TASK1 and TASK3 potassium channels: Determinants of aldosterone secretion and adrenocortical zonation

Hormone and Metabolic Research

Volumn 42, Issue 6, 2010, Pages 450-457

  Bandulik, S ^a   Penton, D ^a   Barhanin, J ^b   Warth, R ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

Author keywords

Adrenal cortex; Adrenocortical zonation; Aldosterone; Angiotensin II; K2P; KCNK2; KCNK3; KCNK9

Indexed keywords

ALDOSTERONE; DEXAMETHASONE; GLUCOCORTICOID; POTASSIUM CHANNEL; POTASSIUM CHANNELS OF THE 2 PORE DOMAIN; PROTEIN TASK1; PROTEIN TASK3; PROTEIN TREK1; UNCLASSIFIED DRUG;

ADRENAL CORTEX; ADRENAL CORTEX CELL; ALDOSTERONE BLOOD LEVEL; ALDOSTERONE RELEASE; CELL MEMBRANE POTENTIAL; DRUG EFFICACY; HORMONE SYNTHESIS; HUMAN; HYPERALDOSTERONISM; HYPERTENSION; MEMBRANE DEPOLARIZATION; NONHUMAN; PHENOTYPE; POTASSIUM CONDUCTANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PUBERTY; REGULATORY MECHANISM; REVIEW; ZONA FASCICULATA; ZONATION;

ADRENAL CORTEX; ALDOSTERONE; ANIMALS; HUMANS; MICE; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; ORGAN SPECIFICITY; POTASSIUM CHANNELS; POTASSIUM CHANNELS, TANDEM PORE DOMAIN; TISSUE DISTRIBUTION;

MUS;

EID: 77952948397     PISSN: 00185043     EISSN: 14394286     Source Type: Journal    
DOI: 10.1055/s-0029-1243601     Document Type: Review

References (80)

