A hierarchy of protein patterns robustly decodes cell shape information

Abstract

Many cellular processes, such as cell division1–3, cell motility4, wound healing5 and tissue folding6,7, rely on the precise positioning of proteins on the membrane. Such protein patterns emerge from a combination of protein interactions, transport, conformational state changes and chemical reactions at the molecular level8. Recent experimental and theoretical work clearly demonstrates the role of geometry, including membrane curvature9–11 and local cytosolic-to-membrane ratios12,13, and advective cortical flow in modulating membrane protein patterns. However, it remains unclear how these proteins achieve robust spatiotemporal organization on the membrane during the dynamic cell shape changes involved in physiological processes. Here we use oocytes of the starfish Patiria miniata as a model system to elucidate a shape-adaptation mechanism that robustly controls spatiotemporal protein dynamics on the membrane in spite of cell shape deformations. By combining experiments with biophysical theory, we show how cell shape information contained in a cytosolic gradient can be decoded by a bistable regulator of the enzyme Rho, which is associated with contractility. This bistable front in turn controls a mechanochemical response by locally triggering excitable dynamics of Rho. We posit that such a shape-adaptation mechanism based on a hierarchy of protein patterns may constitute a general physical principle for cell shape sensing and control. Cells exploit protein pattern formation to perform key processes, and do so while undergoing major shape changes. Experiments and theory together reveal a shape-adaptation mechanism capable of controlling protein dynamics even as the cell deforms.