Potassium ion movement in the inner ear: Insights from genetic disease and mouse models

Physiology

Volumn 24, Issue 5, 2009, Pages 307-316

  Zdebik, Anselm A ^a   Wangemann, Philine ^b   Jentsch, Thomas J ^c  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b KANSAS STATE UNIVERSITY   (United States)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ION; POTASSIUM; POTASSIUM CHANNEL;

ANIMAL; GENETICS; HAIR CELL; HUMAN; INNER EAR; INNER EAR DISEASE; METABOLISM; MOUSE; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW;

ANIMALS; EAR, INNER; HAIR CELLS, AUDITORY; HUMANS; IONS; LABYRINTH DISEASES; MICE; POTASSIUM; POTASSIUM CHANNELS;

EID: 70349916044     PISSN: 15489213     EISSN: 15489221     Source Type: Journal    
DOI: 10.1152/physiol.00018.2009     Document Type: Review

References (76)

1. Ahmad S, Tang W, Chang Q, Qu Y, Hibshman J, Li Y, Sohl G, Willecke K, Chen P, Lin X. Restoration of connexin26 protein level in the cochlea completely rescues hearing in a mouse model of human connexin30-linked deafness. Proc Natl Acad Sci USA 104: 1337-1341, 2007.
2. - currents. Neurosci Lett 284: 171-174, 2000.
3. Angeli S, Utrera R, Dib S, Chiossone E, Naranjo C, Henriquez O, Porta M. GJB2 gene mutations in childhood deafness. Acta Otolaryngol (Stockh) 120: 133-136, 2000.
4. Ashmore J. Cochlear outer hair cell motility. Physiol Rev 88: 173-210, 2008.
5. Bai J P, Surguchev A, Montoya S, Aronson PS, Santos-Sacchi J, Navaratnam D. Prestin's anion transport and voltage-sensing capabilities are independent. Biophys J 96: 3179-3186, 2009.
6. Barhanin J, Lesage F, Guillemare E, Fink M, Lazdunski M, Romey G. K(V)LQT1 and lsK (minK) proteins associate to form the I(Ks) cardiac potassium current. Nature 384: 78-80, 1996.
7. Ben-Yosef T, Belyantseva IA, Saunders TL, Hughes ED, Kawamoto K, Van Itallie CM, Beyer LA, Halsey K, Gardner DJ, Wilcox ER, Rasmussen J, Anderson JM, Dolan D F, Forge A, Raphael Y, Camper SA, Friedman TB. Claudin 14 knockout mice, a model for autosomal recessive deafness DFNB29, are deaf due to cochlear hair cell degeneration. Hum Mol Genet 12: 2049-2061, 2003.
8. Birkenhäger R, Otto E, Schürmann MJ, Vollmer M, Ruf EM, Maier-Lutz I, Beekmann F, Fekete A, Omran H, Feldmann D, Milford DV, Jeck N, Konrad M, Landau D, Knoers NVAM, Antignac C, Sudbrack R, Kispert A, Hildebrandt F. Mutation of BSND causes Bartter syndrome with sensorineural deafness and kidney failure. Nat Genet 29: 310-314, 2001.
9. Bockenhauer D, Feather S, Stanescu HC, Bandulik S, Zdebik AA, Reichold M, Tobin J, Lieberer E, Sterner C, Landoure G, Arora R, Sirimanna T, Thompson D, Cross JH, van't Hoff W, Al Masri O, Tullus K, Yeung S, Anikster Y, Klootwijk E, Hubank M, Dillon MJ, Heitzmann D, Arcos-Burgos M, Knepper MA, Dobbie A, Gahl WA, Warth R, Sheridan E, Kleta R. Epilepsy, ataxia, sensorineural deafness, tubulopathy, and KCNJ10 mutations. N Engl J Med 360: 1960-1970, 2009.
10. Boettger T, Hübner C, Maier H, Rust MB, Beck FX, Jentsch TJ. Deafness and renal tubular acidosis in mice lacking the K-Cl cotransporter Kcc4. Nature 416: 874-878, 2002.
