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The Journal of Neuroscience, June 7, 2006, 26(23):6190-6199; doi:10.1523/JNEUROSCI.1116-06.2006

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Cellular/Molecular
Molecular and Functional Characterization of Gap Junctions in the Avian Inner Ear

Regina Nickel,¹ David Becker,² and Andrew Forge¹

¹Centre for Auditory Research, The Ear Institute, University College London, London WC1X 8EE, United Kingdom, and ²Department of Anatomy and Developmental Biology, University College London, London WC1E 6BT, United Kingdom

Correspondence should be addressed to Dr. Regina Nickel, Centre for Auditory Research, The Ear Institute, University College London, 332 Gray’s Inn Road, London WC1X 8EE, UK. Email: r.nickel{at}ucl.ac.uk

To analyze the fundamental role of gap junctions in the vertebrate inner ear, we examined molecular and functional characteristics of gap junctional communication (GJC) in the auditory and vestibular system of the chicken. By screening inner ear tissues for connexin isoforms using degenerate reverse transcription-PCR, we identified, in addition to chicken Cx43 (cCx43) and the inner-ear-specific cCx30, an as yet uncharacterized connexin predicted to be the ortholog of the mammalian Cx26. In situ hybridization indicated that cCx30 and cCx26 transcripts were both widely expressed in the cochlear duct and utricle in an overlapping pattern, suggesting coexpression of these isoforms similar to that in the mammalian inner ear. Immunohistochemistry demonstrated that cCx43 was present in gap junctions connecting supporting cells of the basilar papilla, in which its immunofluorescence colocalized with that of cCx30. However, cCx43 was absent from supporting cell gap junctions of the utricular macula. This variation in the molecular composition of gap junction plaques coincided with differences in the functional properties of GJC between the auditory and vestibular sensory epithelia. Fluorescence recovery after photobleaching, adapted to examine the diffusion of calcein in inner ear explants, revealed asymmetric communication pathways among supporting cells in the basilar papilla but not in the utricular macula. This study supports the hypothesis that the coexpression of Cx26/Cx30 is unique to gap junctions in the vertebrate inner ear. Furthermore, it demonstrates asymmetric GJC within the supporting cell population of the auditory sensory epithelium, which might mediate potassium cycling and/or intercellular signaling.

Key words: connexin; gap junction; fluorescence recovery after photobleaching; supporting cell; inner ear; chicken

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Received March 15, 2006; revised April 12, 2006; accepted April 27, 2006.

Correspondence should be addressed to Dr. Regina Nickel, Centre for Auditory Research, The Ear Institute, University College London, 332 Gray’s Inn Road, London WC1X 8EE, UK. Email: r.nickel{at}ucl.ac.uk

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