Modeling the Mechanics of Tethers Pulled From the Cochlear Outer Hair Cell Membrane

Cell membrane tethers are formed naturally (e.g., in leukocyte rolling) and experimentally to probe membrane properties. In cochlear outer hair cells, the plasma membrane is part of the trilayer lateral wall, where the membrane is attached to the cytoskeleton by a system of radial pillars. The mechanics of these cells is important to the sound amplification and frequency selectivity of the ear. We present a modeling study to simulate the membrane deflection, bending, and interaction with the cytoskeleton in the outer hair cell tether pulling experiment. In our analysis, three regions of the membrane are considered: the body of a cylindrical tether, the area where the membrane is attached and interacts with the cytoskeleton, and the transition region between the two. By using a computational method, we found the shape of the membrane in all three regions over a range of tether lengths and forces observed in experiments. We also analyze the effects of biophysical properties of the membrane, including the bending modulus and the forces of the membrane adhesion to the cytoskeleton. The model’s results provide a better understanding of the mechanics of tethers pulled from cell membranes.

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Theory of electrically driven shape changes of cochlear outer hair cells

Journal of Neurophysiology ◽

10.1152/jn.1993.70.1.299 ◽

1993 ◽

Vol 70 (1) ◽

pp. 299-323 ◽

Cited By ~ 86

Author(s):

P. Dallos ◽

R. Hallworth ◽

B. N. Evans

Keyword(s):

Cell Membrane ◽

Hair Cell ◽

Outer Hair Cell ◽

Linear Motor ◽

Outer Hair Cells ◽

Pressure Effects ◽

Model Parameters ◽

Minor Importance ◽

Length Changes ◽

Shape Changes

1. A theory of cochlear outer hair cell electromotility is developed and specifically applied to somatic shape changes elicited in a microchamber. The microchamber permits the arbitrary electrical and mechanical partitioning of the outer hair cell along its length. This means that the two partitioned segments are stimulated with different input voltages and undergo different shape changes. Consequently, by imposing more constraints than other methods, experiments in the microchamber are particularly suitable for testing different theories of outer hair cell motility. 2. The present model is based on simple hypotheses. They include a distributed motor associated with the cell membrane or cortex and the assumption that the displacement generated by the motor is related to the transmembrane voltage across the associated membrane element. It is expected that the force generated by the motor is counterbalanced by an elastic restoring force indigenous to the cell membrane and cortex, and a tensile force due to intracellular pressure. It is assumed that all changes take place while total cell volume is conserved. The above elements of the theory taken together permit the development of qualitative and quantitative predictions about the expected motile responses of both partitioned segments of the cell. Only a DC treatment is offered here. 3. Both a linear motor and an expanded treatment that incorporates a stochastic molecular motor model are considered. The latter is represented by a two-state Boltzmann process. We show that the linear motor treatment is an appropriate extrapolation of the stochastic motor theory for the case of small voltage driving signals. Comparison of experimental results with model responses permits the estimation of model parameters. Good match of data is obtained if it is assumed that the molecular motors undergo conformational length changes of 0.7-1.0 nm, that they have an effective displacement vector at approximately -20 degrees with the long axis of the cell, and that their linear density is approximately 80/microns. 4. An effort is made to parcel out motile response components that are a direct consequence of the motor action from those that are mediated by cytoplasmic pressure changes brought about by the concerted action of the motors. We show that pressure effects are of minor importance, and thus rule out models that rely on radial constriction/expansion-mediated internal pressure change as the primary cause of longitudinal motility. 5. As a consequence of the interaction between the Boltzmann process and the mechanical characteristics of the cell, the electromotile response is asymmetric.(ABSTRACT TRUNCATED AT 400 WORDS)

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Cochlear Outer Hair Cell Motility

Physiological Reviews ◽

10.1152/physrev.00044.2006 ◽

2008 ◽

Vol 88 (1) ◽

pp. 173-210 ◽

Cited By ~ 262

Author(s):

Jonathan Ashmore

Keyword(s):

Hair Cell ◽

Cell Motility ◽

Hair Cells ◽

Outer Hair Cell ◽

Outer Hair Cells ◽

Critical Question ◽

Outer Hair Cell Motility ◽

Sensory Hair Cells ◽

Sound Amplification ◽

Motor Cells

Normal hearing depends on sound amplification within the mammalian cochlea. The amplification, without which the auditory system is effectively deaf, can be traced to the correct functioning of a group of motile sensory hair cells, the outer hair cells of the cochlea. Acting like motor cells, outer hair cells produce forces that are driven by graded changes in membrane potential. The forces depend on the presence of a motor protein in the lateral membrane of the cells. This protein, known as prestin, is a member of a transporter superfamily SLC26. The functional and structural properties of prestin are described in this review. Whether outer hair cell motility might account for sound amplification at all frequencies is also a critical question and is reviewed here.

