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and Discussion\nIn situ hybridization in the cochlea has suggested that pendrin mRNA is expressed in cells that reside immediately beneath the spiral prominence on the lateral wall of the external sulcus [8]. To determine the location of pendrin protein expression, we performed confocal immunocytochemistry on cryosections prepared from temporal bones of normal (Slc26a4+/+) mice using an established antibody [3]. Staining was absent when the primary antibody was pre-absorbed with the antigenic peptide (data not shown). Strong expression of pendrin was observed not only in outer sulcus epithelial cells, as predicted from in situ hybridization data, but also in root cells, in apical membranes of spiral prominence surface epithelial cells and in apical membranes of spindle-shaped cells that are part of stria vascularis (Fig. 1a,1b,1c). The presence of pendrin in spindle-shaped cells suggests that these cells secrete HCO3 - into endolymph. Pendrin-mediated HCO3 - transport has previously been shown in the kidney [9]. HCO3 - in the cochlea may be generated from CO2 by carbonic anhydrase located in strial intermediate cells [18,19]. CO2 may be supplied by the metabolically highly active stria marginal cells. It is conceivable that pendrin dysfunction interrupts HCO3 - secretion and leads to an accumulation of HCO3 - in stria vascularis. Preliminary data (Wangemann et al., unpublished) support a role for pendrin in HCO3 - secretion into endolymph.\nFigure 1 Protein localization of pendrin, KCNQ1, ZO-1 and F actin in cochlea and vestibular labyrinth of Slc26a4+/+ and Slc26a4-/- mice. a: Overview of cochlea; bar = 100 μm. b-f: Detail of cochlear lateral wall; bar = 10 μm. g: Detail of utricle; bar = 10 μm. h-i: Detail of ampulla; bar = 10 μm. RM, Reissner's membrane; SC, spindle-shaped cells, SMC, strial marginal cells; SV, stria vascularis; SL, spiral ligament; LIM, spiral limbus. BC, basal cells; SP, spiral prominence epithelial cells; RC, root cells; OS, outer sulcus epithelial cells; VHC, vestibular hair cells; VTC, vestibular transitional cells; VDC, vestibular dark cells; arrows, basal cells at the top and bottom of stria vascularis form tight junctions with surface epithelial cells. The extent of pendrin expression in spiral prominence cells and stria vascularis was determined by labeling KCNQ1, a K+ channel that is expressed in strial marginal cells, and ZO-1, a tight junction protein that labels basal cells and thereby delineates the boundaries of stria vascularis. Dual labeling experiments demonstrated that pendrin is expressed in spindle-shaped cells, which are surface epithelial cells in stria vascularis adjacent to strial marginal cells near the borders of both the spiral prominence and Reissner's membrane (Fig. 1c).\nIn situ hybridization in the vestibular labyrinth suggested that pendrin mRNA is expressed in non-sensory cells [8]. Using confocal immunocytochemistry on cryosections, we observed strong expression of the pendrin protein in the apical membrane of vestibular transitional cells in the utricle and ampullae (Fig. 1g,1h,1i). Dual labeling with KCNQ1 demonstrated that pendrin expression was clearly limited to vestibular transitional cells and did not extend to other non-sensory cells such as vestibular dark cells, which were clearly identified by the expression of KCNQ1 and KCNE1 in their apical membranes.\nThe onset of pendrin expression during development of the mouse inner ear has been determined to be embryonic day (ED) 13 [14]. Morphologically detectable differences in the inner ears of Slc26a4+/+ and Slc26a4-/- mice become evident as early as ED 15, when Slc26a4-/- mice start to develop an enlarged endolymphatic space that persists into adulthood [14]. Interestingly, sensory hair cells in the cochlea appear normal until postnatal day (PD) 7 but show clear evidence of degeneration by PD 15 [14]. These observations suggest that the cochlear environment supports the survival of sensory hair cells in spite of the enlargement of the endolymphatic duct. A normal endolymphatic K+ concentration, which is critical for hair cell survival [20], is established at PD 3 [21] and may persist in Slc26a4-/- at least until PD 7. The time period between PD 7 and 15 is the time when the endocochlear potential develops at the onset of hearing [22]. We hypothesized that a lack of a normal endocochlear potential or an alteration of the endolymphatic K+ concentration could account for deafness in Slc26a4-/- mice. Measurements revealed that the endocochlear potential was absent but that the endolymphatic K+ concentration was normal in adult Slc26a4-/- (Fig. 2a). No significant differences between Slc26a4+/+ and Slc26a4-/- mice were found in perilymphatic (Fig. 2a) or plasma K+ concentrations (Slc26a4+/+, 4.9 ± 0.3 mM, n = 6; Slc26a4-/-, 5.1 ± 0.3 mM, n = 6). These observations suggest that a primary event leading to deafness in Slc26a4-/- mice, and potentially in patients suffering from Pendred syndrome, is the loss of the endocochlear potential. Degeneration of hair cells is probably a response to the loss of the endocochlear potential.\nFigure 2 Potential, K+ concentrations and pigmentation of stria vascularis in Slc26a4+/+ and Slc26a4-/- mice. a: Endocochlear potential and K+ concentrations in endolymph and perilymph at the apex (A) and base (B) of the cochlea. Numbers adjacent to symbols denote number of measurements. b-d: Pigmentation of stria vascularis in Slc26a4+/+ and Slc26a4-/- mice. b: View of stria vascularis through the bony capsule of the cochlea. OW, oval window, RW, round window; arrows, stria vascularis. c-d: Whole-mounts of stria vascularis isolated from age-matched mice. c: Laser-scanning images, bar = 10 μm, d: Quantification of pigmentation based on optical density. The endocochlear potential is generated by stria vascularis in the lateral wall of the cochlea [17,23]. The potential is generated across the basal cell barrier of stria vascularis by the K+ channel KCNJ10 located in intermediate cells [24], which are connected to basal cells by a high density of gap junctions [25]. Marginal cells of stria vascularis, which form the barrier toward endolymph, transport K+ from the intrastrial space into endolymph and keep the K+ concentration low adjacent to the KCNJ10 K+ channel [26]. To determine the cause of the loss of the endocochlear potential in Slc26a4-/- mice, we first determined whether intermediate cells are present in stria vascularis, since a loss of intermediate cells is known to lead to a loss of the endocochlear potential [27,28]. Intermediate cells of stria vascularis were visualized by their pigmentation. Pigmentation was present in stria vascularis of Slc26a4-/- mice (Fig. 2b), which suggests that intermediate cells are present. Interestingly, pigmentation of stria vascularis was much stronger in Slc26a4-/- than in Slc26a4+/+ mice.\nTo determine in greater detail the cause of the loss of the endocochlear potential in Slc26a4-/- mice, we isolated total RNA from stria vascularis and spiral ganglia of young (1–4 month) Slc26a4+/+ and both young and old (~12 month) Slc26a4-/- mice, assessed amounts of isolated tissues by quantification of 18S rRNA, and quantified the expression of KCNJ10 mRNA. Quantities of stria vascularis isolated from these different mice were similar, since no significant differences were found in the numbers of 18S rRNA molecules (log(rRNA) = 9.46 ± 0.08, n = 17, pooled data). In contrast, quantities of spiral ganglia isolated from young and old Slc26a4-/- mice (log(rRNA) = 9.04 ± 0.18, n = 4 and 9.29 ± 0.15, n = 6) were significantly smaller than in Slc26a4+/+ mice (log(rRNA) = 9.48 ± 0.19, n = 7), consistent with morphometric data (see below). Expression of KCNJ10 mRNA was normal in stria vascularis and spiral ganglia of young Slc26a4-/- mice but significantly reduced in old Slc26a4-/- mice (Fig. 3). Quantifications of KCNQ1 and KCNQ4 mRNA were used to assess possible cross-contamination between the stria vascularis and spiral ganglia preparations based on the assumptions that (1) KCNQ1 is expressed in cells of the stria vascularis but not the spiral ganglia preparation and (2) KCNQ4 is expressed in cells of the spiral ganglia but not the stria vascularis preparation. The number of KCNQ1 mRNA molecules in stria vascularis was 24-fold greater than in spiral ganglia, and the number of KCNQ4 mRNA molecules in spiral ganglia was 5-fold greater than in stria vascularis. These observations validate our measurements of KCNJ10 and KCNQ1 by demonstrating that the microdissected preparations of stria vascularis and spiral ganglia were 98% and 78% pure, respectively.