11. Boettger T, Rust MB, Maier H, Seidenbecher T, Schweizer M, Keating DJ, Faulhaber J, Ehmke H, Pfeffer C, Scheel O, Lemcke B, Horst J, Leuwer R, Pape HC, Volkl H, Hübner CA, Jentsch TJ. Loss of K-Cl co-transporter KCC3 causes deafness, neurodegeneration and reduced seizure threshold. EMBO J 22: 5422-5434, 2003.
12. Cohen-Salmon M, Ott T, Michel V, Hardelin J P, Perfettini I, Eybalin M, Wu T, Marcus DC, Wangemann P, Willecke K, Petit C. Targeted ablation of connexin26 in the inner ear epithelial gap junction network causes hearing impairment and cell death. Curr Biol 12: 1106-1111, 2002.
13. Cohen-Salmon M, Regnault B, Cayet N, Caille D, Demuth K, Hardelin J P, Janel N, Meda P, Petit C. Connexin30 deficiency causes instrastrial fluid-blood barrier disruption within the cochlear stria vascularis. Proc Natl Acad Sci USA 104: 6229-6234, 2007.
14. Corey D P. What is the hair cell transduction channel? J Physiol 576: 23-28, 2006.
15. Corey D P, Garcia-Anoveros J, Holt JR, Kwan KY, Lin SY, Vollrath MA, Amalfitano A, Cheung EL, Derfler BH, Duggan A, Geleoc GS, Gray PA, Hoffman M P, Rehm HL, Tamasauskas D, Zhang DS. TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells. Nature 432: 723-730, 2004.
16. Crouch JJ, Sakaguchi N, Lytle C, Schulte BA. Immunohistochemical localization of the Na-K-Cl co-transporter (NKCC1) in the gerbil inner ear. J Histochem Cytochem 45: 773-778, 1997.
17. Dallos P. Cochlear amplification, outer hair cells and prestin. Curr Opin Neurobiol 18: 370-376, 2008.
18. Delpire E, Lu J, England R, Dull C, Thorne T. Deafness and imbalance associated with inactivation of the secretory Na-K-2Cl co-transporter. Nat Genet 22: 192-195, 1999.
19. Dixon MJ, Gazzard J, Chaudhry SS, Sampson N, Schulte BA, Steel K P. Mutation of the Na-K-Cl co-transporter gene Slc12a2 results in deafness in mice. Hum Mol Genet 8: 1579-1584, 1999.
20. + secretion. Nature 414: 558-561, 2001.
21. Everett LA, Belyantseva IA, Noben-Trauth K, Cantos R, Chen A, Thakkar SI, Hoogstraten-Miller SL, Kachar B, Wu DK, Green ED. Targeted disruption of mouse Pds provides insight about the inner-ear defects encountered in Pendred syndrome. Hum Mol Genet 10: 153-161, 2001.
22. Hibino H, Horio Y, Inanobe A, Doi K, Ito M, Yamada M, Gotow T, Uchiyama Y, Kawamura M, Kubo T, Kurachi Y. An ATP-dependent inwardly rectifying potassium channel, KAB-2 (Kir4.1), in cochlear stria vascularis of inner ear: its specific subcellular localization and correlation with the formation of endocochlear potential. J Neurosci 17: 4711-4721, 1997.
23. Jentsch TJ. Chloride transport in the kidney: lessons from human disease and knockout mice. J Am Soc Nephrol 16: 1549-1561, 2005.
24. Johnstone BM, Patuzzi R, Syka J, Sykova E. Stimulus-related potassium changes in the organ of Corti of guinea-pig. J Physiol 408: 77-92, 1989.
25. +-ATPase cause renal tubular acido-sis with sensorineural deafness. Nat Genet 21: 84-90, 1999.
26. + channels implicate sensory outer hair cells in human progressive deafness. EMBO J 25: 642-652, 2006.
27. + channel mutated in a form of dominant deafness, is expressed in the inner ear and the central auditory pathway. Proc Natl Acad Sci USA 97: 4333-4338, 2000.
