Sex hormones and biomarkers of neuroprotection and neurodegeneration: Implications for female reproductive events in bipolar disorder

Bipolar Disorders

Volumn 16, Issue 1, 2014, Pages 48-57

  Frey, Benicio N ^a,b   Dias, Rodrigo S ^c  

^a MCMASTER UNIVERSITY   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

BDNF; Bipolar disorder; Estrogen; Inflammation; Menopause; Oxidative stress; Postpartum; Pregnancy; Premenstrual; Progesterone

Indexed keywords

BIOLOGICAL MARKER; SEX HORMONE;

ANTIINFLAMMATORY ACTIVITY; ASTROCYTE; BINDING SITE; BIPOLAR DISORDER; BRAIN MATURATION; CEREBELLUM; CLINICAL FEATURE; CLINICAL TRIAL (TOPIC); DEPRESSION; ESTROGEN RESPONSIVE ELEMENT; ESTRUS CYCLE; FEMALE GENITAL SYSTEM FUNCTION; HIPPOCAMPUS; HUMAN; INFLAMMATION; INTRACELLULAR SIGNALING; LIPID PEROXIDATION; MEDLINE; MENSTRUAL CYCLE; MICROGLIA; MITOCHONDRIAL MEMBRANE; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVE DEGENERATION; NEUROBIOLOGY; NEUROPROTECTION; NEUROTRANSMISSION; NONHUMAN; OVARY CYCLE; OXIDATIVE STRESS; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW;

BDNF; BIPOLAR DISORDER; ESTROGEN; INFLAMMATION; MENOPAUSE; OXIDATIVE STRESS; POSTPARTUM; PREGNANCY; PREMENSTRUAL; PROGESTERONE;

BIPOLAR DISORDER; BRAIN-DERIVED NEUROTROPHIC FACTOR; FEMALE; GONADAL STEROID HORMONES; HUMANS; INFLAMMATION; MALE; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS;

EID: 84893129567     PISSN: 13985647     EISSN: 13995618     Source Type: Journal    
DOI: 10.1111/bdi.12151     Document Type: Review

References (135)

