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A prestin motor in chicken auditory hair cells: active force generation in a nonmammalian species.

ABSTRACT: Active force generation by outer hair cells (OHCs) underlies amplification and frequency tuning in the mammalian cochlea but whether such a process exists in nonmammals is unclear. Here, we demonstrate that hair cells of the chicken auditory papilla possess an electromechanical force generator in addition to active hair bundle motion due to mechanotransducer channel gating. The properties of the force generator, its voltage dependence and susceptibility to salicylate, as well as an associated chloride-sensitive nonlinear capacitance, suggest involvement of the chicken homolog of prestin, the OHC motor protein. The presence of chicken prestin in the hair cell lateral membrane was confirmed by immunolabeling studies. The hair bundle and prestin motors together create sufficient force to produce fast lateral displacements of the tectorial membrane. Our results imply that the first use of prestin as a motor protein occurred early in amniote evolution and was not a mammalian invention as is usually supposed.

SUBMITTER: Beurg M

PROVIDER: S-EPMC3713163 | biostudies-literature | 2013 Jul

REPOSITORIES: biostudies-literature

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A prestin motor in chicken auditory hair cells: active force generation in a nonmammalian species.

Beurg Maryline M Tan Xiaodong X Fettiplace Robert R

Neuron 20130606 1

Active force generation by outer hair cells (OHCs) underlies amplification and frequency tuning in the mammalian cochlea but whether such a process exists in nonmammals is unclear. Here, we demonstrate that hair cells of the chicken auditory papilla possess an electromechanical force generator in addition to active hair bundle motion due to mechanotransducer channel gating. The properties of the force generator, its voltage dependence and susceptibility to salicylate, as well as an associated ch ...[more]

PMID: 23746629

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Project description:Prestin is a membrane protein in the outer hair cell (OHC) that has been shown to be essential for electromotility. OHCs from prestin-null mice do not express prestin, do not have a nonlinear capacitance (the electrical signature of electromotility), and are smaller in size than wild-type OHCs. We sought to determine whether prestin-null OHCs can be transduced to incorporate functional prestin protein in a normal fashion. A recombinant helper-dependent adenovirus expressing prestin and green fluorescent protein (HDAd-prestin-GFP) was created and tested in human embryonic kidney cells (HEK cells). Transduced HEK cells demonstrated membrane expression of prestin and nonlinear capacitance. HDAd-prestin-GFP was then applied to cochlear sensory epithelium explants harvested from wild-type and prestin-null mice at postnatal days 2-3, the age at which native prestin is just beginning to become functional in wild-type mice. At postnatal days 4-5, we investigated transduced OHCs for (1) their prestin expression pattern as revealed by immunofluorescence; (2) their cell surface area as measured by linear capacitance; and (3) their prestin function as indicated by nonlinear capacitance. HDAd-prestin-GFP efficiently transduced OHCs of both genotypes and prestin protein localized to the plasma membrane. Whole-cell voltage clamp studies revealed a nonlinear capacitance in transduced wild-type and prestin-null OHCs, but not in non-transduced cells of either genotype. Prestin transduction did not increase the linear capacitance (cell surface area) for either genotype. In peak nonlinear capacitance, voltage at peak nonlinear capacitance, charge density of the nonlinear capacitance, and shape of the voltage-capacitance curves, the transduced cells of the two genotypes resembled each other and previously reported data from adult wild-type mouse OHCs. Thus, prestin introduced into prestin-deficient OHCs segregates normally to the cell membrane and generates a normal nonlinear capacitance, indicative of normal prestin function.

Dataset Information

A prestin motor in chicken auditory hair cells: active force generation in a nonmammalian species.

Publications

A prestin motor in chicken auditory hair cells: active force generation in a nonmammalian species.

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