Adrenal Anion Channels: New Roles in Zona Glomerulosa Physiology and in the Pathophysiology of Primary Aldosteronism.

Aldosterone CLCN2 Chloride channel ClC-2 Oscillation

Journal

Handbook of experimental pharmacology
ISSN: 0171-2004
Titre abrégé: Handb Exp Pharmacol
Pays: Germany
ID NLM: 7902231

Informations de publication

Date de publication:
27 Jul 2023
Historique:
medline: 27 7 2023
pubmed: 27 7 2023
entrez: 26 7 2023
Statut: aheadofprint

Résumé

The mineralocorticoid aldosterone is produced in the zona glomerulosa of the adrenal cortex. Its synthesis is regulated by the serum concentrations of the peptide hormone angiotensin II and potassium. The primary role of aldosterone is to control blood volume and electrolytes. The autonomous production of aldosterone (primary aldosteronism, PA) is considered the most frequent cause of secondary hypertension. Aldosterone-producing adenomas and (micro-)nodules are frequent causes of PA and often carry somatic mutations in ion channels and transporters. Rare familial forms of PA are due to germline mutations. Both somatic and germline mutations in the chloride channel gene CLCN2, encoding ClC-2, have been identified in PA. Clinical findings and results from cell culture and animal models have advanced our knowledge about the role of anions in PA. The zona glomerulosa of the adrenal gland has now been firmly established as a tissue in which anions play a significant role for signaling. In this overview, we aim to summarize the current knowledge and highlight novel concepts as well as open questions.

Identifiants

pubmed: 37495852
doi: 10.1007/164_2023_680
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2023. The Author(s), under exclusive license to Springer Nature Switzerland AG.

