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Regulation of potassium (K) handling in the renal collecting duct

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Abstract

This review provides an overview of the molecular mechanisms of K transport in the mammalian connecting tubule (CNT) and cortical collecting duct (CCD), both nephron segments responsible for the regulation of renal K secretion. Aldosterone and dietary K intake are two of the most important factors regulating K secretion in the CNT and CCD. Recently, angiotensin II (AngII) has also been shown to play a role in the regulation of K secretion. In addition, genetic and molecular biological approaches have further identified new mechanisms by which aldosterone and dietary K intake regulate K transport. Thus, the interaction between serum-glucocorticoid-induced kinase 1 (SGK1) and with-no-lysine kinase 4 (WNK4) plays a significant role in mediating the effect of aldosterone on ROMK (Kir1.1), an important apical K channel modulating K secretion. Recent evidence suggests that WNK1, mitogen-activated protein kinases such as P38, ERK, and Src family protein tyrosine kinase are involved in mediating the effect of low K intake on apical K secretory channels.

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References

  1. Ali S, Chen X, Lu M, Xu J-C, Lerea KM, Hebert SC, Wang W (1998) A kinase anchoring protein (AKAP) is required for mediating the effect of PKA on ROMK1. Proc Natl Acad Sci U S A 95:10274–10278

    PubMed  CAS  Google Scholar 

  2. Amorim JB, Bailey MA, Musa-Aziz R, Giebisch G, Malnic G (2003) Role of luminal anion and pH in distal tubule potassium secretion. Am J Physiol Renal Physiol 284:F381–F388

    PubMed  CAS  Google Scholar 

  3. Amorim JBO, Malnic G (2000) V1 receptors in luminal action of vasopressin on distal K+ secretion. AJP–Renal Physiol 278:F809–F816

    CAS  Google Scholar 

  4. Amorim JBO, Musa-Aziz R, Mello-Aires M, Malnic G (2004) Signaling path of the action of AVP on distal K+ secretion. Kidney Int 66:696–704

    PubMed  CAS  Google Scholar 

  5. Amorim JBO, Musa-Aziz R, Lessa LMA, Malnic G, Fonteles MC (2006) Effect of uroguanylin on potassium and bicarbonate transport in rat renal tubules. Can J Physiol Pharmacol 84:1003

    PubMed  CAS  Google Scholar 

  6. Armitage FE, Wingo CS (1994) Luminal acidification in K-replete OMCDi: contributions of H-K-ATPase and bafilomycin-A1-sensitive H-ATPase. Am J Physiol 267:F450–F458

    PubMed  CAS  Google Scholar 

  7. Babilonia E, Li D, Wang ZJ, Sun P, Lin DH, Wang WH (2006) Mitogen-activated protein kinase (MAPK) inhibits ROMK-like small conductance K channels in the CCD of K-restricted rats. J Am Soc Nephrol 17:2687–2696

    PubMed  CAS  Google Scholar 

  8. Babilonia E, Lin D, Zhang Y, Wei Y, Yue P, Wang WH (2007) Role of gp91phox-containing NADPH oxidase in mediating the effect of K restriction on ROMK channels and renal K excretion. J Am Soc Nephrol 18:2037–2045

    PubMed  CAS  Google Scholar 

  9. Bailey MA, Cantone A, Yan QS, MacGregor GG, Leng Q, Amorim JB, Wang T, Hebert SC, Giebisch G, Malnic G (2006) Maxi-K channels contribute to urinary potassium excretion in the ROMK-deficient mouse model of type II Bartter’s syndrome and in adaptation to a high K diet. Kidney Int 70:51–59

    PubMed  CAS  Google Scholar 

  10. Beck F-X, Dorge A, Giebisch G, Thurau K (1990) Effect of diuretics on cell potassium transport: an electron microprobe study. Kidney Int 37:1423–1428

    PubMed  CAS  Google Scholar 

  11. Berger S, Bleich M, Schmid W, Cole TJ, Peters J, Watanabe H, Kriz W, Warth R, Greger R, Schutz G (1998) Mineralocorticoid receptor knockout mice: pathophysiology of Na+ metabolism. Proc Natl Acad Sci 95:9424–9429

    PubMed  CAS  Google Scholar 

  12. Buffin-Meyer B, Younes-Ibrahim M, Barlet-Bas C, Cheval L, Marsy S, Doucet A (1997) K depletion modifies the properties of Sch-28080-sensitive K-ATPase in rat collecting duct. Am J Physiol 272:F124–F131

    PubMed  CAS  Google Scholar 

  13. Cassola AC, Giebisch G, Wang W (1993) Vasopressin increases density of apical low-conductance K+ channels in rat CCD. Am J Physiol 264:F502–F509

    PubMed  CAS  Google Scholar 

  14. Choe H, Zhou H, Palmer LG, Sackin H (1997) A conserved cytoplasmic region of ROMK modulates pH sensitivity, conductance, and gating. Am J Physiol 273:F516–F529

