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  • Open Access

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

Amit Das1, Srikanth Sastry2, and Dapeng Bi1

  • 1Department of Physics, Northeastern University, Boston, Massachusetts 02115, USA
  • 2Jawaharlal Nehru Centre for Advanced Scientific Research, Jakkur Campus, Bangalore 560064, India

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Phys. Rev. X 11, 041037 – Published 22 November, 2021

DOI: https://doi.org/10.1103/PhysRevX.11.041037

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.

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Popular Summary

Embryonic development, tissue repair, and cancer progression all rely on neighboring cells rearranging themselves in biological tissue. One basic unit of such movement of cells in close-packed tissues is the T1 transition, where two cells swap positions. Because of the time required to remodel complex structures at junctions between cells, T1 transition cannot occur instantaneously. How this biological constraint affects collective behaviors among cells inside tissues is not known. Using theoretical modeling and simulations, we demonstrate that cell-level control of the time it takes to complete a T1 transition has unique consequences that change the ways cells mechanically interact, collectively organize, and migrate.

Using a model of cellular dynamics in 2D sheets of cells, we find that in the absence of a time constraint on T1 transitions, the tissue undergoes a transition from a liquidlike state to a glassy solidlike state as the speed of single cells decreases. However, this liquid-to-glass transition gradually disappears as T1 transitions become hindered. As that happens, we also find that the tissue develops a population of mobile cells organized into streamlike patterns in the background of slow or completely static cells. We call this the active streaming glassy state, which has the classic hallmarks of cell streaming observed in invasive cancer tumors. Exploring the origins of this phenomenon, we discover that as the T1 time constraint grows, the tissue develops optimally stable cell collectives that selectively undergo directionally polarized T1 transitions and eventually morph into elongated cellular streams.

The dynamic cell-cell adhesions introduced in this work make several experimentally testable predictions related to cell migration in animal development and cancer, which will open the door to future experiments.

Article Text

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Phys. Rev. X 11, 041037– Published 22 November, 2021
  • Received 1 May 2020
  • Revised 23 August 2021
  • Accepted 23 September 2021
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