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3D Ultrastructure of the Cochlear Outer Hair Cell Lateral Wall Revealed By Electron Tomography

10.1101/534222 ◽

2019 ◽

Author(s):

William Jeffrey Triffo ◽

Hildur Palsdottir ◽

David Gene Morgan ◽

Kent L. McDonald ◽

Robert M. Raphael ◽

...

Keyword(s):

Plasma Membrane ◽

Hair Cell ◽

Actin Filaments ◽

Computational Models ◽

Outer Hair Cell ◽

Electron Tomography ◽

3D Structure ◽

Lateral Wall ◽

Outer Hair Cells ◽

Unique Type

AbstractOuter hair cells in the mammalian cochlea display a unique type of voltage-induced mechanical movement, termed electromotility, which amplifies auditory signals and contributes to the sensitivity and frequency selectivity of mammalian hearing. Electromotility occurs in the outer hair cell (OHC) lateral wall, and it is not fully understood how the supramolecular architecture of the lateral wall enables this unique form of cellular motility. Employing electron tomography of high-pressure frozen and freeze-substituted OHCs, we visualized the 3D structure and organization of the membrane and cytoskeletal components of the OHC lateral wall. The subsurface cisterna (SSC) is a highly prominent feature, and we report that the SSC membranes and lumen possess hexagonally ordered arrays of particles that endow the SSC with a previously unrealized anisotropic structural rigidity. We also find the SSC is tightly connected to adjacent actin filaments by short filamentous protein connections spaced at regular intervals. Pillar proteins that join the plasma membrane to the cytoskeleton appear as variable structures considerably thinner than actin filaments and significantly more flexible than actin-SSC links. The structurally rich organization and rigidity of the SSC coupled with apparently weaker mechanical connections between the plasma membrane and cytoskeleton reveal that the membrane-cytoskeletal architecture of the OHC lateral wall is more complex than previously appreciated. These observations are important for our understanding of OHC mechanics and need to be considered in computational models of OHC electromotility that incorporate subcellular features.

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Filtering Due to the Inner Hair-Cell Membrane Properties and its Relation to the Phase-Locking Limit in Cochlear Nerve Fibres

Auditory Frequency Selectivity ◽

10.1007/978-1-4613-2247-4_23 ◽

1986 ◽

pp. 199-207 ◽

Cited By ~ 1

Author(s):

Ian Russell ◽

Alan Palmer

Keyword(s):

Cell Membrane ◽

Hair Cell ◽

Phase Locking ◽

Cochlear Nerve ◽

Membrane Properties ◽

Inner Hair Cell ◽

Nerve Fibres

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Elastic moduli of the piezoelectric cochlear outer hair cell membrane

Experimental Mechanics ◽

10.1007/bf02410535 ◽

2003 ◽

Vol 43 (3) ◽

pp. 355-360 ◽

Cited By ~ 6

Author(s):

A. A. Spector ◽

R. P. Jean

Keyword(s):

Cell Membrane ◽

Hair Cell ◽

Elastic Moduli ◽

Outer Hair Cell

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Early Evidence of Cochlear Damage in a Large Sample of Percussionists

Medical Problems of Performing Artists ◽

10.21091/mppa.2005.3027 ◽

2005 ◽

Vol 20 (3) ◽

pp. 135-139

Author(s):

Jodee A Pride ◽

David R Cunningham

Keyword(s):

Hearing Loss ◽

Hair Cell ◽

Otoacoustic Emissions ◽

Outer Hair Cell ◽

Cell Damage ◽

Normal Hearing ◽

Outer Hair Cells ◽

Sensory Loss ◽

Distortion Product ◽

Hair Cell Damage

Percussionists can be exposed to intermittent sound stimuli that exceed 145 dB SPL, although damage may occur to the outer hair cells at levels of 120 dB SPL. The present study measured distortion-product otoacoustic emissions (DPOAEs) in a group of 86 normal-hearing percussionists and 39 normal-hearing nonpercussionists. Results indicate that normal-hearing percussionists have lower DPOAE amplitudes than normal-hearing nonpercussionists. DPOAE amplitudes were significantly lower at 6000 Hz in both the left and right ears for percussionists. Percussionists also more frequently had absent DPOAEs, with the greatest differences occurring at 6000 Hz (absent DPOAEs in 25% of percussionists vs 10% of nonpercussionists). When all frequencies are considered as a group, 33% of the percussionists had an absent DPOAE in either ear at some frequency, compared to only 23% of the nonpercussionists. Otoacoustic emissions are more sensitive to outer hair cell damage than pure-tone threshold measurements and can serve as an important measurement of sensory loss (i.e., outer hair cell damage) in musicians before the person perceives the hearing loss. DPOAE monitoring for musicians, along with appropriate education and intervention, might help prevent or minimize music-induced hearing loss.

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