Mineralocorticoid receptor antagonist spironolactone prevents chronic corticosterone induced depression-like behavior

Psychoneuroendocrinology

Volumn 38, Issue 6, 2013, Pages 871-883

  Wu, Ting Ching ^a   Chen, Han Ting ^a   Chang, Han Ying ^a   Yang, Ching Yao ^a   Hsiao, Mei Chun ^b   Cheng, Mei Ling ^a   Chen, Jin Chung ^a  

^a CHANG GUNG UNIVERSITY   (Taiwan)

^b CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

Author keywords

Corticosterone; Depression; Glucocorticoid receptor; Hippocampus; Mineralocorticoid receptor; Serotonin; Spironolactone

Indexed keywords

CORTICOSTEROID RECEPTOR; CORTICOSTERONE 21 ACETATE; MINERALOCORTICOID RECEPTOR; SEROTONIN; SPIRONOLACTONE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPRESSION; DOWN REGULATION; DRUG BLOOD LEVEL; FORCED SWIMMING TEST; HIPPOCAMPUS; HYPOTHALAMUS; MALE; MOUSE; NONHUMAN; PERFORMANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSYCHOLOGIC ASSESSMENT; RECOGNITION;

ANIMALS; BEHAVIOR, ANIMAL; CORTICOSTERONE; DEPRESSION; HIPPOCAMPUS; HYDROXYINDOLEACETIC ACID; HYPOTHALAMUS; MALE; MICE; MINERALOCORTICOID RECEPTOR ANTAGONISTS; RECEPTORS, GLUCOCORTICOID; RECEPTORS, MINERALOCORTICOID; SEROTONIN; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; SPIRONOLACTONE; TRYPTOPHAN HYDROXYLASE;

EID: 84877052713     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2012.09.011     Document Type: Article

References (80)