    PubMed  CAS  Google Scholar 

  15. Codina J, Wall SM, DuBose TD Jr. (1999) Contrasting functional and regulatory profiles of the renal H+,K+-ATPases. Sems Nephrol 19:399–404

    CAS  Google Scholar 

  16. Cope G, Murthy M, Golbang AP, Hamad A, Liu CH, Cuthbert AW, O’Shaughnessy KM (2006) WNK1 affects surface expression of the ROMK potassium channel independent of WNK4. J Am Soc Nephrol 17:1867–1874

    PubMed  CAS  Google Scholar 

  17. Dherbecourt O, Cheval L, Bloch-Faure M, Meneton P, Doucet A (2006) Molecular identification of Sch28080-sensitive K-ATPase activities in the mouse kidney. Pflugers Arch 451:769–775

    PubMed  CAS  Google Scholar 

  18. Dong K, Xu J, Vanoye CG, Welch R, MacGregor GG, Giebisch G, Hebert SC (2001) An amino acid triplet in the NH2 terminus of rat ROMK1 determines interation with SUR2B. J Biol Chem 276:44347–44353

    PubMed  CAS  Google Scholar 

  19. Doucet A, Marsy S (1987) Characterization of K-ATPase activity in distal nephron: stimulation by potassium depletion. Am J Physiol 253:F418–F423

    PubMed  CAS  Google Scholar 

  20. Doyle DA, Cabral JM, Pfuetzner RA, Kuo A, Gulbis JM, Cohen SL, Chait BT, MacKinnon R (1998) The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280:69–77

    PubMed  CAS  Google Scholar 

  21. DuBose TD Jr, Gitomer J, Codina J (1999) H+,K+-ATPase. Curr Opin Nephrol Hypertens 8:597–602

    PubMed  Google Scholar 

  22. Ellison DH, Velazquez H, Wright FS (1985) Stimulation of distal potassium secretion by low lumen chloride in the presence of barium. Am J Physiol 248:638–649

    Google Scholar 

  23. Estilo G, Liu W, Pastor-Soler N, Mitchell P, Carattino MD, Kleyman TR, Satlin LM (2008) Effect of aldosterone on BK channel expression in mammalian cortical collecting duct. AJP–Renal Physiol 295:F780–F788

    CAS  Google Scholar 

  24. Eric F, Davi M, Sand G, Geor D, Manl V, Alai D, Alai V, Vane S, Fran V, Martin PY (2003) Mechanism of control of Na,K-ATPase in principal cells of the mammalian collecting duct. Ann NY Acad Sci 986:570–578

    Google Scholar 

  25. Frindt G, Palmer LG (1987) Ca-activated K channels in apical membrane of mammalian CCT, and their role in K secretion. Am J Physiol (Renal Fluid Electrolyte Physiol) 252–221:F458–F467

    Google Scholar 

  26. Frindt G, Palmer LG (1989) Low-conductance K channels in apical membrane of rat cortical collecting tubule. Am J Physiol (Renal Fluid Electrolyte Physiol) 256–225:F143–F151

    Google Scholar 

  27. Frindt G, Palmer LG (2004) Apical potassium channels in the rat connecting tubule. Am J Physiol Renal Physiol 287:F1030–F1037

    PubMed  CAS  Google Scholar 

  28. Garg LC (1991) Respective role of H-ATPase and H–K-ATPase in ion transport in the kidney. JASN 2(5):949–960

    PubMed  CAS  Google Scholar 

  29. Giebisch G (1998) Renal potassium transport: mechanisms and regulation. Am J Physiol 274:F817–F833

    PubMed  CAS  Google Scholar 

  30. Giebisch G, Hebert SC, Wang WH (2003) New aspects of renal potassium transport. Pflugers Arch 446:289–297

    PubMed  CAS  Google Scholar 

  31. Gray DA, Frindt G, Palmer LG (2005) Quantification of K+ secretion through apical low-conductance K channels in the CCD. Am J Physiol Renal Physiol 289:F117–F126

    PubMed  CAS  Google Scholar 

  32. Gray DA, Frindt G, Zhang YY, Palmer LG (2005) Basolateral K+ conductance in principal cells of rat CCD. Am J Physiol Renal Physiol 288:F493–F504

    PubMed  CAS  Google Scholar 

  33. Guntupalli J, Onuigbo M, Wall S, Alpern RJ, DuBose TD Jr (1997) Adaptation to low-K+ media increases H(+)–K(+)-ATPase but not H(+)-ATPase-mediated pHi recovery in OMCD1 cells. Am J Physiol 273:C558–C571

    PubMed  CAS  Google Scholar 

  34. He G, Wang HR, Huang SK, Huang C-L (2007) Intersectin links WNK kinase to endocytosis of ROMK1. J Clin Invest 117:1078–1087

    PubMed  CAS  Google Scholar 

  35. Hebert SC, Desir G, Giebisch G, Wang W (2005) Molecular diversity and regulation of renal potassium channels. Physiol Rev 85:319–371

    PubMed  CAS  Google Scholar 

  36. Hebert SC, Wang W-H (1997) Structure and function of the low conductance KATP channel, ROMK. Wien Klin Wochenschr 109:471–476