1. Willenberg HS, Schinner S, Ansurudeen I. New mechanisms to control aldosterone synthesis. Horm Metab Res 2008 40 435-441
2. Spat A, Hunyady L. Control of aldosterone secretion: a model for convergence in cellular signaling pathways. Physiol Rev 2004 84 489-539
3. Bassett MH, White PC, Rainey WE. The regulation of aldosterone synthase expression. Mol Cell Endocrinol 2004 217 67-74
4. Cherradi N, Brandenburger Y, Rossier MF, Vallotton MB, Stocco DM, Capponi AM. Atrial natriuretic peptide inhibits calcium-induced steroidogenic acute regulatory protein gene transcription in adrenal glomerulosa cells. Mol Endocrinol 1998 12 962-972
5. Ganz MB, Nee JJ, Isales CM, Barrett PQ. Atrial natriuretic peptide enhances activity of potassium conductance in adrenal glomerulosa cells. Am J Physiol 1994 266 C1357-C1365
6. Spat A. Glomerulosa cell a unique sensor of extracellular K+ concentration. Mol Cell Endocrinol 2004 217 23-26
7. Lotshaw DP. Role of membrane depolarization and T-type Ca2+ channels in angiotensin II and K+ stimulated aldosterone secretion. Mol Cell Endocrinol 2001 175 157-171
8. Liu H, Enyeart JA, Enyeart JJ. Angiotensin II inhibits native bTREK-1 K+ channels through a PLC-, kinase C-, and PIP2-independent pathway requiring ATP hydrolysis. Am J Physiol Cell Physiol 2007 293 C682-C695
9. Chen X, Talley EM, Patel N, Gomis A, McIntire WE, Dong B, Viana F, Garrison JC, Bayliss DA. Inhibition of a background potassium channel by Gq protein alpha-subunits. Proc Natl Acad Sci U S A 2006 103 3422-3427
10. Lopes CM, Rohacs T, Czirjak G, Balla T, Enyedi P, Logothetis DE. PIP2 hydrolysis underlies agonist-induced inhibition and regulates voltage gating of two-pore domain K+ channels. J Physiol 2005 564 117-129
11. Veale EL, Kennard LE, Sutton GL, MacKenzie G, Sandu C, Mathie A. G(alpha)q-mediated regulation of TASK3 two-pore domain potassium channels: the role of protein kinase C. Mol Pharmacol 2007 71 1666-1675
12. Nogueira E, Xing Y, Morris C, Rainey WE. Role of angiotensin II-induced rapid response genes in the regulation of enzymes needed for aldosterone synthesis. J Mol Endocrinol 2009 42 319-330
13. Lymperopoulos A, Rengo G, Zincarelli C, Kim J, Soltys S, Koch WJ. An adrenal beta-arrestin 1-mediated signaling pathway underlies angiotensin II-induced aldosterone production in vitro and in vivo. Proc Natl Acad Sci U S A 2009 106 5825-5830
14. Born-Frontsberg E, Reincke M, Beuschlein F, Quinkler M. Tumor size of Conn's adenoma and comorbidities. Horm Metab Res 2009 41 785-788
15. Young WF. Primary aldosteronism: renaissance of a syndrome. Clin Endocrinol (Oxf) 2007 66 607-618
16. Zajicek G, Ariel I, Arber N. The streaming adrenal cortex: direct evidence of centripetal migration of adrenocytes by estimation of cell turnover rate. J Endocrinol 1986 111 477-482
17. Kim AC, Hammer GD. Adrenocortical cells with stem/progenitor cell properties: recent advances. Mol Cell Endocrinol 2007 265266 10-16
18. Mesiano S, Jaffe RB. Developmental and functional biology of the primate fetal adrenal cortex. Endocr Rev 1997 18 378-403 (Pubitemid 27246882)
19. Plaster NM, Tawil R, Tristani-Firouzi M, Canun S, Bendahhou S, Tsunoda A, Donaldson MR, Iannaccone ST, Brunt E, Barohn R, Clark J, Deymeer F, George AL Jr, Fish FA, Hahn A, Nitu A, Ozdemir C, Serdaroglu P, Subramony SH, Wolfe G, Fu YH, Ptacek LJ. Mutations in Kir2.1 cause the developmental and episodic electrical phenotypes of Andersen's syndrome. Cell 2001 105 511-519
20. Mu D, Chen L, Zhang X, See LH, Koch CM, Yen C, Tong JJ, Spiegel L, Nguyen KC, Servoss A, Peng Y, Pei L, Marks JR, Lowe S, Hoey T, Jan LY, McCombie WR, Wigler MH, Powers S. Genomic amplification and oncogenic properties of the KCNK9 potassium channel gene. Cancer Cell 2003 3 297-302
21. Pei L, Wiser O, Slavin A, Mu D, Powers S, Jan LY, Hoey T. Oncogenic potential of TASK3 (Kcnk9) depends on K+ channel function. Proc Natl Acad Sci U S A 2003 100 7803-7807
22. Kunzelmann K. Ion channels and cancer. J Membr Biol 2005 205 159-173