1. Azmitia E.C., Liao B., Chen Y.S. Increase of tryptophan hydroxylase enzyme protetin by dexamethasone in adrenalectomized rat midbrain. J. Neurosci. 1993, 13:5041-5055.
2. Azmitia E.C., Segal M.J. An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. Comp. Neurol. 1978, 179:641-667.
3. Berton O., Nestler E.J. New approaches to antidepressant drug discovery: beyond monoamines. Nat. Rev. Neurosci. 2006, 7:137-151.
4. Boyle M.P., Brewer J.A., Funatsu M., Wozniak D.F., Tsien J.Z., Izumi Y., Muglia L.J. Acquired deficit of forebrain glucocorticoid receptor produces depression-like changes in adrenal axis regulation and behavior. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:473-478.
5. Brouwer J.P., Appelhof B.C., van Rossum E.F., Koper J.W., Fliers E., Huyser J., Schene A.H., Tijssen J.G., Van Dyck R., Lamberts S.W., Wiersinga W.M., Hoogendijk W.J. Prediction of treatment response by HPA-axis and glucocorticoid receptor polymorphisms in major depression. Psychoneuroendocrinology 2006, 31:1154-1163.
6. Brown E.S., Varghese F.P., McEwen B.S. Association of depression with medical illness: does cortisol play a role?. Biol. Psychiatry 2004, 55:1-9.
7. Caamano C.A., Morano M.I., Akil H. Corticosteroid receptors: a dynamic interplay between protein folding and homeostatic control. Psychopharmacol. Bull. 2001, 35:6-23.
8. Caspi A., Sugden K., Moffitt T.E., Taylor A., Craig I.W., Harrington H.L., McClay J., Mill J., Martin J., Braithwaite A., Poulton R. Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 2003, 301:386-389.
9. Couette B., Lombes M., Baulieu B.B., Rafestin-Oblin M.E. Aldosterone antagonists destabilize the mineralocorticosteroid receptor. Biochem. J. 1992, 282:697-702.
10. DeBattista C., Belanoff J. The use of mifepristone in the treatment of neuropsychiatric disorders. Trends Endocrinol. Metab. 2006, 17:117-121.
11. De Kloet E.R., DeRijk R.H., Meijer O.C. Therapy insight: is there an imbalanced response of mineralocorticoid and glucocorticoid receptors in depression?. Endocrinol. Metab. 2007, 3:168-179.
12. De Kloet E.R., Vreugdenhil E., Oitzl M.S., Joels M. Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 1998, 19:269-301.
13. Ennaceur A., Meliani J. A new one-trial test for neurobiological studies of memory in rats. I. Behavioral data. Behav. Brain Res. 1988, 31:47-59.
14. Fairchild G., Leitch M.M., Ingram C.D. Acute and chronic effects of corticosterone on 5-HT1A receptor-mediated autoinhibition in the rat dorsal raphe nucleus. Neuropharmacology 2003, 45:925-934.
15. Filipovic D., Gavrilovic L., Dronjak S., Radojcic M.B. Brain glucocorticoid receptor and heat shock protein 70 levels in rats exposed to acute, chronic or combined stress. Neuropsychobiology 2005, 51:107-114.
16. Gass P., Reichardt H.M., Strekalova T., Henn F., Tronche F. Mice with targeted mutations of glucocorticoid and mineralocorticoid receptors: models for depression and anxiety?. Physiol. Behav. 2001, 73:811-825.
17. Gourley S.L., Wu F.J., Taylor J.R. Corticosterone regulates pERK1/2 map kinase in a chronic depression model. Ann. N. Y. Acad. Sci. 2008, 1148:509-514.
18. Grad I., Picard D. The glucocorticoid responses are shaped by molecular chaperones. Mol. Cell. Endocrinol. 2007, 275:2-12.
19. Gregus A., Wintink A.J., Davis A.C., Kalynchuk L.E. Effect of repeated corticosterone injections and restraint stress on anxiety and depression-like behavior in male rats. Behav. Brain Res. 2005, 156:105-114.
20. Heim C., Nermeroff C.B. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol. Psychiatry 2001, 49:1023-1039.
21. Hensler J.G., Advani T., Monteggia L.M. Regulation of serotonin-1A receptor function in inducible brain-derived neurotrophic factor knockout mice after administration of corticosterone. Biol Psychiatry 2007, 62:521-529.
