Effects of estrogen and testosterone treatment on serotonin transporter binding in the brain of surgically postmenopausal women - a PET study

NeuroImage

Volumn 106, Issue , 2015, Pages 47-54

  Jovanovic, Hristina ^a   Kocoska Maras, Ljiljana ^a   Rådestad, Angelique Flöter ^a   Halldin, Christer ^a   Borg, Jacqueline ^a   Hirschberg, Angelica Lindén ^a   Nordström, Anna Lena ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Depression; Estrogen treatment; PET; Postmenopausal; Serotonin; Testosterone treatment

Indexed keywords

CARBON 11; ESTRADIOL; RADIOLIGAND; SEROTONIN TRANSPORTER; TESTOSTERONE UNDECANOATE; BENZYLAMINE DERIVATIVE; ESTROGEN; N,N-DIMETHYL-2-(2-AMINO-4-METHYLPHENYLTHIO)BENZYLAMINE; PROTEIN BINDING; RADIOPHARMACEUTICAL AGENT; TESTOSTERONE;

ADULT; AGED; ARTICLE; BRAIN REGION; DRUG EFFECT; DRUG PROTEIN BINDING; FEMALE; HUMAN; LIMBIC CORTEX; MIDDLE AGED; MONOTHERAPY; OVARIECTOMY; POSITRON EMISSION TOMOGRAPHY; POSTMENOPAUSE; PROTEIN EXPRESSION; STRIATE CORTEX; BRAIN; CLINICAL TRIAL; DEPRESSION; DIAGNOSTIC USE; DRUG EFFECTS; HORMONE SUBSTITUTION; METABOLISM; POSTOPERATIVE PERIOD; PROCEDURES; SEROTONINERGIC NERVE CELL; TISSUE DISTRIBUTION;

ADULT; AGED; BENZYLAMINES; BRAIN; DEPRESSION; ESTROGENS; FEMALE; HORMONE REPLACEMENT THERAPY; HUMANS; MIDDLE AGED; POSITRON-EMISSION TOMOGRAPHY; POSTMENOPAUSE; POSTOPERATIVE PERIOD; PROTEIN BINDING; RADIOPHARMACEUTICALS; SEROTONERGIC NEURONS; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; TESTOSTERONE; TISSUE DISTRIBUTION;

EID: 84912084302     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2014.11.003     Document Type: Article

References (71)

