Abstract
Auditory hair cells from nonmammalian vertebrates are electrically tuned to specific sound frequencies primarily by the interactions of voltage-gated calcium channels and calcium-activated potassium (BK) channels colocalized at synaptic active zones. Mammalian inner hair cells are not electrically tuned and, yet, BK channels are also thought to reside at active zones. Using patch-clamp recordings and immunofluorescence, we characterized BK channel expression in mouse inner hair cells. Unexpectedly, these channels have inactivating currents and are clustered near the apex of the cell away from synaptic sites near the base. These results indicate a novel function of BK channels in mammalian inner hair cells and provide a framework for future research.
MeSH Terms
Animals
Fluorescent Antibody Technique
Hair Cells, Auditory, Inner/chemistry,drug effects,physiology,ultrastructure
In Vitro Techniques
Large-Conductance Calcium-Activated Potassium Channels
Membrane Potentials/drug effects,physiology
Mice
Mice, Inbred C57BL
Organ of Corti/growth & development
Patch-Clamp Techniques
Peptides/pharmacology
Potassium Channels, Calcium-Activated/analysis,antagonists & inhibitors,physiology
Subcellular Fractions/chemistry
Chemicals
Large-Conductance Calcium-Activated Potassium Channels
Peptides
Potassium Channels, Calcium-Activated
iberiotoxin
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Pyott Sonja J
Department of Molecular and Cellular Physiology, Howard Hughes Medical Institute, Stanford University School of Medicine, Stanford, California 94305-5345, USA.
Glowatzki Elisabeth
Trimmer James S
Aldrich Richard W
References (22)
22 references, click to expand
-
Mechanisms of hair cell tuning.
Annu Rev Physiol. 1999;61:809-34
PMID: 10099711
-
ATP-Induced Ca(2+) release in cochlear outer hair cells: localization of an inositol triphosphate-gated Ca(2+) store to the base of the sensory hair bundle.
J Neurosci. 1999 Aug 15;19(16):6918-29
PMID: 10436049
-
Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse.
Proc Natl Acad Sci U S A. 2000 Jan 18;97(2):883-8
PMID: 10639174
-
Rapidly inactivating and non-inactivating calcium-activated potassium currents in frog saccular hair cells.
J Physiol. 2001 Oct 1;536(Pt 1):49-65
PMID: 11579156
-
Retardation of cochlear maturation and impaired hair cell function caused by deletion of all known thyroid hormone receptors.
J Neurosci. 2001 Dec 15;21(24):9792-800
PMID: 11739587
-
Expression of Ca2+-activated BK channel mRNA and its splice variants in the rat cochlea.
J Comp Neurol. 2003 Jan 6;455(2):198-209
PMID: 12454985
-
Contribution of BK Ca2+-activated K+ channels to auditory neurotransmission in the Guinea pig cochlea.
J Neurophysiol. 2003 Jul;90(1):320-32
PMID: 12611976
-
Resting potential and submembrane calcium concentration of inner hair cells in the isolated mouse cochlea are set by KCNQ-type potassium channels.
J Neurosci. 2003 Mar 15;23(6):2141-9
PMID: 12657673
-
Potassium current properties in apical and basal inner hair cells from guinea-pig cochlea.
Hear Res. 2003 Jun;180(1-2):85-90
PMID: 12782356
-
The afferent synapse of cochlear hair cells.
Curr Opin Neurobiol. 2003 Aug;13(4):452-8
PMID: 12965293
-
Effects of intracellular stores and extracellular Ca(2+) on Ca(2+)-activated K(+) currents in mature mouse inner hair cells.
J Physiol. 2004 Jun 1;557(Pt 2):613-33
PMID: 15064328
-
Purification and characterization of a unique, potent, peptidyl probe for the high conductance calcium-activated potassium channel from venom of the scorpion Buthus tamulus.
J Biol Chem. 1990 Jul 5;265(19):11083-90
PMID: 1694175
-
Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells.
J Neurosci. 1990 Nov;10(11):3664-84
PMID: 1700083
-
Neurofilament antibodies and spiral ganglion neurons of the mammalian cochlea.
J Comp Neurol. 1991 Apr 15;306(3):393-408
PMID: 1865000
-
Potassium currents in inner hair cells isolated from the guinea-pig cochlea.
J Physiol. 1990 Feb;421:263-91
PMID: 2348394
-
Inactivation of the sodium channel. II. Gating current experiments.
J Gen Physiol. 1977 Nov;70(5):567-90
PMID: 591912
-
Age-related changes in the C57BL/6J mouse cochlea. I. Physiological findings.
Brain Res. 1981 Aug;254(1):65-75
PMID: 7272773
-
Clustering of Ca2+ channels and Ca(2+)-activated K+ channels at fluorescently labeled presynaptic active zones of hair cells.
Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7578-82
PMID: 8052623
-
Generation and characterization of subtype-specific monoclonal antibodies to K+ channel alpha- and beta-subunit polypeptides.
Neuropharmacology. 1996;35(7):851-65
PMID: 8938716
-
Paxilline inhibition of the alpha-subunit of the high-conductance calcium-activated potassium channel.
Neuropharmacology. 1996;35(7):963-8
PMID: 8938726
-
Analysis of rat vestibular hair cell development and regeneration using calretinin as an early marker.
J Neurosci. 1997 Nov 1;17(21):8270-82
PMID: 9334402
-
Expression of a potassium current in inner hair cells during development of hearing in mice.
Nature. 1998 Jul 16;394(6690):281-4
PMID: 9685158