1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Physiology
  4. Volume 83, 2021
  5. Article

Annual Review of Physiology

Volume 83, 2021

Ion Channel Function and Electrical Excitability in the Zona Glomerulosa: A Network Perspective on Aldosterone Regulation

Abstract

Aldosterone excess is a pathogenic factor in many hypertensive disorders. The discovery of numerous somatic and germline mutations in ion channels in primary hyperaldosteronism underscores the importance of plasma membrane conductances in determining the activation state of zona glomerulosa (zG) cells. Electrophysiological recordings describe an electrically quiescent behavior for dispersed zG cells. Yet, emerging data indicate that in native rosette structures in situ, zG cells are electrically excitable, generating slow periodic voltage spikes and coordinated bursts of Ca2+ oscillations. We revisit data to understand how a multitude of conductances may underlie voltage/Ca2+ oscillations, recognizing that zG layer self-renewal and cell heterogeneity may complicate this task. We review recent data to understand rosette architecture and apply maxims derived from computational network modeling to understand rosette function. The challenge going forward is to uncover how the rosette orchestrates the behavior of a functional network of conditional oscillators to control zG layer performance and aldosterone secretion.

Keyword(s): aldosterone, electrical excitability, ion channels, rosette, zona glomerulosa
Loading

Article metrics loading...

/content/journals/10.1146/annurev-physiol-030220-113038
2021-02-10
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/physiol/83/1/annurev-physiol-030220-113038.html?itemId=/content/journals/10.1146/annurev-physiol-030220-113038&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Quinn SJ, Williams GH. 1988. Regulation of aldosterone secretion. Annu. Rev. Physiol. 50:409–26
     [Google Scholar]
  2. 2. 
    Spat A, Hunyady L. 2004. Control of aldosterone secretion: a model for convergence in cellular signaling pathways. Physiol. Rev. 84:489–539
     [Google Scholar]
  3. 3. 
    Seccia TM, Caroccia B, Gomez-Sanchez EP, Gomez-Sanchez CE, Rossi GP 2018. The biology of normal zona glomerulosa and aldosterone-producing adenoma: pathological implications. Endocr. Rev. 39:1029–56
     [Google Scholar]
  4. 4. 
    Fredlund P, Saltman S, Kondo T, Douglas J, Catt KJ 1977. Aldosterone production by isolated glomerulosa cells: modulation of sensitivity to angiotensin II and ACTH by extracellular potassium concentration. Endocrinology 100:481–86
     [Google Scholar]
  5. 5. 
    Himathongkam T, Dluhy RG, Williams GH 1975. Potassium-aldosterone-renin interrelationships. J. Clin. Endocrinol. Metab. 41:153–59
     [Google Scholar]
  6. 6. 
    Aguilera G, Catt KJ. 1986. Participation of voltage-dependent calcium channels in the regulation of adrenal glomerulosa function by angiotensin II and potassium. Endocrinology 118:112–18
     [Google Scholar]
  7. 7. 
    Capponi AM, Lew PD, Jornot L, Vallotton MB 1984. Correlation between cytosolic free Ca2+ and aldosterone production in bovine adrenal glomerulosa cells. Evidence for a difference in the mode of action of angiotensin II and potassium. J. Biol. Chem. 259:8863–69
     [Google Scholar]
  8. 8. 
    Zennaro MC, Fernandes-Rosa F, Boulkroun S 2015. Genetic alterations in primary aldosteronism. Med. Sci. 31:389–96
     [Google Scholar]
  9. 9. 
    Scholl UI. 2017. Unanswered questions in the genetic basis of primary aldosteronism. Horm. Metab. Res. 49:963–68
     [Google Scholar]
  10. 10. 
    Monticone S, Buffolo F, Tetti M, Veglio F, Pasini B, Mulatero P 2018. Genetics in endocrinology: the expanding genetic horizon of primary aldosteronism. Eur. J. Endocrinol. 178:R101–11
     [Google Scholar]
  11. 11. 
    Funder JW. 2019. Primary aldosteronism. Hypertension 74:458–66
     [Google Scholar]
  12. 12. 
    Manosroi W, Williams GH. 2019. Genetics of human primary hypertension: focus on hormonal mechanisms. Endocr. Rev. 40:825–56
     [Google Scholar]
  13. 13. 
    Yang T, He M, Hu C 2018. Regulation of aldosterone production by ion channels: from basal secretion to primary aldosteronism. Biochim. Biophys. Acta Mol. Basis Dis. 1864:871–81
     [Google Scholar]
  14. 14. 
    Natke E Jr, Kabela E. 1979. Electrical responses in cat adrenal cortex: possible relation to aldosterone secretion. Am. J. Physiol. Endocrinol. Metab. 237:E158–62
     [Google Scholar]
  15. 15. 
    Quinn SJ, Cornwall MC, Williams GH 1987. Electrical properties of isolated rat adrenal glomerulosa and fasciculata cells. Endocrinology 120:903–14
     [Google Scholar]
  16. 16. 
    Lotshaw DP. 1997. Characterization of angiotensin II-regulated K+ conductance in rat adrenal glomerulosa cells. J. Membr. Biol. 156:261–77
     [Google Scholar]
  17. 17. 
