Transcriptional initiation and mechanically driven self-propagation of a tissue contractile wave during axis elongation
Posted on: 2 November 2018 , updated on: 8 November 2018
Preprint posted on 29 September 2018
A mechanical relay mechanism drives a wave of polarized constriction during Drosophila endoderm morphogenesis.
Selected by Sundar Naganathan
Categories: biophysics, cell biology, developmental biology
Background
Embryonic tissues undergo intricate reorganizations and deformations that ultimately give rise to a specific shape and form. In many contexts, tissue-scale reorganization is driven by spatiotemporally regulated actomyosin activation and dynamics. For example, myosin activation through Rho1 in the presumptive mesoderm cells of a Drosophila embryo drives apical constriction, leading to tissue bending and furrow formation. A similar process, i.e. Rho1 and Myosin II dependent apical constriction, drives invagination of the posterior endoderm in Drosophila embryos. Interestingly, following this initial invagination in the posterior, the furrow continues invaginating in a wave-like fashion and moves in a polarized fashion towards the anterior. What are the mechanisms by which this polarized furrow movement occurs? The authors uncover a mechanical coupling pathway, where cell shape changes triggered by the initial invagination leads to a wave of myosin activation and associated constriction.
Key findings
The authors performed time-lapse imaging of the invaginating posterior endoderm and quantified the dynamics of apical constriction. In the initial phase of constriction, myosin as well as its upstream regulators, Rho1 and Rok, were found to be uniformly activated across a group of cells in the posterior called the primordium region by regulated transcription of fog, a GPCR ligand. In the second phase, a wave of Rho1-MyosinII activation and associated constriction propagated towards the anterior in a domain that comprised about 8 rows of cells, called the propagation zone.
To what extent is fog transcription involved in myosin activation in the propagation zone? Through live analysis of fog transcripts and by injection of alpha-aminitin, a potent inhibitor of RNA polymerase II, the authors demonstrate that myosin wave propagation does not require gene transcription in the propagation zone. Moreover, diffusion of fog away from the primordium towards the propagation zone also does not play a role, as overexpression of fog in the primordium did not change the wave dynamics in the propagation region. Thus, patterned Fog signaling does not determine the dynamics of Myosin II wave propagation.
Given that invagination involves extensive cell shape changes, can the wave propagate through mechanical feedback with the neighboring cells? By performing a global inhibition of Rok in the embryo, the authors show that anteriorward movement of constriction is mechanically driven. No change in Rho1 activation in the primordium was observed, however, Rok global inhibition severely perturbed Rho1 wave propagation indicating that this requires MyoII activity. The authors then perturbed the mechanical environment of the dorsal epithelium by stitching dorsal epithelial cells that are 30 cell rows away from the primordium to the vitelline membrane or by using dorsalizing mutants. In both cases, cells recruited higher levels of myosin, however, wave propagation significantly slowed down suggesting higher resistance to the invagination. Taken together, wave propagation is dependent on mechanical changes to the tissue influenced by the invaginating epithelium. The authors finally quantified 3D cell deformations during wave propagation and show the existence of a mechanical relay mechanism where neighboring rows of cells sequentially deform that ultimately leads to a wave of myosin activation and constriction.
Why I chose this preprint?
An increasingly number of articles are discussing the importance of mechanical coupling across cells in a tissue and across tissues in an embryo that ultimately drives morphogenesis. The highlighted article is yet another example of mechanical coupling that clearly demonstrates how local activation of myosin through controlled transcription factor expression, leads to a wave of mechanical changes in cells tens of micrometers away from the activated region. This mechanical coupling is important for the resultant self-organization that shapes the tissue into a specific form.
Exciting times are ahead for developmental biophysics, where such quantitative analyses will enable intricate theoretical models to be developed that can explain morphogenesis across length and time scales.
Open questions
- Different tissues undergo diverse transformations and end up in quite different shapes and forms during embryogenesis. Interestingly, the basic constituents, actin, myosin and upstream activators such as Rho remain the same across developmental contexts. How does tissue shape diversity emerge from the same building blocks? How different are the mechanical properties of the surrounding tissues in different contexts? Could a change in the properties of the immediate environment explain the different dynamics observed across contexts?
- The authors propose that sequential 3D cell deformations lead to a wave of myosin activation and constriction. It is not clear what exactly the authors mean by deformation. Do the authors observe 3D cell compression or just a change in cell shape with no change in volume? Also, how does cell deformation activate myosin?
- Why does the tissue undergo sequential constriction? What is the advantage of sequential constriction when compared to global constriction?
- Does attachment to the vitelline membrane provide some traction to the constricting tissue? Can the material properties of the vitelline membrane be specifically targeted and modified?
- Can the authors predict what happens if myosin is activated prematurely in the propagation zone building some prestress in the tissue before activation of myosin in the primordium?
References
- Martin AC and Goldstein B, Apical constriction: themes and variations on a cellular mechanism driving morphogenesis, Development, 2014.
doi: https://doi.org/10.1242/prelights.5353
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