    PubMed  CAS  Google Scholar 

  37. Hirsch J, Schlatter E (1995) K+ channels in the basolateral membrane of rat cortical collecting duct. Kidney Int 48:1036–1046

    PubMed  CAS  Google Scholar 

  38. Ho K (1998) The ROMK-cystic fibrosis transmembrane conductance regulator connection: new insights into the relationship between ROMK and cystic fibrosis transmembrane conductance regulator channels. Curr Opin Nephrol Hypertens 7:49–58

    PubMed  CAS  Google Scholar 

  39. Horisberger J-D, Doucet A (2008) Renal ion-translocating ATPase: the P-type family. In: Alpern RJ, Hebert SC (eds) The kidney: physiology and pathophysiology. Elsevier, Amsterdam, pp 57–90

    Google Scholar 

  40. Huang C-L, Feng S, Hilgemann DW (1998) Direct activation of inward rectifier potassium channels by PIP2 and its stabilization by Gbg. Nature 391:803–806

    PubMed  CAS  Google Scholar 

  41. Huang DY, Wulff P, Volkl H, Loffing J, Richter K, Kuhl D, Lang F, Vallon V (2004) Impaired regulation of renal K+ elimination in the sgk1-knockout mouse. J Am Soc Nephrol 15:885–891

    PubMed  CAS  Google Scholar 

  42. Hunter M, Lopes AG, Boulpaep EL, Giebisch G (1984) Single channel recordings of calcium-activated potassium channels in the apical membrane of rabbit cortical collecting tubules. Proc Natl Acad Sci U S A 81:4237–4239

    PubMed  CAS  Google Scholar 

  43. Jin Y, Wang Z, Zhang Y, Yang B, Wang WH (2007) PGE2 inhibits apical K channels in the CCD through activation of the MAPK pathway. AJP–Renal Physiol 293:F1299–F1307

    CAS  Google Scholar 

  44. Kahle KT, Wilson FH, Leng Q, Lalioti MD, O’Connell AD, Dong K, Rapson AK, MacGregor GG, Giebisch G, Hebert SC, Lifton RP (2003) WNK4 regulates the balance between renal NaCl reabsorption and K+ secretion. Nat Genet 35:372–376

    PubMed  CAS  Google Scholar 

  45. Kahle KT, Gimenez I, Hassan H, Wilson FH, Wong RD, Forbush B, Aronson PS, Lifton RP (2004) WNK4 regulates apical and basolateral Cl-flux in extrarenal epithelia. Proc Natl Acad Sci 101:2064–2069

    PubMed  CAS  Google Scholar 

  46. Kahle KT, Ring AM, Lifton RP (2008) Molecular physiology of the WNK kinases. Annu Rev Physiol 70:329–355

    PubMed  CAS  Google Scholar 

  47. Kone BC (1996) Renal H,K-ATPase: structure, function and regulation. Miner Electrolyte Metab 22:349–365

    PubMed  CAS  Google Scholar 

  48. Lazrak A, Liu Z, Huang CL (2006) Antagonistic regulation of ROMK by long and kidney-specific WNK1 isoforms. Proc Natl Acad Sci 103:1615–1620

    PubMed  CAS  Google Scholar 

  49. Lee FN, Oh G, McDonough AA, Youn JH (2007) Evidence for gut factor in K+ homeostasis. AJP–Renal Physiol 293:F541–F547

    CAS  Google Scholar 

  50. Leng Q, Kahle KT, Rinehart J, MacGregor GG, Wilson FH, Canessa CM, Lifton RP, Hebert SC (2006) WNK3, a kinase related to genes mutated in hereditary hypertension with hyperkaelemia, regulates the K+ channel ROMK1 (Kir1.1). J Physiol 571:275–286

    PubMed  CAS  Google Scholar 

  51. Li DM, Wang ZJ, Sun P, Jin Y, Lin DH, Hebert SC, Giebisch G, Wang WH (2006) Inhibition of mitogen-activated protein kinase stimulates the Ca2+-dependent big conductance K channels (BK) in cortical collecting duct. Proc Natl Acad Sci U S A 103:19569–19574

    PubMed  CAS  Google Scholar 

  52. Liapis H, Nag M, Kaji DM (1998) K–Cl cotransporter expression in the human kidney. AJP–Cell Physiol 275:C1432–C1437

    CAS  Google Scholar 

  53. Lin DH, Sterling H, Lerea KM, Giebisch G, Wang WH (2002) Protein kinase C (PKC)-induced phosphorylation of ROMK1 is essential for the surface expression of ROMK1 channels. J Biol Chem 277:44332–44338

    Google Scholar 

  54. Lin DH, Sterling H, Lerea KM, Welling P, Jin L, Giebisch G, Wang WH (2002) K depletion increases the protein tyrosine-mediated phosphorylation of ROMK. Am J Physiol Renal Physiol 283:F671–F677