    Chen XL, Bayliss DA, Fern RJ, Barrett PQ 1999. A role for T-type Ca2+ channels in the synergistic control of aldosterone production by ANG II and K+. Am. J. Physiol. Ren. Physiol. 276:F674–83
     [Google Scholar]
  18. 18. 
    Davies LA, Hu C, Guagliardo NA, Sen N, Chen X et al. 2008. TASK channel deletion in mice causes primary hyperaldosteronism. PNAS 105:2203–8
     [Google Scholar]
  19. 19. 
    Hu C, Rusin CG, Tan Z, Guagliardo NA, Barrett PQ 2012. Zona glomerulosa cells of the mouse adrenal cortex are intrinsic electrical oscillators. J. Clin. Investig. 122:2046–53
     [Google Scholar]
  20. 20. 
    Matthews EK, Saffran M. 1973. Ionic dependence of adrenal steroidogenesis and ACTH-induced changes in the membrane potential of adrenocortical cells. J. Physiol. 234:43–64
     [Google Scholar]
  21. 21. 
    Quinn SJ, Cornwall MC, Williams GH 1987. Electrophysiological responses to angiotensin II of isolated rat adrenal glomerulosa cells. Endocrinology 120:1581–89
     [Google Scholar]
  22. 22. 
    Lotshaw DP. 1997. Effects of K+ channel blockers on K+ channels, membrane potential, and aldosterone secretion in rat adrenal zona glomerulosa cells. Endocrinology 138:4167–75
     [Google Scholar]
  23. 23. 
    Lotshaw DP. 2001. Role of membrane depolarization and T-type Ca2+ channels in angiotensin II and K+ stimulated aldosterone secretion. Mol. Cell. Endocrinol. 175:157–71
     [Google Scholar]
  24. 24. 
    Durroux T, Gallo-Payet N, Payet MD 1991. Effects of adrenocorticotropin on action potential and calcium currents in cultured rat and bovine glomerulosa cells. Endocrinology 129:2139–47
     [Google Scholar]
  25. 25. 
    Goppner C, Orozco IJ, Hoegg-Beiler MB, Soria AH, Hubner CA et al. 2019. Pathogenesis of hypertension in a mouse model for human CLCN2 related hyperaldosteronism. Nat. Commun. 10:4678
     [Google Scholar]
  26. 26. 
    Guagliardo NA, Klein PM, Gancayco CA, Lu A, Leng S et al. 2020. Angiotensin II induces coordinated calcium bursts in aldosterone-producing adrenal rosettes. Nat. Commun. 11:1679
     [Google Scholar]
  27. 27. 
    Schewe J, Seidel E, Forslund S, Marko L, Peters J et al. 2019. Elevated aldosterone and blood pressure in a mouse model of familial hyperaldosteronism with ClC-2 mutation. Nat. Commun. 10:5155
     [Google Scholar]
  28. 28. 
    Bean BP. 2007. The action potential in mammalian central neurons. Nat. Rev. Neurosci. 8:451–65
     [Google Scholar]
  29. 29. 
    Lesage F, Lazdunski M. 2000. Molecular and functional properties of two-pore-domain potassium channels. Am. J. Physiol. Ren. Physiol. 279:F793–801
     [Google Scholar]
  30. 30. 
    Goldstein SA, Bockenhauer D, O'Kelly I, Zilberberg N 2001. Potassium leak channels and the KCNK family of two-P-domain subunits. Nat. Rev. Neurosci. 2:175–84
     [Google Scholar]
  31. 31. 
    Czirjak G, Enyedi P. 2002. Formation of functional heterodimers between the TASK-1 and TASK-3 two-pore domain potassium channel subunits. J. Biol. Chem. 277:5426–32
     [Google Scholar]
  32. 32. 
    Chen X, Talley EM, Patel N, Gomis A, McIntire WE et al. 2006. Inhibition of a background potassium channel by Gq protein α-subunits. PNAS 103:3422–27
     [Google Scholar]
  33. 33. 
    Wilke BU, Lindner M, Greifenberg L, Albus A, Kronimus Y et al. 2014. Diacylglycerol mediates regulation of TASK potassium channels by Gq-coupled receptors. Nat. Commun. 5:5540
     [Google Scholar]
  34. 34. 
    Bayliss DA. 2019. Tandem pore domain potassium channels. The Oxford Handbook of Neuronal Ion Channels A Bhattacharjee 1–46 Oxford, UK: Oxford Univ. Press
     [Google Scholar]
  35. 35. 
    Maingret F, Patel AJ, Lesage F, Lazdunski M, Honoré E 1999. Mechano- or acid stimulation, two interactive modes of activation of the TREK-1 potassium channel. J. Biol. Chem. 274:26691–96
     [Google Scholar]
  36. 36. 
    Czirjak G, Enyedi P. 2003. Ruthenium red inhibits TASK-3 potassium channel by interconnecting glutamate 70 of the two subunits. Mol. Pharmacol. 63:646–52
     [Google Scholar]
  37. 37. 
    Plant LD, Rajan S, Goldstein SA 2005. K2P channels and their protein partners. Curr. Opin. Neurobiol. 15:326–33
     [Google Scholar]
  38. 38. 
    Czirjak G, Fischer T, Spat A, Lesage F, Enyedi P 2000. TASK (TWIK-related acid-sensitive K+ channel) is expressed in glomerulosa cells of rat adrenal cortex and inhibited by angiotensin II. Mol. Endocrinol. 14:863–74
     [Google Scholar]
  39. 39. 
