentiation. Inhibition of glycogen synthase kinase 3β (GSK3β) through CHIR99021 (CHIR) application sustained transient expression of the transcription factor NANOG at early differentiation stages through Wnt signaling. Wnt signaling and NANOG antagonized OTX2 and in the later stages of differentiation, switched the default rostral cell fate to the caudal one. Our findings have uncovered a mutual antagonism between NANOG and OTX2 underlying cell fate decisions during neural patterning, critical for the regulation of early neural development in humans.The embryonic neurodevelopment is a spatiotemporally regulated process, during which http://www.jbc.org/ Downloaded from 2 distinct cell fates are progressively restricted based on spatial regions (1, 2). At early stage of neurogenesis, the specified neural ectoderm divides into functionally distinct cell fates along the anterior-posterior (A-P) and dorsal-ventral (D-V) axes (3). This neural patterning process is a critical step to specify different neural precursors such as forebrain, midbrain, hindbrain and spinal cord. It has been known that the neural patterning is induced by the temporal and special morphogen gradients along the A-P and D-V axes (4, 5). These morphogens, including BMPs, WNTs, FGFs, RA and SHH (sonic hedgehog), coordinate and form gradients to specify regionally transcriptional program and distinct neural progenitors (6-10). However, the precise timing and mechanisms underlying morphogeninduced neuraxial patterning has not been fully elucidated in mammals, especially in human.Human pluripotent stem cells (hPSCs), including embryonic stem cells (ESCs) and induced pluripotent stem cells (iPSC) could differentiate into neuroepithelial cells , regionally specified neural precursor cells (11-16), thus provides a valuable model to investigate molecular determinants on neural patterning in human background. The mostly used method to induce neural differentiation in hPSCs is through suppression of both TGFβ and BMP signaling (17,18). Dual-inhibition of SMAD-dependent TGF-β and BMP signaling by their inhibitors (SB431542 and Noggin), or SB431542 and Dorsomorphin can efficiently trigger hPSCs differentiation into NPCs (19-21). Dual-SMAD inhibition triggered NPCs are believed to be more close to the anterior forebrai...

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“…For example, “Reagents for microinjection” shows how to prepare the reagents for microinjection into the eggs of H. pulcherrimus . Based on the published data for H. pulcherrimus , the effective concentrations of morpholino oligo‐nucleotides (MO) to knockdown genes are between 100 μmol/L (e.g., Nodal‐MO1) (Yaguchi et al., ) and 3.8 mmol/L (e.g., Wnt7‐MO1)(Yaguchi, Takeda, Inaba, & Yaguchi, ) so far. These experimental concentrations shown in the protocol produced healthy morphants.…”

Section: Resultsmentioning

confidence: 99%

HpBase: A genome database of a sea urchin, Hemicentrotus pulcherrimus

et al. 2018

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To understand the mystery of life, it is important to accumulate genomic information for various organisms because the whole genome encodes the commands for all the genes. Since the genome of Strongylocentrotus purpratus was sequenced in 2006 as the first sequenced genome in echinoderms, the genomic resources of other North American sea urchins have gradually been accumulated, but no sea urchin genomes are available in other areas, where many scientists have used the local species and reported important results. In this manuscript, we report a draft genome of the sea urchin Hemincentrotus pulcherrimus because this species has a long history as the target of developmental and cell biology in East Asia. The genome of H. pulcherrimus was assembled into 16,251 scaffold sequences with an N50 length of 143 kbp, and approximately 25,000 genes were identified in the genome. The size of the genome and the sequencing coverage were estimated to be approximately 800 Mbp and 100×, respectively. To provide these data and information of annotation, we constructed a database, HpBase (http://cell-innovation.nig.ac.jp/Hpul/). In HpBase, gene searches, genome browsing, and blast searches are available. In addition, HpBase includes the "recipes" for experiments from each lab using H. pulcherrimus. These recipes will continue to be updated according to the circumstances of individual scientists and can be powerful tools for experimental biologists and for the community. HpBase is a suitable dataset for evolutionary, developmental, and cell biologists to compare H. pulcherrimus genomic information with that of other species and to isolate gene information.

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Cooperative Wnt-Nodal Signals Regulate the Patterning of Anterior Neuroectoderm

Cited by 37 publications

References 62 publications

Transforming growth factor‐β signal regulates gut bending in the sea urchin embryo

Transforming growth factor‐β signal regulates gut bending in the sea urchin embryo

Antagonism between the transcription factors NANOG and OTX2 specifies rostral or caudal cell fate during neural patterning transition

HpBase: A genome database of a sea urchin, Hemicentrotus pulcherrimus

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