\nFigure 3 Quantification of KCNJ10 and KCNQ1 mRNA expression in stria vascularis and spiral ganglia of Slc26a4+/+ and Slc26a4-/- mice. a: Electropherogram of total RNA isolated from stria vascularis microdissected from one mouse. The amount of total RNA was obtained from the total integral (shaded) and the amount of 18S rRNA was obtained from the integral of the 18S peak. Sharp peaks representing 18S and 28S rRNA demonstrate the high quality of RNA. Insert: Genotype of Slc26a4-/- mice was verified by the observation of one or few very large rhomboedric otoconia in the utricular macula (arrow). A, crista ampullaris; U, utricular macula. Scale bar: 100 μm. b: Example of real-time RT-PCR data used for quantification of 18S, KCNJ10, KCNQ1 and KCNQ4. Known quantities of 18S rRNA were used to calibrate the threshold. SV, stria vascularis; SG, spiral ganglia. c: Quantification of KCNJ10 and KCNQ1 mRNA in young Slc26a4+/+ and young and old Slc26a4-/- mice. The presence of KCNJ10 mRNA in stria vascularis of Slc26a4-/- mice supports the finding that intermediate cells are present. Expression of the KCNJ10 protein was assessed in young Slc26a4-/- mice by confocal immunocytochemistry. Interestingly, expression of the KCNJ10 protein was absent in stria vascularis but normal in spiral ganglia (Fig. 4). The absence of the KCNJ10 K+ channel in stria vascularis is sufficient to explain the loss of the endocochlear potential [17].\nFigure 4 Protein localization of KCNJ10 in the cochlea of Slc26a4+/+ and Slc26a4-/- mice. a: Overview of cochlea; bar = 100 μm. Compare to Fig. 1a to note the enlarged scala media and the distended Reissner's membrane. b-c: Detail of lateral wall and spiral ganglia (insert); main bar: 10 μm, insert: 5 μm. Expression of KCNJ10 in Slc26a4-/- mice was absent in stria vascularis but unchanged in spiral ganglion cells. RM, Reissner's membrane, SV, stria vascularis; SP, spiral prominence; SL, spiral ligament; LIM, spiral limbus; SG, spiral ganglion. Histological evaluation of cryosections revealed an enlargement of scala media with a large bulging of Reissner's membrane and an apparent degeneration of the organ of Corti, as described earlier [14]. Tissue height of stria vascularis was normal (Fig. 5), consistent with the similar numbers of 18S rRNA molecules in isolated preparations (see above). The absence of a change in tissue height is consistent with the presence of intermediate cells [28]. Further, we observed an apparent loss of tissue masses in areas that are normally occupied primarily by type I and II fibrocytes. Spiral prominence in Slc26a4-/- mice was less prominent, spiral ligament thinner and spiral limbus flatter (Fig. 5). The observation that tissue masses were lost in the spiral limbus region is consistent with the finding of a reduced number of 18S rRNA molecules in the spiral ganglia preparation (see above). In addition, we observed an apparent degeneration of stria vascularis, including an increase in pigmentation and an irregular pattern of the tight junctions of marginal cells (Fig. 2c, 6,7). Tight junctions were visualized by F-actin expression. Marginal cells appeared to form a continuous layer.\nFigure 5 Morphometric analysis of cochlear tissue masses in Slc26a4+/+ and Slc26a4-/- mice. a: locations of measurements. Thickness of stria vascularis (SV) was obtained as average of three distance measurements perpendicular to the surface of marginal cells. Thickness of spiral prominence (SP) was measured perpendicular to a tangential line (dashed) that connects the surface of the outer sulcus (OS) with the basal layer of stria vascularis. Thickness of spiral ligament (SL) was measured perpendicular to the tangential line as distance between the surface of spiral prominence and the interface between spiral ligament and bone (B). Thickness of spiral limbus (LIM) was obtained perpendicular to the surface of the bone as a tangential line that touches the inner sulcus (IS) and reaches from the surface of the spiral limbus to the interface between spiral limbus connective tissue and bone. b: Summary. Data from 7–8 animals contributed to each column.\nFigure 6 Analysis of marginal and basal cell barriers by in Slc26a4-/- mice. Tight junctions were visualized by F actin. Whole-mounts of stria vascularis were viewed either from the basal cell side (a-f) or from the marginal cell side (g-l). Bright field images verify that the same area was viewed from either side (b and h). Colored bright field images were mixed with images of F actin staining to indicate the position of pigment granules (d, j, f and l). Focus was varied to either visualize the marginal cell barrier (SMC, c-d and i-j) or the basal cell barrier (BC, e-f and k-l). Both the marginal cell (e-f) and the basal cell barrier (i-f) appeared to be intact. It was critical for this finding that pigmentation did not block the path of the laser. Blockage of the laser by pigmentation produces the untrue impression of a discontinuous marginal cell barrier (c-d) or basal cell barrier (k-l). Comparison of images is aided by marking a significant area with a star. Bars = 10 μm.\nFigure 7 Analysis of marginal and basal cell barriers in Slc26a4+/+ and Slc26a4-/- mice. Tight junctions were visualized by F actin in whole-mounts of stria vascularis. Bright field images were taken to evaluate pigmentation (a, d and g). Note the intact marginal cell (b) and basal cell (c) barriers in Slc26a4+/+ mice. Minimal pigmentation of Slc26a4+/+ mice did not compromise F actin localization. Whole-mounts of stria vascularis from Slc26a4-/- mice were viewed either from the basal cell side (e-f) or from the marginal cell side (h-i). Bright field images verify that the same area was viewed from either side (d and g). Focus was varied to either visualize the marginal cell barrier (SMC, b,e and h) or the basal cell barrier (BC, c,f and i). Both the basal cell (f) and the marginal cell (h) barriers appeared to be intact. Blockage of the laser by pigmentation produces the untrue impression of 'holes' in the marginal cell barrier (e) or basal cell barrier (i). Comparison of images is aided by marking three significant areas with colored stars. Bars = 10 μm. Pendrin-expressing surface epithelial cells in the spiral prominence region are located in an area where basal cells, which are interconnected by tight junctions, form additional tight junctions with surface epithelial cells [29]. A discontinuity of this complex junction in Slc26a4-/- mice would explain the absence of the endocochlear potential. To evaluate the presence of this connection, we determined by confocal immunocytochemistry the expression of ZO-1 and of F-actin, which associate with tight junction complexes. ZO-1 and F-actin expression revealed a continuous layer of basal cells, including a junction of basal cells with surface epithelial cells in Slc26a4-/- mice, as observed in normal mice (Fig. 1c,1d,1e,1f,6,7). These observations make it unlikely that the primary cause of the loss of the endocochlear potential is a compromise in the basal cell barrier.\nThe observation that endolymphatic and perilymphatic K+ concentrations were normal in Slc26a4-/- mice suggests that stria vascularis was able to secrete K+ in spite of the apparent signs of degeneration. The rate of K+ secretion necessary to maintain endolymphatic K+ concentration, however, may be less than necessary in Slc26a4+/+ mice given the reduced numbers of sensory hair cells, which provide a major pathway for K+ exit from endolymph [30,31]. In order to substantiate the view that stria vascularis in Slc26a4-/- secretes K+, we measured the magnitude of the bumetanide-sensitive current exiting stria vascularis across the apical membrane of strial marginal cells and determined the expression of the proteins KCNQ1, KCNE1 and SLC12A2, which are essential for K+ secretion [20,32,33], and of GJB2 (Cx26), which is thought to contribute to K+ cycling [23]. K+ secretion is known to be sensitive to 10-5 M bumetanide, a loop-diuretic that inhibits the Na+/2Cl-/K+ cotransporter SLC12A2 [26]. Bumetanide-sensitive currents were found in both Slc26a4+/+ and Slc26a4-/- mice although the magnitude of the current was significantly smaller in Slc26a4-/- mice (22 ± 6 μA/cm2, n = 4 versus 14 ± 2 μA/cm2, n = 4). KCNQ1 and KCNE1, subunits of the secretory K+ channel, were co-localized in the apical membrane of strial marginal cells; the Na+/2Cl-/K+ cotransporter SLC12A2, which is located in the basolateral membrane of strial marginal cells, was found in stria vascularis; and the gap junction protein GJB2 was found in spiral ligament of Slc26a4+/+ and Slc26a4-/- mice (Fig. 8). Co-localization of KCNQ1 and KCNE1 proteins was also observed in vestibular dark cells (Fig. 1i). Expression of KCNQ1 protein in stria vascularis of Slc26a4-/- mice is consistent with the finding of KCNQ1 mRNA expression (Fig. 3). These observations make it unlikely that the primary cause of the loss of the endocochlear potential is a compromise of K+ secretion by strial marginal cells or a compromise of gap junction mediated K+ cycling.\nFigure 8 Protein localization of KCNQ1, KCNE1, SLC12A2 and GJB2 in the cochlear lateral wall of Slc26a4+/+ and Slc26a4-/- mice. a-f: bars: 10 μm. SMC, strial marginal cells; SV, stria vascularis; BC, basal cells; SL, spiral ligament."}