22. Hesen W., Joels M. Modulation of 5HT1A responsiveness in CA1 pyramidal neurons by in vivo activation of corticosteroid receptors. J. Neuroendocrinol. 1996, 8:433-438.
23. Holsboer F. Stress, hypercortisolism and corticosteroid receptors in depression: implications for therapy. J. Affect. Disord. 2001, 62:77-91.
24. Holsboer F., Ising M. Stress hormone regulation: biological role and translation into therapy. Annu. Rev. Psychol. 2010, 61:81-109.
25. Jahn H., Schick M., Kiefer F., Kellner M., Yassouridis A., Wiedemann K. Metyrapone as additive treatment in major depression. Arch. Gen. Psychiatry 2004, 61:1235-1244.
26. Joels M. Functional actions of corticosteroids in the hippocampus. Eur. J. Pharmacol. 2008, 583:312-321.
27. Johnson D.A., Ingram C.D., Grant E.J., Craighead M., Gartside S.E. Glucocorticoid receptor antagonism augments fluoxetine-induced downregulation of the 5-HT transporter. Neuropsychopharmacology 2009, 34:399-409.
28. Juruena M.F., Cleare A.J., Bauer M.E., Pariante C.M. Molecular mechanism of GR sensitivity and relevance for affective disorders. Acta Neuropshcjiatrica. 2003, 15:354-367.
29. Juruena M.F., Cleare A.J., Pariante C.M. The hypothalamic pituitary adrenal axis glucocorticoid receptor function and relevance to depression. Rev. Bras. Psiguiatr. 2004, 26:189-201.
30. Keeney A., Jessop D.S., Harbuz M.S., Marsden C.A., Hogg S., Blackburn-Munro R.E. Differential effects of acute and chronic social defeat stress on hypothalamic-pituitary-adrenal axis function and hippocampal serotonin release in mice. J. Neuroendocrinol. 2006, 18:330-338.
31. Klok M.D., Alt S.R., Irurzun Lafitte A.J., Turner J.D., Lakke E.A., Huitinga I., Muller C.P., Zitman F.G., de Kloet E.R., Derijk R.H. Decreased expression of mineralocorticoid receptor mRNA and its splice variants in postmortem brain regions of patients with major depressive disorder. J. Psychiatr. Res. 2011, 45:871-878.
32. Koenig H.N., Olive M.F. The glucocorticoid receptor antagonist mifepristone reduces ethanol intake in rats under limited access conditions. Psychoneuroendocrinology 2004, 29:999-1003.
33. Lai M., McCormick J.A., Chapman K.E., Kelly P., Seckl J.R., Yau J.L.W. Differential regulation of corticosteroid receptors by monoamine neurotransmitters and antidepressant drugs in primary hippocampal culture. Neuroscience 2003, 118:975-984.
34. Lanfumey L., Mongeau R., Cohen-Salmon C., Hamon M. Corticosteroid-serotonin interactions in the neurobiological mechanisms of stress-related disorders. Neurosci. Biobehav. Rev. 2008, 32:1174-1184.
35. Leitch M.M., Ingram C.D., Young A.H., McQuade R., Gartside S.E. Flattening the corticosterone rhythm attenuates 5-HT1A autoreceptor function in the rat: relevance for depression. Neuropsychopharmacology 2003, 28:119-125.
36. Lira A., Zhou M., Castanon N., Ansorge M.S., Gordon J.A., Francis J.H., Bradley-Moore M., Lira J., Underwood M.D., Arango V., Kung H.F., Hofer M.A., Hen R., Gingrich J.A. Altered depression-related behaviors and functional changes in the dorsal raphe nucleus of serotonin transporter-deficient mice. Biol. Psychiatry 2003, 54:960-971.
37. Lopez J.F., Chalmers D.T., Little K.Y., Watson S.J. Regulation of serotonin1A, glucocorticoid, and mineralocorticoid receptor in rat and human hippocampus: implications for the neurobiology of depression. Biol. Psychiatry 1998, 43:547-573.
38. Lucas G., Rymar V.V., Du J., Mrie-Filali O., Bisgaard C., Manta S., Lambas-Senas L., Wiborg O., Haddjeri N., Pineyro G., Sadikot A.F., Debonnei G. Serotonin4 (5-HT4) receptor agonists are putative antidepressants with a rapid onset of action. Neuron 2007, 55:712-725.
39. Lupien S.J., McEwen B.S. The acute effects of corticosteroids on cognition: integration of animal and human model studies. Brain Res. Rev. 1997, 24:1-27.
40. Marwah A., Marwah P., Lardy H. Liquid chromatography-electrospray ionization mass spectrometric analysis of corticosterone in rat plasma using selected ion monitoring. J. Chromatogr. 2001, 757:333-342.
