From zebrafish to mammal

Functional evolution of prestin, the motor protein of cochlear outer hair cells

Xiaodong Tan, Jason L. Pecka, Jie Tang, Oseremen E. Okoruwa, Qian Zhang, Kirk Beisel, David Z. He

Research output: Contribution to journalArticle

30 Citations (Scopus)

Abstract

Prestin is the motor protein of cochlear outer hair cells. It belongs to a distinct anion transporter family called solute carrier protein 26A, or SLC26A. Members of this family serve two fundamentally distinct functions. Although most members transport different anion substrates across a variety of epithelia, prestin (SLC26A5) is unique, functioning as a voltage-dependent motor protein. Recent evidence suggests that prestin orthologs from zebrafish and chicken are electrogenic divalent/chloride anion exchangers/transporters with no motor function. These studies appear to suggest that prestin was evolved from an anion transporter. We examined the motor and transport functions of prestin and its orthologs from four different species in the vertebrate lineage, to gain insights of how these two physiological functions became distinct. Somatic motility, voltage-dependent nonlinear capacitance (NLC), and transporter function were measured in transfected human embryonic kidney (HEK) cells using voltage-clamp and anion uptake techniques. Zebrafish and chicken prestins both exhibited weak NLC, with peaks significantly shifted in the depolarization (right) direction. This was contrasted by robust NLC with peaks left shifted in the platypus and gerbil. The platypus and gerbil prestins retained little transporter function compared with robust anion transport capacities in the zebrafish and chicken orthologs. Somatic motility was detected only in the platypus and gerbil prestins. There appears to be an inverse relationship between NLC and anion transport functions, whereas motor function appears to have emerged only in mammalian prestin. Our results suggest that motor function is an innovation of therian prestin and is concurrent with diminished transporter capabilities.

Original languageEnglish
Pages (from-to)36-44
Number of pages9
JournalJournal of Neurophysiology
Volume105
Issue number1
DOIs
StatePublished - Jan 1 2011

Fingerprint

Outer Auditory Hair Cells
Zebrafish
Anions
Mammals
Platypus
Gerbillinae
Proteins
Chickens
Vertebrates
Chlorides
Epithelium

All Science Journal Classification (ASJC) codes

  • Physiology
  • Neuroscience(all)

Cite this

From zebrafish to mammal : Functional evolution of prestin, the motor protein of cochlear outer hair cells. / Tan, Xiaodong; Pecka, Jason L.; Tang, Jie; Okoruwa, Oseremen E.; Zhang, Qian; Beisel, Kirk; He, David Z.

In: Journal of Neurophysiology, Vol. 105, No. 1, 01.01.2011, p. 36-44.

Research output: Contribution to journalArticle

Tan, Xiaodong ; Pecka, Jason L. ; Tang, Jie ; Okoruwa, Oseremen E. ; Zhang, Qian ; Beisel, Kirk ; He, David Z. / From zebrafish to mammal : Functional evolution of prestin, the motor protein of cochlear outer hair cells. In: Journal of Neurophysiology. 2011 ; Vol. 105, No. 1. pp. 36-44.
@article{5e610d6ba1be4bb0968cc0179da790a9,
title = "From zebrafish to mammal: Functional evolution of prestin, the motor protein of cochlear outer hair cells",
abstract = "Prestin is the motor protein of cochlear outer hair cells. It belongs to a distinct anion transporter family called solute carrier protein 26A, or SLC26A. Members of this family serve two fundamentally distinct functions. Although most members transport different anion substrates across a variety of epithelia, prestin (SLC26A5) is unique, functioning as a voltage-dependent motor protein. Recent evidence suggests that prestin orthologs from zebrafish and chicken are electrogenic divalent/chloride anion exchangers/transporters with no motor function. These studies appear to suggest that prestin was evolved from an anion transporter. We examined the motor and transport functions of prestin and its orthologs from four different species in the vertebrate lineage, to gain insights of how these two physiological functions became distinct. Somatic motility, voltage-dependent nonlinear capacitance (NLC), and transporter function were measured in transfected human embryonic kidney (HEK) cells using voltage-clamp and anion uptake techniques. Zebrafish and chicken prestins both exhibited weak NLC, with peaks significantly shifted in the depolarization (right) direction. This was contrasted by robust NLC with peaks left shifted in the platypus and gerbil. The platypus and gerbil prestins retained little transporter function compared with robust anion transport capacities in the zebrafish and chicken orthologs. Somatic motility was detected only in the platypus and gerbil prestins. There appears to be an inverse relationship between NLC and anion transport functions, whereas motor function appears to have emerged only in mammalian prestin. Our results suggest that motor function is an innovation of therian prestin and is concurrent with diminished transporter capabilities.",
author = "Xiaodong Tan and Pecka, {Jason L.} and Jie Tang and Okoruwa, {Oseremen E.} and Qian Zhang and Kirk Beisel and He, {David Z.}",
year = "2011",
month = "1",
day = "1",
doi = "10.1152/jn.00234.2010",
language = "English",
volume = "105",
pages = "36--44",
journal = "Journal of Neurophysiology",
issn = "0022-3077",
publisher = "American Physiological Society",
number = "1",

