Antidepressant fluoxetine enhances glucocorticoid receptor function in vitro by modulating membrane steroid transporters

British Journal of Pharmacology

Volumn 139, Issue 6, 2003, Pages 1111-1118

  Pariante, Carmine M ^a   Kim, Richard B ^b   Makoff, Andrew ^a   Kerwin, Robert W ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b VANDERBILT UNIVERSITY   (United States)

Author keywords

Antidepressant; Caco 2 cells; Corticosterone; Cortisol; Fluoxetine; Glucocorticoid receptor; Hypothalamic pituitary adrenal (HPA) axis; L929 LMCAT cells; Multidrug resistance (MDR); P glycoprotein (PGP)

Indexed keywords

ANTIDEPRESSANT AGENT; CARRIER PROTEIN; CORTICOSTERONE; DEXAMETHASONE; FLUOXETINE; GLUCOCORTICOID RECEPTOR; GLYCOPROTEIN P; HYDROCORTISONE; STEROID;

ANIMAL CELL; ARTICLE; CELL STRAIN CACO 2; DRUG ACTIVITY; FIBROBLAST; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM;

ANIMALS; ANTIDEPRESSIVE AGENTS, SECOND-GENERATION; CACO-2 CELLS; CORTICOSTERONE; FLUOXETINE; HUMANS; HYDROCORTISONE; MEMBRANE TRANSPORT MODULATORS; MEMBRANE TRANSPORT PROTEINS; MICE; RECEPTORS, GLUCOCORTICOID; STEROIDS;

EID: 0042168887     PISSN: 00071188     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.bjp.0705357     Document Type: Article

References (43)