41. McEwen B.S. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol. Rev. 2007, 87:873-904.
42. McKittrick C.R., Blanchard D.C., Blanchard R.J., McEwen B.S., Sakai R.R. Serotonin receptor binding in a colony model of chronic social stress. Biol. Psychiatry 1995, 37:383-393.
43. Mineur Y.S., Belzung C., Crusio W.E. Effect of unpredictable chronic mild stress on anxiety and depression-like behavior in mice. Behav. Brain Res. 2006, 175:43-60.
44. Mitra R., Ferguson D., Sapolsky R.M. Mineralocorticoid receptor overexpression in basolateral amygdale reduces corticosterone secretion and anxiety. Biol. Psychiatry 2009, 66:686-690.
45. Montero-Pedrazuela A., Venero C., Lavado-Autric R., Femandez-Lamo I., Garcia-Verdugo J.M., Bernal J., Guadano-Ferraz A. Modulation of adult hippocampal neurogenesis by thyroid hormones: implications in depressive-like behavior. Mol. Psychiatry 2006, 11:361-371.
46. Nestler E.J., Barrot M., DiLeone R.J., Eisch A.J., Gold S.J., Monteggia L.M. Neurobiology of depression. Neuron 2002, 34:13-25.
47. Oitzl M.S., de Kloet E.R. Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behav. Neurosci. 1992, 106:62-71.
48. Otte C., Hinkelmann K., Moritz S., Yassouridis A., Jahn H., Wiedemann K., Kellner M. Modulation of the mineralocorticoid receptor as add-on treatment in depression: a randomized, double-blind, placebo-controlled proof-of-concept study. J. Psychiatr. Res. 2010, 44:339-346.
49. Ou X.M., Storring J.M., Kushwaha N., Albert P.R. Heterodimerization of mineralocorticoid and glucocorticoid receptors at a novel negative response element of the 5-HT1A receptor gene. J. Biol. Chem. 2001, 276:14299-14307.
50. Ozawa H. Steroid hormones, their receptors and neuroendocrine system. J. Nippon Med. Sch. 2005, 72:316-325.
51. Pariante C.M. The glucocorticoid receptor: part of the solution or part of the problem?. J. Psychopharm. 2006, 20:79-84.
52. Parker K.J., Schatzberg A.F., Lyons D.M. Neuroendocrine aspects of hypercortisolism in major depression. Horm. Behav. 2003, 43:60-66.
53. Pittenger C., Duman R.S. Stress, depression, and neuroplasticity: a convergence of mechanisms. Neuropsychopharmacology 2008, 33:88-109.
54. Porsolt R.D., Bertin A., Jalfre M. Behavioral despair in mice: a primary screening test for antidepressants. Arch. Int. Pharmacol. Ther. 1977, 229:327-336.
55. Reul J.M., de Kloet E.R., van Sluijs F.J., Rijnberk A., Rothuizen J. Binding characteristics of mineralocorticoid and glucocorticoid receptors in dog brain and pituitary. Endocrinology 1990, 127:907-915.
56. Richardson J.S. Brain part monoamines in the neuroendocrine mechanisms activated by immobilization stress in the rat. Int. J. Neurosci. 1984, 23:57-67.
57. Ridder S., Chourbaji S., Hellweq R., Urani A., Zacher C., Schmid W., Zink M., Hortnaql H., Flor H., Henn F.A., Schutz G., Gass P. Mice with genetically altered glucocorticoid receptor expression show altered sensitivity for stress-induced depressive reactions. J. Neurosci. 2005, 25:6243-6250.
58. Robertson D.A.F., Beattie J.E., Reid I.C., Balfour D.J.K. Regulation of corticosteroid receptors in the rat brain: the role of serotonin and stress. Eur. J. Neurosci. 2005, 21:1511-1520.
59. Roozendaal B. Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinology 2000, 25:213-238.
60. Sonino N., Fallo F., Fava G.A. Psychosomatic aspects of Cushing's syndrome. Rev. Endocr. Metab. Disord. 2010, 11:95-104.
61. Srinivasan G., Patel N.T., Thompson E.B. Heat shock protein is tightly associated with the recombinant human glucocorticoid receptor: glucocorticoid response element complex. Mol. Endocrinol. 1994, 8:189-196.
62. Steru L., Chermat R., Thierry B., Simon P. The tail suspension test: a new method for screening antidepressants in mice. Psychopharmacology 1985, 85:367-370.
