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Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Review Article

Role of Estradiol in the Expression of Genes Involved in Serotonin Neurotransmission: Implications for Female Depression

Author(s): Olivia Tania Hernández-Hernández, Lucía Martínez-Mota*, José Jaime Herrera-Pérez and Graciela Jiménez-Rubio

Volume 17, Issue 5, 2019

Page: [459 - 471] Pages: 13

DOI: 10.2174/1570159X16666180628165107

Price: $65

Abstract

Background: In women, changes in estrogen levels may increase the incidence and/or symptomatology of depression and affect the response to antidepressant treatments. Estrogen therapy in females may provide some mood benefits as a single treatment or might augment clinical response to antidepressants that inhibit serotonin reuptake.

Objective: We analyzed the mechanisms of estradiol action involved in the regulation of gene expression that modulates serotonin neurotransmission implicated in depression.

Method: Publications were identified by a literature search on PubMed.

Results: The participation of estradiol in depression may include regulation of the expression of tryptophan hydroxylase-2, monoamine oxidase A and B, serotonin transporter and serotonin-1A receptor. This effect is mediated by estradiol binding to intracellular estrogen receptor that interacts with estrogen response elements in the promoter sequences of tryptophan hydroxylase-2, serotonin transporter and monoamine oxidase-B. In addition to directly binding deoxyribonucleic acid, estrogen receptor can tether to other transcription factors, including activator protein 1, specificity protein 1, CCAAT/enhancer binding protein β and nuclear factor kappa B to regulate gene promoters that lack estrogen response elements, such as monoamine oxidase-A and serotonin 1A receptor.

Conclusion: Estradiol increases tryptophan hydroxylase-2 and serotonin transporter expression and decreases the expression of serotonin 1A receptor and monoamine oxidase A and B through the interaction with its intracellular receptors. The understanding of molecular mechanisms of estradiol regulation on the protein expression that modulates serotonin neurotransmission will be helpful for the development of new and more effective treatment for women with depression.

Keywords: Depression, estradiol, monoamine oxidases, serotonin transporter, serotonin 1A receptor, tryptophan hydroxylase.