}

TY - JOUR

T1 - From zebrafish to mammal

T2 - Functional evolution of prestin, the motor protein of cochlear outer hair cells

AU - Tan, Xiaodong

AU - Pecka, Jason L.

AU - Tang, Jie

AU - Okoruwa, Oseremen E.

AU - Zhang, Qian

AU - Beisel, Kirk

AU - He, David Z.

PY - 2011/1/1

Y1 - 2011/1/1

N2 - Prestin is the motor protein of cochlear outer hair cells. It belongs to a distinct anion transporter family called solute carrier protein 26A, or SLC26A. Members of this family serve two fundamentally distinct functions. Although most members transport different anion substrates across a variety of epithelia, prestin (SLC26A5) is unique, functioning as a voltage-dependent motor protein. Recent evidence suggests that prestin orthologs from zebrafish and chicken are electrogenic divalent/chloride anion exchangers/transporters with no motor function. These studies appear to suggest that prestin was evolved from an anion transporter. We examined the motor and transport functions of prestin and its orthologs from four different species in the vertebrate lineage, to gain insights of how these two physiological functions became distinct. Somatic motility, voltage-dependent nonlinear capacitance (NLC), and transporter function were measured in transfected human embryonic kidney (HEK) cells using voltage-clamp and anion uptake techniques. Zebrafish and chicken prestins both exhibited weak NLC, with peaks significantly shifted in the depolarization (right) direction. This was contrasted by robust NLC with peaks left shifted in the platypus and gerbil. The platypus and gerbil prestins retained little transporter function compared with robust anion transport capacities in the zebrafish and chicken orthologs. Somatic motility was detected only in the platypus and gerbil prestins. There appears to be an inverse relationship between NLC and anion transport functions, whereas motor function appears to have emerged only in mammalian prestin. Our results suggest that motor function is an innovation of therian prestin and is concurrent with diminished transporter capabilities.

AB - Prestin is the motor protein of cochlear outer hair cells. It belongs to a distinct anion transporter family called solute carrier protein 26A, or SLC26A. Members of this family serve two fundamentally distinct functions. Although most members transport different anion substrates across a variety of epithelia, prestin (SLC26A5) is unique, functioning as a voltage-dependent motor protein. Recent evidence suggests that prestin orthologs from zebrafish and chicken are electrogenic divalent/chloride anion exchangers/transporters with no motor function. These studies appear to suggest that prestin was evolved from an anion transporter. We examined the motor and transport functions of prestin and its orthologs from four different species in the vertebrate lineage, to gain insights of how these two physiological functions became distinct. Somatic motility, voltage-dependent nonlinear capacitance (NLC), and transporter function were measured in transfected human embryonic kidney (HEK) cells using voltage-clamp and anion uptake techniques. Zebrafish and chicken prestins both exhibited weak NLC, with peaks significantly shifted in the depolarization (right) direction. This was contrasted by robust NLC with peaks left shifted in the platypus and gerbil. The platypus and gerbil prestins retained little transporter function compared with robust anion transport capacities in the zebrafish and chicken orthologs. Somatic motility was detected only in the platypus and gerbil prestins. There appears to be an inverse relationship between NLC and anion transport functions, whereas motor function appears to have emerged only in mammalian prestin. Our results suggest that motor function is an innovation of therian prestin and is concurrent with diminished transporter capabilities.

UR - http://www.scopus.com/inward/record.url?scp=78651460278&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=78651460278&partnerID=8YFLogxK

U2 - 10.1152/jn.00234.2010

DO - 10.1152/jn.00234.2010

M3 - Article

VL - 105

SP - 36

EP - 44

JO - Journal of Neurophysiology

JF - Journal of Neurophysiology

SN - 0022-3077

IS - 1

ER -