Skip to main content
Top
Published in: Journal of the Association for Research in Otolaryngology 2/2017

01-04-2017 | Research Article

Quantitative Analysis of Aquaporin Expression Levels during the Development and Maturation of the Inner Ear

Authors: Takushi Miyoshi, Taro Yamaguchi, Kiyokazu Ogita, Yasuko Tanaka, Ken-ichi Ishibashi, Hiroaki Ito, Taisuke Kobayashi, Takayuki Nakagawa, Juichi Ito, Koichi Omori, Norio Yamamoto

Published in: Journal of the Association for Research in Otolaryngology | Issue 2/2017

Login to get access

Abstract

Aquaporins (AQPs) are a family of small membrane proteins that transport water molecules across the plasma membrane along the osmotic gradient. Mammals express 13 subtypes of AQPs, including the recently reported “subcellular AQPs”, AQP11 and 12. Each organ expresses specific subsets of AQP subtypes, and in the inner ear, AQPs are essential for the establishment and maintenance of two distinct fluids, endolymph and perilymph. To evaluate the contribution of AQPs during the establishment of inner ear function, we used quantitative reverse transcription polymerase chain reaction to quantify the expression levels of all known AQPs during the entire development and maturation of the inner ear. Using systematic and longitudinal quantification, we found that AQP11 was majorly and constantly expressed in the inner ear, and that the expression levels of several AQPs follow characteristic longitudinal patterns: increasing (Aqp0, 1, and 9), decreasing (Aqp6, 8, and 12), and peak of expression on E18 (Aqp2, 5, and 7). In particular, the expression level of Aqp9 increased by 70-fold during P3–P21. We also performed in situ hybridization of Aqp11, and determined the unique localization of Aqp11 in the outer hair cells. Immunohistochemistry of AQP9 revealed its localization in the supporting cells inside the organ of Corti, and in the root cells. The emergence of AQP9 expression in these cells was during P3–P21, which was coincident with the marked increase of its expression level. Combining these quantification and localization data, we discuss the possible contributions of these AQPs to inner ear function.
Literature
go back to reference Badaut J, Regli L (2004) Distribution and possible roles of aquaporin 9 in the brain. Neuroscience 129:971–981CrossRefPubMed Badaut J, Regli L (2004) Distribution and possible roles of aquaporin 9 in the brain. Neuroscience 129:971–981CrossRefPubMed
go back to reference Badaut J, Petit JM, Brunet JF, Magistretti PJ, Charriaut-Marlangue C, Regli L (2004) Distribution of aquaporin 9 in the adult rat brain: preferential expression in catecholaminergic neurons and in glial cells. Neuroscience 128:27–38CrossRefPubMed Badaut J, Petit JM, Brunet JF, Magistretti PJ, Charriaut-Marlangue C, Regli L (2004) Distribution of aquaporin 9 in the adult rat brain: preferential expression in catecholaminergic neurons and in glial cells. Neuroscience 128:27–38CrossRefPubMed
go back to reference Calamita G, Ferri D, Gena P, Liquori GE, Cavalier A, Thomas D, Svelto M (2005) The inner mitochondrial membrane has aquaporin-8 water channels and is highly permeable to water. J Biol Chem 280:17149–17153CrossRefPubMed Calamita G, Ferri D, Gena P, Liquori GE, Cavalier A, Thomas D, Svelto M (2005) The inner mitochondrial membrane has aquaporin-8 water channels and is highly permeable to water. J Biol Chem 280:17149–17153CrossRefPubMed
