Somatic mutations of the ATP1A1 gene and aldosterone-producing adenomas

Molecular and Cellular Endocrinology

Volumn 408, Issue , 2015, Pages 213-219

  Gomez Sanchez, Celso E ^a,b   Kuppusamy, Maniselvan ^b   Gomez Sanchez, Elise P ^b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

Author keywords

Aldosterone producing adenomas; Primary aldosteronism; Sodium potassium ATPase

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ALDOSTERONE;

ADENOMA; ANIMAL; BIOLOGICAL MODEL; BIOSYNTHESIS; CHEMISTRY; ENZYMOLOGY; GENETICS; HUMAN; MUTATION;

ADENOMA; ALDOSTERONE; ANIMALS; HUMANS; MODELS, BIOLOGICAL; MUTATION; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 84939939176     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2014.12.004     Document Type: Review

References (63)

1. Abdelhamid S., Blomer R., Hommel G., Haack D., Lewicka S., Fiegel P., et al. Urinary tetrahydroaldosterone as a screening method for primary aldosteronism: a comparative study. Am. J. Hypertens 2003, 16:522-530.
2. Akerstrom T., Crona J., Delgado Verdugo A., Starker L.F., Cupisti K., Willenberg H.S., et al. Comprehensive re-sequencing of adrenal aldosterone producing lesions reveal three somatic mutations near the kcnj5 potassium channel selectivity filter. PLoS ONE 2012, 7. e41926.
3. Antonipillai I., Schick K., Horton R. Ouabain is a potent inhibitor of aldosterone secretion and angiotensin action in the human adrenal. J. Clin. Endocrinol. Metab 1996, 81:2335-2337.
4. Aperia A. New roles for an old enzyme: Na,K-ATPase emerges as an interesting drug target. J. Intern. Med 2007, 261:44-52.
5. Aperia A. 2011 Homer Smith Award: to serve and protect: classic and novel roles for Na+, K+-adenosine triphosphatase. J. Am. Soc. Nephrol 2012, 23:1283-1290.
6. Azizan E.A., Murthy M., Stowasser M., Gordon R., Kowalski B., Xu S., et al. Somatic mutations affecting the selectivity filter of KCNJ5 are frequent in 2 large unselected collections of adrenal aldosteronomas. Hypertension 2012, 59:587-591.
7. Azizan E.A., Poulsen H., Tuluc P., Zhou J., Clausen M.V., Lieb A., et al. Somatic mutations in ATP1A1 and CACNA1D underlie a common subtype of adrenal hypertension. Nat. Genet 2013, 45:1055-1060.
8. Berglund G., Andersson O., Wilhelmsen L. Prevalence of primary and secondary hypertension: studies in a random population sample. Br. Med. J. 1976, 2:554-556.
9. Beuschlein F., Boulkroun S., Osswald A., Wieland T., Nielsen H.N., Lichtenauer U.D., et al. Somatic mutations in ATP1A1 and ATP2B3 lead to aldosterone-producing adenomas and secondary hypertension. Nat. Genet 2013, 45:440-444.
10. Boulkroun S., Samson-Couterie B., Dzib J.F., Lefebvre H., Louiset E., Amar L., et al. Adrenal cortex remodeling and functional zona glomerulosa hyperplasia in primary aldosteronism. Hypertension 2010, 56:885-892.
11. Boulkroun S., Samson-Couterie B., Golib-Dzib J.F., Amar L., Plouin P.F., Sibony M., et al. Aldosterone-producing adenoma formation in the adrenal cortex involves expression of stem/progenitor cell markers. Endocrinology 2011, 152:4753-4763.
12. Boulkroun S., Beuschlein F., Rossi G.P., Golib-Dzib J.F., Fischer E., Amar L., et al. Prevalence, clinical, and molecular correlates of KCNJ5 mutations in primary aldosteronism. Hypertension 2012, 59:592-598.
13. Choi M., Scholl U.I., Yue P., Bjorklund P., Zhao B., Nelson-Williams C., et al. K+ channel mutations in adrenal aldosterone-producing adenomas and hereditary hypertension. Science 2011, 331:768-772.
