Functional modulation of nuclear steroid receptors by tauroursodeoxycholic acid reduces amyloid β-peptide-induced apoptosis

Molecular Endocrinology

Volumn 20, Issue 10, 2006, Pages 2292-2303

  Solá, Susana ^a   Amaral, Joana D ^a   Borralho, Pedro M ^a   Ramalho, Rita M ^a   Castro, Rui E ^a   Aranha, Márcia M ^a   Steer, Cifford J ^b   Rodrigues, Cecília M P ^a,c  

^a UNIVERSITY OF LISBON   (Portugal)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c NONE   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; CHAPERONE; HEAT SHOCK PROTEIN 90; STEROID RECEPTOR; TAUROURSODEOXYCHOLIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; IMMUNOFLUORESCENCE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN; ANIMALS; APOPTOSIS; CELL NUCLEUS; CELLS, CULTURED; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MICROSCOPY, FLUORESCENCE; NEURONS; RATS; RECEPTORS, GLUCOCORTICOID; RECEPTORS, MINERALOCORTICOID; RNA, SMALL INTERFERING; TAUROCHENODEOXYCHOLIC ACID; TRANS-ACTIVATION (GENETICS); TRANSCRIPTIONAL ACTIVATION;

EID: 33749332011     PISSN: 08888809     EISSN: 08888809     Source Type: Journal    
DOI: 10.1210/me.2006-0063     Document Type: Article

References (57)