Références

Abou Nader N, Boyer A (2021) Adrenal cortex development and maintenance: knowledge acquired from mouse models. Endocrinology 162(12). https://doi.org/10.1210/endocr/bqab187
Ahmed N, Ramjeesingh M, Wong S, Varga A, Garami E, Bear CE (2000) Chloride channel activity of ClC-2 is modified by the actin cytoskeleton. Biochem J 352(Pt 3):789–794
Azizan EA, Poulsen H, Tuluc P, Zhou J, Clausen MV, Lieb A, Maniero C, Garg S, Bochukova EG, Zhao W, Shaikh LH, Brighton CA, Teo AE, Davenport AP, Dekkers T, Tops B, Kusters B, Ceral J, Yeo GS, Neogi SG, McFarlane I, Rosenfeld N, Marass F, Hadfield J, Margas W, Chaggar K, Solar M, Deinum J, Dolphin AC, Farooqi IS, Striessnig J, Nissen P, Brown MJ (2013) Somatic mutations in ATP1A1 and CACNA1D underlie a common subtype of adrenal hypertension. Nat Genet 45(9):1055–1060. https://doi.org/10.1038/ng.2716
doi: 10.1038/ng.2716
Ben-Ari Y, Khalilov I, Kahle KT, Cherubini E (2012) The GABA excitatory/inhibitory shift in brain maturation and neurological disorders. Neuroscientist 18(5):467–486. https://doi.org/10.1177/1073858412438697
doi: 10.1177/1073858412438697
Beuschlein F, Boulkroun S, Osswald A, Wieland T, Nielsen HN, Lichtenauer UD, Penton D, Schack VR, Amar L, Fischer E, Walther A, Tauber P, Schwarzmayr T, Diener S, Graf E, Allolio B, Samson-Couterie B, Benecke A, Quinkler M, Fallo F, Plouin PF, Mantero F, Meitinger T, Mulatero P, Jeunemaitre X, Warth R, Vilsen B, Zennaro MC, Strom TM, Reincke M (2013) Somatic mutations in ATP1A1 and ATP2B3 lead to aldosterone-producing adenomas and secondary hypertension. Nat Genet 45(4):440–444. https://doi.org/10.1038/ng.2550
doi: 10.1038/ng.2550
Blanz J, Schweizer M, Auberson M, Maier H, Muenscher A, Hubner CA, Jentsch TJ (2007) Leukoencephalopathy upon disruption of the chloride channel ClC-2. J Neurosci 27(24):6581–6589. https://doi.org/10.1523/JNEUROSCI.0338-07.2007
doi: 10.1523/JNEUROSCI.0338-07.2007
Bosl MR, Stein V, Hubner C, Zdebik AA, Jordt SE, Mukhopadhyay AK, Davidoff MS, Holstein AF, Jentsch TJ (2001) Male germ cells and photoreceptors, both dependent on close cell-cell interactions, degenerate upon ClC-2 cl(−) channel disruption. EMBO J 20(6):1289–1299. https://doi.org/10.1093/emboj/20.6.1289
doi: 10.1093/emboj/20.6.1289
Catalan M, Cornejo I, Figueroa CD, Niemeyer MI, Sepulveda FV, Cid LP (2002) ClC-2 in Guinea pig colon: mRNA, immunolabeling, and functional evidence for surface epithelium localization. Am J Physiol Gastrointest Liver Physiol 283(4):G1004–G1013. https://doi.org/10.1152/ajpgi.00158.2002
doi: 10.1152/ajpgi.00158.2002
Choi M, Scholl UI, Yue P, Bjorklund P, Zhao B, Nelson-Williams C, Ji W, Cho Y, Patel A, Men CJ, Lolis E, Wisgerhof MV, Geller DS, Mane S, Hellman P, Westin G, Akerstrom G, Wang W, Carling T, Lifton RP (2011) K+ channel mutations in adrenal aldosterone-producing adenomas and hereditary hypertension. Science 331(6018):768–772. https://doi.org/10.1126/science.1198785
doi: 10.1126/science.1198785
Chorvatova A, Gendron L, Bilodeau L, Gallo-Payet N, Payet MD (2000) A Ras-dependent chloride current activated by adrenocorticotropin in rat adrenal zona glomerulosa cells. Endocrinology 141(2):684–692. https://doi.org/10.1210/endo.141.2.7328
doi: 10.1210/endo.141.2.7328
