scholarly journals A mechanism for the proliferative control of tissue mechanics in the absence of growth

2018 ◽  
Author(s):  
Min Wu ◽  
Madhav Mani

AbstractDuring the development of a multicellular organism, cells coordinate their activities to generate mechanical forces, which in turn drives tissue deformation and eventually defines the shape of the adult tissue. Broadly speaking, it is recognized that mechanical forces can be generated through differential growth and the activity of the cytoskeleton. Based on quantitative analyses of live imaging of the Drosophila dorsal thorax, we suggest a novel mechanism that can generate contractile forces within the plane of an epithelia - via cell proliferation in the absence of growth. Utilizing force inference techniques, we demonstrate that it is not the gradient of junction tension but the divergence of junction-tension associated stresses that induces the area constriction of the proliferating tissue. Using the vertex model simulations, we show that the local averaged stresses can be roughly elevated by a fold of p 2 per cell division without growth. Moreover, this mechanism is robust to disordered cell shapes and the division anisotropy, but can be dominated by growth. In competition with growth, we identify the parameter regime where this mechanism is effective and suggest experiments to test this new mechanism.


2018 ◽  
Author(s):  
Sandra B. Lemke ◽  
Thomas Weidemann ◽  
Anna-Lena Cost ◽  
Carsten Grashoff ◽  
Frank Schnorrer

Cells in a developing organism are subjected to particular mechanical forces, which shape tissues and instruct cell fate decisions. How these forces are sensed and transmitted at the molecular level is thus an important question, which has mainly been investigated in cultured cells in vitro. Here, we elucidate how mechanical forces are transmitted in an intact organism. We studied Drosophila muscle attachment sites, which experience high mechanical forces during development and require integrin-mediated adhesion for stable attachment to tendons. Hence, we quantified molecular forces across the essential integrin-binding protein Talin, which links integrin to the actin cytoskeleton. Generating flies expressing three FRET-based Talin tension sensors reporting different force levels between 1 and 11 pN enabled us to quantify physiologically-relevant, molecular forces. By measuring primary Drosophila muscle cells, we demonstrate that Drosophila Talin experiences mechanical forces in cell culture that are similar to those previously reported for Talin in mammalian cell lines. However, in vivo force measurements at developing flight muscle attachment sites revealed that average forces across Talin are comparatively low and decrease even further while attachments mature and tissue-level tension increases. Concomitantly, Talin concentration at attachment sites increases five-fold as quantified by fluorescence correlation spectroscopy, suggesting that only few Talin molecules are mechanically engaged at any given time. We therefore propose that high tissue forces are shared amongst a large excess of adhesion molecules of which less than 15% are experiencing detectable forces at the same time. Our findings define an important new concept of how cells can adapt to changes in tissue mechanics to prevent mechanical failure in vivo.



1984 ◽  
Vol 105 (2) ◽  
pp. 257-272 ◽  
Author(s):  
Gary C. Schoenwolf ◽  
Mark V. Franks


1994 ◽  
Vol 342 (1) ◽  
pp. 144-151 ◽  
Author(s):  
Jodi L. Smith ◽  
Gary C. Schoenwolf ◽  
Jan Quan


eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Eunice HoYee Chan ◽  
Pruthvi Chavadimane Shivakumar ◽  
Raphaël Clément ◽  
Edith Laugier ◽  
Pierre-François Lenne

Adhesion molecules hold cells together but also couple cell membranes to a contractile actomyosin network, which limits the expansion of cell contacts. Despite their fundamental role in tissue morphogenesis and tissue homeostasis, how adhesion molecules control cell shapes and cell patterns in tissues remains unclear. Here we address this question in vivo using the Drosophila eye. We show that cone cell shapes depend little on adhesion bonds and mostly on contractile forces. However, N-cadherin has an indirect control on cell shape. At homotypic contacts, junctional N-cadherin bonds downregulate Myosin-II contractility. At heterotypic contacts with E-cadherin, unbound N-cadherin induces an asymmetric accumulation of Myosin-II, which leads to a highly contractile cell interface. Such differential regulation of contractility is essential for morphogenesis as loss of N-cadherin disrupts cell rearrangements. Our results establish a quantitative link between adhesion and contractility and reveal an unprecedented role of N-cadherin on cell shapes and cell arrangements.



2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Ondřej Kučera ◽  
Valerie Siahaan ◽  
Daniel Janda ◽  
Sietske H. Dijkstra ◽  
Eliška Pilátová ◽  
...  

AbstractConstriction of the cytokinetic ring, a circular structure of actin filaments, is an essential step during cell division. Mechanical forces driving the constriction are attributed to myosin motor proteins, which slide actin filaments along each other. However, in multiple organisms, ring constriction has been reported to be myosin independent. How actin rings constrict in the absence of motor activity remains unclear. Here, we demonstrate that anillin, a non­motor actin crosslinker, indispensable during cytokinesis, autonomously propels the contractility of actin bundles. Anillin generates contractile forces of tens of pico-Newtons to maximise the lengths of overlaps between bundled actin filaments. The contractility is enhanced by actin disassembly. When multiple actin filaments are arranged into a ring, this contractility leads to ring constriction. Our results indicate that passive actin crosslinkers can substitute for the activity of molecular motors to generate contractile forces in a variety of actin networks, including the cytokinetic ring.



Author(s):  
Emmanuel Martin ◽  
Sophie Theis ◽  
Guillaume Gay ◽  
Bruno Monier ◽  
Christian Rouvière ◽  
...  

