title: Transduction channels' gating can control friction on vibrating hair-cell bundles in the ear.
abstract: Hearing starts when sound-evoked mechanical vibrations of the hair-cell bundle activate mechanosensitive ion channels, giving birth to an electrical signal. As for any mechanical system, friction impedes movements of the hair bundle and thus constrains the sensitivity and frequency selectivity of auditory transduction. Friction is generally thought to result mainly from viscous drag by the surrounding fluid. We demonstrate here that the opening and closing of the transduction channels produce internal frictional forces that can dominate viscous drag on the micrometer-sized hair bundle. We characterized friction by analyzing hysteresis in the force-displacement relation of single hair-cell bundles in response to periodic triangular stimuli. For bundle velocities high enough to outrun adaptation, we found that frictional forces were maximal within the narrow region of deflections that elicited significant channel gating, plummeted upon application of a channel blocker, and displayed a sublinear growth for increasing bundle velocity. At low velocity, the slope of the relation between the frictional force and velocity was nearly fivefold larger than the hydrodynamic friction coefficient that was measured when the transduction machinery was decoupled from bundle motion by severing tip links. A theoretical analysis reveals that channel friction arises from coupling the dynamics of the conformational change associated with channel gating to tip-link tension. Varying channel properties affects friction, with faster channels producing smaller friction. We propose that this intrinsic source of friction may contribute to the process that sets the hair cell's characteristic frequency of responsiveness.
authors.affiliation: Laboratoire Physico-Chimie Curie, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 168, F-75248 Paris, France;Institut Curie, Centre de recherche, F-75248 Paris, France;Université Pierre et Marie Curie, F-75252 Paris, France;
authors.forename: Volker
authors.initials: V
authors.lastname: Bormuth
authors.affiliation: Laboratoire Physico-Chimie Curie, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 168, F-75248 Paris, France;Institut Curie, Centre de recherche, F-75248 Paris, France;Université Pierre et Marie Curie, F-75252 Paris, France;
authors.forename: Jérémie
authors.initials: J
authors.lastname: Barral
authors.affiliation: Laboratoire Physico-Chimie Curie, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 168, F-75248 Paris, France;Institut Curie, Centre de recherche, F-75248 Paris, France;Université Pierre et Marie Curie, F-75252 Paris, France;École Supérieure de Physique et de Chimie Industrielles Paris Tech, F-75231 Paris, France; and.
authors.forename: Jean-François
authors.initials: JF
authors.lastname: Joanny
authors.affiliation: Max Planck Institute for the Physics of Complex Systems, D-01187 Dresden, Germany.
authors.forename: Frank
authors.initials: F
authors.lastname: Jülicher
authors.affiliation: Laboratoire Physico-Chimie Curie, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 168, F-75248 Paris, France;Institut Curie, Centre de recherche, F-75248 Paris, France;Université Pierre et Marie Curie, F-75252 Paris, France; pascal.martin@curie.fr.
authors.forename: Pascal
authors.initials: P
authors.lastname: Martin
mesh_terms: D000818:Animals; D002118:Calcium / Q000737:chemistry; D002614:Chelating Agents / Q000737:chemistry; D004423:Ear / Q000502:physiology; D017276:Friction; D005839:Gentamicins / Q000737:chemistry; D006198:Hair Cells, Auditory / Q000502:physiology*; D006309:Hearing / Q000502:physiology*; D057446:Hydrodynamics; D015640:Ion Channel Gating / Q000502:physiology*; D007473:Ion Channels / Q000737:chemistry; D007478:Iontophoresis; D011892:Rana catesbeiana; D012815:Signal Processing, Computer-Assisted; D015398:Signal Transduction; D013314:Stress, Mechanical; D013816:Thermodynamics; D014732:Vibration
chemical_list: D002614:Chelating Agents; D005839:Gentamicins; D007473:Ion Channels; D002118:Calcium
keywords: auditory system; cell mechanics; hair-bundle mechanosensitivity; mechanosensitive channels; protein friction