Graphical Abstract

[1]
Marcus, S.M.; Young, E.A.; Kerber, K.B.; Kornstein, S.; Farabaugh, A.H.; Mitchell, J.; Wisniewski, S.R.; Balasubramani, G.K.; Trivedi, M.H.; Rush, A.J. Gender differences in depression: findings from the STAR*D study. J. Affect. Disord., 2005, 87(2-3), 141-150. [http://dx.doi.org/10.1016/j.jad.2004.09.008]. [PMID: 15982748].
[2]
Kessler, R.C. Epidemiology of women and depression. J. Affect. Disord., 2003, 74(1), 5-13. [http://dx.doi.org/10.1016/S0165-0327(02)00426-3]. [PMID: 12646294].
[3]
Schmidt, P.J.; Rubinow, D.R. Sex hormones and mood in the perimenopause. Ann. N. Y. Acad. Sci., 2009, 1179, 70-85. [http://dx. doi.org/10.1111/j.1749-6632.2009.04982.x]. [PMID: 19906233].
[4]
Schneider, L.S.; Small, G.W.; Hamilton, S.H.; Bystritsky, A.; Nemeroff, C.B.; Meyers, B.S. Estrogen replacement and response to fluoxetine in a multicenter geriatric depression trial. Am. J. Geriatr. Psychiatry, 1997, 5(2), 97-106. [http://dx.doi.org/10.1097/00019442-199721520-00002]. [PMID: 9106373].
[5]
Schneider, L.S.; Small, G.W.; Clary, C.M. Estrogen replacement therapy and antidepressant response to sertraline in older depressed women. Am. J. Geriatr. Psychiatry, 2001, 9(4), 393-399. [http://dx. doi.org/10.1097/00019442-200111000-00007]. [PMID: 11739065].
[6]
Bethea, C.L.; Smith, A.W.; Centeno, M.L.; Reddy, A.P. Long-term ovariectomy decreases serotonin neuron number and gene expression in free ranging macaques. Neuroscience, 2011, 192, 675-688. [http://dx.doi.org/10.1016/j.neuroscience.2011.06.003]. [PMID: 21763405].
[7]
Björnström, L.; Sjöberg, M. Mechanisms of estrogen receptor signaling: convergence of genomic and nongenomic actions on target genes. Mol. Endocrinol., 2005, 19(4), 833-842. [http://dx.doi. org/10.1210/me.2004-0486]. [PMID: 15695368].
[8]
Flattem, N.L.; Blakely, R.D. Modified structure of the human serotonin transporter promoter. Mol. Psychiatry, 2000, 5(1), 110-115. [http://dx.doi.org/10.1038/sj.mp.4000585]. [PMID: 10673778].
[9]
Hiroi, R.; Handa, R.J. Estrogen receptor-β regulates human tryptophan hydroxylase-2 through an estrogen response element in the 5′ untranslated region. J. Neurochem., 2013, 127(4), 487-495. [http:// dx.doi.org/10.1111/jnc.12401]. [PMID: 24033289].
[10]
Zhang, Z.; Chen, K.; Shih, J.C.; Teng, C.T. Estrogen-related receptors-stimulated monoamine oxidase B promoter activity is down-regulated by estrogen receptors. Mol. Endocrinol., 2006, 20(7), 1547-1561. [http://dx.doi.org/10.1210/me.2005-0252]. [PMID: 16484337].
[11]
Denney, R.M.; Sharma, A.; Dave, S.K.; Waguespack, A. A new look at the promoter of the human monoamine oxidase A gene: mapping transcription initiation sites and capacity to drive luciferase expression. J. Neurochem., 1994, 63(3), 843-856. [http://dx.doi.org/10.1046/j.1471-4159.1994.63030843.x]. [PMID: 7519662].
[12]
Wissink, S.; van der Burg, B.; Katzenellenbogen, B.S.; van der Saag, P.T. Synergistic activation of the serotonin-1A receptor by nuclear factor-κ B and estrogen. Mol. Endocrinol., 2001, 15(4), 543-552. [PMID: 11266506].
[13]
Owens, M.; Herbert, J.; Jones, P.B.; Sahakian, B.J.; Wilkinson, P.O.; Dunn, V.J.; Croudace, T.J.; Goodyer, I.M. Elevated morning cortisol is a stratified population-level biomarker for major depression in boys only with high depressive symptoms. Proc. Natl. Acad. Sci. USA, 2014, 111(9), 3638-3643. [http://dx.doi.org/10. 1073/pnas.1318786111]. [PMID: 24550453].
[14]
Jacobsen, J.P.R.; Medvedev, I.O.; Caron, M.G. The 5-HT deficiency theory of depression: perspectives from a naturalistic 5-HT deficiency model, the tryptophan hydroxylase 2Arg439His knockin mouse. Philos. Trans. R. Soc. Lond. B Biol. Sci., 2012, 367(1601), 2444-2459. [http://dx.doi.org/10.1098/rstb.2012.0109]. [PMID: 22826344].
[15]
Soares, C.N. Mood disorders in midlife women: understanding the critical window and its clinical implications. Menopause, 2014, 21(2), 198-206. [http://dx.doi.org/10.1097/GME.0000000000000193]. [PMID: 24448106].
[16]
Joffe, H.; Cohen, L.S. Estrogen, serotonin, and mood disturbance: where is the therapeutic bridge?, 1998. 798-811
[17]
Deecher, D.; Andree, T.H.; Sloan, D.; Schechter, L.E. From menarche to menopause: exploring the underlying biology of depression in women experiencing hormonal changes. Psychoneuroendocrinology, 2008, 33(1), 3-17. [http://dx.doi.org/10.1016/j.psyneuen.2007.10. 006]. [PMID: 18063486].
[18]
Steiner, M.; Dunn, E.; Born, L. Hormones and mood: from menarche to menopause and beyond. J. Affect. Disord., 2003, 74(1), 67-83. [http://dx.doi.org/10.1016/S0165-0327(02)00432-9]. [PMID: 12646300].
[19]
Lokuge, S.; Frey, B.N.; Foster, J.A.; Soares, C.N.; Steiner, M. Depression in women: windows of vulnerability and new insights into the link between estrogen and serotonin. J. Clin. Psychiatry, 2011, 72(11), e1563-e1569. [http://dx.doi.org/10.4088/JCP.11com 07089]. [PMID: 22127200].
[20]
Martinez, P.E.; Rubinow, D.R.; Nieman, L.K.; Koziol, D.E.; Morrow, A.L.; Schiller, C.E.; Cintron, D.; Thompson, K.D.; Khine, K.K.; Schmidt, P.J. 5α-reductase inhibition prevents the luteal phase increase in plasma allopregnanolone levels and mitigates symptoms in women with premenstrual dysphoric disorder. Neuropsychopharmacology, 2016, 41(4), 1093-1102. [http://dx.doi. org/10.1038/npp.2015.246]. [PMID: 26272051].
