Mechanical coupling of compartments drives polarity and patterning of mouse auditory epithelium

Morphogenetic information arises from a combination of genetically encoded cellular properties and emergent cellular behaviours. The spatio-temporal implementation of this information is critical to ensure robust, reproducible tissue shapes, yet the principles underlying its organisation remain unknown. We investigated this principle using the mouse auditory epithelium, the organ of Corti (OC). OC consists of a sensory domain, which transduces sound through polar mechanosensory hair cells (HC), part of a mosaic with supporting cells (SC). On either side of the sensory domain are non-sensory domains. These domains undergo cellular rearrangements, which, together, lead to a spiral cochlea that contains planar polarised HCs. This makes the mammalian cochlea a compelling system to understand coordination across spatial scales. Using genetic and ex-vivo approaches, we found patterning of OC into sensory and non-sensory domains is associated with a combinatorial expression of adhesion molecules, which underpins OC into spatially defined compartments, enabling planar cell polarity (PCP) cues to regulate compartment-specific organisation. Through compartment-specific knockouts of the PCP protein, Vangl2, we find evidence of compartment coupling, a non-linear influence on the organisation within one compartment when cellular organisation is disrupted in another. In the OC, compartment coupling originates from vinculin-dependent junctional mechanics, coordinating cellular dynamics across spatial scales. Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=115 SRC="FIGDIR/small/613243v2_ufig1.gif" ALT="Figure 1"> View larger version (45K): org.highwire.dtl.DTLVardef@11d31c1org.highwire.dtl.DTLVardef@1ad85dcorg.highwire.dtl.DTLVardef@12f4a0corg.highwire.dtl.DTLVardef@1a663ab_HPS_FORMAT_FIGEXP M_FIG C_FIG