Fluctuation of Motor Charge in the Lateral Membrane of the Cochlear Outer Hair Cell

Dong, Xiaoxia; Ehrenstein, D.; Iwasa, Kuni H.

doi:10.1016/s0006-3495(00)76437-x

Cited by 26 publications

(34 citation statements)

References 17 publications

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“…We have seen above that the OHC motor can be stimulated to move at frequencies in excess of 50 kHz (56,57,100), and charge movement in the membrane can be measured at frequencies in excess of 30 kHz (73,109). On the basis of such observations, the motor charge in OHCs shares properties with charge translocation in transport proteins.…”

Section: B Biophysical Considerationsmentioning

confidence: 82%

Cochlear Outer Hair Cell Motility

Ashmore

2008

Physiological Reviews

398

391

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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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Section: B Biophysical Considerationsmentioning

confidence: 82%

Cochlear Outer Hair Cell Motility

Ashmore

2008

Physiological Reviews

398

391

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“…There have been a number of models proposed to explain the frequency (Iwasa, 1997; Dong et al, 2000) and voltage dependence of charge transfer by the membrane protein prestin (Oliver et al, 2001; Rybalchenko and Santos-Sacchi, 2003; Muallem and Ashmore, 2006). An early model (Iwasa, 1997; Dong et al, 2000) developed before the identification of prestin assumed that the outer hair cell motor (the charge) occupies two or three stable states where motor and charge transfer dynamics, including nonlinear capacitance and current noise, were described by hypothetical rate constants of switching from one state to the other.…”

Section: Resultsmentioning

confidence: 99%

“…An early model (Iwasa, 1997; Dong et al, 2000) developed before the identification of prestin assumed that the outer hair cell motor (the charge) occupies two or three stable states where motor and charge transfer dynamics, including nonlinear capacitance and current noise, were described by hypothetical rate constants of switching from one state to the other. Experimental observations revealed a critical role for chloride ions binding to prestin (Oliver et al, 2001).…”

Section: Resultsmentioning

confidence: 99%

Voltage and frequency dependence of prestin-associated charge transfer

Sun¹,

Farrell²,

Chana³

et al. 2009

Journal of Theoretical Biology

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Membrane protein prestin is a critical component of the motor complex that generates forces and dimensional changes in cells in response to changes in the cell membrane potential. In its native cochlear outer hair cell, prestin is crucial to the amplification and frequency selectivity of the mammalian ear up to frequencies of tens of kHz. Other cells transfected with prestin acquire voltage-dependent properties similar to those of the native cell. The protein performance is critically dependent on chloride ions, and intrinsic protein charges also play a role. We propose an electro-diffusion model to reveal the frequency and voltage dependence of electric charge transfer by prestin. The movement of the combined charge (i.e., anion and protein charges) across the membrane is described with a Fokker-Planck equation coupled to a kinetic equation that describes the binding of chloride ions to prestin. We found a voltage-and frequency-dependent phase shift between the transferred charge and the applied electric field that determines capacitive and resistive components of the transferred charge. The phase shift monotonically decreases from zero to -90 degree as a function of frequency. The capacitive component as a function of voltage is bell-shaped, and decreases with frequency. The resistive component is bell-shaped for both voltage and frequency. The capacitive and resistive components are similar to experimental measurements of charge transfer at high frequencies. The revealed nature of the transferred charge can help reconcile the high-frequency electrical and mechanical observations associated with prestin, and it is important for further analysis of the structure and function of this protein.

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“…In the OHC, membrane capacitance (C m ) arises from two superimposed components; one component (C v ) derives from gating charge movement owing to voltage-dependent activity of motor proteins within the lateral plasma membrane, while the other component (C sa ) derives from the intrinsic dielectric properties of all segments of its plasma membrane [2,8,37]. The latter component, often termed "linear" membrane capacitance, though typically considered independent of voltage, may co-vary with mechanisms, including voltage-dependent ones, that alter the underlying characteristics which define wholecell capacitance, namely the membrane's surface area, dielectric constant, or thickness.…”

Section: Discussionmentioning

confidence: 99%

Voltage-dependent changes in specific membrane capacitance caused by prestin, the outer hair cell lateral membrane motor

Santos‐Sacchi

Navarrete

2002

Pflügers Arch - Eur J Physiol

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In the outer hair cell (OHC), membrane capacitance principally derives from two components - that associated with lateral membrane sensor/motor charge movement, and that proportional to the membrane surface area (C(sa)). We used measures of membrane capacitance to test a model hypothesis that OHC lateral membrane molecular motors, recently identified as the protein prestin, fluctuate between two area states. By measuring membrane capacitance in native OHCs or prestin-transfected HEK cells at extreme voltages (+/-200 mV) where motor-derived charge movement is small or absent, we observed that C(sa) depends on the state of the motors, or correspondingly on membrane voltage. Deiters cells or control HEK cells, which lack motors, do not show this dependence. We modeled the voltage-dependent change in C(sa) as a Boltzmann process with the same parameters that describe the charge movement of the motors' voltage sensors. C(sa) is 3.28+/-0.75 pF (mean +/-SD; n=23) larger during extreme hyperpolarization, and the number of motors in OHCs and prestin-transfected HEK cells correlates with the magnitude of Delta C(sa)( r=0.78). Although these data are consistent with the area motor model, the corresponding area change, assuming 0.5 microF/cm(2) under constant membrane thickness, is unphysiologically large, and indicates that the capacitance change must result from changes not only in lateral membrane area but also specific capacitance. Thus, we conclude that a conformational change in the lateral membrane motor, prestin, additionally alters the dielectric constant and/or thickness of the lateral plasma membrane.

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Fluctuation of Motor Charge in the Lateral Membrane of the Cochlear Outer Hair Cell

Cited by 26 publications

References 17 publications

Cochlear Outer Hair Cell Motility

Cochlear Outer Hair Cell Motility

Voltage and frequency dependence of prestin-associated charge transfer

Voltage-dependent changes in specific membrane capacitance caused by prestin, the outer hair cell lateral membrane motor

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