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The Journal of Neuroscience, October 1, 1999, 19(19):8377-8388
Expression of the P2X2 Receptor Subunit of the
ATP-Gated Ion Channel in the Cochlea: Implications for Sound
Transduction and Auditory Neurotransmission
Gary D.
Housley1,
Refik
Kanjhan1,
Nicholas P.
Raybould1,
Denise
Greenwood1,
Salam G.
Salih1,
Leif
Järlebark1,
Lucille D.
Burton1,
Vera C. M.
Setz1,
Mark B.
Cannell1,
Christian
Soeller1,
David L.
Christie2,
Shin-ichi
Usami3,
Atsushi
Matsubara3,
Haruhide
Yoshie3,
Allen F.
Ryan4, and
Peter R.
Thorne1
1 Department of Physiology, Faculty of Medicine and
Health Science and 2 School of Biological Sciences,
University of Auckland, Private Bag 92019, Auckland, New Zealand,
3 Department of Otorhinolaryngology, Hirosaki University
School of Medicine, Hirosaki 036-8562, Japan, and
4 Departments of Surgery and Neuroscience, University of
California San Diego, La Jolla, California 92093
Extracellular ATP has multimodal actions in the cochlea
affecting hearing sensitivity. ATP-gated ion channels involved in this
process were characterized in the guinea pig cochlea. Voltage-clamped hair cells exhibited a P2 receptor pharmacology compatible with the assembly of ATP-gated ion channels from P2X2 receptor
subunits. Reverse transcription-PCR experiments confirmed
expression of the P2X2-1 receptor subunit mRNA isoform in
the sensory epithelium (organ of Corti); a splice variant that confers
desensitization, P2X2-2, was the predominant subunit
isoform expressed by primary auditory neurons. Expression of the
ATP-gated ion channel protein was localized using a P2X2
receptor subunit-specific antiserum. The highest density of
P2X2 subunit-like immunoreactivity in the cochlea occurred
on the hair cell stereocilia, which faces the endolymph. Tissues lining
this compartment exhibited significant P2X2 receptor
subunit expression, with the exception of the stria vascularis.
Expression of ATP-gated ion channels at these sites provides a pathway
for the observed ATP-induced reduction in endocochlear potential and
likely serves a protective role, decoupling the "cochlear
amplifier" in response to stressors, such as noise and ischemia.
Within the perilymphatic compartment, immunolabeling on Deiters' cells
is compatible with purinergic modulation of cochlear micromechanics.
P2X2 receptor subunit expression was also detected in
spiral ganglion primary afferent neurons, and immunoelectron microscopy
localized these subunits to postsynaptic junctions at both inner and
outer hair cells. The former supports a cotransmitter role for ATP in a
subset of type I spiral ganglion neurons, and latter represents the
first characterization of a receptor for a fast neurotransmitter
associated with the type II spiral ganglion neurons.
Key words:
P2X2 receptor; organ of Corti; cochlea; immunocytochemistry; hair cell stereocilia; spiral ganglion; guinea
pig; hearing; ATP; auditory neurotransmission; inner hair cells; outer
hair cells; sound transduction
Copyright © 1999 Society for Neuroscience 0270-6474/99/19198377-12$05.00/0
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