1. Viguera AC, Tondo L, Koukopoulos AE et al. Episodes of mood disorders in 2, 252 pregnancies and postpartum periods. Am J Psychiatry 2011; 168: 1179-1185.
2. Dias RS, Lafer B, Russo C et al. Longitudinal follow-up of bipolar disorder in women with premenstrual exacerbation: findings from STEP-BD. Am J Psychiatry 2011; 168: 386-394.
3. Marsh WK, Templeton A, Ketter TA, Rasgon NL. Increased frequency of depressive episodes during the menopausal transition in women with bipolar disorder: preliminary report. J Psychiatr Res 2008; 42: 247-251.
4. Rubinow DR, Schmidt PJ. Gonadal steroid regulation of mood: the lessons of premenstrual syndrome. Front Neuroendocrinol 2006; 27: 210-216.
5. Brinton RD, Thompson RF, Foy MR et al. Progesterone receptors: form and function in brain. Front Neuroendocrinol 2008; 29: 313-339.
6. McEwen BS, Alves SE. Estrogen actions in the central nervous system. Endocr Rev 1999; 20: 279-307.
7. Lokuge S, Frey BN, Foster JA, Soares CN, Steiner M. The rapid effects of estrogen: a mini-review. Behav Pharmacol 2010; 21: 465-472.
8. Bloch M, Schmidt PJ, Danaceau M, Murphy J, Nieman L, Rubinow DR. Effects of gonadal steroids in women with a history of postpartum depression. Am J Psychiatry 2000; 157: 924-930.
9. Schmidt PJ, Nieman LK, Danaceau MA, Adams LF, Rubinow DR. Differential behavioral effects of gonadal steroids in women with and in those without premenstrual syndrome. N Engl J Med 1998; 338: 209-216.
10. Wittchen HU, Becker E, Lieb R, Krause P. Prevalence, incidence and stability of premenstrual dysphoric disorder in the community. Psychol Med 2002; 32: 119-132.
11. Fornaro M, Perugi G. The impact of premenstrual dysphoric disorder among 92 bipolar patients. Eur Psychiatry 2010; 25: 450-454.
12. Choi J, Baek JH, Noh J et al. Association of seasonality and premenstrual symptoms in bipolar I and bipolar II disorders. J Affect Disord 2011; 129: 313-316.
13. Karadag F, Akdeniz F, Erten E et al. Menstrually related symptom changes in women with treatment-responsive bipolar disorder. Bipolar Disord 2004; 6: 253-259.
14. Shivakumar G, Bernstein IH, Suppes T et al. Are bipolar mood symptoms affected by the phase of the menstrual cycle? J Womens Health 2008; 17: 473-478.
15. Sit D, Seltman H, Wisner KL. Menstrual effects on mood symptoms in treated women with bipolar disorder. Bipolar Disord 2011; 13: 310-317.
16. Frey BN, Minuzzi L. Comorbid bipolar disorder and premenstrual dysphoric disorder: real patients, unanswered questions. Arch Womens Ment Health 2013; 16: 79-81.
17. Viguera AC, Whitfield T, Baldessarini RJ et al. Risk of recurrence in women with bipolar disorder during pregnancy: prospective study of mood stabilizer discontinuation. Am J Psychiatry 2007; 164: 1817-1824; quiz 923.
18. Freeman MP, Smith KW, Freeman SA et al. The impact of reproductive events on the course of bipolar disorder in women. J Clin Psychiatry 2002; 63: 284-287.
19. Akdeniz F, Vahip S, Pirildar S, Vahip I, Doganer I, Bulut I. Risk factors associated with childbearing-related episodes in women with bipolar disorder. Psychopathology 2003; 36: 234-238.
20. Sharma V, Pope CJ. Pregnancy and bipolar disorder: a systematic review. J Clin Psychiatry 2012; 73: 1447-1455.
21. Jones I, Craddock N. Familiality of the puerperal trigger in bipolar disorder: results of a family study. Am J Psychiatry 2001; 158: 913-917.
22. Munk-Olsen T, Laursen TM, Mendelson T, Pedersen CB, Mors O, Mortensen PB. Risks and predictors of readmission for a mental disorder during the postpartum period. Arch Gen Psychiatry 2009; 66: 189-195.
23. Sharma V, Burt VK. DSM-V: modifying the postpartum-onset specifier to include hypomania. Arch Womens Ment Health 2011; 14: 67-69.
24. Sharma V, Khan M, Corpse C, Sharma P. Missed bipolarity and psychiatric comorbidity in women with postpartum depression. Bipolar Disord 2008; 10: 742-747.
25. Blehar MC, DePaulo JR Jr, Gershon ES, Reich T, Simpson SG, Nurnberger JI Jr. Women with bipolar disorder: findings from the NIMH Genetics Initiative sample. Psychopharmacol Bull 1998; 34: 239-243.
26. Gregory RJ, Masand PS, Yohai NH. Depression across the reproductive life cycle: correlations between events. Prim Care Companion J Clin Psychiatry 2000; 2: 127-129.
27. Robertson Blackmore E, Craddock N, Walters J, Jones I. Is the perimenopause a time of increased risk of recurrence in women with a history of bipolar affective postpartum psychosis? A case series. Arch Womens Ment Health 2008; 11: 75-78.
