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The Journal of Neuroscience, September 27, 2006, 26(39):9944-9955; doi:10.1523/JNEUROSCI.2990-06.2006

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Cellular/Molecular
Vestibular Hair Bundles Control pH with (Na⁺, K⁺)/H⁺ Exchangers NHE6 and NHE9

Jennifer K. Hill,¹ Christopher L. Brett,² Anthony Chyou,² Laura M. Kallay,² Masao Sakaguchi,³ Rajini Rao,² and Peter G. Gillespie¹

¹Oregon Hearing Research Center and Vollum Institute, Oregon Health & Science University, Portland, Oregon 97239, ²Department of Physiology, Johns Hopkins University, Baltimore, Maryland 21205, and ³Graduate School of Life Science, University of Hyogo, Ako, Hyogo 678-1297, Japan

Correspondence should be addressed to Peter G. Gillespie, L335A Auditory Neuroscience, Oregon Health & Science University, 3181 SW Sam Jackson Park Road, Portland, OR 97239. Email: gillespp{at}ohsu.edu

In hair cells of the inner ear, robust Ca²⁺/H⁺ exchange mediated by plasma-membrane Ca²⁺-ATPase would rapidly acidify mechanically sensitive hair bundles without efficient removal of H⁺. We found that, whereas the basolateral membrane of vestibular hair cells from the frog saccule extrudes H⁺ via an Na⁺-dependent mechanism, bundles rapidly remove H⁺ in the absence of Na⁺ and HCO₃^–, even when the soma is acidified. K⁺ was fully effective and sufficient for H⁺ removal; in contrast, Rb⁺ failed to support pH recovery. Na⁺/H⁺-exchanger isoform 1 (NHE1) was present on hair-cell soma membranes and was likely responsible for Na⁺-dependent H⁺ extrusion. NHE6 and NHE9 are organellar isoforms that can appear transiently on plasma membranes and have been proposed to mediate K⁺/H⁺ exchange. We identified NHE6 in a subset of hair bundles; NHE9 was present in all bundles. Heterologous expression of these isoforms in yeast strains lacking endogenous exchangers conferred pH-dependent tolerance to high levels of KCl and NaCl. NHE9 preferred cations in the order K⁺, Na⁺ >> Rb⁺, consistent with the relative efficacies of these ions in promoting pH recovery in hair bundles. Electroneutral K⁺/H⁺ exchange, which we propose is performed by NHE9 in hair bundles, exploits the high-K⁺ endolymph, responds only to pH imbalance across the bundle membrane, is unaffected by the +80 mV endocochlear potential, and uses mechanisms already present in the ear for K⁺ recycling. This mechanism allows the hair cell to remove H⁺ generated by Ca²⁺ pumping without ATP hydrolysis in the cell.

Key words: hair cells; H⁺; pH; NHE; ion transport; mechanotransduction

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Received July 14, 2006; revised Aug. 14, 2006; accepted Aug. 16, 2006.

Correspondence should be addressed to Peter G. Gillespie, L335A Auditory Neuroscience, Oregon Health & Science University, 3181 SW Sam Jackson Park Road, Portland, OR 97239. Email: gillespp{at}ohsu.edu

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