[21]
Bloch, M.; Rotenberg, N.; Koren, D.; Klein, E. Risk factors for early postpartum depressive symptoms. Gen. Hosp. Psychiatry, 2006, 28(1), 3-8. [http://dx.doi.org/10.1016/j.genhosppsych.2005. 08.006]. [PMID: 16377359].
[22]
Freeman, E.W. Associations of depression with the transition to menopause. Menopause, 2010, 17(4), 823-827. [http://dx.doi.org/ 10.1097/gme.0b013e3181db9f8b]. [PMID: 20531231].
[23]
Cohen, L.S.; Soares, C.N.; Vitonis, A.F.; Otto, M.W.; Harlow, B.L. Risk for new onset of depression during the menopausal transition: the Harvard study of moods and cycles. Arch. Gen. Psychiatry, 2006, 63(4), 385-390. [http://dx.doi.org/10.1001/archpsyc.63.4.385]. [PMID: 16585467].
[24]
O’Lone, R.; Frith, M.C.; Karlsson, E.K.; Hansen, U. Genomic targets of nuclear estrogen receptors. Mol. Endocrinol., 2004, 18(8), 1859-1875. [http://dx.doi.org/10.1210/me.2003-0044]. [PMID: 15031323].
[25]
McEwen, B.S.; Alves, S.E. Estrogen actions in the central nervous system. Endocr. Rev., 1999, 20(3), 279-307. [PMID: 10368772].
[26]
Nilsson, S.; Mäkelä, S.; Treuter, E.; Tujague, M.; Thomsen, J.; Andersson, G.; Enmark, E.; Pettersson, K.; Warner, M.; Gustafsson, J.A. Mechanisms of estrogen action. Physiol. Rev., 2001, 81(4), 1535-1565. [http://dx.doi.org/10.1152/physrev.2001.81.4.1535]. [PMID: 11581496].
[27]
Berry, M.; Metzger, D.; Chambon, P. Role of the two activating domains of the oestrogen receptor in the cell-type and promoter-context dependent agonistic activity of the anti-oestrogen 4-hydroxytamoxifen. EMBO J., 1990, 9(9), 2811-2818. [PMID: 2118104].
[28]
Xu, J.; Li, Q. Review of the in vivo functions of the p160 steroid receptor coactivator family. Mol. Endocrinol., 2003, 17(9), 1681-1692. [http://dx.doi.org/10.1210/me.2003-0116]. [PMID: 12805412].
[29]
Göttlicher, M.; Heck, S.; Herrlich, P. Transcriptional cross-talk, the second mode of steroid hormone receptor action. J. Mol. Med. (Berl.), 1998, 76(7), 480-489. [http://dx.doi.org/10.1007/s001090050242]. [PMID: 9660166].
[30]
Nawaz, Z.; Lonard, D.M.; Dennis, A.P.; Smith, C.L.; O’Malley, B.W. Proteasome-dependent degradation of the human estrogen receptor. Proc. Natl. Acad. Sci. USA, 1999, 96(5), 1858-1862. [http:// dx.doi.org/10.1073/pnas.96.5.1858]. [PMID: 10051559].
[31]
Migliaccio, A.; Piccolo, D.; Castoria, G.; Di Domenico, M.; Bilancio, A.; Lombardi, M.; Gong, W.; Beato, M.; Auricchio, F. Activation of the Src/p21ras/Erk pathway by progesterone receptor via cross-talk with estrogen receptor. EMBO J., 1998, 17(7), 2008-2018. [http://dx.doi.org/10.1093/emboj/17.7.2008]. [PMID: 9524123].
[32]
Boonyaratanakornkit, V.; Edwards, D.P. Receptor mechanisms mediating non-genomic actions of sex steroids. Semin. Reprod. Med., 2007, 25(3), 139-153. [http://dx.doi.org/10.1055/s-2007-973427]. [PMID: 17447204].
[33]
Heldring, N.; Pike, A.; Andersson, S.; Matthews, J.; Cheng, G.; Hartman, J.; Tujague, M.; Ström, A.; Treuter, E.; Warner, M.; Gustafsson, J.A. Estrogen receptors: how do they signal and what are their targets. Physiol. Rev., 2007, 87(3), 905-931. [http://dx.doi. org/10.1152/physrev.00026.2006]. [PMID: 17615392].
[34]
Lu, C.L.; Herndon, C. New roles for neuronal estrogen receptors. Neurogastroenterol. Motil., 2017, 29(7), 1-7. [http://dx.doi.org/ 10.1111/nmo.13121]. [PMID: 28597596].
[35]
Vrtačnik, P.; Ostanek, B.; Mencej-Bedrač, S.; Marc, J. The many faces of estrogen signaling. Biochem. Med. (Zagreb), 2014, 24(3), 329-342. [http://dx.doi.org/10.11613/BM.2014.035]. [PMID: 25351351].
[36]
Hayward, C.; Sanborn, K. Puberty and the emergence of gender differences in psychopathology. J. Adolesc. Health, 2002, 30(4)(Suppl.), 49-58. [http://dx.doi.org/10.1016/S1054-139X(02)00336-1]. [PMID: 11943575].
[37]
Kessler, R.C.; Walters, E.E. Epidemiology of DSM-III-R major depression and minor depression among adolescents and young adults in the National Comorbidity Survey. Depress. Anxiety, 1998, 7(1), 3-14. [http://dx.doi.org/10.1002/(SICI)1520-6394(1998)7:1 <3:AID-DA2>3.0.CO;2-F]. [PMID: 9592628].
[38]
Walf, A.A.; Frye, C.A. A review and update of mechanisms of estrogen in the hippocampus and amygdala for anxiety and depression behavior. Neuropsychopharmacology, 2006, 31(6), 1097-1111. [http://dx.doi.org/10.1038/sj.npp.1301067]. [PMID: 16554740].
[39]
Borrow, A.P.; Cameron, N.M. Estrogenic mediation of serotonergic and neurotrophic systems: implications for female mood disorders. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2014, 54, 13-25. [http://dx.doi.org/10.1016/j.pnpbp.2014.05.009]. [PMID: 24865152].
[40]
Holsen, L.M.; Ph, D.; Spaeth, S.B.; Lee, J.; Ogden, L. a; Klibanski, A.; Whitfield-gabrieli, S.; Goldstein, J.M. Stress Response Circuitry Hypoactivation Related to Hormonal Dysfunction in Women with Major Depression. J. Affect. Disord., 2011, 131, 379-387.
[41]
Bloch, M.; Schmidt, P.J.; Danaceau, M.; Murphy, J.; Nieman, L.; Rubinow, D.R. Effects of gonadal steroids in women with a history of postpartum depression. Am. J. Psychiatry, 2000, 157(6), 924-930. [http://dx.doi.org/10.1176/appi.ajp.157.6.924]. [PMID: 10831472].
[42]
