Cooperation of polarized cell intercalations drives convergence and extension of presomitic mesoderm during zebrafish gastrulation

During vertebrate gastrulation, convergence and extension (C&E) movements narrow and lengthen the embryonic tissues, respectively. In zebrafish, regional differences of C&E movements have been observed; however, the underlying cell behaviors are poorly understood. Using time-lapse analyses and computational modeling, we demonstrate that C&E of the medial presomitic mesoderm is achieved by cooperation of planar and radial cell intercalations. Radial intercalations preferentially separate anterior and posterior neighbors to promote extension. In knypek;trilobite noncanonical Wnt mutants, the frequencies of cell intercalations are altered and the anteroposterior bias of radial intercalations is lost. This provides evidence for noncanonical Wnt signaling polarizing cell movements between different mesodermal cell layers. We further show using fluorescent fusion proteins that during dorsal mesoderm C&E, the noncanonical Wnt component Prickle localizes at the anterior cell edge, whereas Dishevelled is enriched posteriorly. Asymmetrical localization of Prickle and Dishevelled to the opposite cell edges in zebrafish gastrula parallels their distribution in fly, and suggests that noncanonical Wnt signaling defines distinct anterior and posterior cell properties to bias cell intercalations

Polarized cortical tension drives zebrafish epiboly movements

The principles underlying the biomechanics of morphogenesis are largely unknown. Epiboly is an essential embryonic event in which three tissues coordinate to direct the expansion of the blastoderm. How and where forces are generated during epiboly, and how these are globally coupled remains elusive. Here we developed a method, hydrodynamic regression (HR), to infer 3D pressure fields, mechanical power, and cortical surface tension profiles. HR is based on velocity measurements retrieved from 2D+T microscopy and their hydrodynamic modeling. We applied HR to identify biomechanically active structures and changes in cortex local tension during epiboly in zebrafish. Based on our results, we propose a novel physical description for epiboly, where tissue movements are directed by a polarized gradient of cortical tension. We found that this gradient relies on local contractile forces at the cortex, differences in elastic properties between cortex components and the passive transmission of forces within the yolk cell. All in all, our work identifies a novel way to physically regulate concerted cellular movements that might be instrumental for the mechanical control of many morphogenetic processes.Peer ReviewedPostprint (author's final draft

Biomécanique de la gastrulation chez Drosophila Melanogaster

PARIS7-Bibliothèque centrale (751132105) / SudocSudocFranceF

Hydrodynamic simulation of multicellular embryo invagination Related content Mechanotransduction in mechanically coupled pulsating cells

International audienceThe mechanical aspects of embryonic morphogenesis have been widely analysed by numerical simulations of invagination in sea urchins and Drosophila gastrulation. Finite element models, which describe the tissue as a continuous medium, lead to the global invagination morphogenesis observed in vivo. Here we develop a simulation of multicellular embryo invagination that allows access to both cellular and multicellular mechanical behaviours of the embryo. In this model, the tissue is composed of adhesive individual cells, in which shape change dynamics is governed by internal acto-myosin forces and the hydrodynamic flow associated with membrane movements. We investigated the minimal structural and force elements sufficient to phenocopy mesoderm invagination. The minimal structures are cell membranes characterized by an acto-myosin cortical tension and connected by apical and basal junctions and an acto-myosin contractile ring connected to the apical junctions. An increase in the apical-cortical surface tension is the only control parameter change required to phenocopy most known multicellular and cellular shape changes of Drosophila gastrulation. Specifically, behaviours observed in vivo, including apical junction movements at the onset of gastrulation, cell elongation and subsequent shortening during invagination, and the development of a dorso-ventral gradient of thickness of the embryo, are predicted by this model as passive mechanical consequences of the genetically controlled increase in the apical surface tension in invaginating mesoderm cells, thus demonstrating the accurate description of structures at both global and single cell scales

Reverse engineering using a knowledge-based approach

International audienceThis paper focuses on Reverse Engineering (RE) domain in mechanical design. RE is an activity which consists of creating a Computer-Aided Design (CAD) model from a 3D point cloud. The CAD models obtained using modern software applications are generally 'frozen' (i.e. a set of free form surfaces or a set of geometrical features in a manifold static model). Redesigning activities of these models are thus impossible. This paper proposes Knowledge-Based Reverse Engineering (KBRE), an approach which combines knowledge-based engineering with classical approaches in RE. The combination allows us to obtain a dynamic model (i.e. a set of manufacturing and design features with constraints, parameters, rules and relationships). A redesigning activity is then possible from this type of model

Rab5ab-Mediated Yolk Cell Membrane Endocytosis Is Essential for Zebrafish Epiboly and Mechanical Equilibrium During Gastrulation

© 2021 Marsal, Hernández-Vega, Pouille and Martin-Blanco.Morphogenesis in early embryos demands the coordinated distribution of cells and tissues to their final destination in a spatio-temporal controlled way. Spatial and scalar differences in adhesion and contractility are essential for these morphogenetic movements, while the role that membrane remodeling may play remains less clear. To evaluate how membrane turnover modulates tissue arrangements we studied the role of endocytosis in zebrafish epiboly. Experimental analyses and modeling have shown that the expansion of the blastoderm relies on an asymmetry of mechanical tension in the yolk cell generated as a result of actomyosin-dependent contraction and membrane removal. Here we show that the GTPase Rab5ab is essential for the endocytosis and the removal of the external yolk cell syncytial layer (E-YSL) membrane. Interfering in its expression exclusively in the yolk resulted in the reduction of yolk cell actomyosin contractility, the disruption of cortical and internal flows, a disequilibrium in force balance and epiboly impairment. We conclude that regulated membrane remodeling is crucial for directing cell and tissue mechanics, preserving embryo geometry and coordinating morphogenetic movements during epiboly.This work was supported by the 2009SGR1009 Consolidated Scientific Group grant of the Generalitat de Catalunya and BFU2014-23451 and CSD-2007-00008 grants from the Ministry of Science and Innovation of Spain to EM-B