    PubMed  Google Scholar 

  55. Lin DH, Sterling H, Yang B, Hebert SC, Giebisch G, Wang WH (2004) Protein tyrosine kinase is expressed and regulates ROMK1 location in the cortical collecting duct. Am J Physiol Renal Physiol 286:F881–F892

    PubMed  CAS  Google Scholar 

  56. Ling BN, Hinton CF, Eaton DC (1991) Potassium permeable channels in primary cultures of rabbit cortical collecting tubule. Kidney Int 40:441–452

    PubMed  CAS  Google Scholar 

  57. Liou HH, Zhou SS, Huang CL (1999) 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

    PubMed  CAS  Google Scholar 

  58. Lu M, Hebert SC, Giebisch G (2002) Hydrolyzable ATP and PIP2 modulate the small-conductance K channel in apical membrane of rat cortical collecting duct. J Gen Physiol 120:603–615

    PubMed  CAS  Google Scholar 

  59. Lu M, Leng Q, Egan ME, Caplan MJ, Boulpaep E, Giebisch G, Hebert SC (2006) CFTR is required for PKA-regulated ATP sensitivity of Kir1.1 potassium channels in mouse kidney. J Clin Invest 116:797–806

    PubMed  CAS  Google Scholar 

  60. Lu R, Alioua A, Kumar Y, Eghbali M, Stefani E, Toro L (2006) MaxiK channel partners: physiological impact. J Physiol 570:65–72

    PubMed  CAS  Google Scholar 

  61. Ma J, Qu W, Scarborough PE, Tomer KB, Moomaw CR, Maronpot R, Davis LS, Breyer MD, Zeldin DC (1999) Molecular cloning, enzymatic characterization, developmental expression, and cellular localization of a mouse cytochrome P450 highly expressed in kidney. J Biol Chem 274:17777–17788

    PubMed  CAS  Google Scholar 

  62. Marsy S, Elalouf J-M, Doucet A (1996) Quantitative RT-PCR analysis of mRNA encoding a colonic H,K-ATPase alpha subunit along the rat nephron: effect of K+ depletion. Pflugers Arch 432:494–500

    PubMed  CAS  Google Scholar 

  63. McNicholas CM, Nason MW, Guggino WB, Schwiebert EM, Hebert S, Giebisch G, Egan ME (1997) The functional CFTR-NBF1 is required for ROMK2-CFTR interaction. Am J Physiol 273:F843–F848

    PubMed  CAS  Google Scholar 

  64. McNicholas CM, Wang W, Ho K, Hebert SC, Giebisch G (1994) Regulation of ROMK1 K+ channel activity involves phosphorylation processes. Proc Natl Acad Sci U S A 91:8077–8081

    PubMed  CAS  Google Scholar 

  65. Meneton P, Schultheis PJ, Greeb J, Nieman ML, Liu LH, Clarke LL, Duffy JJ, Doetschman T, Lorenz JN, Shull GE (1998) Increased sensitivity to K+ deprivation in colonic H,K-ATPase-deficient mice. J Clin Invest 101:536–542

    PubMed  CAS  Google Scholar 

  66. Minor DL, Masseling SJ, Jan YN, Jan LY (1999) Transmembrane structure of an inwardly rectifying potassium channel. Cell 97:879–891

    Google Scholar 

  67. Moral Z, Deng K, Wei Y, Sterling H, Deng H, Ali S, Gu RM, Huang XY, Hebert SC, Giebisch G, Wang WH (2001) Regulation of ROMK1 channels by protein tyrosine kinase and tyrosine phosphatase. J Biol Chem 276:7156–7163

    PubMed  CAS  Google Scholar 

  68. Muto S, Sansom S, Giebisch G (1988) Effects of a high potassium diet on electrical properties of cortical collecting duct from adrenalectomized rabbits. J Clin Invest 81:376–380

    PubMed  CAS  Google Scholar 

  69. Muto S, Tsuruoka S, Miyata Y, Fujimura A, Kusano E, Wang WH, Seldin D, Giebing G (2008) Basolateral Na+/H+ exchange is involved in maintaining K+ secretion during diminished Na+ transport in rabbit CCD. Kid Int. doi:10.1038/ki.2008.447

  70. Najjar F, Zhou H, Morimoto T, Bruns JB, Li HS, Liu W, Kleyman TR, Satlin LM (2005) Dietary K+ regulates apical membrane expression of maxi-K channels in rabbit cortical collecting duct. Am J Physiol Renal Physiol 289:F922–F932

    PubMed  CAS  Google Scholar 

  71. Nakagawa K, Holla VR, Wei Y, Wang WH, Gatica A, Wei S, Mei S, Miller CM, Cha DR, Price EJ, Zent R, Pozzi A, Breyer MD, Guan Y, Falck JR, Waterman MR, Capdevila JH (2006) Salt sensitive hypertension is associated with a dysfunctional Cyp4a10 gene and kidney epithelial sodium channel. J Clin Invest 116:1696–1702