1. Selkoe DJ 2001 Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 81:741-766
2. Haass C, Selkoe DJ 1993 Cellular processing of β-amyloid precursor protein and the genesis of amyloid β-peptide. Cell 75:1039-1042
3. Culmsee C, Zhu X, Yu QS, Chan SL, Camandola S, Guo Z, Greig NH, Mattson MP 2001 A synthetic inhibitor of p53 protects neurons against death induced by ischemic and excitotoxic insults, and amyloid β-peptide. J Neurochem 77:220-228
4. Yao M, Nguyen TV, Pike CJ 2005 β-Amyloid-induced neuronal apoptosis involves c-Jun N-terminal kinase-dependent downregulation of Bcl-w. J Neurosci 25:1149-1158
5. Watson K, Fan GH 2005 Macrophage inflammatory protein 2 inhibits β-amyloid peptide (1-42)-mediated hippocampal neuronal apoptosis through activation of mitogen-activated protein kinase and phosphatidylinositol 3-kinase signaling pathways. Mol Pharmacol 67:757-765
6. Rodrigues CMP, Fan G, Ma X, Kren BT, Steer CJ 1998 A novel role for ursodeoxycholic acid in inhibiting apoptosis by modulating mitochondrial membrane perturbation. J Clin Invest 101:2790-2799
7. Rodrigues CMP, Stieers CL, Keene CD, Ma X, Kren BT, Low WC, Steer CJ 2000 Tauroursodeoxycholic acid partially prevents apoptosis induced by 3-nitropropionic acid: evidence for a mitochondrial pathway independent of the permeability transition. J Neurochem 75:2368-2379
8. Rodrigues CMP, Solá S, Brites D 2002 Bilirubin induces apoptosis via the mitochondrial pathway in developing rat brain neurons. Hepatology 35:1186-1195
9. Solá S, Ma X, Castro RE, Kren BT, Steer CJ, Rodrigues CMP 2003 Ursodeoxycholic acid modulates E2F-1 and p53 expression through a caspase-independent mechanism in transforming growth factor β1-induced apoptosis of rat hepatocytes. J Biol Chem 278:48831-48838
10. Keene CD, Rodrigues CMP, Eich T, Linehan-Stieers C, Abt A, Kren BT, Steer CJ, Low WC 2001 A bile acid protects against motor and cognitive deficits and reduces striatal degeneration in the 3-nitropropionic acid model of Huntington's disease. Exp Neurol 171:351-360
11. Keene CD, Rodrigues CMP, Eich T, Chhabra MS, Steer CJ, Low WC 2002 Tauroursodeoxycholic acid, a bile acid, is neuroprotective in a transgenic animal model of Huntington's disease. Proc Natl Acad Sci USA 99:10671-10676
12. Rodrigues CMP, Spellman SR, Solá S, Grande AW, Linehan-Stieers C, Low WC, Steer CJ 2002 Neuroprotection by a bile acid in an acute stroke model in the rat. J Cereb Blood Flow Metab 22:463-471
13. Rodrigues CMP, Solá S, Nan Z, Castro RE, Ribeiro PS, Low WC, Steer CJ 2003 Tauroursodeoxycholic acid reduces apoptosis and protects against neurological injury after acute hemorrhagic stroke in rats. Proc Natl Acad Sci USA 100:6087-6092
14. Duan WM, Rodrigues CMP, Zhao LR, Steer CJ, Low WC 2002 Tauroursodeoxycholic acid improves the survival and function of nigral transplants in a rat model of Parkinson's disease. Cell Transplant 11:195-205
15. Ved R, Saha S, Westlund B, Perier C, Burnam LG, Sluder A, Hoener M, Rodrigues CMP, Alfonso A, Steer C, Liu L, Przedborski S, Wolozin B 2005 Similar patterns of mitochondrial vulnerability and rescue induced by genetic modification of α-synuclein, parkin and DJ-1 in C. elegans. J Biol Chem 280:42655-42668
16. Solá S, Castro RE, Laires PA, Steer CJ, Rodrigues CMP 2003 Tauroursodeoxycholic acid prevents amyloid-β peptide-induced neuronal death via a phosphatidylinositol 3-kinase-dependent signaling pathway. Mol Med 9:226-234
17. Ramalho RM, Ribeiro PS, Solá S, Castro RE, Steer CJ, Rodrigues CMP 2004 Inhibition of the E2F-1/p53/Bax pathway by tauroursodeoxycholic acid in amyloid β-peptide-induced apoptosis of PC12 cells. J Neurochem 90:567-575
18. McCormick JA, Lyons V, Jacobson MD, Noble J, Diorio J, Nyirenda M, Weaver S, Ester W, Yau JL, Meaney MJ, Seckl JR, Chapman KE 2000 5′-Heterogeneity of glucocorticoid receptor messenger RNA is tissue specific: differential regulation of variant transcripts by early-life events. Mol Endocrinol 14:506-517
