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Release and elementary mechanisms of nitric oxide in hair cells

Release and elementary mechanisms of nitric oxide in hair cells
Release and elementary mechanisms of nitric oxide in hair cells
The enzyme nitric oxide (NO) synthase, that produces the signaling molecule NO, has been identified in several cell types in the inner ear. However, it is unclear whether a measurable quantity of NO is released in the inner ear to confer specific functions. Indeed, the functional significance of NO and the elementary cellular mechanism thereof are most uncertain. Here, we demonstrate that the sensory epithelia of the frog saccule release NO and explore its release mechanisms by using self-referencing NO-selective electrodes. Additionally, we investigated the functional effects of NO on electrical properties of hair cells and determined their underlying cellular mechanism. We show detectable amounts of NO are released by hair cells (>50 nM). Furthermore, a hair-cell efferent modulator acetylcholine produces at least a threefold increase in NO release. NO not only attenuated the baseline membrane oscillations but it also increased the magnitude of current required to generate the characteristic membrane potential oscillations. This resulted in a rightward shift in the frequency-current relationship and altered the excitability of hair cells. Our data suggest that these effects ensue because NO reduces whole cell Ca(2+) current and drastically decreases the open probability of single-channel events of the L-type and non L-type Ca(2+) channels in hair cells, an effect that is mediated through direct nitrosylation of the channel and activation of protein kinase G. Finally, NO increases the magnitude of Ca(2+)-activated K(+) currents via direct NO nitrosylation. We conclude that NO-mediated inhibition serves as a component of efferent nerve modulation of hair cells.
0022-3077
2494-505
Lv, Ping
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Rodriguez-Contreras, Adrian
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Kim, Hyo Jeong
c339d0ec-1580-4303-9830-6333cc3f2cbe
Zhu, Jun
e25fa87d-445b-4bb8-b15f-1e608b4d8b1c
Wei, Dongguang
b170083b-61a9-4923-a1d5-c656b9d7d86f
Choong-Ryoul, Sihn
e2e24126-481e-4ceb-be24-574766b90382
Eastwood, Emily
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Mu, Karen
22f9b174-1c16-4a2f-b0a2-8baef4573f90
Levic, Snezana
e62fb627-04e0-411e-8c79-8837516f0b08
Song, Haitao
95856702-2fbb-4d91-a3d0-8a514755e5e7
Yevgeniy, Petrov Y
953c9b6c-9d1c-42ec-baca-a00f65cfcd2a
Smith, Peter J S
003de469-9420-4f12-8f0e-8e8d76d28d6c
Yamoah, Ebenezer N
70c308a1-355e-4ce1-bf69-a3807dcb78ad
Lv, Ping
16fbbe92-846a-4526-b7d9-5a5ccf890331
Rodriguez-Contreras, Adrian
859e3398-9ed4-42f1-b603-6a00a9be11ed
Kim, Hyo Jeong
c339d0ec-1580-4303-9830-6333cc3f2cbe
Zhu, Jun
e25fa87d-445b-4bb8-b15f-1e608b4d8b1c
Wei, Dongguang
b170083b-61a9-4923-a1d5-c656b9d7d86f
Choong-Ryoul, Sihn
e2e24126-481e-4ceb-be24-574766b90382
Eastwood, Emily
5d5f5c05-c293-4ede-b084-e08147763b03
Mu, Karen
22f9b174-1c16-4a2f-b0a2-8baef4573f90
Levic, Snezana
e62fb627-04e0-411e-8c79-8837516f0b08
Song, Haitao
95856702-2fbb-4d91-a3d0-8a514755e5e7
Yevgeniy, Petrov Y
953c9b6c-9d1c-42ec-baca-a00f65cfcd2a
Smith, Peter J S
003de469-9420-4f12-8f0e-8e8d76d28d6c
Yamoah, Ebenezer N
70c308a1-355e-4ce1-bf69-a3807dcb78ad

Lv, Ping, Rodriguez-Contreras, Adrian, Kim, Hyo Jeong, Zhu, Jun, Wei, Dongguang, Choong-Ryoul, Sihn, Eastwood, Emily, Mu, Karen, Levic, Snezana, Song, Haitao, Yevgeniy, Petrov Y, Smith, Peter J S and Yamoah, Ebenezer N (2010) Release and elementary mechanisms of nitric oxide in hair cells. Journal of Neurophysiology, 103 (5), 2494-505. (doi:10.1152/jn.00017.2010). (PMID:20220083)

Record type: Article

Abstract

The enzyme nitric oxide (NO) synthase, that produces the signaling molecule NO, has been identified in several cell types in the inner ear. However, it is unclear whether a measurable quantity of NO is released in the inner ear to confer specific functions. Indeed, the functional significance of NO and the elementary cellular mechanism thereof are most uncertain. Here, we demonstrate that the sensory epithelia of the frog saccule release NO and explore its release mechanisms by using self-referencing NO-selective electrodes. Additionally, we investigated the functional effects of NO on electrical properties of hair cells and determined their underlying cellular mechanism. We show detectable amounts of NO are released by hair cells (>50 nM). Furthermore, a hair-cell efferent modulator acetylcholine produces at least a threefold increase in NO release. NO not only attenuated the baseline membrane oscillations but it also increased the magnitude of current required to generate the characteristic membrane potential oscillations. This resulted in a rightward shift in the frequency-current relationship and altered the excitability of hair cells. Our data suggest that these effects ensue because NO reduces whole cell Ca(2+) current and drastically decreases the open probability of single-channel events of the L-type and non L-type Ca(2+) channels in hair cells, an effect that is mediated through direct nitrosylation of the channel and activation of protein kinase G. Finally, NO increases the magnitude of Ca(2+)-activated K(+) currents via direct NO nitrosylation. We conclude that NO-mediated inhibition serves as a component of efferent nerve modulation of hair cells.

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Published date: May 2010
Organisations: Centre for Biological Sciences

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Local EPrints ID: 190271
URI: http://eprints.soton.ac.uk/id/eprint/190271
ISSN: 0022-3077
PURE UUID: 4ccbe684-bcd0-4943-85e1-71db5322c200
ORCID for Peter J S Smith: ORCID iD orcid.org/0000-0003-4400-6853

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Date deposited: 13 Jun 2011 07:57
Last modified: 15 Mar 2024 03:38

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Contributors

Author: Ping Lv
Author: Adrian Rodriguez-Contreras
Author: Hyo Jeong Kim
Author: Jun Zhu
Author: Dongguang Wei
Author: Sihn Choong-Ryoul
Author: Emily Eastwood
Author: Karen Mu
Author: Snezana Levic
Author: Haitao Song
Author: Petrov Y Yevgeniy
Author: Peter J S Smith ORCID iD
Author: Ebenezer N Yamoah

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