23. Bayliss DA, Barrett PQ. Emerging roles for two-pore-domain potassium channels and their potential therapeutic impact. Trends Pharmacol Sci 2008 29 566-575
24. Czirjak G, Enyedi P. TASK-3 dominates the background potassium conductance in rat adrenal glomerulosa cells. Mol Endocrinol 2002 16 621-629
25. Czirjak G, Fischer T, Spat A, Lesage F, Enyedi P. TASK (TWIK-related acid-sensitive K+ channel) is expressed in glomerulosa cells of rat adrenal cortex and inhibited by angiotensin II. Mol Endocrinol 2000 14 863-874
26. Heitzmann D, Derand R, Jungbauer S, Bandulik S, Sterner C, Schweda F, El Wakil A, Lalli E, Guy N, Mengual R, Reichold M, Tegtmeier I, Bendahhou S, Gomez-Sanchez CE, Aller MI, Wisden W, Weber A, Lesage F, Warth R, Barhanin J. Invalidation of TASK1 potassium channels disrupts adrenal gland zonation and mineralocorticoid homeostasis. EMBO J 2008 27 179-187
27. Davies LA, Hu C, Guagliardo NA, Sen N, Chen X, Talley EM, Carey RM, Bayliss DA, Barrett PQ. TASK channel deletion in mice causes primary hyperaldosteronism. Proc Natl Acad Sci U S A 2008 105 2203-2208
28. Lesage F, Guillemare E, Fink M, Duprat F, Lazdunski M, Romey G, Barhanin J. TWIK-1, a ubiquitous human weakly inward rectifying K+ channel with a novel structure. EMBO J 1996 15 1004-1011
29. Lesage F, Lazdunski M. Molecular and functional properties of two-pore-domain potassium channels. Am J Physiol Renal Physiol 2000 279 F793-F801
30. Duprat F, Lesage F, Fink M, Reyes R, Heurteaux C, Lazdunski M. TASK, a human background K+ channel to sense external pH variations near physiological pH. EMBO J 1997 16 5464-5471
31. Brauneis U, Vassilev PM, Quinn SJ, Williams GH, Tillotson DL. ANG II blocks potassium currents in zona glomerulosa cells from rat, bovine, and human adrenals. Am J Physiol 1991 260 E772-E779
32. Payet MD, Benabderrazik M, Gallo-Payet N. Excitation-secretion coupling: ionic currents in glomerulosa cells: effects of adrenocorticotropin and K+ channel blockers. Endocrinology 1987 121 875-882
33. Lotshaw DP. Characterization of angiotensin II-regulated K+ conductance in rat adrenal glomerulosa cells. J Membr Biol 1997 156 261-277
34. Payet MD, Durroux T, Bilodeau L, Guillon G, Gallo-Payet N. Characterization of K+ and Ca2+ ionic currents in glomerulosa cells from human adrenal glands. Endocrinology 1994 134 2589-2598
35. Patel AJ, Honore E. Properties and modulation of mammalian 2P domain K+ channels. Trends Neurosci 2001 24 339-346
36. Enyeart JJ, Danthi SJ, Liu H, Enyeart JA. Angiotensin II inhibits bTREK-1 K+ channels in adrenocortical cells by separate Ca2+- and ATP hydrolysis-dependent mechanisms. J Biol Chem 2005 280 30814-30828
37. Enyeart JA, Danthi SJ, Enyeart JJ. TREK-1 K+ channels couple angiotensin II receptors to membrane depolarization and aldosterone secretion in bovine adrenal glomerulosa cells. Am J Physiol Endocrinol Metab 2004 287 E1154-E1165
38. Enyeart JJ, Xu L, Danthi S, Enyeart JA. An ACTH- and ATP-regulated background K+ channel in adrenocortical cells is TREK-1. J Biol Chem 2002 277 49186-49199
39. Liu H, Enyeart JA, Enyeart JJ. ACTH inhibits bTREK-1 K+ channels through multiple cAMP-dependent signaling pathways. J Gen Physiol 2008 132 279-294
40. Wada A, Ohnishi T, Nonaka Y, Okamoto M, Yamano T. Synthesis of aldosterone by a reconstituted system of cytochrome P-45011 beta from bovine adrenocortical mitochondria. J Biochem 1985 98 245-256
41. Lisurek M, Bernhardt R. Modulation of aldosterone and cortisol synthesis on the molecular level. Mol Cell Endocrinol 2004 215 149-159
42. Brenner T, O'Shaughnessy KM. Both TASK-3 and TREK-1 two-pore loop K channels are expressed in H295R cells and modulate their membrane potential and aldosterone secretion. Am J Physiol Endocrinol Metab 2008 295 E1480-E1486
43. Bayliss DA, Sirois JE, Talley EM. The TASK family: two-pore domain background K+ channels. Mol Interv 2003 3 205-219