Young, E.A.; Midgley, A.R.; Carlson, N.E.; Brown, M.B. Alteration in the hypothalamic-pituitary-ovarian axis in depressed women. Arch. Gen. Psychiatry, 2000, 57(12), 1157-1162. [http://dx.doi.org/ 10.1001/archpsyc.57.12.1157]. [PMID: 11115329].
[43]
Cohen, L.S.; Soares, C.N.; Poitras, J.R.; Prouty, J.; Alexander, A.B.; Shifren, J.L. Short-term use of estradiol for depression in perimenopausal and postmenopausal women: a preliminary report. Am. J. Psychiatry, 2003, 160(8), 1519-1522. [http://dx.doi.org/10. 1176/appi.ajp.160.8.1519]. [PMID: 12900318].
[44]
Soares, C.N.; Almeida, O.P.; Joffe, H.; Cohen, L.S.S.; de Novaes Soares, C.; Almedia, O.; Joff, H.; Cohen, L.S.S. Efficacy of estradiol for the treatment of depressive disorders in perimenopausal women: a double-blind, randomized, placebo-controlled trial. Arch. Gen. Psychiatry, 2001, 58(6), 529-534. [http://dx.doi.org/10.1001/ archpsyc.58.6.529]. [PMID: 11386980].
[45]
Fischer, B.; Gleason, C.; Asthana, S. Effects of hormone therapy on cognition and mood. Fertil. Steril., 2014, 101(4), 898-904. [http:// dx.doi.org/10.1016/j.fertnstert.2014.02.025]. [PMID: 24680649].
[46]
Bastos, C.P.; Pereira, L.M.; Ferreira-Vieira, T.H.; Drumond, L.E.; Massensini, A.R.; Moraes, M.F.D.; Pereira, G.S. Object recognition memory deficit and depressive-like behavior caused by chronic ovariectomy can be transitorialy recovered by the acute activation of hippocampal estrogen receptors. Psychoneuroendocrinology, 2015, 57, 14-25. [http://dx.doi.org/10.1016/j.psyneuen.2015.03.020]. [PMID: 25867995].
[47]
Zweifel, J.E.; O’Brien, W.H. A meta-analysis of the effect of hormone replacement therapy upon depressed mood. Psychoneuroendocrinology, 1997, 22(3), 189-212. [http://dx.doi.org/10.1016/S0306-4530(96)00034-0]. [PMID: 9203229].
[48]
Rubinow, D.R.; Johnson, S.L.; Schmidt, P.J.; Girdler, S.; Gaynes, B. Efficacy of Estradiol in Perimenopausal Depression: So Much Promise and so Few Answers. Depress. Anxiety, 2015, 32(8), 539-549. [http://dx.doi.org/10.1002/da.22391]. [PMID: 26130315].
[49]
Carranza-Lira, S.; MacGregor-Gooch, A.L.; Saráchaga-Osterwalder, M. Mood modifications with raloxifene and continuous combined estrogen plus progestin hormone therapy. Int. J. Fertil. Womens Med., 2004, 49(3), 120-122. [PMID: 15303313].
[50]
Lemini, C.; García-Albor, E.; Cruz-López, B.; Matamoros-Trejo, G.; Martínez-Mota, L. Differential effect of the 17β-aminoestrogens prolame, butolame and pentolame in anxiety and depression models in rats. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2016, 64, 102-108. [http://dx.doi.org/10.1016/j.pnpbp.2015.07.013]. [PMID: 26239795].
[51]
Westlund Tam, L.; Parry, B.L. Does estrogen enhance the antidepressant effects of fluoxetine? J. Affect. Disord., 2003, 77(1), 87-92. [http://dx.doi.org/10.1016/S0165-0327(02)00357-9]. [PMID: 14550939].
[52]
Owens, M.J.; Nemeroff, C.B. Role of serotonin in the pathophysiology of depression: focus on the serotonin transporter. Clin. Chem., 1994, 40(2), 288-295. [PMID: 7508830].
[53]
Köhler, S.; Cierpinsky, K.; Kronenberg, G.; Adli, M. The serotonergic system in the neurobiology of depression: Relevance for novel antidepressants. J. Psychopharmacol. (Oxford), 2016, 30(1), 13-22. [http://dx.doi.org/10.1177/0269881115609072]. [PMID: 26464458].
[54]
Lasiuk, G.C.; Hegadoren, K.M. The effects of estradiol on central serotonergic systems and its relationship to mood in women. Biol. Res. Nurs., 2007, 9(2), 147-160. [http://dx.doi.org/10.1177/ 1099800407305600]. [PMID: 17909167].
[55]
Akiskal, H.S.; McKinney, W.T. Jr depressive disorders: Toward a unified hypothesis Science, (80). 1973, 182 20-29
[56]
Leyton, M.; Young, S.N.; Benkelfat, C. Relapse of depression after rapid depletion of tryptophan. Lancet, 1997, 349(9068), 1840-1841. [http://dx.doi.org/10.1016/S0140-6736(05)61726-6]. [PMID: 9269238].
[57]
Smith, K.A.; Clifford, E.M.; Hockney, R.A.; Clark, D.M.; Cowen, P.J. Effect of tryptophan depletion on mood in male and female volunteers: A pilot study. Psychopharmacology (Berl.), 1997, 12, 111-117.
[58]
Savitz, J.; Lucki, I.; Drevets, W.C.W. 5-HT(1A) receptor function in major depressive disorder. Prog. Neurobiol., 2009, 88(1), 17-31. [http://dx.doi.org/10.1016/j.pneurobio.2009.01.009]. [PMID: 19428959].
[59]
Drevets, W.C.; Frank, E.; Price, J.C.; Kupfer, D.J.; Holt, D.; Greer, P.J.; Huang, Y.; Gautier, C.; Mathis, C. PET imaging of serotonin 1A receptor binding in depression. Biol. Psychiatry, 1999, 46(10), 1375-1387. [http://dx.doi.org/10.1016/S0006-3223(99)00189-4]. [PMID: 10578452].
[60]
Meltzer, C.C.; Price, J.C.; Mathis, C.A.; Butters, M.A.; Ziolko, S.K.; Moses-Kolko, E.; Mazumdar, S.; Mulsant, B.H.; Houck, P.R.; Lopresti, B.J.; Weissfeld, L.A.; Reynolds, C.F. Serotonin 1A receptor binding and treatment response in late-life depression. Neuropsychopharmacology, 2004, 29(12), 2258-2265. [http://dx.doi.org/ 10.1038/sj.npp.1300556]. [PMID: 15483563].
[61]
Nugent, A.C.; Bain, E.E.; Carlson, P.J.; Neumeister, A.; Bonne, O.; Carson, R.E.; Eckelman, W.; Herscovitch, P.; Zarate, C.A., Jr; Charney, D.S.; Drevets, W.C. Reduced post-synaptic serotonin type 1A receptor binding in bipolar depression. Eur. Neuropsychopharmacol., 2013, 23(8), 822-829. [http://dx.doi.org/10.1016/ j.euroneuro.2012.11.005]. [PMID: 23434290].
[62]
