Intercellular friction and motility drive orientational order in cell monolayers

Proc Natl Acad Sci U S A. 2024 Oct;121(40):e2319310121. doi: 10.1073/pnas.2319310121. Epub 2024 Sep 20.

Abstract

Spatiotemporal patterns in multicellular systems are important to understanding tissue dynamics, for instance, during embryonic development and disease. Here, we use a multiphase field model to study numerically the behavior of a near-confluent monolayer of deformable cells with intercellular friction. Varying friction and cell motility drives a solid-liquid transition, and near the transition boundary, we find the emergence of local nematic order of cell deformation driven by shear-aligning cellular flows. Intercellular friction contributes to the monolayer's viscosity, which significantly increases the spatial correlation in the flow and, concomitantly, the extent of nematic order. We also show that local hexatic and nematic order are tightly coupled and propose a mechanical-geometric model for the colocalization of [Formula: see text] nematic defects and 5-7 disclination pairs, which are the structural defects in the hexatic phase. Such topological defects coincide with regions of high cell-cell overlap, suggesting that they may mediate cellular extrusion from the monolayer, as found experimentally. Our results delineate a mechanical basis for the recent observation of nematic and hexatic order in multicellular collectives in experiments and simulations and pinpoint a generic pathway to couple topological and physical effects in these systems.

Keywords: cellular extrusion; intercellular friction; nematic and hexatic order; solid–liquid transition; topological defects.

MeSH terms

  • Cell Movement* / physiology
  • Friction*
  • Models, Biological*
  • Viscosity