Estradiol accelerates the effects of fluoxetine on serotonin 1A receptor signaling

Psychoneuroendocrinology

Volumn 38, Issue 7, 2013, Pages 1145-1157

  Li, Qian ^a   Sullivan, Nicole R ^b   McAllister, Carrie E ^a   Van de Kar, Louis D ^b   Muma, Nancy A ^a  

^a UNIVERSITY OF KANSAS   (United States)

^b LOYOLA UNIVERSITY CHICAGO   (United States)

Author keywords

5 HT1A receptors; ACTH; Detergent resistant microdomain; G z; GPR30; Lipid raft; Oxytocin; SSRIs; Sumoylation

Indexed keywords

2 DIPROPYLAMINO 8 HYDROXYTETRALIN; CORTICOTROPIN; ESTRADIOL; FLUOXETINE; G PROTEIN COUPLED RECEPTOR 30; OXYTOCIN; SEROTONIN 1A RECEPTOR; SUMO 1 PROTEIN; TRITON X 100;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DESENSITIZATION; ENZYME ACTIVITY; FEMALE; MOLECULAR DYNAMICS; MOLECULAR WEIGHT; NONHUMAN; OVARIECTOMY; PARAVENTRICULAR THALAMIC NUCLEUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION; SUMOYLATION;

8-HYDROXY-2-(DI-N-PROPYLAMINO)TETRALIN; ADRENOCORTICOTROPIC HORMONE; ANIMALS; DRUG INTERACTIONS; ESTRADIOL; FEMALE; FLUOXETINE; HIPPOCAMPUS; OXYTOCIN; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, SEROTONIN, 5-HT1A; SEROTONIN RECEPTOR AGONISTS; SEROTONIN UPTAKE INHIBITORS; SIGNAL TRANSDUCTION;

EID: 84877924636     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2012.11.005     Document Type: Article

References (54)