1. BOSSUYT, X., MULLER, M., HAGENBUCH, B. & MEIER, P.J. (1996). Polyspecific drug and steroid clearance by an organic anion transporter of mammalian liver. J. Pharmacol. Exp. Ther., 276, 891-896.
2. BOURGEOIS, S., GRUOL, D.J., NEWBY, R.F. & RAJAH, F.M. (1993). Expression of an mdr gene is associated with a new form of resistance to dexamethasone-induced apoptosis. Mol. Endocrinol., 7, 840-851.
3. BOUWER, C., CLAASSEN, J., DINAN, T.G. & NEMEROFF, C.B. (2000). Prednisone augmentation in treatment-resistant depression with fatigue and hypocortisolaemia: a case series. Depress. Anxiety, 12, 44-50.
4. BROOKSBANK, B.W., BRAMMALL, M.A. & SHAW, D.M. (1973). Estimation of cortisol, cortisone and corticosterone in cerebral cortex, hypothalamus and other regions of the human brain after natural death and after death by suicide. Steroids Lipids Res., 4, 162-183.
5. BUDZISZEWSKA, B., JAWORSKA-FEIL, L., KAJTA, M. & LASON, W. (2000). Antidepressant drugs inhibit glucocorticoid receptor-mediated gene transcription - a possible mechanism. Br. J. Pharmacol., 130, 1385-1393.
6. CASTAING, M., BROUANT, P., LOISEAU, A., SANTELLI-ROUVIER, C., SANTELLI, M., ALIBERT-FRANCO, S., MAHAMOUD, A. & BARBE, J. (2000). Membrane permeation by multidrug-resistance-modulators and non-modulators: effects of hydrophobicity and electric charge. J. Pharm. Pharmacol., 52, 289-296.
7. COTTER, D. & PARIANTE, C.M. (2002). Stress and the progression of the developmental hypothesis of schizophrenia. Br. J. Psychiatry, 181, 363-365.
8. DE KLOET, E.R., VREUGDENHIL, E., OITZL, M.S. & JOELS, M. (1998). Brain corticosteroid receptor balance in health and disease. Endocr. Rev., 19, 269-301.
9. DEBATTISTA, C., POSENER, J.A., KALEHZAN, B.M. & SCHATZBERG, A.F. (2000). Acute antidepressant effects of intravenous hydrocortisone and CRH in depressed patients: a double-blind, placebo-controlled study. Am. J. Psychiatry, 157, 1334-1337.
10. DINAN, T.G., LAVELLE, E., COONEY, J., BURNETT, F., SCOTT, L., DASH, A., THAKORE, J. & BERTI, C. (1997). Dexamethasone augmentation in treatment-resistant depression. Acta Psychiatr. Scand., 95, 58-61.
11. DUMAN, R.S., NAKAGAWA, S. & MALBERG, J. (2001). Regulation of adult neurogenesis by antidepressant treatment. Neuropsychopharmacology, 25, 836-844.
12. EDGAR, V.A., STERIN-BORDA, L., CREMASCHI, G.A. & GENARO, A.M. (1999). Role of protein kinase C and cAMP in fluoxetine effects on human T-cell proliferation. Eur. J. Pharmacol., 372, 65-73.
13. EKINS, S., KIM, R.B., LEAKE, B.F., DANTZIG, A.H., SCHUETZ, E.G., LAN, L.B., YASUDA, K., SHEPARD, R.L., WINTER, M.A., SCHUETZ, J.D., WIKEL, J.H. & WRIGHTON, S.A. (2002). Three-dimensional quantitative structure-activity relationships of inhibitors of P-glycoprotein. Mol. Pharmacol., 61, 964-973.
14. FORD, J.M. (1996). Experimental reversal of P-glycoprotein-mediated multidrug resistance by pharmacological chemosensitisers. Eur. J. Cancer, 32A, 991-1001.
15. GLOTZBACH, R.K. & PRESKORN, S.H. (1982). Brain concentrations of tricyclic antidepressants: single-dose kinetics and relationship to plasma concentrations in chronically dosed rats. Psychopharmacology (Berl.), 78, 25-27.
16. KARSSEN, A.M., MEIJER, O.C., VAN DER SANDT, I., LUCASSEN, P.J., DE LANGE, E.G., DE BOER, A.G. & DE KLOET, E.R. (2001). Multidrug resistance P-glycoprotein hampers the access of cortisol but not of corticosterone to mouse and human brain. Endocrinology, 142, 2686-2694.
17. KRALLI, A. & YAMAMOTO, K.R. (1996). An FK506-sensitive transporter selectively decreases intracellular levels and potency of steroid hormones. J. Biol. Chem., 271, 17152-17156.
18. LACKNER, C., DAUFELDT, S., WILDT, L. & ALLERA, A. (1998). Glucocorticoid-recognizing and -effector sites in rat liver plasma membrane. Kinetics of corticosterone uptake by isolated membrane vesicles. III. Specificity and stereospecificity. J. Steroid Biochem. Mol. Biol., 64, 69-82.
19. LAI, M., MCCORMICK, J.A., CHAPMAN, K.E., KELLY, P.A.T., SECKL, J.R. & YAU, J.L.W. (2003). Differential regulation of corticosteroid receptors by monoamine neurotransmitters and antidepressant drugs in primary hippocampal culture. Neuroscience, 118, 975-984.
20. MARSAUD, V., MERCIER-BODARD, C., FORTIN, D., LE BIHAN, S. & RENOIR, J.M. (1998). Dexamethasone and triamcinolone acetonide accumulation in mouse fibroblasts is differently modulated by the immunosuppressants cyclosporin A, FK506, rapamycin and their analogues, as well as by other P-glycoprotein ligands. J. Steroid Biochem. Mol. Biol., 66, 11-25.
21. MCEWEN, B.S. (2000). The neurobiology of stress: from serendipity to clinical relevance. Brain Res., 886, 172-189.
