Lovastatin-induced phosphatidylinositol-4-phosphate 5-kinase diffusion from microvilli stimulates ROMK channels

Journal of the American Society of Nephrology

Volumn 26, Issue 7, 2015, Pages 1576-1587

  Liu, Bing Chen ^a,b   Yang, Li Li ^a,b   Lu, Xiao Yu ^a,b   Song, Xiang ^a,b   Li, Xue Chen ^b   Chen, Guangping ^b   Li, Yichao ^c   Yao, Xincheng ^c   Humphrey, Donald R ^b   Eaton, Douglas C ^b   Shen, Bao Zhong ^a   Ma, He Ping ^b  

^a HARBIN MEDICAL UNIVERSITY   (China)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c and Radiation Oncology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; MEVINOLIN; PHOSPHATIDYLINOSITOL 4 PHOSPHATE KINASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; POTASSIUM CHANNEL; RENAL OUTER MEDULLARY POTASSIUM CHANNEL; UNCLASSIFIED DRUG; CYCLOSPORIN DERIVATIVE; INWARDLY RECTIFYING POTASSIUM CHANNEL; KCNJ1 PROTEIN, MOUSE; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; KIDNEY CELL; KIDNEY COLLECTING TUBULE; LIPID RAFT; MICROVILLUS; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; WESTERN BLOTTING; ANALYSIS OF VARIANCE; ANIMAL; ANIMAL MODEL; CELL CULTURE; CELL MEMBRANE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROCEDURES; REAL TIME POLYMERASE CHAIN REACTION; REFERENCE VALUE; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION; ULTRASTRUCTURE;

ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; CELL MEMBRANE; CELLS, CULTURED; CHOLESTEROL; CYCLOSPORINS; GENE EXPRESSION REGULATION; KIDNEY TUBULES, COLLECTING; LOVASTATIN; MICE; MICROSCOPY, CONFOCAL; MICROVILLI; MODELS, ANIMAL; POTASSIUM CHANNELS, INWARDLY RECTIFYING; REAL-TIME POLYMERASE CHAIN REACTION; REFERENCE VALUES; RNA, SMALL INTERFERING; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION;

EID: 84934758709     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2013121326     Document Type: Article

References (45)

