Nuclear shuttling precedes dimerization in mineralocorticoid receptor signaling

Chemistry and Biology

Volumn 19, Issue 6, 2012, Pages 742-751

  Grossmann, Claudia ^a   Ruhs, Stefanie ^a   Langenbruch, Lisa ^a   Mildenberger, Sigrid ^a   Strätz, Nicole ^a   Schumann, Katja ^a   Gekle, Michael ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALDOSTERONE; DNA; GELDANAMYCIN; GREEN FLUORESCENT PROTEIN; HEAT SHOCK PROTEIN 90; MINERALOCORTICOID RECEPTOR;

ARTICLE; BIOLUMINESCENCE RESONANCE ENERGY TRANSFER; CONTROLLED STUDY; DIMERIZATION; GENETIC TRANSFECTION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; TRANSACTIVATION;

BENZOQUINONES; BIOLUMINESCENCE RESONANCE ENERGY TRANSFER TECHNIQUES; CELL NUCLEUS; CELLS, CULTURED; DNA; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEK293 CELLS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LACTAMS, MACROCYCLIC; MINERALOCORTICOID RECEPTOR ANTAGONISTS; PROTEIN MULTIMERIZATION; RECEPTORS, MINERALOCORTICOID; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84862744026     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2012.04.014     Document Type: Article

References (52)