22. MEDH, R.D., LAY, R.H. & SCHMIDT, T.J. (1998). Agonist-specific modulation of glucocorticoid receptor-mediated transcription by immunosuppressants. Mol. Cell Endocrinol., 138, 11-23.
23. MERRY, S., HAMILTON, T.G., FLANIGAN, P., FRESHNEY, R.I. & KAYE, S.B. (1991). Circumvention of pleiotropic drug resistance in subcutaneous tumours in vivo with verapamil and clomipramine. Eur. J. Cancer, 27, 31-34.
24. MILLER, A.H., VOGT, G.J. & PEARCE, B.D. (2002). The phosphodiesterase type 4 inhibitor, rolipram, enhances glucocorticoid receptor function. Neuropsychopharmacology, 27, 939-948.
25. ORTH, D. & KOVACS, W. (1998). The adrenal cortex. In: 9th edn. Williams Textbook of Endocrinology. Wilson, J., Foster, D., Kronenberg, H. & Larsen, P. pp. 517-664. Philadelphia: W.B. Saunders Company.
26. PARIANTE, C.M., HYE, A., WILLIAMSON, R., MAKOFF, A., LOVESTONE, S. & KERWIN, R.W. (2003). The antidepressant clomipramine regulates cortisol intracellular concentrations and glucocorticoid receptor expression in fibroblasts and rat primary neurones. Neuropsychopharmacology. (in press).
27. PARIANTE, C.M., MAKOFF, A., LOVESTONE, S., FEROLI, S., HEYDEN, A., MILLER, A.H. & KERWIN, R.W. (2001a). Antidepressants enhance glucocorticoid receptor function in vitro by modulating the membrane steroid transporters. Br. J. Pharmacol., 134, 1335-1343.
28. PARIANTE, C.M. & MILLER, A.H. (2001). Glucocorticoid receptors in major depression: relevance to pathophysiology and treatment. Biol. Psychiatry, 49, 391-404.
29. PARIANTE, C.M., PAPADOPOULOS, A.S., POON, L., CHECKLEY, S.A., ENGLISH, J., KERWIN, R.W. & LIGHTMAN, S. (2002). A novel prednisolone suppression test for the hypothalamic-pituitary-adrenal axis. Biol. Psychiatry, 51, 922-930.
30. PARIANTE, C.M., PEARCE, B.D., PISELL, T.L., OWENS, M.J. & MILLER, A.H. (1997). Steroid-independent translocation of the glucocorticoid receptor by the antidepressant desipramine. Mol. Pharmacol., 52, 571-581.
31. PARIANTE, C.M., PEARCE, B.D., PISELL, T.L., SANCHEZ, C.I., PO, C., SU, C. & MILLER, A.H. (1999). The proinflammatory cytokine, interleukin-1 alpha, reduces glucocorticoid receptor translocation and function. Endocrinology, 140, 4359-4366.
32. PARIANTE, C.M., PEARCE, B.D., PISELL, T.L., SU, C. & MILLER, A.H. (2001b). The steroid receptor antagonists RU40555 and RU486 activate glucocorticoid receptor translocation and are not excreted by the steroid hormones transporter in L929 cells. J. Endocrinol., 169, 309-320.
33. PEPIN, M.C., GOVINDAN, M.V. & BARDEN, N. (1992). Increased glucocorticoid receptor gene promoter activity after antidepressant treatment. Mol. Pharmacol., 41, 1016-1022.
34. RANGARAJAN, P.N., UMESONO, K. & EVANS, R.M. (1992). Modulation of glucocorticoid receptor function by protein kinase A. Mol. Endocrinol., 6, 1451-1457.
35. REGINA, A., KOMAN, A., PICIOTTI, M., EL HAFNY, B., CENTER, M.S., BERGMANN, R., COURAUD, P.O. & ROUX, F. (1998). Mrp1 multidrug resistance-associated protein and P-glycoprotein expression in rat brain microvessel endothelial cells. J. Neurochem., 71, 705-715.
36. SANCHEZ, E.R., HU, J.L., ZHONG, S., SHEN, P., GREENE, M.J. & HOUSLEY, P.R. (1994). Potentiation of glucocorticoid receptor-mediated gene expression by heat and chemical shock. Mol. Endocrinol., 8, 408-421.
37. THOME, J., SAKAI, R., SHIN, K., STEEPEN, C., ZHANG, Y.J., IMPEY, S., STORM, D. & DUMAN, R.S. (2000). cAMP response element-mediated gene transcription is upregulated by chronic antidepressant treatment. J. Neurosci., 20, 4030-4036.
38. UHR, M. & GRAUER, M.T. (2003). abcblab P-glycoprotein is involved in the uptake of citalopram and trimipramine into the brain of mice. J. Psychiatr Res., 37, 179-185.
39. UHR, M., HOLSBOER, F. & MULLER, M.B. (2002). Penetration of endogenous steroid hormones corticosterone, cortisol, aldosterone and progesterone into the brain is enhanced in mice deficient for both mdr1a and mdr1b P-glycoproteins. J. Neuroendocrinol., 14, 753-759.
40. UHR, M., STECKLER, T., YASSOURIDIS, A. & HOLSBOER, F. (2000). Penetration of amitriptyline, but not of fluoxetine, into brain is enhanced in mice with blood-brain barrier deficiency due to mdr1a P-glycoprotein gene disruption. Neuropsychopharmacology, 22, 380-387.
41. WEBSTER, J.I. & CARLSTEDT-DUKE, J. (2002). Involvement of multidrug resistance proteins (MDR) in the modulation of glucocorticoid response. J. Steroid Biochem. Mol. Biol., 82, 277-288.
42. WOLF, D.C. & HORWITZ, S.B. (1992). P-glycoprotein transports corticosterone and is photoaffinity-labeled by the steroid. Int. J. Cancer, 52, 141-146.
43. YAU, J.L., NOBLE, J., HIBBERD, C. & SECKL, J.R. (2001). Short-term administration of fluoxetine and venlafaxine decreases corticosteroid receptor mRNA expression in the rat hippocampus. Neurosci. Lett., 306, 161-164.