    Bandulik S, Tauber P, Lalli E, Barhanin J, Warth R 2015. Two-pore domain potassium channels in the adrenal cortex. Pflügers Arch 467:1027–42
     [Google Scholar]
  40. 40. 
    Enyeart JA, Danthi SJ, Enyeart JJ 2004. TREK-1 K+ channels couple angiotensin II receptors to membrane depolarization and aldosterone secretion in bovine adrenal glomerulosa cells. Am. J. Physiol. Endocrinol. Metab. 287:E1154–65
     [Google Scholar]
  41. 41. 
    Choi M, Scholl UI, Yue P, Björklund P, Zhao B et al. 2011. K+ channel mutations in adrenal aldosterone-producing adenomas and hereditary hypertension. Science 331:768–72
     [Google Scholar]
  42. 42. 
    Nogueira EF, Gerry D, Mantero F, Mariniello B, Rainey WE 2010. The role of TASK1 in aldosterone production and its expression in normal adrenal and aldosterone-producing adenomas. Clin. Endocrinol. 73:22–29
     [Google Scholar]
  43. 43. 
    Penton D, Bandulik S, Schweda F, Haubs S, Tauber P et al. 2012. Task3 potassium channel gene invalidation causes low renin and salt-sensitive arterial hypertension. Endocrinology 153:4740–48
     [Google Scholar]
  44. 44. 
    Chen AX, Nishimoto K, Nanba K, Rainey WE 2015. Potassium channels related to primary aldosteronism: Expression similarities and differences between human and rat adrenals. Mol. Cell. Endocrinol. 417:141–48
     [Google Scholar]
  45. 45. 
    Brenner T, O'Shaughnessy KM. 2008. 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. 295:E1480–86
     [Google Scholar]
  46. 46. 
    Yao J, McHedlishvili D, McIntire WE, Guagliardo NA, Erisir A et al. 2017. Functional TASK-3-like channels in mitochondria of aldosterone-producing zona glomerulosa cells. Hypertension 70:347–56
     [Google Scholar]
  47. 47. 
    Lenzini L, Caroccia B, Campos AG, Fassina A, Belloni AS et al. 2014. Lower expression of the TWIK-related acid-sensitive K+ channel 2 (TASK-2) gene is a hallmark of aldosterone-producing adenoma causing human primary aldosteronism. J. Clin. Endocrinol. Metab. 99:E674–82
     [Google Scholar]
  48. 48. 
    Lenzini L, Prisco S, Gallina M, Kuppusamy M, Rossi GP 2018. Mutations of the Twik-related acid-sensitive K+ channel 2 promoter in human primary aldosteronism. Endocrinology 159:1352–59
     [Google Scholar]
  49. 49. 
    Manichaikul A, Rich SS, Allison MA, Guagliardo NA, Bayliss DA et al. 2016. KCNK3 variants are associated with hyperaldosteronism and hypertension. Hypertension 68:356–64
     [Google Scholar]
  50. 50. 
    Lotshaw DP. 2006. Biophysical and pharmacological characteristics of native two-pore domain TASK channels in rat adrenal glomerulosa cells. J. Membr. Biol. 210:51–70
     [Google Scholar]
  51. 51. 
    Heitzmann D, Derand R, Jungbauer S, Bandulik S, Sterner C et al. 2008. Invalidation of TASK1 potassium channels disrupts adrenal gland zonation and mineralocorticoid homeostasis. EMBO J 27:179–87
     [Google Scholar]
  52. 52. 
    Guagliardo NA, Yao J, Hu C, Schertz EM, Tyson DA et al. 2012. TASK-3 channel deletion in mice recapitulates low-renin essential hypertension. Hypertension 59:999–1005
     [Google Scholar]
  53. 53. 
    Guagliardo NA, Yao J, Stipes EJ, Cechova S, Le TH et al. 2019. Adrenal tissue-specific deletion of TASK channels causes aldosterone-driven angiotensin II-independent hypertension. Hypertension 73:407–14
     [Google Scholar]
  54. 54. 
    Hibino H, Inanobe A, Furutani K, Murakami S, Findlay I, Kurachi Y 2010. Inwardly rectifying potassium channels: their structure, function, and physiological roles. Physiol. Rev. 90:291–366
     [Google Scholar]
  55. 55. 
    Lopatin AN, Makhina EN, Nichols CG 1994. Potassium channel block by cytoplasmic polyamines as the mechanism of intrinsic rectification. Nature 372:366–69
     [Google Scholar]
  56. 56. 
    Lopatin AN, Nichols CG. 1996. [K+] dependence of polyamine-induced rectification in inward rectifier potassium channels (IRK1, Kir2.1). J. Gen. Physiol. 108:105–13
     [Google Scholar]
  57. 57. 
    Hilgemann DW, Ball R. 1996. Regulation of cardiac Na+,Ca2+ exchange and KATP potassium channels by PIP2. Science 273:956–59
     [Google Scholar]
  58. 58. 
    Chan KW, Sui JL, Vivaudou M, Logothetis DE 1997. Specific regions of heteromeric subunits involved in enhancement of G protein-gated K+ channel activity. J. Biol. Chem. 272:6548–55
     [Google Scholar]
  59. 59. 