28. Kikuchi T, Adams JC, Miyabe Y, So E, Kobayashi T. Potassium ion recycling pathway via gap junction systems in the mammalian cochlea and its interruption in hereditary nonsyndromic deafness. Med Electron Microsc 33: 51-56, 2000.
29. Kitajiri S, Miyamoto T, Mineharu A, Sonoda N, Furuse K, Hata M, Sasaki H, Mori Y, Kubota T, Ito J, Furuse M, Tsukita S. Compartmentalization established by claudin-11-based tight junctions in stria vascularis is required for hearing through generation of endocochlear potential. J Cell Sci 117: 5087-5096, 2004.
30. Konishi T, Hamrick PE, Walsh PJ. Ion transport in guinea pig cochlea. I. Potassium and sodium transport. Acta Otolaryngol (Stockh) 86: 22-34, 1978. (Pubitemid 8400504)
31. Kubisch C, Schroeder BC, Friedrich T, Lutjohann B, El-Amraoui A, Marlin S, Petit C, Jentsch TJ. KCNQ4, a novel potassium channel expressed in sensory outer hair cells, is mutated in dominant deafness. Cell 96: 437-446, 1999.
32. Kwan K Y, Allchorne AJ, Vollrath MA, Christensen A P, Zhang DS, Woolf CJ, Corey D P. TRPA1 contributes to cold, mechanical, and chemical noci-ception but is not essential for hair-cell transduc-tion. Neuron 50: 277-289, 2006.
33. Lee M P, Ravenel JD, Hu RJ, Lustig LR, Tomaselli G, Berger RD, Brandenburg SA, Litzi TJ, Bunton TE, Limb C, Francis H, Gorelikow M, Gu H, Washington K, Argani P, Goldenring JR, Coffey RJ, Feinberg A P. Targeted disruption of the Kvlqt1 gene causes deafness and gastric hyperplasia in mice. J Clin Invest 106: 1447-1455, 2000.
34. Liberman MC, Gao J, He DZ, Wu X, Jia S, Zuo J. Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier. Nature 419: 300-304, 2002.
35. Maehara H, Okamura HO, Kobayashi K, Uchida S, Sasaki S, Kitamura K. Expression of CLC-KB gene promoter in the mouse cochlea. Neuroreport 14: 1571-1573, 2003.
36. + secretion in vestibular dark cells. Am J Physiol Cell Physiol 267: C857-C864, 1994.
37. Marcus DC, Takeuchi S, Wangemann P. Two types of chloride channel in the basolateral membrane of vestibular dark cells. Hear Res 69: 124-132, 1993.
38. Marcus DC, Wangemann P. Cochlear and vestibu-lar function and dysfunction. In: Physiology and Pathology of Chloride Transporters and Channels in the Nervous System-From Molecules to Diseases, edited by Alvarez-Leefmans FJ, Delpier E. Oxford, UK: Elsevier, 2009. In press.
39. Marcus DC, Wu T, Wangemann P, Kofuji P. KCNJ10 (Kir4.1) potassium channel knockout abolishes endocochlear potential. Am J Physiol Cell Physiol 282: C403-C407, 2002.
40. Melichar I, Syka J. Electrophysiological measurements of the stria vascularis potentials in vivo. Hear Res 25: 35-43, 1987. (Pubitemid 17201711)
41. Muallem D, Ashmore J. An anion antiporter model of prestin, the outer hair cell motor protein. Biophys J 90: 4035-4045, 2006.
42. Mustapha M, Fang Q, Gong TW, Dolan DF, Raphael Y, Camper SA, Duncan RK. Deafness and permanently reduced potassium channel gene expression and function in hypothyroid Pit1dw mutants. J Neurosci 29: 1212-1223, 2009.
43. Nakano Y, Kim SH, Kim HM, Sannemann JD, Zhang Y, Smith RJH, Marcus DC, Wangemann Nessler P, Banfi RA, B. A Claudin-9-based permeability barrier is essential for hearing. PLoS Genetics. In press.
44. 2+] by inhibition of acid-sensitive TRPV5 and TRPV6 channels. Am J Physiol Renal Physiol 292: F1314-F1321, 2007.