Cohen JJ, Hulter HN, Smithline N, Melby JC, Schwartz WB (1976) The critical role of the adrenal gland in the renal regulation of acid-base equilibrium during chronic hypotonic expansion. Evidence that chronic hyponatremia is a potent stimulus to aldosterone secretion. J Clin Invest 58(5):1201–1208. https://doi.org/10.1172/JCI108573
doi: 10.1172/JCI108573
Collaboration NCDRF (2021) Worldwide trends in hypertension prevalence and progress in treatment and control from 1990 to 2019: a pooled analysis of 1201 population-representative studies with 104 million participants. Lancet 398(10304):957–980. https://doi.org/10.1016/S0140-6736(21)01330-1
doi: 10.1016/S0140-6736(21)01330-1
de Santiago JA, Nehrke K, Arreola J (2005) Quantitative analysis of the voltage-dependent gating of mouse parotid ClC-2 chloride channel. J Gen Physiol 126(6):591–603. https://doi.org/10.1085/jgp.200509310
doi: 10.1085/jgp.200509310
Depienne C, Bugiani M, Dupuits C, Galanaud D, Touitou V, Postma N, van Berkel C, Polder E, Tollard E, Darios F, Brice A, de Die-Smulders CE, Vles JS, Vanderver A, Uziel G, Yalcinkaya C, Frints SG, Kalscheuer VM, Klooster J, Kamermans M, Abbink TE, Wolf NI, Sedel F, van der Knaap MS (2013) Brain white matter oedema due to ClC-2 chloride channel deficiency: an observational analytical study. Lancet Neurol 12(7):659–668. https://doi.org/10.1016/S1474-4422(13)70053-X
doi: 10.1016/S1474-4422(13)70053-X
Dutta RK, Arnesen T, Heie A, Walz M, Alesina P, Soderkvist P, Gimm O (2019) A somatic mutation in CLCN2 identified in a sporadic aldosterone-producing adenoma. Eur J Endocrinol 181(5):K37–K41. https://doi.org/10.1530/EJE-19-0377
doi: 10.1530/EJE-19-0377
Elias H, Pauly JE (1956) The structure of the human adrenal cortex. Endocrinology 58(6):714–738. https://doi.org/10.1210/endo-58-6-714
doi: 10.1210/endo-58-6-714
Fernandes-Rosa FL, Daniil G, Orozco IJ, Goppner C, El Zein R, Jain V, Boulkroun S, Jeunemaitre X, Amar L, Lefebvre H, Schwarzmayr T, Strom TM, Jentsch TJ, Zennaro MC (2018) A gain-of-function mutation in the CLCN2 chloride channel gene causes primary aldosteronism. Nat Genet 50(3):355–361. https://doi.org/10.1038/s41588-018-0053-8
doi: 10.1038/s41588-018-0053-8
Funder JW, Carey RM, Mantero F, Murad MH, Reincke M, Shibata H, Stowasser M, Young WF Jr (2016) The management of primary aldosteronism: case detection, diagnosis, and treatment: an endocrine society clinical practice guideline. J Clin Endocrinol Metab 101(5):1889–1916. https://doi.org/10.1210/jc.2015-4061
doi: 10.1210/jc.2015-4061
Gaitan-Penas H, Apaja PM, Arnedo T, Castellanos A, Elorza-Vidal X, Soto D, Gasull X, Lukacs GL, Estevez R (2017) Leukoencephalopathy-causing CLCN2 mutations are associated with impaired Cl(−) channel function and trafficking. J Physiol 595(22):6993–7008. https://doi.org/10.1113/JP275087
doi: 10.1113/JP275087
Gancayco CA, Gerding MR, Breault DT, Beenhakker MP, Barrett PQ, Guagliardo NA (2022) Intrinsic adrenal TWIK-related acid-sensitive TASK channel dysfunction produces spontaneous calcium oscillations sufficient to drive AngII (angiotensin II)-unresponsive hyperaldosteronism. Hypertension 79(11):2552–2564. https://doi.org/10.1161/HYPERTENSIONAHA.122.19557
doi: 10.1161/HYPERTENSIONAHA.122.19557
Garcia-Olivares J, Alekov A, Boroumand MR, Begemann B, Hidalgo P, Fahlke C (2008) Gating of human ClC-2 chloride channels and regulation by carboxy-terminal domains. J Physiol 586(22):5325–5336. https://doi.org/10.1113/jphysiol.2008.158097