    PubMed  CAS  Google Scholar 

  72. Nichols CG, Lopatin AN (1997) Inward rectifier potassium channels. Ann Rev Physiol 59:171–191

    CAS  Google Scholar 

  73. O’Connell AD, Leng Q, Dong K, MacGregor GG, Giebisch G, Hebert SC (2005) Phosphorylation-regulated endoplasmic reticulum retention signal in the renal outer-medullary K+ channel (ROMK). Proc Natl Acad Sci 102:9954–9959

    PubMed  Google Scholar 

  74. O’Neil RG (1981) Potassium secretion by the cortical collecting tubule. Federation Proc 40:2403–2407

    Google Scholar 

  75. O’Neil RG, Hayhurst AR (1985) Functional differentiation of cell types of cortical collecting duct. Am J Physiol 248:449–453

    Google Scholar 

  76. O’Neil RG, Sansom SC (1984) Characterization of apical cell membrane Na+ and K+ conductances of cortical collecting duct using microelectrode techniques. Am J Physiol 247(Renal 16):F14–F24

    PubMed  Google Scholar 

  77. O’Reilly M, Marshall E, Speirs HJL, Brown RW (2003) WNK1, a gene within a novel blood pressure control pathway, tissue-specifically generates radically different isoforms with and without a kinase domain. J Am Soc Nephrol 14:2447–2456

    PubMed  Google Scholar 

  78. Orias M, Velazquez H, Tung F, Lee G, Desir GV (1997) Cloning and localization of a double-pore K channel, KCNK1: exclusive expression in distal nephron segments. AJP–Renal Physiol 273:F663–F666

    CAS  Google Scholar 

  79. Palmer LG (1999) Potassium secretion and the regulation of distal nephron K channels. Am J Physiol 277:F821–F825

    PubMed  CAS  Google Scholar 

  80. Palmer LG, Antonian L, Frindt G (1993) Regulation of the Na–K pump of the rat cortical collecting tubule by aldosterone. J Gen Physiol 102:43–57

    PubMed  CAS  Google Scholar 

  81. Palmer LG, Antonian L, Frindt G (1994) Regulation of apical K and Na channels and Na/K pumps in rat cortical collecting tubule by dietary K. J Gen Physiol 104:693–710

    PubMed  CAS  Google Scholar 

  82. Palmer LG, Frindt G (1992) Regulation of apical membrane Na and K channels in rat renal collecting tubules by aldosterone. Sems Nephrol 12:37–43

    CAS  Google Scholar 

  83. Palmer LG, Frindt G (1999) Regulation of apical K channels in rat cortical collecting tubule during changes in dietary K intake. Am J Physiol 277:F805–F812

    PubMed  CAS  Google Scholar 

  84. Palmer LG, Frindt G (2007) High-conductance K channels in intercalated cells of the rat distal nephron. AJP–Renal Physiol 292:F966–F973

    CAS  Google Scholar 

  85. Rapedius M, Haider S, Browner KF, Shang L, Sanson MSP, Baukroitz T, Tucker SJ (2006) Structural and functional analysis of the putative pH sensor in the Kir1.1 (ROMK) potassium channel. EMBO Rep 7:611–616

    PubMed  CAS  Google Scholar 

  86. Ray PE, Suga SI, Liu XH, Huang X, Johnson RJ (2001) Chronic potassium depletion induces renal injury, salt sensitivity, and hypertension in young rats. Kidney Int 59:1850–1858

    PubMed  CAS  Google Scholar 

  87. Rieg T, Vallon V, Sausbier M, Sausbier U, Kaissling B, Ruth P, Osswald H (2007) The role of the BK channel in potassium homeostasis and flow-induced renal potassium excretion. Kidney Int 72:566–573

    PubMed  CAS  Google Scholar 

  88. Ring AM, Leng Q, Rinehart J, Wilson FH, Kahle KT, Hebert SC, Lifton RP (2007) An SGK1 site in WNK4 regulates Na+ channel and K+ channel activity and has implications for aldosterone signaling and K+ homeostasis. Proc Natl Acad Sci 104:4025–4029

    PubMed  CAS  Google Scholar 

  89. Rossier BC, Canessa CM, Schild L, Horisberger J-D (1994) Epithelial sodium channels. Curr Opin Nephrol Hyperten 3:487–496

    CAS  Google Scholar 

  90. Saikaley A, Bichet D, Kucharczyk J, Peterson LN (1986) Neuroendocrine factors mediating polydipsia induced by dietary Na, Cl, and K depletion. Am J Physiol Regul Integr Comp Physiol 251:R1071–R1077

    CAS  Google Scholar 

  91. Salkoff L, Butler A, Ferreira G, Santi C, Wei A (2006) High-conductance potassium channels of the SLO family. Nat Rev Neurosci 7:921–931

    PubMed  CAS  Google Scholar 

  92. Sansom SC, O’Neil RG (1986) Effects of mineralocorticoids on transport properties of the cortical collecting duct basolateral membrane. Am J Physiol 251:743–757

    Google Scholar 

  93. Satlin LM (1994) Postnatal maturation of potassium transport in rabbit cortical collecting duct. Am J Physiol 266:F57–F65

