Critical roles of transitional cells and Na/K-ATPase in the formation of vestibular endolymph

Journal of Neuroscience

Volumn 31, Issue 46, 2011, Pages 16541-16549

  Bartolami, Sylvain ^a,c   Gaboyard, Sophie ^a   Quentin, Julie ^a   Travo, Cécile ^a   Cavalier, Mélanie ^a   Barhanin, Jacques ^b   Chabbert, Christian ^a  

^a HÔPITAL SAINT ELOI   (France)

^b INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^c UNIV MONTPELLIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); AMIKACIN; BUMETANIDE; GADOLINIUM; GENTAMICIN; OUABAIN; POTASSIUM ION; SODIUM POTASSIUM CHLORIDE COTRANSPORTER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CELL FUNCTION; CONTROLLED STUDY; ENDOLYMPH; ENZYME ACTIVITY; EPITHELIUM CELL; FEMALE; GENE DELETION; INCUBATION TIME; KCNE1 GENE; MALE; MOUSE; NERVE CELL MEMBRANE STEADY POTENTIAL; NEWBORN; NONHUMAN; ORGANOGENESIS; PERINATAL DEVELOPMENT; POTASSIUM CELL LEVEL; POTASSIUM TRANSPORT; PRIORITY JOURNAL; PROTEIN TARGETING; RAT; SENSORY NERVE CELL; TRANSITIONAL CELL; UTRICLE;

AMINOGLYCOSIDES; ANIMALS; ANIMALS, NEWBORN; BUMETANIDE; ENDOCYTOSIS; ENDOLYMPH; ENZYME INHIBITORS; EPITHELIAL CELLS; FEMALE; GADOLINIUM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORGAN CULTURE TECHNIQUES; OUABAIN; POTASSIUM; POTASSIUM CHANNELS, VOLTAGE-GATED; PYRIDINIUM COMPOUNDS; QUATERNARY AMMONIUM COMPOUNDS; RATS; RATS, WISTAR; SACCULE AND UTRICLE; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS; SODIUM-POTASSIUM-EXCHANGING ATPASE; TIME FACTORS;

EID: 81255211977     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2430-11.2011     Document Type: Article

References (55)