go back to reference Chou CL, Ma T, Yang B, Knepper MA, Verkman AS (1998) Fourfold reduction of water permeability in inner medullary collecting duct of aquaporin-4 knockout mice. Am J Phys 274:C549–C554 Chou CL, Ma T, Yang B, Knepper MA, Verkman AS (1998) Fourfold reduction of water permeability in inner medullary collecting duct of aquaporin-4 knockout mice. Am J Phys 274:C549–C554
go back to reference Dallos P, Harris D (1978) Properties of auditory nerve responses in absence of outer hair cells. J Neurophysiol 41:365–383PubMed Dallos P, Harris D (1978) Properties of auditory nerve responses in absence of outer hair cells. J Neurophysiol 41:365–383PubMed
go back to reference Dallos P, Wu X, Cheatham MA, Gao J, Zheng J, Anderson CT, Jia S, Wang X, Cheng WH, Sengupta S, He DZ, Zuo J (2008) Prestin-based outer hair cell motility is necessary for mammalian cochlear amplification. Neuron 58:333–339CrossRefPubMedPubMedCentral Dallos P, Wu X, Cheatham MA, Gao J, Zheng J, Anderson CT, Jia S, Wang X, Cheng WH, Sengupta S, He DZ, Zuo J (2008) Prestin-based outer hair cell motility is necessary for mammalian cochlear amplification. Neuron 58:333–339CrossRefPubMedPubMedCentral
go back to reference Eckhard A, Gleiser C, Arnold H, Rask-Andersen H, Kumagami H, Muller M, Hirt B, Lowenheim H (2012a) Water channel proteins in the inner ear and their link to hearing impairment and deafness. Mol Asp Med 33:612–637CrossRef Eckhard A, Gleiser C, Arnold H, Rask-Andersen H, Kumagami H, Muller M, Hirt B, Lowenheim H (2012a) Water channel proteins in the inner ear and their link to hearing impairment and deafness. Mol Asp Med 33:612–637CrossRef
go back to reference Eckhard A, Gleiser C, Rask-Andersen H, Arnold H, Liu W, Mack A, Muller M, Lowenheim H, Hirt B (2012b) Co-localisation of K(ir)4.1 and AQP4 in rat and human cochleae reveals a gap in water channel expression at the transduction sites of endocochlear K(+) recycling routes. Cell Tissue Res 350:27–43CrossRefPubMed Eckhard A, Gleiser C, Rask-Andersen H, Arnold H, Liu W, Mack A, Muller M, Lowenheim H, Hirt B (2012b) Co-localisation of K(ir)4.1 and AQP4 in rat and human cochleae reveals a gap in water channel expression at the transduction sites of endocochlear K(+) recycling routes. Cell Tissue Res 350:27–43CrossRefPubMed
go back to reference Ehret G (2005) Infant rodent ultrasounds -- a gate to the understanding of sound communication. Behav Genet 35:19–29CrossRefPubMed Ehret G (2005) Infant rodent ultrasounds -- a gate to the understanding of sound communication. Behav Genet 35:19–29CrossRefPubMed
go back to reference Frank G, Hemmert W, Gummer AW (1999) Limiting dynamics of highfrequency electromechanical transduction of outer hair cells. Proc Natl Acad Sci 96:4420–4425CrossRefPubMedPubMedCentral Frank G, Hemmert W, Gummer AW (1999) Limiting dynamics of highfrequency electromechanical transduction of outer hair cells. Proc Natl Acad Sci 96:4420–4425CrossRefPubMedPubMedCentral
go back to reference Hashem MA (2010) Biochemical and expression studies on aquaporin 9 (AQP9) in wild and AQP9 knockout mice. Vet Arhiv 80:93–112 Hashem MA (2010) Biochemical and expression studies on aquaporin 9 (AQP9) in wild and AQP9 knockout mice. Vet Arhiv 80:93–112
