Molecular basis of decreased Kir4.1 function in SeSAME/EAST syndrome

Journal of the American Society of Nephrology

Volumn 21, Issue 12, 2010, Pages 2117-2129

  Williams, David M ^a   Lopes, Coeli M B ^a   Rosenhouse Dantsker, Avia ^b   Connelly, Heather L ^a   Matavel, Alessandra ^a   O Uchi, Jin ^a   McBeath, Elena ^a   Gray, Daniel A ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POTASSIUM CHANNEL; POTASSIUM CHANNEL A167V R297C; POTASSIUM CHANNEL C140R; POTASSIUM CHANNEL G77R; POTASSIUM CHANNEL KIR4.1; POTASSIUM CHANNEL R65P; POTASSIUM CHANNEL R65P RI99X; POTASSIUM CHANNEL T1641; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; HUMAN; NUCLEOTIDE SEQUENCE; PH MEASUREMENT; POTASSIUM CHANNELOPATHY; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SESAME EAST SYNDROME;

EID: 78649891905     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2009121227     Document Type: Article

References (56)

1. Scholl UI, Choi M, Liu T, Ramaekers VT, Hausler MG, Grimmer J, Tobe SW, Farhi A, Nelson-Williams C, Lifton RP: Seizures, sensorineural deafness, ataxia, mental retardation, and electrolyte imbalance (SeSAME syndrome) caused by mutations in KCNJ10. Proc Natl Acad Sci U.S.A. 106: 5842-5847, 2009
2. 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
3. Reimann F, Ashcroft FM: Inwardly rectifying potassium channels. Curr Opin Cell Biol 11: 503-508, 1999
4. Nichols CG, Lopatin AN: Inward rectifier potassium channels. Annu Rev Physiol 59: 171-191, 1997
5. Higashi K, Fujita A, Inanobe A, Tanemoto M, Doi K, Kubo T, Kurachi Y: An inwardly rectifying K(+) channel, Kir4.1, expressed in astrocytes surrounds synapses and blood vessels in brain. Am J Physiol Cell Physiol 281: C922-C931, 2001
6. Djukic B, Casper KB, Philpot BD, Chin LS, McCarthy KD: Conditional knock-out of Kir4.1 leads to glial membrane depolarization, inhibition of potassium and glutamate uptake, and enhanced short-term synaptic potentiation. J Neurosci 27: 11354-11365, 2007
7. 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 (Pubitemid 34663200)
8. Rozengurt N, Lopez I, Chiu CS, Kofuji P, Lester HA, Neusch C: Time course of inner ear degeneration and deafness in mice lacking the Kir4.1 potassium channel subunit. Hear Res 177: 71-80, 2003
9. Ito M, Inanobe A, Horio Y, Hibino H, Isomoto S, Ito H, Mori K, Tonosaki A, Tomoike H, Kurachi Y: Immunolocalization of an inwardly rectifying K+ channel, K(AB)-2 (Kir4.1), in the basolateral membrane of renal distal tubular epithelia. FEBS Lett 388: 11-15, 1996
10. Kofuji P, Ceelen P, Zahs KR, Surbeck LW, Lester HA, Newman EA: Genetic inactivation of an inwardly rectifying potassium channel (Kir4.1 subunit) in mice: Phenotypic impact in retina. J Neurosci 20: 5733-5740, 2000
11. Wu J, Marmorstein AD, Kofuji P, Peachey NS: Contribution of Kir4.1 to the mouse electroretinogram. Mol Vis 10: 650-654, 2004
12. Kucheryavykh YV, Kucheryavykh LY, Nichols CG, Maldonado HM, Baksi K, Reichenbach A, Skatchkov SN, Eaton MJ: Downregulation of Kir4.1 inward rectifying potassium channel subunits by RNAi impairs potassium transfer and glutamate uptake by cultured cortical astrocytes. Glia 55: 274-281, 2007
13. Neusch C, Rozengurt N, Jacobs RE, Lester HA, Kofuji P: Kir4.1 potassium channel subunit is crucial for oligodendrocyte development and in vivo myelination. J Neurosci 21: 5429-5438, 2001
14. Gitelman HJ, Graham JB, Welt LG: A new familial disorder characterized by hypokalemia and hypomagnesemia. Trans Assoc Am Physicians 79: 221-235, 1966
15. Reilly RF, Ellison DH: Mammalian distal tubule: physiology, pathophysiology, and molecular anatomy. Physiol Rev 80: 277-313, 2000
16. Glaudemans B, Knoers NV, Hoenderop JG, Bindels RJ: New molecular players facilitating Mg(2+) reabsorption in the distal convoluted tubule. Kidney Int 77: 17-22, 2010
