Mineralocorticoid receptor inhibits CREB signaling by calcineurin activation

FASEB Journal

Volumn 24, Issue 6, 2010, Pages 2010-2019

  Grossmann, Claudia ^a   Wuttke, Martin ^a   Ruhs, Stefanie ^a   Seiferth, Anja ^a   Mildenberger, Sigrid ^a   Rabe, Sindy ^a   Schwerdt, Gerald ^a   Gekle, Michael ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

Aldosterone; cAMP; Glucose 6 phosphate dehydrogenase; Steroid hormone; Vascular smooth muscle cells

Indexed keywords

ADENYLATE CYCLASE; ALDOSTERONE; BETA 1 ADRENERGIC RECEPTOR; BETA 2 ADRENERGIC RECEPTOR; CALCINEURIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; MINERALOCORTICOID RECEPTOR;

ARTICLE; ENZYME ACTIVATION; HETEROLOGOUS EXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE;

AORTA; BLOTTING, WESTERN; CALCINEURIN; CELLS, CULTURED; CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT MODULATOR; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; ENZYME-LINKED IMMUNOSORBENT ASSAY; GLUCOSEPHOSPHATE DEHYDROGENASE; HUMANS; MYOCYTES, SMOOTH MUSCLE; PHOSPHORYLATION; RECEPTORS, ADRENERGIC; RECEPTORS, MINERALOCORTICOID; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 77953497672     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-146985     Document Type: Article

References (59)

