Stress ball morphogenesis: How the lizard builds its lung
Michael A. Palmer, Bryan A. Nerger, Katharine Goodwin, Anvitha Sudhakar, Sandra B. Lemke, Pavithran T. Ravindran, Jared E. Toettcher, Andrej Košmrlj, Celeste M. Nelson
Abstract
The function of the lung is closely coupled to its structural anatomy, which varies greatly across vertebrates. Although architecturally simple, a complex pattern of airflow is thought to be achieved in the lizard lung due to its cavernous central lumen and honeycomb-shaped wall. We find that the wall of the lizard lung is generated from an initially smooth epithelial sheet, which is pushed through holes in a hexagonal smooth muscle meshwork by forces from fluid pressure, similar to a stress ball. Combining transcriptomics with time-lapse imaging reveals that the hexagonal meshwork self-assembles in response to circumferential and axial stresses downstream of pressure. A computational model predicts the pressure-driven changes in epithelial topology, which we probe using optogenetically driven contraction of 3D-printed engineered muscle. These results reveal the physical principles used to sculpt the unusual architecture of the lizard lung, which could be exploited as a novel strategy to engineer tissues.