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The Development of Cooperative Channels Explains the Maturation of Hair Cell’s Mechanotransduction
- Source :
- Biophysical Journal, Biophysical Journal, Biophysical Society, 2019, 117 (8), pp.1536-1548. ⟨10.1016/j.bpj.2019.08.042⟩
- Publication Year :
- 2019
- Publisher :
- HAL CCSD, 2019.
-
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.SIGNIFICANCEHair 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.
- Subjects :
- [PHYS.PHYS.PHYS-BIO-PH]Physics [physics]/Physics [physics]/Biological Physics [physics.bio-ph]
Models, Neurological
Biophysics
Mechanotransduction, Cellular
Ion Channels
Mice
03 medical and health sciences
0302 clinical medicine
Hair Cells, Auditory
medicine
otorhinolaryngologic diseases
Animals
Inner ear
Mechanotransduction
[PHYS.MECA.BIOM]Physics [physics]/Mechanics [physics]/Biomechanics [physics.med-ph]
Ion channel
030304 developmental biology
Physics
0303 health sciences
02 Physical Sciences
Cell Differentiation
Articles
06 Biological Sciences
medicine.anatomical_structure
Excitatory postsynaptic potential
Mechanosensitive channels
sense organs
Hair cell
03 Chemical Sciences
Ion Channel Gating
Transduction (physiology)
Tip link
030217 neurology & neurosurgery
Subjects
Details
- Language :
- English
- ISSN :
- 00063495 and 15420086
- Database :
- OpenAIRE
- Journal :
- Biophysical Journal, Biophysical Journal, Biophysical Society, 2019, 117 (8), pp.1536-1548. ⟨10.1016/j.bpj.2019.08.042⟩
- Accession number :
- edsair.doi.dedup.....8c9480e7ed02ae0373da51fe0968aa28