López, J.F.; Chalmers, D.T.; Little, K.Y.; Watson, S.J.A.E. Bennett Research Award. Regulation of serotonin1A, glucocorticoid, and mineralocorticoid receptor in rat and human hippocampus: implications for the neurobiology of depression. Biol. Psychiatry, 1998, 43(8), 547-573. [http://dx.doi.org/10.1016/S0006-3223(97) 00484-8]. [PMID: 9564441].
[63]
Parsey, R.V.; Olvet, D.M.; Oquendo, M.A.; Huang, Y-Y.; Ogden, R.T.; Mann, J.J. Higher 5-HT1A receptor binding potential during a major depressive episode predicts poor treatment response: preliminary data from a naturalistic study. Neuropsychopharmacology, 2006, 31(8), 1745-1749. [http://dx.doi.org/10.1038/sj.npp.1300992]. [PMID: 16395308].
[64]
Staley, J.K.; Sanacora, G.; Tamagnan, G.; Maciejewski, P.K.; Malison, R.T.; Berman, R.M.; Vythilingam, M.; Kugaya, A.; Baldwin, R.M.; Seibyl, J.P.; Charney, D.; Innis, R.B. Sex differences in diencephalon serotonin transporter availability in major depression. Biol. Psychiatry, 2006, 59(1), 40-47. [http://dx.doi. org/10.1016/j.biopsych.2005.06.012]. [PMID: 16139815].
[65]
Paech, K.; Webb, P.; Kuiper, G.G.; Nilsson, S.; Gustafsson, J.; Kushner, P.J.; Scanlan, T.S. Differential Ligand Activation of Estrogen Receptors ERalpha and ERbeta at AP1 Sites Science, 1997, 277 1508-1510
[66]
Alves, S.E.; Weiland, N.G.; Hayashi, S.; McEwen, B.S. Immunocytochemical localization of nuclear estrogen receptors and progestin receptors within the rat dorsal raphe nucleus. J. Comp. Neurol., 1998, 391(3), 322-334. [http://dx.doi.org/10.1002/(SICI)1096-9861 (19980216)391:3<322:AID-CNE3>3.0.CO;2-3]. [PMID: 9492203].
[67]
Sheng, Z.; Kawano, J.; Yanai, A.; Fujinaga, R.; Tanaka, M.; Watanabe, Y.; Shinoda, K. Expression of estrogen receptors (A, β) and androgen receptor in serotonin neurons of the rat and mouse dorsal raphe nuclei. sex and species differences. Neurosci. Res., 2004, 49, 185-196. [PMID: 15140561].
[68]
Gundlah, C.; Lu, N.Z.; Bethea, C.L. Ovarian steroid regulation of monoamine oxidase-A and -B mRNAs in the macaque dorsal raphe and hypothalamic nuclei. Psychopharmacology (Berl.), 2002, 160(3), 271-282. [http://dx.doi.org/10.1007/s00213-001-0959-0]. [PMID: 11889496].
[69]
Osterlund, M.K.; Hurd, Y.L. Acute 17 beta-estradiol treatment down-regulates serotonin 5HT1A receptor mRNA expression in the limbic system of female rats. Brain Res. Mol. Brain Res., 1998, 55(1), 169-172. [http://dx.doi.org/10.1016/S0169-328X(98)00018-7]. [PMID: 9645972].
[70]
McQueen, J.K.; Wilson, H.; Fink, G. Estradiol-17 beta increases serotonin transporter (SERT) mRNA levels and the density of SERT-binding sites in female rat brain. Brain Res. Mol. Brain Res., 1997, 45(1), 13-23. [http://dx.doi.org/10.1016/S0169-328X(96) 00233-1]. [PMID: 9105666].
[71]
Soares, C.N. Depression in peri- and postmenopausal women: prevalence, pathophysiology and pharmacological management. Drugs Aging, 2013, 30(9), 677-685. [http://dx.doi.org/10.1007/ s40266-013-0100-1]. [PMID: 23801148].
[72]
Schiller, C.E.; Schmidt, P.J.; Rubinow, D.R. Allopregnanolone as a mediator of affective switching in reproductive mood disorders. Psychopharmacology (Berl.), 2014, 231(17), 3557-3567. [http://dx. doi.org/10.1007/s00213-014-3599-x]. [PMID: 24846476].
[73]
Serova, L.; Nakashima, A.; Sabban, L. Estradiol stimulates gene expression of norepinephrine biosynthetic enzymes in rat locus coeruleus. Neuroendocrinology, 2002, 10595, 193-200.
[74]
Maharjan, S.; Serova, L.; Sabban, E.L. Transcriptional regulation of tyrosine hydroxylase by estrogen: opposite effects with estrogen receptors α and β and interactions with cyclic AMP. J. Neurochem., 2005, 93(6), 1502-1514. [http://dx.doi.org/10.1111/j.1471-4159. 2005.03142.x]. [PMID: 15935066].
[75]
Pau, K.Y.; Hess, D.L.; Kohama, S.; Bao, J.; Pau, C.Y.; Spies, H.G. Oestrogen upregulates noradrenaline release in the mediobasal hypothalamus and tyrosine hydroxylase gene expression in the brainstem of ovariectomized rhesus macaques. J. Neuroendocrinol., 2000, 12(9), 899-909. [http://dx.doi.org/10.1046/j.1365-2826.2000. 00549.x]. [PMID: 10971815].
[76]
Jiang, H.; Xie, T.; Ramsden, D.B.; Ho, S.L. Human catechol-O-methyltransferase down-regulation by estradiol. Neuropharmacology, 2003, 45(7), 1011-1018. [http://dx.doi.org/10.1016/S0028-3908 (03)00286-7]. [PMID: 14573393].
[77]
Bangasser, D.A.; Wiersielis, K.R.; Khantsis, S. Sex differences in the locus coeruleus-norepinephrine system and its regulation by stress. Brain Res, 2016, 1641 (Pt B), 177-188. [http://dx.doi.org/10. 1016/j.brainres.2015.11.021] [PMID: 26607253]
[78]
Xie, T.; Ho, S-L.; Ramsden, D. Characterization and implications of estrogenic down-regulation of human catechol-O-methyltransferase gene transcription. Mol. Pharmacol., 1999, 56(1), 31-38. [http:// dx.doi.org/10.1124/mol.56.1.31]. [PMID: 10385681].
[79]
Grahame-Smith, D.G. Tryptophan hydroxylation in brain. Biochem. Biophys. Res. Commun., 1964, 16(6), 586-592. [http://dx.doi. org/10.1016/0006-291X(64)90197-4]. [PMID: 5297063].
[80]
Walther, D.J.; Peter, J.U.; Bashammakh, S.; Hörtnagl, H.; Voits, M.; Fink, H.; Bader, M. Synthesis of Serotonin by a Second Tryptophan Hydroxylase Isoform. Science, 2003, 299, 76. [http://dx.doi.org/10.1126/science.1078197].
[81]