    He C, Zhang H, Mirshahi T, Logothetis DE 1999. Identification of a potassium channel site that interacts with G protein βγ subunits to mediate agonist-induced signaling. J. Biol. Chem. 274:12517–24
     [Google Scholar]
  60. 60. 
    Krapivinsky G, Gordon EA, Wickman K, Velimirović B, Krapivinsky L, Clapham DE 1995. The G-protein-gated atrial K+ channel IKAch is a heteromultimer of two inwardly rectifying K+-channel proteins. Nature 374:135–41
     [Google Scholar]
  61. 61. 
    Ho IHM, Murrell-Lagnado RD. 1999. Molecular determinants for sodium-dependent activation of G protein-gated K+ channels. J. Biol. Chem. 274:8639–48
     [Google Scholar]
  62. 62. 
    Vassilev PM, Kanazirska MV, Quinn SJ, Tillotson DL, Williams GH 1992. K+ channels in adrenal zona glomerulosa cells. I. Characterization of distinct channel types. Am. J. Physiol. Endocrinol. Metab. 263:E752–59
     [Google Scholar]
  63. 63. 
    Kanazirska MV, Vassilev PM, Quinn SJ, Tillotson DL, Williams GH 1992. Single K+ channels in adrenal zona glomerulosa cells. II. Inhibition by angiotensin II. Am. J. Physiol. Endocrinol. Metab. 263:E760–65
     [Google Scholar]
  64. 64. 
    Boulkroun S, Beuschlein F, Rossi GP, Golib-Dzib JF, Fischer E et al. 2012. Prevalence, clinical, and molecular correlates of KCNJ5 mutations in primary aldosteronism. Hypertension 59:592–98
     [Google Scholar]
  65. 65. 
    Lenzini L, Rossitto G, Maiolino G, Letizia C, Funder JW, Rossi GP 2015. A meta-analysis of somatic KCNJ5 K+ channel mutations in 1636 patients with an aldosterone-producing adenoma. J. Clin. Endocrinol. Metab. 100:E1089–95
     [Google Scholar]
  66. 66. 
    Åkerström T, Crona J, Delgado Verdugo A, Starker LF, Cupisti K et al. 2012. Comprehensive re-sequencing of adrenal aldosterone producing lesions reveal three somatic mutations near the KCNJ5 potassium channel selectivity filter. PLOS ONE 7:e41926
     [Google Scholar]
  67. 67. 
    Yang Y, Gomez-Sanchez CE, Jaquin D, Aristizabal Prada ET, Meyer LS et al. 2019. Primary aldosteronism: KCNJ5 mutations and adrenocortical cell growth. Hypertension 74:809–16
     [Google Scholar]
  68. 68. 
    Chen TY. 2005. Structure and function of CLC channels. Annu. Rev. Physiol. 67:809–39
     [Google Scholar]
  69. 69. 
    Jentsch TJ, Pusch M. 2018. CLC chloride channels and transporters: structure, function, physiology, and disease. Physiol. Rev. 98:1493–590
     [Google Scholar]
  70. 70. 
    Fernandes-Rosa FL, Daniil G, Orozco IJ, Goppner C, El Zein R et al. 2018. A gain-of-function mutation in the CLCN2 chloride channel gene causes primary aldosteronism. Nat. Genet. 50:355–61
     [Google Scholar]
  71. 71. 
    Scholl UI, Stölting G, Schewe J, Thiel A, Tan H et al. 2018. CLCN2 chloride channel mutations in familial hyperaldosteronism type II. Nat. Genet. 50:349–54
     [Google Scholar]
  72. 72. 
    Llinas R, Yarom Y. 1981. Electrophysiology of mammalian inferior olivary neurones in vitro. Different types of voltage-dependent ionic conductances. J. Physiol. 315:549–67
     [Google Scholar]
  73. 73. 
    Tsien RW, Lipscombe D, Madison DV, Bley KR, Fox AP 1988. Multiple types of neuronal calcium channels and their selective modulation. Trends Neurosci 11:431–38
     [Google Scholar]
  74. 74. 
    Talavera K, Nilius B. 2006. Biophysics and structure-function relationship of T-type Ca2+ channels. Cell Calcium 40:97–114
     [Google Scholar]
  75. 75. 
    Ben-Johny M, Yue DT. 2014. Calmodulin regulation (calmodulation) of voltage-gated calcium channels. J. Gen. Physiol. 143:679–92
     [Google Scholar]
  76. 76. 
    Guia A, Stern MD, Lakatta EG, Josephson IR 2001. Ion concentration-dependence of rat cardiac unitary L-type calcium channel conductance. Biophys. J. 80:2742–50
     [Google Scholar]
  77. 77. 
    Shorofsky SR, January CT. 1992. L- and T-type Ca2+ channels in canine cardiac Purkinje cells. Single-channel demonstration of L-type Ca2+ window current. Circ. Res. 70:456–64
     [Google Scholar]
  78. 78. 
    Perez-Reyes E. 2003. Molecular physiology of low-voltage-activated T-type calcium channels. Physiol. Rev. 83:117–61
     [Google Scholar]
  79. 79. 
    Wolfe JT, Wang H, Perez-Reyes E, Barrett PQ 2002. Stimulation of recombinant CaV3.2, T-type, Ca2+ channel currents by CaMKIIγC. J. Physiol. 538:343–55
     [Google Scholar]
  80. 80. 