1. Albert P.R., Lemonde S. 5-HT1A receptors, gene repression, and depression: guilt by association. Neuroscientist 2004, 10:575-593.
2. Alexander J.L., Dennerstein L., Woods N.F., Kotz K., Halbreich U., Burt V., Richardson G. Neurobehavioral impact of menopause on mood. Expert. Rev. Neurother. 2007, 7:S81-S91.
3. Allen J.A., Halverson-Tamboli R.A., Rasenick M.M. Lipid raft microdomains and neurotransmitter signalling. Nat. Rev. Neurosci. 2007, 8:128-140.
4. Allen J.A., Yu J.Z., Dave R.H., Bhatnagar A., Roth B.L., Rasenick M.M. Caveolin-1 and lipid microdomains regulate Gs trafficking and attenuate Gs/adenylyl cyclase signaling. Mol. Pharmacol. 2009, 76:1082-1093.
5. Artigas F., Adell A., Celada P. Pindolol augmentation of antidepressant response. Curr. Drug Targets 2006, 7:139-147.
6. Bagdy G. Role of the hypothalamic paraventricular nucleus in 5-HT1A, 5-HT2A and 5-HT2C receptor-mediated oxytocin, prolactin and ACTH/corticosterone responses. Behav. Brain Res. 1996, 73:277-280.
7. Bethea C.L., Gundlah C., Mirkes S.J. Ovarian steroid action in the serotonin neural system of macaques. Novartis. Found. Symp. 2000, 230:112-130.
8. Carrasco G.A., Van de Kar L.D. Neuroendocrine pharmacology of stress. Eur. J. Pharmacol. 2003, 463:235-272.
9. Cheng S.B., Quinn J.A., Graeber C.T., Filardo E.J. Down-modulation of the G-protein-coupled estrogen receptor, GPER, from the cell surface occurs via a trans-Golgi-proteasome pathway. J. Biol. Chem. 2011, 286:22441-22455.
10. Chini B., Parenti M. G-protein coupled receptors in lipid rafts and caveolae: how, when and why do they go there?. J. Mol. Endocrinol. 2004, 32:325-338.
11. Coryell W., Fiedorowicz J., Zimmerman M., Young E. HPA-axis hyperactivity and mortality in psychotic depressive disorder: preliminary findings. Psychoneuroendocrinology 2008, 33:654-658.
12. Creech R.D., Li Q., Carrasco G.A., Van de Kar L.D., Muma N.A. Estradiol induces partial desensitization of serotonin 1A receptor signaling in the paraventricular nucleus of the hypothalamus and alters expression and interaction of RGSZ1 and Galphaz. Neuropharmacology 2012, 62:2040-2049.
13. Dai Y., Dudek N.L., Patel T.B., Muma N.A. Transglutaminase-catalyzed transamidation: a novel mechanism for Rac1 activation by 5-hydroxytryptamine2A receptor stimulation. J. Pharmacol. Exp. Ther. 2008, 326:153-162.
14. Dennis M.K., Burai R., Ramesh C., Petrie W.K., Alcon S.N., Nayak T.K., Bologa C.G., Leitao A., Brailoiu E., Deliu E., Dun N.J., Sklar L.A., Hathaway H.J., Arterburn J.B., Oprea T.I., Prossnitz E.R. In vivo effects of a GPR30 antagonist. Nat. Chem. Biol. 2009, 5:421-427.
15. Estrada-Camarena E., Lopez-Rubalcava C., Fernandez-Guasti A. Facilitating antidepressant-like actions of estrogens are mediated by 5-HT1A and estrogen receptors in the rat forced swimming test. Psychoneuroendocrinology 2006, 31:905-914.
16. Fichter K.M., Flajolet M., Greengard P., Vu T.Q. Kinetics of G-protein-coupled receptor endosomal trafficking pathways revealed by single quantum dots. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:18658-18663.
17. Filardo E.J. Epidermal growth factor receptor (EGFR) transactivation by estrogen via the G-protein-coupled receptor. GPR30: a novel signaling pathway with potential significance for breast cancer. J. Steroid Biochem. Mol. Biol. 2002, 80:231-238.
18. Filardo E.J., Quinn J.A., Bland K.I., Frackelton A.R. Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Mol. Endocrinol. 2000, 14:1649-1660.
19. Filardo E.J., Thomas P. GPR30: a seven-transmembrane-spanning estrogen receptor that triggers EGF release. Trends Endocrinol. Metab. 2005, 16:362-367.