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and Discussion\nIn situ hybridization in the cochlea has suggested that pendrin mRNA is expressed in cells that reside immediately beneath the spiral prominence on the lateral wall of the external sulcus [8]. To determine the location of pendrin protein expression, we performed confocal immunocytochemistry on cryosections prepared from temporal bones of normal (Slc26a4+/+) mice using an established antibody [3]. Staining was absent when the primary antibody was pre-absorbed with the antigenic peptide (data not shown). Strong expression of pendrin was observed not only in outer sulcus epithelial cells, as predicted from in situ hybridization data, but also in root cells, in apical membranes of spiral prominence surface epithelial cells and in apical membranes of spindle-shaped cells that are part of stria vascularis (Fig. 1a,1b,1c). The presence of pendrin in spindle-shaped cells suggests that these cells secrete HCO3 - into endolymph. Pendrin-mediated HCO3 - transport has previously been shown in the kidney [9]. HCO3 - in the cochlea may be generated from CO2 by carbonic anhydrase located in strial intermediate cells [18,19]. CO2 may be supplied by the metabolically highly active stria marginal cells. It is conceivable that pendrin dysfunction interrupts HCO3 - secretion and leads to an accumulation of HCO3 - in stria vascularis. Preliminary data (Wangemann et al., unpublished) support a role for pendrin in HCO3 - secretion into endolymph.\nFigure 1 Protein localization of pendrin, KCNQ1, ZO-1 and F actin in cochlea and vestibular labyrinth of Slc26a4+/+ and Slc26a4-/- mice. a: Overview of cochlea; bar = 100 μm. b-f: Detail of cochlear lateral wall; bar = 10 μm. g: Detail of utricle; bar = 10 μm. h-i: Detail of ampulla; bar = 10 μm. RM, Reissner's membrane; SC, spindle-shaped cells, SMC, strial marginal cells; SV, stria vascularis; SL, spiral ligament; LIM, spiral limbus. BC, basal cells; SP, spiral prominence epithelial cells; RC, root cells; OS, outer sulcus epithelial cells; VHC, vestibular hair cells; VTC, vestibular transitional cells; VDC, vestibular dark cells; arrows, basal cells at the top and bottom of stria vascularis form tight junctions with surface epithelial cells. The extent of pendrin expression in spiral prominence cells and stria vascularis was determined by labeling KCNQ1, a K+ channel that is expressed in strial marginal cells, and ZO-1, a tight junction protein that labels basal cells and thereby delineates the boundaries of stria vascularis. Dual labeling experiments demonstrated that pendrin is expressed in spindle-shaped cells, which are surface epithelial cells in stria vascularis adjacent to strial marginal cells near the borders of both the spiral prominence and Reissner's membrane (Fig. 1c).\nIn situ hybridization in the vestibular labyrinth suggested that pendrin mRNA is expressed in non-sensory cells [8]. Using confocal immunocytochemistry on cryosections, we observed strong expression of the pendrin protein in the apical membrane of vestibular transitional cells in the utricle and ampullae (Fig. 1g,1h,1i). Dual labeling with KCNQ1 demonstrated that pendrin expression was clearly limited to vestibular transitional cells and did not extend to other non-sensory cells such as vestibular dark cells, which were clearly identified by the expression of KCNQ1 and KCNE1 in their apical membranes.\nThe onset of pendrin expression during development of the mouse inner ear has been determined to be embryonic day (ED) 13 [14]. Morphologically detectable differences in the inner ears of Slc26a4+/+ and Slc26a4-/- mice become evident as early as ED 15, when Slc26a4-/- mice start to develop an enlarged endolymphatic space that persists into adulthood [14]. Interestingly, sensory hair cells in the cochlea appear normal until postnatal day (PD) 7 but show clear evidence of degeneration by PD 15 [14]. These observations suggest that the cochlear environment supports the survival of sensory hair cells in spite of the enlargement of the endolymphatic duct. A normal endolymphatic K+ concentration, which is critical for hair cell survival [20], is established at PD 3 [21] and may persist in Slc26a4-/- at least until PD 7. The time period between PD 7 and 15 is the time when the endocochlear potential develops at the onset of hearing [22]. We hypothesized that a lack of a normal endocochlear potential or an alteration of the endolymphatic K+ concentration could account for deafness in Slc26a4-/- mice. Measurements revealed that the endocochlear potential was absent but that the endolymphatic K+ concentration was normal in adult Slc26a4-/- (Fig. 2a). No significant differences between Slc26a4+/+ and Slc26a4-/- mice were found in perilymphatic (Fig. 2a) or plasma K+ concentrations (Slc26a4+/+, 4.9 ± 0.3 mM, n = 6; Slc26a4-/-, 5.1 ± 0.3 mM, n = 6). These observations suggest that a primary event leading to deafness in Slc26a4-/- mice, and potentially in patients suffering from Pendred syndrome, is the loss of the endocochlear potential. Degeneration of hair cells is probably a response to the loss of the endocochlear potential.\nFigure 2 Potential, K+ concentrations and pigmentation of stria vascularis in Slc26a4+/+ and Slc26a4-/- mice. a: Endocochlear potential and K+ concentrations in endolymph and perilymph at the apex (A) and base (B) of the cochlea. Numbers adjacent to symbols denote number of measurements. b-d: Pigmentation of stria vascularis in Slc26a4+/+ and Slc26a4-/- mice. b: View of stria vascularis through the bony capsule of the cochlea. OW, oval window, RW, round window; arrows, stria vascularis. c-d: Whole-mounts of stria vascularis isolated from age-matched mice. c: Laser-scanning images, bar = 10 μm, d: Quantification of pigmentation based on optical density. The endocochlear potential is generated by stria vascularis in the lateral wall of the cochlea [17,23]. The potential is generated across the basal cell barrier of stria vascularis by the K+ channel KCNJ10 located in intermediate cells [24], which are connected to basal cells by a high density of gap junctions [25]. Marginal cells of stria vascularis, which form the barrier toward endolymph, transport K+ from the intrastrial space into endolymph and keep the K+ concentration low adjacent to the KCNJ10 K+ channel [26]. To determine the cause of the loss of the endocochlear potential in Slc26a4-/- mice, we first determined whether intermediate cells are present in stria vascularis, since a loss of intermediate cells is known to lead to a loss of the endocochlear potential [27,28]. Intermediate cells of stria vascularis were visualized by their pigmentation. Pigmentation was present in stria vascularis of Slc26a4-/- mice (Fig. 2b), which suggests that intermediate cells are present. Interestingly, pigmentation of stria vascularis was much stronger in Slc26a4-/- than in Slc26a4+/+ mice.\nTo determine in greater detail the cause of the loss of the endocochlear potential in Slc26a4-/- mice, we isolated total RNA from stria vascularis and spiral ganglia of young (1–4 month) Slc26a4+/+ and both young and old (~12 month) Slc26a4-/- mice, assessed amounts of isolated tissues by quantification of 18S rRNA, and quantified the expression of KCNJ10 mRNA. Quantities of stria vascularis isolated from these different mice were similar, since no significant differences were found in the numbers of 18S rRNA molecules (log(rRNA) = 9.46 ± 0.08, n = 17, pooled data). In contrast, quantities of spiral ganglia isolated from young and old Slc26a4-/- mice (log(rRNA) = 9.04 ± 0.18, n = 4 and 9.29 ± 0.15, n = 6) were significantly smaller than in Slc26a4+/+ mice (log(rRNA) = 9.48 ± 0.19, n = 7), consistent with morphometric data (see below). Expression of KCNJ10 mRNA was normal in stria vascularis and spiral ganglia of young Slc26a4-/- mice but significantly reduced in old Slc26a4-/- mice (Fig. 3). Quantifications of KCNQ1 and KCNQ4 mRNA were used to assess possible cross-contamination between the stria vascularis and spiral ganglia preparations based on the assumptions that (1) KCNQ1 is expressed in cells of the stria vascularis but not the spiral ganglia preparation and (2) KCNQ4 is expressed in cells of the spiral ganglia but not the stria vascularis preparation. The number of KCNQ1 mRNA molecules in stria vascularis was 24-fold greater than in spiral ganglia, and the number of KCNQ4 mRNA molecules in spiral ganglia was 5-fold greater than in stria vascularis. These observations validate our measurements of KCNJ10 and KCNQ1 by demonstrating that the microdissected preparations of stria vascularis and spiral ganglia were 98% and 78% pure, respectively.\nFigure 3 Quantification of KCNJ10 and KCNQ1 mRNA expression in stria vascularis and spiral ganglia of Slc26a4+/+ and Slc26a4-/- mice. a: Electropherogram of total RNA isolated from stria vascularis microdissected from one mouse. The amount of total RNA was obtained from the total integral (shaded) and the amount of 18S rRNA was obtained from the integral of the 18S peak. Sharp peaks representing 18S and 28S rRNA demonstrate the high quality of RNA. Insert: Genotype of Slc26a4-/- mice was verified by the observation of one or few very large rhomboedric otoconia in the utricular macula (arrow). A, crista ampullaris; U, utricular macula. Scale bar: 100 μm. b: Example of real-time RT-PCR data used for quantification of 18S, KCNJ10, KCNQ1 and KCNQ4. Known quantities of 18S rRNA were used to calibrate the threshold. SV, stria vascularis; SG, spiral ganglia. c: Quantification of KCNJ10 and KCNQ1 mRNA in young Slc26a4+/+ and young and old Slc26a4-/- mice. The presence of KCNJ10 mRNA in stria vascularis of Slc26a4-/- mice supports the finding that intermediate cells are present. Expression of the KCNJ10 protein was assessed in young Slc26a4-/- mice by confocal immunocytochemistry. Interestingly, expression of the KCNJ10 protein was absent in stria vascularis but normal in spiral ganglia (Fig. 4). The absence of the KCNJ10 K+ channel in stria vascularis is sufficient to explain the loss of the endocochlear potential [17].