1. G.F. Allan, S.Y. Tsai, M.J. Tsai, and B.W. O'Malley Ligand-dependent conformational changes in the progesterone receptor are necessary for events that follow DNA binding Proc. Natl. Acad. Sci. USA 89 1992 11750 11754
2. J.L. Arriza, C. Weinberger, G. Cerelli, T.M. Glaser, B.L. Handelin, D.E. Housman, and R.M. Evans Cloning of human mineralocorticoid receptor complementary DNA: structural and functional kinship with the glucocorticoid receptor Science 237 1987 268 275
3. D.L. Bain, A.F. Heneghan, K.D. Connaghan-Jones, and M.T. Miura Nuclear receptor structure: implications for function Annu. Rev. Physiol. 69 2007 201 220
4. C.M. Bamberger, M. Wald, A.M. Bamberger, and H.M. Schulte Inhibition of mineralocorticoid and glucocorticoid receptor function by the heat shock protein 90-binding agent geldanamycin Mol. Cell. Endocrinol. 131 1997 233 240
5. A. Banerjee, S. Periyasamy, I.M. Wolf, T.D. Hinds Jr., W. Yong, W. Shou, and E.R. Sanchez Control of glucocorticoid and progesterone receptor subcellular localization by the ligand-binding domain is mediated by distinct interactions with tetratricopeptide repeat proteins Biochemistry 47 2008 10471 10480
6. N. Binart, M. Lombès, and E.-E. Baulieu Distinct functions of the 90 kDa heat-shock protein (hsp90) in oestrogen and mineralocorticosteroid receptor activity: effects of hsp90 deletion mutants Biochem. J. 311 1995 797 804
7. E.R. Blasi, R. Rocha, A.E. Rudolph, E.A. Blomme, M.L. Polly, and E.G. McMahon Aldosterone/salt induces renal inflammation and fibrosis in hypertensive rats Kidney Int. 63 2003 1791 1800
8. C.G. Brilla, and K.T. Weber Mineralocorticoid excess, dietary sodium, and myocardial fibrosis J. Lab. Clin. Med. 120 1992 893 901
9. C.A. Caamaño, M.I. Morano, P.D. Patel, S.J. Watson, and H. Akil A bacterially expressed mineralocorticoid receptor is associated in vitro with the 90-kilodalton heat shock protein and shows typical hormone- and DNA-binding characteristics Biochemistry 32 1993 8589 8595
10. A. Chrysostomou, E. Pedagogos, L. MacGregor, and G.J. Becker Double-blind, placebo-controlled study on the effect of the aldosterone receptor antagonist spironolactone in patients who have persistent proteinuria and are on long-term angiotensin-converting enzyme inhibitor therapy, with or without an angiotensin II receptor blocker Clin. J. Am. Soc. Nephrol. 1 2006 256 262
11. B. Couette, S. Jalaguier, C. Hellal-Levy, B. Lupo, J. Fagart, G. Auzou, and M.E. Rafestin-Oblin Folding requirements of the ligand-binding domain of the human mineralocorticoid receptor Mol. Endocrinol. 12 1998 855 863
12. M.J. Czar, M.D. Galigniana, A.M. Silverstein, and W.B. Pratt Geldanamycin, a heat shock protein 90-binding benzoquinone ansamycin, inhibits steroid-dependent translocation of the glucocorticoid receptor from the cytoplasm to the nucleus Biochemistry 36 1997 7776 7785
13. J. Drouin, Y.L. Sun, S. Tremblay, P. Lavender, T.J. Schmidt, A. de Léan, and M. Nemer Homodimer formation is rate-limiting for high affinity DNA binding by glucocorticoid receptor Mol. Endocrinol. 6 1992 1299 1309
14. P.C. Echeverría, G. Mazaira, A. Erlejman, C. Gomez-Sanchez, G. Piwien Pilipuk, and M.D. Galigniana Nuclear import of the glucocorticoid receptor-hsp90 complex through the nuclear pore complex is mediated by its interaction with Nup62 and importin beta Mol. Cell. Biol. 29 2009 4788 4797
15. G. Fejes-Tóth, D. Pearce, and A. Náray-Fejes-Tóth Subcellular localization of mineralocorticoid receptors in living cells: effects of receptor agonists and antagonists Proc. Natl. Acad. Sci. USA 95 1998 2973 2978
16. B.C. Freeman, and K.R. Yamamoto Disassembly of transcriptional regulatory complexes by molecular chaperones Science 296 2002 2232 2235
17. M.D. Galigniana, P.R. Housley, D.B. DeFranco, and W.B. Pratt Inhibition of glucocorticoid receptor nucleocytoplasmic shuttling by okadaic acid requires intact cytoskeleton J. Biol. Chem. 274 1999 16222 16227