45. Nickel R, Forge A. Gap junctions and connexins in the inner ear: their roles in homeostasis and deafness. Curr Opin Otolaryngol Head Neck Surg 16: 452-457, 2008.
46. + diffusion potentials and an electrical barrier in the stria vascularis of the inner ear. Proc Natl Acad Sci USA 105: 1751-1756, 2008.
47. Nozu K, Inagaki T, Fu XJ, Nozu Y, Kaito H, Kanda K, Sekine T, Igarashi T, Nakanishi K, Yoshikawa N, Iijima K, Matsuo M. Molecular analysis of digenic inheritance in Bartter syndrome with sensorineur-al deafness. J Med Genet 45: 182-186, 2008.
48. Pfeffer CK, Stein V, Keating DJ, Maier H, Rinke I, Rudhard Y, Hentschke M, Rune GM, Jentsch TJ, Hübner CA. NKCC1-dependent GABAergic excitation drives synaptic network maturation during early hippocampal development. J Neurosci 29: 3419-3430, 2009.
49. - channels: mechanism underlying deafness in Bartter syndrome IV. EMBO J 27: 2907-2917, 2008.
50. 2+-activated potassium (BK) alpha-subunit but not the BKbeta1-subunit leads to progressive hearing loss. Proc Natl Acad Sci USA 101: 12922-12927, 2004.
51. Sage CL, Marcus DC. Immunolocalization of ClC-K chloride channel in strial marginal cells and vestibular dark cells. Hear Res 160: 1-9, 2001.
52. Salt AN, Melichar I, Thalmann R. Mechanisms of endocochlear potential generation by stria vascu-laris. Laryngoscope 97: 984-991, 1987.
53. Sanguinetti MC, Curran ME, Zou A, Shen J, Spector PS, Atkinson DL, Keating MT. Coassembly of K(V)LQT1 and minK (IsK) proteins to form cardiac I(Ks) potassium channel. Nature 384: 80-83, 1996.
54. Schaechinger TJ, Oliver D. Nonmammalian orthologs of prestin (SLC26A5) are electrogenic divalent/chloride anion exchangers. Proc Natl Acad Sci USA 104: 7693-7698, 2007.
55. Schlingmann K P, Konrad M, Jeck N, Waldegger P, Reinalter SC, Holder M, Seyberth HW, Waldegger S. Salt wasting and deafness resulting from mutations in two chloride channels. N Engl J Med 350: 1314-1319, 2004.
56. Scholl UI, Choi M, Liu T, Ramaekers VT, Hausler MG, Grimmer J, Tobe SW, Farhi A, Nelson-Williams C, Lifton R P. Seizures, sensorineural deafness, ataxia, mental retardation, and electrolyte imbalance (SeSAME syndrome) caused by mutations in KCNJ10. Proc Natl Acad Sci USA 106: 5842-5847, 2009.
57. +-ATPase in the cochlear lateral wall is critically involved in formation of the endocochlear potential. Am J Physiol Cell Physiol 291: C1038-C1048, 2006.
58. Simon DB, Bindra RS, Mansfield TA, Nelson-Williams C, Mendonca E, Stone R, Schurman S, Nayir A, Alpay H, Bakkaloglu A, Rodriguez-Soriano J, Morales JM, Sanjad SA, Taylor CM, Pilz D, Brem A, Trachtman H, Griswold W, Richard GA, John E, Lifton R P. Mutations in the chloride channel gene, CLCNKB, cause Bartter's syndrome type III. Nat Genet 17: 171-178, 1997.
59. Singh R, Wangemann P. Free radical stress-mediated loss of Kcnj10 protein expression in stria vas-cularis contributes to deafness in Pendred syndrome mouse model. Am J Physiol Renal Physiol 294: F139-F148, 2008.
60. + recycling pathway from inner hair cells. Hear Res 118: 1-12, 1998.
61. Spicer SS, Schulte BA. The fine structure of spiral ligament cells relates to ion return to the stria and varies with place-frequency. Hear Res 100: 80-100, 1996.
