Cytonemes in development

Zhang, Chengting; Scholpp, Steffen

doi:10.1016/j.gde.2019.06.005

Cited by 54 publications

(53 citation statements)

References 37 publications

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“…However, beyond the ECM layer of the basal side, the hemolymph current may disrupt any gradient of diffusive signals. Cytonemes, originally found in the fruit fly wing imaginal discs [75][76][77], have been detected on the basal side (but not the apical side) of the pupal wing epithelial cells in butterflies [45,46] and may play an important role in delivering signaling molecules to distant cells, resulting in a stable gradient of molecular morphogens. Nonmolecular (physical) morphogens, potentially in the form of a mechanical distortion signal of epithelial sheets, may require extracellular support materials to travel.…”

Section: Discussionmentioning

confidence: 99%

Butterfly eyespot color pattern formation requires physical contact of the pupal wing epithelium with extracellular materials for morphogenic signal propagation

Otaki

2020

BMC Dev Biol

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Background: Eyespot color pattern formation on butterfly wings is sensitive to physical damage and physical distortion as well as physical contact with materials on the surface of wing epithelial tissue at the pupal stage. Contact-mediated eyespot color pattern changes may imply a developmental role of the extracellular matrix in morphogenic signal propagation. Here, we examined eyespot responses to various contact materials, focusing on the hindwing posterior eyespots of the blue pansy butterfly, Junonia orithya. Results: Contact with various materials, including both nonbiological and biological materials, induced eyespot enlargement, reduction, or no change in eyespot size, and each material was characterized by a unique response profile. For example, silicone glassine paper almost always induced a considerable reduction, while glass plates most frequently induced enlargement, and plastic plates generally produced no change. The biological materials tested here (fibronectin, polylysine, collagen type I, and gelatin) resulted in various responses, but polylysine induced more cases of enlargement, similar to glass plates. The response profile of the materials was not readily predictable from the chemical composition of the materials but was significantly correlated with the water contact angle (water repellency) of the material surface, suggesting that the surface physical chemistry of materials is a determinant of eyespot size. When the proximal side of a prospective eyespot was covered with a size-reducing material (silicone glassine paper) and the distal side and the organizer were covered with a material that rarely induced size reduction (plastic film), the proximal side of the eyespot was reduced in size in comparison with the distal side, suggesting that signal propagation but not organizer activity was inhibited by silicone glassine paper. Conclusions: These results suggest that physical contact with an appropriate hydrophobic surface is required for morphogenic signals from organizers to propagate normally. The binding of the apical surface of the epithelium with an opposing surface may provide mechanical support for signal propagation. In addition to conventional molecular morphogens, there is a possibility that mechanical distortion of the epithelium that is propagated mechanically serves as a nonmolecular morphogen to induce subsequent molecular changes, in accordance with the distortion hypothesis for butterfly wing color pattern formation.

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Section: Discussionmentioning

confidence: 99%

Butterfly eyespot color pattern formation requires physical contact of the pupal wing epithelium with extracellular materials for morphogenic signal propagation

Otaki

2020

BMC Dev Biol

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“…The underlying assumption of simple diffusion of morphogens produced by source cells, which ultimately determines cell fate through the establishment of morphogen gradients, has been recently challenged due to the observation of other complex transport mechanisms [8]. Recently, a cytoneme-based transport mechanism has been linked to morphogen distribution [10]. Cytonemes are specialized filopodia that can, despite only delivering morphogens by short range directed transport, mediate long-distance signaling during development [9].…”

Section: Cytonemes As Transport Vehicle For Wnt Morphogensmentioning

confidence: 99%

“…Recent observations in other signaling systems, however, question the universality of both of these assumptions. Experiments in Drosophila and vertebrates suggest that distribution of morphogens through signaling filopodia—known as cytonemes—are a prerequisite to orchestrate patterning in quickly reorganizing developing tissue [ 8 – 10 ]. Recently, there is also evidence that cytonemes may play a further essential role in cancer progression [ 11 , 12 ].…”

Section: Introductionmentioning

confidence: 99%

Modeling of Wnt-mediated tissue patterning in vertebrate embryogenesis

et al. 2020

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During embryogenesis, morphogens form a concentration gradient in responsive tissue, which is then translated into a spatial cellular pattern. The mechanisms by which morphogens spread through a tissue to establish such a morphogenetic field remain elusive. Here, we investigate by mutually complementary simulations and in vivo experiments how Wnt morphogen transport by cytonemes differs from typically assumed diffusion-based transport for patterning of highly dynamic tissue such as the neural plate in zebrafish. Stochasticity strongly influences fate acquisition at the single cell level and results in fluctuating boundaries between pattern regions. Stable patterning can be achieved by sorting through concentration dependent cell migration and apoptosis, independent of the morphogen transport mechanism. We show that Wnt transport by cytonemes achieves distinct Wnt thresholds for the brain primordia earlier compared with diffusion-based transport. We conclude that a cytoneme-mediated morphogen transport together with directed cell sorting is a potentially favored mechanism to establish morphogen gradients in rapidly expanding developmental systems.

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“…However, a high cross-correlation amplitude indicates co-diffusion of bound Ror2-mCherry and Wnt8a-GFP and further experiments demonstrated that Wnt8a/Ror2 can activate the β-catenin-independent Wnt/PCP signalling pathway and thus promote filopodia formation (Mattes et al 2018 ). Based on the FCCS data, a further analysis showed that these filopodia are Wnt8a/Ror2-bearing protrusions—known as cytonemes—regulating extracellular Wnt dispersal (Zhang and Scholpp 2019 ; Mattes et al 2018 ).…”

Section: Introductionmentioning

confidence: 99%

Studying molecular interactions in the intact organism: fluorescence correlation spectroscopy in the living zebrafish embryo

Dawes

Soeller

Scholpp

2020

Histochem Cell Biol

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Cell behaviour and function is determined through the interactions of a multitude of molecules working in concert. To observe these molecular dynamics, biophysical studies have been developed that track single interactions. Fluorescence correlation spectroscopy (FCS) is an optical biophysical technique that non-invasively resolves single molecules through recording the signal intensity at the femtolitre scale. However, recording the behaviour of these biomolecules using in vitro-based assays often fails to recapitulate the full range of variables in vivo that directly confer dynamics. Therefore, there has been an increasing interest in observing the state of these biomolecules within living organisms such as the zebrafish Danio rerio. In this review, we explore the advancements of FCS within the zebrafish and compare and contrast these findings to those found in vitro.

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Cytonemes in development

Cited by 54 publications

References 37 publications

Butterfly eyespot color pattern formation requires physical contact of the pupal wing epithelium with extracellular materials for morphogenic signal propagation

Butterfly eyespot color pattern formation requires physical contact of the pupal wing epithelium with extracellular materials for morphogenic signal propagation

Modeling of Wnt-mediated tissue patterning in vertebrate embryogenesis

Studying molecular interactions in the intact organism: fluorescence correlation spectroscopy in the living zebrafish embryo

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