63. Sullivan P.F., Neale M.C., Kendler K.S. Genetic epidemiology of major depression: review and meta-analysis. Am. J. Psychiatry 2000, 157:1552-1562.
64. Tata D.A., Anderson B.J. The effects of chronic glucocorticoid exposure on dendritic length, synapse numbers and glial volume in animal models: implications for hippocampal volume reductions in depression. Physiol. Behav. 2010, 99:186-193.
65. Ter Horst J.P., van der Mark M.H., Arp M., Berger S., de Kloet E.R., Oitzl M.S. Stress or no stress: mineralocorticoid receptors in the forebrain regulate behavioral adaptation. Neurobiol. Learn. Mem. 2012, 98:33-40.
66. Terouanne B., Tahiri B., Georget V., Belon C., Poujol N., Avances B., Orio F., Balaguer B., Sultan C. A stable prostatic bioluminescent cell line to investigate androgen and antiandrogen effects. Mol. Cell. Endocrinol. 2000, 160:39-49.
67. Tuck M.L., Sowers J.R., Fittingoff D.B., Fisher J.S., Berg G.J., Asp N.D., Mayes D.M. Plasma corticosteroid concentrations during spironolactone administration: evidence for adrenal biosynthetic blockade in man. J. Clin. Endocrinol. Metab. 1981, 52:1057-1061.
68. van der Lely A.-J., Foeken K., van der Mast R.C., Lamberts S.W.J. Rapid reversal of acute psychosis in the Cushing syndrome with the cortisol-receptor antagonist mifepristone (RU486). Ann. Intern. Med. 1991, 114:143-144.
69. Vermeer H., Hendriks-Stegeman B.I., van der Burg B., van Buul-Offers S.C., Jansen M. Glucocorticoid-induced increase in lymphocytic FKBP51 messenger ribonucleic acid expression: a potential marker for glucocorticoid sensitivity, potency, and bioavailability. J. Clin. Endocrinol. Metab. 2003, 88:277-284.
70. Vyas A., Mitra R., Rao B.S.S., Chattarji S. Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J. Neurosci. 2002, 22:6810-6818.
71. Webster J.I., Carlstedt-Duke J. Involvement of multidrug resistance proteins (MDR) in the modulation of glucocorticoid response. J. Steroid Biochem. Mol. Biol. 2002, 82:277-288.
72. Webster M.J., O'Grady J., Orthmann C., Weickert C. Decreased glucocorticoid receptor mRNA levels in individuals with depression, bipolar disorder and schizophrenia. Schizophr. Res. 2000, 41:111.
73. Wei Q., Lu X.Y., Liu L., Schafer G., Shieh K.R., Burke S., Robinson T.E., Watson S.J., Seasholtz A.F., Akil H. Glucocorticoid receptor overexpression in forebrain: a mouse model of increased emotional liability. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:11851-11856.
74. Wissink S., Meijer O., Pearce D., van der Burg B., van der Saag P.T. Regulation of the rat serotonin-1A receptor gene by corticosteroids. J. Biol. Chem. 2000, 275:1321-1326.
75. Wulsin A.C., Herman J.P., Solomon M.B. Mifepristone decreases depression-like behavior and modulates neuroendocrine and central hypothalamic-pituitary-adrenocortical axis responsiveness to stress. Psychoneuroendocrinology 2010, 35:1100-1112.
76. Xing G.Q., Russell S., Webster M.J., Post R.M. Decreased expression of mineralocorticoid receptor mRNA in the prefrontal cortex in schizophrenia and bipolar disorder. Int. J. Neuropsychopharmacol. 2004, 7:143-153.
77. Xu Z., Zhang Y., Hou B., Gao Y., Wu Y., Zhang C. Chronic corticosterone administration from adolescence through early adulthood attenuates depression-like behaviors in mice. J. Affect. Disord. 2010, 131:128-135.
78. Young A.H., Gallagher P., Watson S., Del-Estal D., Owen B.M., Ferrier I.N. Improvements in neurocognitive function and mood following adjunctive treatment with mifepristone (RU-486) in bipolar disorder. Neuropsychopharmacology 2004, 29:1538-1545.
79. Zhe D., Fang H., Yuxiu S. Expression of hippocampal mineralocorticoid receptor (MR) and glucocorticoid receptor (GR) in the single-prolonged stress-rats. Acta Histochem. Cytochem. 2008, 41:89-95.
80. Zhou M., Kindt M., Joels M., Krugers H.J. Blocking mineralocorticoid receptors prior to retrieval reduces contextual fear memory in mice. PLoS ONE 2011, 6:1-9.