doi: 10.1113/jphysiol.2008.158097
Goppner C, Orozco IJ, Hoegg-Beiler MB, Soria AH, Hubner CA, Fernandes-Rosa FL, Boulkroun S, Zennaro MC, Jentsch TJ (2019) Pathogenesis of hypertension in a mouse model for human CLCN2 related hyperaldosteronism. Nat Commun 10(1):4678. https://doi.org/10.1038/s41467-019-12113-9
doi: 10.1038/s41467-019-12113-9
Goppner C, Soria AH, Hoegg-Beiler MB, Jentsch TJ (2021) Cellular basis of ClC-2 Cl(−) channel-related brain and testis pathologies. J Biol Chem 296:100074. https://doi.org/10.1074/jbc.RA120.016031
doi: 10.1074/jbc.RA120.016031
Grunder S, Thiemann A, Pusch M, Jentsch TJ (1992) Regions involved in the opening of CIC-2 chloride channel by voltage and cell volume. Nature 360(6406):759–762. https://doi.org/10.1038/360759a0
doi: 10.1038/360759a0
Hayama N, Wang W, Schneider EG (1995) Osmolality-induced changes in aldosterone secretion involve a chloride-dependent process. Am J Phys 268(1 Pt 2):R8–R13. https://doi.org/10.1152/ajpregu.1995.268.1.R8
Hinzpeter A, Fritsch J, Borot F, Trudel S, Vieu DL, Brouillard F, Baudouin-Legros M, Clain J, Edelman A, Ollero M (2007) Membrane cholesterol content modulates ClC-2 gating and sensitivity to oxidative stress. J Biol Chem 282(4):2423–2432. https://doi.org/10.1074/jbc.M608251200
doi: 10.1074/jbc.M608251200
Hoffmann EK, Lambert IH, Pedersen SF (2009) Physiology of cell volume regulation in vertebrates. Physiol Rev 89(1):193–277. https://doi.org/10.1152/physrev.00037.2007
doi: 10.1152/physrev.00037.2007
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 Invest 122(6):2046–2053. https://doi.org/10.1172/JCI61996
doi: 10.1172/JCI61996
Huang ZM, Prasad C, Britton FC, Ye LL, Hatton WJ, Duan D (2009) Functional role of CLC-2 chloride inward rectifier channels in cardiac sinoatrial nodal pacemaker cells. J Mol Cell Cardiol 47(1):121–132. https://doi.org/10.1016/j.yjmcc.2009.04.008
doi: 10.1016/j.yjmcc.2009.04.008
Jaffe G, Gray Z, Krishnan G, Stedman M, Zheng Y, Han J, Chertow GM, Leppert JT, Bhalla V (2020) Screening rates for primary aldosteronism in resistant hypertension: a cohort study. Hypertension 75(3):650–659. https://doi.org/10.1161/HYPERTENSIONAHA.119.14359
doi: 10.1161/HYPERTENSIONAHA.119.14359
Jentsch TJ, Pusch M (2018) CLC chloride channels and transporters: structure, function, physiology, and disease. Physiol Rev 98(3):1493–1590. https://doi.org/10.1152/physrev.00047.2017
doi: 10.1152/physrev.00047.2017
Jeworutzki E, Lopez-Hernandez T, Capdevila-Nortes X, Sirisi S, Bengtsson L, Montolio M, Zifarelli G, Arnedo T, Muller CS, Schulte U, Nunes V, Martinez A, Jentsch TJ, Gasull X, Pusch M, Estevez R (2012) GlialCAM, a protein defective in a leukodystrophy, serves as a ClC-2 Cl(−) channel auxiliary subunit. Neuron 73(5):951–961. https://doi.org/10.1016/j.neuron.2011.12.039
doi: 10.1016/j.neuron.2011.12.039
Jordt SE, Jentsch TJ (1997) Molecular dissection of gating in the ClC-2 chloride channel. EMBO J 16(7):1582–1592. https://doi.org/10.1093/emboj/16.7.1582
doi: 10.1093/emboj/16.7.1582
Kojima I, Kojima K, Kreutter D, Rasmussen H (1984) The temporal integration of the aldosterone secretory response to angiotensin occurs via two intracellular pathways. J Biol Chem 259(23):14448–14457
