Mineralocorticoid receptor overexpression in embryonic stem cell-derived cardiomyocytes increases their beating frequency

Cardiovascular Research

Volumn 87, Issue 3, 2010, Pages 467-475

  Le Menuet, Damien ^a,b   Munier, Mathilde ^a,b   Meduri, Geri ^a,c   Viengchareun, Say ^a,b   Lombs, Marc ^a,b,c  

^a INSERM   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c BICÊTRE HOSPITAL   (France)

Author keywords

Arrhythmia; Cell differentiation; Chronotropic agents; Stem cells; Transgenic animal models

Indexed keywords

CALCIUM CHANNEL CAV1.2; CALCIUM CHANNEL L TYPE; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR2.1; MESSENGER RNA; MINERALOCORTICOID RECEPTOR; SPIRONOLACTONE; UNCLASSIFIED DRUG; CACNA1C PROTEIN, MOUSE; CYCLIC NUCLEOTIDE GATED CHANNEL; HCN1 PROTEIN, HUMAN; HCN1 PROTEIN, MOUSE; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL; KCNJ2 PROTEIN, HUMAN; MINERALOCORTICOID ANTAGONIST; POTASSIUM CHANNEL;

ANIMAL CELL; ARTICLE; CARDIOMYOPATHY; CELL DIFFERENTIATION; CHRONOTROPISM; CONTROLLED STUDY; EMBRYONIC STEM CELL; HEART ARRHYTHMIA; HEART MUSCLE CELL; MARKER GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TACHYCARDIA; TRANSGENIC MOUSE; ANIMAL; CELL LINE; DRUG EFFECTS; GENETICS; HEART CONTRACTION; HEART RATE; HUMAN; MEMBRANE POTENTIAL; METABOLISM; TIME; UPREGULATION;

ANIMALS; CALCIUM CHANNELS, L-TYPE; CELL DIFFERENTIATION; CELL LINE; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; EMBRYONIC STEM CELLS; HEART RATE; HUMANS; HYPERPOLARIZATION-ACTIVATED CYCLIC NUCLEOTIDE-GATED CHANNELS; MEMBRANE POTENTIALS; MICE; MICE, TRANSGENIC; MINERALOCORTICOID RECEPTOR ANTAGONISTS; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; POTASSIUM CHANNELS; POTASSIUM CHANNELS, INWARDLY RECTIFYING; RECEPTORS, MINERALOCORTICOID; RNA, MESSENGER; SPIRONOLACTONE; TIME FACTORS; UP-REGULATION;

EID: 77954813624     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvq087     Document Type: Article

References (42)

