Differences in molecular mechanisms of K+ clearance in the auditory sensory epithelium of birds and mammals

Abstract

Mechanoelectrical transduction in the vertebrate inner ear is a highly conserved mechanism that is dependent on K influx into hair cells. Here, we investigated the molecular underpinnings of subsequent K recycling in the chicken basilar papilla and compared them with those in the mammalian auditory sensory epithelium. As in mammals, the avian auditory hair cell uses KCNQ4, KCNMA1 and KCNMB1 in its K efflux system. Expression of and suggests an additional efflux apparatus in avian hair cells. Marked differences were observed for K clearance. In mammals, KCC3, KCC4, Kir4.1 and CLC-K are present in supporting cells. Of these, only is expressed in avian supporting cells. Instead, they possess NKCC1 to move K across the membrane. This expression pattern suggests an avian clearance mechanism reminiscent of the well-established K uptake apparatus present in inner ear secretory cells. Altogether, tetrapod hair cells show similar mechanisms and supporting cells show distinct molecular underpinnings of K recycling.

Immunohistochemical and ultrastructural characterization of the inner ear epithelial cells of splitnose rockfish (Sebastes diploproa)

“…The exact mechanism(s) is still being debated, and multiple pathways have been proposed for mammalian and avian models (26, 63). However, the mechanistic pathway for K + recycling in fish likely differ as mammalian Deiters’ cells (analogous to the SCs) have neither NKA nor NKCC while avian Deiters’ cells have both basolateral NKA and NKCC (66), whereas our results suggest teleost SCs do not express NKA but do have apical and basolateral NKCC signal. It is unlikely for a cell to possess both apical and basolateral NKCC.…”

Immunohistochemical and ultrastructural characterization of the inner ear epithelial cells of splitnose rockfish (Sebastes diploproa)

“…The primary role of the T1-I has long been proposed to be responsible for maintaining the ionic and acid-base balance of the inner ear endolymph given its ample expression of mitochondria (18,38), NKA (24,37,54), NKCC (37,59), and the potassium channel KCNQ1 (59). In fact, the proposed mechanism for K + secretion within the inner ear appears to be evolutionary conserved (63,66): the teleost T1-I (37) seems to function very similarly to their analogous counterparts, the mammalian marginal cells (72,73) and the avian vestibular dark cells (74). However, and unlike their mammalian and avian counterparts, the teleost inner ear is unique in that their otoliths biomineralizes continuously throughout the fish's life.…”

The evolutionary tuning of hearing

“…The gradient stems from a positive endolymphatic potential, driven by high K + (and low Na + ) concentration in the endolymph, the fluid that bathes the apical surface of hair cells [24]. The K + that enters through mechanotransduction channels is cleared out of the hair cells by passive transport through the basolateral membrane, removed from the extracellular space and pumped back into the endolymph by specialised cells that differ across vertebrates [25][26][27]. The tegmentum vasculosum and the stria vascularis, evolved independently [25] and maintain the high endolymphatic potential in the auditory organs of birds (~10 mV; ~30 mV in owls) and mammals (~100 mV), respectively.…”

“…In mammals, K + leaves the hair cells mainly via kir4.7 channels (encoded by Kcnq4) and via BK Ca 2+ -dependent K + channels. In chicken hair cells, Kcnq1 and Kcne1 are also involved [27].…”

“…Signatures of positive selection have been identified in the coding region of the Cldn14 gene in echolocating toothed whales [82]. Additionally, Slc12a2, which encodes the Na + /K + transporter NKCC1 involved in K + secretion to the endolymph [26] and in K + reuptake by supporting cells in chickens [27], has been under positive selection in naked mole rats [62]. Finally, Gjb2 and Gjb6, the genes coding for connexin 26 and connexin 30 that participate in K + recirculation [83], have been described under convergent evolution in echolocating mammals [50,51].…”