28. Kapczinski F, Dal-Pizzol F, Teixeira AL et al. Peripheral biomarkers and illness activity in bipolar disorder. J Psychiatr Res 2011; 45: 156-161.
29. Frey BN, Andreazza AC, Houenou J et al. Biomarkers in bipolar disorder: a positional paper from the International Society for Bipolar Disorders Biomarkers Task Force. Aust N Z J Psychiatry 2013; 47: 321-332.
30. Cunha AB, Frey BN, Andreazza AC et al. Serum brain-derived neurotrophic factor is decreased in bipolar disorder during depressive and manic episodes. Neurosci Lett 2006; 398: 215-219.
31. Machado-Vieira R, Dietrich MO, Leke R et al. Decreased plasma brain derived neurotrophic factor levels in unmedicated bipolar patients during manic episode. Biol Psychiatry 2007; 61: 142-144.
32. Tramontina JF, Andreazza AC, Kauer-Sant'Anna M et al. Brain-derived neurotrophic factor serum levels before and after treatment for acute mania. Neurosci Lett 2009; 452: 111-113.
33. de Sousa RT, van de Bilt MT, Diniz BS et al. Lithium increases plasma brain-derived neurotrophic factor in acute bipolar mania: a preliminary 4-week study. Neurosci Lett 2011; 494: 54-56.
34. Kauer-Sant'Anna M, Kapczinski F, Andreazza AC et al. Brain-derived neurotrophic factor and inflammatory markers in patients with early- vs. late-stage bipolar disorder. Int J Neuropsychopharmacol 2009; 12: 447-458.
35. Fernandes BS, Gama CS, Maria Cereser K et al. Brain-derived neurotrophic factor as a state-marker of mood episodes in bipolar disorders: a systematic review and meta-regression analysis. J Psychiatr Res 2011; 45: 995-1004.
36. Thompson Ray M, Weickert CS, Wyatt E, Webster MJ. Decreased BDNF, trkB-TK+ and GAD67 mRNA expression in the hippocampus of individuals with schizophrenia and mood disorders. J Psychiatry Neurosci 2011; 36: 195-203.
37. Dunham JS, Deakin JF, Miyajima F, Payton A, Toro CT. Expression of hippocampal brain-derived neurotrophic factor and its receptors in Stanley consortium brains. J Psychiatr Res 2009; 43: 1175-1184.
38. Soontornniyomkij B, Everall IP, Chana G, Tsuang MT, Achim CL, Soontornniyomkij V. Tyrosine kinase B protein expression is reduced in the cerebellum of patients with bipolar disorder. J Affect Disord 2011; 133: 646-654.
39. Bernard R, Kerman IA, Thompson RC et al. Altered expression of glutamate signaling, growth factor, and glia genes in the locus coeruleus of patients with major depression. Mol Psychiatry 2011; 16: 634-646.
40. Balu DT, Hoshaw BA, Malberg JE, Rosenzweig-Lipson S, Schechter LE, Lucki I. Differential regulation of central BDNF protein levels by antidepressant and non-antidepressant drug treatments. Brain Res 2008; 1211: 37-43.
41. Frey BN, Andreazza AC, Cereser KM et al. Effects of mood stabilizers on hippocampus BDNF levels in an animal model of mania. Life Sci 2006; 79: 281-286.
42. Valdes JJ, Ramirez FM, Juarez B, Weeks OI. Lithium enhances cortical mRNA expression in ovariectomized C57BL/6J mice. Acta Neurobiol Exp (Wars) 2010; 70: 288-296.
43. Jacobsen JP, Mork A. The effect of escitalopram, desipramine, electroconvulsive seizures and lithium on brain-derived neurotrophic factor mRNA and protein expression in the rat brain and the correlation to 5-HT and 5-HIAA levels. Brain Res 2004; 1024: 183-192.
44. Mai L, Jope RS, Li X. BDNF-mediated signal transduction is modulated by GSK3beta and mood stabilizing agents. J Neurochem 2002; 82: 75-83.
45. Numakawa T, Yokomaku D, Richards M, Hori H, Adachi N, Kunugi H. Functional interactions between steroid hormones and neurotrophin BDNF. World J Biol Chem 2010; 1: 133-143.
46. Scharfman HE, MacLusky NJ. Estrogen and brain-derived neurotrophic factor (BDNF) in hippocampus: complexity of steroid hormone-growth factor interactions in the adult CNS. Front Neuroendocrinol 2006; 27: 415-435.
47. Sohrabji F, Miranda RC, Toran-Allerand CD. Identification of a putative estrogen response element in the gene encoding brain-derived neurotrophic factor. Proc Natl Acad Sci USA 1995; 92: 11110-11114.
48. Cavus I, Duman RS. Influence of estradiol, stress, and 5-HT2A agonist treatment on brain-derived neurotrophic factor expression in female rats. Biol Psychiatry 2003; 54: 59-69.
49. Gibbs RB. Levels of trkA and BDNF mRNA, but not NGF mRNA, fluctuate across the estrous cycle and increase in response to acute hormone replacement. Brain Res 1998; 810: 294.