14. Conn J.W. Primary aldosteronism, a new clinical syndrome. J. Lab. Clin. Med 1955, 45:3-7.
15. Conn J.W., Knopf R.F., Nesbit R.M. Clinical characteristics of primary aldosteronism from an analysis of 145 cases. Am. J. Surg 1964, 107:159-172.
16. Dekkers T., ter Meer M., Lenders J.W., Hermus A.R., Schultze Kool L., Langenhuijsen J.F., et al. Adrenal nodularity and somatic mutations in primary aldosteronism: one node is the culprit?. J. Clin. Endocrinol. Metab 2014, 99:E1341-E1351.
17. Dutta R.K., Welander J., Brauckhoff M., Walz M., Alesina P., Arnesen T., et al. Complementary somatic mutations of KCNJ5, ATP1A1, and ATP2B3 in sporadic aldosterone producing adrenal adenomas. Endocr. Relat. Cancer 2014, 21:L1-L4.
18. Einholm A.P., Andersen J.P., Vilsen B. Importance of Leu99 in transmembrane segment M1 of the Na+, K+-ATPase in the binding and occlusion of K . J. Biol. Chem 2007, 282:23854-23866.
19. Einholm A.P., Andersen J.P., Vilsen B. Roles of transmembrane segment M1 of Na+,K+-ATPase and Ca2-ATPase, the gatekeeper and the pivot. J. Bioenerg. Biomembr 2007, 39:357-366.
20. Fardella C.E., Mosso L., Gomez-Sanchez C.E., Soto J., Montero J., Gomez L., et al. Primary hyperaldosteronism in essential hypertensives: prevalence, biochemical profile and molecular biology. J. Clin. Endocrinol. Metab 2000, 85:1863-1867.
21. Feraille E., Doucet A. Sodium-potassium-adenosinetriphosphatase-dependent sodium transport in the kidney: hormonal control. Physiol. Rev 2001, 81:345-418.
22. Fernandes-Rosa F.L., Williams T.A., Riester A., Steichen O., Beuschlein F., Boulkroun S., et al. Genetic spectrum and clinical correlates of somatic mutations in aldosterone-producing adenoma. Hypertension 2014, 64:354-361.
23. Funder J.W., Carey R.M., Fardella C., Gomez-Sanchez C.E., Mantero F., Stowasser M., et al. Case detection, diagnosis, and treatment of patients with primary aldosteronism: an endocrine society clinical practice guideline. J. Clin. Endocrinol. Metab 2008, 93:3266-3281.
24. Gomez-Sanchez C.E., Oki K. Minireview: potassium channels and aldosterone dysregulation: is primary aldosteronism a potassium channelopathy?. Endocrinology 2014, 155:47-55.
25. Hajnoczky G., Csordas G., Hunyady L., Kalapos M.P., Balla T., Enyedi P., et al. Angiotensin-II inhibits Na+/K+ pump in rat adrenal glomerulosa cells: possible contribution to stimulation of aldosterone production. Endocrinology 1992, 130:1637-1644.
26. Hannemann A., Bidlingmaier M., Friedrich N., Manolopoulou J., Spyroglou A., Volzke H., et al. Screening for primary aldosteronism in hypertensive subjects: results from two German epidemiological studies. Eur. J. Endocrinol 2012, 167:7-15.
27. Hiramatsu K., Yamada T., Yukimura Y., Komiya I., Ichikawa M., Nagata H., et al. A screening test to identify aldosterone-producing adenoma by measuring plasma renin activity. Results in hypertensive patients. Arch. Intern. Med 1981, 141:1589-1593.
28. Kanai R., Ogawa H., Vilsen B., Cornelius F., Toyoshima C. Crystal structure of a Na+-bound Na+,K+-ATPase preceding the E1P state. Nature 2013, 502:201-206.
29. Kaplan J.H. Biochemistry of Na,K-ATPase. Annu. Rev. Biochem 2002, 71:511-535.
30. Kau M.M., Kan S.F., Wang J.R., Wang P.S., Lau Y.T., Wang S.W. Acute effects of digoxin on plasma aldosterone and cortisol in monkeys. Metabolism 2009, 58:55-61.