19. Bastian LS, Nordeen SK 1991 Concerted stimulation of transcription by glucocorticoid receptors and basal transcription factors: limited transcriptional synergism suggests mediation by coactivators/adaptors. Mol Endocrinol 5:619-627
20. Almeida OF, Conde GL, Crochemore C, Demeneix BA, Fischer D, Hassan AH, Meyer M, Holsboer F, Michaelidis TM 2000 Subtle shifts in the ratio between pro- and antiapoptotic molecules after activation of corticosteroid receptors decide neuronal fate. FASEB J 14:779-790
21. Crochemore C, Michaelidis TM, Fischer D, Loeffler JP, Almeida OF 2002 Enhancement of p53 activity and inhibition of neural cell proliferation by glucocorticoid receptor activation. FASEB J 16:761-770
22. Wang Z, Garabedian MJ 2003 Modulation of glucocorticoid receptor transcriptional activation, phosphorylation, and growth inhibition by p27Kip1. J Biol Chem 278:50897-50901
23. Wetzel DM, Bohn MC, Kazee AM, Hamill RW 1995 Glucocorticoid receptor mRNA in Alzheimer's diseased hippocampus. Brain Res 679:72-81
24. Rasmuson S, Andrew R, Nasman B, Seckl JR, Walker BR, Olsson T 2001 Increased glucocorticoid production and altered cortisol metabolism in women with mild to moderate Alzheimer's disease. Biol Psychiatry 49:547-552
25. Tsolakidou AF, Coulocheri SA, Trikkas G, Moutsatsou P 2004 Gene analysis of the glucocorticoid receptor α in Alzheimer's disease. Clin Chim Acta 349:167-172
26. Behl C, Lezoualc'h F, Trapp T, Widmann M, Skutella T, Holsboer F 1997 Glucocorticoids enhance oxidative stress-induced cell death in hippocampal neurons in vitro. Endocrinology 138:101-106
27. Macleod MR, Johansson IM, Soderstrom I, Lai M, Gido G, Wieloch T, Seckl JR, Olsson T 2003 Mineralocorticoid receptor expression and increased survival following neuronal injury. Eur J Neurosci 17:1549-1555
28. Planey SL, Derfoul A, Steplewski A, Robertson NM, Litwack G 2002 Inhibition of glucocorticoid-induced apoptosis in 697 pre-B lymphocytes by the mineralocorticoid receptor N-terminal domain. J Biol Chem 277:42188-42196
29. Mendoza ME, Monte MJ, El-Mir MY, Badia MD, Marin JJ 2002 Changes in the pattern of bile acids in the nuclei of rat liver cells during hepatocarcinogenesis. Clin Sci (Lond) 102:143-150
30. Solá S, Amaral JD, Castro RE, Ramalho RM, Borralho PM, Kren BT, Tanaka H, Steer CJ, Rodrigues CMP 2005 Nuclear translocation of UDCA by the glucocorticoid receptor is required to reduce TGF-β1-induced apoptosis in rat hepatocytes. Hepatology 42:925-934
31. Miura T, Ouchida R, Yoshikawa N, Okamoto K, Makino Y, Nakamura T, Morimoto C, Makino I, Tanaka H 2001 Functional modulation of the glucocorticoid receptor and suppression of NF-κB-dependent transcription by ursodeoxycholic acid. J Biol Chem 276:47371-47378
32. Solá S, Castro RE, Kren BT, Steer CJ, Rodrigues CMP 2004 Modulation of nuclear steroid receptors by ursodeoxycholic acid inhibits TGF-β1-induced E2F-1/p53-mediated apoptosis of rat hepatocytes. Biochemistry 43:8429-8438
33. Pratt WB, Toft DO 1997 Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr Rev 18:306-360
34. Prima V, Depoix C, Masselot B, Formstecher P, Lefebvre P 2000 Alteration of the glucocorticoid receptor subcellular localization by non steroidal compounds. J Steroid Biochem Mol Biol 72:1-12
35. Bohen SP, Kralli A, Yamamoto KR 1995 Hold 'em and fold 'em: chaperones and signal transduction. Science 268:1303-1304
36. Whitfield GK, Jurutka PW, Haussler CA, Haussler MR 1999 Steroid hormone receptors: evolution, ligands, and molecular basis of biologic function. J Cell Biochem Suppl 32-33:110-122
37. Setchell KD, Rodrigues CMP, Clerici C, Solinas A, Morelli A, Gartung C, Boyer J 1997 Bile acid concentrations in human and rat liver tissue and in hepatocyte nuclei. Gastroenterology 112:226-235
38. Rodrigues CMP, Ma X, Linehan-Stieers C, Fan G, Kren BT, Steer CJ 1999 Ursodeoxycholic acid prevents cytochrome c release in apoptosis by inhibiting mitochondrial membrane depolarization and channel formation. Cell Death Differ 6:842-854