go back to reference Hirt B, Penkova ZH, Eckhard A, Liu W, Rask-Andersen H, Muller M, Lowenheim H (2010) The subcellular distribution of aquaporin 5 in the cochlea reveals a water shunt at the perilymph-endolymph barrier. Neuroscience 168:957–970CrossRefPubMed Hirt B, Penkova ZH, Eckhard A, Liu W, Rask-Andersen H, Muller M, Lowenheim H (2010) The subcellular distribution of aquaporin 5 in the cochlea reveals a water shunt at the perilymph-endolymph barrier. Neuroscience 168:957–970CrossRefPubMed
go back to reference Huang D, Chen P, Chen S, Nagura M, Lim DJ, Lin X (2002) Expression patterns of aquaporins in the inner ear: evidence for concerted actions of multiple types of aquaporins to facilitate water transport in the cochlea. Hear Res 165:85–95CrossRefPubMed Huang D, Chen P, Chen S, Nagura M, Lim DJ, Lin X (2002) Expression patterns of aquaporins in the inner ear: evidence for concerted actions of multiple types of aquaporins to facilitate water transport in the cochlea. Hear Res 165:85–95CrossRefPubMed
go back to reference Huang G, Santos-Sacchi J (1993) Mapping the distribution of the outer hair cell motility voltage sensor by electrical amputation. Biophys J 65:2228–2236CrossRefPubMedPubMedCentral Huang G, Santos-Sacchi J (1993) Mapping the distribution of the outer hair cell motility voltage sensor by electrical amputation. Biophys J 65:2228–2236CrossRefPubMedPubMedCentral
go back to reference Ikeda M, Beitz E, Kozono D, Guggino WB, Agre P, Yasui M (2002) Characterization of aquaporin-6 as a nitrate channel in mammalian cells. Requirement of pore-lining residue threonine 63. J Biol Chem 277:39873–39879CrossRefPubMed Ikeda M, Beitz E, Kozono D, Guggino WB, Agre P, Yasui M (2002) Characterization of aquaporin-6 as a nitrate channel in mammalian cells. Requirement of pore-lining residue threonine 63. J Biol Chem 277:39873–39879CrossRefPubMed
go back to reference Ishibashi K, Hara S, Kondo S (2009) Aquaporin water channels in mammals. Clin Exp Nephrol 13:107–117CrossRefPubMed Ishibashi K, Hara S, Kondo S (2009) Aquaporin water channels in mammals. Clin Exp Nephrol 13:107–117CrossRefPubMed
go back to reference Ishibashi K, Kuwahara M, Kageyama Y, Sasaki S, Suzuki M, Imai M (2000) Molecular cloning of a new aquaporin superfamily in mammals. In: Hohmann S, Nielsen S (eds) Molecular biology and physiology of water and solute transport. Kluwer Academic/Plenum, New York, pp. 123–126CrossRef Ishibashi K, Kuwahara M, Kageyama Y, Sasaki S, Suzuki M, Imai M (2000) Molecular cloning of a new aquaporin superfamily in mammals. In: Hohmann S, Nielsen S (eds) Molecular biology and physiology of water and solute transport. Kluwer Academic/Plenum, New York, pp. 123–126CrossRef
go back to reference Itoh T, Rai T, Kuwahara M, Ko SB, Uchida S, Sasaki S, Ishibashi K (2005) Identification of a novel aquaporin, AQP12, expressed in pancreatic acinar cells. Biochem Biophys Res Commun 330:832–838CrossRefPubMed Itoh T, Rai T, Kuwahara M, Ko SB, Uchida S, Sasaki S, Ishibashi K (2005) Identification of a novel aquaporin, AQP12, expressed in pancreatic acinar cells. Biochem Biophys Res Commun 330:832–838CrossRefPubMed
