Controlled Neighbor Exchanges Drive Glassy Behavior, Intermittency, and Cell Streaming in Epithelial Tissues

Abstract

Cell neighbor exchanges are integral to tissue rearrangements in biology, including development and repair. Often, these processes occur via topological T1 transitions analogous to those observed in foams, grains, and colloids. However, in contrast to those in nonliving materials, the T1 transitions in biological tissues are rate limited and cannot occur instantaneously due to the finite time required to remodel complex structures at cell-cell junctions. Here, we study how this rate-limiting process affects the mechanics and collective behavior of cells in a tissue by introducing this important biological constraint in a theoretical vertex-based model as an intrinsic single-cell property. We report that, in the absence of this time constraint, the tissue undergoes a glass transition with lowering of cell motility characterized by a sharp increase in the intermittency of cell-cell rearrangements. Remarkably, this glass transition disappears, as T1 transitions are temporally limited. As a unique consequence of limited rearrangements, we also find that the tissue develops spatially correlated populations of fast and slow cells, in which the fast cells organize into streamlike patterns and maintain optimally stable cell-cell contacts. The predictions of this work are compared with existing in vivo experiments in Drosophila pupal development.