DACH1, a zona glomerulosa selective gene in the human adrenal, activates transforming growth factor-β signaling and suppresses aldosterone secretion

Hypertension

Volumn 65, Issue 5, 2015, Pages 1103-1110

  Zhou, Junhua ^a   Shaikh, Lalarukh Haris ^a   Neogi, Sudeshna G ^c   Mcfarlane, Ian ^c   Zhao, Wanfeng ^d   Figg, Nichola ^b   Brighton, Cheryl A ^a   Maniero, Carmela ^a   Teo, Ada E D ^a   Azizan, Elena A B ^a,e   Brown, Morris J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c NIHR Cambridge BRC   (United Kingdom)

^d ADDENBROOKE S HOSPITAL   (United Kingdom)

^e UNIVERSITI KEBANGSAAN MALAYSIA   (Malaysia)

Author keywords

aldosterone; DACH1 protein human; hyperaldosteronism; transforming growth factor beta; zona glomerulosa

Indexed keywords

ALDOSTERONE; ANGIOTENSIN II; MESSENGER RNA; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEIN; DACH1 PROTEIN, HUMAN; EYE PROTEIN; RNA; TRANSCRIPTION FACTOR;

ADRENAL CORTEX CELL; ADRENAL GLAND; ADULT; ALDOSTERONE RELEASE; ARTICLE; CELL STIMULATION; CLINICAL ARTICLE; CLINICAL FEATURE; COMPUTER PROGRAM; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYP11B2 GENE; DACH1 GENE; FEMALE; GENE; GENE EXPRESSION; GENE FUNCTION; GENE OVEREXPRESSION; GENE SEQUENCE; GENE SILENCING; GENOME; HORMONE RELEASE; HORMONE SYNTHESIS; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; PHEOCHROMOCYTOMA; PRIMARY HYPERALDOSTERONISM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STEROIDOGENESIS; TUMOR GROWTH; UPREGULATION; VALIDATION PROCESS; WNT SIGNALING PATHWAY; ZONA FASCICULATA; ZONA GLOMERULOSA; ADRENAL CORTEX CARCINOMA; BIOSYNTHESIS; DISEASE COURSE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MIDDLE AGED; PATHOLOGY; SECRETION (PROCESS); TUMOR CELL CULTURE;

ADRENOCORTICAL CARCINOMA; ALDOSTERONE; DISEASE PROGRESSION; EYE PROTEINS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; REAL-TIME POLYMERASE CHAIN REACTION; RNA, NEOPLASM; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA; TUMOR CELLS, CULTURED; ZONA GLOMERULOSA;

EID: 84929704804     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYP.0000000000000025     Document Type: Article

References (40)

