Mechanical control of morphogenesis robustness
Posted on: 10 February 2020
Preprint posted on 6 January 2020
Feel the force - anisotropic tissue tension, away from cell shape changes, is essential for morphogenesis robustness in Drosophila leg formation
Selected by Helen ZennerCategories: developmental biology
Feel the force – anisotropic tissue tension away from cell shape changes is essential for morphogenesis robustness in Drosophila leg formation
Background
Patterning is essential for ensuring that morphogenetic events occur with appropriate timing and position. The best known process is the specification of body plans by the Hox genes. Patterning genes are ordinally transcriptional factors that control huge gene networks, including cytoskeletal regulators, which are responsible for the downstream changes in cell behaviour and shape. More recently, research in this area has focussed on morphogenesis robustness, which refers to the idea of constraining the level of variation, in processes where variation is likely to occur. The latest preprint from the Suzanne group highlights the importance of the actin cytoskeleton in ensuring morphogenesis robustness, in a separate process to generating force in the morphogenetic event itself. The model used by Martin et al. was the Drosophila leg. During development the forming appendage must form four strictly parallel folds. How this patterning occurs has been well described and is dependent on sequential Notch activation, expression of pro-apoptotic genes, subsequent force generation by apical myosin in the apoptotic cells, resulting in constriction and tissue folding.
Findings
Using an RNAi screen, the authors found that depletion of Arp2/3 caused defects in folding, but with a highly variable array of phenotypes, making it a good candidate for involvement in morphogenesis robustness. When focussing on Arpc5 knockdown, they found no defects in Notch activation, apoptotic pattern formation, or the ability of these cells to send mechanical signals to induce the fold. In fact, they found that the folds are initially correctly positioned but then lose their way, heading for regions enriched in Myosin II (MyoII) and under high tension. These findings are recapitulated in silico, when a mechanical perturbation, in close vicinity to the fold, is introduced into a previously published computational model from the authors.
However, these regions of high tension are also present in the wild type tissue, but in this case, the fold formations are immune to its effects, indicating that isolation is required between fold domains and the rest of the tissue. The authors speculated that this isolation arises from the planar polarised enrichment of MyoII and the resulting anisotropic junctional tension, directing biased force transmission. To test whether this is important for fold formation, the authors used a non-planar polarised GFP trap to redistribute Myosin Regulatory Light Chain::GFP. The resulting leg discs recapitulated the Arpc5 phenotype with deviated folds. Because the authors have the in silico model they are also able ask the converse question, whether introducing planar polarity into a non-polarised tissue is sufficient to rescue the fold formation, and find that it is.
Overall this preprint combines elegant experiments, both in vivo and in silico to describe a new, direct role for the actin cytoskeleton in morphogenesis robustness.
Questions arising from this work
- Is the role of the actin cytoskeleton a process novel to Drosophila leg development, or general feature of tissues undergoing morphogenesis?
- Is Arp2/3 complex itself planar polarised and how does it transduce planar polarity to MyoII?
- Is the planar polarity of the tissue more generally disrupted and does this have any functional consequences independent of tissue folding?
Hox info – McGinnis and Krumlauf, 1992
The science behind the folds – de Celis et al., 1998; Rauskolb and Irvine, 1999 Manjón et al., 2007
What is morphogenesis robustness – Frankel et al., 2010; Smith et al., 2018
doi: https://doi.org/10.1242/prelights.16742
Read preprintHave your say
Sign up to customise the site to your preferences and to receive alerts
Register hereAlso in the developmental biology category:
Specialized signaling centers direct cell fate and spatial organization in a limb organoid model
Ryan Harrison
Adult caudal fin shape is imprinted in the embryonic fin fold
Isabella Cisneros
TAK1 operates at the primary cilium in non-canonical TGFB/BMP signaling to control heart development
Reinier Prosee
preListsdevelopmental biology category:
in theBSDB/GenSoc Spring Meeting 2024
A list of preprints highlighted at the British Society for Developmental Biology and Genetics Society joint Spring meeting 2024 at Warwick, UK.
List by | Joyce Yu, Katherine Brown |
GfE/ DSDB meeting 2024
This preList highlights the preprints discussed at the 2024 joint German and Dutch developmental biology societies meeting that took place in March 2024 in Osnabrück, Germany.
List by | Joyce Yu |
‘In preprints’ from Development 2022-2023
A list of the preprints featured in Development's 'In preprints' articles between 2022-2023
List by | Alex Eve, Katherine Brown |
preLights peer support – preprints of interest
This is a preprint repository to organise the preprints and preLights covered through the 'preLights peer support' initiative.
List by | preLights peer support |
The Society for Developmental Biology 82nd Annual Meeting
This preList is made up of the preprints discussed during the Society for Developmental Biology 82nd Annual Meeting that took place in Chicago in July 2023.
