Endolymphatic Sodium Homeostasis by Extramacular Epithelium of the Saccule

Kim, Sung Huhn; Marcus, Daniel C.

doi:10.1523/jneurosci.3044-09.2009

Cited by 18 publications

(13 citation statements)

References 64 publications

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“…In addition, Pisam et al [1998] identified what they termed a "patches area" in the roof of the saccular chamber with cellular morphologies suggestive of secretory activity, but heterogeneous across the different teleost species (trout and turbot). The location of their "patches area" is consistent with what has been termed the "extramacular epithelium" of the sacculus in mammals [Kim and Marcus, 2009].…”

Section: Evolution Of the Inner Ear Endolymphatic Systemsupporting

confidence: 67%

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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Section: Evolution Of the Inner Ear Endolymphatic Systemsupporting

confidence: 67%

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

et al. 2018

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“…ENaC is involved in fluid transport in the inner ear, being important for maintaining a much lower sodium concentration in the endolymph in the saccule (220,221), and the semicircular canals (310,311), as compared with that in the perilymph. These findings are of relevance for conditions such as Meniere's disease, where an increased volume of endolymph underlies the dysregulation of balance and symptoms of vertigo experienced by those afflicted.…”

Section: Enac In the Peripheral And Central Nervous Systems And In Sementioning

confidence: 99%

ENaCs and ASICs as therapeutic targets

Qadri

Rooj

Fuller

2012

American Journal of Physiology-Cell Physiology

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The epithelial Na+channel (ENaC) and acid-sensitive ion channel (ASIC) branches of the ENaC/degenerin superfamily of cation channels have drawn increasing attention as potential therapeutic targets in a variety of diseases and conditions. Originally thought to be solely expressed in fluid absorptive epithelia and in neurons, it has become apparent that members of this family exhibit nearly ubiquitous expression. Therapeutic opportunities range from hypertension, due to the role of ENaC in maintaining whole body salt and water homeostasis, to anxiety disorders and pain associated with ASIC activity. As a physiologist intrigued by the fundamental mechanics of salt and water transport, it was natural that Dale Benos, to whom this series of reviews is dedicated, should have been at the forefront of research into the amiloride-sensitive sodium channel. The cloning of ENaC and subsequently the ASIC channels has revealed a far wider role for this channel family than was previously imagined. In this review, we will discuss the known and potential roles of ENaC and ASIC subunits in the wide variety of pathologies in which these channels have been implicated. Some of these, such as the role of ENaC in Liddle's syndrome are well established, others less so; however, all are related in that the fundamental defect is due to inappropriate channel activity.

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“…ENaC was identified in the semicircular canal duct (Pondugula et al, 2006) and non-sensorycells of the extramacular epithelium of the saccul e (Kim and Marcus, 2009). Na + ,K + -ATPase was found in the basolateral surface of semicircular canal duct epithelial cells (α 1 -, α 3 -, β 1 - and β 3 -isoforms) (Pondugula et al, 2006; Pondugula et al, 2004), extramacular epithelium of the saccule (Kim and Marcus, 2009), vestibular dark cells (α 1 -and β 2 -isoforms) (McGuirt and Schulte, 1994), and vestibular transitional cells (α 1 -and β 1 -isoforms) (McGuirt and Schulte, 1994). NKCC1 was found in the basolateral membrane of vestibular dark cells and cellular membrane of transitional cells (Young et al, 2005).…”

Section: Vestibular Systemmentioning

confidence: 99%

Regulation of sodium transport in the inner ear

Kim

Marcus

2011

Hearing Research

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Na+ concentrations in endolymph must be controlled to maintain hair cell function since the transduction channels of hair cells are cation-permeable, but not K+-selective. Flooding or fluctuations of the hair cell cytosol with Na+ would be expected to lead to cellular dysfunction, hearing loss and vertigo. This review briefly describes cellular mechanisms known to be responsible for Na+homeostasis in each compartment of the inner ear, including the cochlea, saccule, semicircular canals and endolymphatic sac. The influx of Na+into endolymph of each of the organs is likely via passive diffusion, but these pathways have not yet been identified or characterized. Na+ absorption is controlled by gate -keeper channels in the apical (endolymphatic) membrane of the transporting cells. Highly Na+-selective epithelial sodium channels (ENaC) control absorption by Reissner’s membrane, saccular extramacular epithelium, semicircular canal duct epithelium and endolymphatic sac. ENaC activity is controlled by a number of signal pathways, but most notably by genomic regulation of channel numbers in the membrane via glucocorticoid signaling. Nonselective cation channels in the apical membrane of outer sulcus epithelial cells and vestibular transitional cells mediate Na+ and parasensory K+ absorption. The K+-mediated transduction current in hair cells is also accompanied by a Na+ flux since the transduction channels are nonselective cation channels. Cation absorption by all of these cells is regulated by extracellular ATP via apical nonselective cation channels (P2X receptors). The heterogeneous population of epithelial cells in the endolymphatic sac is thought to have multiple absorptive pathways for Na+ with regulatory pathways that include glucocorticoids and purinergic agonists.

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Endolymphatic Sodium Homeostasis by Extramacular Epithelium of the Saccule

Cited by 18 publications

References 64 publications

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

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

ENaCs and ASICs as therapeutic targets

Regulation of sodium transport in the inner ear

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