Koster AK, Reese AL, Kuryshev Y, Wen X, McKiernan KA, Gray EE, Wu C, Huguenard JR, Maduke M, Du Bois J (2020) Development and validation of a potent and specific inhibitor for the CLC-2 chloride channel. Proc Natl Acad Sci U S A 117(51):32711–32721. https://doi.org/10.1073/pnas.2009977117
doi: 10.1073/pnas.2009977117
Lifton RP, Dluhy RG, Powers M, Rich GM, Cook S, Ulick S, Lalouel JM (1992) A chimaeric 11 beta-hydroxylase/aldosterone synthase gene causes glucocorticoid-remediable aldosteronism and human hypertension. Nature 355(6357):262–265. https://doi.org/10.1038/355262a0
doi: 10.1038/355262a0
Losel R, Wehling M (2003) Nongenomic actions of steroid hormones. Nat Rev Mol Cell Biol 4(1):46–56. https://doi.org/10.1038/nrm1009
doi: 10.1038/nrm1009
Lu NZ, Wardell SE, Burnstein KL, Defranco D, Fuller PJ, Giguere V, Hochberg RB, McKay L, Renoir JM, Weigel NL, Wilson EM, McDonnell DP, Cidlowski JA (2006) International Union of Pharmacology. LXV. The pharmacology and classification of the nuclear receptor superfamily: glucocorticoid, mineralocorticoid, progesterone, and androgen receptors. Pharmacol Rev 58(4):782–797. https://doi.org/10.1124/pr.58.4.9
doi: 10.1124/pr.58.4.9
Ma T, Wang L, Chai A, Liu C, Cui W, Yuan S, Wing Ngor AS, Sun L, Zhang X, Zhang Z, Lu J, Gao Y, Wang P, Li Z, Liang Y, Vogel H, Wang YT, Wang D, Yan K, Zhang H (2023) Cryo-EM structures of ClC-2 chloride channel reveal the blocking mechanism of its specific inhibitor AK-42. Nat Commun 14(1):3424. https://doi.org/10.1038/s41467-023-39218-6
doi: 10.1038/s41467-023-39218-6
Maniero C, Zhou J, Shaikh LH, Azizan EA, McFarlane I, Neogi S, Scudieri P, Galietta LJ, Brown MJ (2015) Role of ANO4 in regulation of aldosterone secretion in the zona glomerulosa of the human adrenal gland. Lancet 385 Suppl 1:S62. https://doi.org/10.1016/S0140-6736(15)60377-4
doi: 10.1016/S0140-6736(15)60377-4
Monticone S, Burrello J, Tizzani D, Bertello C, Viola A, Buffolo F, Gabetti L, Mengozzi G, Williams TA, Rabbia F, Veglio F, Mulatero P (2017) Prevalence and clinical manifestations of primary aldosteronism encountered in primary care practice. J Am Coll Cardiol 69(14):1811–1820. https://doi.org/10.1016/j.jacc.2017.01.052
doi: 10.1016/j.jacc.2017.01.052
Nanba K, Rainey WE (2021) GENETICS IN ENDOCRINOLOGY: impact of race and sex on genetic causes of aldosterone-producing adenomas. Eur J Endocrinol 185(1):R1–R11. https://doi.org/10.1530/EJE-21-0031
doi: 10.1530/EJE-21-0031
Nanba K, Blinder AR, Rege J, Hattangady NG, Else T, Liu CJ, Tomlins SA, Vats P, Kumar-Sinha C, Giordano TJ, Rainey WE (2020) Somatic CACNA1H mutation as a cause of aldosterone-producing adenoma. Hypertension 75(3):645–649. https://doi.org/10.1161/HYPERTENSIONAHA.119.14349
doi: 10.1161/HYPERTENSIONAHA.119.14349
Nishimoto K, Tomlins SA, Kuick R, Cani AK, Giordano TJ, Hovelson DH, Liu CJ, Sanjanwala AR, Edwards MA, Gomez-Sanchez CE, Nanba K, Rainey WE (2015) Aldosterone-stimulating somatic gene mutations are common in normal adrenal glands. Proc Natl Acad Sci U S A 112(33):E4591–E4599. https://doi.org/10.1073/pnas.1505529112
doi: 10.1073/pnas.1505529112
Omata K, Anand SK, Hovelson DH, Liu CJ, Yamazaki Y, Nakamura Y, Ito S, Satoh F, Sasano H, Rainey WE, Tomlins SA (2017) Aldosterone-producing cell clusters frequently harbor somatic mutations and accumulate with age in normal adrenals. J Endocr Soc 1(7):787–799. https://doi.org/10.1210/js.2017-00134
doi: 10.1210/js.2017-00134