    Klockner U, Lee JH, Cribbs LL, Daud A, Hescheler J et al. 1999. Comparison of the Ca2+ currents induced by expression of three cloned α1 subunits, α1G, α1H and α1I, of low-voltage-activated T-type Ca2+ channels. Eur. J. Neurosci. 11:4171–78
     [Google Scholar]
  81. 81. 
    Martin RL, Lee JH, Cribbs LL, Perez-Reyes E, Hanck DA 2000. Mibefradil block of cloned T-type calcium channels. J. Pharmacol. Exp. Ther. 295:302–8
     [Google Scholar]
  82. 82. 
    Chemin J, Mezghrani A, Bidaud I, Dupasquier S, Marger F et al. 2007. Temperature-dependent modulation of CaV3 T-type calcium channels by protein kinases C and A in mammalian cells. J. Biol. Chem. 282:32710–18
     [Google Scholar]
  83. 83. 
    Kim JA, Park JY, Kang HW, Huh SU, Jeong SW, Lee JH 2006. Augmentation of CaV3.2 T-type calcium channel activity by cAMP-dependent protein kinase A. J. Pharmacol. Exp. Ther. 318:230–37
     [Google Scholar]
  84. 84. 
    Park JY, Kang HW, Moon HJ, Huh SU, Jeong SW et al. 2006. Activation of protein kinase C augments T-type Ca2+ channel activity without changing channel surface density. J. Physiol. 577:513–23
     [Google Scholar]
  85. 85. 
    Lu HK, Fern RJ, Nee JJ, Barrett PQ 1994. Ca2+-dependent activation of T-type Ca2+ channels by calmodulin-dependent protein kinase II. Am. J. Physiol. Ren. Physiol. 267:F183–89
     [Google Scholar]
  86. 86. 
    Yao J, Davies LA, Howard JD, Adney SK, Welsby PJ et al. 2006. Molecular basis for the modulation of native T-type Ca2+ channels in vivo by Ca2+/calmodulin-dependent protein kinase II. J. Clin. Investig. 116:2403–12
     [Google Scholar]
  87. 87. 
    Welsby PJ, Wang H, Wolfe JT, Colbran RJ, Johnson ML, Barrett PQ 2003. A mechanism for the direct regulation of T-type calcium channels by Ca2+/calmodulin-dependent kinase II. J. Neurosci. 23:10116–21
     [Google Scholar]
  88. 88. 
    Iftinca M, Hamid J, Chen L, Varela D, Tadayonnejad R et al. 2007. Regulation of T-type calcium channels by Rho-associated kinase. Nat. Neurosci. 10:854–60
     [Google Scholar]
  89. 89. 
    Wolfe JT, Wang H, Howard J, Garrison JC, Barrett PQ 2003. T-type calcium channel regulation by specific G-protein βγ subunits. Nature 424:209–13
     [Google Scholar]
  90. 90. 
    DePuy SD, Yao J, Hu C, McIntire W, Bidaud I et al. 2006. The molecular basis for T-type Ca2+ channel inhibition by G protein β2γ2 subunits. PNAS 103:14590–95
     [Google Scholar]
  91. 91. 
    Blesneac I, Chemin J, Bidaud I, Huc-Brandt S, Vandermoere F, Lory P 2015. Phosphorylation of the CaV3.2 T-type calcium channel directly regulates its gating properties. PNAS 112:13705–10
     [Google Scholar]
  92. 92. 
    Perez-Reyes E. 2010. Characterization of the gating brake in the I-II loop of CaV3 T-type calcium channels. Channels 4:453–58
     [Google Scholar]
  93. 93. 
    Schrier AD, Wang H, Talley EM, Perez-Reyes E, Barrett PQ 2001. α1H T-type Ca2+ channel is the predominant subtype expressed in bovine and rat zona glomerulosa. Am. J. Physiol. Cell Physiol. 280:C265–72
     [Google Scholar]
  94. 94. 
    Lesouhaitier O, Chiappe A, Rossier MF 2001. Aldosterone increases T-type calcium currents in human adrenocarcinoma (H295R) cells by inducing channel expression. Endocrinology 142:4320–30
     [Google Scholar]
  95. 95. 
    Rossier MF, Lesouhaitier O, Perrier E, Bockhorn L, Chiappe A, Lalevee N 2003. Aldosterone regulation of T-type calcium channels. J. Steroid Biochem. Mol. Biol. 85:383–88
     [Google Scholar]
  96. 96. 
    Felizola SJ, Maekawa T, Nakamura Y, Satoh F, Ono Y et al. 2014. Voltage-gated calcium channels in the human adrenal and primary aldosteronism. J. Steroid Biochem. Mol. Biol. 144:Part B410–16
     [Google Scholar]
  97. 97. 
    Yang T, He M, Zhang H, Barrett P, Hu C 2019. L- and T-type calcium channels control aldosterone production from human adrenals. J. Endocrinol. 244:237–47
     [Google Scholar]
  98. 98. 
    Scholl UI, Goh G, Stolting G, de Oliveira RC, Choi M et al. 2013. Somatic and germline CACNA1D calcium channel mutations in aldosterone-producing adenomas and primary aldosteronism. Nat. Genet. 45:1050–54
     [Google Scholar]
  99. 99. 
