Mineralocorticoid receptor and embryonic stem cell models: Molecular insights and pathophysiological relevance

Molecular and Cellular Endocrinology

Volumn 350, Issue 2, 2012, Pages 216-222

  Le Menuet, Damien ^a,b   Munier, Mathilde ^a,b   Campostrini, Giulia ^a,b   Lombès, Marc ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Adipocyte; Cardiomyocyte; Early development; Embryonic stem cells; Mineralocorticoid receptor; Neuron

Indexed keywords

CELL NUCLEUS RECEPTOR; ION CHANNEL; MINERALOCORTICOID RECEPTOR; STEROID RECEPTOR;

ADIPOCYTE; CARDIOMYOPATHY; CARDIOVASCULAR DISEASE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELL TYPE; EMBRYONIC STEM CELL; GENE; GENE EXPRESSION; GENE FUNCTION; HEART ARRHYTHMIA; HEART INFARCTION; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HUMAN; METABOLIC SYNDROME X; MR GENE; NERVE CELL; NERVE CELL DIFFERENTIATION; NONHUMAN; OBESITY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; TACHYCARDIA; TRANSGENE;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; DISEASE; EMBRYONIC STEM CELLS; HUMANS; MICE; MODELS, THEORETICAL; RECEPTORS, MINERALOCORTICOID;

EID: 84856323881     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2011.06.036     Document Type: Review

References (57)