go back to reference Kelley MW (2005) Development of the inner ear Kelley MW (2005) Development of the inner ear
go back to reference Kim HM, Wangemann P (2010) Failure of fluid absorption in the endolymphatic sac initiates cochlear enlargement that leads to deafness in mice lacking pendrin expression. PLoS One 5:e14041CrossRefPubMedPubMedCentral Kim HM, Wangemann P (2010) Failure of fluid absorption in the endolymphatic sac initiates cochlear enlargement that leads to deafness in mice lacking pendrin expression. PLoS One 5:e14041CrossRefPubMedPubMedCentral
go back to reference Li J, Verkman AS (2001) Impaired hearing in mice lacking aquaporin-4 water channels. J Biol Chem 276:31233–31237CrossRefPubMed Li J, Verkman AS (2001) Impaired hearing in mice lacking aquaporin-4 water channels. J Biol Chem 276:31233–31237CrossRefPubMed
go back to reference Li X, Zhou F, Marcus DC, Wangemann P (2013) Endolymphatic Na(+) and K(+) concentrations during cochlear growth and enlargement in mice lacking Slc26a4/pendrin. PLoS One 8:e65977CrossRefPubMedPubMedCentral Li X, Zhou F, Marcus DC, Wangemann P (2013) Endolymphatic Na(+) and K(+) concentrations during cochlear growth and enlargement in mice lacking Slc26a4/pendrin. PLoS One 8:e65977CrossRefPubMedPubMedCentral
go back to reference Liberman MC, Gao JG, He DZZ, Wu XD, Jia SP, Zuo J (2002) Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier. Nature 419:300–304CrossRefPubMed Liberman MC, Gao JG, He DZZ, Wu XD, Jia SP, Zuo J (2002) Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier. Nature 419:300–304CrossRefPubMed
go back to reference Liu H, Pecka JL, Zhang Q, Soukup GA, Beisel KW, He DZ (2014) Characterization of transcriptomes of cochlear inner and outer hair cells. J Neurosci Off J Soc Neurosci 34:11085–11095CrossRef Liu H, Pecka JL, Zhang Q, Soukup GA, Beisel KW, He DZ (2014) Characterization of transcriptomes of cochlear inner and outer hair cells. J Neurosci Off J Soc Neurosci 34:11085–11095CrossRef
go back to reference Lopez IA, Ishiyama G, Lee M, Baloh RW, Ishiyama A (2007) Immunohistochemical localization of aquaporins in the human inner ear. Cell Tissue Res 328:453–460CrossRefPubMed Lopez IA, Ishiyama G, Lee M, Baloh RW, Ishiyama A (2007) Immunohistochemical localization of aquaporins in the human inner ear. Cell Tissue Res 328:453–460CrossRefPubMed
go back to reference Ma T, Yang B, Gillespie A, Carlson EJ, Epstein CJ, Verkman AS (1998) Severely impaired urinary concentrating ability in transgenic mice lacking aquaporin-1 water channels. J Biol Chem 273:4296–4299CrossRefPubMed Ma T, Yang B, Gillespie A, Carlson EJ, Epstein CJ, Verkman AS (1998) Severely impaired urinary concentrating ability in transgenic mice lacking aquaporin-1 water channels. J Biol Chem 273:4296–4299CrossRefPubMed
go back to reference Ma T, Song Y, Yang B, Gillespie A, Carlson EJ, Epstein CJ, Verkman AS (2000) Nephrogenic diabetes insipidus in mice lacking aquaporin-3 water channels. Proc Natl Acad Sci U S A 97:4386–4391CrossRefPubMedPubMedCentral Ma T, Song Y, Yang B, Gillespie A, Carlson EJ, Epstein CJ, Verkman AS (2000) Nephrogenic diabetes insipidus in mice lacking aquaporin-3 water channels. Proc Natl Acad Sci U S A 97:4386–4391CrossRefPubMedPubMedCentral
