Abstract

Hair cells are specialized sensors located in the inner ear that enable the transduction of sound, motion, and gravity into neuronal impulses. In birds some hair cells contain an iron-rich organelle, the cuticulosome, that has been implicated in the magnetic sense. Here, we exploit histological, transcriptomic, and tomographic methods to investigate the development of cuticulosomes, as well as the molecular and subcellular architecture of cuticulosome positive hair cells. We show that this organelle forms rapidly after hatching in a process that involves vesicle fusion and nucleation of ferritin nanoparticles. We further report that transcripts involved in endocytosis, extracellular exosomes, and metal ion binding are differentially expressed in cuticulosome positive hair cells. These data suggest that the cuticulosome and the associated molecular machinery regulate the concentration of iron within the labyrinth of the inner ear, which might indirectly tune a magnetic sensor that relies on electromagnetic induction.

Highlights

  • Hair cells are located in defined sensory epithelia within the vertebrate inner ear, enabling the transduction of sound, motion, and gravity into neuronal impulses (Torres and Giraldez, 1998)

  • Stereocilia are composed of tightly packed parallel filaments of f-actin, which taper at their base forming a rootlet that inserts into the cuticular plate (Pollock and McDermott, 2015)

  • The kinocillium, with its distinctive core of microtubules, inserts into the cuticular plate serving as an important guidepost for stereocilia development and orientation (Montcouquiol et al, 2003)

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Summary

Introduction

Hair cells are located in defined sensory epithelia within the vertebrate inner ear, enabling the transduction of sound, motion, and gravity into neuronal impulses (Torres and Giraldez, 1998) This is mediated by mechanical deflection of stereocilia, which are bristle-like projections that emerge from the apical surface of the cell. The kinocillium, with its distinctive core of microtubules, inserts into the cuticular plate serving as an important guidepost for stereocilia development and orientation (Montcouquiol et al, 2003). These unique structures were initially identified using transmission electron microscopy, but have been further characterized using electron tomographic methods. Insight into the molecules that are required to construct them has resulted primarily from genetic and transcriptomic studies in various model systems (Mburu et al, 2003; Kitajiri et al, 2010; Antonellis et al, 2014; Liu et al, 2014)

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