\nFigure 4 Protein localization of KCNJ10 in the cochlea of Slc26a4+/+ and Slc26a4-/- mice. a: Overview of cochlea; bar = 100 μm. Compare to Fig. 1a to note the enlarged scala media and the distended Reissner's membrane. b-c: Detail of lateral wall and spiral ganglia (insert); main bar: 10 μm, insert: 5 μm. Expression of KCNJ10 in Slc26a4-/- mice was absent in stria vascularis but unchanged in spiral ganglion cells. RM, Reissner's membrane, SV, stria vascularis; SP, spiral prominence; SL, spiral ligament; LIM, spiral limbus; SG, spiral ganglion. Histological evaluation of cryosections revealed an enlargement of scala media with a large bulging of Reissner's membrane and an apparent degeneration of the organ of Corti, as described earlier [14]. Tissue height of stria vascularis was normal (Fig. 5), consistent with the similar numbers of 18S rRNA molecules in isolated preparations (see above). The absence of a change in tissue height is consistent with the presence of intermediate cells [28]. Further, we observed an apparent loss of tissue masses in areas that are normally occupied primarily by type I and II fibrocytes. Spiral prominence in Slc26a4-/- mice was less prominent, spiral ligament thinner and spiral limbus flatter (Fig. 5). The observation that tissue masses were lost in the spiral limbus region is consistent with the finding of a reduced number of 18S rRNA molecules in the spiral ganglia preparation (see above). In addition, we observed an apparent degeneration of stria vascularis, including an increase in pigmentation and an irregular pattern of the tight junctions of marginal cells (Fig. 2c, 6,7). Tight junctions were visualized by F-actin expression. Marginal cells appeared to form a continuous layer.\nFigure 5 Morphometric analysis of cochlear tissue masses in Slc26a4+/+ and Slc26a4-/- mice. a: locations of measurements. Thickness of stria vascularis (SV) was obtained as average of three distance measurements perpendicular to the surface of marginal cells. Thickness of spiral prominence (SP) was measured perpendicular to a tangential line (dashed) that connects the surface of the outer sulcus (OS) with the basal layer of stria vascularis. Thickness of spiral ligament (SL) was measured perpendicular to the tangential line as distance between the surface of spiral prominence and the interface between spiral ligament and bone (B). Thickness of spiral limbus (LIM) was obtained perpendicular to the surface of the bone as a tangential line that touches the inner sulcus (IS) and reaches from the surface of the spiral limbus to the interface between spiral limbus connective tissue and bone. b: Summary. Data from 7–8 animals contributed to each column.\nFigure 6 Analysis of marginal and basal cell barriers by in Slc26a4-/- mice. Tight junctions were visualized by F actin. Whole-mounts of stria vascularis were viewed either from the basal cell side (a-f) or from the marginal cell side (g-l). Bright field images verify that the same area was viewed from either side (b and h). Colored bright field images were mixed with images of F actin staining to indicate the position of pigment granules (d, j, f and l). Focus was varied to either visualize the marginal cell barrier (SMC, c-d and i-j) or the basal cell barrier (BC, e-f and k-l). Both the marginal cell (e-f) and the basal cell barrier (i-f) appeared to be intact. It was critical for this finding that pigmentation did not block the path of the laser. Blockage of the laser by pigmentation produces the untrue impression of a discontinuous marginal cell barrier (c-d) or basal cell barrier (k-l). Comparison of images is aided by marking a significant area with a star. Bars = 10 μm.\nFigure 7 Analysis of marginal and basal cell barriers in Slc26a4+/+ and Slc26a4-/- mice. Tight junctions were visualized by F actin in whole-mounts of stria vascularis. Bright field images were taken to evaluate pigmentation (a, d and g). Note the intact marginal cell (b) and basal cell (c) barriers in Slc26a4+/+ mice. Minimal pigmentation of Slc26a4+/+ mice did not compromise F actin localization. Whole-mounts of stria vascularis from Slc26a4-/- mice were viewed either from the basal cell side (e-f) or from the marginal cell side (h-i). Bright field images verify that the same area was viewed from either side (d and g). Focus was varied to either visualize the marginal cell barrier (SMC, b,e and h) or the basal cell barrier (BC, c,f and i). Both the basal cell (f) and the marginal cell (h) barriers appeared to be intact. Blockage of the laser by pigmentation produces the untrue impression of 'holes' in the marginal cell barrier (e) or basal cell barrier (i). Comparison of images is aided by marking three significant areas with colored stars. Bars = 10 μm. Pendrin-expressing surface epithelial cells in the spiral prominence region are located in an area where basal cells, which are interconnected by tight junctions, form additional tight junctions with surface epithelial cells [29]. A discontinuity of this complex junction in Slc26a4-/- mice would explain the absence of the endocochlear potential. To evaluate the presence of this connection, we determined by confocal immunocytochemistry the expression of ZO-1 and of F-actin, which associate with tight junction complexes. ZO-1 and F-actin expression revealed a continuous layer of basal cells, including a junction of basal cells with surface epithelial cells in Slc26a4-/- mice, as observed in normal mice (Fig. 1c,1d,1e,1f,6,7). These observations make it unlikely that the primary cause of the loss of the endocochlear potential is a compromise in the basal cell barrier.\nThe observation that endolymphatic and perilymphatic K+ concentrations were normal in Slc26a4-/- mice suggests that stria vascularis was able to secrete K+ in spite of the apparent signs of degeneration. The rate of K+ secretion necessary to maintain endolymphatic K+ concentration, however, may be less than necessary in Slc26a4+/+ mice given the reduced numbers of sensory hair cells, which provide a major pathway for K+ exit from endolymph [30,31]. In order to substantiate the view that stria vascularis in Slc26a4-/- secretes K+, we measured the magnitude of the bumetanide-sensitive current exiting stria vascularis across the apical membrane of strial marginal cells and determined the expression of the proteins KCNQ1, KCNE1 and SLC12A2, which are essential for K+ secretion [20,32,33], and of GJB2 (Cx26), which is thought to contribute to K+ cycling [23]. K+ secretion is known to be sensitive to 10-5 M bumetanide, a loop-diuretic that inhibits the Na+/2Cl-/K+ cotransporter SLC12A2 [26]. Bumetanide-sensitive currents were found in both Slc26a4+/+ and Slc26a4-/- mice although the magnitude of the current was significantly smaller in Slc26a4-/- mice (22 ± 6 μA/cm2, n = 4 versus 14 ± 2 μA/cm2, n = 4). KCNQ1 and KCNE1, subunits of the secretory K+ channel, were co-localized in the apical membrane of strial marginal cells; the Na+/2Cl-/K+ cotransporter SLC12A2, which is located in the basolateral membrane of strial marginal cells, was found in stria vascularis; and the gap junction protein GJB2 was found in spiral ligament of Slc26a4+/+ and Slc26a4-/- mice (Fig. 8). Co-localization of KCNQ1 and KCNE1 proteins was also observed in vestibular dark cells (Fig. 1i). Expression of KCNQ1 protein in stria vascularis of Slc26a4-/- mice is consistent with the finding of KCNQ1 mRNA expression (Fig. 3). These observations make it unlikely that the primary cause of the loss of the endocochlear potential is a compromise of K+ secretion by strial marginal cells or a compromise of gap junction mediated K+ cycling.\nFigure 8 Protein localization of KCNQ1, KCNE1, SLC12A2 and GJB2 in the cochlear lateral wall of Slc26a4+/+ and Slc26a4-/- mice. a-f: bars: 10 μm. SMC, strial marginal cells; SV, stria vascularis; BC, basal cells; SL, spiral ligament."}