17. Tucker SJ, Imbrici P, Salvatore L, D'Adamo MC, Pessia M: pH dependence of the inwardly rectifying potassium channel, Kir5.1, and localization in renal tubular epithelia. J Biol Chem 275: 16404-16407, 2000
18. Tanemoto M, Kittaka N, Inanobe A, Kurachi Y: In vivo formation of a proton-sensitive K+ channel by heteromeric subunit assembly of Kir5.1 with Kir4.1. J Physiol 525: 587-592, 2000
19. Lourdel S, Paulais M, Cluzeaud F, Bens M, Tanemoto M, Kurachi Y, Vandewalle A, Teulon J: An inward rectifier K(+) channel at the basolateral membrane of the mouse distal convoluted tubule: Similarities with Kir4-Kir5.1 heteromeric channels. J Physiol 538: 391-404, 2002
20. Tanemoto M, Abe T, Onogawa T, Ito S: PDZ binding motif-dependent localization of K+ channel on the basolateral side in distal tubules. Am J Physiol Renal Physiol 287: F1148-F1153, 2004
21. Gray DA, Frindt G, Zhang YY, Palmer LG: Basolateral K+ conductance in principal cells of rat CCD. Am J Physiol Renal Physiol 288: F493-F504, 2005
22. Lachheb S, Cluzeaud F, Bens M, Genete M, Hibino H, Lourdel S, Kurachi Y, Vandewalle A, Teulon J, Paulais M: Kir4.1/Kir5.1 channel forms the major K+ channel in the basolateral membrane of mouse renal collecting duct principal cells. Am J Physiol Renal Physiol 294: F1398-F1407, 2008
23. Rapedius M, Paynter JJ, Fowler PW, Shang L, Sansom MS, Tucker SJ, Baukrowitz T: Control of pH and PIP2 gating in heteromeric Kir4.1/ Kir5.1 channels by H-bonding at the helix-bundle crossing. Channels 1: 327-330, 2007
24. Pessia M, Imbrici P, D'Adamo MC, Salvatore L, Tucker SJ: Differential pH sensitivity of Kir4.1 and Kir4.2 potassium channels and their modulation by heteropolymerisation with Kir5.1. J Physiol 532: 359-367, 2001 (Pubitemid 32390394)
25. Rapedius M, Fowler PW, Shang L, Sansom MS, Tucker SJ, Baukrowitz T: H bonding at the helix-bundle crossing controls gating in Kir potassium channels. Neuron 55: 602-614, 2007
26. Hibino H, Fujita A, Iwai K, Yamada M, Kurachi Y: Differential assembly of inwardly rectifying K+ channel subunits, Kir4.1 and Kir5.1, in brain astrocytes. J Biol Chem 279: 44065-44073, 2004
27. Hibino H, Higashi-Shingai K, Fujita A, Iwai K, Ishii M, Kurachi Y: Expression of an inwardly rectifying K+ channel, Kir5.1, in specific types of fibrocytes in the cochlear lateral wall suggests its functional importance in the establishment of endocochlear potential. Eur J Neurosci 19: 76-84, 2004
28. Ishii M, Fujita A, Iwai K, Kusaka S, Higashi K, Inanobe A, Hibino H, Kurachi Y: Differential expression and distribution of Kir5.1 and Kir4.1 inwardly rectifying K+ channels in retina. Am J Physiol Cell Physiol 285: C260-C267, 2003
29. Pessia M, Tucker SJ, Lee K, Bond CT, Adelman JP: Subunit positional effects revealed by novel heteromeric inwardly rectifying K+ channels. EMBO J 15: 2980-2987, 1996
30. Tanemoto M, Fujita A, Higashi K, Kurachi Y: PSD-95 mediates formation of a functional homomeric Kir5.1 channel in the brain. Neuron 34: 387-397, 2002
31. Yang Z, Jiang C: Opposite effects of pH on open-state probability and single channel conductance of kir4.1 channels. J Physiol 520: 921-927, 1999
32. Choe H, Zhou H, Palmer LG, Sackin H: A conserved cytoplasmic region of ROMK modulates pH sensitivity, conductance, and gating. Am J Physiol 273: F516-F529, 1997
33. Bidet M, Tauc M, Gastineau M, Poujeol P: Effect of calcitonin on the regulation of intracellular pH in primary cultures of rabbit early distal tubule. Pflugers Arch 421: 523-529, 1992
34. Dagher G, Thomas SR, Griffiths N, Siaume-Perez S, Sauterey C: Calcitonin activates an Na(+)-independent HCO3(-)-dependent pathway in the rabbit distal convoluted tubule. Am J Physiol 273: F97-F103, 1997 (Pubitemid 27382177)
35. Orloff J, Kennedy TJ, Jr, Berliner RW: The effect of potassium in nephrectomized rats with hypokalemic alkalosis. J Clin Invest 32: 538-542, 1953
