Xenopus TRPN1 (NOMPC) localizes to microtubule-based cilia in epithelial cells, including inner-ear hair cells

Jung Bum Shin, Dany Adams, Martin Paukert, Maria Siba, Samuel Sidi, Michael Levin, Peter Barr-Gillespie, Stefan Gründer

Research output: Contribution to journalArticle

66 Citations (Scopus)

Abstract

In vertebrates, the senses of hearing and balance depend on hair cells, which transduce sounds with their hair bundles, containing actin-based stereocilia and microtubule-based kinocilia. A long-standing question in auditory science is the identity of the mechanically sensitive transduction channel of hair cells, thought to be localized at the tips of their stereocilia. Experiments in zebrafish implicated the transient receptor potential (TRP) channel NOMPC (drTRPN1) in this role; TRPN1 is absent from the genomes of higher vertebrates, however, and has not been localized in hair cells. Another candidate for the transduction channel, TRPA1, apparently is required for transduction in mammalian and nonmammalian vertebrates. This discrepancy raises the question of the relative contribution of TRPN1 and TRPA1 to transduction in nonmammalian vertebrates. To address this question, we cloned the TRPN1 ortholog from the amphibian Xenopus laevis, generated an antibody against the protein, and determined the protein's cellular and subcellular localization. We found that TRPN1 is prominently located in lateral-line hair cells, auditory hair cells, and ciliated epidermal cells of developing Xenopus embryos. In ciliated epidermal cells TRPN1 staining was enriched at the tips and bases of the cilia. In saccular hair cells, TRPN1 was located prominently in the kinocilial bulb, a component of the mechanosensory hair bundles. Moreover, we observed redistribution of TRPN1 upon treatment of hair cells with calcium chelators, which disrupts the transduction apparatus. This result suggests that although TRPN1 is unlikely to be the transduction channel of stereocilia, it plays an essential role, functionally related to transduction, in the kinocilium.

Original languageEnglish (US)
Pages (from-to)12572-12577
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume102
Issue number35
DOIs
StatePublished - Aug 30 2005

Fingerprint

Inner Auditory Hair Cells
Cilia
Inner Ear
Xenopus
Microtubules
Epithelial Cells
Stereocilia
Vertebrates
Auditory Hair Cells
Transient Receptor Potential Channels
Xenopus laevis
Amphibians
Zebrafish
Hearing
Actins
Proteins
Embryonic Structures
Genome
Staining and Labeling

Keywords

  • Ciliary
  • Mechanosensory
  • Transduction
  • Transient receptor potential channel

ASJC Scopus subject areas

  • Genetics
  • General

Cite this

Xenopus TRPN1 (NOMPC) localizes to microtubule-based cilia in epithelial cells, including inner-ear hair cells. / Shin, Jung Bum; Adams, Dany; Paukert, Martin; Siba, Maria; Sidi, Samuel; Levin, Michael; Barr-Gillespie, Peter; Gründer, Stefan.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 102, No. 35, 30.08.2005, p. 12572-12577.

Research output: Contribution to journalArticle

Shin, Jung Bum ; Adams, Dany ; Paukert, Martin ; Siba, Maria ; Sidi, Samuel ; Levin, Michael ; Barr-Gillespie, Peter ; Gründer, Stefan. / Xenopus TRPN1 (NOMPC) localizes to microtubule-based cilia in epithelial cells, including inner-ear hair cells. In: Proceedings of the National Academy of Sciences of the United States of America. 2005 ; Vol. 102, No. 35. pp. 12572-12577.
@article{8c938b3315fd4d5a8b77af869363ba42,
title = "Xenopus TRPN1 (NOMPC) localizes to microtubule-based cilia in epithelial cells, including inner-ear hair cells",
abstract = "In vertebrates, the senses of hearing and balance depend on hair cells, which transduce sounds with their hair bundles, containing actin-based stereocilia and microtubule-based kinocilia. A long-standing question in auditory science is the identity of the mechanically sensitive transduction channel of hair cells, thought to be localized at the tips of their stereocilia. Experiments in zebrafish implicated the transient receptor potential (TRP) channel NOMPC (drTRPN1) in this role; TRPN1 is absent from the genomes of higher vertebrates, however, and has not been localized in hair cells. Another candidate for the transduction channel, TRPA1, apparently is required for transduction in mammalian and nonmammalian vertebrates. This discrepancy raises the question of the relative contribution of TRPN1 and TRPA1 to transduction in nonmammalian vertebrates. To address this question, we cloned the TRPN1 ortholog from the amphibian Xenopus laevis, generated an antibody against the protein, and determined the protein's cellular and subcellular localization. We found that TRPN1 is prominently located in lateral-line hair cells, auditory hair cells, and ciliated epidermal cells of developing Xenopus embryos. In ciliated epidermal cells TRPN1 staining was enriched at the tips and bases of the cilia. In saccular hair cells, TRPN1 was located prominently in the kinocilial bulb, a component of the mechanosensory hair bundles. Moreover, we observed redistribution of TRPN1 upon treatment of hair cells with calcium chelators, which disrupts the transduction apparatus. This result suggests that although TRPN1 is unlikely to be the transduction channel of stereocilia, it plays an essential role, functionally related to transduction, in the kinocilium.",
keywords = "Ciliary, Mechanosensory, Transduction, Transient receptor potential channel",
author = "Shin, {Jung Bum} and Dany Adams and Martin Paukert and Maria Siba and Samuel Sidi and Michael Levin and Peter Barr-Gillespie and Stefan Gr{\"u}nder",
year = "2005",
month = "8",
day = "30",
doi = "10.1073/pnas.0502403102",
language = "English (US)",
volume = "102",
pages = "12572--12577",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "35",