Tissue deformation modulates Twist expression to determine anterior midgut differentiation in Drosophila embryos

International audienceMechanical deformations associated with embryonic morphogenetic movements have been suggested to actively participate in the signaling cascades regulating developmental gene expression. Here we develop an appropriate experimental approach to ascertain the existence and the physiological relevance of this phenomenon. By combining the use of magnetic tweezers with in vivo laser ablation, we locally control physiologically relevant deformations in wild-type Drosophila embryonic tissues. We demonstrate that the deformations caused by germ band extension upregulate Twist expression in the stomodeal primordium. We find that stomodeal compression triggers Src42A-dependent nuclear translocation of Armadillo/β-catenin, which is required for Twist mechanical induction in the stomodeum. Finally, stomodeal-specific RNAi-mediated silencing of Twist during compression impairs the differentiation of midgut cells, resulting in larval lethality. These experiments show that mechanically induced Twist upregulation in stomodeal cells is necessary for subsequent midgut differentiation. DEVBI

Mechanical coordination is sufficient to promote tissue replacement during metamorphosis in Drosophila

During development, cells coordinate to organize in coherent structures. Although it is now well established that physical forces are essential for implementing this coordination, the instructive roles of mechanical inputs are not clear. Here, we show that the replacement of the larval epithelia by the adult one in Drosophila demands the coordinated exchange of mechanical signals between two cell types, the histoblasts (adult precursors) organized in nests and the surrounding larval epidermal cells (LECs). An increasing stress gradient develops from the center of the nests toward the LECs as a result of the forces generated by histoblasts as they proliferate and by the LECs as they delaminate (push/pull coordination). This asymmetric radial coordination of expansive and contractile activities contributes to epithelial replacement. Our analyses support a model in which cell–cell mechanical communication is sufficient for the rearrangements that implement epithelial morphogenesis.The Martín-Blanco and Buceta's laboratories were supported by funds from Programa Estatal de Fomento de la Investigación Científica y Técnica de Excelencia (BFU2014-57019-P and BFU2017-82876-P for EM-B and BFU2010-21847-C02-01/BMC for JB, respectively) and from Fundación Ramón Areces to EM-B. CP-R was supported by a FPI Fellowship from the Ministry of Science and Innovation, Spain

Plasticity of the MAPK signaling network in response to mechanical stress

Cells display versatile responses to mechanical inputs and recent studies have identified the mitogen-activated protein kinase (MAPK) cascades mediating the biological effects observed upon mechanical stimulation. Although, MAPK pathways can act insulated from each other, several mechanisms facilitate the crosstalk between the components of these cascades. Yet, the combinatorial complexity of potential molecular interactions between these elements have prevented the understanding of their concerted functions. To analyze the plasticity of the MAPK signaling network in response to mechanical stress we performed a non-saturating epistatic screen in resting and stretched conditions employing as readout a JNK responsive dJun-FRET biosensor. By knocking down MAPKs, and JNK pathway regulators, singly or in pairs in Drosophila S2R+ cells, we have uncovered unexpected regulatory links between JNK cascade kinases, Rho GTPases, MAPKs and the JNK phosphatase Puc. These relationships have been integrated in a system network model at equilibrium accounting for all experimentally validated interactions. This model allows predicting the global reaction of the network to its modulation in response to mechanical stress. It also highlights its context-dependent sensitivity. © 2014 Pereira et al.A.M.P held a Spanish FPU PhD studentship, and C.T. was supported by the Marie Curie Research Training Network IMMUNANOMAP. Research in the E.M.-B. laboratory is funded by grants of the Ministry of Economy and Competitivity (DGI and Consolider). Research in the V.S. laboratory is supported by “Stitching voor Fundamenteel Onderzoek der Materie” (FOM), the Nederlandse Organisatie voor Wetenschappelik Onderzoek (N.W.O.), and the European UnionPeer Reviewe

Embryos Drosophila Invagination in Mechanical Signals Trigger Myosin II Redistribution and Mesoderm

International audienceThe following resources related to this article are available online at http://stke.sciencemag.org. Article Tools http://stke.sciencemag.org/cgi/content/full/sigtrans;2/66/ra16 Visit the online version of this article to access the personalization and article tools: Materials Supplemental http://stke.sciencemag.org/cgi/content/full/sigtrans;2/66/ra16/DC1 "Supplementary Materials" Related Content http://stke.sciencemag.org/cgi/content/abstract/sigtrans;2/66/eg4 's sites: Science The editors suggest related resources on References http://stke.sciencemag.org/cgi/content/full/sigtrans;2/66/ra16#otherarticles This article cites 34 articles, 13 of which can be accessed for free: Glossary http://stke.sciencemag.org/glossary/ Look up definitions for abbreviations and terms found in this article: Permissions http://www.sciencemag.org/about/permissions.dt