1. Amin Z., Gueorguieva R., Cappiello A., Czarkowski K.A., Stiklus S., Anderson G.M., Naftolin F., Epperson C.N. Estradiol and tryptophan depletion interact to modulate cognition in menopausal women. Neuropsychopharmacology 2006, 31(11):2489-2497.
2. Bachmann G., Oza D. Female androgen insufficiency. Obstet. Gynecol. Clin. North Am. 2006, 33:589-598.
3. Baron-Cohen S., Knickmeyer R.C., Belmonte M.K. Sex differences in the brain: implications for explaining autism. Science 2005, 310:819-823.
4. Beck A.T., Ward C.H., Mendelson M., Mock J., Erbaugh J. An inventory for measuring depression. Arch. Gen. Psychiatry 1961, 4:561-571.
5. Berman K.F., Schmidt P.J., Rubinow D.R., Danaceau M.A., Van Horn J.D., Esposito G., Ostrem J.L., Weinberger D.R. Modulation of cognition-specific cortical activity by gonadal steroids: a positron-emission tomography study in women. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:8836-8841.
6. Bethea C.L., Lu N.Z., Gundlah C., Streicher J.M. Diverse actions of ovarian steroids in the serotonin neural system. Front. Neuroendocrinol. 2002, 23:41-100.
7. Celotti F., Negri-Cesi P., Poletti A. Steroid metabolism in the mammalian brain: 5alpha-reduction and aromatization. Brain Res. Bull. 1997, 44:365-375.
8. Cone R.I., Davis G.A., Goy R.W. Effects of ovarian steroids on serotonin metabolism within grossly dissected and microdissected brain regions of the ovariectomised rat. Brain Res. Bull. 1981, 7:639-644.
9. Corradetti R., Laaris N., Hanoun N. Antagonist properties of (-)-pindolol and WAY 100635 at somatodendritic and postsynaptic 5-HT1A receptors in the rat brain. Br. J. Pharmacol. 1998, 123:449-462.
10. Cortes R., Soriano E., Pazos A., Probst A., Palacios J.M. Autoradiography of antidepressant binding sites in the human brain: localization using [3H]imipramine and [3H]paroxetine. Neuroscience 1988, 27:473-496.
11. Davison S.L., Bell R., Donath S., Montalto J.G., Davis S.R. Androgen levels in adult females: changes with age, menopause, and oophorectomy. J. Clin. Endocrinol. Metab. 2005, 90:3847-3853.
12. Drevets W.C., Price J.L., Furey M.L. Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Struct. Funct. 2008, 213:93-118.
13. Espeland M.A., Rapp S.R., Shumaker S.A., Brunner R., Manson J.E., Sherwin B.B., et al. Conjugated equine estrogens and global cognitive function in postmenopausal women: Women's Health Initiative Memory Study. JAMA 2004, 291:2959-2968.
14. Fink G., Sumner B., Rosie R., Wilson H., McQueen J. Androgen actions on central serotonin neurotransmission: relevance for mood, mental state and memory. Behav. Brain Res. 1999, 105:53-68.
15. Flöter A., Nathorst-Böös J., Carlström K., von Schoultz B. Addition of testosterone to estrogen replacement therapy in oophorectomized women: Effects on sexuality and well-being. Climacteric 2002, 5:357-365.
16. Frokjaer V.G., Erritzoe D., Juul A., Nielsen F.A., Holst K., Svarer C., Madsen J., Paulson O.B., Knudsen G.M. Endogenous plasma estradiol in healthy men is positively correlated with cerebral cortical serotonin 2A receptor binding. Psychoneuroendocrinology 2010, 35:1311-1320.
17. 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, 34:1096-1103. (published online 7 May 2014). 10.1038/jcbfm.2014.82.
18. Halldin C., Lundberg J., Sovago J., Gulyas B., Guilloteau D., Vercouillie J., Edmond P., Chalon S., Tarkianen J., Hiltunen J., Farde L. [(11)C]MADAM, a new serotonin transporter radioligand characterized in the monkey brain by PET. Synapse 2005, 58:173-183.
19. Hermans E.J., Bos P.A., Ossewaarde L., Ramsey N.F., Fernandez G., van Honk J. Effects of exogenous testosterone on the ventral striatal BOLD response during reward anticipation in healthy women. NeuroImage 2010, 52:277-283.