    PubMed  CAS  Google Scholar 

  94. Satlin LM (2004) Developmental regulation of expression of renal potassium secretory channels. Curr Opin Nephrol Hypertens 13:445–450

    PubMed  CAS  Google Scholar 

  95. Satlin LM, Palmer LG (1997) Apical K+ conductance in maturing rabbit principal cell. Am J Physiol 272:F397–F404

    PubMed  CAS  Google Scholar 

  96. Schafer JA, Troutman SL (1987) Potassium transport in cortical collecting tubules from mineralocorticoid-treated rat. Am J Physiol (Renal Fluid Electrolyte Physiol) 253:F76–F88

    CAS  Google Scholar 

  97. Schafer JA, Troutman SL, Schlatter E (1990) Vasopressin and mineralocorticoid increase apical membrane driving force for K+ secretion in rat CCD. Am J Physiol 258:F199–F210

    PubMed  CAS  Google Scholar 

  98. Schlatter E (1993) Regulation of ion channels in the cortical collecting duct. Renal Physiol Biochem 16:21–36

    PubMed  CAS  Google Scholar 

  99. Schlatter E, Haxelmans S, Hirsch J, Leipziger J (1994) pH dependence of K+ conductances of rat cortical collecting duct principal cells. Pflugers Archiv 428:631–640

    PubMed  CAS  Google Scholar 

  100. Schlatter E, Lohrmann E, Greger R (1992) Properties of the potassium conductances of principal cells of rat cortical collecting ducts. Pflugers Arch 420:39–45

    PubMed  CAS  Google Scholar 

  101. Schlatter E, Schafer JA (1987) Electrophysiological studies in principal cells of rat cortical collecting tubules. Pflugers Arch 409:81–92

    PubMed  CAS  Google Scholar 

  102. Sealey JE, Clark I, Bull MB, Laragh JH (1970) Potassium balance and the control of renin secretion. J Clin Invest 49:2119–2127

    PubMed  CAS  Google Scholar 

  103. Silver RB, Soleimani M (1999) H–K-ATPase regulation and role in pathophysiological states. Am J Physiol Renal Physiol 276:F799–F811

    CAS  Google Scholar 

  104. Sindic A, Hirsch JR, Velic A, Piechota H, Schlatter E (2005) Guanylin and uroguanylin regulate electrolyte transport in isolated human cortical collecting ducts. Kidney Int 67:1420–1427

    PubMed  CAS  Google Scholar 

  105. Sindic A, Velic A, Basoglu C, Hirsch JR, Edemir B, Kuhn M, Schlatter E (2005) Uroguanylin and guanylin regulate transport of mouse cortical collecting duct independent of guanylate cyclase C. Kidney Int 68:1008–1017

    PubMed  CAS  Google Scholar 

  106. Soundararajan R, Zhang TT, Wang J, Vandewalle A, Pearce D (2005) A novel role for glucocorticoid-induced leucine zipper protein in epithelial sodium channel-mediated sodium transport. J Biol Chem 280:39970–39981

    PubMed  CAS  Google Scholar 

  107. Sterling H, Lin DH, Gu RM, Dong K, Hebert SC, Wang WH (2002) Inhibition of protein-tyrosine phosphatase stimulates the dynamin-dependent endocytosis of ROMK1. J Biol Chem 277:4317–4323

    PubMed  CAS  Google Scholar 

  108. Sterling H, Lin DH, Wei Y, Wang WH (2003) Tetanus toxin abolishes exocytosis of ROMK1 induced by inhibition of protein tyrosine kinase. Am J Physiol Renal Physiol 284:F510–F517

    PubMed  CAS  Google Scholar 

  109. Summa V, Camargo SMR, Bauch C, Zecevic M, Verrey F (2004) Isoform specificity of human Na+,K+-ATPase localization and aldosterone regulation in mouse kidney cells. J Physiol 555:355–364

    PubMed  CAS  Google Scholar 

  110. Sun P, Lin DH, Wang T, Babilonia E, Wang ZJ, Jin Y, Kemp R, Nasjletti A, Wang WH (2006) Low Na intake suppresses the expression of CYP2C23 and the arachidonic acid-induced inhibition of ENaC. Am J Physiol Renal Physiol 291:1192–1200

    Google Scholar 

  111. Sun P, Liu W, Lin DH, Yue P, Kemp R, Satlin LM, Wang WH (2008) Epoxyeicosatrienoic acid (EET) activates the Ca2+-dependent bid conductance K channel in the cortical collecting duct. J Am Soc Nephrol (in press)

  112. Taniguchi J, Imai M (1998) Flow-dependent activation of maxi K+ channels in apical membrane of rabbit connecting tubule. J Membr Biol 164:35–45

    PubMed  CAS  Google Scholar 

  113. Vallon V, Wulff P, Huang DY, Loffing J, Volkl H, Kuhl D, Lang F (2005) Role of Sgk1 in salt and potassium homeostasis. Am J Physiol Regul Integr Comp Physiol 288:R4–R10