1. Anniko M, Nordemar H (1980) Embryogenesis of the inner ear. IV. Postnatal maturation of the secretory epithelia of the inner ear in correlation with the elemental composition in the endolymphatic space. Arch Otorhinolaryngol 229:281-288
2. Aran JM, Chappert C, Dulon D, Erre JP, Aurousseau C (1995) Uptake of amikacin by hair cells of the guinea pig cochlea and vestibule and ototoxicity: comparison with gentamicin. Hear Res 82:179-183
3. Bagrov AY, Shapiro JI, Federova OV (2009) Endogenous cardiotonic steroids: physiology, pharmacology and novel therapeutic targets. Pharmacol Rev 61:9-38
4. Crouch JJ, Sakaguchi N, Lytle C, Schulte BA (1997) Immunohistochemical localization of the Na-K-Cl co-transporter (NKCC1) in the gerbil inner ear. J Histochem Cytochem 45:773-778
5. Delpire E, Lu J, England R, Dull C, Thorne T (1999) Deafness and imbalance associated with inactivation of the secretory Na-K-2Cl cotransporter. Nat Genet 22:192-195
6. Delprat B, Schaer D, Roy S, Wang J, Puel JL, Geering K (2007) FXYD6 is a novel regulator of Na,K-ATPase expressed in the inner ear. J Biol Chem 282:7450-7456
7. Deol MS (1968) Inherited diseases of the inner ear in man in light of studies on the mouse. J Med Genet 5:137-158
8. Diaz RC, Vazquez AE, Dou H, Wei D, Cardell EL, Lingrel J, Shull GE, Doyle KJ, Yamoah EN (2007) Conservation of hearing by simultaneous mutation of NaK-ATPase and NKCC1. J Assoc Res Otolaryngol 8:422-434
9. Dravis C, Wu T, Chumley MJ, Yokoyama N, Wei S, Wu DK, Marcus DC, Henkemeyer M (2007) EphB2 and ephrin-B2 regulate the ionic homeostasis of vestibular endolymph. Hear Res 223:93-104
10. Gaboyard S, Chabbert C, Travo C, Bancel F, Lehouelleur J, Yamauchi D, Marcus DC, Sans A (2005) Three-dimensional culture of newborn rat utricle using an extracellular matrix promotes formation of a cyst. Neuroscience 133:253-265
11. Gale JE, Marcotti W, Kennedy HJ, Kros CJ, Richardson GP (2001) FM1-43 dye behaves as a permeant blocker of the hair-cell mechanotransducer channel. J Neurosci 21:7013-7025
12. Gamba G (2005) Molecular physiology and physiopathology of electroneutral cation-chloride cotransporters. Physiol Rev 85:423-493
13. Geering K (2008) Functional roles of Na,K-ATPase subunits. Curr Opin Nephrol Hypertens 17:526-532
14. Géléoc GS, Holt JR (2003) Developmental acquisition of sensory transduction in hair cells of the mouse inner ear. Nat Neurosci 6:1019-1020
15. Glitsch HG (2001) Electrophysiology of the sodium-potassium-ATPase in cardiac cells. Physiol Rev 81:1791-1826
16. Hsu CJ (1991) Ultrastructural study of cytochemical localization of carbonic anhydrase in the inner ear. Acta Otolaryngol 111:75-84
17. Kawasaki K, Yamamoto A, Omori K, Iwano T, Kumazawa T, Tashiro Y (1992) Quantitative immunoelectron microscopic localization of Na, K-ATPase alpha-subunit in the epithelial cells of rat vestibular apparatus. Hear Res 60:64-72
18. Kimitsuki T, Nakagawa T, Hisashi K, Komune S, Komiyama S (1996) Gadolinium blocks mechano-electric transducer current in chick cochlear hair cells. Hear Res 101:75-80
19. Kroese AB, Das A, Hudspeth AJ (1989) Blockage of the transduction channels of hair cells in the bullfrog's sacculus by aminoglycoside antibiotics. Hear Res 37:203-217
20. Lang F, Vallon V, Knipper M, Wangemann P (2007) Functional significance of channels and transporters expressed in the inner ear and kidney. Am J Physiol Cell Physiol 293:C1187-C1208.
21. Lee JH, Chiba T, Marcus DC (2001) P2X2 receptor mediates stimulation of parasensory cation absorption by cochlear outer sulcus cells and vestibular transitional cells. J Neurosci 21:9168-9174
22. Lewis RS, Hudspeth AJ (1983) Voltage-and ion-dependent conductances in solitary vertebrate hair cells. Nature 304:538-541
23. Lim DJ, Erway LC, Clark DL (1978) Tilted head mice with genetic otoconial anomaly: behavioral and morphological correlates. In: Vestibular mechanisms in health and disease. (Hood JD, ed), pp 195-206 New York: Academic.
24. Lim DJ, Karabinas C, Trune DR (1983) Histochemical localization of carbonic anhydrase in the inner ear. Am J Otolaryngol 4:33-42
25. Marcus DC, Shen Z (1994) Slowly activating voltage-dependent K+ conductance is apical pathway for K+secretion in vestibular dark cells. Am J Physiol 267:C857-C864.
26. Marcus DC, Liu J, Wangemann P (1994) Transepithelial voltage and resistance of vestibular dark cell epithelium from the gerbil ampulla. Hear Res 73:101-108
27. Marcus DC, Wu T, Wangemann P, Kofuji P (2002) KCNJ10 (Kir4.1) potassium knockout abolishes endocochlear potential. Am J Physiol Cell Physiol 282:C403-C407.
28. Masetto S, Zucca G, Bottà L, Valli P (2005) Endolymphatic potassium of the chicken vestibule during embryonic development. Int J Dev Neurosci 23:439-448
29. Meyers JR, MacDonald RB, Duggan A, Lenzi D, Standaert DG, Corwin JT, Corey DP (2003) Lighting up the senses: FM1-43 loading of sensory cells through nonselective ion channels. J Neurosci 23:4054-4065