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and Discussion\nIn situ hybridization in the cochlea has suggested that pendrin mRNA is expressed in cells that reside immediately beneath the spiral prominence on the lateral wall of the external sulcus [8]. To determine the location of pendrin protein expression, we performed confocal immunocytochemistry on cryosections prepared from temporal bones of normal (Slc26a4+/+) mice using an established antibody [3]. Staining was absent when the primary antibody was pre-absorbed with the antigenic peptide (data not shown). Strong expression of pendrin was observed not only in outer sulcus epithelial cells, as predicted from in situ hybridization data, but also in root cells, in apical membranes of spiral prominence surface epithelial cells and in apical membranes of spindle-shaped cells that are part of stria vascularis (Fig. 1a,1b,1c). The presence of pendrin in spindle-shaped cells suggests that these cells secrete HCO3 - into endolymph. Pendrin-mediated HCO3 - transport has previously been shown in the kidney [9]. HCO3 - in the cochlea may be generated from CO2 by carbonic anhydrase located in strial intermediate cells [18,19]. CO2 may be supplied by the metabolically highly active stria marginal cells. It is conceivable that pendrin dysfunction interrupts HCO3 - secretion and leads to an accumulation of HCO3 - in stria vascularis. Preliminary data (Wangemann et al., unpublished) support a role for pendrin in HCO3 - secretion into endolymph.\nFigure 1 Protein localization of pendrin, KCNQ1, ZO-1 and F actin in cochlea and vestibular labyrinth of Slc26a4+/+ and Slc26a4-/- mice. a: Overview of cochlea; bar = 100 μm. b-f: Detail of cochlear lateral wall; bar = 10 μm. g: Detail of utricle; bar = 10 μm. h-i: Detail of ampulla; bar = 10 μm. RM, Reissner's membrane; SC, spindle-shaped cells, SMC, strial marginal cells; SV, stria vascularis; SL, spiral ligament; LIM, spiral limbus. BC, basal cells; SP, spiral prominence epithelial cells; RC, root cells; OS, outer sulcus epithelial cells; VHC, vestibular hair cells; VTC, vestibular transitional cells; VDC, vestibular dark cells; arrows, basal cells at the top and bottom of stria vascularis form tight junctions with surface epithelial cells. The extent of pendrin expression in spiral prominence cells and stria vascularis was determined by labeling KCNQ1, a K+ channel that is expressed in strial marginal cells, and ZO-1, a tight junction protein that labels basal cells and thereby delineates the boundaries of stria vascularis. Dual labeling experiments demonstrated that pendrin is expressed in spindle-shaped cells, which are surface epithelial cells in stria vascularis adjacent to strial marginal cells near the borders of both the spiral prominence and Reissner's membrane (Fig. 1c).\nIn situ hybridization in the vestibular labyrinth suggested that pendrin mRNA is expressed in non-sensory cells [8]. Using confocal immunocytochemistry on cryosections, we observed strong expression of the pendrin protein in the apical membrane of vestibular transitional cells in the utricle and ampullae (Fig. 1g,1h,1i). Dual labeling with KCNQ1 demonstrated that pendrin expression was clearly limited to vestibular transitional cells and did not extend to other non-sensory cells such as vestibular dark cells, which were clearly identified by the expression of KCNQ1 and KCNE1 in their apical membranes.\nThe onset of pendrin expression during development of the mouse inner ear has been determined to be embryonic day (ED) 13 [14]. Morphologically detectable differences in the inner ears of Slc26a4+/+ and Slc26a4-/- mice become evident as early as ED 15, when Slc26a4-/- mice start to develop an enlarged endolymphatic space that persists into adulthood [14]. Interestingly, sensory hair cells in the cochlea appear normal until postnatal day (PD) 7 but show clear evidence of degeneration by PD 15 [14]. These observations suggest that the cochlear environment supports the survival of sensory hair cells in spite of the enlargement of the endolymphatic duct. A normal endolymphatic K+ concentration, which is critical for hair cell survival [20], is established at PD 3 [21] and may persist in Slc26a4-/- at least until PD 7. The time period between PD 7 and 15 is the time when the endocochlear potential develops at the onset of hearing [22]. We hypothesized that a lack of a normal endocochlear potential or an alteration of the endolymphatic K+ concentration could account for deafness in Slc26a4-/- mice. Measurements revealed that the endocochlear potential was absent but that the endolymphatic K+ concentration was normal in adult Slc26a4-/- (Fig. 2a). No significant differences between Slc26a4+/+ and Slc26a4-/- mice were found in perilymphatic (Fig. 2a) or plasma K+ concentrations (Slc26a4+/+, 4.9 ± 0.3 mM, n = 6; Slc26a4-/-, 5.1 ± 0.3 mM, n = 6). These observations suggest that a primary event leading to deafness in Slc26a4-/- mice, and potentially in patients suffering from Pendred syndrome, is the loss of the endocochlear potential. Degeneration of hair cells is probably a response to the loss of the endocochlear potential.\nFigure 2 Potential, K+ concentrations and pigmentation of stria vascularis in Slc26a4+/+ and Slc26a4-/- mice. a: Endocochlear potential and K+ concentrations in endolymph and perilymph at the apex (A) and base (B) of the cochlea. Numbers adjacent to symbols denote number of measurements. b-d: Pigmentation of stria vascularis in Slc26a4+/+ and Slc26a4-/- mice. b: View of stria vascularis through the bony capsule of the cochlea. OW, oval window, RW, round window; arrows, stria vascularis. c-d: Whole-mounts of stria vascularis isolated from age-matched mice. c: Laser-scanning images, bar = 10 μm, d: Quantification of pigmentation based on optical density. The endocochlear potential is generated by stria vascularis in the lateral wall of the cochlea [17,23]. The potential is generated across the basal cell barrier of stria vascularis by the K+ channel KCNJ10 located in intermediate cells [24], which are connected to basal cells by a high density of gap junctions [25]. Marginal cells of stria vascularis, which form the barrier toward endolymph, transport K+ from the intrastrial space into endolymph and keep the K+ concentration low adjacent to the KCNJ10 K+ channel [26]. To determine the cause of the loss of the endocochlear potential in Slc26a4-/- mice, we first determined whether intermediate cells are present in stria vascularis, since a loss of intermediate cells is known to lead to a loss of the endocochlear potential [27,28]. Intermediate cells of stria vascularis were visualized by their pigmentation. Pigmentation was present in stria vascularis of Slc26a4-/- mice (Fig. 2b), which suggests that intermediate cells are present. Interestingly, pigmentation of stria vascularis was much stronger in Slc26a4-/- than in Slc26a4+/+ mice.\nTo determine in greater detail the cause of the loss of the endocochlear potential in Slc26a4-/- mice, we isolated total RNA from stria vascularis and spiral ganglia of young (1–4 month) Slc26a4+/+ and both young and old (~12 month) Slc26a4-/- mice, assessed amounts of isolated tissues by quantification of 18S rRNA, and quantified the expression of KCNJ10 mRNA. Quantities of stria vascularis isolated from these different mice were similar, since no significant differences were found in the numbers of 18S rRNA molecules (log(rRNA) = 9.46 ± 0.08, n = 17, pooled data). In contrast, quantities of spiral ganglia isolated from young and old Slc26a4-/- mice (log(rRNA) = 9.04 ± 0.18, n = 4 and 9.29 ± 0.15, n = 6) were significantly smaller than in Slc26a4+/+ mice (log(rRNA) = 9.48 ± 0.19, n = 7), consistent with morphometric data (see below). Expression of KCNJ10 mRNA was normal in stria vascularis and spiral ganglia of young Slc26a4-/- mice but significantly reduced in old Slc26a4-/- mice (Fig. 3). Quantifications of KCNQ1 and KCNQ4 mRNA were used to assess possible cross-contamination between the stria vascularis and spiral ganglia preparations based on the assumptions that (1) KCNQ1 is expressed in cells of the stria vascularis but not the spiral ganglia preparation and (2) KCNQ4 is expressed in cells of the spiral ganglia but not the stria vascularis preparation. The number of KCNQ1 mRNA molecules in stria vascularis was 24-fold greater than in spiral ganglia, and the number of KCNQ4 mRNA molecules in spiral ganglia was 5-fold greater than in stria vascularis. These observations validate our measurements of KCNJ10 and KCNQ1 by demonstrating that the microdissected preparations of stria vascularis and spiral ganglia were 98% and 78% pure, respectively.\nFigure 3 Quantification of KCNJ10 and KCNQ1 mRNA expression in stria vascularis and spiral ganglia of Slc26a4+/+ and Slc26a4-/- mice. a: Electropherogram of total RNA isolated from stria vascularis microdissected from one mouse. The amount of total RNA was obtained from the total integral (shaded) and the amount of 18S rRNA was obtained from the integral of the 18S peak. Sharp peaks representing 18S and 28S rRNA demonstrate the high quality of RNA. Insert: Genotype of Slc26a4-/- mice was verified by the observation of one or few very large rhomboedric otoconia in the utricular macula (arrow). A, crista ampullaris; U, utricular macula. Scale bar: 100 μm. b: Example of real-time RT-PCR data used for quantification of 18S, KCNJ10, KCNQ1 and KCNQ4. Known quantities of 18S rRNA were used to calibrate the threshold. SV, stria vascularis; SG, spiral ganglia. c: Quantification of KCNJ10 and KCNQ1 mRNA in young Slc26a4+/+ and young and old Slc26a4-/- mice. The presence of KCNJ10 mRNA in stria vascularis of Slc26a4-/- mice supports the finding that intermediate cells are present. Expression of the KCNJ10 protein was assessed in young Slc26a4-/- mice by confocal immunocytochemistry. Interestingly, expression of the KCNJ10 protein was absent in stria vascularis but normal in spiral ganglia (Fig. 4). The absence of the KCNJ10 K+ channel in stria vascularis is sufficient to explain the loss of the endocochlear potential [17].