50. Begliuomini S, Casarosa E, Pluchino N et al. Influence of endogenous and exogenous sex hormones on plasma brain-derived neurotrophic factor. Hum Reprod 2007; 22: 995-1002.
51. Cubeddu A, Bucci F, Giannini A et al. Brain-derived neurotrophic factor plasma variation during the different phases of the menstrual cycle in women with premenstrual syndrome. Psychoneuroendocrinology 2011; 36: 523-530.
52. Takuma K, Matsuo A, Himeno Y et al. 17beta-estradiol attenuates hippocampal neuronal loss and cognitive dysfunction induced by chronic restraint stress in ovariectomized rats. Neuroscience 2007; 146: 60-68.
53. Tripanichkul W, Gerdprasert O, Jaroensuppaperch EO. Estrogen reduces BDNF level, but maintains dopaminergic cell density in the striatum of MPTP mouse model. Int J Neurosci 2010; 120: 489-495.
54. Yang LC, Zhang QG, Zhou CF et al. Extranuclear estrogen receptors mediate the neuroprotective effects of estrogen in the rat hippocampus. PLoS ONE 2010; 5: e9851.
55. Sato K, Akaishi T, Matsuki N, Ohno Y, Nakazawa K. beta-Estradiol induces synaptogenesis in the hippocampus by enhancing brain-derived neurotrophic factor release from dentate gyrus granule cells. Brain Res 2007; 1150: 108-120.
56. Ivanova T, Kuppers E, Engele J, Beyer C. Estrogen stimulates brain-derived neurotrophic factor expression in embryonic mouse midbrain neurons through a membrane-mediated and calcium-dependent mechanism. J Neurosci Res 2001; 66: 221-230.
57. Ren-Patterson RF, Cochran LW, Holmes A, Lesch KP, Lu B, Murphy DL. Gender-dependent modulation of brain monoamines and anxiety-like behaviors in mice with genetic serotonin transporter and BDNF deficiencies. Cell Mol Neurobiol 2006; 26: 755-780.
58. Frye CA, Rhodes ME. Estrogen-priming can enhance progesterone's anti-seizure effects in part by increasing hippocampal levels of allopregnanolone. Pharmacol Biochem Behav 2005; 81: 907-916.
59. Bimonte-Nelson HA, Nelson ME, Granholm AC. Progesterone counteracts estrogen-induced increases in neurotrophins in the aged female rat brain. NeuroReport 2004; 15: 2659-2663.
60. Aguirre CC, Baudry M. Progesterone reverses 17beta-estradiol-mediated neuroprotection and BDNF induction in cultured hippocampal slices. Eur J Neurosci 2009; 29: 447-454.
61. Coughlan T, Gibson C, Murphy S. Progesterone, BDNF and neuroprotection in the injured CNS. Int J Neurosci 2009; 119: 1718-1740.
62. Morita K, Her S. Progesterone pretreatment enhances serotonin-stimulated BDNF gene expression in rat c6 glioma cells through production of 5alpha-reduced neurosteroids. J Mol Neurosci 2008; 34: 193-200.
63. Kaur P, Jodhka PK, Underwood WA et al. Progesterone increases brain-derived neuroptrophic factor expression and protects against glutamate toxicity in a mitogen-activated protein kinase- and phosphoinositide-3 kinase-dependent manner in cerebral cortical explants. J Neurosci Res 2007; 85: 2441-2449.
64. Bishop NA, Lu T, Yankner BA. Neural mechanisms of ageing and cognitive decline. Nature 2010; 464: 529-535.
65. Machado-Vieira R, Andreazza AC, Viale CI et al. Oxidative stress parameters in unmedicated and treated bipolar subjects during initial manic episode: a possible role for lithium antioxidant effects. Neurosci Lett 2007; 421: 33-36.
66. Andreazza AC, Kauer-Sant'Anna M, Frey BN et al. Oxidative stress markers in bipolar disorder: a meta-analysis. J Affect Disord 2008; 111: 135-144.
67. Andreazza AC, Frey BN, Erdtmann B et al. DNA damage in bipolar disorder. Psychiatry Res 2007; 153: 27-32.
68. Andreazza AC, Shao L, Wang JF, Young LT. Mitochondrial complex I activity and oxidative damage to mitochondrial proteins in the prefrontal cortex of patients with bipolar disorder. Arch Gen Psychiatry 2010; 67: 360-368.
69. Che Y, Wang JF, Shao L, Young T. Oxidative damage to RNA but not DNA in the hippocampus of patients with major mental illness. J Psychiatry Neurosci 2010; 35: 296-302.
70. Wang J-F, Shao L, Sun X, Young LT. Increased oxidative stress in the anterior cingulate cortex of subjects with bipolar disorder and schizophrenia. Bipolar Disord 2009; 11: 523-529.
71. Buttner N, Bhattacharyya S, Walsh J, Benes FM. DNA fragmentation is increased in non-GABAergic neurons in bipolar disorder but not in schizophrenia. Schizophr Res 2007; 93: 33-41.