1. Almeida O.F., Conde G.L., Crochemore C., Demeneix B.A., Fischer D., Hassan A.H., Meyer M., Holsboer F., Michaelidis T.M. Subtle shifts in the ratio between pro- and antiapoptotic molecules after activation of corticosteroid receptors decide neuronal fate. FASEB J. 2000, 14:779-790.
2. Berger S., Bleich M., Schmid W., Cole T.J., Peters J., Watanabe H., Kriz W., Warth R., Greger R., Schutz G. Mineralocorticoid receptor knockout mice: pathophysiology of Na+ metabolism. Proc. Natl. Acad. Sci. USA 1998, 95:9424-9429.
3. Berger S., Wolfer D.P., Selbach O., Alter H., Erdmann G., Reichardt H.M., Chepkova A.N., Welzl H., Haas H.L., Lipp H.P., Schutz G. Loss of the limbic mineralocorticoid receptor impairs behavioral plasticity. Proc. Natl. Acad. Sci. USA 2006, 103:195-200.
4. Bhargava A., Wang J., Pearce D. Regulation of epithelial ion transport by aldosterone through changes in gene expression. Mol. Cell. Endocrinol. 2004, 217:189-196.
5. Bibel M., Richter J., Lacroix E., Barde Y.A. Generation of a defined and uniform population of CNS progenitors and neurons from mouse embryonic stem cells. Nat. Protoc. 2007, 2:1034-1043.
6. Bleich M., Warth R., Schmidt-Hieber M., Schulz-Baldes A., Hasselblatt P., Fisch D., Berger S., Kunzelmann K., Kriz W., Schutz G., Greger R. Rescue of the mineralocorticoid receptor knock-out mouse. Pflugers Arch. 1999, 438:245-254.
7. Caprio M., Feve B., Claes A., Viengchareun S., Lombes M., Zennaro M.C. Pivotal role of the mineralocorticoid receptor in corticosteroid-induced adipogenesis. FASEB J. 2007, 21:2185-2194.
8. Caprio M., Antelmi A., Chetrite G., Muscat A., Mammi C., Marzolla V., Fabbri A., Zennaro M.C., Feve B. Antiadipogenic effects of the mineralocorticoid receptor antagonist drospirenone: potential implications for the treatment of metabolic syndrome. Endocrinology 2011, 152:113-125.
9. Crochemore C., Lu J., Wu Y., Liposits Z., Sousa N., Holsboer F., Almeida O.F. Direct targeting of hippocampal neurons for apoptosis by glucocorticoids is reversible by mineralocorticoid receptor activation. Mol. Psychiatry 2005, 10:790-798.
10. Dani C., Smith A.G., Dessolin S., Leroy P., Staccini L., Villageois P., Darimont C., Ailhaud G. Differentiation of embryonic stem cells into adipocytes in vitro. J. Cell Sci. 1997, 110(Pt. 11):1279-1285.
11. Farman N., Bocchi B. Mineralocorticoid selectivity: molecular and cellular aspects. Kidney Int. 2000, 57:1364-1369.
12. Farokhpour M., Karbalaie K., Tanhaei S., Nematollahi M., Etebari M., Sadeghi H.M., Nasr-Esfahani M.H., Baharvand H. Embryonic stem cell-derived cardiomyocytes as a model system to study cardioprotective effects of dexamethasone in doxorubicin cardiotoxicity. Toxicol. In Vitro 2009, 23:1422-1428.
13. Fraccarollo D., Berger S., Galuppo P., Kneitz S., Hein L., Schutz G., Frantz S., Ertl G., Bauersachs J. Deletion of cardiomyocyte mineralocorticoid receptor ameliorates adverse remodeling after myocardial infarction. Circulation 2011, 123:400-408.
14. Goldman-Johnson D.R., de Kretser D.M., Morrison J.R. Evidence that androgens regulate early developmental events, prior to sexual differentiation. Endocrinology 2008, 149:5-14.
15. Hong S.H., Nah H.Y., Lee Y.J., Lee J.W., Park J.H., Kim S.J., Lee J.B., Yoon H.S., Kim C.H. Expression of estrogen receptor-alpha and -beta, glucocorticoid receptor, and progesterone receptor genes in human embryonic stem cells and embryoid bodies. Mol. Cells 2004, 18:320-325.
16. Jeong Y., Mangelsdorf D.J. Nuclear receptor regulation of stemness and stem cell differentiation. Exp. Mol. Med. 2009, 41:525-537.
17. Joels M., Karst H., Krugers H.J., Lucassen P.J. Chronic stress: implications for neuronal morphology, function and neurogenesis. Front. Neuroendocrinol. 2007, 28:72-96.
18. Joels M. Functional actions of corticosteroids in the hippocampus. Eur. J. Pharmacol. 2008, 583:312-321.
19. Joels M., Karst H., DeRijk R., de Kloet E.R. The coming out of the brain mineralocorticoid receptor. Trends Neurosci. 2008, 31:1-7.
20. Kawase E., Suemori H., Takahashi N., Okazaki K., Hashimoto K., Nakatsuji N. Strain difference in establishment of mouse embryonic stem (ES) cell lines. Int. J. Dev. Biol. 1994, 38:385-390.
