Ionic Composition of Endolymph and Perilymph in the Inner Ear of the Oyster Toadfish,<i>Opsanus tau</i>

Ghanem, Tamer; Breneman, Kathryn D.; Rabbitt, Richard D.; Brown, H. M.

doi:10.2307/25066662

Cited by 17 publications

(15 citation statements)

References 60 publications

(73 reference statements)

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“…In addition to being surrounded at basolateral sites by high Na ϩ , low K ϩ -containing physiological extracellular fluids, hair cells, apically via stereocilia (hair cell cytoplasmic extensions), contact endolymph, an extracellular fluid high in K ϩ and low in Na ϩ found in the inner ears of lower and higher vertebrates. Endolymph contains K ϩ at 72.9 mM for the saccule of rainbow trout, Salmo irideus, now O. mykiss (35), and 51.4 mM for the saccule of oyster toadfish, Opsanus tau (36). Measurements in the rat cochlea indicate that endolymph contains K ϩ at 177-171 mM, Na ϩ at 1.0 -2.6 mM, and Cl Ϫ at 140 -132 mM, across basal-apical cochlear turns (37).…”

Section: Discussionmentioning

confidence: 99%

Calcium-dependent Binding of HCN1 Channel Protein to Hair Cell Stereociliary Tip Link Protein Protocadherin 15 CD3

Ramakrishnan

Drescher

Barretto

et al. 2009

Journal of Biological Chemistry

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The cytoplasmic amino terminus of HCN1, the primary full-length HCN isoform expressed in trout saccular hair cells, was found by yeast two-hybrid protocols to bind the cytoplasmic carboxyl-terminal domain of a protocadherin 15a-like protein. HCN1 was immunolocalized to discrete sites on saccular hair cell stereocilia, consistent with gradated distribution expected for tip link sites of protocadherin 15a. HCN1 message was also detected in cDNA libraries of rat cochlear inner and outer hair cells, and HCN1 protein was immunolocalized to cochlear hair cell stereocilia. As predicted by the trout hair cell model, the amino terminus of rat organ of Corti HCN1 was found by yeast two-hybrid analysis to bind the carboxyl terminus of protocadherin 15 CD3, a tip link protein implicated in mechanosensory transduction. Specific binding between HCN1 and protocadherin 15 CD3 was confirmed with pull-down assays and surface plasmon resonance analysis, both predicting dependence on Ca HCN12 is the primary full-length HCN isoform underlying I h (hyperpolarization-activated, cyclic nucleotide-gated, nonselective cation channel current) in a model hair cell preparation from the trout sacccule (1). cAMP-gated I h , possibly in addition to the mechanosensory-transduction current, sets the membrane potential for a subpopulation of saccular hair cells (2, 3). The membrane potential in the saccular hair cell subpopulation is sufficiently depolarized to activate voltage-gated calcium channels, permitting influx of calcium and secretion of hair cell transmitter (2). Given that saccular hair cells expressing I K1 in addition to I h are more hyperpolarized, not supporting activation of the voltage-gated calcium channels, we predicted that spontaneous release of transmitter from the subpopulation of hair cells would constitute hair cell-generated spontaneous activity for the saccule (1). However, little has been previously reported on the morphological localization of the HCN1 isoform in hair cells or possible links to structural proteins that mechanistically would localize HCN1 in hair cells (for preliminary report, see Ref. 4). In general, little is known about proteinprotein interactions for the HCN isoforms that would modulate I h and/or the associated instantaneous current (5).Protocadherin 15 is a proposed tip link protein involved in connecting shorter stereocilia to adjacent taller stereocilia in the stereociliary array of inner ear hair cells, facilitating the opening of the mechanosensory transduction channel in response to auditory and vestibular stimuli. The active tip link protein in Danio rerio is protocadherin 15a (6), characterized by splice variants in its carboxyl terminus. In the mammal, protocadherin 15 CD3 is hypothesized to be a tip link protein at insertion sites in the tips of the shorter stereocilia of the stereociliary array (7,8). EXPERIMENTAL PROCEDURES Acquisition of a Model Hair Cell Preparation from the Trout Saccule and an Organ of Corti Subfraction from theRat Cochlea-Hair cell layers were isolated from the t...

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Section: Discussionmentioning

confidence: 99%

Calcium-dependent Binding of HCN1 Channel Protein to Hair Cell Stereociliary Tip Link Protein Protocadherin 15 CD3

Ramakrishnan

Drescher

Barretto

et al. 2009

Journal of Biological Chemistry

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“…Furthermore, (Na + ) was nearly the same in endolymph and perilymph (295 and 281 mM, respectively) [Murray, 1960]. Similar results were obtained in skates [Peterson et al, 1978] and toadfish [Ghanem et al, 2008]. (Ca 2+ ) concentrations are typically in the range of several mM in fish endolymph [reviewed by Ghanem et al, 2008].…”