72. Shao L, Young LT, Wang J-F. Chronic treatment with mood stabilizers lithium and valproate prevents excitotoxicity by inhibiting oxidative stress in rat cerebral cortical cells. Biol Psychiatry 2005; 58: 879-884.
73. Lai JS, Zhao C, Warsh JJ, Li PP. Cytoprotection by lithium and valproate varies between cell types and cellular stresses. Eur J Pharmacol 2006; 539: 18-26.
74. Andreazza AC, Kauer-Sant'Anna M, Frey BN et al. Effects of mood stabilizers on DNA damage in an animal model of mania. J Psychiatry Neurosci 2008; 33: 516-524.
75. Frey BN, Valvassori SS, Reus GZ et al. Effects of lithium and valproate on amphetamine-induced oxidative stress generation in an animal model of mania. J Psychiatry Neurosci 2006; 31: 326-332.
76. Numakawa T, Matsumoto T, Numakawa Y, Richards M, Yamawaki S, Kunugi H. Protective action of neurotrophic factors and estrogen against oxidative stress-mediated neurodegeneration. J Toxicol 2011; 2011: 405194. doi: 10.1155/2011/405194.
77. Irwin RW, Yao J, Hamilton RT, Cadenas E, Brinton RD, Nilsen J. Progesterone and estrogen regulate oxidative metabolism in brain mitochondria. Endocrinology 2008; 149: 3167-3175.
78. Razmara A, Duckles SP, Krause DN, Procaccio V. Estrogen suppresses brain mitochondrial oxidative stress in female and male rats. Brain Res 2007; 1176: 71-81.
79. Stirone C, Duckles SP, Krause DN, Procaccio V. Estrogen increases mitochondrial efficiency and reduces oxidative stress in cerebral blood vessels. Mol Pharmacol 2005; 68: 959-965.
80. Giordano C, Montopoli M, Perli E et al. Oestrogens ameliorate mitochondrial dysfunction in Leber's hereditary optic neuropathy. Brain 2011; 134: 220-234.
81. Razmara A, Sunday L, Stirone C et al. Mitochondrial effects of estrogen are mediated by estrogen receptor alpha in brain endothelial cells. J Pharmacol Exp Ther 2008; 325: 782-790.
82. Numakawa Y, Matsumoto T, Yokomaku D et al. 17beta-estradiol protects cortical neurons against oxidative stress-induced cell death through reduction in the activity of mitogen-activated protein kinase and in the accumulation of intracellular calcium. Endocrinology 2007; 148: 627-637.
83. Grove-Strawser D, Boulware MI, Mermelstein PG. Membrane estrogen receptors activate the metabotropic glutamate receptors mGluR5 and mGluR3 to bidirectionally regulate CREB phosphorylation in female rat striatal neurons. Neuroscience 2010; 170: 1045-1055.
84. Gingerich S, Kim GL, Chalmers JA et al. Estrogen receptor alpha and G-protein coupled receptor 30 mediate the neuroprotective effects of 17beta-estradiol in novel murine hippocampal cell models. Neuroscience 2010; 170: 54-66.
85. Irwin RW, Yao J, Ahmed SS, Hamilton RT, Cadenas E, Brinton RD. Medroxyprogesterone acetate antagonizes estrogen up-regulation of brain mitochondrial function. Endocrinology 2011; 152: 556-567.
86. Behl C, Widmann M, Trapp T, Holsboer F. 17-beta estradiol protects neurons from oxidative stress-induced cell death in vitro. Biochem Biophys Res Commun 1995; 216: 473-482.
87. Goodman Y, Bruce AJ, Cheng B, Mattson MP. Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury, and amyloid beta-peptide toxicity in hippocampal neurons. J Neurochem 1996; 66: 1836-1844.
88. Sharma AK, Bhattacharya SK, Khanna N et al. Effect of progesterone on phosphamidon-induced impairment of memory and oxidative stress in rats. Hum Exp Toxicol 2011; 30: 1626-1634.
89. Schmidt AJ, Krieg JC, Vedder H. Differential effects of glucocorticoids and gonadal steroids on glutathione levels in neuronal and glial cell systems. J Neurosci Res 2002; 67: 544-550.
90. Pajovic SB, Saicic ZS, Spasic MB, Petrovic VM, Martinovic JV. Effects of progesterone and estradiol benzoate on glutathione dependent antioxidant enzyme activities in the brain of female rats. Gen Physiol Biophys 1999; 18: 35-44.
91. Bishnoi M, Chopra K, Kulkarni SK. Progesterone attenuates neuroleptic-induced orofacial dyskinesia via the activity of its metabolite, allopregnanolone, a positive GABA(A) modulating neurosteroid. Prog Neuropsychopharmacol Biol Psychiatry 2008; 32: 451-461.
92. Brietzke E, Stertz L, Fernandes BS et al. Comparison of cytokine levels in depressed, manic and euthymic patients with bipolar disorder. J Affect Disord 2009; 116: 214-217.
93. Kunz M, Cereser KM, Goi PD et al. Serum levels of IL-6, IL-10 and TNF-α in patients with bipolar disorder and schizophrenia: differences in pro- and anti-inflammatory balance. Rev Bras Psiquiatr 2011; 33: 268-274.
94. Guloksuz S, Cetin EA, