Filopodial-Tension Model of Convergent-Extension of Tissues

In convergent-extension (CE), a planar-polarized epithelial tissue elongates (extends) in-plane in one direction while shortening (converging) in the perpendicular in-plane direction, with the cells both elongating and intercalating along the converging axis. CE occurs during the development of most multicellular organisms. Current CE models assume cell or tissue asymmetry, but neglect the preferential filopodial activity along the convergent axis observed in many tissues. We propose a cell-based CE model based on asymmetric filopodial tension forces between cells and investigate how cell-level filopodial interactions drive tissue-level CE. The final tissue geometry depends on the balance between external rounding forces and cell-intercalation traction. Filopodial-tension CE is robust to relatively high levels of planar cell polarity misalignment and to the presence of non-active cells. Addition of a simple mechanical feedback between cells fully rescues and even improves CE of tissues with high levels of polarity misalignments. Our model extends easily to three dimensions, with either one converging and two extending axes, or two converging and one extending axes, producing distinct tissue morphologies, as observed in vivo.Author Summary: The development of an embryo from a fertilized egg to an adult organism requires not only cell proliferation and differentiation, but also numerous types of tissue restructuring. The development of a relatively round initial embryo into one elongated along its rostral-caudal axis involves coordinated tissue elongation and cell reorganization in one or more groups of cells or tissues. Counterintuitively, in many organisms, cells in elongating tissues elongate and increase their protrusive activity in the direction perpendicular to the axis of elongation (convergent extension). Experimental and theoretical studies have not determined how this cell-level oriented protrusive activity leads to observed tissue-level changes in morphology. We propose a filopodial-tension model that shows how tension from oriented cell protrusions leads to observed patterns of tissue CE.