1. Pitt, B., Zannad, F., Remme, W. J., Cody, R., Castaigne, A., Perez, A., Palensky, J., and Wittes, J. (1999) The effect of spironolactone on morbidity and mortality in patients with severe heart failure. Randomized aldactone evaluation study investigators. N. Engl. J. Med. 341, 709-717
2. Pitt, B., Remme, W., Zannad, F., Neaton, J., Martinez, F., Roniker, B., Bittman, R., Hurley, S., Kleiman, J., and Gatlin, M. (2003) Eplerenone, a selective aldosterone blocker, in patients with left ventricular dysfunction after myocardial infarction. N. Engl. J. Med. 348, 1309-1321
3. Arriza, J. L., Weinberger, C., Cerelli, G., Glaser, T. M., Handelin, B. L., Housman, D. E., and Evans, R. M. (1987) Cloning of human mineralocorticoid receptor complementary DNA: structural and functional kinship with the glucocorticoid receptor. Science 237, 268-275 (Pubitemid 17095145)
4. Krug, A. W., Grossmann, C., Schuster, C., Freudinger, R., Mildenberger, S., Govindan, M. V., and Gekle, M. (2003) Aldosterone stimulates epidermal growth factor receptor (EGFR) expression. J. Biol. Chem. 278, 43060-43066
5. + reabsorption. Am. J. Physiol. Renal. Physiol. 286, F1226-F1231
6. 2+ and stimulation of a plasma membrane proton conductance. Proc. Natl. Acad. Sci. U. S. A. 93, 10500-10504
7. Losel, R., and Wehling, M. (2003) Nongenomic actions of steroid hormones. Nat. Rev. Mol. Cell Biol. 4, 46-56
8. Thomas, W., McEneaney, V., and Harvey, B. J. (2007) Aldosterone- stimulated PKC signalling cascades: from receptor to effector. Biochem. Soc. Trans. 35, 1049-1051
9. Grossmann, C., Benesic, A., Krug, A. W., Freudinger, R., Mildenberger, S., Gassner, B., and Gekle, M. (2005) Human mineralocorticoid receptor expression renders cells responsive for nongenotropic aldosterone actions. Mol. Endocrinol. 19, 1697-1710
10. Christ, M., Günther, A., Heck, M., Schmidt, B. M. W., Falkenstein, E., and Wehling, M. (1999) Aldosterone, not estradiol, is the physiological agonist for rapid increases in cAMP in vascular smooth muscle cells. Circulation 99, 1485-1491 (Pubitemid 29140916)
11. Haseroth, K., Gerdes, D., Berger, S., Feuring, M., Gunther, A., Herbst, C., Christ, M., and Wehling, M. (1999) Rapid nongenomic effects of aldosterone in mineralocorticoid-receptor-knockout mice. Biochem. Biophys. Res. Commun. 266, 257-261
12. Sheader, E. A., Wargent, E. T., Ashton, N., and Balment, R. J. (2002) Rapid stimulation of cyclic AMP production by aldosterone in rat inner medullary collecting ducts. J. Endocrinol. 175, 343-347
13. Goto, J., Otsuka, F., Yamashita, M., Suzuki, J., Otani, H., Takahashi, H., Miyoshi, T., Mimura, Y., Ogura, T., and Makino, H. (2009) Enhancement of aldosterone-induced catecholamine production by bone morphogenetic protein-4 through activating Rho and SAPK/JNK pathway in adrenomedullar cells. Am. J. Physiol. Endocrinol. Metab. 296, E904-E916
14. Christ, M., Wehling, M., Kirsch, E., Viengchareun, S., Zennaro, M. C., and Lombes, M. (2005) Enhancement of β-adrenergic cAMP-signaling by the mineralocorticoid receptor. Mol. Cell. Endocrinol. 231, 23-31
15. Jazayeri, A., and Meyer, W. J., III (1989) Mineralocorticoid-induced increase in beta-adrenergic receptors of cultured rat arterial smooth muscle cells. J. Steroid Biochem. 33, 987-991
16. Klar, J., Vitzthum, H., and Kurtz, A. (2004) Aldosterone enhances renin gene expression in juxtaglomerular cells. Am. J. Physiol. Renal Physiol. 286, F349-F355 (Pubitemid 38141679)
17. Ahmad, M., and Medford, R. M. (1995) Evidence for the regulation of Na+, K+-ATPase α1 gene expression through the interaction of aldosterone and cAMP-inducible transcriptional factors. Steroids 60, 147-152
18. Gonzalez-Nunez, D., Morales-Ruiz, M., Leivas, A., Hebert, S. C., and Poch, E. (2004) In vitro characterization of aldosterone and cAMP effects in mouse distal convoluted tubule cells. Am. J. Physiol. Renal Physiol. 286, F936-F944
19. Zhou, Z. H., and Bubien, J. K. (2001) Nongenomic regulation of ENaC by aldosterone. Am. J. Physiol. Cell Physiol. 281, C1118-C1130
20. Massaad, C., Houard, N., Lombes, M., and Barouki, R. (1999) Modulation of human mineralocorticoid receptor function by protein kinase A. Mol. Endocrinol. 13, 57-65
21. Lim-Tio, S. S., and Fuller, P. J. (1998) Intracellular signaling pathways confer specificity of transactivation by mineralocorticoid and glucocorticoid receptors. Endocrinology 139, 1653-1661