1. Conn JW. Presidential address. I. Painting background. II. Primary aldosteronism, a new clinical syndrome. J Lab Clin Med. 1955; 45: 3-17
2. Rossi GP, Bernini G, Caliumi C, et al; PAPY Study Investigators. A prospective study of the prevalence of primary aldosteronism in 1, 125 hypertensive patients. J Am Coll Cardiol. 2006; 48: 2293-2300. doi: 10.1016/j. jacc.2006.07.059
3. Choi M, Scholl UI, Yue P, et al. K+ channel mutations in adrenal aldosterone- producing adenomas and hereditary hypertension. Science. 2011; 331: 768-772. doi: 10.1126/science.1198785
4. Azizan EA, Lam BY, Newhouse SJ, Zhou J, Kuc RE, Clarke J, Happerfield L, Marker A, Hoffman GJ, Brown MJ. Microarray, qPCR, and KCNJ5 sequencing of aldosterone-producing adenomas reveal differences in genotype and phenotype between zona glomerulosa- and zona fasciculata-like tumors. J Clin Endocrinol Metab. 2012; 97: E819-E829. doi: 10.1210/jc.2011-2965
5. Azizan EA, Poulsen H, Tuluc P, et al. Somatic mutations in ATP1A1 and CACNA1D underlie a common subtype of adrenal hypertension. Nat Genet. 2013; 45: 1055-1060. doi: 10.1038/ng.2716
6. Wu K, Li A, Rao M, Liu M, Dailey V, Yang Y, Di Vizio D, Wang C, Lisanti MP, Sauter G, Russell RG, Cvekl A, Pestell RG. DACH1 is a cell fate determination factor that inhibits cyclin D1 and breast tumor growth. Mol Cell Biol. 2006; 26: 7116-7129. doi: 10.1128/MCB.00268-06
7. Wu K, Katiyar S, Witkiewicz A, Li A, McCue P, Song LN, Tian L, Jin M, Pestell RG. The cell fate determination factor dachshund inhibits androgen receptor signaling and prostate cancer cellular growth. Cancer Res. 2009; 69: 3347-3355. doi: 10.1158/0008-5472.CAN-08-3821
8. Nan F, Lü Q, Zhou J, Cheng L, Popov VM, Wei S, Kong B, Pestell RG, Lisanti MP, Jiang J, Wang C. Altered expression of DACH1 and cyclin D1 in endometrial cancer. Cancer Biol Ther. 2009; 8: 1534-1539
9. Ye P, Mariniello B, Mantero F, Shibata H, Rainey WE. G-protein-coupled receptors in aldosterone-producing adenomas: a potential cause of hyperaldosteronism. J Endocrinol. 2007; 195: 39-48. doi: 10.1677/JOE-07-0037
10. Felizola SJ, Nakamura Y, Ono Y, Kitamura K, Kikuchi K, Onodera Y, Ise K, Takase K, Sugawara A, Hattangady N, Rainey WE, Satoh F, Sasano H. PCP4: a regulator of aldosterone synthesis in human adrenocortical tissues. J Mol Endocrinol. 2014; 52: 159-167. doi: 10.1530/JME-13-0248
11. Gomez-Sanchez CE, Qi X, Velarde-Miranda C, Plonczynski MW, Parker CR, Rainey W, Satoh F, Maekawa T, Nakamura Y, Sasano H, Gomez- Sanchez EP. Development of monoclonal antibodies against human CYP11B1 and CYP11B2. Mol Cell Endocrinol. 2014; 383: 111-117. doi: 10.1016/j.mce.2013.11.022
12. Arnold J. Ein Beitrag zu Der feiner Struktur und dem Chemismus Der Nebennieren. Virchows Arch. 1866; 35: 64-107
13. Mitani F, Mukai K, Miyamoto H, Suematsu M, Ishimura Y. Development of functional zonation in the rat adrenal cortex. Endocrinology. 1999; 140: 3342-3353. doi: 10.1210/endo.140.7.6859
14. Vinson GP. Adrenocortical zonation and ACTH. Microsc Res Tech. 2003; 61: 227-239. doi: 10.1002/jemt.10331
15. Vinson GP, Ho MM. Origins of zonation: the adrenocortical model of tissue development and differentiation. Clin Exp Pharmacol Physiol Suppl. 1998; 25: S91-S96
16. Schinner S, Willenberg HS, Krause D, Schott M, Lamounier-Zepter V, Krug AW, Ehrhart-Bornstein M, Bornstein SR, Scherbaum WA. Adipocyte-derived products induce the transcription of the StAR promoter and stimulate aldosterone and cortisol secretion from adrenocortical cells through the Wnt-signaling pathway. Int J Obes (Lond). 2007; 31: 864-870. doi: 10.1038/sj.ijo.0803508
17. Suwa T, Chen M, Hawks CL, Hornsby PJ. Zonal expression of dickkopf-3 and components of the Wnt signalling pathways in the human adrenal cortex. J Endocrinol. 2003; 178: 149-158
18. Nishimoto K, Rainey WE, Bollag WB, Seki T. Lessons from the gene expression pattern of the rat zona glomerulosa. Mol Cell Endocrinol. 2013; 371: 107-113. doi: 10.1016/j.mce.2012.12.023
19. Williams TA, Monticone S, Crudo V, Warth R, Veglio F, Mulatero P. Visininlike 1 is upregulated in aldosterone-producing adenomas with KCNJ5 mutations and protects from calcium-induced apoptosis. Hypertension. 2012; 59: 833-839. doi: 10.1161/HYPERTENSIONAHA.111.188532
20. Bassett MH, Suzuki T, Sasano H, White PC, Rainey WE. The orphan nuclear receptors NURR1 and NGFIB regulate adrenal aldosterone production. Mol Endocrinol. 2004; 18: 279-290. doi: 10.1210/me.2003-0005
