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The development of cooperative channels explains the maturation of hair cell’s mechanotransduction

View ORCID ProfileFrancesco Gianoli, View ORCID ProfileThomas Risler, View ORCID ProfileAndrei S. Kozlov
doi: https://doi.org/10.1101/654764
Francesco Gianoli
Department of Bioengineering, Imperial College London, London SW7 2AZ, United Kingdom
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Thomas Risler
Laboratoire Physico-Chimie Curie, Institut Curie, PSL Research University, Sorbonne Université, CNRS, 26 rue d’Ulm, 75005 Paris, France
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  • For correspondence: a.kozlov@imperial.ac.uk thomas.risler@curie.fr
Andrei S. Kozlov
Department of Bioengineering, Imperial College London, London SW7 2AZ, United Kingdom
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  • ORCID record for Andrei S. Kozlov
  • For correspondence: a.kozlov@imperial.ac.uk thomas.risler@curie.fr
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ABSTRACT

Hearing relies on the conversion of mechanical stimuli into electrical signals. In vertebrates, this process of mechano-electrical transduction (MET) is performed by specialized receptors of the inner ear, the hair cells. Each hair cell is crowned by a hair bundle, a cluster of microvilli that pivot in response to sound vibrations, causing the opening and closing of mechanosensitive ion channels. Mechanical forces are projected onto the channels by molecular springs called tip links. Each tip link is thought to connect to a small number of MET channels that gate cooperatively and operate as a single transduction unit. Pushing the hair bundle in the excitatory direction opens the channels, after which they rapidly reclose in a process called fast adaptation. It has been experimentally observed that the hair cell’s biophysical properties mature gradually during postnatal development: the maximal transduction current increases, sensitivity sharpens, transduction occurs at smaller hair-bundle displacements, and adaptation becomes faster. Similar observations have been reported during tip-link regeneration after acoustic damage. Moreover, when measured at intermediate developmental stages, the kinetics of fast adaptation varies in a given cell depending on the magnitude of the imposed displacement. The mechanisms underlying these seemingly disparate observations have so far remained elusive. Here, we show that these phenomena can all be explained by the progressive addition of MET channels of constant properties, which populate the hair bundle first as isolated entities, then progressively as clusters of more sensitive, cooperative MET channels. As the proposed mechanism relies on the difference in biophysical properties between isolated and clustered channels, this work highlights the importance of cooperative interactions between mechanosensitive ion channels for hearing.

SIGNIFICANCE Hair cells are the sensory receptors of the inner ear that convert mechanical stimuli into electrical signals transmitted to the brain. Sensitivity to mechanical stimuli and the kinetics of mechanotransduction currents change during hair-cell development. The same trend, albeit on a shorter timescale, is also observed during hair-cell recovery from acoustic trauma. Furthermore, the current kinetics in a given hair cell depends on the stimulus magnitude, and the degree of that dependence varies with development. These phenomena have so far remained unexplained. Here, we show that they can all be reproduced using a single unifying mechanism: the progressive formation of channel pairs, in which individual channels interact through the lipid bilayer and gate cooperatively.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted June 12, 2019.
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The development of cooperative channels explains the maturation of hair cell’s mechanotransduction
Francesco Gianoli, Thomas Risler, Andrei S. Kozlov
bioRxiv 654764; doi: https://doi.org/10.1101/654764
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The development of cooperative channels explains the maturation of hair cell’s mechanotransduction
Francesco Gianoli, Thomas Risler, Andrei S. Kozlov
bioRxiv 654764; doi: https://doi.org/10.1101/654764

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