18. M.D. Galigniana, A.G. Erlejman, M. Monte, C. Gomez-Sanchez, and G. Piwien-Pilipuk The hsp90-FKBP52 complex links the mineralocorticoid receptor to motor proteins and persists bound to the receptor in early nuclear events Mol. Cell. Biol. 30 2010 1285 1298
19. C. Grossmann, B. Husse, S. Mildenberger, B. Schreier, K. Schuman, and M. Gekle Colocalization of mineralocorticoid and EGF receptor at the plasma membrane Biochim. Biophys. Acta 1803 2010 584 590
20. A. Guiochon-Mantel, H. Loosfelt, P. Lescop, S. Sar, M. Atger, M. Perrot-Applanat, and E. Milgrom Mechanisms of nuclear localization of the progesterone receptor: evidence for interaction between monomers Cell 57 1989 1147 1154
21. C. Hellal-Levy, J. Fagart, A. Souque, and M.E. Rafestin-Oblin Mechanistic aspects of mineralocorticoid receptor activation Kidney Int. 57 2000 1250 1255
22. I. Hernández-Díaz, T. Giraldez, M.R. Arnau, V.A.J. Smits, F. Jaisser, N. Farman, and D. Alvarez de la Rosa The mineralocorticoid receptor is a constitutive nuclear factor in cardiomyocytes due to hyperactive nuclear localization signals Endocrinology 151 2010 3888 3899
23. J. Huyet, G.M. Pinon, M.R. Fay, J. Fagart, and M.E. Rafestin-Oblin Structural basis of spirolactone recognition by the mineralocorticoid receptor Mol. Pharmacol. 72 2007 563 571
24. K.I. Kang, J. Devin, F. Cadepond, N. Jibard, A. Guiochon-Mantel, E.E. Baulieu, and M.G. Catelli In vivo functional protein-protein interaction: nuclear targeted hsp90 shifts cytoplasmic steroid receptor mutants into the nucleus Proc. Natl. Acad. Sci. USA 91 1994 340 344
25. K.I. Kang, X. Meng, J. Devin-Leclerc, I. Bouhouche, A. Chadli, F. Cadepond, E.E. Baulieu, and M.G. Catelli The molecular chaperone Hsp90 can negatively regulate the activity of a glucocorticosteroid-dependent promoter Proc. Natl. Acad. Sci. USA 96 1999 1439 1444
26. W. Liu, J. Wang, N.K. Sauter, and D. Pearce Steroid receptor heterodimerization demonstrated in vitro and in vivo Proc. Natl. Acad. Sci. USA 92 1995 12480 12484
27. M. Lombès, N. Binart, F. Delahaye, E.E. Baulieu, and M.E. Rafestin-Oblin Differential intracellular localization of human mineralocorticosteroid receptor on binding of agonists and antagonists Biochem. J. 302 1994 191 197
28. T. Nemoto, Y. Ohara-Nemoto, N. Sato, and M. Ota Dual roles of 90-kDa heat shock protein in the function of the mineralocorticoid receptor J. Biochem. 113 1993 769 775
29. M. Nishi, H. Ogawa, T. Ito, K.I. Matsuda, and M. Kawata Dynamic changes in subcellular localization of mineralocorticoid receptor in living cells: in comparison with glucocorticoid receptor using dual-color labeling with green fluorescent protein spectral variants Mol. Endocrinol. 15 2001 1077 1092
30. M. Nishi, M. Tanaka, K.i. Matsuda, M. Sunaguchi, and M. Kawata Visualization of glucocorticoid receptor and mineralocorticoid receptor interactions in living cells with GFP-based fluorescence resonance energy transfer J. Neurosci. 24 2004 4918 4927
31. D. Pearce, A. Náray-Fejes-Tóth, and G. Fejes-Tóth Determinants of subnuclear organization of mineralocorticoid receptor characterized through analysis of wild type and mutant receptors J. Biol. Chem. 277 2002 1451 1456
32. A. Pfau, C. Grossmann, R. Freudinger, S. Mildenberger, A. Benesic, and M. Gekle Ca2+ but not H2O2 modulates GRE-element activation by the human mineralocorticoid receptor in HEK cells Mol. Cell. Endocrinol. 264 2007 35 43
33. K.D.G. Pfleger, and K.A. Eidne Illuminating insights into protein-protein interactions using bioluminescence resonance energy transfer (BRET) Nat. Methods 3 2006 165 174
34. D. Picard, and K.R. Yamamoto Two signals mediate hormone-dependent nuclear localization of the glucocorticoid receptor EMBO J. 6 1987 3333 3340
35. B. Pitt, W. Remme, F. Zannad, J. Neaton, F. Martinez, B. Roniker, R. Bittman, S. Hurley, J. Kleiman, M. Gatlin Eplerenone Post-Acute Myocardial Infarction Heart Failure Efficacy and Survival Study Investigators Eplerenone, a selective aldosterone blocker, in patients with left ventricular dysfunction after myocardial infarction N. Engl. J. Med. 348 2003 1309 1321