    Cohen CJ, McCarthy RT, Barrett PQ, Rasmussen H 1988. Ca channels in adrenal glomerulosa cells: K+ and angiotensin II increase T-type Ca channel current. PNAS 85:2412–16
     [Google Scholar]
  100. 100. 
    Matsunaga H, Yamashita N, Maruyama Y, Kojima I, Kurokawa K 1987. Evidence for two distinct voltage-gated calcium channel currents in bovine adrenal glomerulosa cells. Biochem. Biophys. Res. Commun. 149:1049–54
     [Google Scholar]
  101. 101. 
    Payet MD, Durroux T, Bilodeau L, Guillon G, Gallo-Payet N 1994. Characterization of K+ and Ca2+ ionic currents in glomerulosa cells from human adrenal glands. Endocrinology 134:2589–98
     [Google Scholar]
  102. 102. 
    Rossier MF. 2016. T-type calcium channel: a privileged gate for calcium entry and control of adrenal steroidogenesis. Front. Endocrinol. 7:43
     [Google Scholar]
  103. 103. 
    Barrett PQ, Ertel EA, Smith MM, Nee JJ, Cohen CJ 1995. Voltage-gated calcium currents have two opposing effects on the secretion of aldosterone. Am. J. Physiol. Cell Physiol. 268:C985–92
     [Google Scholar]
  104. 104. 
    Rossier MF, Burnay MM, Vallotton MB, Capponi AM 1996. Distinct functions of T- and L-type calcium channels during activation of bovine adrenal glomerulosa cells. Endocrinology 137:4817–26
     [Google Scholar]
  105. 105. 
    Lenglet S, Louiset E, Delarue C, Vaudry H, Contesse V 2002. Activation of 5-HT7 receptor in rat glomerulosa cells is associated with an increase in adenylyl cyclase activity and calcium influx through T-type calcium channels. Endocrinology 143:1748–60
     [Google Scholar]
  106. 106. 
    Drolet P, Bilodeau L, Chorvatova A, Laflamme L, Gallo-Payet N, Payet MD 1997. Inhibition of the T-type Ca2+ current by the dopamine D1 receptor in rat adrenal glomerulosa cells: requirement of the combined action of the G βγ protein subunit and cyclic adenosine 3′,5′-monophosphate. Mol. Endocrinol. 11:503–14
     [Google Scholar]
  107. 107. 
    Hu C, Depuy SD, Yao J, McIntire WE, Barrett PQ 2009. Protein kinase A activity controls the regulation of T-type CaV3.2 channels by Gβγ dimers. J. Biol. Chem. 284:7465–73
     [Google Scholar]
  108. 108. 
    Lu HK, Fern RJ, Luthin D, Linden J, Liu LP et al. 1996. Angiotensin II stimulates T-type Ca2+ channel currents via activation of a G protein, Gi. Am. J. Physiol. Cell Physiol. 271:C1340–49
     [Google Scholar]
  109. 109. 
    Fern RJ, Hahm MS, Lu HK, Liu LP, Gorelick FS, Barrett PQ 1995. Ca2+/calmodulin-dependent protein kinase II activation and regulation of adrenal glomerulosa Ca2+ signaling. Am. J. Physiol. Ren. Physiol. 269:F751–60
     [Google Scholar]
  110. 110. 
    Barrett PQ, Lu HK, Colbran R, Czernik A, Pancrazio JJ 2000. Stimulation of unitary T-type Ca2+ channel currents by calmodulin-dependent protein kinase II. Am. J. Physiol. Cell Physiol. 279:C1694–703
     [Google Scholar]
  111. 111. 
    Rossier MF, Aptel HB, Python CP, Burnay MM, Vallotton MB, Capponi AM 1995. Inhibition of low threshold calcium channels by angiotensin II in adrenal glomerulosa cells through activation of protein kinase C. J. Biol. Chem. 270:15137–42
     [Google Scholar]
  112. 112. 
    Catterall WA. 2011. Voltage-gated calcium channels. Cold Spring Harb. Perspect. Biol. 3:a003947
     [Google Scholar]
  113. 113. 
    Dolphin AC. 2018. Voltage-gated calcium channel α2δ subunits: an assessment of proposed novel roles. F1000Research 7:1830
     [Google Scholar]
  114. 114. 
    Helton TD, Xu W, Lipscombe D 2005. Neuronal L-type calcium channels open quickly and are inhibited slowly. J. Neurosci. 25:10247–51
     [Google Scholar]
  115. 115. 
    Anderson ME, Braun AP, Schulman H, Premack BA 1994. Multifunctional Ca2+/calmodulin-dependent protein kinase mediates Ca2+-induced enhancement of the L-type Ca2+ current in rabbit ventricular myocytes. Circ. Res. 75:854–61
     [Google Scholar]
  116. 116. 
    Jenkins MA, Christel CJ, Jiao Y, Abiria S, Kim KY et al. 2010. Ca2+-dependent facilitation of CaV1.3 Ca2+ channels by densin and Ca2+/calmodulin-dependent protein kinase II. J. Neurosci. 30:5125–35
     [Google Scholar]
  117. 117. 
    Mahapatra S, Marcantoni A, Zuccotti A, Carabelli V, Carbone E 2012. Equal sensitivity of Cav1.2 and Cav1.3 channels to the opposing modulations of PKA and PKG in mouse chromaffin cells. J. Physiol. 590:5053–73
     [Google Scholar]
  118. 118. 
