Abstract
Among the vertebrate lineages with different hearing frequency ranges, humans lie between the low-frequency hearing (1 kHz) of fish and amphibians and the high-frequency hearing (100 kHz) of bats and dolphins. Little is known about the mechanism underlying such a striking difference in the limits of hearing frequency. Prestin, responsible for cochlear amplification and frequency selectivity in mammals, seems to be the only candidate to date. Mammalian prestin is densely expressed in the lateral plasma membrane of the outer hair cells (OHCs) and functions as a voltage-dependent motor protein. To explore the molecular basis for the contribution of prestin in hearing frequency detection, we collected audiogram data from humans, dogs, gerbils, bats, and dolphins because their average hearing frequency rises in steps. We generated stable cell lines transfected with human, dog, gerbil, bat, and dolphin prestins (hPres, dPres, gPres, bPres, and nPres, respectively). The non-linear capacitance (NLC) of different prestins was measured using a whole-cell patch clamp. We found that the Qmax/Clin of bPres and nPres was significantly higher than that of humans. The V1/2 of hPres was more hyperpolarized than that of nPres. The z values of hPres and bPres were higher than that of nPres. We further analyzed the relationship between the high-frequency hearing limit (Fmax) and the functional parameters (V1/2, z, and Qmax/Clin) of NLC among five prestins. Interestingly, no significant correlation was found between the functional parameters and Fmax. Additionally, a comparative study showed that the amino acid sequences and tertiary structures of five prestins were quite similar. There might be a common fundamental mechanism driving the function of prestins. These findings call for a reconsideration of the leading role of prestin in hearing frequency perception. Other intriguing kinetics underlying the hearing frequency response of auditory organs might exist.
Highlights
Hearing frequency resolution is a result of selective pressure for accurate and instantaneous localization of the source of brief sounds
Amino Acid Sequence Comparing Among human prestin (hPres), dog prestin (dPres), gerbil prestin (gPres), bat prestin (bPres), and nPres
Our alignment results were consistent with previous comparative peptide sequence analyses that stated that amino acid sequences of mammalian prestin are highly conserved
Summary
Hearing frequency resolution is a result of selective pressure for accurate and instantaneous localization of the source of brief sounds. Most fishes can only detect sounds below 0.74 kHz (Popper and Fay, 1997). In some species of frogs, Fmax values are nearly five times higher than that of fish (Ji et al, 2018). Fmax tends to increase phylogenetically from fish to amphibians and mammals. Humans have an Fmax value of approximately 20 kHz, while bats and dolphins can hear sounds with frequencies near 150 kHz (Heffner et al, 2013; Nachtigall et al, 2016; Simmons et al, 2017). The hearing frequency of humans is lower than that of other mammals, like dogs and gerbils, whose Fmax is 45 and 60 kHz, respectively (Heffner et al, 1994; Ogawa et al, 2018). Little is known about the mechanism underlying such a large hearing frequency difference among them
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