20. Flugge G., Pfender D., Rudolph S., Jarry H., Fuchs E. 5HT1A-receptor binding in the brain of cyclic and ovariectomized female rats. J. Neuroendocrinol. 1999, 11:243-249.
21. Garzon J., Rodriguez-Munoz M., Vicente-Sanchez A., Garcia-Lopez M.A., Martinez-Murillo R., Fischer T., Sanchez-Blazquez P. SUMO-SIM interactions regulate the activity of RGSZ2 proteins. PLoS One 2011, 6:e28557.
22. Gaynes B.N., Warden D., Trivedi M.H., Wisniewski S.R., Fava M., Rush A.J. What did STAR*D teach us? Results from a large-scale, practical, clinical trial for patients with depression. Psychiatr. Serv. 2009, 60:1439-1445.
23. Gomez-Gil E., Navines R., Martinez De Osaba M.J., Diaz-Ricart M., Escolar G., Salamero M., Martin-Santos R., Galan A., Gasto C. Hormonal responses to the 5-HT1A agonist buspirone in remitted endogenous depressive patients after long-term imipramine treatment. Psychoneuroendocrinology 2010, 35:481-489.
24. Hoyer D., Clarke D.E., Fozard J.R., Hartig P.R., Martin G.R., Mylecharane E.J., Saxena P.R., Humphrey P.P.A. VII. International Union of Pharmacology classification of receptors for 5-hydroxytryptamine (serotonin). Pharmacol. Rev. 1994, 46:157-204.
25. Kumari R., Francesconi A. Identification of GPCR localization in detergent resistant membranes. Methods Mol. Biol. 2011, 746:411-423.
26. Lents N.H., Irintcheva V., Goel R., Wheeler L.W., Baldassare J.J. The rapid activation of N-Ras by alpha-thrombin in fibroblasts is mediated by the specific G-protein Galphai2-Gbeta1-Ggamma5 and occurs in lipid rafts. Cell. Signal. 2009, 21:1007-1014.
27. Lerer B., Gelfin Y., Gorfine M., Allolio B., Lesch K.P., Newman M.E. 5-HT1A receptor function in normal subjects on clinical doses of fluoxetine: blunted temperature and hormone responses to ipsapirone challenge. Neuropsychopharmacology 1999, 20:628-639.
28. Lesch K.P., Schulte H.M., Osterheider M., Muller T. Long-term fluoxetine treatment decreases 5-HT 1A receptor responsivity in obsessive-compulsive disorder. Psychopharmacology (Berl.) 1991, 105:415-420.
29. Li Q., Battaglia G., Van de Kar L.D. Autoradiographic evidence for differential G-protein coupling of 5-HT1A receptors in rat brain: lack of effect of repeated injections of fluoxetine. Brain Res. 1997, 769:141-151.
30. Li Q., Holmes A., Ma L., Van de Kar L.D., Garcia F., Murphy D.L. Medial hypothalamic 5-hydroxytryptamine (5-HT)1A receptors regulate neuroendocrine responses to stress and exploratory locomotor activity: application of recombinant adenovirus containing 5-HT1A sequences. J. Neurosci. 2004, 24:10868-10877.
31. Li Q., Muma N.A., Battaglia G., Van de Kar L.D. A desensitization of hypothalamic 5-HT1A receptors by repeated injections of paroxetine: reduction in the levels of G(i) and G(o) proteins and neuroendocrine responses, but not in the density of 5-HT1A receptors. J. Pharmacol. Exp. Ther. 1997, 282:1581-1590.
32. Li Q., Muma N.A., Van de Kar L.D. Chronic fluoxetine induces a gradual desensitization of 5-HT 1A receptors: reductions in hypothalamic and midbrain G i and G o proteins and in neuroendocrine responses to a 5-HT 1A agonist. J. Pharmacol. Exp. Ther. 1996, 279:1035-1042.
33. Lu N.Z., Bethea C.L. Ovarian steroid regulation of 5-HT1A receptor binding and G protein activation in female monkeys. Neuropsychopharmacology 2002, 27:12-24.
34. McAllister C.E., Creech R.D., Kimball P.A., Muma N.A., Li Q. GPR30 is necessary for estradiol-induced desensitization of 5-HT(1A) receptor signaling in the paraventricular nucleus of the rat hypothalamus. Psychoneuroendocrinology 2012, 37:1248-1260.
35. Millan M.J. The neurobiology and control of anxious states. Prog. Neurobiol. 2003, 70:83-244.