}

TY - JOUR

T1 - Xenopus TRPN1 (NOMPC) localizes to microtubule-based cilia in epithelial cells, including inner-ear hair cells

AU - Shin, Jung Bum

AU - Adams, Dany

AU - Paukert, Martin

AU - Siba, Maria

AU - Sidi, Samuel

AU - Levin, Michael

AU - Barr-Gillespie, Peter

AU - Gründer, Stefan

PY - 2005/8/30

Y1 - 2005/8/30

N2 - In vertebrates, the senses of hearing and balance depend on hair cells, which transduce sounds with their hair bundles, containing actin-based stereocilia and microtubule-based kinocilia. A long-standing question in auditory science is the identity of the mechanically sensitive transduction channel of hair cells, thought to be localized at the tips of their stereocilia. Experiments in zebrafish implicated the transient receptor potential (TRP) channel NOMPC (drTRPN1) in this role; TRPN1 is absent from the genomes of higher vertebrates, however, and has not been localized in hair cells. Another candidate for the transduction channel, TRPA1, apparently is required for transduction in mammalian and nonmammalian vertebrates. This discrepancy raises the question of the relative contribution of TRPN1 and TRPA1 to transduction in nonmammalian vertebrates. To address this question, we cloned the TRPN1 ortholog from the amphibian Xenopus laevis, generated an antibody against the protein, and determined the protein's cellular and subcellular localization. We found that TRPN1 is prominently located in lateral-line hair cells, auditory hair cells, and ciliated epidermal cells of developing Xenopus embryos. In ciliated epidermal cells TRPN1 staining was enriched at the tips and bases of the cilia. In saccular hair cells, TRPN1 was located prominently in the kinocilial bulb, a component of the mechanosensory hair bundles. Moreover, we observed redistribution of TRPN1 upon treatment of hair cells with calcium chelators, which disrupts the transduction apparatus. This result suggests that although TRPN1 is unlikely to be the transduction channel of stereocilia, it plays an essential role, functionally related to transduction, in the kinocilium.

AB - In vertebrates, the senses of hearing and balance depend on hair cells, which transduce sounds with their hair bundles, containing actin-based stereocilia and microtubule-based kinocilia. A long-standing question in auditory science is the identity of the mechanically sensitive transduction channel of hair cells, thought to be localized at the tips of their stereocilia. Experiments in zebrafish implicated the transient receptor potential (TRP) channel NOMPC (drTRPN1) in this role; TRPN1 is absent from the genomes of higher vertebrates, however, and has not been localized in hair cells. Another candidate for the transduction channel, TRPA1, apparently is required for transduction in mammalian and nonmammalian vertebrates. This discrepancy raises the question of the relative contribution of TRPN1 and TRPA1 to transduction in nonmammalian vertebrates. To address this question, we cloned the TRPN1 ortholog from the amphibian Xenopus laevis, generated an antibody against the protein, and determined the protein's cellular and subcellular localization. We found that TRPN1 is prominently located in lateral-line hair cells, auditory hair cells, and ciliated epidermal cells of developing Xenopus embryos. In ciliated epidermal cells TRPN1 staining was enriched at the tips and bases of the cilia. In saccular hair cells, TRPN1 was located prominently in the kinocilial bulb, a component of the mechanosensory hair bundles. Moreover, we observed redistribution of TRPN1 upon treatment of hair cells with calcium chelators, which disrupts the transduction apparatus. This result suggests that although TRPN1 is unlikely to be the transduction channel of stereocilia, it plays an essential role, functionally related to transduction, in the kinocilium.

KW - Ciliary

KW - Mechanosensory

KW - Transduction

KW - Transient receptor potential channel

UR - http://www.scopus.com/inward/record.url?scp=24644461068&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=24644461068&partnerID=8YFLogxK

U2 - 10.1073/pnas.0502403102

DO - 10.1073/pnas.0502403102

M3 - Article

C2 - 16116094

AN - SCOPUS:24644461068

VL - 102

SP - 12572

EP - 12577

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 35

ER -