Section: Endolymph Composition In the Vestibular Systemmentioning

confidence: 52%

“…Perhaps the least variation is seen in the semicircular canals, of which there are three (except in jawless vertebrates, i.e., hagfish and lam- ) in perilymph (a) and endolymph (b). Different colors identify data from different sources: fish [Ghanem et al, 2008], amphibia (frog) [Corey and Hudspeth, 1983;Bernard et al, 1986], reptiles (pigeon) [Sauer et al, 1999], mammalian vestibular [perilymph: Sterkers et al, 1988;endolymph: Wangemann and Schacht, 1996], and mammalian cochlea [Wangemann, 2006]. Arrows highlight that in fish, endolymphatic (Na + ) is as high as (K + ), and that endolymphatic (Ca 2+ ) varies most drastically between groups.…”

Section: Vestibular Tissues Associated With Endolymph Production and mentioning

confidence: 99%

Evolution of Endolymph Secretion and Endolymphatic Potential Generation in the Vertebrate Inner Ear

et al. 2018

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The ear of extant vertebrates reflects multiple independent evolutionary trajectories. Examples include the middle ear or the unique specializations of the mammalian cochlea. Another striking difference between vertebrate inner ears concerns the differences in the magnitude of the endolymphatic potential. This differs both between the vestibular and auditory part of the inner ear as well as between the auditory periphery in different vertebrates. Here we provide a comparison of the cellular and molecular mechanisms in different endorgans across vertebrates. We begin with the lateral line and vestibular systems, as they likely represent plesiomorphic conditions, then review the situation in different vertebrate auditory endorgans. All three systems harbor hair cells bathed in a high (K⁺) environment. Superficial lateral line neuromasts are bathed in an electrogenically maintained high (K⁺) microenvironment provided by the complex gelatinous cupula. This is associated with a positive endocupular potential. Whether this is a special or a universal feature of lateral line and possibly vestibular cupulae remains to be discovered. The vestibular system represents a closed system with an endolymph that is characterized by an enhanced (K⁺) relative to the perilymph. Yet only in land vertebrates does (K⁺) exceed (Na⁺). The endolymphatic potential ranges from +1 to +11 mV, albeit we note intriguing reports of substantially higher potentials of up to +70 mV in the cupula of ampullae of the semicircular canals. Similarly, in the auditory system, a high (K⁺) is observed. However, in contrast to the vestibular system, the positive endolymphatic potential varies more substantially between vertebrates, ranging from near zero mV to approximately +100 mV. The tissues generating endolymph in the inner ear show considerable differences in cell types and location. So-called dark cells and the possibly homologous ionocytes in fish appear to be the common elements, but there is always at least one additional cell type present. To inspire research in this field, we propose a classification for these cell types and discuss potential evolutionary relationships. Their molecular repertoire is largely unknown and provides further fertile ground for future investigation. Finally, we propose that the ultimate selective pressure for an increased endolymphatic potential, as observed in mammals and to a lesser extent in birds, is specifically to maintain the AC component of the hair-cell receptor potential at high frequencies. In summary, we identify intriguing questions for future directions of research into the molecular and cellular basis of the endolymph in the different compartments of the inner ear. The answers will provide important insights into evolutionary and developmental processes in a sensory organ essential to many species, including humans.

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“…Finally, this signal is transmitted to the brainstem via the 112 cochlear nerve and ultimately to the cerebral cortex where the information is translated into 113 auditory sensations (Lee et al, 2003). 114 Inner ear fluids 115 Mechanoelectrical transduction of sound and motion by the inner ear is highly dependent on 116 the ionic composition of inner ear fluids bathing the auditory hair cells (Ghanem et al, 2008). 117 Endolymph (~ 8µL in human), that bathes the apical surface of hair cells, is an unusual 118 extracellular fluid with a high potassium concentration ([K + ] ~ 160 mM) and a low sodium 119 concentration ([Na + ] < 1 mM) and is positively polarized (~ + 80 mV) compared to 120 cerebrospinal fluid or plasma (Table 1).…”

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confidence: 99%

“…Conversely, perilymph (~ 70µL in human), at the 121 basolateral side of hair cells, has a high [Na + ] (~ 150 mM) and a low [K + ] (~ 4 mM) (Sterkers et 122 al., 1988, Ferrary andSterkers, 1998). The electrochemical gradients between apical 123 endolymph and intracellular space on the one hand, and the basolateral perilymph on the 124 other hand, drive K + transport into hair cells for mechano-bio-transduction of the signal 125 (Ghanem et al, 2008). Small changes from the normal state of perilymph and endolymph 126 (composition, pH, osmolality, potential, volume) result in a decrease of hearing sensitivity 127 (Juhn et al, 2001).…”

mentioning

confidence: 99%

Recent advances in local drug delivery to the inner ear

Kechai

Agnely

Mamelle

et al. 2015

International Journal of Pharmaceutics

137

111

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Ionic Composition of Endolymph and Perilymph in the Inner Ear of the Oyster Toadfish,Opsanus tau

Cited by 17 publications

References 60 publications

Calcium-dependent Binding of HCN1 Channel Protein to Hair Cell Stereociliary Tip Link Protein Protocadherin 15 CD3

Calcium-dependent Binding of HCN1 Channel Protein to Hair Cell Stereociliary Tip Link Protein Protocadherin 15 CD3

Evolution of Endolymph Secretion and Endolymphatic Potential Generation in the Vertebrate Inner Ear

Recent advances in local drug delivery to the inner ear

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