36. Mize A.L., Young L.J., Alper R.H. Uncoupling of 5-HT1A receptors in the brain by estrogens: regional variations in antagonism by ICI 182,780. Neuropharmacology 2003, 44:584-591.
37. Moffett S., Brown D.A., Linder M.E. Lipid-dependent targeting of G proteins into rafts. J. Biol. Chem. 2000, 275:2191-2198.
38. Osei-Owusu P., James A., Crane J., Scrogin K.E. 5-Hydroxytryptamine 1A receptors in the paraventricular nucleus of the hypothalamus mediate oxytocin and adrenocorticotropin hormone release and some behavioral components of the serotonin syndrome. J. Pharmacol. Exp. Ther. 2005, 313:1324-1330.
39. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2007, Academic Press Inc. 6th ed.
40. Polter A.M., Li X. 5-HT1A receptor-regulated signal transduction pathways in brain. Cell. Signal. 2010, 22:1406-1412.
41. Prossnitz E.R., Oprea T.I., Sklar L.A., Arterburn J.B. The ins and outs of GPR30: a transmembrane estrogen receptor. J. Steroid Biochem. Mol. Biol. 2008, 109:350-353.
42. Pucadyil T.J., Chattopadhyay A. Cholesterol modulates ligand binding and G-protein coupling to serotonin(1A) receptors from bovine hippocampus. Biochim. Biophys. Acta 2004, 1663:188-200.
43. Raap D.K., DonCarlos L., Garcia F., Muma N.A., Wolf W.A., Battaglia G., Van de Kar L.D. Estrogen desensitizes 5-HT1A receptors and reduces levels of G(z), G(i1) and G(i3) proteins in the hypothalamus. Neuropharmacology 2000, 39:1823-1832.
44. Raap D.K., Evans S., Garcia F., Li Q., Muma N.A., Wolf W.A., Battaglia G., Van de Kar L.D. Daily injections of fluoxetine induce dose-dependent desensitization of hypothalamic 5-HT1A receptors: reductions in neuroendocrine responses to 8-OH-DPAT and in levels of G(z) and G(i) proteins. J. Pharmacol. Exp. Ther. 1999, 288:98-106.
45. Rossi D.V., Dai Y., Thomas P., Carrasco G.A., DonCarlos L.L., Muma N.A., Li Q. Estradiol-induced desensitization of 5-HT1A receptor signaling in the paraventricular nucleus of the hypothalamus is independent of estrogen receptor-beta. Psychoneuroendocrinology 2010, 35:1023-1033.
46. Sanchez M.G., Estrada-Camarena E., Belanger N., Morissette M., Di Paolo T. Estradiol modulation of cortical, striatal and raphe nucleus 5-HT1A and 5-HT2A receptors of female hemiparkinsonian monkeys after long-term ovariectomy. Neuropharmacology 2011, 60:642-652.
47. Serres F., Li Q., Garcia F., Raap D.K., Battaglia G., Muma N.A., Van de Kar L.D. Evidence that G(z)-proteins couple to hypothalamic 5-HT1A receptors in vivo. J. Neurosci. 2000, 20:3095-3103.
48. Simons K., Gerl M.J. Revitalizing membrane rafts: new tools and insights. Nat. Rev. Mol. Cell Biol. 2010, 11:688-699.
49. Sugama J., Yu J.Z., Rasenick M.M., Nakahata N. Mastoparan inhibits beta-adrenoceptor-G(s) signaling by changing the localization of Galpha(s) in lipid rafts. Cell. Signal. 2007, 19:2247-2254.
50. Tu Y., Wang J., Ross E.M. Inhibition of brain Gz GAP and other RGS proteins by palmitoylation of G protein alpha subunits. Science 1997, 278:1132-1135.
51. Van de Kar L.D., Blair M.L. Forebrain pathways mediating stress-induced hormone secretion. Front. Neuroendocrinol. 1999, 20:1-48.
52. Wasserman D., Wasserman J., Sokolowski M. Genetics of HPA-axis, depression and suicidality. Eur. Psychiatry 2010, 25:278-280.
53. Xu H., Qin S., Carrasco G.A., Dai Y., Filardo E.J., Prossnitz E.R., Battaglia G., DonCarlos L.L., Muma N.A. Extra-nuclear estrogen receptor GPR30 regulates serotonin function in rat hypothalamus. Neuroscience 2009, 158:1599-1607.
54. Yuyama K., Sekino-Suzuki N., Sanai Y., Kasahara K. Translocation of activated heterotrimeric G protein Galpha(o) to ganglioside-enriched detergent-resistant membrane rafts in developing cerebellum. J. Biol. Chem. 2007, 282:26392-26400.