Zhang, X.; Gainetdinov, R.R.; Beaulieu, J.M.; Sotnikova, T.D.; Burch, L.H.; Williams, R.B.; Schwartz, D.A.; Krishnan, K.R.R.; Caron, M.G. Loss-of-function mutation in tryptophan hydroxylase-2 identified in unipolar major depression. Neuron, 2005, 45(1), 11-16. [http://dx.doi.org/10.1016/j.neuron.2004.12.014]. [PMID: 15629698].
[82]
Haghighi, F.; Bach-Mizrachi, H.; Huang, Y.Y.; Arango, V.; Shi, S.; Dwork, A.J.; Rosoklija, G.; Sheng, H.T.; Morozova, I.; Ju, J.; Russo, J.J.; Mann, J.J. Genetic architecture of the human tryptophan hydroxylase 2 Gene: existence of neural isoforms and relevance for major depression. Mol. Psychiatry, 2008, 13(8), 813-820. [http://dx.doi.org/10.1038/sj.mp.4002127]. [PMID: 18180764].
[83]
Bach-Mizrachi, H.; Underwood, M.D.; Tin, A.; Ellis, S.P.; Mann, J.J.; Arango, V. Elevated expression of tryptophan hydroxylase-2 mRNA at the neuronal level in the dorsal and median raphe nuclei of depressed suicides. Mol. Psychiatry, 2008, 13 507-513, 465.[http://dx.doi.org/10.1038/sj.mp.4002143]
[84]
Boldrini, M.; Underwood, M.D.; Mann, J.J.; Arango, V. More tryptophan hydroxylase in the brainstem dorsal raphe nucleus in depressed suicides. Brain Res., 2005, 1041(1), 19-28. [http://dx. doi.org/10.1016/j.brainres.2005.01.083]. [PMID: 15804496].
[85]
Bonkale, W.L.; Murdock, S.; Janosky, J.E.; Austin, M.C. Normal levels of tryptophan hydroxylase immunoreactivity in the dorsal raphe of depressed suicide victims. J. Neurochem., 2004, 88(4), 958-964. [http://dx.doi.org/10.1046/j.1471-4159.2003.02225.x]. [PMID: 14756817].
[86]
Bethea, C.L.; Mirkes, S.J.; Shively, C.A.; Adams, M.R. Steroid regulation of tryptophan hydroxylase protein in the dorsal raphe of macaques. Biol. Psychiatry, 2000, 47(6), 562-576. [http://dx.doi. org/10.1016/S0006-3223(99)00156-0]. [PMID: 10715363].
[87]
Nomura, M.; Akama, K.T.; Alves, S.E.; Korach, K.S.; Gustafsson, J.Å.; Pfaff, D.W.; Ogawa, S. Differential distribution of estrogen receptor (ER)-α and ER-β in the midbrain raphe nuclei and periaqueductal gray in male mouse: Predominant role of ER-β in midbrain serotonergic systems. Neuroscience, 2005, 130(2), 445-456. [http://dx.doi.org/10.1016/j.neuroscience.2004.09.028]. [PMID: 15664701].
[88]
Gundlah, C.; Lu, N.Z.; Bethea, C.L. Ovarian steroid regulation of monoamine oxidase-A and -B mRNAs in the macaque dorsal raphe and hypothalamic nuclei. Psychopharmacology (Berl.), 2002, 160(3), 271-282. [http://dx.doi.org/10.1007/s00213-001-0959-0]. [PMID: 11889496].
[89]
Lu, H.; Ozawa, H.; Nishi, M.; Ito, T.; Kawata, M. Serotonergic neurones in the dorsal raphe nucleus that project into the medial preoptic area contain oestrogen receptor beta. J. Neuroendocrinol., 2001, 13(10), 839-845. [http://dx.doi.org/10.1046/j.1365-2826. 2001.00695.x]. [PMID: 11679052].
[90]
Donner, N.C.; Handa, R.J. Estrogen receptor beta regulates the expression of tryptophan- hydroxylase 2 mRNA within serotonergic neurons of the rat dorsal raphe nuclei. 2009, 163 705-718
[91]
Borsini, F.; Meli, A. Is the forced swimming test a suitable model for revealing antidepressant activity? Psychopharmacology (Berl.), 1988, 94(2), 147-160. [http://dx.doi.org/10.1007/BF00176837]. [PMID: 3127840].
[92]
Paul, I.A.; Duncan, G.E.; Kuhn, C.; Mueller, R.A.; Hong, J.S.; Breese, G.R. Neural adaptation in imipramine-treated rats processed in forced swim test: assessment of time course, handling, rat strain and amine uptake. J. Pharmacol. Exp. Ther., 1990, 252(3), 997-1005. [PMID: 2157002].
[93]
Porsolt, R.D.; Anton, G.; Blavet, N.; Jalfre, M. Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur. J. Pharmacol., 1978, 47(4), 379-391. [http://dx.doi.org/10.1016/0014-2999(78)90118-8]. [PMID: 204499].
[94]
Detke, M.J.; Rickels, M.; Lucki, I. Active behaviors in the rat forced swimming test differentially produced by serotonergic and noradrenergic antidepressants. Psychopharmacology (Berl.), 1995, 121(1), 66-72. [http://dx.doi.org/10.1007/BF02245592]. [PMID: 8539342].
[95]
Contreras, C.M.; Martınez-Mota, L. Desipramine Restricts Estrous Cycle Oscillations, M.S. in Swimming. Prog. Neuropsychopharmacol. Biol. Psychiatry, 1998, 22, 1121-1128.
[96]
Yang, F-Z.; Wu, Y.; Zhang, W-G.; Cai, Y-Y.; Shi, S-X. Estradiol or fluoxetine alters depressive behavior and tryptophan hydroxylase in rat raphe. Neuroreport, 2010, 21(4), 309-312. [http://dx. doi.org/10.1097/WNR.0b013e3283377445]. [PMID: 20134355].
[97]
Benmansour, S.; Weaver, R.S.; Barton, A.K.; Adeniji, O.S.; Frazer, A. Comparison of effects of E2 and progesterone on serotonergic function. Biol. Psychiatry, 2012, 71, 633-641. [PMID: 22225849].
[98]
Koldzic-Zivanovic, N.; Seitz, P.K.; Watson, C.S.; Cunningham, K.A.; Thomas, M.L. Intracellular signaling involved in estrogen regulation of serotonin reuptake. Mol. Cell. Endocrinol., 2004, 226(1-2), 33-42. [http://dx.doi.org/10.1016/j.mce.2004.07.017]. [PMID: 15489003].
[99]
Chen, G.L.; Miller, G.M. 5′-Untranslated region of the tryptophan hydroxylase-2 gene harbors an asymmetric bidirectional promoter but not internal ribosome entry site in vitro. Gene, 2009, 435(1-2), 53-62. [http://dx.doi.org/10.1016/j.gene.2008.12.019]. [PMID: 19344641].
[100]
