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Plasma membrane Ca2+-ATPase extrudes Ca2+ from hair cell stereocilia

Plasma membrane Ca2+-ATPase extrudes Ca2+ from hair cell stereocilia
Plasma membrane Ca2+-ATPase extrudes Ca2+ from hair cell stereocilia
Mechanically sensitive hair cells of the auditory and vestibular systems use Ca2+ to control adaptation of mechanical transduction, to effect frequency tuning, to trigger neurotransmitter release, and to mediate efferent synaptic signaling. To determine the role that pumps play in regulation of Ca2+ in the hair bundle, the organelle responsible for mechanoelectrical transduction, we localized and quantified the plasma membrane Ca2+-ATPase (PMCA) of the bundle. We found that each hair bundle contains approximately 10(6) PMCA molecules or approximately 2000 per square micrometer of bundle membrane and that PMCA is the principal calmodulin binding protein of the bundle. Consistent with biochemical estimates of PMCA density, we measured with extracellular Ca2+-selective electrodes a substantial Ca2+ efflux from bundles. The number of bundle Ca2+ pumps and magnitude of resting Ca2+ efflux suggested that PMCA should generate a substantial membrane current as bundles expel Ca2+. Measurement of whole-cell currents revealed a transduction-dependent outward current that was consistent with the activity of PMCA. Finally, dialysis of hair cells with PMCA inhibitors led to a large increase in the concentration of Ca2+ in bundles, which suggests that PMCA plays a major role in regulating bundle Ca2+ concentration. Our data further indicate that PMCA could elevate the extracellular Ca2+ concentration close to hair bundles above the low level found in bulk endolymph.
0270-6474
610-624
Yamoah, Ebenezer N.
78da5e87-c125-449f-b8c0-b15624dfc45d
Lumpkin, Ellen A.
e186ee7d-c087-4299-9bce-2d4f3357b38d
Dumont, Rachel A.
4984bae6-d082-472a-b3e4-172f70f50c28
Smith, Peter J.S.
003de469-9420-4f12-8f0e-8e8d76d28d6c
Hudspeth, A.J.
6f6cc8a6-0265-4594-824c-3f3a0dbb171a
Gillespie, Peter G.
38e0863b-e6cc-4758-ba1f-80ac60b2ceb0
Yamoah, Ebenezer N.
78da5e87-c125-449f-b8c0-b15624dfc45d
Lumpkin, Ellen A.
e186ee7d-c087-4299-9bce-2d4f3357b38d
Dumont, Rachel A.
4984bae6-d082-472a-b3e4-172f70f50c28
Smith, Peter J.S.
003de469-9420-4f12-8f0e-8e8d76d28d6c
Hudspeth, A.J.
6f6cc8a6-0265-4594-824c-3f3a0dbb171a
Gillespie, Peter G.
38e0863b-e6cc-4758-ba1f-80ac60b2ceb0

Yamoah, Ebenezer N., Lumpkin, Ellen A., Dumont, Rachel A., Smith, Peter J.S., Hudspeth, A.J. and Gillespie, Peter G. (1998) Plasma membrane Ca2+-ATPase extrudes Ca2+ from hair cell stereocilia. Journal of Neuroscience, 18 (2), 610-624. (PMID:9425003)

Record type: Article

Abstract

Mechanically sensitive hair cells of the auditory and vestibular systems use Ca2+ to control adaptation of mechanical transduction, to effect frequency tuning, to trigger neurotransmitter release, and to mediate efferent synaptic signaling. To determine the role that pumps play in regulation of Ca2+ in the hair bundle, the organelle responsible for mechanoelectrical transduction, we localized and quantified the plasma membrane Ca2+-ATPase (PMCA) of the bundle. We found that each hair bundle contains approximately 10(6) PMCA molecules or approximately 2000 per square micrometer of bundle membrane and that PMCA is the principal calmodulin binding protein of the bundle. Consistent with biochemical estimates of PMCA density, we measured with extracellular Ca2+-selective electrodes a substantial Ca2+ efflux from bundles. The number of bundle Ca2+ pumps and magnitude of resting Ca2+ efflux suggested that PMCA should generate a substantial membrane current as bundles expel Ca2+. Measurement of whole-cell currents revealed a transduction-dependent outward current that was consistent with the activity of PMCA. Finally, dialysis of hair cells with PMCA inhibitors led to a large increase in the concentration of Ca2+ in bundles, which suggests that PMCA plays a major role in regulating bundle Ca2+ concentration. Our data further indicate that PMCA could elevate the extracellular Ca2+ concentration close to hair bundles above the low level found in bulk endolymph.

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Published date: 15 January 1998

Identifiers

Local EPrints ID: 190287
URI: http://eprints.soton.ac.uk/id/eprint/190287
ISSN: 0270-6474
PURE UUID: 9d1c963e-de4b-4eeb-9705-14487a2e58f1
ORCID for Peter J.S. Smith: ORCID iD orcid.org/0000-0003-4400-6853

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Date deposited: 17 Jun 2011 14:17
Last modified: 21 Nov 2021 03:04

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Contributors

Author: Ebenezer N. Yamoah
Author: Ellen A. Lumpkin
Author: Rachel A. Dumont
Author: A.J. Hudspeth
Author: Peter G. Gillespie

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