go back to reference Merves M, Krane CM, Dou H, Greinwald JH, Menon AG, Choo D (2003) Expression of aquaporin 1 and 5 in the developing mouse inner ear and audiovestibular assessment of an Aqp5 null mutant. J Assoc Res Otolaryngol 4:264–275CrossRefPubMedPubMedCentral Merves M, Krane CM, Dou H, Greinwald JH, Menon AG, Choo D (2003) Expression of aquaporin 1 and 5 in the developing mouse inner ear and audiovestibular assessment of an Aqp5 null mutant. J Assoc Res Otolaryngol 4:264–275CrossRefPubMedPubMedCentral
go back to reference Meyer J, Mack AF, Gummer AW (2001) Pronounced infracuticular endocytosis in mammalian outer hair cells. Hear Res 161:10–22CrossRefPubMed Meyer J, Mack AF, Gummer AW (2001) Pronounced infracuticular endocytosis in mammalian outer hair cells. Hear Res 161:10–22CrossRefPubMed
go back to reference Mhatre AN, Steinbach S, Hribar K, Hoque AT, Lalwani AK (1999) Identification of aquaporin 5 (AQP5) within the cochlea: cDNA cloning and in situ localization. Biochem Biophys Res Commun 264:157–162CrossRefPubMed Mhatre AN, Steinbach S, Hribar K, Hoque AT, Lalwani AK (1999) Identification of aquaporin 5 (AQP5) within the cochlea: cDNA cloning and in situ localization. Biochem Biophys Res Commun 264:157–162CrossRefPubMed
go back to reference Mhatre AN, Jero J, Chiappini I, Bolasco G, Barbara M, Lalwani AK (2002) Aquaporin-2 expression in the mammalian cochlea and investigation of its role in Meniere’s disease. Hear Res 170:59–69CrossRefPubMed Mhatre AN, Jero J, Chiappini I, Bolasco G, Barbara M, Lalwani AK (2002) Aquaporin-2 expression in the mammalian cochlea and investigation of its role in Meniere’s disease. Hear Res 170:59–69CrossRefPubMed
go back to reference Morinaga T, Nakakoshi M, Hirao A, Imai M, Ishibashi K (2002) Mouse aquaporin 10 gene (AQP10) is a pseudogene. Biochem Biophys Res Commun 294:630–634CrossRefPubMed Morinaga T, Nakakoshi M, Hirao A, Imai M, Ishibashi K (2002) Mouse aquaporin 10 gene (AQP10) is a pseudogene. Biochem Biophys Res Commun 294:630–634CrossRefPubMed
go back to reference Morishita Y, Matsuzaki T, Hara-chikuma M, Andoo A, Shimono M, Matsuki A, Kobayashi K, Ikeda M, Yamamoto T, Verkman A, Kusano E, Ookawara S, Takata K, Sasaki S, Ishibashi K (2005) Disruption of aquaporin-11 produces polycystic kidneys following vacuolization of the proximal tubule. Mol Cell Biol 25:7770–7779CrossRefPubMedPubMedCentral Morishita Y, Matsuzaki T, Hara-chikuma M, Andoo A, Shimono M, Matsuki A, Kobayashi K, Ikeda M, Yamamoto T, Verkman A, Kusano E, Ookawara S, Takata K, Sasaki S, Ishibashi K (2005) Disruption of aquaporin-11 produces polycystic kidneys following vacuolization of the proximal tubule. Mol Cell Biol 25:7770–7779CrossRefPubMedPubMedCentral
go back to reference Mulders SM, Knoers NV, Van Lieburg AF, Monnens LA, Leumann E, Wuhl E, Schober E, Rijss JP, Van Os CH, Deen PM (1997) New mutations in the AQP2 gene in nephrogenic diabetes insipidus resulting in functional but misrouted water channels. Journal of the American Society of Nephrology: JASN 8:242–248PubMed Mulders SM, Knoers NV, Van Lieburg AF, Monnens LA, Leumann E, Wuhl E, Schober E, Rijss JP, Van Os CH, Deen PM (1997) New mutations in the AQP2 gene in nephrogenic diabetes insipidus resulting in functional but misrouted water channels. Journal of the American Society of Nephrology: JASN 8:242–248PubMed
