Core PCP mutations affect short time mechanical properties but not tissue morphogenesis in the Drosophila pupal wing
- Max Planck Institute of Molecular Cell Biology and Genetics, Germany
- University of Dundee, United Kingdom
- Laboratoire Physico-Chimie Curie, Institut Curie, France
- Center for Systems Biology Dresden, Germany
- Max Planck Institute for the Physics of Complex Systems, Germany
- Technische Universität Dresden, Germany
Abstract
How morphogenetic movements are robustly coordinated in space and time is a fundamental open question in biology. We study this question using the wing of Drosophila melanogaster, an epithelial tissue that undergoes large-scale tissue flows during pupal stages. Previously, we showed that pupal wing morphogenesis involves both cellular behaviors that allow relaxation of mechanical tissue stress, as well as cellular behaviors that appear to be actively patterned (Etournay et al., 2015). Here, we show that these active cellular behaviors are not guided by the core planar cell polarity (PCP) pathway, a conserved signaling system that guides tissue development in many other contexts. We find no significant phenotype on the cellular dynamics underlying pupal morphogenesis in mutants of core PCP. Furthermore, using laser ablation experiments, coupled with a rheological model to describe the dynamics of the response to laser ablation, we conclude that while core PCP mutations affect the fast timescale response to laser ablation they do not significantly affect overall tissue mechanics. In conclusion, our work shows that cellular dynamics and tissue shape changes during Drosophila pupal wing morphogenesis do not require core PCP as an orientational guiding cue.
Data availability
Source data and code are provided for each figure
Article and author information
Author details
Funding
Max Planck Society
- Romina Piscitello-Gómez
- Franz S Gruber
- Abhijeet Krishna
- Charlie Duclut
- Carl D Modes
- Marko Popović
- Frank Jülicher
- Natalie A Dye
- Suzanne Eaton
Deutsche Forschungsgemeinschaft (EXC-2068-390729961)
- Romina Piscitello-Gómez
- Abhijeet Krishna
- Carl D Modes
- Frank Jülicher
- Natalie A Dye
- Suzanne Eaton
Deutsche Forschungsgemeinschaft (SPP1782)
- Romina Piscitello-Gómez
- Franz S Gruber
- Natalie A Dye
- Suzanne Eaton
Deutsche Krebshilfe (MSNZ-P2 Dresden)
- Natalie A Dye
Austrian Academy of Sciences (DOC Fellowship)
- Franz S Gruber
Agence Nationale de la Recherche (ANR-11-LABX-0071)
- Charlie Duclut
Agence Nationale de la Recherche (ANR-18-IDEX-0001)
- Charlie Duclut
Deutsche Forschungsgemeinschaft (EA4/10-1,EA4/10-2)
- Romina Piscitello-Gómez
- Franz S Gruber
- Natalie A Dye
- Suzanne Eaton
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2023, Piscitello-Gómez et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 757
- views
-
- 169
- downloads
-
- 1
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Core PCP mutations affect short time mechanical properties but not tissue morphogenesis in the Drosophila pupal wing
eLife 12:e85581.
https://doi.org/10.7554/eLife.85581
Further reading
-
- Developmental Biology
- Neuroscience
During development axons undergo long-distance migrations as instructed by guidance molecules and their receptors, such as UNC-6/Netrin and UNC-40/DCC. Guidance cues act through long-range diffusive gradients (chemotaxis) or local adhesion (haptotaxis). However, how these discrete modes of action guide axons in vivo is poorly understood. Using time-lapse imaging of axon guidance in C. elegans, we demonstrate that UNC-6 and UNC-40 are required for local adhesion to an intermediate target and subsequent directional growth. Exogenous membrane-tethered UNC-6 is sufficient to mediate adhesion but not directional growth, demonstrating the separability of haptotaxis and chemotaxis. This conclusion is further supported by the endogenous UNC-6 distribution along the axon’s route. The intermediate and final targets are enriched in UNC-6 and separated by a ventrodorsal UNC-6 gradient. Continuous growth through the gradient requires UNC-40, which recruits UNC-6 to the growth cone tip. Overall, these data suggest that UNC-6 stimulates stepwise haptotaxis and chemotaxis in vivo.
-
- Developmental Biology
- Stem Cells and Regenerative Medicine
The purpose of these studies is to investigate how Sphingosine-1-phosphate (S1P) signaling regulates glial phenotype, dedifferentiation of Müller glia (MG), reprogramming into proliferating MG-derived progenitor cells (MGPCs), and neuronal differentiation of the progeny of MGPCs in the chick retina. We found that S1P-related genes are highly expressed by retinal neurons and glia, and levels of expression were dynamically regulated following retinal damage. Drug treatments that activate S1P receptor 1 (S1PR1) or increase levels of S1P suppressed the formation of MGPCs. Conversely, treatments that inhibit S1PR1 or decrease levels of S1P stimulated the formation of MGPCs. Inhibition of S1P receptors or S1P synthesis significantly enhanced the neuronal differentiation of the progeny of MGPCs. We report that S1P-related gene expression in MG is modulated by microglia and inhibition of S1P receptors or S1P synthesis partially rescues the loss of MGPC formation in damaged retinas missing microglia. Finally, we show that TGFβ/Smad3 signaling in the resting retina maintains S1PR1 expression in MG. We conclude that the S1P signaling is dynamically regulated in MG and MGPCs in the chick retina, and activation of S1P signaling depends, in part, on signals produced by reactive microglia.
