Physical explanation of coupled cell-cell rotational behavior and interfacial morphology: a particle dynamics model

Previous studies have reported persistent rotational behavior between adherent cell-cell pairs cultured on micropatterned substrates, and this rotation is often accompanied by a sigmoidal deflection of the cell-cell interface. Interestingly, the cell-cell rotation runs in the opposite reference frame from what could be expected of single cell locomotion. Specifically, the rotation of the cell pair consists of each individual cell protruding from the inwardly regressive arm of the cell-cell interface, and retracting from the other outwardly protrusive arm. To this author's knowledge, the cause of this elusive behavior has not yet been clarified. Here, we propose a physical model based on particle dynamics, accounting for actomyosin forcing, viscous dissipation, and cortical tension. The results show that a correlation in actomyosin force vectors leads to both persistent rotational behavior and interfacial deflection in a simulated cell cluster. Significantly, the model, without any artificial cues, spontaneously and consistently reproduces the same rotational reference frame as experimentally observed. Further analyses show that the interfacial deflection depends predominantly on cortical tension, whereas the cluster rotation depends predominantly on actomyosin forcing. Together, these results corroborate the hypothesis that both rotational and morphological phenomena are, in fact, physically coupled by an intracellular torque of a common origin.