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Review
. 2013 Oct;14(10):733-44.
doi: 10.1038/nrg3513.

The interplay between cell signalling and mechanics in developmental processes

Callie Johnson Miller  1 , Lance A Davidson
Affiliations
Review

The interplay between cell signalling and mechanics in developmental processes

Callie Johnson Miller et al. Nat Rev Genet. 2013 Oct.

Abstract

Force production and the propagation of stress and strain within embryos and organisms are crucial physical processes that direct morphogenesis. In addition, there is mounting evidence that biomechanical cues created by these processes guide cell behaviours and cell fates. In this Review we discuss key roles for biomechanics during development to directly shape tissues, to provide positional information for cell fate decisions and to enable robust programmes of development. Several recently identified molecular mechanisms suggest how cells and tissues might coordinate their responses to biomechanical cues. Finally, we outline long-term challenges in integrating biomechanics with genetic analysis of developing embryos.

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Figures

Figure 1
Figure 1. Forces contributing to tissue movements in development
This cartoon shows the process of Drosophila dorsal closure and illustrates the individual mechanical components which help complete closure. In the early stage embryo, the amnioserosa (AS) cells are located in the “hole” which prospective epidermal cells will cover. The embryo is already polarized with anterior (A), where the head will form, and posterior (P) axes. Closure is driven to completion by three distinct cellular processes that contribute to global tissue movements: 1) The actomyosin purse string is shown in pink and is located at the edge of the epithelial cells and AS cells. 2) As epidermal cells meet at the anterior and posterior ends of the AS they fuse and create a zipper, shown in pink, that progressively seals the epidermal sheet over the AS. .3) Cells in the AS, shown in pink, undergo cycles of actomyosin contractions (AS contractility) to narrow their exposed apical faces and draw the epidermal margins of the AS together.
Figure 2
Figure 2. Information flow and molecular origins of mechanics
(A) This flow chart shows the intricacies involved with connecting molecular, cellular, and tissue scale behaviors and mechanisms. At the molecular scale, there is molecular signaling which causes intermolecular force production. This force production then feeds back into more molecular signaling. From the molecular scale, there are resultant forces and cell shape changes/movements on the cellular scale, which induce signaling into neighboring cells. The cellular scale can then feedback into molecular scale dynamics or result in tissue scale movements or bulk mechanical property changes. Isolating any portion of this intricate feedback loop is extremely difficult without considering all upstream and downstream effects. (B) Different molecules involved in sensing and signaling to force are shown. Vinculin is located inside the cell at sites of focal adhesions and is also a candidate for sensing forces during development. Fibronectin is an extensible ECM fiber that may sense tension within the tissue. TRPV4 is a membrane mechanosensitive ion channel, believed to open based on tension in the cell membrane. Piezo is a protein part of a cation channel which induces an electrical current based on force. I-bar protein is located at protrusions of the cell membrane and F-bar protein is located at invaginations of the cell membrane. KLF2 is a transcription factor which becomes transcribed when the cell experiences shear flow. YAP/TAZ is activated when the cell is on stiff substrates. Dorsal is a transcription factor upstream of Twist/Snail which is responsible for mesoderm invagination.
Figure 3
Figure 3. Mechanical feedback during morphogenesis
A pathway depicting genetic control of ventral furrow and anterior midgut invagination and a role in that network for mechanical cues. Snail expression is responsible for the mechanical cues produced by the first phase of myosin II contraction. Strain within the epithelium may redirect actomyosin to the apical cap and activate fog signaling which act during the second, Twist-dependent phase to stabilize actomyosin contractions and drive epithelial folding. Furrowing and invagination in Twist mutants can be rescued by exogenously applied strain either by laser ablation or by physical indentation. In the case of invagination-rescued anterior midgut differentiation, larval development was also reported to be rescued.
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