Xenopus Dusp6 modulates FGF signaling to precisely pattern pre-placodal ectoderm

Tsukano, Kohei; Yamamoto, Takayoshi; Watanabe, Tomoko; Michiue, Tatsuo

doi:10.1016/j.ydbio.2022.05.009

Cited by 6 publications

(2 citation statements)

References 62 publications

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“…mechanism (s) to establish localized activation of morphogenmediated signaling have been proposed. For instance, this is achieved by intracellular positive or negative feedback regulation (eldar et al, 2003;Tsukano et al, 2022;watanabe et al, 2018;yamamoto et al, 2022), and accumulation of a ligand by expressing a type of heparan sulfate (han et al, 2005; yamamoto et al, 2023b; yamamoto et al, 2023) in specific cells. We propose that mechanical force serves as an additional mechanism to locally activate signaling pathways, i.e., activating them only in a region (nc) adjacent to a shrinking region (nP).…”

Section: Discussionmentioning

confidence: 99%

Enhancement of neural crest formation by mechanical force in Xenopus development

Kaneshima,

Ogawa,

Yamamoto

et al. 2024

Int. J. Dev. Biol.

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In vertebrate development, ectoderm is specified into neural plate (NP), neural plate border (NPB), and epidermis. Although such patterning is thought to be achieved by molecular concentration gradients, it has been revealed, mainly by in vitro analysis, that mechanical force can regulate cell specification. During in vivo patterning, cells deform and migrate, and this applies force to surrounding tissues, shaping the embryo. However, the role of mechanical force for cell specification in vivo is largely unknown. In this study, with an aspiration assay and atomic force microscopy, we have demonstrated that tension on ectodermal cells decreases laterally from the midline in Xenopus early neurula. Ectopically applied force laterally expanded the neural crest (NC) region, a derivative of the NPB, whereas force relaxation suppressed it. Furthermore, force application activated both the FGF and Wnt pathways, which are required for NC formation during neuroectodermal patterning. Taken together, mechanical force is necessary for NC formation in order to regulate signaling pathways. Furthermore, molecular signals specify the NP and generate force on neighboring tissue, the NPB, with its closure. This force activates signals, possibly determining the appropriate width of a narrow tissue, the NC.

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Section: Discussionmentioning

confidence: 99%

Enhancement of neural crest formation by mechanical force in Xenopus development

Kaneshima,

Ogawa,

Yamamoto

et al. 2024

Int. J. Dev. Biol.

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show abstract

“…Neural tissue comprises many types of cells that are derived from neural plate (NP), neural crest (NC), or preplacodal ectoderm (PPE) (Grocott et al, 2012; Thawani & Groves, 2020). These differentiation processes are regulated by multiple morphogens, such as Wnt, BMP, and FGF (Ozair et al, 2013; Rogers et al, 2009; Schlosser, 2014; Stern, 2006; Tsukano et al, 2022; Yamamoto et al., 2023). However, it remains unclear how these processes are precisely regulated by diffusing molecules.…”

Section: Introductionmentioning

confidence: 99%

Ndst1, a heparan sulfate modification enzyme, regulates neuroectodermal patterning by enhancing Wnt signaling in Xenopus

et al. 2023

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Neural tissue is derived from three precursor regions: neural plate, neural crest, and preplacodal ectoderm. These regions are determined by morphogen-mediated signaling.Morphogen distribution is generally regulated by binding to an extracellular matrix component, heparan sulfate (HS) proteoglycan. HS is modified by many enzymes, such as Ndeacetyl sulfotransferase 1 (Ndst1), which is highly expressed in early development.However, functions of HS modifications in ectodermal patterning are largely unknown.In this study, we analyzed the role of Ndst1 using Xenopus embryos. We found that ndst1 was expressed in anterior neural plate and the trigeminal region at the neurula stage. ndst1 overexpression expanded the neural crest (NC) region, whereas translational inhibition reduced not only the trigeminal region, but also the adjacent NC region, especially the anterior part. At a later stage, ndst1 knocked-down embryos showed defects in cranial ganglion formation. We also found that Ndst1 activates Wnt signaling pathway at the neurula stage. Taken together, our results suggest that N-sulfonated HS accumulates Wnt ligand and activates Wnt signaling in ndst1-expressing cells, but that it inhibits signaling in non-ndst1-expressing cells, leading to proper neuroectodermal patterning.

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The heparan sulfate modification enzyme, Hs6st1, governs Xenopus neuroectodermal patterning by regulating distributions of Fgf and Noggin

Yamamoto

Kaneshima

Tsukano

et al. 2023

Developmental Biology

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Xenopus Dusp6 modulates FGF signaling to precisely pattern pre-placodal ectoderm

Cited by 6 publications

References 62 publications

Enhancement of neural crest formation by mechanical force in Xenopus development

Enhancement of neural crest formation by mechanical force in Xenopus development

Ndst1, a heparan sulfate modification enzyme, regulates neuroectodermal patterning by enhancing Wnt signaling in Xenopus

The heparan sulfate modification enzyme, Hs6st1, governs Xenopus neuroectodermal patterning by regulating distributions of Fgf and Noggin

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