20. Hogervorst E., Williams J., Budge M., Riedel W., Jolles J. The nature of the effect of female gonadal hormone replacement therapy on cognitive function in post-menopausal women: a meta-analysis. Neuroscience 2000, 101:485-512.
21. Joffe H., Hall J.E., Gruber S., Sarmiento I.A., Cohen L.S., Yurgelun-Todd D., et al. Estrogen therapy selectively enhances prefrontal cognitive processes: a randomized, double-blind, placebo-controlled study with functional magnetic resonance imaging in perimenopausal and recently postmenopausal women. Menopause 2006, 13:411-422.
22. Johnson M.D., Crowley W.R. Acute effects of estradiol on circulating luteinizing hormone and prolactin concentrations and on serotonin turnover in individual brain nuclei. Endocrinology 1983, 113:1935-1941.
23. Jovanovic H., Cerin A., Karlsson P., Lundberg J., Halldin C., Nordstrom A.L. A PET study of 5-HT1A receptors at different phases of the menstrual cycle in women with premenstrual dysphoria. Psychiatry Res. 2006, 148:185-193.
24. Jovanovic H., Lundberg J., Karlsson P., Cerin A., Saijo T., Varrone A., Halldin C., Nordstrom A.L. Sex differences in the serotonin 1A receptor and serotonin transporter binding in the human brain measured by PET. NeuroImage 2008, 39:1408-1419.
25. Kranz G.S., Rami-Mark C., Kaufmann U., Baldinger P., Hahn A., Höflich A., Savli M., Stein P., Wadsak W., Mitterhauser M., Winkler D., Lanzenberger R., Kasper S. Effects of hormone replacement therapy on cerebral serotonin-1A receptor binding in postmenopausal women examined with [carbonyl-11C]WAY-100635. Psychoneuroendocrinology 2014, 45:1-10.
26. Kugaya A., Epperson C.N., Zoghbi S., van Dyck C.H., Hou Y., Fujita M., Staley J.K., Garg P.K., Seibyl J.P., Innis R.B. Increase in prefrontal cortex serotonin 2A receptors following estrogen treatment in postmenopausal women. Am. J. Psychiatry 2003, 160:1522-1524.
27. Lammertsma A.A., Hume S.P. Simplified reference tissue model for PET receptor studies. NeuroImage 1996, 4:153-158.
28. Lezak M.D. Neuropsychological assessment 1995, Oxford University Press, New York, (xviii, 1026 p. p.). 3rd ed.
29. 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, 8:353-360.
30. Lundberg J., Odano I., Olsson H., Halldin C., Farde L. Quantification of 11C-MADAM binding to the serotonin transporter in the human brain. J. Nucl. Med. 2005, 46:1505-1515.
31. McHenry J., Carrier N., Hull E., Kabbaj M. Sex differences in anxiety and depression: Role of testosterone. Front. Neuroendocrinol. 2013, S0091-3022(13). (00057-5, Epub ahead of print). 10.1016/j.yfrne.2013.09.001.
32. 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, 45:13-23.
33. Meyer J.H., Wilson A.A., Sagrati S., Hussey D., Carella A., Potter W.Z., Ginovart N., Spencer E.P., Cheok A., Houle S. Serotonin transporter occupancy of five selective serotonin reuptake inhibitors at different doses: an [11C]DASB positron emission tomography study. Am. J. Psychiatry 2004, 161:826-835.
34. Miller K.K., Deckersbach T., Rauch S.L., Fischman A.J., Grieco K.A., Herzog D.B., Klibanski A. Testosterone administration attenuates regional brain hypometabolism in women with anorexia nervosa. Psychiatry Res. 2004, 132:197-207.
35. Möller M.C., Bartfai A.B., Flöter Rådestad A. Effects of testosterone and estrogen replacement on memory function. Menopause 2010, 17(5):983-989.
36. Mooradian A.D., Morley J.E., Korenman S.G. Biological actions of androgens. Endocr. Rev. 1987, 8:1-28.
37. Moser U., Wadsak W., Spindelegger C., Mitterhauser M., Mien L.K., Bieglmayer C., Kletter K., Kasper S., Lanzenberger R. Hypothalamic serotonin-1A receptor binding measured by PET predicts the plasma level of dehydroepiandrosterone sulfate in healthy women. Neurosci. Lett. 2010, 476:161-165.