go back to reference Nishimura M, Kakigi A, Takeda T, Takeda S, Doi K (2009) Expression of aquaporins, vasopressin type 2 receptor, and Na + (−)K+(−)Cl(−) cotransporters in the rat endolymphatic sac. Acta Otolaryngol 129:812–818CrossRefPubMed Nishimura M, Kakigi A, Takeda T, Takeda S, Doi K (2009) Expression of aquaporins, vasopressin type 2 receptor, and Na + (−)K+(−)Cl(−) cotransporters in the rat endolymphatic sac. Acta Otolaryngol 129:812–818CrossRefPubMed
go back to reference Nishioka R, Takeda T, Kakigi A, Okada T, Takebayashi S, Taguchi D, Nishimura M, Hyodo M (2010) Expression of aquaporins and vasopressin type 2 receptor in the stria vascularis of the cochlea. Hear Res 260:11–19CrossRefPubMed Nishioka R, Takeda T, Kakigi A, Okada T, Takebayashi S, Taguchi D, Nishimura M, Hyodo M (2010) Expression of aquaporins and vasopressin type 2 receptor in the stria vascularis of the cochlea. Hear Res 260:11–19CrossRefPubMed
go back to reference Oshio K, Binder DK, Yang B, Schecter S, Verkman AS, Manley GT (2004) Expression of aquaporin water channels in mouse spinal cord. Neuroscience 127:685–693CrossRefPubMed Oshio K, Binder DK, Yang B, Schecter S, Verkman AS, Manley GT (2004) Expression of aquaporin water channels in mouse spinal cord. Neuroscience 127:685–693CrossRefPubMed
go back to reference Preston GM, Carroll TP, Guggino WB, Agre P (1992) Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256:385–387CrossRefPubMed Preston GM, Carroll TP, Guggino WB, Agre P (1992) Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256:385–387CrossRefPubMed
go back to reference Rojek A, Fuchtbauer EM, Fuchtbauer A, Jelen S, Malmendal A, Fenton RA, Nielsen S (2013) Liver-specific aquaporin 11 knockout mice show rapid vacuolization of the rough endoplasmic reticulum in periportal hepatocytes after amino acid feeding. Am J Physiol Gastrointest Liver Physiol 304:G501–G515CrossRefPubMed Rojek A, Fuchtbauer EM, Fuchtbauer A, Jelen S, Malmendal A, Fenton RA, Nielsen S (2013) Liver-specific aquaporin 11 knockout mice show rapid vacuolization of the rough endoplasmic reticulum in periportal hepatocytes after amino acid feeding. Am J Physiol Gastrointest Liver Physiol 304:G501–G515CrossRefPubMed
go back to reference Rojek AM, Skowronski MT, Fuchtbauer EM, Fuchtbauer AC, Fenton RA, Agre P, Frokiaer J, Nielsen S (2007) Defective glycerol metabolism in aquaporin 9 (AQP9) knockout mice. Proc Natl Acad Sci U S A 104:3609–3614CrossRefPubMedPubMedCentral Rojek AM, Skowronski MT, Fuchtbauer EM, Fuchtbauer AC, Fenton RA, Agre P, Frokiaer J, Nielsen S (2007) Defective glycerol metabolism in aquaporin 9 (AQP9) knockout mice. Proc Natl Acad Sci U S A 104:3609–3614CrossRefPubMedPubMedCentral
go back to reference Shiels A, Bassnett S (1996) Mutations in the founder of the MIP gene family underlie cataract development in the mouse. Nat Genet 12:212–215CrossRefPubMed Shiels A, Bassnett S (1996) Mutations in the founder of the MIP gene family underlie cataract development in the mouse. Nat Genet 12:212–215CrossRefPubMed
go back to reference Stankovic KM, Adams JC, Brown D (1995) Immunolocalization of aquaporin CHIP in the Guinea pig inner ear. Am J Phys 269:C1450–C1456 Stankovic KM, Adams JC, Brown D (1995) Immunolocalization of aquaporin CHIP in the Guinea pig inner ear. Am J Phys 269:C1450–C1456