1. Bichet D, Haass FA, Jan LY: Merging functional studies with structures of inward-rectifier K(+) channels. Nat Rev Neurosci 4: 957-967, 2003
2. MinorDL Jr.,Masseling SJ, Jan YN, Jan LY: Transmembrane structure of an inwardly rectifying potassium channel. Cell 96: 879-891, 1999
3. Tinker A, Jan YN, Jan LY: Regions responsible for the assembly of inwardly rectifying potassium channels. Cell 87: 857-868, 1996
4. Yang J, Jan YN, Jan LY: Determination of the subunit stoichiometry of an inwardly rectifying potassiumchannel. Neuron 15: 1441-1447, 1995
5. Yang J, Jan YN, Jan LY: Control of rectification and permeation by residues in two distinct domains in an inward rectifier K+ channel. Neuron 14: 1047-1054, 1995
6. Kubo Y, Baldwin TJ, Jan YN, Jan LY: Primary structure and functional expression of a mouse inward rectifier potassium channel. Nature 362: 127-133, 1993
7. BoimMA,Ho K, ShuckME, BienkowskiMJ, Block JH, SlightomJL, Yang Y, Brenner BM, Hebert SC: ROMK inwardly rectifying ATP-sensitive K+ channel. II. Cloning and distribution of alternative forms. Am J Physiol 268: F1132-F1140, 1995
8. Lee WS, Hebert SC: ROMK inwardly rectifying ATP-sensitive K+ channel. I. Expression in rat distal nephron segments. Am J Physiol 268: F1124-F1131, 1995
9. LuM,Wang T, YanQ, Yang X,Dong K, KnepperMA,WangW,Giebisch G, Shull GE, Hebert SC: Absence of small conductance K+ channel (SK) activity in apical membranes of thick ascending limb and cortical collecting duct in ROMK (Bartter's) knockout mice. J Biol Chem 277: 37881-37887, 2002
10. Zhang Y, Lin DH, Wang ZJ, Jin Y, Yang B, Wang WH: K restriction inhibits protein phosphatase 2B (PP2B) and suppression of PP2B decreases ROMK channel activity in the CCD. Am J Physiol Cell Physiol 294: C765-C773, 2008
11. Ling BN, Eaton DC: Cyclosporin A inhibits apical secretory K+ channels in rabbit cortical collecting tubule principal cells. Kidney Int 44: 974-984, 1993
12. Wang J, Zhang ZR, Chou CF, Liang YY, Gu Y, Ma HP: Cyclosporine stimulates the renal epithelial sodiumchannel by elevating cholesterol. Am J Physiol Renal Physiol 296: F284-F290, 2009
13. Rosenhouse-Dantsker A, Noskov S, Han H, Adney SK, Tang QY, Rodríguez-Menchaca AA, Kowalsky GB, Petrou VI, Osborn CV, Logothetis DE, Levitan I: Distant cytosolic residues mediate a two-way molecular switch that controls the modulation of inwardly rectifying potassium (Kir) channels by cholesterol and phosphatidylinositol 4,5-bisphosphate (PI(4,5)P(2)). J Biol Chem287: 40266-40278, 2012
14. Singh DK, Shentu TP, Enkvetchakul D, Levitan I: Cholesterol regulates prokaryotic Kir channel by direct binding to channel protein. Biochim Biophys Acta 1808: 2527-2533, 2011
15. Singh DK, Rosenhouse-Dantsker A, Nichols CG, Enkvetchakul D, Levitan I: Direct regulation of prokaryotic Kir channel by cholesterol. J Biol Chem 284: 30727-30736, 2009
16. Rosenhouse-Dantsker A, Leal-Pinto E, Logothetis DE, Levitan I: Comparative analysis of cholesterol sensitivity of Kir channels: Role of the CD loop. Channels (Austin) 4: 63-66, 2010
17. Liu BC, Song X, Lu XY, Fang CZ,Wei SP, Alli AA, Eaton DC, Shen BZ, Li XQ, Ma HP: Lovastatin attenuates effects of cyclosporine A on tight junctions and apoptosis in cultured cortical collecting duct principal cells. Am J Physiol Renal Physiol 305: F304-F313, 2013
18. Simons K, Ikonen E: Functional rafts in cell membranes. Nature 387: 569-572, 1997
19. Huang CL, Feng S, Hilgemann DW: Direct activation of inward rectifier potassium channels by PIP2 and its stabilization by Gbetagamma. Nature 391: 803-806, 1998
20. Baukrowitz T, Schulte U, Oliver D, Herlitze S, Krauter T, Tucker SJ, Ruppersberg JP, Fakler B: PIP2 and PIP as determinants for ATP inhibition of KATP channels. Science 282: 1141-1144, 1998
21. Shyng SL, Nichols CG: Membrane phospholipid control of nucleotide sensitivity of KATP channels. Science 282: 1138-1141, 1998
22. Rosenhouse-Dantsker A, Logothetis DE: Molecular characteristics of phosphoinositide binding. Pflugers Arch 455: 45-53, 2007
23. Koushik AB, Powell RR, Temesvari LA: Localization of phosphatidylinositol 4,5-bisphosphate to lipid rafts and uroids in the human protozoan parasite Entamoeba histolytica. Infect Immun 81: 2145-2155, 2013