Omata K, Satoh F, Morimoto R, Ito S, Yamazaki Y, Nakamura Y, Anand SK, Guo Z, Stowasser M, Sasano H, Tomlins SA, Rainey WE (2018) Cellular and genetic causes of idiopathic hyperaldosteronism. Hypertension 72(4):874–880. https://doi.org/10.1161/HYPERTENSIONAHA.118.11086
doi: 10.1161/HYPERTENSIONAHA.118.11086
Park E, MacKinnon R (2018) Structure of the CLC-1 chloride channel from Homo sapiens. elife 7. https://doi.org/10.7554/eLife.36629
Park E, Campbell EB, MacKinnon R (2017) Structure of a CLC chloride ion channel by cryo-electron microscopy. Nature 541(7638):500–505. https://doi.org/10.1038/nature20812
doi: 10.1038/nature20812
Penton D, Bandulik S, Schweda F, Haubs S, Tauber P, Reichold M, Cong LD, El Wakil A, Budde T, Lesage F, Lalli E, Zennaro MC, Warth R, Barhanin J (2012) Task3 potassium channel gene invalidation causes low renin and salt-sensitive arterial hypertension. Endocrinology 153(10):4740–4748. https://doi.org/10.1210/en.2012-1527
doi: 10.1210/en.2012-1527
Rege J, Nanba K, Blinder AR, Plaska S, Udager AM, Vats P, Kumar-Sinha C, Giordano TJ, Rainey WE, Else T (2020) Identification of somatic mutations in CLCN2 in aldosterone-producing adenomas. J Endocr Soc 4(10):bvaa123. https://doi.org/10.1210/jendso/bvaa123
doi: 10.1210/jendso/bvaa123
Rege J, Nanba K, Bandulik S, Kosmann C, Blinder AR, Vats P, Kumar-Sinha C, Lerario AM, Else T, Yamazaki Y (2022) Zinc transporter somatic gene mutations cause primary aldosteronism. bioRxiv:2022.2007. 2025.501443
Reichhart N, Schoberl S, Keckeis S, Alfaar AS, Roubeix C, Cordes M, Crespo-Garcia S, Haeckel A, Kociok N, Fockler R, Fels G, Mataruga A, Rauh R, Milenkovic VM, Zuhlke K, Klussmann E, Schellenberger E, Strauss O (2019) Anoctamin-4 is a bona fide Ca(2+)-dependent non-selective cation channel. Sci Rep 9(1):2257. https://doi.org/10.1038/s41598-018-37287-y
doi: 10.1038/s41598-018-37287-y
Rossi GP, Bernini G, Caliumi C, Desideri G, Fabris B, Ferri C, Ganzaroli C, Giacchetti G, Letizia C, Maccario M, Mallamaci F, Mannelli M, Mattarello MJ, Moretti A, Palumbo G, Parenti G, Porteri E, Semplicini A, Rizzoni D, Rossi E, Boscaro M, Pessina AC, Mantero F (2006) A prospective study of the prevalence of primary aldosteronism in 1,125 hypertensive patients. J Am Coll Cardiol 48(11):2293–2300. https://doi.org/10.1016/j.jacc.2006.07.059
doi: 10.1016/j.jacc.2006.07.059
Saint-Martin C, Gauvain G, Teodorescu G, Gourfinkel-An I, Fedirko E, Weber YG, Maljevic S, Ernst JP, Garcia-Olivares J, Fahlke C, Nabbout R, LeGuern E, Lerche H, Poncer JC, Depienne C (2009) Two novel CLCN2 mutations accelerating chloride channel deactivation are associated with idiopathic generalized epilepsy. Hum Mutat 30(3):397–405. https://doi.org/10.1002/humu.20876
doi: 10.1002/humu.20876
Schewe J, Seidel E, Forslund S, Marko L, Peters J, Muller DN, Fahlke C, Stolting G, Scholl U (2019) Elevated aldosterone and blood pressure in a mouse model of familial hyperaldosteronism with ClC-2 mutation. Nat Commun 10(1):5155. https://doi.org/10.1038/s41467-019-13033-4
doi: 10.1038/s41467-019-13033-4
Scholl UI, Nelson-Williams C, Yue P, Grekin R, Wyatt RJ, Dillon MJ, Couch R, Hammer LK, Harley FL, Farhi A, Wang WH, Lifton RP (2012) Hypertension with or without adrenal hyperplasia due to different inherited mutations in the potassium channel KCNJ5. Proc Natl Acad Sci U S A 109(7):2533–2538. https://doi.org/10.1073/pnas.1121407109