\nFigure 4 Protein localization of KCNJ10 in the cochlea of Slc26a4+/+ and Slc26a4-/- mice. a: Overview of cochlea; bar = 100 μm. Compare to Fig. 1a to note the enlarged scala media and the distended Reissner's membrane. b-c: Detail of lateral wall and spiral ganglia (insert); main bar: 10 μm, insert: 5 μm. Expression of KCNJ10 in Slc26a4-/- mice was absent in stria vascularis but unchanged in spiral ganglion cells. RM, Reissner's membrane, SV, stria vascularis; SP, spiral prominence; SL, spiral ligament; LIM, spiral limbus; SG, spiral ganglion. Histological evaluation of cryosections revealed an enlargement of scala media with a large bulging of Reissner's membrane and an apparent degeneration of the organ of Corti, as described earlier [14]. Tissue height of stria vascularis was normal (Fig. 5), consistent with the similar numbers of 18S rRNA molecules in isolated preparations (see above). The absence of a change in tissue height is consistent with the presence of intermediate cells [28]. Further, we observed an apparent loss of tissue masses in areas that are normally occupied primarily by type I and II fibrocytes. Spiral prominence in Slc26a4-/- mice was less prominent, spiral ligament thinner and spiral limbus flatter (Fig. 5). The observation that tissue masses were lost in the spiral limbus region is consistent with the finding of a reduced number of 18S rRNA molecules in the spiral ganglia preparation (see above). In addition, we observed an apparent degeneration of stria vascularis, including an increase in pigmentation and an irregular pattern of the tight junctions of marginal cells (Fig. 2c, 6,7). Tight junctions were visualized by F-actin expression. Marginal cells appeared to form a continuous layer.\nFigure 5 Morphometric analysis of cochlear tissue masses in Slc26a4+/+ and Slc26a4-/- mice. a: locations of measurements. Thickness of stria vascularis (SV) was obtained as average of three distance measurements perpendicular to the surface of marginal cells. Thickness of spiral prominence (SP) was measured perpendicular to a tangential line (dashed) that connects the surface of the outer sulcus (OS) with the basal layer of stria vascularis. Thickness of spiral ligament (SL) was measured perpendicular to the tangential line as distance between the surface of spiral prominence and the interface between spiral ligament and bone (B). Thickness of spiral limbus (LIM) was obtained perpendicular to the surface of the bone as a tangential line that touches the inner sulcus (IS) and reaches from the surface of the spiral limbus to the interface between spiral limbus connective tissue and bone. b: Summary. Data from 7–8 animals contributed to each column.\nFigure 6 Analysis of marginal and basal cell barriers by in Slc26a4-/- mice. Tight junctions were visualized by F actin. Whole-mounts of stria vascularis were viewed either from the basal cell side (a-f) or from the marginal cell side (g-l). Bright field images verify that the same area was viewed from either side (b and h). Colored bright field images were mixed with images of F actin staining to indicate the position of pigment granules (d, j, f and l). Focus was varied to either visualize the marginal cell barrier (SMC, c-d and i-j) or the basal cell barrier (BC, e-f and k-l). Both the marginal cell (e-f) and the basal cell barrier (i-f) appeared to be intact. It was critical for this finding that pigmentation did not block the path of the laser. Blockage of the laser by pigmentation produces the untrue impression of a discontinuous marginal cell barrier (c-d) or basal cell barrier (k-l). Comparison of images is aided by marking a significant area with a star. Bars = 10 μm.\nFigure 7 Analysis of marginal and basal cell barriers in Slc26a4+/+ and Slc26a4-/- mice. Tight junctions were visualized by F actin in whole-mounts of stria vascularis. Bright field images were taken to evaluate pigmentation (a, d and g). Note the intact marginal cell (b) and basal cell (c) barriers in Slc26a4+/+ mice. Minimal pigmentation of Slc26a4+/+ mice did not compromise F actin localization. Whole-mounts of stria vascularis from Slc26a4-/- mice were viewed either from the basal cell side (e-f) or from the marginal cell side (h-i). Bright field images verify that the same area was viewed from either side (d and g). Focus was varied to either visualize the marginal cell barrier (SMC, b,e and h) or the basal cell barrier (BC, c,f and i). Both the basal cell (f) and the marginal cell (h) barriers appeared to be intact. Blockage of the laser by pigmentation produces the untrue impression of 'holes' in the marginal cell barrier (e) or basal cell barrier (i). Comparison of images is aided by marking three significant areas with colored stars. Bars = 10 μm. Pendrin-expressing surface epithelial cells in the spiral prominence region are located in an area where basal cells, which are interconnected by tight junctions, form additional tight junctions with surface epithelial cells [29]. A discontinuity of this complex junction in Slc26a4-/- mice would explain the absence of the endocochlear potential. To evaluate the presence of this connection, we determined by confocal immunocytochemistry the expression of ZO-1 and of F-actin, which associate with tight junction complexes. ZO-1 and F-actin expression revealed a continuous layer of basal cells, including a junction of basal cells with surface epithelial cells in Slc26a4-/- mice, as observed in normal mice (Fig. 1c,1d,1e,1f,6,7). These observations make it unlikely that the primary cause of the loss of the endocochlear potential is a compromise in the basal cell barrier.\nThe observation that endolymphatic and perilymphatic K+ concentrations were normal in Slc26a4-/- mice suggests that stria vascularis was able to secrete K+ in spite of the apparent signs of degeneration. The rate of K+ secretion necessary to maintain endolymphatic K+ concentration, however, may be less than necessary in Slc26a4+/+ mice given the reduced numbers of sensory hair cells, which provide a major pathway for K+ exit from endolymph [30,31]. In order to substantiate the view that stria vascularis in Slc26a4-/- secretes K+, we measured the magnitude of the bumetanide-sensitive current exiting stria vascularis across the apical membrane of strial marginal cells and determined the expression of the proteins KCNQ1, KCNE1 and SLC12A2, which are essential for K+ secretion [20,32,33], and of GJB2 (Cx26), which is thought to contribute to K+ cycling [23]. K+ secretion is known to be sensitive to 10-5 M bumetanide, a loop-diuretic that inhibits the Na+/2Cl-/K+ cotransporter SLC12A2 [26]. Bumetanide-sensitive currents were found in both Slc26a4+/+ and Slc26a4-/- mice although the magnitude of the current was significantly smaller in Slc26a4-/- mice (22 ± 6 μA/cm2, n = 4 versus 14 ± 2 μA/cm2, n = 4). KCNQ1 and KCNE1, subunits of the secretory K+ channel, were co-localized in the apical membrane of strial marginal cells; the Na+/2Cl-/K+ cotransporter SLC12A2, which is located in the basolateral membrane of strial marginal cells, was found in stria vascularis; and the gap junction protein GJB2 was found in spiral ligament of Slc26a4+/+ and Slc26a4-/- mice (Fig. 8). Co-localization of KCNQ1 and KCNE1 proteins was also observed in vestibular dark cells (Fig. 1i). Expression of KCNQ1 protein in stria vascularis of Slc26a4-/- mice is consistent with the finding of KCNQ1 mRNA expression (Fig. 3). These observations make it unlikely that the primary cause of the loss of the endocochlear potential is a compromise of K+ secretion by strial marginal cells or a compromise of gap junction mediated K+ cycling.\nFigure 8 Protein localization of KCNQ1, KCNE1, SLC12A2 and GJB2 in the cochlear lateral wall of Slc26a4+/+ and Slc26a4-/- mice. a-f: bars: 10 μm. SMC, strial marginal cells; SV, stria vascularis; BC, basal cells; SL, spiral ligament."}

{"project":"2_test","denotations":[{"id":"15320950-10449762-12070959","span":{"begin":212,"end":213},"obj":"10449762"},{"id":"15320950-10650967-12070960","span":{"begin":419,"end":420},"obj":"10650967"},{"id":"15320950-11274445-12070961","span":{"begin":1031,"end":1032},"obj":"11274445"},{"id":"15320950-8911971-12070962","span":{"begin":1143,"end":1145},"obj":"8911971"},{"id":"15320950-6424489-12070963","span":{"begin":1146,"end":1148},"obj":"6424489"},{"id":"15320950-10449762-12070964","span":{"begin":2890,"end":2891},"obj":"10449762"},{"id":"15320950-11152663-12070965","span":{"begin":3509,"end":3511},"obj":"11152663"},{"id":"15320950-11152663-12070966","span":{"begin":3739,"end":3741},"obj":"11152663"},{"id":"15320950-11152663-12070967","span":{"begin":3884,"end":3886},"obj":"11152663"},{"id":"15320950-8982171-12070968","span":{"begin":4128,"end":4130},"obj":"8982171"},{"id":"15320950-6970572-12070969","span":{"begin":4157,"end":4159},"obj":"6970572"},{"id":"15320950-8600121-12070970","span":{"begin":4326,"end":4328},"obj":"8600121"},{"id":"15320950-11788352-12070971","span":{"begin":5890,"end":5892},"obj":"11788352"},{"id":"15320950-12031509-12070972","span":{"begin":5893,"end":5895},"obj":"12031509"},{"id":"15320950-10409112-12070973","span":{"begin":6031,"end":6033},"obj":"10409112"},{"id":"15320950-9662649-12070974","span":{"begin":6107,"end":6109},"obj":"9662649"},{"id":"15320950-7642451-12070975","span":{"begin":6313,"end":6315},"obj":"7642451"},{"id":"15320950-2380119-12070976","span":{"begin":6576,"end":6578},"obj":"2380119"},{"id":"15320950-2076537-12070977","span":{"begin":6579,"end":6581},"obj":"2076537"},{"id":"15320950-11788352-12070978","span":{"begin":10104,"end":10106},"obj":"11788352"},{"id":"15320950-11152663-12070979","span":{"begin":10857,"end":10859},"obj":"11152663"},{"id":"15320950-2076537-12070980","span":{"begin":11109,"end":11111},"obj":"2076537"},{"id":"15320950-7559175-12070981","span":{"begin":15107,"end":15109},"obj":"7559175"},{"id":"15320950-2778743-12070982","span":{"begin":16204,"end":16206},"obj":"2778743"},{"id":"15320950-2393707-12070983","span":{"begin":16207,"end":16209},"obj":"2393707"},{"id":"15320950-8982171-12070984","span":{"begin":16544,"end":16546},"obj":"8982171"},{"id":"15320950-11226272-12070985","span":{"begin":16547,"end":16549},"obj":"11226272"},{"id":"15320950-10401008-12070986","span":{"begin":16550,"end":16552},"obj":"10401008"},{"id":"15320950-12031509-12070987","span":{"begin":16621,"end":16623},"obj":"12031509"},{"id":"15320950-7642451-12070988","span":{"begin":16755,"end":16757},"obj":"7642451"}],"text":"Results