1. 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.
2. Meyer WJ 3rd, Nichols NR. Mineralocorticoid binding in cultured smooth muscle cells and fibroblasts from rat aorta. J Steroid Biochem 1981;14:1157-1168.
3. Lombes M, Oblin ME, Gasc JM, Baulieu EE, Farman N, Bonvalet JP. Immunohistochem-ical and biochemical evidence for a cardiovascular mineralocorticoid receptor. Circ Res 1992;71:503-510.
4. Lombes M, Alfaidy N, Eugene E, Lessana A, Farman N, Bonvalet JP. Prerequisite for cardiac aldosterone action. Mineralocorticoid receptor and 11 beta-hydroxysteroid dehydrogenase in the human heart. Circulation 1995;92:175-182.
5. Nichols NR, Hall CE, Meyer WJ 3rd. Aldosterone binding sites in aortic cell cultures from spontaneously hypertensive rats. Hypertension 1982;4:646-651.
6. Rickard AJ, Morgan J, Tesch G, Funder JW, Fuller PJ, Young MJ. Deletion of minera-locorticoid receptors from macrophages protects against deoxycorticosterone/salt-induced cardiac fibrosis and increased blood pressure. Hypertension 2009;54: 537-543.
7. Pitt B, Zannad F, Remme WJ, Cody R, Castaigne A, Perez A et al. The effect of spir-onolactone on morbidity and mortality in patients with severe heart failure. Randomized Aldactone Evaluation Study Investigators. N Engl J Med 1999;341:709-717.
8. Pitt B, Remme W, Zannad F, Neaton J, Martinez F, Roniker B et al. Eplerenone, a selective aldosterone blocker, in patients with left ventricular dysfunction after myo-cardial infarction. N Engl J Med 2003;348:1309-1321.
9. Funder JW, Pearce PT, Smith R, Smith AI. Mineralocorticoid action: target tissue specificity is enzyme, not receptor, mediated. Science 1988;242:583-585.
10. Yoshimoto T, Hirata Y. Aldosterone as a cardiovascular risk hormone. Endocr J 2007; 54:359-370.
11. Qin W, Rudolph AE, Bond BR, Rocha R, Blomme EA, Goellner JJ et al. Transgenic model of aldosterone-driven cardiac hypertrophy and heart failure. Circ Res 2003; 93:69-76.
12. + metabolism. Proc Natl Acad Sci USA 1998;95:9424-9429.
13. Bleich M, Warth R, Schmidt-Hieber M, Schulz-Baldes A, Hasselblatt P, Fisch D et al. Rescue of the mineralocorticoid receptor knock-out mouse. Pflugers Arch 1999;438: 245-254.
14. Hubert C, Gasc JM, Berger S, Schutz G, Corvol P. Effects of mineralocorticoid receptor gene disruption on the components of the renin-angiotensin system in 8-day-old mice. Mol Endocrinol 1999;13:297-306.
15. Le Menuet D, Isnard R, Bichara M, Viengchareun S, Muffat-Joly M, Walker F et al. Alteration of cardiac and renal functions in transgenic mice overexpressing human mineralocorticoid receptor. J Biol Chem 2001;276:38911-38920.
16. Ouvrard-Pascaud A, Sainte-Marie Y, Benitah JP, Perrier R, Soukaseum C, Cat AN et al. Conditional mineralocorticoid receptor expression in the heart leads to life-threatening arrhythmias. Circulation 2005;111:3025-3033.
17. Sun Y, Zhang J, Lu L, Chen SS, Quinn MT, Weber KT. Aldosterone-induced inflammation in the rat heart: role of oxidative stress. Am J Pathol 2002;161:1773-1781.
18. Lalevee N, Rebsamen MC, Barrere-Lemaire S, Perrier E, Nargeot J, Benitah JP et al. Aldosterone increases T-type calcium channel expression and in vitro beating frequency in neonatal rat cardiomyocytes. Cardiovasc Res 2005;67:216-224.
19. Maturana A, Lenglet S, Python M, Kuroda S, Rossier MF. 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.
20. Boheler KR, Czyz J, Tweedie D, Yang HT, Anisimov SV, Wobus AM. Differentiation of pluripotent embryonic stem cells into cardiomyocytes. Circ Res 2002;91:189-201.
21. Wobus AM, Boheler KR. Embryonic stem cells: prospects for developmental biology and cell therapy. Physiol Rev 2005;85:635-678.
22. Gu P, LeMenuet D, Chung AC, Mancini M, Wheeler DA, Cooney AJ. Orphan nuclear receptor GCNF is required for the repression of pluripotency genes during retinoic acid-induced embryonic stem cell differentiation. Mol Cell Biol 2005;25:8507-8519.