doi: 10.1073/pnas.1121407109
Scholl UI, Goh G, Stolting G, de Oliveira RC, Choi M, Overton JD, Fonseca AL, Korah R, Starker LF, Kunstman JW, Prasad ML, Hartung EA, Mauras N, Benson MR, Brady T, Shapiro JR, Loring E, Nelson-Williams C, Libutti SK, Mane S, Hellman P, Westin G, Akerstrom G, Bjorklund P, Carling T, Fahlke C, Hidalgo P, Lifton RP (2013) Somatic and germline CACNA1D calcium channel mutations in aldosterone-producing adenomas and primary aldosteronism. Nat Genet 45(9):1050–1054. https://doi.org/10.1038/ng.2695
doi: 10.1038/ng.2695
Scholl UI, Stolting G, Nelson-Williams C, Vichot AA, Choi M, Loring E, Prasad ML, Goh G, Carling T, Juhlin CC, Quack I, Rump LC, Thiel A, Lande M, Frazier BG, Rasoulpour M, Bowlin DL, Sethna CB, Trachtman H, Fahlke C, Lifton RP (2015) Recurrent gain of function mutation in calcium channel CACNA1H causes early-onset hypertension with primary aldosteronism. elife 4. https://doi.org/10.7554/eLife.06315
Scholl UI, Stolting G, Schewe J, Thiel A, Tan H, Nelson-Williams C, Vichot AA, Jin SC, Loring E, Untiet V, Yoo T, Choi J, Xu S, Wu A, Kirchner M, Mertins P, Rump LC, Onder AM, Gamble C, McKenney D, Lash RW, Jones DP, Chune G, Gagliardi P, Choi M, Gordon R, Stowasser M, Fahlke C, Lifton RP (2018) CLCN2 chloride channel mutations in familial hyperaldosteronism type II. Nat Genet 50(3):349–354. https://doi.org/10.1038/s41588-018-0048-5
doi: 10.1038/s41588-018-0048-5
Seidel E, Schewe J, Zhang J, Dinh HA, Forslund SK, Marko L, Hellmig N, Peters J, Muller DN, Lifton RP, Nottoli T, Stolting G, Scholl UI (2021) Enhanced Ca(2+) signaling, mild primary aldosteronism, and hypertension in a familial hyperaldosteronism mouse model (Cacna1h (M1560V/+) ). Proc Natl Acad Sci U S A 118(17). https://doi.org/10.1073/pnas.2014876118
Spat A, Hunyady L (2004) Control of aldosterone secretion: a model for convergence in cellular signaling pathways. Physiol Rev 84(2):489–539. https://doi.org/10.1152/physrev.00030.2003
doi: 10.1152/physrev.00030.2003
Spyroglou A, Bozoglu T, Rawal R, De Leonardis F, Sterner C, Boulkroun S, Benecke AG, Monti L, Zennaro MC, Petersen AK, Doring A, Rossi A, Bidlingmaier M, Warth R, Gieger C, Reincke M, Beuschlein F (2014) Diastrophic dysplasia sulfate transporter (SLC26A2) is expressed in the adrenal cortex and regulates aldosterone secretion. Hypertension 63(5):1102–1109. https://doi.org/10.1161/HYPERTENSIONAHA.113.02504
doi: 10.1161/HYPERTENSIONAHA.113.02504
Stolting G, Teodorescu G, Begemann B, Schubert J, Nabbout R, Toliat MR, Sander T, Nurnberg P, Lerche H, Fahlke C (2013) Regulation of ClC-2 gating by intracellular ATP. Pflugers Arch 465(10):1423–1437. https://doi.org/10.1007/s00424-013-1286-0
doi: 10.1007/s00424-013-1286-0
Stolting G, Fischer M, Fahlke C (2014) CLC channel function and dysfunction in health and disease. Front Physiol 5:378. https://doi.org/10.3389/fphys.2014.00378
doi: 10.3389/fphys.2014.00378
Stowasser M, Gordon RD, Tunny TJ, Klemm SA, Finn WL, Krek AL (1992) Familial hyperaldosteronism type II: five families with a new variety of primary aldosteronism. Clin Exp Pharmacol Physiol 19(5):319–322
Tadjine M, Lampron A, Ouadi L, Bourdeau I (2008) Frequent mutations of beta-catenin gene in sporadic secreting adrenocortical adenomas. Clin Endocrinol 68(2):264–270. https://doi.org/10.1111/j.1365-2265.2007.03033.x