62. Splawski I, Timothy KW, Vincent GM, Atkinson DL, Keating George M Cober Lecturer: Mark T Keating MT. Molecular basis of the long-QT syndrome associated with deafness. Proc Assoc Am Physicians 109: 504-511, 1997. (Pubitemid 27381469)
63. Stover EH, Borthwick KJ, Bavalia C, Eady N, Fritz DM, Rungroj N, Giersch AB, Morton CC, Axon PR, Akil I, Al-Sabban EA, Baguley DM, Bianca S, Bakkaloglu A, Bircan Z, Chauveau D, Clermont MJ, Guala A, Hulton SA, Kroes H, Li Volti G, Mir S, Mocan H, Nayir A, Ozen S, Rodriguez Soriano J, Sanjad SA, Tasic V, Taylor CM, Topaloglu R, Smith AN, Karet FE. Novel ATP6V1B1 and ATP6V0A4 mutations in autosomal recessive distal renal tubular acidosis with new evidence for hearing loss. J Med Genet 39: 796-803, 2002.
64. + currents in intermediate cells in the cochlea of ger-bils: a possible contribution to the endocochlear potential. Neurosci Lett 247: 175-178, 1998.
65. Teubner B, Michel V, Pesch J, Lautermann J, Cohen-Salmon M, Sohl G, Jahnke K, Winterhager E, Herberhold C, Hardelin J P, Petit C, Willecke K. Connexin30 (Gjb6)-deficiency causes severe hearing impairment and lack of endocochlear potential. Hum Mol Genet 12: 13-21, 2003.
66. Vetter DE, Mann JR, Wangemann P, Liu J, McLaughlin KJ, Lesage F, Marcus DC, Lazdunski M, Heinemann S F, Barhanin J. Inner ear defects induced by null mutation of the isk gene. Neuron 17: 1251-1264, 1996.
67. Wangemann P. Comparison of ion transport mechanisms between vestibular dark cells and strial marginal cells. Hear Res 90: 149-157, 1995.
68. Wangemann P. Supporting sensory transduction: cochlear fluid homeostasis and the endocochlear potential. J Physiol 576: 11-21, 2006.
69. Wangemann P, Itza EM, Albrecht B, Wu T, Jabba SV, Maganti RJ, Lee JH, Everett LA, Wall SM, Royaux IE, Green ED, Marcus DC. Loss of KCNJ10 protein expression abolishes endocochlear potential and causes deafness in Pendred syndrome mouse model. BMC Med 2: 30, 2004.
70. 2+ reabsorption in a Pendred syndrome mouse model. Am J Physiol Renal Physiol 292: F1345-F1353, 2007.
71. Wilcox ER, Burton QL, Naz S, Riazuddin S, Smith TN, Ploplis B, Belyantseva I, Ben-Yosef T, Liburd NA, Morell RJ, Kachar B, Wu DK, Griffith AJ, Friedman TB. Mutations in the gene encoding tight junction claudin-14 cause autosomal recessive deafness DFNB29. Cell 104: 165-172, 2001.
72. + channel mutations found in inherited cardiac arrhythmias. Hum Mol Genet 6: 1943-1949, 1997.
73. Yamauchi K, Rai T, Kobayashi K, Sohara E, Suzuki T, Itoh T, Suda S, Hayama A, Sasaki S, Uchida S. Disease-causing mutant WNK4 increases paracel-lular chloride permeability and phosphorylates claudins. Proc Natl Acad Sci USA 101: 4690-4694, 2004.
74. Yang T, Gurrola JG, 2nd Wu H, Chiu SM, Wangemann P, Snyder PM, Smith RJ. 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, 2009.
75. Zhang Y, Tang W, Ahmad S, Sipp JA, Chen P, Lin X. Gap junction-mediated intercellular biochemical coupling in cochlear supporting cells is required for normal cochlear functions. Proc Natl Acad Sci USA 102: 15201-15206, 2005.
76. Zidanic M, Brownell WE. Fine structure of the intracochlear potential field. I. The silent current. Biophys J 57: 1253-1268, 1990.