23. Hescheler J, Fleischmann BK, Lentini S, Maltsev VA, Rohwedel J, Wobus AM et al. Embryonic stem cells: a model to study structural and functional properties in cardi-omyogenesis. Cardiovasc Res 1997;36:149-162.
24. Viengchareun S, Kamenicky P, Teixeira M, Butlen D, Meduri G, Blanchard-Gutton N et al. Osmotic stress regulates mineralocorticoid receptor expression in a novel aldosterone-sensitive cortical collecting duct cell line. Mol Endocrinol 2009;23:1948-1962.
25. Le Menuet D, Zennaro MC, Viengchareun S, Lombes M. Transgenic mouse models to study human mineralocorticoid receptor function in vivo. Kidney Int 2000;57:1299-1306.
26. 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.
27. Chandler NJ, Greener ID, Tellez JO, Inada S, Musa H, Molenaar P et al. Molecular architecture of the human sinus node: insights into the function of the cardiac pacemaker. Circulation 2009;119:1562-1575.
28. Baruscotti M, Barbuti A, Bucchi A. The cardiac pacemaker current. J Mol Cell Cardiol 2010;48:55-64.
29. DiFrancesco D. Funny channels in the control of cardiac rhythm and mode of action of selective blockers. Pharmacol Res 2006;53:399-406.
30. Maltsev VA, Wobus AM, Rohwedel J, Bader M, Hescheler J. Cardiomyocytes differentiated in vitro from embryonic stem cells developmentally express cardiac-specific genes and ionic currents. Circ Res 1994;75:233-244.
31. Mihailidou AS, Loan Le TY, Mardini M, Funder JW. Glucocorticoids activate cardiac mineralocorticoid receptors during experimental myocardial infarction. Hypertension 2009;54:1306-1312.
32. Muto T, Ueda N, Opthof T, Ohkusa T, Nagata K, Suzuki S et al. Aldosterone modulates I(f) current through gene expression in cultured neonatal rat ventricular myo-cytes. Am J Physiol Heart Circ Physiol 2007;293:H2710-H2718.
33. Perrier E, Kerfant BG, Lalevee N, Bideaux P, Rossier MF, Richard S et al. Mineralocor-ticoid receptor antagonism prevents the electrical remodeling that precedes cellular hypertrophy after myocardial infarction. Circulation 2004;110:776-783.
34. Shibata S, Nagase M, Yoshida S, Kawarazaki W, Kurihara H, Tanaka H et al. Modification of mineralocorticoid receptor function by Rac1 GTPase: implication in proteinuric kidney disease. Nat Med 2008;14:1370-1376.
35. Yanagi K, Takano M, Narazaki G, Uosaki H, Hoshino T, Ishii T et al. Hyperpolarization-activated cyclic nucleotide-gated channels and T-type calcium channels confer automaticity of embryonic stem cell-derived cardiomyocytes. Stem Cells 2007;25:2712-2719.
36. Barbuti A, Crespi A, Capilupo D, Mazzocchi N, Baruscotti M, DiFrancesco D. Molecular composition and functional properties of f-channels in murine embryonic stem cell-derived pacemaker cells. J Mol Cell Cardiol 2009;46:343-351.
37. Herrmann S, Stieber J, Stockl G, Hofmann F, Ludwig A. HCN4 provides a 'depolarization reserve' and is not required for heart rate acceleration in mice. EMBO J 2007; 26:4423-4432.
38. Schweizer PA, Yampolsky P, Malik R, Thomas D, Zehelein J, Katus HA et al. Transcription profiling of HCN-channel isotypes throughout mouse cardiac development. Basic Res Cardiol 2009;104:621-629.
39. Biel M, Wahl-Schott C, Michalakis S, Zong X. Hyperpolarization-activated cation channels: from genes to function. Physiol Rev 2009;89:847-885.
40. Harzheim D, Pfeiffer KH, Fabritz L, Kremmer E, Buch T, Waisman A et al. Cardiac pacemaker function of HCN4 channels in mice is confined to embryonic development and requires cyclic AMP. EMBO J 2008;27:692-703.
41. Gomez AM, Rueda A, Sainte-Marie Y, Pereira L, Zissimopoulos S, Zhu X et al. Miner-alocorticoid modulation of cardiac ryanodine receptor activity is associated with downregulation of FK506-binding proteins. Circulation 2009;119:2179-2187.
42. Boldt LH, Rolf S, Huemer M, Parwani AS, Luft FC, Dietz R et al. Optimal heart failure therapy and successful cardioversion in heart failure patients with atrial fibrillation. Am Heart J 2008;155:890-895.