The magnificent outer hair cell of Corti's organ
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1 The magnificent outer hair cell of Corti's organ Yale University J. Santos-Sacchi School of Medicine, New Haver, CT, USA Abstract The outer hair cell is one of two receptor cell types in the organ of Corti. It alone, however, functions as both receptor and mechanical effector. It is currently held that this cell is the basis of the cochlear amplifier. In this presentation, a brief overview is provided on selected aspects of the cell's mechanical activity. The original work of von Bekesy (1960), which won him the Nobel prize in Medicine in 1961, heralded the modern era of cochlea neurobiology, where cochlear micromechanics would be a prime target of intense research. Improvements in technologies to measure basilar membrane motion extended Bekesy's observations by demonstrating not only that the basilar membrane was as sharply tuned as eighth nerve fibers, but that compressive nonlinearity was present in its motion (see Ruggero and Santos-Sacchi, 1998). It is now know that this nonlinearity is a characteristic of the cochlear amplifier that promotes the exquisite sense of hearing that mammals enjoy. The metabolic lability of the cochlea amplifier identifies the chief component of this system as cellular in nature. in the OHC membrane does not interfere with movements induced under in vitro voltage clamp stimulation (Santos-Sacchi and Dilger, 1988) Furthermore, the existence of a voltage dependent process within the OHC lateral membrane suggests that a charged voltage sensor should reside within the membrane, as exists for voltage-gated ionic channels. Charge movement associated with such a voltage sensor has been demonstrated (Ashmore, 1989) and many of its characteristics (e.g., voltage dependence, and susceptivility to certain blocking agents) are similar to motility characteristics (Santos-Sacchi, 1990; 1991). Finally, the speed of both the mechanical response and charge movement is directly related to the speed of the voltage change across the OHC membrane, and for AC stimulation, the phase of the motility corresponds to the phase of transmembrane voltage, not current Brownell discovered that isolated outer hair cells, but neither inner hair cells nor supporting cells, change their length when stimulated electrically (Brownell et al., 1985; Kachar et al., 1986). The underlying mechanism is unlike any other form of cellular motility (Ashmore and Meech, 1986 ; Kachar et al., 1986; Holley and Ashmore, 1988 ; Santos-Sacchi and Dilger, 1988), and despite the existence of numerous models, remains unidentified to this day. (Santos-Sacchi, 1992). The voltage dependent nature of OHC motility and the Boltzmann characteristics of the nonlinear charge movement (up to 3 pc per OHC [for apical OHCs] or equivalently a voltage dependent capacitance of `20 pf) indicate that the mechanical response is dependent upon discrete sensor-motor elements within the plasma membrane (Santos-Sacchi, 1991a; Huang and Santos-Sacchi, 1993b). From these data it is estimated that the number of voltage sensors within the plasma membrane is about /ƒÊm2, Although, the mechanism is unknown, there is a wealth of evidence indicating that the phenomenon relies on transmembrane potential. Thus, it has been shown that blockade of the various ionic conductances somewhat similar to the number of intramembranous 10nm particles observed with freeze-fracture or surface freeze-etch electronmicroscopy (Gulley and Reese, 1977; Forge, 1989; Kalinec et al., 1991; however, see Santos-Sacchi
2 et al., 1998b). Indeed, Dallos et al. (1991) have convincingly shown with their microchamber technique that the total length change is the sum of many independent mechanical elements along the lateral surface of the cell. Huang and Santos-Sacchi have similarly demonstrated, using a combined microchamber (1993b) and whole cell voltage clamp, that independent motility voltage sensors are distributed along the central extent of the OHC length. With the same technique it was recently shown that the voltage dependent conductances of the OHC reside exclusively in the basal pole of the cell (Santos-Sacchi et al., 1997). Thus, the OHC possesses an amazingly compartmentalized plasma membrane (Fig.1). Apical membrane-stereocilia mechano-electrical transduction Lateral membraneelectro-mechanical transduction Basal membrane-synaptic pole voltage dependent conductances Fig.1 The OHC has a highly compartmentalized membrane. Apical, lateral and basal membranes possess characteristic membrane constituents. Blow-up depicts molecular motors in lateral membrane. The voltage-to-mechanical response (V-(YL)function of the OHC, thus, derives from the statistical properties of its elementary