21. Kim D., Kim C.H., Moon J.I., Chung Y.G., Chang M.Y., Han B.S., Ko S., Yang E., Cha K.Y., Lanza R., Kim K.S. Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell 2009, 4:472-476.
22. Kiyomoto H., Rafiq K., Mostofa M., Nishiyama A. Possible underlying mechanisms responsible for aldosterone and mineralocorticoid receptor-dependent renal injury. J. Pharmacol. Sci. 2008, 108:399-405.
23. Lai M., Seckl J., Macleod M. Overexpression of the mineralocorticoid receptor protects against injury in PC12 cells. Brain Res. Mol. Brain Res. 2005, 135:276-279.
24. Lalevee N., Rebsamen M.C., Barrere-Lemaire S., Perrier E., Nargeot J., Benitah J.P., Rossier M.F. Aldosterone increases T-type calcium channel expression and in vitro beating frequency in neonatal rat cardiomyocytes. Cardiovasc. Res. 2005, 67:216-224.
25. Le Menuet D., Viengchareun S., Penfornis P., Walker F., Zennaro M.C., Lombes M. Targeted oncogenesis reveals a distinct tissue-specific utilization of alternative promoters of the human mineralocorticoid receptor gene in transgenic mice. J. Biol. Chem. 2000, 275:7878-7886.
26. Le Menuet D., Isnard R., Bichara M., Viengchareun S., Muffat-Joly M., Walker F., Zennaro M.C., Lombes M. Alteration of cardiac and renal functions in transgenic mice overexpressing human mineralocorticoid receptor. J. Biol. Chem. 2001, 276:38911-38920.
27. Le Menuet D., Viengchareun S., Muffat-Joly M., Zennaro M.C., Lombes M. Expression and function of the human mineralocorticoid receptor: lessons from transgenic mouse models. Mol. Cell. Endocrinol. 2004, 217:127-136.
28. Le Menuet D., Munier M., Meduri G., Viengchareun S., Lombes M. Mineralocorticoid receptor overexpression in embryonic stem cell-derived cardiomyocytes increases their beating frequency. Cardiovasc. Res. 2010, 87:467-475.
29. LeMenuet D., Gu P., Chung A.C., Mancini M., Wheeler D.A., Cooney A.J. Orphan nuclear receptor GCNF is required for the repression of pluripotency genes during retinoic acid-induced embryonic stem cell differentiation *equally contributed. Mol. Cell. Biol. 2005, 25:8507-8519.
30. Maroof A.M., Brown K., Shi S.H., Studer L., Anderson S.A. Prospective isolation of cortical interneuron precursors from mouse embryonic stem cells. J. Neurosci. 2010, 30:4667-4675.
31. Maturana A., Lenglet S., Python M., Kuroda S., Rossier M.F. Role of the T-type calcium channel CaV3.2 in the chronotropic action of corticosteroids in isolated rat ventricular myocytes. Endocrinology 2009, 150:3726-3734.
32. Meek S., Buehr M., Sutherland L., Thomson A., Mullins J.J., Smith A.J., Burdon T. Efficient gene targeting by homologous recombination in rat embryonic stem cells. PLoS One 2010, 5:e14225.
33. Mitra R., Ferguson D., Sapolsky R.M. Mineralocorticoid receptor overexpression in basolateral amygdala reduces corticosterone secretion and anxiety. Biol. Psychiatry 2009, 66:686-690.
34. Munier M., Meduri G., Viengchareun S., Leclerc P., Le Menuet D., Lombes M. Regulation of mineralocorticoid receptor expression during neuronal differentiation of murine embryonic stem cells. Endocrinology 2010, 151:2244-2254.
35. Ouvrard-Pascaud A., Sainte-Marie Y., Benitah J.P., Perrier R., Soukaseum C., Cat A.N., Royer A., Le Quang K., Charpentier F., Demolombe S., Mechta-Grigoriou F., Beggah A.T., Maison-Blanche P., Oblin M.E., Delcayre C., Fishman G.I., Farman N., Escoubet B., Jaisser F. Conditional mineralocorticoid receptor expression in the heart leads to life-threatening arrhythmias. Circulation 2005, 111:3025-3033.
36. Penfornis P., Viengchareun S., Le Menuet D., Cluzeaud F., Zennaro M.C., Lombes M. The mineralocorticoid receptor mediates aldosterone-induced differentiation of T37i cells into brown adipocytes. Am. J. Physiol. Endocrinol. Metab. 2000, 279:E386-E394.
37. Pera M.F. Stem cells: the dark side of induced pluripotency. Nature 2011, 471:46-47.
38. Pitt B., Zannad F., Remme W.J., Cody R., Castaigne A., Perez A., Palensky J., Wittes J. The effect of spironolactone on morbidity and mortality in patients with severe heart failure. Randomized aldactone evaluation study investigators. N. Engl. J. Med. 1999, 341:709-717.