30. Milhaud PG, Pondugula SR, Lee JH, Herzog M, Lehouelleur J, Wangemann P, Sans A, Marcus DC (2002) Chloride secretion by semicircular canal duct epithelium is stimulated via beta 2-adrenergic receptors. Am J Physiol Cell Physiol 283:C1752-C1760.
31. Nakaya K, Harbidge DG, Wangemann P, Schultz BD, Green ED, Wall SM, Marcus DC (2007) Lack of pendrin HCO3-transport elevates vestibular endolymphatic [Ca2+] by inhibition of acid-sensitive TRPV5 and TRPV6 channels. Am J Physiol Renal Physiol 292:F1314-F1321.
32. Nicolas M, Demêmes D, Martin A, Kupershmidt S, Barhanin J (2001) KCNQ1/KCNE1 potassium channels in mammalian vestibular dark cells. Hear Res 153:132-145
33. Nicolas MT, Lesage F, Reyes R, Barhanin J, Demêmes D (2004) Localization of Trek-1, a two pore domain K+ channel in the peripheral vestibular system of mouse and rat. Brain Res 1017:46-52
34. Pitovski DZ, Kerr TP (2002) Sodium and potassium activated ATPase in the mammalian vestibular system. Hear Res 171:51-65
35. Popper P, Winkler J, Erbe CB, Lerch-Gaggl A, Siebeneich W, Wackym PA (2008) Distribution of two pore domain potassium channel in the adult rat vestibular periphery. Hear Res 246:1-8
36. Richardson GP, Russell IJ (1991) Cochlear cultures as a model system for studying aminoglycoside induced ototoxicity. Hear Res 53:293-311
37. Roberts WM, Howard J, Hudspeth AJ (1988) Hair cells: transduction, tuning, and transmission in the inner ear. Annu Rev Cell Biol 4:63-92
38. Roehm P, Hoffer M, Balaban CD (2007) Gentamicin uptake in the chinchilla inner ear. Hear Res 230:43-52
39. Royaux IE, Belyantseva IA, Wu T, Kachar B, Everett LA, Marcus DC, Green ED (2003) Localization and functional studies of pendrin in the mouse inner ear provide insight about the etiology of deafness in pendred syndrome. J Assoc Res Otolaryngol 4:394-404
40. Sakaguchi N, Crouch JJ, Lytle C, Schulte BA (1998) Na-K-Cl cotransporter expression in the developing and senescent gerbil cochlea. Hear Res 118;114-122
41. Singh R, Wangemann P (2008) Free radical stress-mediated loss of Kcnj10 protein expression in the stria vascularis contributes to deafness in Pendred syndrome mouse model. Am J Physiol Renal Physiol 294:F139-F148.
42. +-ATPase and carbonic anhydrase in the gerbil's vestibular system. Hear Res 43:205-217
43. Takumida M, Bagger-Sjöbäck D, Wersäll J, Harada Y (1989) Ultrastructural localization of carbonic anhydrase in the vestibular end organs of the guinea pig. Arch Otorhinolaryngol 246:56-60
44. Taura A, Kojima K, Ito J, Ohmori H (2006) Recovery of hair cell function after damage induced by gentamicin in organ culture of rat vestibular maculae. Brain Res 1098:33-48
45. Teggi R, Lanzani C, Zagato L, Delli Carpini S, Manunta P, Bianchi G, Bussi M (2008) Gly460Trp a-adducin mutation as a possible mechanism leading to endolymphatic hydrops in Méniére's syndrome. Otol Neurotol 29:824-828
46. Teggi R, Zagato L, Delli Carpini S, Messaggio E, Casamassima N, Lanzani C, Manunta P, Bussi M (2010) Endogenous ouabain in Méniére's disease. Otol Neurotol 31:153-156
47. Vetter DE, Mann JR, Wangemann P, Liu J, McLaughlin KJ, Lesage F, Marcus DC, Lazdunski M, Heinemann SF, Barhanin J (1996) Inner ear defects induced by null mutation of isk gene. Neuron 17:1251-1264
48. Wangemann P (1995) Comparison of ion transport mechanisms between vestibular dark cells and strial marginal cells. Hear Res 90:149-157
49. Wangemann P (2002) K(+) cycling and its regulation in the cochlea and the vestibular labyrinth. Audiol Neurootol 7:199-205
50. Wangemann P, Marcus DC (1989) Membrane potential measurements of transitional cells from the crista ampullaris of the gerbil: effects of barium, quinidine, quinine, tetraethylammonium, cesium, ammonium, thallium and ouabain. Pflugers Arch 414:656-662
51. Wangemann P, Shen Z, Liu J (1996) K(+)-induced stimulation of K+ secretion involves activation of the IsK channel in vestibular dark cells. Hear Res 100:201-210
52. Wangemann P, Itza EM, Albrecht B, Wu T, Jabba SV, Maganti RJ, Lee JH, Everett LA, Wall SM, Royaux IE, Green ED, Marcus DC (2004) Loss of KCNJ10 protein expression abolishes endocochlear potential and causes deafness in Pendred syndrome mouse model. BMC Med 2:30-44
53. Yang T, Gurrola JG 2nd, Wu H, Chiu SM, Wangemann P, Snyder PM, Smith RJ (2009) Mutations of KCNJ10 together with mutations of SLC26A4 cause digenic nonsyndromic hearing loss associated with enlarged vestibular aqueduct syndrome. Am J Hum Genet 84:651-657
54. Yoshihara T, Kaname H, Ishii T, Igarashi M (1994) Effect of gentamicin on vestibular dark cells and melanocytes: an ultrastructural and cytochemical study. ORL J Otorhinolaryngol Relat Spec 56:24-30
55. Young Choi J, Ho Jung S, Namkung W, Lee JH, Jin Son E, Wook Shin J, Park HY, Sang Lee W, Kim HN (2005) Vestibular malformation in mice lacking Na-K-2Cl cotransporter 1 and expression of Na-K-2Cl cotranspoter 1 in human vestibular end organs. Acta Otolaryngol 125:1252-1257