36. G. Piwien Pilipuk, G.P. Vinson, C.G. Sanchez, and M.D. Galigniana Evidence for NL1-independent nuclear translocation of the mineralocorticoid receptor Biochemistry 46 2007 1389 1397
37. N.M. Robertson, G. Schulman, S. Karnik, E. Alnemri, and G. Litwack Demonstration of nuclear translocation of the mineralocorticoid receptor (MR) using an anti-MR antibody and confocal laser scanning microscopy Mol. Endocrinol. 7 1993 1226 1239
38. E.R. Sanchez, D.O. Toft, M.J. Schlesinger, and W.B. Pratt Evidence that the 90-kDa phosphoprotein associated with the untransformed L-cell glucocorticoid receptor is a murine heat shock protein J. Biol. Chem. 260 1985 12398 12401
39. C.L. Sartório, D. Fraccarollo, P. Galuppo, M. Leutke, G. Ertl, I. Stefanon, and J. Bauersachs Mineralocorticoid receptor blockade improves vasomotor dysfunction and vascular oxidative stress early after myocardial infarction Hypertension 50 2007 919 925
40. J.G. Savory, B. Hsu, I.R. Laquian, W. Giffin, T. Reich, R.J. Haché, and Y.A. Lefebvre Discrimination between NL1- and NL2-mediated nuclear localization of the glucocorticoid receptor Mol. Cell. Biol. 19 1999 1025 1037
41. J.G. Savory, G.G. Préfontaine, C. Lamprecht, M. Liao, R.F. Walther, Y.A. Lefebvre, and R.J. Haché Glucocorticoid receptor homodimers and glucocorticoid-mineralocorticoid receptor heterodimers form in the cytoplasm through alternative dimerization interfaces Mol. Cell. Biol. 21 2001 781 793
42. I. Segard-Maurel, K. Rajkowski, N. Jibard, G. Schweizer-Groyer, E.E. Baulieu, and F. Cadepond Glucocorticosteroid receptor dimerization investigated by analysis of receptor binding to glucocorticosteroid responsive elements using a monomer-dimer equilibrium model Biochemistry 35 1996 1634 1642
43. D.F. Smith, L. Whitesell, S.C. Nair, S. Chen, V. Prapapanich, and R.A. Rimerman Progesterone receptor structure and function altered by geldanamycin, an hsp90-binding agent Mol. Cell. Biol. 15 1995 6804 6812
44. D.A. Stavreva, W.G. Müller, G.L. Hager, C.L. Smith, and J.G. McNally Rapid glucocorticoid receptor exchange at a promoter is coupled to transcription and regulated by chaperones and proteasomes Mol. Cell. Biol. 24 2004 2682 2697
45. C.E. Stebbins, A.A. Russo, C. Schneider, N. Rosen, F.U. Hartl, and N.P. Pavletich Crystal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent Cell 89 1997 239 250
46. M. Tanaka, M. Nishi, M. Morimoto, T. Sugimoto, and M. Kawata Imaging analysis of mineralocorticoid receptor and importins in single living cells by using GFP color variants Cell Tissue Res. 320 2005 447 453
47. M.J. Tsai, and B.W. O'Malley Molecular mechanisms of action of steroid/thyroid receptor superfamily members Annu. Rev. Biochem. 63 1994 451 486
48. S.Y. Tsai, J. Carlstedt-Duke, N.L. Weigel, K. Dahlman, J.A. Gustafsson, M.J. Tsai, and B.W. O'Malley Molecular interactions of steroid hormone receptor with its enhancer element: evidence for receptor dimer formation Cell 55 1988 361 369
49. R.F. Walther, C. Lamprecht, A. Ridsdale, I. Groulx, S. Lee, Y.A. Lefebvre, and R.J. Haché Nuclear export of the glucocorticoid receptor is accelerated by cell fusion-dependent release of calreticulin J. Biol. Chem. 278 2003 37858 37864
50. R.F. Walther, E. Atlas, A. Carrigan, Y. Rouleau, A. Edgecombe, L. Visentin, C. Lamprecht, G.C. Addicks, R.J. Haché, and Y.A. Lefebvre A serine/threonine-rich motif is one of three nuclear localization signals that determine unidirectional transport of the mineralocorticoid receptor to the nucleus J. Biol. Chem. 280 2005 17549 17561
51. L. Whitesell, and P. Cook Stable and specific binding of heat shock protein 90 by geldanamycin disrupts glucocorticoid receptor function in intact cells Mol. Endocrinol. 10 1996 705 712
52. O. Wrange, P. Eriksson, and T. Perlmann The purified activated glucocorticoid receptor is a homodimer J. Biol. Chem. 264 1989 5253 5259