44. Decher N, Maier M, Dittrich W, Gassenhuber J, Bruggemann A, Busch AE, Steinmeyer K. Characterization of TASK-4, a novel member of the pH-sensitive, two-pore domain potassium channel family. FEBS Lett 2001 492 84-89
45. Kim D, Gnatenco C. TASK-5, a new member of the tandem-pore K(+) channel family. Biochem Biophys Res Commun 2001 284 923-930
46. Lotshaw DP. Biophysical and pharmacological characteristics of native two-pore domain TASK channels in rat adrenal glomerulosa cells. J Membr Biol 2006 210 51-70
47. Radke KJ, Taylor RE Jr, Schneider EG. Effect of hydrogen ion concentration on aldosterone secretion by isolated perfused canine adrenal glands. J Endocrinol 1986 110 293-301
48. Czirjak G, Enyedi P. Formation of functional heterodimers between the TASK-1 and TASK-3 two-pore domain potassium channel subunits. J Biol Chem 2002 277 5426-5432
49. Clarke CE, Veale EL, Green PJ, Meadows HJ, Mathie A. Selective block of the human 2-P domain potassium channel, TASK-3, and the native leak potassium current, IKSO, by zinc. J Physiol 2004 560 51-62
50. Maingret F, Patel AJ, Lazdunski M, Honore E. The endocannabinoid anandamide is a direct and selective blocker of the background K(+) channel TASK-1. EMBO J 2001 20 47-54
51. Lesage F, Reyes R, Fink M, Duprat F, Guillemare E, Lazdunski M. Dimerization of TWIK-1 K+ channel subunits via a disulfide bridge. EMBO J 1996 15 6400-6407
52. Kang D, Han J, Talley EM, Bayliss DA, Kim D. Functional expression of TASK-1/TASK-3 heteromers in cerebellar granule cells. J Physiol 2004 554 64-77
53. Linden AM, Aller MI, Leppa E, Vekovischeva O, Aitta-Aho T, Veale EL, Mathie A, Rosenberg P, Wisden W, Korpi ER. The in vivo contributions of TASK-1-containing channels to the actions of inhalation anesthetics, the alpha(2) adrenergic sedative dexmedetomidine, and cannabinoid agonists. J Pharmacol Exp Ther 2006 317 615-626
54. Meuth SG, Aller MI, Munsch T, Schuhmacher T, Seidenbecher T, Meuth P, Kleinschnitz C, Pape HC, Wiendl H, Wisden W, Budde T. The contribution of TWIK-related acid-sensitive K+-containing channels to the function of dorsal lateral geniculate thalamocortical relay neurons. Mol Pharmacol 2006 69 1468-1476
55. Aller MI, Veale EL, Linden AM, Sandu C, Schwaninger M, Evans LJ, Korpi ER, Mathie A, Wisden W, Brickley SG. Modifying the subunit composition of TASK channels alters the modulation of a leak conductance in cerebellar granule neurons. J Neurosci 2005 25 11455-11467
56. Linden AM, Aller MI, Leppa E, Rosenberg PH, Wisden W, Korpi ER. K+ channel TASK-1 knockout mice show enhanced sensitivities to ataxic and hypnotic effects of GABA(A) receptor ligands. J Pharmacol Exp Ther 2008 327 277-286
57. Trapp S, Aller MI, Wisden W, Gourine AV. A role for TASK-1 (KCNK3) channels in the chemosensory control of breathing. J Neurosci 2008 28 8844-8850
58. Romero DG, Yanes LL, de Rodriguez AF, Plonczynski MW, Welsh BL, Reckelhoff JF, Gomez-Sanchez EP, Gomez-Sanchez CE. Disabled-2 is expressed in adrenal zona glomerulosa and is involved in aldosterone secretion. Endocrinology 2007 148 2644-2652
59. Gummow BM, Scheys JO, Cancelli VR, Hammer GD. Reciprocal regulation of a glucocorticoid receptor-steroidogenic factor-1 transcription complex on the Dax-1 promoter by glucocorticoids and adrenocorticotropic hormone in the adrenal cortex. Mol Endocrinol 2006 20 2711-2723
60. Ashmole I, Goodwin PA, Stanfield PR. TASK-5, a novel member of the tandem pore K+ channel family. Pflugers Arch 2001 442 828-833
61. Karschin C, Wischmeyer E, Preisig-Muller R, Rajan S, Derst C, Grzeschik KH, Daut J, Karschin A. Expression pattern in brain of TASK-1, TASK-3, and a tandem pore domain K(+) channel subunit, TASK-5, associated with the central auditory nervous system. Mol Cell Neurosci 2001 18 632-648
62. Jespersen T, Grunnet M, Olesen SP. The KCNQ1 potassium channel: from gene to physiological function. Physiology (Bethesda) 2005 20 408-416
63. Arrighi I, Bloch-Faure M, Grahammer F, Bleich M, Warth R, Mengual R, Drici MD, Barhanin J, Meneton P. Altered potassium balance and aldosterone secretion in a mouse model of human congenital long QT syndrome. Proc Natl Acad Sci U S A 2001 98 8792-8797
