Three-ring circus without a ringmaster: Self-organization of supracellular actin ring patterns during epithelial morphogenesis

Formation of patterns during development has been a long-standing puzzle. Alan Turing proposed chemical gradients as a solution to the problem (1), and many chemical signals that pattern cells have since been found. However, only recently have roles for mechanical forces in patterning become apparent (2–6). In PNAS, Hannezo et al. (7) present and test a biophysical model involving three key elements—actin, myosin II, and anisotropic "effective friction" arising from interactions with the extracellular matrix (ECM)—that recapitulates the formation of the periodic subcellular actin bundles that coherently span several cells to form rings in the developing Drosophila tracheal (airway) tubes (Fig. 1A). Strikingly, although the mechanism of ring formation was previously unknown, Hannezo et al.’s model predicts that formation of the bundles, as well as their periodicity and orientation, will arise within each cell through self-organization. Experimental tests of predictions of the model show that it correctly describes multiple unexpected behaviors of the system in vivo, including imperfections in the actin rings (Fig. 1 B and C) and the formation of only a single unanchored actin ring per cell when the ECM is eliminated. Hannezo et al.’s work provides a mechanistic basis for understanding formation of patterned actin ring structures in Drosophila and other species, and highlights the potential of the ECM to influence actin organization through mechanical rather than biochemical signaling interactions.