Abstract
In the cochlea, mammals maintain a uniquely high endolymphatic potential (EP), which is not observed in other vertebrate groups. However, a high [K+] is always present in the inner ear endolymph. Here, we show that Kir4.1, which is required in the mammalian stria vascularis to generate the highly positive EP, is absent in the functionally equivalent avian tegmentum vasculosum. In contrast, the molecular repertoire required for K+ secretion, specifically NKCC1, KCNQ1, KCNE1, BSND and CLC-K, is shared between the tegmentum vasculosum, the vestibular dark cells and the marginal cells of the stria vascularis. We further show that in barn owls, the tegmentum vasculosum is enlarged and a higher EP (~+34 mV) maintained, compared to other birds. Our data suggest that both the tegmentum vasculosum and the stratified stria vascularis evolved from an ancestral vestibular epithelium that already featured the major cell types of the auditory epithelia. Genetic recruitment of Kir4.1 specifically to strial melanocytes was then a crucial step in mammalian evolution enabling an increase in the cochlear EP. An increased EP may be related to high-frequency hearing, as this is a hallmark of barn owls among birds and mammals among amniotes.
Highlights
In the cochlea, mammals maintain a uniquely high endolymphatic potential (EP), which is not observed in other vertebrate groups
Since the driving force for K+ to enter hair cells is predominantly electrical, the EP critically contributes to the exquisite sensitivity of hair-cell mechanotransduction[2]
An unusually highly positive EP is a hallmark of the mammalian cochlear endolymph. To investigate whether this uniquely high EP is associated with evolutionary differences in the molecular underpinnings, we decided to characterize in the chicken the expression pattern of genes that are known to be involved in mammals
Summary
Mammals maintain a uniquely high endolymphatic potential (EP), which is not observed in other vertebrate groups. The apical part of hair cells, their mechanosensitive hair bundle, is bathed in a very unusual extracellular fluid, the endolymph of scala media[1,2] This fluid resembles in its ionic composition an intracellular milieu, as it features a high concentration of K+ and a low concentration of Na+ (elasmobranchs[3], frogs[4], turtles[4], lizards[3,4], birds[4], mammals[1]). This endolymph shows a positive potential (endolymphatic potential, EP) compared to other extracellular spaces[5]. CLC-K protein family member Homo sapiens CLC-Ka Homo sapiens CLC-Kb Rattus norvegicus CLC-K1 Rattus norvegicus CLC-K2 Monodelphis domesticus CLC-Kx1 Monodelphis domesticus CLC-Kx2 Gallus gallus CLC-k Taeniopygia gutatta CLC-k Anolis carolinensis CLC-k Latimeria chalumnae CLC-k Danio rerio CLC-k Takifugu rubripes CLC-k
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