    Qian H, Patriarchi T, Price JL, Matt L, Lee B et al. 2017. Phosphorylation of Ser1928 mediates the enhanced activity of the L-type Ca2+ channel CaV1.2 by the β2-adrenergic receptor in neurons. Sci. Signal. 10:eaaf9659
     [Google Scholar]
  119. 119. 
    Fischmeister R, Castro L, Abi-Gerges A, Rochais F, Vandecasteele G 2005. Species- and tissue-dependent effects of NO and cyclic GMP on cardiac ion channels. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 142:136–43
     [Google Scholar]
  120. 120. 
    Hofmann F, Flockerzi V, Kahl S, Wegener JW 2014. L-type CaV1.2 calcium channels: from in vitro findings to in vivo function. Physiol. Rev. 94:303–26
     [Google Scholar]
  121. 121. 
    Szabadkai G, Horvath A, Spat A, Enyedi P 1998. Expression of voltage-dependent calcium channel α1 subunits in rat adrenal capsular tissue and single glomerulosa cells. Endocr. Res. 24:425–26
     [Google Scholar]
  122. 122. 
    Xu W, Lipscombe D. 2001. Neuronal CaV1.3α1 L-type channels activate at relatively hyperpolarized membrane potentials and are incompletely inhibited by dihydropyridines. J. Neurosci. 21:5944–51
     [Google Scholar]
  123. 123. 
    Maturana AD, Casal AJ, Demaurex N, Vallotton MB, Capponi AM, Rossier MF 1999. Angiotensin II negatively modulates L-type calcium channels through a pertussis toxin-sensitive G protein in adrenal glomerulosa cells. J. Biol. Chem. 274:19943–48
     [Google Scholar]
  124. 124. 
    Nishimoto K, Tomlins SA, Kuick R, Cani AK, Giordano TJ et al. 2015. Aldosterone-stimulating somatic gene mutations are common in normal adrenal glands. PNAS 112:E4591–99
     [Google Scholar]
  125. 125. 
    Azizan EA, Poulsen H, Tuluc P, Zhou J, Clausen MV et al. 2013. Somatic mutations in ATP1A1 and CACNA1D underlie a common subtype of adrenal hypertension. Nat. Genet. 45:1055–60
     [Google Scholar]
  126. 126. 
    Fernandes-Rosa FL, Williams TA, Riester A, Steichen O, Beuschlein F et al. 2014. Genetic spectrum and clinical correlates of somatic mutations in aldosterone-producing adenoma. Hypertension 64:354–61
     [Google Scholar]
  127. 127. 
    Wei AD, Gutman GA, Aldrich R, Chandy KG, Grissmer S, Wulff H 2005. International Union of Pharmacology. LII. Nomenclature and molecular relationships of calcium-activated potassium channels. Pharmacol. Rev. 57:463–72
     [Google Scholar]
  128. 128. 
    Adelman JP, Maylie J, Sah P 2012. Small-conductance Ca2+-activated K+ channels: form and function. Annu. Rev. Physiol. 74:245–69
     [Google Scholar]
  129. 129. 
    Kaczmarek LK, Aldrich RW, Chandy KG, Grissmer S, Wei AD, Wulff H 2017. International Union of Basic and Clinical Pharmacology. C. Nomenclature and properties of calcium-activated and sodium-activated potassium channels. Pharmacol. Rev. 69:1–11
     [Google Scholar]
  130. 130. 
    Xia XM, Fakler B, Rivard A, Wayman G, Johnson-Pais T et al. 1998. Mechanism of calcium gating in small-conductance calcium-activated potassium channels. Nature 395:503–7
     [Google Scholar]
  131. 131. 
    Yang T, Zhang HL, Liang Q, Shi Y, Mei YA et al. 2016. Small-conductance Ca2+-activated potassium channels negatively regulate aldosterone secretion in human adrenocortical cells. Hypertension 68:785–95
     [Google Scholar]
  132. 132. 
    Nishimoto K, Rigsby CS, Wang T, Mukai K, Gomez-Sanchez CE et al. 2012. Transcriptome analysis reveals differentially expressed transcripts in rat adrenal zona glomerulosa and zona fasciculata. Endocrinology 153:1755–63
     [Google Scholar]
  133. 133. 
    Contreras GF, Castillo K, Enrique N, Carrasquel-Ursulaez W, Castillo JP et al. 2013. A BK (Slo1) channel journey from molecule to physiology. Channels 7:442–58
     [Google Scholar]
  134. 134. 
    Gueguinou M, Chantome A, Fromont G, Bougnoux P, Vandier C, Potier-Cartereau M 2014. KCa and Ca2+ channels: the complex thought. Biochim. Biophys. Acta Mol. Cell Res. 1843:2322–33
     [Google Scholar]
  135. 135. 
    Sausbier M, Arntz C, Bucurenciu I, Zhao H, Zhou XB et al. 2005. Elevated blood pressure linked to primary hyperaldosteronism and impaired vasodilation in BK channel-deficient mice. Circulation 112:60–68
     [Google Scholar]
  136. 136. 
