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Emergent material properties of developing epithelial tissues



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Machado, Pedro F 
Duque, Julia 
Étienne, Jocelyn 
Martinez-Arias, Alfonso  ORCID logo


Background: Force generation and the material properties of cells and tissues are central to morphogenesis but remain difficult to measure in vivo. Insight is often limited to the ratios of mechanical properties obtained through disruptive manipulation, and the appropriate models relating stress and strain are unknown. The Drosophila amnioserosa epithelium progressively contracts over three hours of Dorsal Closure, during which cell apices exhibit area fluctuations driven by medial Myosin pulses with periods of 1.5-6 minutes. Linking these two time-scales and understanding how pulsatile contractions drive morphogenetic movements is an urgent challenge.

Results: We present a novel framework to measure in a continuous manner the mechanical properties of epithelial cells in the natural context of a tissue undergoing morphogenesis. We show that the relationship between apicomedial Myosin fluorescence intensity and strain during fluctuations is consistent with a linear behaviour, although with a lag. We thus used Myosin fluorescence intensity as a proxy for active force generation and treated cells as natural experiments of mechanical response under cyclic loading, revealing unambiguous mechanical properties from the hysteresis loop relating stress to strain.

Amnioserosa cells can be described as a contractile viscoelastic fluid. We show that their emergent mechanical behaviour can be described by a linear viscoelastic rheology at timescales relevant for tissue morphogenesis. For the first time, we establish relative changes in separate effective mechanical properties in vivo. Over the course of Dorsal Closure, the tissue solidifies and effective stiffness doubles as net contraction of the tissue commences. Combining our findings with those from previous laser ablation experiments, we show that both apicomedial and junctional stress also increases over time, with the relative increase in apicomedial stress approximately twice that of other obtained measures.

Conclusions: Our results show that in an epithelial tissue undergoing net contraction, stiffness and stress are coupled. Dorsal Closure cell apical contraction is driven by the medial region where the relative increase in stress is greater than that of stiffness. At junctions, by contrast, the relative increase in the mechanical properties is the same, so the junctional contribution to tissue deformation is constant over time. An increase in Myosin activity is likely to underlie, at least in part, the change in medioapical properties and we suggest that its greater effect on stress relative to stiffness is fundamental to actomyosin systems and confers on tissues the ability to regulate contraction rates in response to changes in external mechanics.



visco-elastic fluid, mechanical properties, apical contraction, actomyosin, oscillations, hysteresis

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BMC Biology

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BBSRC (BB/J010278/1)
We thank the following funding bodies for their support: Herchel Smith Fund (PFM), Ministerio de Ciencia e Innovación (NG and JD, BFU2011-25828 and “Ramón y Cajal” fellowship award), Marie Curie Career Integration Grant (NG, PCIG09-GA-2011-293479), Biotechnology and Biological Sciences Research Council (GBB, grant No. BB/J010278/1) and Rhône-Alpes Complex System Institute (JE).