go back to reference Taguchi D, Takeda T, Kakigi A, Okada T, Nishioka R, Kitano H (2008) Expression and immunolocalization of aquaporin-6 (Aqp6) in the rat inner ear. Acta Otolaryngol 128:832–840CrossRefPubMed Taguchi D, Takeda T, Kakigi A, Okada T, Nishioka R, Kitano H (2008) Expression and immunolocalization of aquaporin-6 (Aqp6) in the rat inner ear. Acta Otolaryngol 128:832–840CrossRefPubMed
go back to reference Takumi Y, Nagelhus EA, Eidet J, Matsubara A, Usami S, Shinkawa H, Nielsen S, Ottersen OP (1998) Select types of supporting cell in the inner ear express aquaporin-4 water channel protein. Eur J Neurosci 10:3584–3595CrossRefPubMed Takumi Y, Nagelhus EA, Eidet J, Matsubara A, Usami S, Shinkawa H, Nielsen S, Ottersen OP (1998) Select types of supporting cell in the inner ear express aquaporin-4 water channel protein. Eur J Neurosci 10:3584–3595CrossRefPubMed
go back to reference Tchekneva EE, Khuchua Z, Davis LS, Kadkina V, Dunn SR, Bachman S, Ishibashi K, Rinchik EM, Harris RC, Dikov MM, Breyer MD (2008) Single amino acid substitution in aquaporin 11 causes renal failure. Journal of the American Society of Nephrology: JASN 19:1955–1964CrossRefPubMedPubMedCentral Tchekneva EE, Khuchua Z, Davis LS, Kadkina V, Dunn SR, Bachman S, Ishibashi K, Rinchik EM, Harris RC, Dikov MM, Breyer MD (2008) Single amino acid substitution in aquaporin 11 causes renal failure. Journal of the American Society of Nephrology: JASN 19:1955–1964CrossRefPubMedPubMedCentral
go back to reference Yakata K, Hiroaki Y, Ishibashi K, Sohara E, Sasaki S, Mitsuoka K, Fujiyoshi Y (2007) Aquaporin-11 containing a divergent NPA motif has normal water channel activity. Biochim Biophys Acta 1768:688–693CrossRefPubMed Yakata K, Hiroaki Y, Ishibashi K, Sohara E, Sasaki S, Mitsuoka K, Fujiyoshi Y (2007) Aquaporin-11 containing a divergent NPA motif has normal water channel activity. Biochim Biophys Acta 1768:688–693CrossRefPubMed
go back to reference Yamamoto T, Sasaki S (1998) Aquaporins in the kidney: emerging new aspects. Kidney Int 54:1041–1051CrossRefPubMed Yamamoto T, Sasaki S (1998) Aquaporins in the kidney: emerging new aspects. Kidney Int 54:1041–1051CrossRefPubMed
go back to reference Yasui M, Kwon TH, Knepper MA, Nielsen S, Agre P (1999) Aquaporin-6: an intracellular vesicle water channel protein in renal epithelia. Proc Natl Acad Sci U S A 96:5808–5813CrossRefPubMedPubMedCentral Yasui M, Kwon TH, Knepper MA, Nielsen S, Agre P (1999) Aquaporin-6: an intracellular vesicle water channel protein in renal epithelia. Proc Natl Acad Sci U S A 96:5808–5813CrossRefPubMedPubMedCentral
Metadata
Title
Quantitative Analysis of Aquaporin Expression Levels during the Development and Maturation of the Inner Ear
Authors
Takushi Miyoshi
Taro Yamaguchi
Kiyokazu Ogita
Yasuko Tanaka
Ken-ichi Ishibashi
Hiroaki Ito
Taisuke Kobayashi
Takayuki Nakagawa
Juichi Ito
Koichi Omori
Norio Yamamoto
Publication date
01-04-2017
Publisher
Springer US
Published in
Journal of the Association for Research in Otolaryngology / Issue 2/2017
Print ISSN: 1525-3961
Electronic ISSN: 1438-7573
DOI
https://doi.org/10.1007/s10162-016-0607-3

Other articles of this Issue 2/2017

Journal of the Association for Research in Otolaryngology 2/2017 Go to the issue