    Rieg T, Vallon V, Sausbier M, Sausbier U, Kaissling B et al. 2007. The role of the BK channel in potassium homeostasis and flow-induced renal potassium excretion. Kidney Int 72:566–73
     [Google Scholar]
  137. 137. 
    Larsen CK, Jensen IS, Sorensen MV, de Bruijn PI, Bleich M et al. 2016. Hyperaldosteronism after decreased renal K+ excretion in KCNMB2 knockout mice. Am. J. Physiol. Ren. Physiol. 310:F1035–46
     [Google Scholar]
  138. 138. 
    Grimm PR, Irsik DL, Settles DC, Holtzclaw JD, Sansom SC 2009. Hypertension of Kcnmb1−/− is linked to deficient K secretion and aldosteronism. PNAS 106:11800–5
     [Google Scholar]
  139. 139. 
    Ha TS, Heo MS, Park CS 2004. Functional effects of auxiliary β4-subunit on rat large-conductance Ca2+-activated K+ channel. Biophys. J. 86:2871–82
     [Google Scholar]
  140. 140. 
    Wulff H, Castle NA, Pardo LA 2009. Voltage-gated potassium channels as therapeutic targets. Nat. Rev. Drug Discov. 8:982–1001
     [Google Scholar]
  141. 141. 
    Long SB, Campbell EB, MacKinnon R 2005. Voltage sensor of Kv1.2: structural basis of electromechanical coupling. Science 309:903–8
     [Google Scholar]
  142. 142. 
    Gutman GA, Chandy KG, Grissmer S, Lazdunski M, McKinnon D et al. 2005. International Union of Pharmacology. LIII. Nomenclature and molecular relationships of voltage-gated potassium channels. Pharmacol. Rev. 57:473–508
     [Google Scholar]
  143. 143. 
    Pongs O, Schwarz JR. 2010. Ancillary subunits associated with voltage-dependent K+ channels. Physiol. Rev. 90:755–96
     [Google Scholar]
  144. 144. 
    Brauneis U, Vassilev PM, Quinn SJ, Williams GH, Tillotson DL 1991. ANG II blocks potassium currents in zona glomerulosa cells from rat, bovine, and human adrenals. Am. J. Physiol. Endocrinol. Metab. 260:E772–79
     [Google Scholar]
  145. 145. 
    Payet MD, Benabderrazik M, Gallo-Payet N 1987. Excitation-secretion coupling: ionic currents in glomerulosa cells: effects of adrenocorticotropin and K+ channel blockers. Endocrinology 121:875–82
     [Google Scholar]
  146. 146. 
    Arrighi I, Bloch-Faure M, Grahammer F, Bleich M, Warth R et al. 2001. Altered potassium balance and aldosterone secretion in a mouse model of human congenital long QT syndrome. PNAS 98:8792–97
     [Google Scholar]
  147. 147. 
    Leng S, Pignatti E, Kehtani RS, Shah MS, Xu S et al. 2020. β-Catenin and FGFR2 regulate postnatal rosette-based adrenocortical morphogenesis. Nat. Commun. 11:1680
     [Google Scholar]
  148. 148. 
    Blankenship JT, Backovic ST, Sanny JS, Weitz O, Zallen JA 2006. Multicellular rosette formation links planar cell polarity to tissue morphogenesis. Dev. Cell 11:459–70
     [Google Scholar]
  149. 149. 
    Freedman BD, Kempna PB, Carlone DL, Shah M, Guagliardo NA et al. 2013. Adrenocortical zonation results from lineage conversion of differentiated zona glomerulosa cells. Dev. Cell 26:666–73
     [Google Scholar]
  150. 150. 
    Lecuit T, Lenne PF. 2007. Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat. Rev. Mol. Cell Biol. 8:633–44
     [Google Scholar]
  151. 151. 
    Bell CL, Murray SA. 2016. Adrenocortical gap junctions and their functions. Front. Endocrinol. 7:82
     [Google Scholar]
  152. 152. 
    Burnstock G, Ralevic V. 2014. Purinergic signaling and blood vessels in health and disease. Pharmacol. Rev. 66:102–92
     [Google Scholar]
  153. 153. 
    Sperelakis N, McConnell K. 2002. Electric field interactions between closely abutting excitable cells. IEEE Eng. Med. Biol. Mag. 21:77–89
     [Google Scholar]
  154. 154. 
    Octeau JC, Gangwani MR, Allam SL, Tran D, Huang S et al. 2019. Transient, consequential increases in extracellular potassium ions accompany channelrhodopsin2 excitation. Cell Rep 27:2249–61.e7
     [Google Scholar]
  155. 155. 
    Ladoux B, Nelson WJ, Yan J, Mege RM 2015. The mechanotransduction machinery at work at adherens junctions. Integr. Biol. 7:1109–19
     [Google Scholar]
  156. 156. 
    Prinz AA, Bucher D, Marder E 2004. Similar network activity from disparate circuit parameters. Nat. Neurosci. 7:1345–52
     [Google Scholar]
/content/journals/10.1146/annurev-physiol-030220-113038
Loading
Ion Channel Function and Electrical Excitability in the Zona Glomerulosa: A Network Perspective on Aldosterone Regulation
Annual Review of Physiology 83, 451 (2021); https://doi.org/10.1146/annurev-physiol-030220-113038
/content/journals/10.1146/annurev-physiol-030220-113038
/content/journals/10.1146/annurev-physiol-030220-113038
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error