22. Nordeen, S. K., Moyer, M. L., and Bona, B. J. (1994) The coupling of multiple signal transduction pathways with steroid response mechanisms. Endocrinology 134, 1723-1732
23. Ouvrard-Pascaud, A., Sainte-Marie, Y., Benitah, J. P., Perrier, R., Soukaseum, C., Cat, A. N. D., 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., and Jaisser, F. (2005) Conditional mineralocorticoid receptor expression in the heart leads to life-threatening arrhythmias. Circulation 111, 3025-3033
24. Leopold, J. A., Dam, A., Maron, B. A., Scribner, A. W., Liao, R., Handy, D. E., Stanton, R. C., Pitt, B., and Loscalzo, J. (2007) Aldosterone impairs vascular reactivity by decreasing glucose-6-phosphate dehydrogenase activity. Nat. Med. 189-197
25. Leopold, J. A., and Loscalzo, J. (2000) Cyclic strain modulates resistance to oxidant stress by increasing G6PDH expression in smooth muscle cells. Am. J. Physiol. Heart Circ. Physiol. 279, H2477-H2485
26. Swaney, J. S., Roth, D. M., Olson, E. R., Naugle, J. E., Meszaros, J. G., and Insel, P. A. (2005) Inhibition of cardiac myofibroblast formation and collagen synthesis by activation and overexpression of adenylyl cyclase. Proc. Nat. Acad. Sci. 102, 437-442
27. Liu, X., Ostrom, R. S., and Insel, P. A. (2004) cAMP-elevating agents and adenylyl cyclase overexpression promote an antifibrotic phenotype in pulmonary fibroblasts. Am. J. Physiol. Cell Physiol. 286, C1089-C1099
28. Savoia, C., Touyz, R. M., Endemann, D. H., Pu, Q., Ko, E. A., De Ciuceis, C., and Schiffrin, E. L. (2006) Angiotensin receptor blocker added to previous antihypertensive agents on arteries of diabetic hypertensive patients. Hypertension 48, 271-277
29. Savoia, C., Touyz, R. M., Amiri, F., and Schiffrin, E. L. (2008) Selective mineralocorticoid receptor blocker eplerenone reduces resistance artery stiffness in hypertensive patients. Hypertension 51, 432-439
30. Zacchigna, L., Vecchione, C., Notte, A., Cordenonsi, M., Dupont, S., Maretto, S., Cifelli, G., Ferrari, A., Maffei, A., Fabbro, C., Braghetta, P., Marino, G., Selvetella, G., Aretini, A., Colonnese, C., Bettarini, U., Russo, G., Soligo, S., Adorno, M., Bonaldo, P., Volpin, D., Piccolo, S., Lembo, G., and Bressan, G. M. (2006) Emilin1 links TGF-β maturation to blood pressure homeostasis. Cell 124, 929-942
31. Gekle, M., Freudinger, R., Mildenberger, S., and Silbernagl, S. (2002) Aldosterone interaction with epidermal growth factor receptor signaling in MDCK cells. Am. J. Physiol. Renal Physiol. 282, F669-F679 (Pubitemid 34654514)
32. Ouvrard-Pascaud, A., Puttini, S., Sainte-Marie, Y., Athman, R., Fontaine, V., Cluzeaud, F., Farman, N., Rafestin-Oblin, M. E., Blot-Chabaud, M., and Jaisser, F. (2004) Conditional gene expression in renal collecting duct epithelial cells: use of the inducible Cre-lox system. Am. J. Physiol. Renal Physiol. 286, F180-F187
33. Fuse, H., Kitagawa, H., and Kato, S. (2000) Characterization of transactivational property and coactivator mediation of rat mineralocorticoid receptor activation function-1 (AF-1). Mol. Endocrinol. 14, 889-899
34. 2+ but not H2O2 modulates GRE-element activation by the human mineralocorticoid receptor in HEK cells. Mol. Cell. Endocrinol. 264, 35-43
35. Wohlfarth, V., Drumm, K., Mildenberger, S., Freudinger, R., and Gekle, M. (2003) Protein uptake disturbs collagen homeostasis in proximal tubule-derived cells. Kidney Int. Suppl. 84, 103-109
36. Ziyadeh, F. N., Snipes, E. R., Watanabe, M., Alvarez, R. J., Goldfarb, S., and Haverty, T. P. (1990) High glucose induces cell hypertrophy and stimulates collagen gene transcription in proximal tubule. Am. J. Physiol. 259, F704-F714
37. Esposito, C., Fornoni, A., Cornacchia, F., Bellotti, N., Fasoli, G., Foschi, A., Mazzucchelli, I., Mazzullo, T., Semeraro, L., and Dal Canton, A. (2000) Cyclosporine induces different responses in human epithelial, endothelial and fibroblast cell cultures. Kidney Int. 58, 123-130
38. Vesey, D. A., Cheung, C. W. Y., Cuttle, L., Endre, Z. A., Gobe, G., and Johnson, D. W. (2002) Interleukin-1beta induces human proximal tubule cell injury, alpha-smooth muscle actin expression and fibronectin production1. Kidney. Int. 62, 31-40
39. Ziera, T., Irlbacher, H., Fromm, A., Latouche, C., Krug, S. M., Fromm, M., Jaisser, F., and Borden, S. A. (2009) Cnksr3 is a direct mineralocorticoid receptor target gene and plays a key role in the regulation of the epithelial sodium channel. FASEB J. 23, 3936-3946