and Discussion\nIn situ hybridization in the cochlea has suggested that pendrin mRNA is expressed in cells that reside immediately beneath the spiral prominence on the lateral wall of the external sulcus [8]. To determine the location of pendrin protein expression, we performed confocal immunocytochemistry on cryosections prepared from temporal bones of normal (Slc26a4+/+) mice using an established antibody [3]. Staining was absent when the primary antibody was pre-absorbed with the antigenic peptide (data not shown). Strong expression of pendrin was observed not only in outer sulcus epithelial cells, as predicted from in situ hybridization data, but also in root cells, in apical membranes of spiral prominence surface epithelial cells and in apical membranes of spindle-shaped cells that are part of stria vascularis (Fig. 1a,1b,1c). The presence of pendrin in spindle-shaped cells suggests that these cells secrete HCO3 - into endolymph. Pendrin-mediated HCO3 - transport has previously been shown in the kidney [9]. HCO3 - in the cochlea may be generated from CO2 by carbonic anhydrase located in strial intermediate cells [18,19]. CO2 may be supplied by the metabolically highly active stria marginal cells. It is conceivable that pendrin dysfunction interrupts HCO3 - secretion and leads to an accumulation of HCO3 - in stria vascularis. Preliminary data (Wangemann et al., unpublished) support a role for pendrin in HCO3 - secretion into endolymph.\nFigure 1 Protein localization of pendrin, KCNQ1, ZO-1 and F actin in cochlea and vestibular labyrinth of Slc26a4+/+ and Slc26a4-/- mice. a: Overview of cochlea; bar = 100 μm. b-f: Detail of cochlear lateral wall; bar = 10 μm. g: Detail of utricle; bar = 10 μm. h-i: Detail of ampulla; bar = 10 μm. RM, Reissner's membrane; SC, spindle-shaped cells, SMC, strial marginal cells; SV, stria vascularis; SL, spiral ligament; LIM, spiral limbus. BC, basal cells; SP, spiral prominence epithelial cells; RC, root cells; OS, outer sulcus epithelial cells; VHC, vestibular hair cells; VTC, vestibular transitional cells; VDC, vestibular dark cells; arrows, basal cells at the top and bottom of stria vascularis form tight junctions with surface epithelial cells. The extent of pendrin expression in spiral prominence cells and stria vascularis was determined by labeling KCNQ1, a K+ channel that is expressed in strial marginal cells, and ZO-1, a tight junction protein that labels basal cells and thereby delineates the boundaries of stria vascularis. Dual labeling experiments demonstrated that pendrin is expressed in spindle-shaped cells, which are surface epithelial cells in stria vascularis adjacent to strial marginal cells near the borders of both the spiral prominence and Reissner's membrane (Fig. 1c).\nIn situ hybridization in the vestibular labyrinth suggested that pendrin mRNA is expressed in non-sensory cells [8]. Using confocal immunocytochemistry on cryosections, we observed strong expression of the pendrin protein in the apical membrane of vestibular transitional cells in the utricle and ampullae (Fig. 1g,1h,1i). Dual labeling with KCNQ1 demonstrated that pendrin expression was clearly limited to vestibular transitional cells and did not extend to other non-sensory cells such as vestibular dark cells, which were clearly identified by the expression of KCNQ1 and KCNE1 in their apical membranes.\nThe onset of pendrin expression during development of the mouse inner ear has been determined to be embryonic day (ED) 13 [14]. Morphologically detectable differences in the inner ears of Slc26a4+/+ and Slc26a4-/- mice become evident as early as ED 15, when Slc26a4-/- mice start to develop an enlarged endolymphatic space that persists into adulthood [14]. Interestingly, sensory hair cells in the cochlea appear normal until postnatal day (PD) 7 but show clear evidence of degeneration by PD 15 [14]. These observations suggest that the cochlear environment supports the survival of sensory hair cells in spite of the enlargement of the endolymphatic duct. A normal endolymphatic K+ concentration, which is critical for hair cell survival [20], is established at PD 3 [21] and may persist in Slc26a4-/- at least until PD 7. The time period between PD 7 and 15 is the time when the endocochlear potential develops at the onset of hearing [22]. We hypothesized that a lack of a normal endocochlear potential or an alteration of the endolymphatic K+ concentration could account for deafness in Slc26a4-/- mice. Measurements revealed that the endocochlear potential was absent but that the endolymphatic K+ concentration was normal in adult Slc26a4-/- (Fig. 2a). No significant differences between Slc26a4+/+ and Slc26a4-/- mice were found in perilymphatic (Fig. 2a) or plasma K+ concentrations (Slc26a4+/+, 4.9 ± 0.3 mM, n = 6; Slc26a4-/-, 5.1 ± 0.3 mM, n = 6). These observations suggest that a primary event leading to deafness in Slc26a4-/- mice, and potentially in patients suffering from Pendred syndrome, is the loss of the endocochlear potential. Degeneration of hair cells is probably a response to the loss of the endocochlear potential.\nFigure 2 Potential, K+ concentrations and pigmentation of stria vascularis in Slc26a4+/+ and Slc26a4-/- mice. a: Endocochlear potential and K+ concentrations in endolymph and perilymph at the apex (A) and base (B) of the cochlea. Numbers adjacent to symbols denote number of measurements. b-d: Pigmentation of stria vascularis in Slc26a4+/+ and Slc26a4-/- mice. b: View of stria vascularis through the bony capsule of the cochlea. OW, oval window, RW, round window; arrows, stria vascularis. c-d: Whole-mounts of stria vascularis isolated from age-matched mice. c: Laser-scanning images, bar = 10 μm, d: Quantification of pigmentation based on optical density. The endocochlear potential is generated by stria vascularis in the lateral wall of the cochlea [17,23]. The potential is generated across the basal cell barrier of stria vascularis by the K+ channel KCNJ10 located in intermediate cells [24], which are connected to basal cells by a high density of gap junctions [25]. Marginal cells of stria vascularis, which form the barrier toward endolymph, transport K+ from the intrastrial space into endolymph and keep the K+ concentration low adjacent to the KCNJ10 K+ channel [26]. To determine the cause of the loss of the endocochlear potential in Slc26a4-/- mice, we first determined whether intermediate cells are present in stria vascularis, since a loss of intermediate cells is known to lead to a loss of the endocochlear potential [27,28]. Intermediate cells of stria vascularis were visualized by their pigmentation. Pigmentation was present in stria vascularis of Slc26a4-/- mice (Fig. 2b), which suggests that intermediate cells are present. Interestingly, pigmentation of stria vascularis was much stronger in Slc26a4-/- than in Slc26a4+/+ mice.\nTo determine in greater detail the cause of the loss of the endocochlear potential in Slc26a4-/- mice, we isolated total RNA from stria vascularis and spiral ganglia of young (1–4 month) Slc26a4+/+ and both young and old (~12 month) Slc26a4-/- mice, assessed amounts of isolated tissues by quantification of 18S rRNA, and quantified the expression of KCNJ10 mRNA. Quantities of stria vascularis isolated from these different mice were similar, since no significant differences were found in the numbers of 18S rRNA molecules (log(rRNA) = 9.46 ± 0.08, n = 17, pooled data). In contrast, quantities of spiral ganglia isolated from young and old Slc26a4-/- mice (log(rRNA) = 9.04 ± 0.18, n = 4 and 9.29 ± 0.15, n = 6) were significantly smaller than in Slc26a4+/+ mice (log(rRNA) = 9.48 ± 0.19, n = 7), consistent with morphometric data (see below). Expression of KCNJ10 mRNA was normal in stria vascularis and spiral ganglia of young Slc26a4-/- mice but significantly reduced in old Slc26a4-/- mice (Fig. 3). Quantifications of KCNQ1 and KCNQ4 mRNA were used to assess possible cross-contamination between the stria vascularis and spiral ganglia preparations based on the assumptions that (1) KCNQ1 is expressed in cells of the stria vascularis but not the spiral ganglia preparation and (2) KCNQ4 is expressed in cells of the spiral ganglia but not the stria vascularis preparation. The number of KCNQ1 mRNA molecules in stria vascularis was 24-fold greater than in spiral ganglia, and the number of KCNQ4 mRNA molecules in spiral ganglia was 5-fold greater than in stria vascularis. These observations validate our measurements of KCNJ10 and KCNQ1 by demonstrating that the microdissected preparations of stria vascularis and spiral ganglia were 98% and 78% pure, respectively.