64. Vallon V, Grahammer F, Volkl H, Sandu CD, Richter K, Rexhepaj R, Gerlach U, Rong Q, Pfeifer K, Lang F. KCNQ1-dependent transport in renal and gastrointestinal epithelia. Proc Natl Acad Sci U S A 2005 102 17864-17869
65. Sarzani R, Pietrucci F, Francioni M, Salvi F, Letizia C, D'Erasmo E, Dessi FP, Rappelli A. Expression of potassium channel isoforms mRNA in normal human adrenals and aldosterone-secreting adenomas. J Endocrinol Invest 2006 29 147-153
66. Abbott GW, Goldstein SA. Potassium channel subunits encoded by the KCNE gene family: physiology and pathophysiology of the MinK-related peptides (MiRPs). Mol Interv 2001 1 95-107
67. Vallon V, Grahammer F, Richter K, Bleich M, Lang F, Barhanin J, Volkl H, Warth R. Role of KCNE1-dependent K+ fluxes in mouse proximal tubule. J Am Soc Nephrol 2001 12 2003-2011
68. Sausbier M, Arntz C, Bucurenciu I, Zhao H, Zhou XB, Sausbier U, Feil S, Kamm S, Essin K, Sailer CA, Abdullah U, Krippeit-Drews P, Feil R, Hofmann F, Knaus HG, Kenyon C, Shipston MJ, Storm JF, Neuhuber W, Korth M, Schubert R, Gollasch M, Ruth P. Elevated blood pressure linked to primary hyperaldosteronism and impaired vasodilation in BK channel-deficient mice. Circulation 2005 112 60-68
69. Grimm PR, Irsik DL, Settles DC, Holtzclaw JD, Sansom SC. Hypertension of Kcnmb1-/- is linked to deficient K secretion and aldosteronism. Proc Natl Acad Sci U S A 2009 106 11800-11805
70. Knaus HG, Garcia-Calvo M, Kaczorowski GJ, Garcia ML. Subunit composition of the high conductance calcium-activated potassium channel from smooth muscle, a representative of the mSlo and slowpoke family of potassium channels. J Biol Chem 1994 269 3921-3924
71. Meera P, Wallner M, Song M, Toro L. Large conductance voltage- and calcium-dependent K+ channel, a distinct member of voltage-dependent ion channels with seven N-terminal transmembrane segments (S0-S6), an extracellular N terminus, and an intracellular (S9-S10) C terminus. Proc Natl Acad Sci U S A 1997 94 14066-14071
72. Sorensen MV, Matos JE, Sausbier M, Sausbier U, Ruth P, Praetorius HA, Leipziger J. Aldosterone increases KCa1.1 (BK) channel-mediated colonic K+ secretion. J Physiol 2008 586 4251-4264
73. Lifton RP, Dluhy RG, Powers M, Rich GM, Gutkin M, Fallo F, Gill JR Jr, Feld L, Ganguly A, Laidlaw JC. Hereditary hypertension caused by chimaeric gene duplications and ectopic expression of aldosterone synthase. Nat Genet 1992 2 66-74
74. Gordon RD, Stowasser M, Klemm SA, Tunny TJ. Primary aldosteronism - some genetic, morphological, and biochemical aspects of subtypes. Steroids 1995 60 35-41
75. Mulatero P, Veglio F, Pilon C, Rabbia F, Zocchi C, Limone P, Boscaro M, Sonino N, Fallo F. Diagnosis of glucocorticoid-remediable aldosteronism in primary aldosteronism: aldosterone response to dexamethasone and long polymerase chain reaction for chimeric gene. J Clin Endocrinol Metab 1998 83 2573-2575
76. Fardella CE, Pinto M, Mosso L, Gomez-Sanchez C, Jalil J, Montero J. Genetic study of patients with dexamethasone-suppressible aldosteronism without the chimeric CYP11B1/CYP11B2 gene. J Clin Endocrinol Metab 2001 86 4805-4807
77. Wotus C, Levay-Young BK, Rogers LM, Gomez-Sanchez CE, Engeland WC. Development of adrenal zonation in fetal rats defined by expression of aldosterone synthase and 11beta-hydroxylase. Endocrinology 1998 139 4397-4403
78. Enyeart JA, Danthi S, Enyeart JJ. Corticotropin induces the expression of TREK-1 mRNA and K+ current in adrenocortical cells. Mol Pharmacol 2003 64 132-142
79. Kanazirska MV, Vassilev PM, Quinn SJ, Tillotson DL, Williams GH. Single K+ channels in adrenal zona glomerulosa cells. II. Inhibition by angiotensin II. Am J Physiol 1992 263 E760-E765
80. Vassilev PM, Kanazirska MV, Quinn SJ, Tillotson DL, Williams GH. K+ channels in adrenal zona glomerulosa cells. I. Characterization of distinct channel types. Am J Physiol 1992 263 E752-E759