40. Pascual-Le Tallec, L., and Lombes, M. (2005) The mineralocorticoid receptor: a journey exploring its diversity and specificity of action. Mol. Endocrinol. 19, 2211-2221
41. Grossmann, C., and Gekle, M. (2008) Nongenotropic aldosterone effects and the EGFR: interaction and biological relevance. Steroids 73, 973-978
42. Rupprecht, R., Arriza, J. L., Spengler, D., Reul, J. M., Evans, R. M., Holsboer, F., and Damm, K. (1993) Transactivation and synergistic properties of the mineralocorticoid receptor: relationship to the glucocorticoid receptor. Mol. Endocrinol. 7, 597-603
43. Callera, G. E., Touyz, R. M., Tostes, R. C., Yogi, A., He, Y., Malkinson, S., and Schiffrin, E. L. (2005) Aldosterone activates vascular p38MAP kinase and NADPH oxidase via c-Src. Hypertension 45, 1-7
44. Callera, G. E., Montezano, A. C. I., Yogi, A., Tostes, R. C., He, Y., Schiffrin, E. L., and Touyz, R. M. (2005) c-Src-Dependent nongenomic signaling responses to aldosterone are increased in vascular myocytes from spontaneously hypertensive rats. Hypertension 46, 1032-1038
45. Jaffe, I. Z., and Mendelsohn, M. E. (2005) Angiotensin II and Aldosterone regulate gene transcription via functional mineralocortocoid receptors in human coronary artery smooth muscle cells. Circ. Res. 96, 643-650
46. Alzamora, R., Michea, L., and Marusic, E. T. (2000) Role of 11beta-hydroxysteroid dehydrogenase in nongenomic aldosterone effects in human arteries. Hypertension 35, 1099-1104 (Pubitemid 30327264)
47. Gekle, M., Mildenberger, S., Freudinger, R., and Grossmann, C. (2007) Altered collagen homeostasis in human aortic smooth muscle cells (HAoSMCs) induced by aldosterone. Pflügers Arch. 454, 403-413
48. Rochette-Egly, C. (2005) Dynamic combinatorial networks in nuclear receptor-mediated transcription. J. Biol. Chem. 280, 32565-32568
49. Levin, E. R. (2003) Bidirectional signaling between the estrogen receptor and the epidermal growth factor receptor. Mol. Endocrinol. 17, 309-317
50. Edwards, D. P. (2005) Regulation of signal transduction pathways by estrogen and progesterone. Annu. Rev. Physiol. 67, 335-376
51. Rogatsky, I., Waase, C. L., and Garabedian, M. J. (1998) Phosphorylation and inhibition of rat glucocorticoid receptor transcriptional activation by glycogen synthase kinase-3 (GSK-3). Species-specific differences between human and rat glucocorticoid receptor signaling as revealed through GSK-3 phosphorylation. J. Biol. Chem. 273, 14315-14321
52. Someren, J. S., Faber, L. E., Klein, J. D., and Tumlin, J. A. (1999) Heat shock proteins 70 and 90 increase calcineurin activity in vitro through calmodulin-dependent and independent mechanisms. Biochem. Biophys. Res. Commun. 260, 619-625
53. Tumlin, J. A., Lea, J. P., Swanson, C. E., Smith, C. L., Edge, S. S., and Someren, J. S. (1997) Aldosterone and dexamethasone stimulate calcineurin activity through a transcription-independent mechanism involving steroid receptor-associated heat shock proteins. J. Clin. Invest. 99, 1217-1223
54. Pratt, W. B., and Toft, D. O. (2003) Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp. Biol. Med. 228, 111-133 (Pubitemid 36187918)
55. Colella, M., Grisan, F., Robert, V., Turner, J. D., Thomas, A. P., and Pozzan, T. (2008) Ca2+ oscillation frequency decoding in cardiac cell hypertrophy: role of calcineurin/NFAT as Ca2+ signal integrators. Proc. Natl. Acad. Sci. U. S. A. 26, 2859-2864 (Pubitemid 351723634)
56. Hallhuber, M., Burkard, N., Wu, R., Buch, M. H., Engelhardt, S., Hein, L., Neyses, L., Schuh, K., and Ritter, O. (2006) Inhibition of nuclear import of calcineurin prevents myocardial hypertrophy. Circ. Res. 99, 626-635
57. Takeda, Y., Yoneda, T., Demura, M., Usukura, M., and Mabuchi, H. (2002) Calcineurin inhibition attenuates mineralocorticoid-induced cardiac hypertrophy. Circulation 105, 677-679
58. Mano, A., Tatsumi, T., Shiraishi, J., Keira, N., Nomura, T., Takeda, M., Nishikawa, S., Yamanaka, S., Matoba, S., Kobara, M., Tanaka, H., Shirayama, T., Takamatsu, T., Nozawa, Y., and Matsubara, H. (2004) Aldosterone directly induces myocyte apoptosis through calcineurin-dependent pathways. Circulation 110, 317-323
59. Pedram, A., Razandi, M., Lubahn, D., Liu, J., Vannan, M., and Levin, E. R. (2008) Estrogen inhibits cardiac hypertrophy: role of estrogen receptor-β to inhibit calcineurin. Endocrinology 149, 3361-3369