\nFigure 3 Quantification of KCNJ10 and KCNQ1 mRNA expression in stria vascularis and spiral ganglia of Slc26a4+/+ and Slc26a4-/- mice. a: Electropherogram of total RNA isolated from stria vascularis microdissected from one mouse. The amount of total RNA was obtained from the total integral (shaded) and the amount of 18S rRNA was obtained from the integral of the 18S peak. Sharp peaks representing 18S and 28S rRNA demonstrate the high quality of RNA. Insert: Genotype of Slc26a4-/- mice was verified by the observation of one or few very large rhomboedric otoconia in the utricular macula (arrow). A, crista ampullaris; U, utricular macula. Scale bar: 100 μm. b: Example of real-time RT-PCR data used for quantification of 18S, KCNJ10, KCNQ1 and KCNQ4. Known quantities of 18S rRNA were used to calibrate the threshold. SV, stria vascularis; SG, spiral ganglia. c: Quantification of KCNJ10 and KCNQ1 mRNA in young Slc26a4+/+ and young and old Slc26a4-/- mice. The presence of KCNJ10 mRNA in stria vascularis of Slc26a4-/- mice supports the finding that intermediate cells are present. Expression of the KCNJ10 protein was assessed in young Slc26a4-/- mice by confocal immunocytochemistry. Interestingly, expression of the KCNJ10 protein was absent in stria vascularis but normal in spiral ganglia (Fig. 4). The absence of the KCNJ10 K+ channel in stria vascularis is sufficient to explain the loss of the endocochlear potential [17].\nFigure 4 Protein localization of KCNJ10 in the cochlea of Slc26a4+/+ and Slc26a4-/- mice. a: Overview of cochlea; bar = 100 μm. Compare to Fig. 1a to note the enlarged scala media and the distended Reissner's membrane. b-c: Detail of lateral wall and spiral ganglia (insert); main bar: 10 μm, insert: 5 μm. Expression of KCNJ10 in Slc26a4-/- mice was absent in stria vascularis but unchanged in spiral ganglion cells. RM, Reissner's membrane, SV, stria vascularis; SP, spiral prominence; SL, spiral ligament; LIM, spiral limbus; SG, spiral ganglion. Histological evaluation of cryosections revealed an enlargement of scala media with a large bulging of Reissner's membrane and an apparent degeneration of the organ of Corti, as described earlier [14]. Tissue height of stria vascularis was normal (Fig. 5), consistent with the similar numbers of 18S rRNA molecules in isolated preparations (see above). The absence of a change in tissue height is consistent with the presence of intermediate cells [28]. Further, we observed an apparent loss of tissue masses in areas that are normally occupied primarily by type I and II fibrocytes. Spiral prominence in Slc26a4-/- mice was less prominent, spiral ligament thinner and spiral limbus flatter (Fig. 5). The observation that tissue masses were lost in the spiral limbus region is consistent with the finding of a reduced number of 18S rRNA molecules in the spiral ganglia preparation (see above). In addition, we observed an apparent degeneration of stria vascularis, including an increase in pigmentation and an irregular pattern of the tight junctions of marginal cells (Fig. 2c, 6,7). Tight junctions were visualized by F-actin expression. Marginal cells appeared to form a continuous layer.\nFigure 5 Morphometric analysis of cochlear tissue masses in Slc26a4+/+ and Slc26a4-/- mice. a: locations of measurements. Thickness of stria vascularis (SV) was obtained as average of three distance measurements perpendicular to the surface of marginal cells. Thickness of spiral prominence (SP) was measured perpendicular to a tangential line (dashed) that connects the surface of the outer sulcus (OS) with the basal layer of stria vascularis. Thickness of spiral ligament (SL) was measured perpendicular to the tangential line as distance between the surface of spiral prominence and the interface between spiral ligament and bone (B). Thickness of spiral limbus (LIM) was obtained perpendicular to the surface of the bone as a tangential line that touches the inner sulcus (IS) and reaches from the surface of the spiral limbus to the interface between spiral limbus connective tissue and bone. b: Summary. Data from 7–8 animals contributed to each column.\nFigure 6 Analysis of marginal and basal cell barriers by in Slc26a4-/- mice. Tight junctions were visualized by F actin. Whole-mounts of stria vascularis were viewed either from the basal cell side (a-f) or from the marginal cell side (g-l). Bright field images verify that the same area was viewed from either side (b and h). Colored bright field images were mixed with images of F actin staining to indicate the position of pigment granules (d, j, f and l). Focus was varied to either visualize the marginal cell barrier (SMC, c-d and i-j) or the basal cell barrier (BC, e-f and k-l). Both the marginal cell (e-f) and the basal cell barrier (i-f) appeared to be intact. It was critical for this finding that pigmentation did not block the path of the laser. Blockage of the laser by pigmentation produces the untrue impression of a discontinuous marginal cell barrier (c-d) or basal cell barrier (k-l). Comparison of images is aided by marking a significant area with a star. Bars = 10 μm.\nFigure 7 Analysis of marginal and basal cell barriers in Slc26a4+/+ and Slc26a4-/- mice. Tight junctions were visualized by F actin in whole-mounts of stria vascularis. Bright field images were taken to evaluate pigmentation (a, d and g). Note the intact marginal cell (b) and basal cell (c) barriers in Slc26a4+/+ mice. Minimal pigmentation of Slc26a4+/+ mice did not compromise F actin localization. Whole-mounts of stria vascularis from Slc26a4-/- mice were viewed either from the basal cell side (e-f) or from the marginal cell side (h-i). Bright field images verify that the same area was viewed from either side (d and g). Focus was varied to either visualize the marginal cell barrier (SMC, b,e and h) or the basal cell barrier (BC, c,f and i). Both the basal cell (f) and the marginal cell (h) barriers appeared to be intact. Blockage of the laser by pigmentation produces the untrue impression of 'holes' in the marginal cell barrier (e) or basal cell barrier (i). Comparison of images is aided by marking three significant areas with colored stars. Bars = 10 μm. Pendrin-expressing surface epithelial cells in the spiral prominence region are located in an area where basal cells, which are interconnected by tight junctions, form additional tight junctions with surface epithelial cells [29]. A discontinuity of this complex junction in Slc26a4-/- mice would explain the absence of the endocochlear potential. To evaluate the presence of this connection, we determined by confocal immunocytochemistry the expression of ZO-1 and of F-actin, which associate with tight junction complexes. ZO-1 and F-actin expression revealed a continuous layer of basal cells, including a junction of basal cells with surface epithelial cells in Slc26a4-/- mice, as observed in normal mice (Fig. 1c,1d,1e,1f,6,7). These observations make it unlikely that the primary cause of the loss of the endocochlear potential is a compromise in the basal cell barrier.\nThe observation that endolymphatic and perilymphatic K+ concentrations were normal in Slc26a4-/- mice suggests that stria vascularis was able to secrete K+ in spite of the apparent signs of degeneration. The rate of K+ secretion necessary to maintain endolymphatic K+ concentration, however, may be less than necessary in Slc26a4+/+ mice given the reduced numbers of sensory hair cells, which provide a major pathway for K+ exit from endolymph [30,31]. In order to substantiate the view that stria vascularis in Slc26a4-/- secretes K+, we measured the magnitude of the bumetanide-sensitive current exiting stria vascularis across the apical membrane of strial marginal cells and determined the expression of the proteins KCNQ1, KCNE1 and SLC12A2, which are essential for K+ secretion [20,32,33], and of GJB2 (Cx26), which is thought to contribute to K+ cycling [23]. K+ secretion is known to be sensitive to 10-5 M bumetanide, a loop-diuretic that inhibits the Na+/2Cl-/K+ cotransporter SLC12A2 [26]. Bumetanide-sensitive currents were found in both Slc26a4+/+ and Slc26a4-/- mice although the magnitude of the current was significantly smaller in Slc26a4-/- mice (22 ± 6 μA/cm2, n = 4 versus 14 ± 2 μA/cm2, n = 4). KCNQ1 and KCNE1, subunits of the secretory K+ channel, were co-localized in the apical membrane of strial marginal cells; the Na+/2Cl-/K+ cotransporter SLC12A2, which is located in the basolateral membrane of strial marginal cells, was found in stria vascularis; and the gap junction protein GJB2 was found in spiral ligament of Slc26a4+/+ and Slc26a4-/- mice (Fig. 8). Co-localization of KCNQ1 and KCNE1 proteins was also observed in vestibular dark cells (Fig. 1i). Expression of KCNQ1 protein in stria vascularis of Slc26a4-/- mice is consistent with the finding of KCNQ1 mRNA expression (Fig. 3). These observations make it unlikely that the primary cause of the loss of the endocochlear potential is a compromise of K+ secretion by strial marginal cells or a compromise of gap junction mediated K+ cycling.\nFigure 8 Protein localization of KCNQ1, KCNE1, SLC12A2 and GJB2 in the cochlear lateral wall of Slc26a4+/+ and Slc26a4-/- mice. a-f: bars: 10 μm. SMC, strial marginal cells; SV, stria vascularis; BC, basal cells; SL, spiral ligament."}