39. Pitt B., Remme W., Zannad F., Neaton J., Martinez F., Roniker B., Bittman R., Hurley S., Kleiman J., Gatlin M. Eplerenone, a selective aldosterone blocker, in patients with left ventricular dysfunction after myocardial infarction. N. Engl. J. Med. 2003, 348:1309-1321.
40. Rickard A.J., Morgan J., Tesch G., Funder J.W., Fuller P.J., Young M.J. Deletion of mineralocorticoid receptors from macrophages protects against deoxycorticosterone/salt-induced cardiac fibrosis and increased blood pressure. Hypertension 2009, 54:537-543.
41. Robert V., Silvestre J.S., Charlemagne D., Sabri A., Trouve P., Wassef M., Swynghedauw B., Delcayre C. Biological determinants of aldosterone-induced cardiac fibrosis in rats. Hypertension 1995, 26:971-978.
42. Sainte Marie Y., Toulon A., Paus R., Maubec E., Cherfa A., Grossin M., Descamps V., Clemessy M., Gasc J.M., Peuchmaur M., Glick A., Farman N., Jaisser F. Targeted skin overexpression of the mineralocorticoid receptor in mice causes epidermal atrophy, premature skin barrier formation, eye abnormalities, and alopecia. Am. J. Pathol. 2007, 171:846-860.
43. Smith A.G. Embryo-derived stem cells: of mice and men. Annu. Rev. Cell Dev. Biol. 2001, 17:435-462.
44. Stadtfeld M., Hochedlinger K. Induced pluripotency: history, mechanisms, and applications. Genes Dev. 2010, 24:2239-2263.
45. Takahashi K., Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676.
46. Teixeira M., Viengchareun S., Butlen D., Ferreira C., Cluzeaud F., Blot-Chabaud M., Lombes M., Ferrary E. Functional IsK/KvLQT1 potassium channel in a new corticosteroid-sensitive cell line derived from the inner ear. J. Biol. Chem. 2006, 281:10496-10507.
47. Thomas W., McEneaney V., Harvey B.J. Aldosterone-induced signalling and cation transport in the distal nephron. Steroids 2008, 73:979-984.
48. Usher M.G., Duan S.Z., Ivaschenko C.Y., Frieler R.A., Berger S., Schutz G., Lumeng C.N., Mortensen R.M. Myeloid mineralocorticoid receptor controls macrophage polarization and cardiovascular hypertrophy and remodeling in mice. J. Clin. Invest. 2010, 120:3350-3364.
49. Vazin T., Freed W.J. Human embryonic stem cells: derivation, culture, and differentiation: a review. Restor. Neurol. Neurosci. 2010, 28:589-603.
50. Viengchareun S., Le Menuet D., Martinerie L., Munier M., Pascual-Le Tallec L., Lombes M. The mineralocorticoid receptor: insights into its molecular and (patho)physiological biology. Nucl. Recept. Signal. 2007, 5:e012.
51. Viengchareun S., Kamenicky P., Teixeira M., Butlen D., Meduri G., Blanchard-Gutton N., Kurschat C., Lanel A., Martinerie L., Sztal-Mazer S., Blot-Chabaud M., Ferrary E., Cherradi N., Lombes M. Osmotic stress regulates mineralocorticoid receptor expression in a novel aldosterone-sensitive cortical collecting duct cell line. Mol. Endocrinol. 2009, 23:1948-1962.
52. Wobus A.M., Boheler K.R. Embryonic stem cells: prospects for developmental biology and cell therapy. Physiol. Rev. 2005, 85:635-678.
53. Woolley C.S., Gould E., Sakai R.R., Spencer R.L., McEwen B.S. Effects of aldosterone or RU28362 treatment on adrenalectomy-induced cell death in the dentate gyrus of the adult rat. Brain Res. 1991, 554:312-315.
54. Xie C.Q., Jeong Y., Fu M., Bookout A.L., Garcia-Barrio M.T., Sun T., Kim B.H., Xie Y., Root S., Zhang J., Xu R.H., Chen Y.E., Mangelsdorf D.J. Expression profiling of nuclear receptors in human and mouse embryonic stem cells. Mol. Endocrinol. 2009, 23:724-733.
55. Young M., Fullerton M., Dilley R., Funder J. Mineralocorticoids, hypertension, and cardiac fibrosis. J. Clin. Invest. 1994, 93:2578-2583.
56. Zannad F., McMurray J.J., Krum H., van Veldhuisen D.J., Swedberg K., Shi H., Vincent J., Pocock S.J., Pitt B. Eplerenone in patients with systolic heart failure and mild symptoms. N. Engl. J. Med. 2011, 364:11-21.
57. Zennaro M.C., Le Menuet D., Lombes M. Characterization of the human mineralocorticoid receptor gene 5'-regulatory region: evidence for differential hormonal regulation of two alternative promoters via nonclassical mechanisms. Mol. Endocrinol. 1996, 10:1549-1560.