Integration of contractile forces during tissue invagination

108

111

Significance Animal cells continuously move, divide, and transmit forces by actively reorganizing their internal scaffold or cytoskeleton. Molecular motors pull actin filaments together and generate contraction of the cytoskeleton underneath the cell membrane. We address the detailed mechanism of contraction by using a minimal in vitro assay: a liposome membrane to which we attach actin filaments and molecular motors in a controlled manner. We reproduce contraction like in cells. We show that the scaffold needs to be tightly attached to the membrane for efficient contraction, but, under some conditions, efficient contraction can lead to liposome destruction. These results suggest that cells must precisely control their contractility to remain intact during cellular events.

Section: Force Analysis and Estimates Of Characteristic Times And Crimentioning

confidence: 94%

Cell-sized liposomes reveal how actomyosin cortical tension drives shape change

Carvalho

Tsai

Lees

et al. 2013

108

111

“…Because apical volume loss is associated with apical constriction, we next asked whether apical volume loss and signs of pronounced cell lengthening were absent in cta; T48 mutants (12,28), in which the contractile actomyosin meshwork that normally drives apical constriction fails to stabilize (29). During cellularization, cells in cta; T48 mutants followed length (Fig.…”

Section: Constriction-induced Basal Movement Of Cytoplasm Seems To Drivementioning

confidence: 99%

Volume conservation principle involved in cell lengthening and nucleus movement during tissue morphogenesis

Gelbart

Martin

et al. 2012

Self Cite

129

124

Tissue morphogenesis is the process in which coordinated movements and shape changes of large numbers of cells form tissues, organs, and the internal body structure. Understanding morphogenetic movements requires precise measurements of whole-cell shape changes over time. Tissue folding and invagination are thought to be facilitated by apical constriction, but the mechanism by which changes near the apical cell surface affect changes along the entire apical-basal axis of the cell remains elusive. Here, we developed Embryo Development Geometry Explorer, an approach for quantifying rapid whole-cell shape changes over time, and we combined it with deep-tissue time-lapse imaging based on fast two-photon microscopy to study Drosophila ventral furrow formation. We found that both the cell lengthening along the apical-basal axis and the movement of the nucleus to the basal side proceeded stepwise and were correlated with apical constriction. Moreover, cell volume lost apically due to constriction largely balanced the volume gained basally by cell lengthening. The volume above the nucleus was conserved during its basal movement. Both apical volume loss and cell lengthening were absent in mutants showing deficits in the contractile cytoskeleton underlying apical constriction. We conclude that a single mechanical mechanism involving volume conservation and apical constriction-induced basal movement of cytoplasm accounts quantitatively for the cell shape changes and the nucleus movement in Drosophila ventral furrow formation. Our study provides a comprehensive quantitative analysis of the fast dynamics of whole-cell shape changes during tissue folding and points to a simplified model for Drosophila gastrulation.two-photon imaging | 4D reconstruction | segmentation

“…Tissue-scale mechanical phenomena are particularly important in developmental morphogenesis (12), homeostasis (13), and wound healing (14) in epithelial tissues. Cells exert mechanical force on each other at sites of intercellular adhesion, typically through cadherins (15,16), as well as on the underlying extracellular matrix (ECM) through integrins (17)(18)(19).…”

mentioning

confidence: 99%

Cadherin-based intercellular adhesions organize epithelial cell–matrix traction forces

Mertz¹,

Che²,

Banerjee³

et al. 2012

217

201

Cell-cell and cell-matrix adhesions play essential roles in the function of tissues. There is growing evidence for the importance of cross talk between these two adhesion types, yet little is known about the impact of these interactions on the mechanical coupling of cells to the extracellular matrix (ECM). Here, we combine experiment and theory to reveal how intercellular adhesions modulate forces transmitted to the ECM. In the absence of cadherin-based adhesions, primary mouse keratinocytes within a colony appear to act independently, with significant traction forces extending throughout the colony. In contrast, with strong cadherin-based adhesions, keratinocytes in a cohesive colony localize traction forces to the colony periphery. Through genetic or antibody-mediated loss of cadherin expression or function, we show that cadherin-based adhesions are essential for this mechanical cooperativity. A minimal physical model in which cell-cell adhesions modulate the physical cohesion between contractile cells is sufficient to recreate the spatial rearrangement of traction forces observed experimentally with varying strength of cadherin-based adhesions. This work defines the importance of cadherin-based cell-cell adhesions in coordinating mechanical activity of epithelial cells and has implications for the mechanical regulation of epithelial tissues during development, homeostasis, and disease. mechanotransduction | traction force microscopy M echanical interactions of individual cells have a crucial role in the spatial organization of tissues (1, 2) and in embryonic development (3-5). The mechanical cooperation of cells is evident in dynamic processes such as flow-induced alignment of vascular endothelial cells (6) and muscle contraction (7). However, mechanical interactions of cells within a tissue also affect the tissue's static mechanical properties including elastic modulus (8), surface tension (9), and fracture toughness (10). Little is known about how these tissue-scale mechanical phenomena emerge from interactions at the molecular and cellular levels (11).Tissue-scale mechanical phenomena are particularly important in developmental morphogenesis (12), homeostasis (13), and wound healing (14) in epithelial tissues. Cells exert mechanical force on each other at sites of intercellular adhesion, typically through cadherins (15, 16), as well as on the underlying extracellular matrix (ECM) through integrins (17-19). Cadherin-based adhesions can alter physical aspects of cells such as the surface tension of cellular aggregates (20) and the spreading (21) and migration (22) of single cells adherent to cadherin-patterned substrates. Integrity of intercellular adhesions may also contribute to metastatic potential (23). We and others have shown that epithelial cell clusters with strong cell-cell adhesions exhibit coordinated mechanical behavior over length scales much larger than a single cell (24-27). Several studies have implicated cross talk between cell-ECM and cell-cell adhesions (28, 29) that can be modulated by ac...