Positive feedback regulation of frizzled-7 expression robustly shapes a steep Wnt gradient in Xenopus heart development, together with sFRP1 and heparan sulfate

Yamamoto, Takayoshi; Kambayashi, Yuta; Otsuka, Yoshihisa; Afouda, Boni A.; Giuraniuc, Claudiu V.; Michiue, Tatsuo; Hoppler, Stefan

doi:10.7554/elife.73818

Cited by 11 publications

(4 citation statements)

References 43 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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“…Gradients of signaling molecules are ubiquitous in embryonic development and cellular activities, modulating cell migration, proliferation, and survival (Griffith, Sokol et al, 2014, Yamamoto, Kambayashi et al, 2022, Yu, Burkhardt et al, 2009. Chemokines, belonging to a ∼45-member family of small (8-12 kDa) proteins, are signaling molecules that can induce distinct cellular chemotaxis in response to inflammatory stimuli in a concentration-dependent gradient (Weber, Hauschild et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Heparan sulfate-dependent phase separation of CCL5 and its chemotactic activity

Yu,

Duan,

Pei

et al. 2024

eLife

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Secreted chemokines form concentration gradients in target tissues to control migratory directions and patterns of immune cells in response to inflammatory stimulation; however, how the gradients are formed is much debated. Heparan sulfate (HS) binds to chemokines and modulates their activities. In this study, we investigated the roles of HS in the gradient formation and chemoattractant activity of CCL5 that is known to bind to HS. CCL5 and heparin underwent liquid–liquid phase separation (LLPS) and formed gradient, which was confirmed using CCL5 immobilized on heparin-beads. The biological implication of HS in CCL5 gradient formation was established in CHO-K1 (wild type) and CHO-677 (lacking HS) cells by Transwell assay. The effect of HS on CCL5 chemoattractant activity was further proved by transwell assay of human peripheral blood cells. Finally, peritoneal injection of the chemokine into mice showed reduced recruitment of inflammatory cells either by mutant CCL5 (lacking heparin binding sequence) or by addition of heparin to wild type CCL5. Our experimental data propose that co-phase separation of CCL5 with HS establishes a specific chemokine concentration gradient to trigger directional cell migration. The results warrant further investigation on other heparin binding chemokines and allows for a more elaborate insight into disease process and new treatment strategies.

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“…Extracellular molecules are important regulators of morphogen distribution (Rogers & Schier, 2011; Yamamoto et al, 2022). Among them, an extracellular matrix component, heparan sulfate (HS), binds to morphogens, and restricts their diffusion (Yan & Lin, 2009).…”

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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Positive feedback regulation of frizzled-7 expression robustly shapes a steep Wnt gradient in Xenopus heart development, together with sFRP1 and heparan sulfate

Cited by 11 publications

References 43 publications

Enhancement of neural crest formation by mechanical force in Xenopus development

Enhancement of neural crest formation by mechanical force in Xenopus development

Heparan sulfate-dependent phase separation of CCL5 and its chemotactic activity

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

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