    PubMed  CAS  Google Scholar 

  114. Velazquez H, Ellison DH, Wright FS (1992) Luminal influences on potassium secretion: chloride, sodium, and thiazide diuretics. Am J Physiol (Renal Fluid Electrolyte Physiol) 262–231:F1076–F1082

    Google Scholar 

  115. Verlander JW, Moudy RM, Campbell WG, Cain BD, Wingo CS (2001) Immunohistochemical localization of H–K-ATPase alpha 2c-subunit in rabbit kidney. AJP–Renal Physiology 281:F357–F365

    PubMed  CAS  Google Scholar 

  116. Fran V, Vane S, Dirk H, Davi M, Alai V, Eric F, Mari Z (2003) Short-term aldosterone action on Na,K-ATPase surface expression: role of aldosterone-induced SGK1? Ann NY Acad Sci 986:554–561

    Article  Google Scholar 

  117. Wade JB, Fang L, Liu J, Li D, Yang CL, Subramanya AR, Maouyo D, Mason A, Ellison DH, Welling PA (2006) WNK1 kinase isoform switch regulates renal potassium excretion. Proc Natl Acad Sci 103:8558–8563

    PubMed  CAS  Google Scholar 

  118. Wang T, Giebisch G (1996) Effects of angiotensin II on electrolyte transport in the early and late distal tubule in rat kidney. Am J Physiol 271:F143–F149

    PubMed  CAS  Google Scholar 

  119. Wang W, Schwab A, Giebisch G (1990) Regulation of small-conductance K channel in apical membrane of rat cortical collecting tubule. Am J Physiol 259:F494–F502

    PubMed  CAS  Google Scholar 

  120. Wang WH (2000) The cGMP-dependent protein kinase stimulates the basolateral 18 pS K channel of the rat CCD. Am J Physiol Renal Physiol 278:C1212–C1217

    CAS  Google Scholar 

  121. Wang WH (2004) Regulation of Renal K transport by dietary K intake. Annu Rev Physiol 66:547–569

    PubMed  CAS  Google Scholar 

  122. Wang WH, Lerea KM, Chan M, Giebisch G (2000) Protein tyrosine kinase regulates the number of renal secretory K channel. Am J Physiol Renal Physiol 278:F165–F171

    PubMed  CAS  Google Scholar 

  123. Wang WH, McNicholas CM, Segal AS, Giebisch G (1994) A novel approach allows identification of K channels in the lateral membrane of rat CCD. Am J Physiol 266:F813–F822

    PubMed  CAS  Google Scholar 

  124. Wei Y, Bloom P, Gu R, Wang W (2000) Protein-tyrosine phosphatase reduces the number of apical small conductance K+ channels in the rat cortical collecting duct. J Biol Chem 275:20502–20507

    PubMed  CAS  Google Scholar 

  125. Wei Y, Bloom P, Gu RM, Wang WH (2000) Protein-tyrosine phosphatase reduces the number of apical small conductance K channels in the rat cortical collecting duct. J Biol Chem 275:20502–20507

    PubMed  CAS  Google Scholar 

  126. Wei Y, Bloom P, Lin DH, Gu RM, Wang WH (2001) Effect of dietary K intake on the apical small-conductance K channel in the CCD: Role of protein tyrosine kinase. Am J Physiol Renal Physiol 281:F206–F212

    PubMed  CAS  Google Scholar 

  127. Wei Y, Bloom P, Lin DH, Gu RM, Wang WH (2001) Effect of dietary K intake on the apical small-conductance K channel in the CCD: Role of protein tyrosine kinase. Am J Physiol Renal Physiol 281:F206–F212

    PubMed  CAS  Google Scholar 

  128. Wei Y, Wang WH (2001) The role of cytoskeleton in mediating the effect of vasopressin and herbimycin A on the secretory K channels in the CCD. Am J Physiol Renal Physiol 282:F680–F686

    Google Scholar 

  129. Wei Y, Wang ZJ, Babilonia E, Sterling H, Sun P, Wang WH (2006) Effect of hydrogen peroxide on ROMK channels in the cortical collecting duct. Am J Physiol Renal Physiol 0:0

    Google Scholar 

  130. Wei Y, Zavilowitz B, Satlin LM, Wang WH (2007) Angiotensin II inhibits the ROMK-like small-conductance K channel in renal cortical collecting duct during dietary K restriction. J Biol Chem 0:0

    Google Scholar 

  131. Welling PA, Caplan M, Sutters M, Giebisch G (1993) Aldosterone-mediated Na/K-ATPase expression is alpha 1 isoform specific in the renal cortical collecting duct. J Biol Chem 268:23469–23476

    PubMed  CAS  Google Scholar 

  132. Wingo CS, Cain BD (1993) The renal H–K-ATPase: physiological significance and role in potassium homeostasis. Annu Rev Physiol 55:323–347

    PubMed  CAS  Google Scholar 

  133. Wingo CS (1987) Potassium transport by medullary collecting tubule of rabbit: effects of variation in K intake. Am J Physiol (Renal Fluid Electrolyte Physiol) 253–22:F1136–F1141