31. Kau M.M., Wang J.R., Tsai S.C., Yu C.H., Wang P.S. Inhibitory effect of bufalin and cinobufagin on steroidogenesis via the activation of ERK in human adrenocortical cells. Br. J. Pharmacol 2012, 165:1868-1876.
32. Kopec W., Loubet B., Poulsen H., Khandelia H. Molecular mechanism of Na(+),K(+)-ATPase malfunction in mutations characteristic of adrenal hypertension. Biochemistry 2014, 53:746-754.
33. Kuppusamy M., Caroccia B., Stindl J., Bandulik S., Lenzini L., Gioco F., et al. A novel KCNJ5-insT149 somatic mutation close to, but outside, the selectivity filter causes resistant hypertension by loss of selectivity for potassium. J. Clin. Endocrinol. Metab 2014, 99:E1765-E1773.
34. Lai F., Madan N., Ye Q., Duan Q., Li Z., Wang S., et al. Identification of a mutant alpha1 Na/K-ATPase that pumps but is defective in signal transduction. J. Biol. Chem 2013, 288:13295-13304.
35. Li J., Zelenin S., Aperia A., Aizman O. Low doses of ouabain protect from serum deprivation-triggered apoptosis and stimulate kidney cell proliferation via activation of NF-kappaB. J. Am. Soc. Nephrol 2006, 17:1848-1857.
36. Li Z., Xie Z. The Na/K-ATPase/Src complex and cardiotonic steroid-activated protein kinase cascades. Pflugers Arch 2009, 457:635-644.
37. Liang M., Cai T., Tian J., Qu W., Xie Z.J. Functional characterization of Src-interacting Na/K-ATPase using RNA interference assay. J. Biol. Chem 2006, 281:19709-19719.
38. Lingrel J., Moseley A., Dostanic I., Cougnon M., He S., James P., et al. Functional roles of the alpha isoforms of the Na,K-ATPase. Ann. N. Y. Acad. Sci 2003, 986:354-359.
39. Liu J., Xie Z.J. The sodium pump and cardiotonic steroids-induced signal transduction protein kinases and calcium-signaling microdomain in regulation of transporter trafficking. Biochim. Biophys. Acta 2010, 1802:1237-1245.
40. Michiels C. Physiological and pathological responses to hypoxia. Am. J. Pathol 2004, 164:1875-1882.
41. Moseley A.E., Huddleson J.P., Bohanan C.S., James P.F., Lorenz J.N., Aronow B.J., et al. Genetic profiling reveals global changes in multiple biological pathways in the hearts of Na, K-ATPase alpha 1 isoform haploinsufficient mice. Cell. Physiol. Biochem 2005, 15:145-158.
42. Mosso L., Carvajal C., Gonzalez A., Barraza A., Avila F., Montero J., et al. Primary aldosteronism and hypertensive disease. Hypertension 2003, 42:161-165.
43. Mulatero P., Tauber P., Zennaro M.C., Monticone S., Lang K., Beuschlein F., et al. KCNJ5 mutations in European families with nonglucocorticoid remediable familial hyperaldosteronism. Hypertension 2012, 59:235-240.
44. Murthy M., Xu S., Massimo G., Wolley M., Gordon R.D., Stowasser M., et al. Role for germline mutations and a rare coding single nucleotide polymorphism within the KCNJ5 potassium channel in a large cohort of sporadic cases of primary aldosteronism. Hypertension 2014, 63:783-789.
45. Neri G., De Toni R., Tortorella C., Rebuffat P., Bova S., Cargnelli G., et al. Ouabain chronic infusion enhances the growth and steroidogenic capacity of rat adrenal zona glomerulosa: the possible involvement of the endothelin system. Int. J. Mol. Med 2006, 18:315-319.
46. Oki K., Plonczynski M.W., Luis Lam M., Gomez-Sanchez E.P., Gomez-Sanchez C.E. Potassium channel mutant KCNJ5 T158A expression in HAC-15 cells increases aldosterone synthesis. Endocrinology 2012, 153:1774-1782.