Machado-Vieira, R.; Mallinger, A.G. Abnormal function of monoamine oxidase-A in comorbid major depressive disorder and cardiovascular disease: pathophysiological and therapeutic implications.(review) Mol. Med. Rep., 2012, 6(5), 915-922. [PMID: 22948532].
[101]
Bach, A.W.; Lan, N.C.; Johnson, D.L.; Abell, C.W.; Bembenek, M.E.; Kwan, S.W.; Seeburg, P.H.; Shih, J.C. cDNA cloning of human liver monoamine oxidase A and B: molecular basis of differences in enzymatic properties. Proc. Natl. Acad. Sci. USA, 1988, 85(13), 4934-4938. [http://dx.doi.org/10.1073/pnas.85.13.4934]. [PMID: 3387449].
[102]
Youdim, M.B.; Finberg, J.P. New directions in monoamine oxidase A and B selective inhibitors and substrates. Biochem. Pharmacol., 1991, 41(2), 155-162. [http://dx.doi.org/10.1016/0006-2952(91) 90471-G]. [PMID: 1989626].
[103]
Luque, J.M.; Bleuel, Z.; Hendrickson, A.; Richards, J.G. Detection of MAO-A and MAO-B mRNAs in monkey brainstem by cross-hybridization with human oligonucleotide probes. Brain Res. Mol. Brain Res., 1996, 36(2), 357-360. [http://dx.doi.org/10.1016/0169-328X(96)88407-5]. [PMID: 8965658].
[104]
Shulman, K.I.; Herrmann, N.; Walker, S.E. Current place of monoamine oxidase inhibitors in the treatment of depression. CNS Drugs, 2013, 27(10), 789-797. [http://dx.doi.org/10.1007/s40263-013-0097-3]. [PMID: 23934742].
[105]
Duncan, J.; Johnson, S.; Ou, X.M. Monoamine oxidases in major depressive disorder and alcoholism. Drug Discov. Ther., 2012, 6(3), 112-122. [PMID: 22890201].
[106]
Meyer, J.H.; Ginovart, N.; Boovariwala, A.; Sagrati, S.; Hussey, D.; Garcia, A.; Young, T.; Praschak-Rieder, N.; Wilson, A.A.; Houle, S. Elevated monoamine oxidase a levels in the brain. Arch. Gen. Psychiatry, 2006, 63, 1209. [http://dx.doi.org/10.1001/ archpsyc.63.11.1209]. [PMID: 17088501].
[107]
Rekkas, P.V.; Wilson, A.A.; Lee, V.W.H.; Yogalingam, P.; Sacher, J.; Rusjan, P.; Houle, S.; Stewart, D.E.; Kolla, N.J.; Kish, S.; Chiuccariello, L.; Meyer, J.H. Greater monoamine oxidase a binding in perimenopausal age as measured with carbon 11-labeled harmine positron emission tomography. JAMA Psychiatry, 2014, 71(8), 873-879. [http://dx.doi.org/10.1001/jamapsychiatry.2014.250]. [PMID: 24898155].
[108]
Chiuccariello, L.; Houle, S.; Miler, L.; Cooke, R.G.; Rusjan, P.M.; Rajkowska, G.; Levitan, R.D.; Kish, S.J.; Kolla, N.J.; Ou, X.; Wilson, A.A.; Meyer, J.H. Elevated monoamine oxidase a binding during major depressive episodes is associated with greater severity and reversed neurovegetative symptoms. Neuropsychopharmacology, 2014, 39(4), 973-980. [http://dx.doi.org/10.1038/npp.2013.297]. [PMID: 24154665].
[109]
Klimek, V.; Roberson, G.; Stockmeier, C.A.; Ordway, G.A. Serotonin transporter and MAO-B levels in monoamine nuclei of the human brainstem are normal in major depression. J. Psychiatr. Res., 2003, 37(5), 387-397. [http://dx.doi.org/10.1016/S0022-3956 (03)00045-1]. [PMID: 12849931].
[110]
Smith, L.J.; Henderson, J.A.; Abell, C.W.; Bethea, C.L. Effects of ovarian steroids and raloxifene on proteins that synthesize, transport, and degrade serotonin in the raphe region of macaques. Neuropsychopharmacology, 2004, 29(11), 2035-2045. [http://dx.doi. org/10.1038/sj.npp.1300510]. [PMID: 15199371].
[111]
Ortega-Corona, B.G.; Valencia-Sánchez, A.; Kubli-Garfias, C.; Anton-Tay, F.; Salazar, L.A.; Villarreal, J.E.; Ponce-Monter, H. Hypothalamic monoamine oxidase activity in ovariectomized rats after sexual behavior restoration. Arch. Med. Res., 1994, 25(3), 337-340. [PMID: 7803985].
[112]
Chevillard, C.; Barden, N.; Saavedra, J.M. Estradiol treatment decreases type A and increases type B monoamine oxidase in specific brain stem areas and cerebellum of ovariectomized rats. Brain Res., 1981, 222(1), 177-181. [http://dx.doi.org/10.1016/0006-8993 (81)90955-0]. [PMID: 7296265].
[113]
Bethea, C.L.; Lu, N.Z.; Gundlah, C.; Streicher, J.M. Diverse actions of ovarian steroids in the serotonin neural system. Front. Neuroendocrinol., 2002, 23(1), 41-100. [http://dx.doi.org/10.1006/ frne.2001.0225]. [PMID: 11906203].
[114]
Olivier, B. Serotonin: a never-ending story. Eur. J. Pharmacol., 2015, 753, 2-18. [http://dx.doi.org/10.1016/j.ejphar.2014.10.031]. [PMID: 25446560].
[115]
Haase, J. Killian, a; Magnani, F.; Williams, C. SERT is regulated by syntaxin I A one potential regulatory protein is the neuronal. Biochem. Soc. Trans., 2001, 29, 722-728. [http://dx.doi.org/10. 1042/bst0290722]. [PMID: 11709063].
[116]
White, K.J.; Walline, C.C.; Barker, E.L. Serotonin transporters: implications for antidepressant drug development. AAPS J., 2005, 7(2), E421-E433. [http://dx.doi.org/10.1208/aapsj070242]. [PMID: 16353921].
[117]
Gryglewski, G.; Lanzenberger, R.; Kranz, G.S.; Cumming, P. Meta-analysis of molecular imaging of serotonin transporters in major depression. J. Cereb. Blood Flow Metab., 2014, 34(7), 1096-1103. [http://dx.doi.org/10.1038/jcbfm.2014.82]. [PMID: 24802331].
[118]
Pecins-Thompson, M.; Bethea, C.L. Ovarian steroid regulation of serotonin-1A autoreceptor messenger RNA expression in the dorsal raphe of rhesus macaques. Neuroscience, 1999, 89(1), 267-277. [http:// dx.doi.org/10.1016/S0306-4522(98)00326-1]. [PMID: 10051234].
[119]
