Communication between distant epithelial cells by filopodia-like protrusions during embryonic development

Sagar,; Pröls, Felicitas; Wiegreffe, Christoph; Scaal, Martin

doi:10.1242/dev.115964

“…For example, cytonemes help mediate Hedgehog signaling in fly (Bischoff et al, 2013;Kornberg and Roy, 2014). Similarly, in vertebrate embryos, long filopodia convey Shh in the developing limb bud and Wnt in the dorsal side of somites (Sanders et al, 2013;Sagar et al, 2015). We demonstrated the localization of Shh and Smo around filopodia in somite epithelial cells and provide supporting data for the requirement of filopodia for activation of the Shh signaling pathway (Fig.…”

Section: Role Of Basal Filopodia In Somite Morphogenesissupporting

confidence: 74%

Basal filopodia and vascular mechanical stress organize fibronectin into pillars bridging the mesoderm-endoderm gap

Sato

¹

,

Nagatoshi

²

,

Hamano

³

et al. 2017

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Cells may exchange information with other cells and tissues by exerting forces on the extracellular matrix (ECM). Fibronectin (FN) is an important ECM component that forms fibrils through cell contacts and creates directionally biased geometry. Here, we demonstrate that FN is deposited as pillars between widely separated germ layers, namely the somitic mesoderm and the endoderm, in quail embryos. Alongside the FN pillars, long filopodia protrude from the basal surfaces of somite epithelial cells. Loss-of-function of Ena/VASP, α5β1-integrins or talin in the somitic cells abolished the FN pillars, indicating that FN pillar formation is dependent on the basal filopodia through these molecules. The basal filopodia and FN pillars are also necessary for proper somite morphogenesis. We identified a new mechanism contributing to FN pillar formation by focusing on cyclic expansion of adjacent dorsal aorta. Maintenance of the directional alignment of the FN pillars depends on pulsatile blood flow through the dorsal aortae. These results suggest that the FN pillars are specifically established through filopodia-mediated and pulsating force-related mechanisms.

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“…It has previously been reported that dorsal epithelial cells in the somites protrude filopodia toward ectoderm during segmentation (S0 level; Martins et al, 2009) and myotome differentiation (SVIII level; Sagar et al, 2015). Our study demonstrates that ventral somite epithelial cells protrude filopodia toward endoderm (S0 to VI levels, Fig.…”

Section: Spatiomechanical Organization Of Fn Pillars In the Somiteendsupporting

confidence: 72%

Basal filopodia and vascular mechanical stress organize fibronectin into pillars bridging the mesoderm-endoderm gap

Sato¹,

Nagatoshi²,

Hamano³

et al. 2017

Journal of Cell Science

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Cells may exchange information with other cells and tissues by exerting forces on the extracellular matrix (ECM). Fibronectin (FN) is an important ECM component that forms fibrils through cell contacts and creates directionally biased geometry. Here, we demonstrate that FN is deposited as pillars between widely separated germ layers, namely the somitic mesoderm and the endoderm, in quail embryos. Alongside the FN pillars, long filopodia protrude from the basal surfaces of somite epithelial cells. Loss-of-function of Ena/VASP, α5β1-integrins or talin in the somitic cells abolished the FN pillars, indicating that FN pillar formation is dependent on the basal filopodia through these molecules. The basal filopodia and FN pillars are also necessary for proper somite morphogenesis. We identified a new mechanism contributing to FN pillar formation by focusing on cyclic expansion of adjacent dorsal aorta. Maintenance of the directional alignment of the FN pillars depends on pulsatile blood flow through the dorsal aortae. These results suggest that the FN pillars are specifically established through filopodia-mediated and pulsating force-related mechanisms.

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“…For instance, myoblast progenitors of flight muscles have been shown to send out cytonemes that contain the Wnt receptor Frizzled (Frz) and contact the Wnt-producing cells in the wing imaginal disc; the resulting Wnt-Frz complexes then move in a retrograde manner along the dynamic myoblast cytonemes (Huang and Kornberg, 2015). Similarly, the Wnt receptor Frz7 has been identified on the filopodia of dermomyotome cells in chicken (Sagar et al, 2015). Taken together, there is increasing evidence, suggesting that a conserved filopodia-based mechanism contributes to the distribution of both Wnt ligands and their receptors during development of vertebrate and invertebrates.…”

Section: Wnt Cytonemes In Developmentmentioning

confidence: 99%

“…Concomitantly, the Wnt receptor Frz was identified on cytonemes to enable the retrograde transport of Wnt proteins on these protrusions during flight muscle formation in Drosophila (Huang and Kornberg, 2015). In chicken, Frz7 was found on extensions that are positive for actin and microtubules during dermomyotome development (Sagar et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Role of cytonemes in Wnt transport

Stanganello

¹

,

Scholpp

²

2016

Journal of Cell Science

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Wnt signaling regulates a broad variety of processes during embryonic development and disease. A hallmark of the Wnt signaling pathway is the formation of concentration gradients by Wnt proteins across responsive tissues, which determines cell fate in invertebrates and vertebrates. To fulfill its paracrine function, trafficking of the Wnt morphogen from an origin cell to a recipient cell must be tightly regulated. A variety of models have been proposed to explain the extracellular transport of these lipid-modified signaling proteins in the aqueous extracellular space; however, there is still considerable debate with regard to which mechanisms allow the precise distribution of ligand in order to generate a morphogenetic gradient within growing tissue. Recent evidence suggests that Wnt proteins are distributed along signaling filopodia during vertebrate and invertebrate embryogenesis. Cytoneme-mediated transport has profound impact on our understanding of how Wnt signaling propagates through tissues and allows the formation of a precise ligand distribution in the recipient tissue during embryonic growth. In this Commentary, we review extracellular trafficking mechanisms for Wnt proteins and discuss the growing evidence of cytoneme-based Wnt distribution in development and stem cell biology. We will also discuss their implication for Wnt signaling in the formation of the Wnt morphogenetic gradient during tissue patterning.

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Communication between distant epithelial cells by filopodia-like protrusions during embryonic development

Cited by 92 publications

References 25 publications

Basal filopodia and vascular mechanical stress organize fibronectin into pillars bridging the mesoderm-endoderm gap

Basal filopodia and vascular mechanical stress organize fibronectin into pillars bridging the mesoderm-endoderm gap

Basal filopodia and vascular mechanical stress organize fibronectin into pillars bridging the mesoderm-endoderm gap

Role of cytonemes in Wnt transport

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