voltage sensors and the coupling of these sensors to elementary displacement effectors. This coupling, at least in the longitudinal direction, has been shown to depend upon cell turgor or cytoplasmic volume (Holley and Ashmore, 1988; Brownell et al., 1989; Santos-Sacchi, 1991a). Reduction of cytoplasmic volume reduces or abolishes voltage dependent length changes in OHCs. Sensing of the voltage stimulus is not impaired, however, as is evident by relatively unperturbed charge movement within the membrane during turgor reduction (Santos-Sacchi, 1991). Interestingly, the motor component may reside solely within the plasma membrane, since disruption of intracellular structural elements adjacent to the plasma membrane does not abolish voltage-dependent membrane deformation (Kalinec et al., 1992). This results has been confirmed and extended by observing that, in addition to the mechanical response, the nonlinear charge movement (voltage sensor) is also resistant to the effects of intracellular of the plasma membrane trypsin, and is localized within the plane (Huang and Santos-Sacchi, 1994). A further line of evidence linking mechanical response to the nonlinear capacitance was recently obtained by inducing nonlinear capacitance changes by mechanical deformation of the OHC membrane (Iwasa, 1993; Gale and Ashmore, 1994; Kakehata Santos-Sacchi, 1995). The V- bl function is sigmoidal or Boltzmann-like and (Santos-Sacchi, 1989b; Evans et al., 1989), and begins to saturate in the depolarizing direction at voltages well above physiologically meaningful values (Fig. 2; Santos-Sacchi and Dilger, 1988). However, saturation of the mechanical response in the hyperpolarizing direction occurs near normal in vivo resting potentials. Consequently, whereas mechanical responses as large as 30nm/mV have been observed (Santos-Sacchi and Dilger, 1988), responses occurring at physiological potentials are much smaller (Santos-Sacchi, 1989a). Essentially, the mechanical gain of the cell is variable, and depends on the potential"seen" by the voltagesensing element. The significance of this asymmetry in the v- 5L function is similar to that of the hair cell stereociliar transducer asymmetry -- sinusoidal voltage stimulation at the normal in vivo resting potential(70 mv; Dallos, Santos-Sacchi, and Flock, 1982) produces AC and DC response components. The DC mechanical componenet is in the contraction-depolarizing direction. Unlike the DC component of the receptor potential which is unaffected by the RC time constant of the basolateral membrane of the cell, the mechanical DC component is immensely, though indirectly, vulnerable to the effects of the cell's low pass characteristics (Santos-Sacchi, 1992). The physiological consequence
3 The magnificent outer hair cell of Corti's organ of the voltage dependent nature of OHC motility is substantial. Since the in vivo driving force for the mechanical response is ultimately the receptor potential of the OHC, the magnitude and phase of the mechanical response must be governed by the nonlinear RC characteristic of the cell membrane. Under whole cell voltage clamp the mechanical activity of the OHC is low pass (Ashmore 1987). However, the frequency response obtained under whole cell voltage clamp is simply a reflection of the instrumentation's ability to generate voltages across the cell's membrane (Santos-Sacchi, 1990). By optimizing the patch clamp amplifier's performance (reducing the clamp's time constant by using low resistance electrodes and compensation circuitry), a mechanical response cutoff frequency approaching 1 khz was possible (Santos-Sacchi, 1991). Thus, the mechanical cutoff frequency was shown to be instrumentation limited, indicating that the OHC mechanical response can follow rapid changes in transmembrane voltage and that the cell may be capable of mechanical responses at much higher frequencies. Those data also confirmed the voltage dependence hypothesis of OHC motility since the phase of the mechanical response corresponded to the phase of transmembrane voltage not current. Recently, Dallos and Evans (1995) were able to increase the bandwidth of voltage delivery to the OHC with the microchamber method, and showed mechanical responses flat out to about 20kHz. Similarly, Gale and Ashmore, (1997) used patches of OHC lateral membrane to rapidly apply voltages to the motor and measure motility-related gating currents which evidenced time constants indicating mechanical limits out to about 25kHz. Latest indications are that the mechanical response can be driven above 70kHz, and force generation is equally wideband (Frank et al., 1998). Nevertheless, while the ability of the cell to follow fast experimentally induced voltage changes is quite robust, it is the receptor potential