Emergent chirality in active solid rotation of pancreas spheres

Abstract

Collective cell dynamics play a crucial role in many developmental and physiological contexts. While two-dimensional (2D) cell migration has been widely studied, how three-dimensional (3D) geometry and topology interplay with collective cell behavior to determine dynamics and functions remains an open question. In this work, we elucidate the biophysical mechanism underlying rotation in spherical tissues, a phenomenon widely reported both and . Using murine pancreas-derived organoids as a model system, we find that epithelial spheres exhibit persistent rotation, rotational axis drift, and rotation arrest. Using a 3D vertex model, we demonstrate how the combined action of traction force and polarity alignment can account for these distinct rotational dynamics near a solid to flow transition. Furthermore, our analysis shows that the spherical tissue rotates as an active solid occasionally switching to a flowing state and exhibits spontaneous chiral symmetry breaking. Using a continuum model, we demonstrate how the topological defects in the polarity field underlie this symmetry breaking process, which is revealed by asymmetries in the cell elongation pattern. For cell elongation to reveal the chiral asymmetry, shear flow is required in addition to the solid body rotation. Altogether, our work reveals a robust chiral symmetry breaking mechanism with potential implications for left-right symmetry breaking processes in morphogenetic events. Published by the American Physical Society 2024