38. Moses E.L., Drevets W.C., Smith G., Mathis C.A., Kalro B.N., Butters M.A., Leondires M.P., Greer P.J., Lopresti B., Loucks T.L., Berga S.L. Effects of estradiol and progesterone administration on human serotonin 2A receptor binding: a PET study. Biol. Psychiatry 2000, 48:854-860.
39. Moses-Kolko E.L., Berga S.L., Greer P.J., Smith G., Meltzer C.C., Wayne C., Drevets W.C. Widespread increases of cortical serotonin type 2A receptor availability after hormone therapy in euthymic postmenopausal women. Fertil. Steril. 2003, 80(3):554-559.
40. Moses-Kolko E.L., Price J.C., Shah N., Berga S., Sereika S.M., Fisher P.M., Coleman R., Becker C., Mason N.S., Loucks T., Meltzer C.C. Age, sex, and reproductive hormone effects on brain serotonin-1A and serotonin-2A receptor binding in a healthy population. Neuropsychopharmacology 2011, 36:2729-2740.
41. Nathorst-Boos J., Floter A., Jarkander-Rolff M., Carlstrom K., Schoultz B. Treatment with percutanous testosterone gel in postmenopausal women with decreased libido-effects on sexuality and psychological general well-being. Maturitas 2006, 53:11-18.
42. Parsey R.V., Hastings R.S., Oquendo M.A., Huang Y.Y., Simpson N., Arcement J., Huang Y., Ogden R.T., Van Heertum R.L., Arango V., Mann J.J. Lower serotonin transporter binding potential in the human brain during major depressive episodes. Am. J. Psychiatry 2006, 163:52-58.
43. Pecins-Thompson M., Brown N.A., Bethea C.L. Regulation of serotonin re-uptake transporter mRNA expression by ovarian steroids in rhesus macaques. Brain Res. Mol. Brain Res. 1998, 53:120-129.
44. Plenge P., Mellerup E.T., Laursen H. Regional distribution of the serotonin transport complex in human brain, identified with 3H-paroxetine, 3H-citalopram and 3H-imipramine. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 1990, 14:61-72.
45. Rapp S.R., Espeland M.A., Shumaker S.A., Henderson V.W., Brunner R.L., Manson J.E., et al. Effect of estrogen plus progestin on global cognitive function in postmenopausal women: the Women's Health Initiative Memory Study: a randomized controlled trial. JAMA 2003, 289:2663-2672.
46. Rasgon N.L., Dunkin J., Fairbanks L., Altshuler L.L., Troung C., Elman S., Wroolie T.E., Brunhuber M.V., Rapkin A. Estrogen and response to sertraline in postmenopausal women with major depressive disorder: a pilot study. J. Psychiatr. Res. 2007, 41:338-343.
47. Robichaud M., Debonnel G. Oestrogen and testosterone modulate the firing activity of dorsal raphe nucleus serotonergic neurones in both male and female rats. J. Neuroendocrinol. 2005, 17:179-185.
48. Rubinow D.R., Schmidt P.J., Roca C.A. Estrogen-serotonin interactions: implications for affective regulation. Biol. Psychiatry 1998, 44:839-850.
49. Rundnick G., Wall S.C. The molecular mechanism of "ecstasy" [3,4-methylenedioxy-methamphetamine (MDMA)]: serotonin transporters are targets for MDMA-induced serotonin release. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:1817-1821.
50. Savitz J., Lucki I., Drevets W.C. 5-HT(1A) receptor function in major depressive disorder. Prog. Neurobiol. 2009, 88:17-31.
51. 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, 9:393-399.
52. Shaywitz S.E., Shaywitz B.A., Pugh K.R., Fulbright R.K., Skudlarski P., Mencl W.E., Constable R.T., Naftolin F., Palter S.F., Marchione K.E., Katz L., Shankweiler D.P., Fletcher J.M., Lacadie C., Keltz M., Gore J.C. Effect of estrogen on brain activation patterns in postmenopausal women during working memory tasks. JAMA 1999, 281:1197-1202.
53. Shaywitz S.E., Naftolin F., Zelterman D., Marchione K.E., Holahan J.M., Palter S.F., et al. Better oral reading and short-term memory in midlife, postmenopausal women taking estrogen. Menopause 2003, 10:420-426.