24. Pike LJ, Miller JM: Cholesterol depletion delocalizes phosphatidylinositol bisphosphate and inhibits hormone-stimulated phosphatidylinositol turnover. J Biol Chem 273: 22298-22304, 1998
25. Wade JB, Fang L, Coleman RA, Liu J, Grimm PR, Wang T, Welling PA: Differential regulation of ROMK (Kir1.1) in distal nephron segments by dietary potassium. AmJ Physiol Renal Physiol 300: F1385-F1393, 2011
26. Bao HF, Thai TL, Yue Q, Ma HP, Eaton AF, Cai H, Klein JD, Sands JM, Eaton DC: ENaC activity is increased in isolated, split-open cortical collecting ducts from protein kinase Ca knockout mice. Am J Physiol Renal Physiol 306: F309-F320, 2014
27. Lu M, Hebert SC, Giebisch G: Hydrolyzable ATP and PIP(2) modulate the small-conductance K+ channel in apical membranes of rat corticalcollecting duct (CCD). J Gen Physiol 120: 603-615, 2002
28. Wang W, Lerea KM, Chan M, Giebisch G: Protein tyrosine kinase regulates the number of renal secretory K channels. Am J Physiol Renal Physiol 278: F165-F171, 2000
29. Lingwood D, Simons K: Lipid rafts as a membrane-organizing principle. Science 327: 46-50, 2010
30. Janich P, Corbeil D: GM1 and GM3 gangliosides highlight distinct lipid microdomains within the apical domain of epithelial cells. FEBS Lett 581: 1783-1787, 2007
31. Marzesco AM, Wilsch-Bräuninger M, Dubreuil V, Janich P, Langenfeld K, Thiele C, HuttnerWB, Corbeil D: Release of extracellular membrane vesicles from microvilli of epithelial cells is enhanced by depleting membrane cholesterol. FEBS Lett 583: 897-902, 2009
32. Vasudevan L, Jeromin A, Volpicelli-Daley L, De Camilli P, Holowka D, Baird B: The beta-and gamma-isoforms of type I PIP5K regulate distinct stages of Ca2+ signaling in mast cells. J Cell Sci 122: 2567-2574, 2009
33. Liou HH, Zhou SS, Huang CL: Regulation of ROMK1 channel by protein kinase A via a phosphatidylinositol 4,5-bisphosphate-dependent mechanism. Proc Natl Acad Sci U S A 96: 5820-5825, 1999
34. Balut C, Steels P, Radu M, Ameloot M, Driessche WV, Jans D: Membrane cholesterol extraction decreases Na+ transport in A6 renal epithelia. Am J Physiol Cell Physiol 290: C87-C94, 2006
35. Wei SP, Li XQ, Chou CF, Liang YY, Peng JB, Warnock DG, Ma HP: Membrane tension modulates the effects of apical cholesterol on the renal epithelial sodium channel. J Membr Biol 220: 21-31, 2007
36. Pochynyuk O, Tong Q, Medina J, Vandewalle A, Staruschenko A, Bugaj V, Stockand JD: Molecular determinants of PI(4,5)P2 and PI(3,4,5)P3 regulation of the epithelial Na+ channel. J Gen Physiol 130: 399-413, 2007
37. Yue G, Malik B, Yue G, Eaton DC: Phosphatidylinositol 4,5-bisphosphate (PIP2) stimulates epithelial sodium channel activity in A6 cells. J Biol Chem 277: 11965-11969, 2002
38. Ma HP, Saxena S, Warnock DG: Anionic phospholipids regulate native and expressed epithelial sodium channel (ENaC). J Biol Chem 277: 7641-7644, 2002
39. Smith PR, Bradford AL, Schneider S, Benos DJ, Geibel JP: Localization of amiloride-sensitive sodium channels in A6 cells by atomic force microscopy. Am J Physiol 272: C1295-C1298, 1997
40. Fang L, Li D, Welling PA: Hypertension resistance polymorphisms in ROMK (Kir1.1) alter channel function by different mechanisms. Am J Physiol Renal Physiol 299: F1359-F1364, 2010
41. BensM, Vallet V, Cluzeaud F, Pascual-Letallec L, Kahn A, Rafestin-Oblin ME, Rossier BC, Vandewalle A: Corticosteroid-dependent sodium transport in a novel immortalized mouse collecting duct principal cell line. J AmSoc Nephrol 10: 923-934, 1999
42. HelmsMN, Liu L, Liang YY, Al-Khalili O, Vandewalle A, Saxena S, Eaton DC, Ma HP: Phosphatidylinositol 3,4,5-trisphosphate mediates aldosterone stimulation of epithelial sodium channel (ENaC) and interacts with gamma-ENaC. J Biol Chem280: 40885-40891, 2005
43. Ma HP: Hydrogen peroxide stimulates the epithelial sodium channel through a phosphatidylinositide 3-kinase-dependent pathway. J Biol Chem 286: 32444-32453, 2011
44. ChenG,HoweAG, Xu G, Fröhlich O,Klein JD, Sands JM:Mature N-linked glycans facilitate UT-A1 urea transporter lipid raft compartmentalization. FASEB J 25: 4531-4539, 2011
45. Liu BC, Lu XY, Song X, Lei KY, Alli AA,Bao HF, Eaton DC, Ma HP: Scanning ion conductance microscopy: A nanotechnology for biological studies in live cells. Front Physiol 3: 483, 2012