List by | Joyce Yu, Katherine Brown |
CSHL 87th Symposium: Stem Cells
Preprints mentioned by speakers at the #CSHLsymp23
List by | Alex Eve |
Journal of Cell Science meeting ‘Imaging Cell Dynamics’
This preList highlights the preprints discussed at the JCS meeting 'Imaging Cell Dynamics'. The meeting was held from 14 - 17 May 2023 in Lisbon, Portugal and was organised by Erika Holzbaur, Jennifer Lippincott-Schwartz, Rob Parton and Michael Way.
List by | Helen Zenner |
9th International Symposium on the Biology of Vertebrate Sex Determination
This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.
List by | Martin Estermann |
Alumni picks – preLights 5th Birthday
This preList contains preprints that were picked and highlighted by preLights Alumni - an initiative that was set up to mark preLights 5th birthday. More entries will follow throughout February and March 2023.
List by | Sergio Menchero et al. |
CellBio 2022 – An ASCB/EMBO Meeting
This preLists features preprints that were discussed and presented during the CellBio 2022 meeting in Washington, DC in December 2022.
List by | Nadja Hümpfer et al. |
2nd Conference of the Visegrád Group Society for Developmental Biology
Preprints from the 2nd Conference of the Visegrád Group Society for Developmental Biology (2-5 September, 2021, Szeged, Hungary)
List by | Nándor Lipták |
Fibroblasts
The advances in fibroblast biology preList explores the recent discoveries and preprints of the fibroblast world. Get ready to immerse yourself with this list created for fibroblasts aficionados and lovers, and beyond. Here, my goal is to include preprints of fibroblast biology, heterogeneity, fate, extracellular matrix, behavior, topography, single-cell atlases, spatial transcriptomics, and their matrix!
List by | Osvaldo Contreras |
EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)
A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.
List by | Alex Eve |
EMBL Conference: From functional genomics to systems biology
Preprints presented at the virtual EMBL conference "from functional genomics and systems biology", 16-19 November 2020
List by | Jesus Victorino |
Single Cell Biology 2020
A list of preprints mentioned at the Wellcome Genome Campus Single Cell Biology 2020 meeting.
List by | Alex Eve |
Society for Developmental Biology 79th Annual Meeting
Preprints at SDB 2020
List by | Irepan Salvador-Martinez, Martin Estermann |
FENS 2020
A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020
List by | Ana Dorrego-Rivas |
Planar Cell Polarity – PCP
This preList contains preprints about the latest findings on Planar Cell Polarity (PCP) in various model organisms at the molecular, cellular and tissue levels.
List by | Ana Dorrego-Rivas |
Cell Polarity
Recent research from the field of cell polarity is summarized in this list of preprints. It comprises of studies focusing on various forms of cell polarity ranging from epithelial polarity, planar cell polarity to front-to-rear polarity.
List by | Yamini Ravichandran |
TAGC 2020
Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20
List by | Maiko Kitaoka et al. |
3D Gastruloids
A curated list of preprints related to Gastruloids (in vitro models of early development obtained by 3D aggregation of embryonic cells). Updated until July 2021.
List by | Paul Gerald L. Sanchez and Stefano Vianello |
ASCB EMBO Annual Meeting 2019
A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)
List by | Madhuja Samaddar et al. |
EDBC Alicante 2019
Preprints presented at the European Developmental Biology Congress (EDBC) in Alicante, October 23-26 2019.
List by | Sergio Menchero et al. |
EMBL Seeing is Believing – Imaging the Molecular Processes of Life
Preprints discussed at the 2019 edition of Seeing is Believing, at EMBL Heidelberg from the 9th-12th October 2019
List by | Dey Lab |
SDB 78th Annual Meeting 2019
A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.
List by | Alex Eve |
Lung Disease and Regeneration
This preprint list compiles highlights from the field of lung biology.
List by | Rob Hynds |
Young Embryologist Network Conference 2019
Preprints presented at the Young Embryologist Network 2019 conference, 13 May, The Francis Crick Institute, London
List by | Alex Eve |
Pattern formation during development
The aim of this preList is to integrate results about the mechanisms that govern patterning during development, from genes implicated in the processes to theoritical models of pattern formation in nature.
List by | Alexa Sadier |
BSCB/BSDB Annual Meeting 2019
Preprints presented at the BSCB/BSDB Annual Meeting 2019
List by | Dey Lab |
Zebrafish immunology
A compilation of cutting-edge research that uses the zebrafish as a model system to elucidate novel immunological mechanisms in health and disease.
List by | Shikha Nayar |
4 years
Mathieu Hautefeuille
Very interesting paper.
I would suggest reading this one as the two papers complement very well:
“Leading edge stability in motile cells is an emergent property of branched actin network growth”
Garner & Theriot.
https://www.biorxiv.org/content/10.1101/2020.08.22.262907v1