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Membrane Thickness Sensitivity of Prestin Orthologs: the Evolution of a Piezoelectric Protein

Overview
Journal Biophys J
Publisher Cell Press
Specialty Biophysics
Date 2011 Jun 7
PMID 21641306
Citations 8
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Abstract

How proteins evolve new functionality is an important question in biology; prestin (SLC26A5) is a case in point. Prestin drives outer hair cell somatic motility and amplifies mechanical vibrations in the mammalian cochlea. The motility of mammalian prestin is analogous to piezoelectricity, in which charge transfer is coupled to changes in membrane area occupied by the protein. Intriguingly, nonmammalian prestin orthologs function as anion exchangers but are apparently nonmotile. We previously found that mammalian prestin is sensitive to membrane thickness, suggesting that prestin's extended conformation has a thinner hydrophobic height in the lipid bilayer. Because prestin-based motility is a mammalian specialization, we initially hypothesized that nonmotile prestin orthologs, while functioning as anion transporters, should be much less sensitive to membrane thickness. We found the exact opposite to be true. Chicken prestin was the most sensitive to thickness changes, displaying the largest shift in voltage dependence. Platypus prestin displayed an intermediate response to membrane thickness and gerbil prestin was the least sensitive. To explain these observations, we present a theory where force production, rather than displacement, was selected for the evolution of prestin as a piezoelectric membrane motor.

Citing Articles

Cryo-EM structures of thermostabilized prestin provide mechanistic insights underlying outer hair cell electromotility.

Futamata H, Fukuda M, Umeda R, Yamashita K, Tomita A, Takahashi S Nat Commun. 2022; 13(1):6208.

PMID: 36266333 PMC: 9584906. DOI: 10.1038/s41467-022-34017-x.


The conformational cycle of prestin underlies outer-hair cell electromotility.

Bavi N, Clark M, Contreras G, Shen R, Reddy B, Milewski W Nature. 2021; 600(7889):553-558.

PMID: 34695838 DOI: 10.1038/s41586-021-04152-4.


Outer hair cell electromotility is low-pass filtered relative to the molecular conformational changes that produce nonlinear capacitance.

Santos-Sacchi J, Iwasa K, Tan W J Gen Physiol. 2019; 151(12):1369-1385.

PMID: 31676485 PMC: 6888751. DOI: 10.1085/jgp.201812280.


The speed limit of outer hair cell electromechanical activity.

Santos-Sacchi J HNO. 2019; 67(3):159-164.

PMID: 30747242 DOI: 10.1007/s00106-019-0615-9.


Mechanical transduction by ion channels: A cautionary tale.

Sachs F World J Neurol. 2017; 5(3):74-87.

PMID: 28078202 PMC: 5221657. DOI: 10.5316/wjn.v5.i3.74.


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