Zhou, W.; Koldzic-Zivanovic, N.; Clarke, C.H.; de Beun, R.; Wassermann, K.; Bury, P.S.; Cunningham, K.A.; Thomas, M.L. Selective estrogen receptor modulator effects in the rat brain. Neuroendocrinology, 2002, 75(1), 24-33. [http://dx.doi.org/10.1159/ 000048218]. [PMID: 11810032].
[120]
Lu, N.Z.; Eshleman, A.J.; Janowsky, A.; Bethea, C.L. Ovarian steroid regulation of serotonin reuptake transporter (SERT) binding, distribution, and function in female macaques. Mol. Psychiatry, 2003, 8(3), 353-360. [http://dx.doi.org/10.1038/sj.mp.4001243]. [PMID: 12660809].
[121]
Sumner, B.E.; Grant, K.E.; Rosie, R.; Hegele-Hartung, C.; Fritzemeier, K-H.; Fink, G. Effects of tamoxifen on serotonin transporter and 5-hydroxytryptamine(2A) receptor binding sites and mRNA levels in the brain of ovariectomized rats with or without acute estradiol replacement. Brain Res. Mol. Brain Res., 1999, 73(1-2), 119-128. [http://dx.doi.org/10.1016/S0169-328X(99)00243-0]. [PMID: 10581405].
[122]
Rivera, H.M.; Oberbeck, D.R.; Kwon, B.; Houpt, T.A.; Eckel, L.A. Estradiol increases Pet-1 and serotonin transporter mRNA in the midbrain raphe nuclei of ovariectomized rats. Brain Res., 2009, 1259, 51-58. [http://dx.doi.org/10.1016/j.brainres.2008.12.067]. [PMID: 19168037].
[123]
Shively, C.A.; Mirkes, S.J.; Lu, N.Z.; Henderson, J.A.; Bethea, C.L. Soy and social stress affect serotonin neurotransmission in primates. Pharmacogenomics J., 2003, 3(2), 114-121. [http://dx. doi.org/10.1038/sj.tpj.6500166]. [PMID: 12746737].
[124]
Jovanovic, H.; Karlsson, P.; Cerin, A.; Halldin, C.; Nordström, A.L. 5-HT(1A) receptor and 5-HTT binding during the menstrual cycle in healthy women examined with [(11)C] WAY100635 and [(11)C] MADAM PET. Psychiatry Res., 2009, 172(1), 31-37. [http://dx.doi.org/10.1016/j.pscychresns.2008.07.002]. [PMID: 19118985].
[125]
Mitra, C.; Guha, S.R. Serotonin oxidation by type B MAO of rat brain. Biochem. Pharmacol., 1980, 29(9), 1213-1216. [http://dx. doi.org/10.1016/0006-2952(80)90276-2]. [PMID: 6772194].
[126]
Jabeen, H.D. Raphe-hippocampal serotonin neurotransmission in the sex related differences of adaptation to stress: Focus on serotonin-1A receptor. Curr. Neuropharmacol., 2011, 9(3), 512-521. [http://dx.doi.org/10.2174/157015911796558019]. [PMID: 22379463].
[127]
Sharp, T.; Boothman, L.; Raley, J.; Quérée, P. Important messages in the ‘post’: recent discoveries in 5-HT neurone feedback control. Trends Pharmacol. Sci., 2007, 28(12), 629-636. [http://dx.doi. org/10.1016/j.tips.2007.10.009]. [PMID: 17996955].
[128]
Invernizzi, R.; Carli, M.; Di Clemente, A.; Samanin, R. Administration of 8-hydroxy-2-(Di-n-propylamino)tetralin in raphe nuclei dorsalis and medianus reduces serotonin synthesis in the rat brain: differences in potency and regional sensitivity. J. Neurochem., 1991, 56(1), 243-247. [http://dx.doi.org/10.1111/j.1471-4159.1991. tb02587.x]. [PMID: 1824782].
[129]
Blier, P.; Ward, N.M. Is there a role for 5-HT1A agonists in the treatment of depression? Biol. Psychiatry, 2003, 53(3), 193-203. [http://dx.doi.org/10.1016/S0006-3223(02)01643-8]. [PMID: 12559651].
[130]
Bhagwagar, Z.; Rabiner, E.A.; Sargent, P.A.; Grasby, P.M.; Cowen, P.J. Persistent reduction in brain serotonin1A receptor binding in recovered depressed men measured by positron emission tomography with [11C]WAY-100635. Mol. Psychiatry, 2004, 9(4), 386-392. [http://dx.doi.org/10.1038/sj.mp.4001401]. [PMID: 15042104].
[131]
Albert, P.R.; Le François, B.; Millar, A.M. Transcriptional dysregulation of 5-HT1A autoreceptors in mental illness. Mol. Brain, 2011, 4, 21. [http://dx.doi.org/10.1186/1756-6606-4-21]. [PMID: 21619616].
[132]
Sargent, P. a; Kjaer, K.H.; Bench, C.J.; Rabiner, E. a; Messa, C.; Meyer, J.; Gunn, R.N.; Grasby, P.M.; Cowen, P.J. Brain serotonin 1A receptor binding measured by positron emission tomography with [11C]WAY-100635. Effects of depression and antidepressant treatment. Arch. Gen. Psychiatry, 2000, 57, 174-180.
[133]
Savitz, J.B.; Drevets, W.C. Neuroreceptor imaging in depression. Neurobiol. Dis., 2013, 52, 49-65. [http://dx.doi.org/10.1016/ j.nbd.2012.06.001]. [PMID: 22691454].
[134]
Richardson-Jones, J.W.; Craige, C.P.; Guiard, B.P.; Stephen, A.; Metzger, K.L.; Kung, H.F.; Gardier, A.M.; Dranovsky, A.; David, D.J.; Beck, S.G.; Hen, R.; Leonardo, E.D. 5-HT1A autoreceptor levels determine vulnerability to stress and response to antidepressants. Neuron, 2010, 65(1), 40-52. [http://dx.doi.org/10.1016/ j.neuron.2009.12.003]. [PMID: 20152112].
[135]
Chalmers, D.T.; Watson, S.J. Comparative anatomical distribution of 5-HT1A receptor mRNA and 5-HT1A binding in rat brain--a combined in situ hybridisation/in vitro receptor autoradiographic study. Brain Res., 1991, 561(1), 51-60. [http://dx.doi.org/10. 1016/0006-8993(91)90748-K]. [PMID: 1797349].
[136]
Landry, M.; Di Paolo, T. Effect of chronic estradiol, tamoxifen or raloxifene treatment on serotonin 5-HT1A receptor. Brain Res. Mol. Brain Res., 2003, 112(1-2), 82-89. [http://dx.doi.org/10. 1016/S0169-328X(03)00049-4]. [PMID: 12670705].
[137]
Gundlah, C.; Lu, N.Z.; Mirkes, S.J.; Bethea, C.L. Estrogen receptor beta (ERbeta) mRNA and protein in serotonin neurons of macaques. Brain Res. Mol. Brain Res., 2001, 91(1-2), 14-22. [http:// dx.doi.org/10.1016/S0169-328X(01)00108-5]. [PMID: 11457488].

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