36. Rose BD, Post TW: Potassium Homeostasis: Clinical Physiology of Acid-Base and Electrolyte Disorders, Fifth Ed., New York, McGraw-Hill Co., Inc., 2001, pp 372-402
37. Reichold M, Zdebik AA, Lieberer E, Rapedius M, Schmidt K, Bandulik S, Sterner C, Tegtmeier I, Penton D, Baukrowitz T, Hulton SA, Witzgall R, Ben-Zeev B, Howie AJ, Kleta R, Bockenhauer D, Warth R: KCNJ10 gene mutations causing EAST syndrome (epilepsy, ataxia, sensorineural deafness, and tubulopathy) disrupt channel function. Proc Natl Acad Sci U.S.A. 107: 14490-14495, 2010
38. Tang X, Hang D, Sand A, Kofuji P: Variable loss of Kir4.1 channel function in SeSAME syndrome mutations. Biochem Biophys Res Commun 399: 537-541, 2010
39. Weber YG, Lerche H: Genetic mechanisms in idiopathic epilepsies. Dev Med Child Neurol 50: 648-654, 2008
40. Yang T, Gurrola JG, 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
41. Ji W, Foo JN, O'Roak BJ, Zhao H, Larson MG, Simon DB, Newton- Cheh C, State MW, Levy D, Lifton RP: Rare independent mutations in renal salt handling genes contribute to blood pressure variation. Nat Genet 40: 592-599, 2008
42. Nishida M, Cadene M, Chait BT, MacKinnon R: Crystal structure of a Kir3.1-prokaryotic Kir channel chimera. EMBO J 26: 4005-4015, 2007
43. Schulte U, Hahn H, Konrad M, Jeck N, Derst C, Wild K, Weidemann S, Ruppersberg JP, Fakler B, Ludwig J: pH gating of ROMK (K(ir)1.1) channels: Control by an Arg-Lys-Arg triad disrupted in antenatal Bartter syndrome. Proc Natl Acad Sci U.S.A. 96: 15298-15303, 1999
44. Lopes CM, Zhang H, Rohacs T, Jin T, Yang J, Logothetis DE: Alterations in conserved Kir channel-PIP2 interactions underlie channelopathies. Neuron 34: 933-944, 2002
45. Shyng SL, Cukras CA, Harwood J, Nichols CG: Structural determinants of PIP(2) regulation of inward rectifier K(ATP) channels. J Gen Physiol 116: 599-608, 2000
46. Rapedius M, Haider S, Browne KF, Shang L, Sansom MS, Baukrowitz T, Tucker SJ: Structural and functional analysis of the putative pH sensor in the Kir1.1 (ROMK) potassium channel. EMBO Rep 7: 611-616, 2006
47. Gibor G, Yakubovich D, Rosenhouse-Dantsker A, Peretz A, Schottelndreier H, Seebohm G, Dascal N, Logothetis DE, Paas Y, Attali B: An inactivation gate in the selectivity filter of KCNQ1 potassium channels. Biophys J 93: 4159-4172, 2007
48. Schulte U, Hahn H, Wiesinger H, Ruppersberg JP, Fakler B: pH-dependent gating of ROMK (Kir1.1) channels involves conformational changes in both N and C termini. J Biol Chem 273: 34575-34579, 1998
49. Cho HC, Tsushima RG, Nguyen TT, Guy HR, Backx PH: Two critical cysteine residues implicated in disulfide bond formation and proper folding of Kir2.1. Biochemistry 39: 4649-4657, 2000
50. Tanemoto M, Abe T, Ito S: PDZ-binding and di-hydrophobic motifs regulate distribution of Kir4.1 channels in renal cells. J Am Soc Nephrol 16: 2608-2614, 2005
51. Liman ER, Tytgat J, Hess P: Subunit stoichiometry of a mammalian K+ channel determined by construction of multimeric cDNAs. Neuron 9: 861-871, 1992
52. Zhang YY, Robertson JL, Gray DA, Palmer LG: Carboxy-terminal determinants of conductance in inward-rectifier K channels. J Gen Physiol 124: 729-739, 2004
53. Hoover RS, Poch E, Monroy A, Vazquez N, Nishio T, Gamba G, Hebert SC: N-Glycosylation at two sites critically alters thiazide binding and activity of the rat thiazide-sensitive Na(+):Cl(-) cotransporter. J AmSoc Nephrol 14: 271-282, 2003 (Pubitemid 36150849)
54. Armstrong CM, Gilly WF: Access resistance and space clamp problems associated with whole-cell patch clamping. Methods Enzymol 207: 100-122, 1992
55. Nagel G: CFTR, investigated with the two-electrode voltage-clamp technique: The importance of knowing the series resistance. J Cyst Fibros 3[Suppl 2]: 109-111, 2004
56. Brooks BR: CHARMM: A program for macromolecular energy, minimization, and dynamics calculations. J Comp Chem 4: 187-217, 1983