doi: 10.1111/j.1365-2265.2007.03033.x
Thiemann A, Grunder S, Pusch M, Jentsch TJ (1992) A chloride channel widely expressed in epithelial and non-epithelial cells. Nature 356(6364):57–60. https://doi.org/10.1038/356057a0
doi: 10.1038/356057a0
Timmermans S, Souffriau J, Libert C (2019) A general introduction to glucocorticoid biology. Front Immunol 10:1545. https://doi.org/10.3389/fimmu.2019.01545
doi: 10.3389/fimmu.2019.01545
Tuzel IH (1981) Comparison of adverse reactions to bumetanide and furosemide. J Clin Pharmacol 21(11):615–619. https://doi.org/10.1002/j.1552-4604.1981.tb05673.x
doi: 10.1002/j.1552-4604.1981.tb05673.x
Varela D, Niemeyer MI, Cid LP, Sepulveda FV (2002) Effect of an N-terminus deletion on voltage-dependent gating of the ClC-2 chloride channel. J Physiol 544(Pt 2):363–372
Wang W, Schneider EG (1997) Potassium-induced aldosterone secretion involves a Cl(−)-dependent mechanism. Am J Phys 272(1 Pt 2):R183–R187. https://doi.org/10.1152/ajpregu.1997.272.1.R183
doi: 10.1152/ajpregu.1997.272.1.R183
Wilke BU, Lindner M, Greifenberg L, Albus A, Kronimus Y, Bunemann M, Leitner MG, Oliver D (2014) Diacylglycerol mediates regulation of TASK potassium channels by Gq-coupled receptors. Nat Commun 5:5540. https://doi.org/10.1038/ncomms6540
doi: 10.1038/ncomms6540
Williams TA, Gomez-Sanchez CE, Rainey WE, Giordano TJ, Lam AK, Marker A, Mete O, Yamazaki Y, Zerbini MCN, Beuschlein F, Satoh F, Burrello J, Schneider H, Lenders JWM, Mulatero P, Castellano I, Knosel T, Papotti M, Saeger W, Sasano H, Reincke M (2021) International histopathology consensus for unilateral primary aldosteronism. J Clin Endocrinol Metab 106(1):42–54. https://doi.org/10.1210/clinem/dgaa484
doi: 10.1210/clinem/dgaa484
Wu X, Garg S, Cabrera C, Azizan E, Zhou J, Mein C, Takaoka Y, Wozniak E, Zhao W, Marker A (2019) Somatic transmembrane domain mutations of a cell adhesion molecule, CADM1, cause primary aldosteronism by preventing gap junction communication between adrenocortical cells. In: Endocrine abstracts. Bioscientifica
Wu CH, Peng KY, Hwang DY, Lin YH, Wu VC, Chueh JS (2021) Novel mutations detection with next-generation sequencing and its association with clinical outcome in unilateral primary aldosteronism. Biomedicine 9(9). https://doi.org/10.3390/biomedicines9091167
Zhou J, Azizan EAB, Cabrera CP, Fernandes-Rosa FL, Boulkroun S, Argentesi G, Cottrell E, Amar L, Wu X, O'Toole S, Goodchild E, Marker A, Senanayake R, Garg S, Akerstrom T, Backman S, Jordan S, Polubothu S, Berney DM, Gluck A, Lines KE, Thakker RV, Tuthill A, Joyce C, Kaski JP, Karet Frankl FE, Metherell LA, Teo AED, Gurnell M, Parvanta L, Drake WM, Wozniak E, Klinzing D, Kuan JL, Tiang Z, Gomez Sanchez CE, Hellman P, Foo RSY, Mein CA, Kinsler VA, Bjorklund P, Storr HL, Zennaro MC, Brown MJ (2021) Somatic mutations of GNA11 and GNAQ in CTNNB1-mutant aldosterone-producing adenomas presenting in puberty, pregnancy or menopause. Nat Genet 53(9):1360–1372. https://doi.org/10.1038/s41588-021-00906-y
doi: 10.1038/s41588-021-00906-y

Auteurs

Gabriel Stölting (G)

Center of Functional Genomics, Berlin Institute of Health at Charité - Universitätsmedizin Berlin, Berlin, Germany.

Ute I Scholl (UI)

Center of Functional Genomics, Berlin Institute of Health at Charité - Universitätsmedizin Berlin, Berlin, Germany. ute.scholl@bih-charite.de.

Classifications MeSH