54. Sherwin B.B. Estrogen and/or androgen replacement therapy and cognitive functioning in surgically menopausal women. Psychoneuroendocrinology 1988, 13:345-357.
55. Shifren J.L., Braunstein G.D., Simon J.A., Casson P.R., Buster J.E., Redmond G.P. Transdermal testosterone treatment in women with impaired sexual function after oophorectomy. N. Engl. J. Med. 2000, 343:682-688.
56. Simerly R.B. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu. Rev. Neurosci. 2002, 25:507-536.
57. Simpson E.R. Aromatization of androgens in women: current concepts and findings. Fertil. Steril. 2002, 77:6-10.
58. Smith Y.R., Bowen L., Love L.T., Berent-Spillson A., Frey K.A., Persad C.C., Reame N.K., Koeppe R.A., Zubieta J.-K. Early initiation of hormone therapy in menopausal women is associated with increased hippocampal and posterior cingulate cholinergic activity. J. Clin. Endocrinol. Metab. 2011, 96(11):E1761-E1770.
59. Soares C.N. Depression during the menopausal transition: window of vulnerability or continuum of risk?. Menopause 2008, 15:207-209.
60. Soares C.N., Zitek B. Reproductive hormone sensitivity and risk for depression across the female life cycle: a continuum of vulnerability?. J. Psychiatry Neurosci. 2008, 33:331-343.
61. Sodergard R., Backstrom T., Shanbhag V., Carstensen H. Calculation of free and bound fractions of testosterone and estradiol-17 beta to human plasma proteins at body temperature. J. Steroid Biochem. 1982, 16:801-810.
62. Steer R.A., Rissmiller D.J., Ranieri W.F., Beck A.T. Structure of the computer-assisted Beck Anxiety Inventory with psychiatric inpatients. J. Pers. Assess. 1993, 60:532-542.
63. Stein P., Savli M., Wadsak W., Mitterhauser M., Fink M., Spindelegger C., Mien L.K., Moser U., Dudczak R., Kletter K., Kasper S., Lanzenberger R. The serotonin-1A receptor distribution in healthy men and women measured by PET and [carbonyl-11C]WAY-100635. Eur. J. Nucl. Med. Mol. Imaging 2008, 35:2159-2168.
64. Stein P., Baldinger P., Kaufmann U., Christina R.M., Hahn A., Höflich A., Kranz G.S., Savli M., Wadsak W., Mitterhauser M., Winkler D., Kasper S., Lanzenberger R. Relation of progesterone and DHEAS serum levels to 5-HT1A receptor binding potential in pre- and postmenopausal women. Psychoneuroendocrinology 2014, 46:52-63.
65. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 2002, 15:273-289.
66. van Honk J., Schutter D.J., Bos P.A., Kruijt A.W., Lentjes E.G., Baron-Cohen S. Testosterone administration impairs cognitive empathy in women depending on second-to-fourth digit ratio. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:3448-3452.
67. van Wingen G.A., Zylicz S.A., Pieters S., Mattern C., Verkes R.J., Buitelaar J.K., Fernández G. Testosterone increases amygdala reactivity in middle-aged women to a young adulthood level. Neuropsychopharmacology 2009, 34:539-547.
68. Wienhard K., Dahlbom M., Eriksson L., Michel C., Bruckbauer T., Pietrzyk U., Heiss W.D. The ECAT EXACT HR: performance of a new high resolution positron scanner. J. Comput. Assist. Tomogr. 1994, 18:110-118.
69. Witte A.V., Floel A., Stein P., Savli M., Mien L.K., Wadsak W., Spindelegger C., Moser U., Fink M., Hahn A., Mitterhauser M., Kletter K., Kasper S., Lanzenberger R. Aggression is related to frontal serotonin-1A receptor distribution as revealed by PET in healthy subjects. Hum. Brain Mapp. 2009, 30:2558-2570.
70. Zuloaga D.G., Puts D.A., Jordan C.L., Breedlove S.M. The role of androgen receptors in the masculinization of brain and behavior: what we've learned from the testicular feminization mutation. Horm. Behav. 2008, 53:613-626.
71. Zweifel J.E., O'Brien W.H. A meta-analysis of the effect of hormone replacement therapy upon depressed mood. Psychoneuroendocrinology 1997, 22:189-212.