AbstractEpithelial sheets undergo highly reproducible remodeling to shape organs. This stereotyped morphogenesis depends on a well-defined sequence of events leading to the regionalized expression of developmental patterning genes that finally triggers downstream mechanical forces to drive tissue remodeling at a pre-defined position. However, how tissue mechanics controls morphogenetic robustness when challenged by intrinsic perturbations in close proximity has never been addressed.Here, we show that a bias in force propagation ensures stereotyped morphogenesis despite the presence of mechanical noise in the environment. We found that knockdown of the Arp2/3 complex member Arpc5 specifically affects fold directionality without altering neither the developmental nor the force generation patterns. By combining in silico modeling, biophysical and ad hoc genetic tools, our data reveal that junctional Myosin II planar polarity favors long-range force channeling and ensures folding robustness, avoiding force scattering and thus isolating the fold domain from surrounding mechanical perturbations.



F1000Research ◽  
2018 ◽  
Vol 7 ◽  
pp. 241 ◽  
Author(s):  
Sven van Teeffelen ◽  
Lars D. Renner

Cell shape and cell volume are important for many bacterial functions. In recent years, we have seen a range of experimental and theoretical work that led to a better understanding of the determinants of cell shape and size. The roles of different molecular machineries for cell-wall expansion have been detailed and partially redefined, mechanical forces have been shown to influence cell shape, and new connections between metabolism and cell shape have been proposed. Yet the fundamental determinants of the different cellular dimensions remain to be identified. Here, we highlight some of the recent developments and focus on the determinants of rod-like cell shape and size in the well-studied model organismsEscherichia coliandBacillus subtilis.



2021 ◽  
Author(s):  
Paula C. Sanematsu ◽  
Gonca Erdemci-Tandogan ◽  
Himani Patel ◽  
Emma M. Retzlaff ◽  
Jeffrey D. Amack ◽  
...  

AbstractThe left-right organizer in zebrafish embryos, Kupffer’s Vesicle (KV), is a simple organ that undergoes programmed asymmetric cell shape changes that are necessary to establish the left-right axis of the embryo. We use simulations and experiments to investigate whether 3D mechanical drag forces generated by the posteriorly-directed motion of the KV through the tailbud tissue are sufficient to drive such shape changes. We develop a fully 3D vertex-like (Voronoi) model for the tissue architecture, and demonstrate that the tissue can generate drag forces and drive cell shape changes. Furthermore, we find that tailbud tissue presents a shear-thinning, viscoelastic behavior consistent with those observed in published experiments. We then perform live imaging experiments and particle image velocimetry analysis to quantify the precise tissue velocity gradients around KV as a function of developmental time. We observe robust velocity gradients around the KV, indicating that mechanical drag forces must be exerted on the KV by the tailbud tissue. We demonstrate that experimentally observed velocity fields are consistent with the viscoelastic response seen in simulations. This work also suggests that 3D viscoelastic drag forces could be a generic mechanism for cell shape change in other biological processes.Highlightsnew physics-based simulation method allows study of dynamic tissue structures in 3Dmovement of an organ through tissue generates viscoelastic drag forces on the organthese drag forces can generate precisely the cell shape changes seen in experimentPIV analysis of experimental data matches simulations and probes tissue mechanicsGraphical abstract



2021 ◽  
Vol 13 (1) ◽  
Author(s):  
Wei Du ◽  
Arshia Bhojwani ◽  
Jimmy K. Hu

AbstractDuring embryonic development, organs undergo distinct and programmed morphological changes as they develop into their functional forms. While genetics and biochemical signals are well recognized regulators of morphogenesis, mechanical forces and the physical properties of tissues are now emerging as integral parts of this process as well. These physical factors drive coordinated cell movements and reorganizations, shape and size changes, proliferation and differentiation, as well as gene expression changes, and ultimately sculpt any developing structure by guiding correct cellular architectures and compositions. In this review we focus on several craniofacial structures, including the tooth, the mandible, the palate, and the cranium. We discuss the spatiotemporal regulation of different mechanical cues at both the cellular and tissue scales during craniofacial development and examine how tissue mechanics control various aspects of cell biology and signaling to shape a developing craniofacial organ.



2013 ◽  
Vol 10 (84) ◽  
pp. 20130179 ◽  
Author(s):  
Luke MacQueen ◽  
Yu Sun ◽  
Craig A. Simmons

Experimental control over progenitor cell lineage specification can be achieved by modulating properties of the cell's microenvironment. These include physical properties of the cell adhesion substrate, such as rigidity, topography and deformation owing to dynamic mechanical forces. Multipotent mesenchymal stem cells (MSCs) generate contractile forces to sense and remodel their extracellular microenvironments and thereby obtain information that directs broad aspects of MSC function, including lineage specification. Various physical factors are important regulators of MSC function, but improved understanding of MSC mechanobiology requires novel experimental platforms. Engineers are bridging this gap by developing tools to control mechanical factors with improved precision and throughput, thereby enabling biological investigation of mechanics-driven MSC function. In this review, we introduce MSC mechanobiology and review emerging cell culture platforms that enable new insights into mechanobiological control of MSCs. Our main goals are to provide engineers and microtechnology developers with an up-to-date description of MSC mechanobiology that is relevant to the design of experimental platforms and to introduce biologists to these emerging platforms.



Sign in / Sign up

Export Citation Format

Share Document