frequency response which ultimately will determine the effectiveness of the OHC in influencing basilar membrane micromechanics. For this reason, the effectiveness of OHC motility in influencing basilar membrane micromechanics at high frequencies, near threshold has been questioned (Santos-Sacchi, 1989a; 1992). Estimates of OHC motility derived from measures of OHC receptor potentials in the high frequency region of the guinea pig cochlea (Russell et al., 1986) indicate that the AC component would be about 20dB smaller than basilar membrane motion (Santos-Sacchi, 1989a). Because of the inherent linearization of the Boltzmann V- b function at small signal levels, the corresponding DC mechanical component would be about 80dB smaller than basilar membrane motion (Santos-Sacchi, 1992). Clearly, it is difficult to reconcile these observations with current concepts of OHC function. In this regard, it has recently been found that the specific voltage-dependent capacitance, which corresponds to the charge movement associated with the OHC mechanical response, increases as cell length decreases, that is, as the cell's characteristic frequency increases (Santos-Sacchi et al. 1998). These data indicate that, whereas the voltage driving OHC motility, i.e., the receptor potential, may decrease with frequency due to the OHC's low-pass membrane filter, the electrical energy (QV) supplied to the lateral membrane will tend to remain stable. Perhaps, this energy conservation is crucial for the function of the cochlear amplifier in the mammal's high frequency region. Additionally, it is important to realize that the voltage dependent mechanical response may be dynamically modulated by a variety of physiologically important factors. For example, a shift of the V- 61, function along the voltage axis may modify the mechanical gain of the cell (Fig. 2). Many manipulations are known to shift the voltage-dependent capacitance function along the voltage axis, including phosphorylation, turgor pressure [membrane tension], lanthanides, salicylate and temperature (Huang and Santos-Sacchi, 1991; 1993a; Iwasa, 1993; Gale and Ashmore, 1994; Kakehata and Santos-Sacchi, 1995; 1996; Santos-Sacchi and Huang, 1997). Shifts in the OHC Voltage-dependent capacitance function are mirrored by correspon-
4 be assured that ultimately, through continued experimental effort, the secrets of this most magnificent cell will be uncovered. References Ashmore, J. F. and R. W. Meech. Ionic basis of the resting potential in outer hair cells isolated from the guinea pig cochlea. Nature 322, , Ashmore JF A fast motile response in guinea-pig outer hair cells: the cellular basis of the cochlear amplifier. J Physiol (Lond) 388: , Ashmore JF Transducer motor coupling in cochlear outer hair cells. In: Mechanics of Hearing (Kemp D and Wilson JP eds) Plenum Press, New York, pp 107 Fig. 2 The mechanical response (closed circles) of the OHC can be fit by a two state Boltzmann function. The first derivative defines the mechanical gain of the cell at a particular resting potential. Changes in either the resting potential or the voltage dependence of motility can change the gain. From Santos-Sacchi and Dilger, ding shifts in the V- ĉl function (Santos-Sacchi, 1991a; Kakehata and Santos-Sacchi, 1995). Factors that directly affect the OHC membrane potential will have similar effects. For example, ligand gated ionic channels may shift the operating point (resting potential) on the V- 61. function (Housley and Ashmore, 1991; Nakagawa et al., 1990; Ashmore and Ohmori, 1990). Interestingly, it has been recently found that initial voltage conditions affect the voltage dependence of motility-related charge movement, indicating that the two parameters controlling the gain of the cochlea amplifier, viz., resting membrane potential and the intrinsic voltage dependence of motility, are not independent, as previously thought (Santos-Sacchi et al., 1998a). While a tremendous amount of information has been garnered during the past decade concerning OHC structure and function, we are far from understanding the basic mechanisms underlying OHC motility, not to mention the contribution of this phenomenon to the so called "cochlear amplifier". Nevertheless, we can Ashmore, JF Neuroscience Res Suppl 12, S39 S50, Ashmore JF and Ohmori H, Control of intracellular calcium by ATP in isolated OHCs of the guinea pig cochlea. J. Physiol. 428, , Gale, J. E. & Ashmore, J. F. Charge displacement induced by rapid stretch in the basolateral membrane of the guinea pig OHC. Proceedings of Royal Society of London- Series B: Biological Sciences 255, , Gale, J. E. and Ashmore, J. F. An intrinsic frequency limit to the cochlear amplifier. Nature. 389, 63-6, Brownell WE, Bader CR, Bertrand D, and de Ribaupierre Y Evoked mechanical responses of isolated cochlear outer hair cells. Science 227: , Brownell, W. E., W. Shehata and J. B. Imredy Slow electrically and chemically evoked volume changes in guinea pig outer hair cells. In: Biomechanics of Active Movement and Deformation of Cells, N. Akas, ed., Springer-Verlag, New York, pp , Dallos, P, Santos-Sacchi J and Flock Intracellular recordings from outer hair cells. Science 218: , Dallos P, Evans BN, and Hallworth R On the nature of the motor element in cochlear outer hair cells. Nature 350: , Dallos P, Evans BN High-frequency motility of outer hair cells and the cochlear amplifier. Science 267 : 2006, Evans BN, Dallos P and Hallworth R Asymmetries in