21. Zhu H, Wu K, Yan W, Hu L, Yuan J, Dong Y, Li Y, Jing K, Yang Y, Guo M. Epigenetic silencing of DACH1 induces loss of transforming growth factor-β1 antiproliferative response in human hepatocellular carcinoma. Hepatology. 2013; 58: 2012-2022. doi: 10.1002/hep.26587
22. Wu K, Katiyar S, Li A, Liu M, Ju X, Popov VM, Jiao X, Lisanti MP, Casola A, Pestell RG. Dachshund inhibits oncogene-induced breast cancer cellular migration and invasion through suppression of interleukin-8. Proc Natl Acad Sci U S A. 2008; 105: 6924-6929. doi: 10.1073/pnas.0802085105
23. Chen K, Wu K, Cai S, et al. Dachshund binds p53 to block the growth of lung adenocarcinoma cells. Cancer Res. 2013; 73: 3262-3274. doi: 10.1158/0008-5472.CAN-12-3191
24. Yan W, Wu K, Herman JG, Brock MV, Fuks F, Yang L, Zhu H, Li Y, Yang Y, Guo M. Epigenetic regulation of DACH1, a novel Wnt signaling component in colorectal cancer. Epigenetics. 2013; 8: 1373-1383. doi: 10.4161/epi.26781
25. Liang F, Lü Q, Sun S, Zhou J, Popov VM, Li S, Li W, Liu Y, Jiang J, Kong B. Increased expression of dachshund homolog 1 in ovarian cancer as a predictor for poor outcome. Int J Gynecol Cancer. 2012; 22: 386-393. doi: 10.1097/IGC.0b013e31824311e6
26. Wu K, Yang Y, Wang C, Davoli MA, D'Amico M, Li A, Cveklova K, Kozmik Z, Lisanti MP, Russell RG, Cvekl A, Pestell RG. DACH1 inhibits transforming growth factor-beta signaling through binding Smad4. J Biol Chem. 2003; 278: 51673-51684. doi: 10.1074/jbc.M310021200
27. Gupta P, Franco-Saenz R, Gentry LE, Mulrow PJ. Transforming growth factor-beta 1 inhibits aldosterone and stimulates adrenal renin in cultured bovine zona glomerulosa cells. Endocrinology. 1992; 131: 631-636. doi: 10.1210/endo.131.2.1322277
28. Berthon A, Drelon C, Ragazzon B, et al. WNT/β-catenin signalling is activated in aldosterone-producing adenomas and controls aldosterone production. Hum Mol Genet. 2014; 23: 889-905. doi: 10.1093/hmg/ddt484
29. Siianova EIu, Mirkin SM. Expansion of trinucleotide repeats. Mol Biol (Mosk). 2001; 35: 208-223
30. Ferro P, Catalano MG, Dell'Eva R, Fortunati N, Pfeffer U. The androgen receptor CAG repeat: a modifier of carcinogenesis?. Mol Cell Endocrinol. 2002; 193: 109-120
31. Boccuzzi A, Terzolo M, Cappia S, De Giuli P, De Risi C, Leonardo E, Bovio S, Borriero M, Paccotti P, Angeli A. Different immunohistochemical patterns of TGF-beta1 expression in benign and malignant adrenocortical tumours. Clin Endocrinol (Oxf). 1999; 50: 801-808
32. Gupta P, Franco-Saenz R, Mulrow PJ. Transforming growth factorbeta 1 inhibits aldosterone biosynthesis in cultured bovine zona glomerulosa cells. Endocrinology. 1993; 132: 1184-1188. doi: 10.1210/endo.132.3.8440178
33. Berthon A, Martinez A, Bertherat J, Val P. Wnt/β-catenin signalling in adrenal physiology and tumour development. Mol Cell Endocrinol. 2012; 351: 87-95. doi: 10.1016/j.mce.2011.09.009
34. El Wakil A, Lalli E. The Wnt/beta-catenin pathway in adrenocortical development and cancer. Mol Cell Endocrinol. 2011; 332: 32-37. doi: 10.1016/j.mce.2010.11.014
35. Nishita M, Hashimoto MK, Ogata S, Laurent MN, Ueno N, Shibuya H, Cho KW. Interaction between Wnt and TGF-beta signalling pathways during formation of Spemann's organizer. Nature. 2000; 403: 781-785. doi: 10.1038/35001602
36. Tadjine M, Lampron A, Ouadi L, Bourdeau I. Frequent mutations of betacatenin gene in sporadic secreting adrenocortical adenomas. Clin Endocrinol (Oxf). 2008; 68: 264-270. doi: 10.1111/j.1365-2265.2007.03033.x.
37. Wang T, Satoh F, Morimoto R, Nakamura Y, Sasano H, Auchus RJ, Edwards MA, Rainey WE. Gene expression profiles in aldosteroneproducing adenomas and adjacent adrenal glands. Eur J Endocrinol. 2011; 164: 613-619. doi: 10.1530/EJE-10-1085
38. Lenzini L, Seccia TM, Aldighieri E, Belloni AS, Bernante P, Giuliani L, Nussdorfer GG, Pessina AC, Rossi GP. Heterogeneity of aldosterone-producing adenomas revealed by a whole transcriptome analysis. Hypertension. 2007; 50: 1106-1113. doi: 10.1161/HYPERTENSIONAHA.107.100438
39. Nishimoto K, Rigsby CS, Wang T, Mukai K, Gomez-Sanchez CE, Rainey WE, Seki T. Transcriptome analysis reveals differentially expressed transcripts in rat adrenal zona glomerulosa and zona fasciculata. Endocrinology. 2012; 153: 1755-1763. doi: 10.1210/en.2011-1915
40. Gazdar AF Oie HK, Shackleton CH, Chen TR, Triche TJ, Myers CE, Chrousos GP, Brennan MF, Stein CA, La Rocca RV. Establishment and characterization of a human adrenocortical carcinoma cell line that expresses multiple pathways of steroid biosynthesis. Cancer Res. 1990; 50: 5488-5496