Mechanical forces drive ordered patterning of hair cells in the mammalian inner ear

Roie Cohen,Shiran Woland,Fumio Matsuzaki,Liat Amir-Zilberstein,David Sprinzak,Micha Hersch,Sven Bergmann,Olga Loza,Karen B Avraham,Shahar Taiber

doi:10.1038/s41467-020-18894-8

Abstract

Periodic organization of cells is required for the function of many organs and tissues. The development of such periodic patterns is typically associated with mechanisms based on intercellular signaling such as lateral inhibition and Turing patterning. Here we show that the transition from disordered to ordered checkerboard-like pattern of hair cells and supporting cells in the mammalian hearing organ, the organ of Corti, is likely based on mechanical forces rather than signaling events. Using time-lapse imaging of mouse cochlear explants, we show that hair cells rearrange gradually into a checkerboard-like pattern through a tissue-wide shear motion that coordinates intercalation and delamination events. Using mechanical models of the tissue, we show that global shear and local repulsion forces on hair cells are sufficient to drive the transition from disordered to ordered cellular pattern. Our findings suggest that mechanical forces drive ordered hair cell patterning in a process strikingly analogous to the process of shear-induced crystallization in polymer and granular physics.

Highlights

Periodic organization of cells is required for the function of many organs and tissues
The mature organ of Corti is a strip of epithelial cells that extends along the base-to-apex axis within the cochlear duct (Fig. 1a, b) which comprises of exactly four rows of hair cells (HCs), three rows of outer hair cells (OHCs) and one row inner hair cells (IHCs), regularly interspersed by non-sensory supporting cells (SCs)
To determine the processes that drive the transition from a disordered undifferentiated tissue to an ordered pattern of HCs and SCs we first quantitatively analyzed the morphological changes that occur in the organ of Corti in space and time

Summary

Introduction

Periodic organization of cells is required for the function of many organs and tissues The development of such periodic patterns is typically associated with mechanisms based on intercellular signaling such as lateral inhibition and Turing patterning. We show that the transition from disordered to ordered checkerboard-like pattern of hair cells and supporting cells in the mammalian hearing organ, the organ of Corti, is likely based on mechanical forces rather than signaling events. Using time-lapse imaging of mouse cochlear explants, we show that hair cells rearrange gradually into a checkerboard-like pattern through a tissue-wide shear motion that coordinates intercalation and delamination events. Using mechanical models of the tissue, we show that global shear and local repulsion forces on hair cells are sufficient to drive the transition from disordered to ordered cellular pattern. No significant cell division or cell death events are observed within the organ of Corti during this process[4,8]

Methods

Results

Conclusion