    Google Scholar 

  134. Wingo CS (1989) Reversible chloride-dependent potassium transport in cortical collecting tubule. Am J Physiol 256:F697–F704

    PubMed  CAS  Google Scholar 

  135. Wingo CS, Armitage FE (1992) Rubidium absorption and proton secretion by rabbit outer medullary collecting duct via H–K-ATPase. Am J Physiol (Renal Fluid Electrolyte Physiol) 263:F849–F857

    CAS  Google Scholar 

  136. Woda CB, Bragin A, Kleyman TR, Satlin LM (2001) Flow-dependent K+ secretion in the cortical collecting duct is mediated by a maxi-K channel. Am J Physiol Renal Physiol 280:F786–F793

    PubMed  CAS  Google Scholar 

  137. Xu B, Stippec S, Lazrak A, Huang CL, Cobb MH (2005) WNK1 Activates SGK1 by a phosphatidylinositol 3-kinase-dependent and non-catalytic mechanism. J Biol Chem 280:34218–34223

    PubMed  CAS  Google Scholar 

  138. Xu ZC, Yang Y, Hebert SC (1996) Phosphorylation of the ATP-sensitive, inwardly rectifying K+ channel, ROMK, by cyclic AMP-dependent protein kinase. J Biol Chem 271:9313–9319

    PubMed  CAS  Google Scholar 

  139. Yang T, Singh I, Pham H, Sun D, Smart A, Schnermann JB, Briggs JP (1998) Regulation of cyclooxygenase expression in the kidney by dietary salt intake. AJP–Renal Physiol 274:F481–F489

    CAS  Google Scholar 

  140. Yoo D, Kim BY, Campo C, Nance L, King A, Maouyo D, Welling PA (2003) Cell surface expression of the ROMK (Kir 1.1) channel is regulated by the aldosterone-induced kinase, SGK-1, and protein kinase A. J Biol Chem 278:23066–23075

    PubMed  CAS  Google Scholar 

  141. Yoo D, Fang L, Mason A, Kim BY, Welling PA (2005) A phosphorylation-dependent export structure in ROMK (Kir 1.1) channel overrides an endoplasmic reticulum localization signal. J Biol Chem 280:35281–35289

    PubMed  CAS  Google Scholar 

  142. Younes-Ibrahim M, Barlet-Bas C, Buffin-Meyer B, Cheval L, Rajerison R, Doucet A (1995) Ouabain-sensitive and -insensitive K-ATPases in rat nephron: effect of K depletion. Am J Physiol 268:F1141–F1147

    PubMed  CAS  Google Scholar 

  143. Yun CC, Palmada M, Embark HM, Fedorenko O, feng Y, Henke G, Setiawan I, Boehmer C, Weinman EJ, Sandrasagra S, Korbmacher C, Cohen P, Pearce D, Lang F (2002) The serum and glucocorticoid-inducible kinase SGK1 and Na/H exchange regulating factor NHERF2 synergize to stimulate the renal outer medullary K channel ROMK1. JASN 13:2823–2830

    PubMed  CAS  Google Scholar 

  144. Zhen WZ, Li XJ, Hilgemann DW, Huang CL (2003) Protein kinase C inhibits ROMK1 channel activity via phosphotidylinositol-4,5-bisphosphosphate-dependent mechanism. J Biol Chem 276:16852–16856

    Google Scholar 

  145. Zhou X, Lynch IJ, Xia SL, Wingo CS (2000) Activation of H-K-ATPase by CO2 requires a basolateral Ba2+-sensitive pathway during K restriction. Am J Physiol Renal Physiol 279:F153–F160

    PubMed  CAS  Google Scholar 

  146. Zhou X, Wingo CS (1992) H-K-ATPase enhancement of Rb efflux by cortical collecting duct. Am J Physiol (Renal Fluid Electrolyte Physiol) 263:F43–F48

    CAS  Google Scholar 

  147. Zhou X, Wingo CS (1992) Mechanisms of rubidium permeability by rabbit cortical collecting duct during potassium restriction. Am J Physiol 263:F1134–F1141

    PubMed  CAS  Google Scholar 

  148. Zhou X, Wingo CS (1994) Stimulation of total CO2 flux by 10% CO2 in rabbit CCD: role of an apical Sch-28080- and Ba-sensitive mechanism. Am J Physiol 267(Renal 36):F114–F120

    PubMed  CAS  Google Scholar 

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Acknowledgment

We dedicate this manuscript to Dr. Steven H. Hebert, our friend and colleague who died quite unexpectedly on April 15th 2008. We lost with him a long-standing collaborator, friend, and an investigator who made major contributions in the field of potassium transport. The authors also thank Drs. D. Mount and R. B. Silver for their insightful comments. The work is supported by NIH grants DK 47402, DK54983 and HL34100.

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Correspondence to Wen-Hui Wang.

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Wang, WH., Giebisch, G. Regulation of potassium (K) handling in the renal collecting duct. Pflugers Arch - Eur J Physiol 458, 157–168 (2009). https://doi.org/10.1007/s00424-008-0593-3

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