A Geometric Tension Dynamics Model of Epithelial Convergent Extension

Kavli Affiliate: Boris I. Shraiman

| First 5 Authors: Nikolas H. Claussen, Fridtjof Brauns, Boris I. Shraiman, ,

| Summary:

Epithelial tissue elongation by convergent extension is a key motif of animal
morphogenesis. On a coarse scale, cell motion resembles laminar fluid flow; yet
in contrast to a fluid, epithelial cells adhere to each other and maintain the
tissue layer under actively generated internal tension. To resolve this
apparent paradox, we formulate a model in which tissue flow occurs through
adiabatic remodelling of the cellular force balance causing local cell
rearrangement. We propose that the gradual shifting of the force balance is
caused by positive feedback on myosin-generated cytoskeletal tension. Shifting
force balance within a tension network causes active T1s oriented by the global
anisotropy of tension. Rigidity of cells against shape changes converts the
oriented internal rearrangements into net tissue deformation. Strikingly, we
find that the total amount of tissue extension depends on the initial magnitude
of anisotropy and on cellular packing order. T1s degrade this order so that
tissue flow is self-limiting. We explain these findings by showing that
coordination of T1s depends on coherence in local tension configurations,
quantified by a certain order parameter in tension space. Our model reproduces
the salient tissue- and cell-scale features of germ band elongation during
Drosophila gastrulation, in particular the slowdown of tissue flow after
approximately twofold extension concomitant with a loss of order in tension
configurations. This suggests local cell geometry contains morphogenetic
information and yields predictions testable in future experiments. Furthermore,
our focus on defining biologically controlled active tension dynamics on the
manifold of force-balanced states may provide a general approach to the
description of morphogenetic flow.

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