5 The magnificent outer hair cell of Corti's organ motile responses of outer hair cells in simulated in vivo conditions In: Mechanics of Hearing (Eds: Kemp, D and Wilson, JP), pp Plenum Press, New York, Forge, A. Structural features of the lateral walls in mammalian cochlear outer hair cells. Cell Tiss. Res 265: , Frank, G., W. Hemmert, M. Wirth, A. W. Gummer High frequency limit of electrically induced length changes of mammalian outer hair cells. Midwinter Meeting, Assoc. for Res. in Otolaryngol., St. Petersburg, FL, February, Gale, JE and Ashmore, JF Charge displacement induced by rapid stretch in the basolateral membrane of the guinea pig OHC. Proc. Roy. Soc. Lond. B 255: 243 Gale, J. E. and Ashmore, J. F. An intrinsic frequency limit to the cochlear amplifier. Nature. 389, 63-6, Gulley, R. L. and T. S. Reese. Regional specialization the hair cell plasmalemma Rec. 189: , in the organ of Corti. Anat. Holley, M. C. and J. F. Ashmore On the mechanism of a high frequency force generator in outer hair cells isolated from the guinea pig cochlea. Proc. R. Soc. Lond. B 232, , 1988a. Housley GD and Ashmore, JF Direct measurement the action of ACh on isolated OHCs of the guinea pig cochlea. Proc. Royal Soc. Lon. 244, , Huang G-J, and Santos-Sacchi, OHC function : Phosphorylation agents shift the voltage dependence of of J. Metabolic control of and dephosphorylation of motility related capacitance. Midwinter Meeting, Assoc. for Res. in Otolaryngol., St. Petersburg, Fl, February, 1993a. Huang, G.-J. and Santos-Sacchi, J. Mapping the distribution of the outer hair cell motility voltage sensor by electrical amputation. Biophysical J. 65, 2228 Huang, G. -J. and Santos-Sacchi, J. Motility voltage sensor of the outer hair cell resides within the lateral plasma membrane. PNAS, 91, , Iwasa, KH Effect of stress on the membrane capacitance of the auditory outer hair cell. Biophysical J. 65, , 1993, Kachar, B., W. E. Brownell, R.Altschuler and J. Fex Electrokinetic shape changes of cochlear outer hair cells. Nature 322: , Kalenic, F., M. C. Holley, K.H. Iwasa, D. J. Lim, and B. Kachar. A membrane-based force generation mechanism in auditory sensory cells. Proc. Natl. Acad. Sci. 89: , Nakagawa, T, et al. ATP-induced current in isolated OHCs of the guinea pig cochlea. J. Neurophysiol. 63, , Ruggero, M. A. and Santos-Sacchi, J. Cochlear mechanics and biophysics., In: Handbook of Acoustics, (Ed. M. J. Croker), John Wiley & Sons., Santos-Sacchi J and Dilger JP Whole cell currents and mechanical responses of isolated outer hair cells. Hearing Res 35: , Santos-Sacchi J Asymmetry in voltage dependent movements of isolated outer hair cells from the organ of Corti. J Neurosci 9: , Santos-Sacchi J Fast outer hair cell motility: how fast is fast? In: The Mechanics and Biophysics of Hearing (Dallos, P, Geisler, CD, Matthews JW, Ruggero MA, Steele CR eds), pp69-5. Springer-Verlag, Berlin, Santos-Sacchi, J. Reversible inhibition of voltage dependent outer hair cell motility and capacitance. J. Neuroscience 11, , Santos-Sacchi, J. On the frequency limit and phase of outer hair cell motility: effects of the membrane filter. J. Neuroscience 12, , Santos-Sacchi, J, Huang G-J, and Wu, M. Mapping the distribution of outer hair cell voltage-dependent conductances by electrical amputation. Biophysical J. 73: , Santos-Sacchi, J., Kakehata, S. and Takahashi, S. The outer hair cell membrane potential directly affects the voltage dependence of motility-related gating chage. J. Physiology (London) 510: , 1998a. Santos-Sacchi, J., Kakehata, S., Kikuchi, T., Katori, Y. and Takasaka, T. Density of motility-related charge in the outer hair cell of the guinea pig is inversely related to best frequency. Neuroscience Letters 256: , 1998b.
Functional motor microdomains of the outer hair cell lateral membrane
Pflugers Arch - Eur J Physiol (2002) 445:331 336 DOI 10.1007/s00424-002-0928-4 CELL AND MOLECULAR PHYSIOLOGY Joseph Santos-Sacchi Functional motor microdomains of the outer hair cell lateral membrane Received:
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