39. Rodrigues CMP, Solá S, Brito MA, Brondino CD, Brites D, Moura JJ 2001 Amyloid β-peptide disrupts mitochondrial membrane lipid and protein structure: protective role of tauroursodeoxycholate. Biochem Biophys Res Commun 281:468-474
40. Parks DJ, Blanchard SG, Bledsoe RK, Chandra G, Consler TG, Kliewer SA, Stimmel JB, Willson TM, Zavacki AM, Moore DD, Lehmann JM 1999 Bile acids: natural ligands for an orphan nuclear receptor. Science 284:1365-1368
41. Makishima M, Okamoto AY, Repa JJ, Tu H, Learned RM, Luk A, Hull MV, Lustig KD, Mangelsdorf DJ, Shan B 1999 Identification of a nuclear receptor for bile acids. Science 284:1362-1365
42. Wang H, Chen J, Hollister K, Sowers LC, Forman BM 1999 Endogenous bile acids are ligands for the nuclear receptor FXR/BAR. Mol Cell 3:543-553
43. Tanaka H, Makino Y, Miura T, Hirano F, Okamoto K, Komura K, Sato Y, Makino I 1996 Ligand-independent activation of the glucocorticoid receptor by ursodeoxycholic acid. Repression of IFN-γ-induced MHC class II gene expression via a glucocorticoid receptor-dependent pathway. J Immunol 156:1601-1608
44. Yamamoto M, Fukuda K, Miura N, Suzuki R, Kido T, Komatsu Y 1998 Inhibition by dexamethasone of transforming growth factor β1-induced apoptosis in rat hepatoma cells: a possible association with Bcl-xL induction. Hepatology 27:959-966
45. Webster JC, Huber RM, Hanson RL, Collier PM, Haws TF, Mills JK, Burn TC, Allegretto EA 2002 Dexamethasone and tumor necrosis factor-α act together to induce the cellular inhibitor of apoptosis-2 gene and prevent apoptosis in a variety of cell types. Endocrinology 143:3866-3874
46. Rogerson FM, Dimopoulos N, Sluka P, Chu S, Curtis AJ, Fuller PJ 1999 Structural determinants of aldosterone binding selectivity in the mineralocorticoid receptor. J Biol Chem 274:36305-36311
47. Lim-Tio SS, Fuller PJ 1998 Intracellular signaling pathways confer specificity of transactivation by mineralocorticoid and glucocorticoid receptors. Endocrinology 139:1653-1661
48. Nishi M, Ogawa H, Ito T, Matsuda KI, Kawata M 2001 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 15:1077-1092
49. Hellal-Levy C, Couette B, Fagart J, Souque A, Gomez-Sanchez C, Rafestin-Oblin M 1999 Specific hydroxylations determine selective corticosteroid recognition by human glucocorticoid and mineralocorticoid receptors. FEBS Lett 464:9-13
50. Stevens A, Garside H, Berry A, Waters C, White A, Ray D 2003 Dissociation of steroid receptor coactivator 1 and nuclear receptor corepressor recruitment to the human glucocorticoid receptor by modification of the ligand-receptor interface: the role of tyrosine 735. Mol Endocrinol 17:845-859
51. Hassan AH, von Rosenstiel P, Patchev VK, Holsboer F, Almeida OF 1996 Exacerbation of apoptosis in the dentate gyrus of the aged rat by dexamethasone and the protective role of corticosterone. Exp Neurol 140:43-52
52. Hassan AH, Patchev VK, von Rosenstiel P, Holsboer F, Almeida OF 1999 Plasticity of hippocampal corticosteroid receptors during aging in the rat. FASEB J 13:115-122
53. McCullers DL, Herman JP 1998 Mineralocorticoid receptors regulate bcl-2 and p53 mRNA expression in hippocampus. Neuroreport 9:3085-3089
54. Holzinger F, Schteingart CD, Ton-Nu HT, Eming SA, Monte MJ, Hagey LR, Hofmann AF 1997 Fluorescent bile acid derivatives: relationship between chemical structure and hepatic and intestinal transport in the rat. Hepatology 26:1263-1271
55. Yoshikawa N, Makino Y, Okamoto K, Morimoto C, Makino I, Tanaka H 2002 Distinct interaction of cortivazol with the ligand binding domain confers glucocorticoid receptor specificity: cortivazol is a specific ligand for the glucocorticoid receptor. J Biol Chem 277:5529-5540
56. Yoshikawa N, Yamamoto K, Shimizu N, Yamada S, Morimoto C, Tanaka H 2005 The distinct agonist properties of the phenylpyrazolosteroid cortivasol reveal interdomain communication within the glucocorticoid receptor. Mol Endocrinol 19:1110-1124
57. Makino Y, Yoshikawa N, Okamoto K, Hirota K, Yodoi J, Makino I, Tanaka H 1999 Direct association with thioredoxin allows redox regulation of glucocorticoid receptor function. J Biol Chem 274:3182-3188