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2015 ; 13
(ä): 98
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Emergent material properties of developing epithelial tissues
#MMPMID26596771
Machado PF
; Duque J
; Étienne J
; Martinez-Arias A
; Blanchard GB
; Gorfinkiel N
BMC Biol
2015[Nov]; 13
(ä): 98
PMID26596771
show ga
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 3 hours of
dorsal closure, during which cell apices exhibit area fluctuations driven by
medial myosin pulses with periods of 1.5-6 min. Linking these two timescales 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 increase 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.
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