47. Perraudin V., Delarue C., Lefebvre H., Do Rego J.L., Vaudry H., Kuhn J.M. Evidence for a role of vasopressin in the control of aldosterone secretion in primary aldosteronism: in vitro and in vivo studies. J. Clin. Endocrinol. Metab 2006, 91:1566-1572.
48. Post R.L., Hegyvary C., Kume S. Activation by adenosine triphosphate in the phosphorylation kinetics of sodium and potassium ion transport adenosine triphosphatase. J. Biol. Chem 1972, 247:6530-6540.
49. Reincke M., Fischer E., Gerum S., Merkle K., Schulz S., Pallauf A., et al. Observational study mortality in treated primary aldosteronism: the German Conn's Registry. Hypertension 2012, 60:618-624.
50. Saner-Amigh K., Mayhew B.A., Mantero F., Schiavi F., White P.C., Rao C.V., et al. Elevated expression of luteinizing hormone receptor in aldosterone-producing adenomas. J. Clin. Endocrinol. Metab 2006, 91:1136-1142.
51. Savard S., Amar L., Plouin P.F., Steichen O. Cardiovascular complications associated with primary aldosteronism: a controlled cross-sectional study. Hypertension 2013, 62:331-336.
52. Scholl U.I., Nelson-Williams C., Yue P., Grekin R., Wyatt R.J., Dillon M.J., et al. Hypertension with or without adrenal hyperplasia due to different inherited mutations in the potassium channel KCNJ5. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:2533-2538.
53. Scholl U.I., Goh G., Stolting G., de Oliveira R.C., Choi M., Overton J.D., et al. Somatic and germline CACNA1D calcium channel mutations in aldosterone-producing adenomas and primary aldosteronism. Nat. Genet 2013, 45:1050-1054.
54. Skou J.C. The influence of some cations on an adenosine triphosphatase from peripheral nerves. Biochim. Biophys. Acta 1957, 23:394-401.
55. Taguchi R., Yamada M., Nakajima Y., Satoh T., Hashimoto K., Shibusawa N., et al. Expression and mutations of KCNJ5 mRNA in Japanese patients with aldosterone-producing adenomas. J. Clin. Endocrinol. Metab 2012, 97:1311-1319.
56. Tauber P., Penton D., Stindl J., Humberg E., Tegtmeier I., Sterner C., et al. Pharmacology and pathophysiology of mutated KCNJ5 found in adrenal aldosterone-producing adenomas. Endocrinology 2014, 155:1353-1362.
57. Tian J., Li X., Liang M., Liu L., Xie J.X., Ye Q., et al. Changes in sodium pump expression dictate the effects of ouabain on cell growth. J. Biol. Chem 2009, 284:14921-14929.
58. Wansapura A.N., Lasko V.M., Lingrel J.B., Lorenz J.N. Mice expressing ouabain-sensitive alpha1-Na,K-ATPase have increased susceptibility to pressure overload-induced cardiac hypertrophy. Am. J. Physiol. Heart Circ. Physiol 2011, 300:H347-H355.
59. Williams T.A., Monticone S., Schack V.R., Stindl J., Burrello J., Buffolo F., et al. Somatic ATP1A1, ATP2B3, and KCNJ5 mutations in aldosterone-producing adenomas. Hypertension 2014, 63:188-195.
60. Xie Z., Xie J. The Na/K-ATPase-mediated signal transduction as a target for new drug development. Front. Biosci 2005, 10:3100-3109.
61. Ye P., Mariniello B., Mantero F., Shibata H., Rainey W.E. G-protein-coupled receptors in aldosterone-producing adenomas: a potential cause of hyperaldosteronism. J. Endocrinol 2007, 195:39-48.
62. Yingst D.R., Davis J., Krenz S., Schiebinger R.J. Insights into the mechanism by which inhibition of Na,K-ATPase stimulates aldosterone production. Metabolism 1999, 48:1167-1171.
63. Zwermann O., Suttmann Y., Bidlingmaier M., Beuschlein F., Reincke M. Screening for membrane hormone receptor expression in primary aldosteronism. Eur. J. Endocrinol 2009, 160:443-451.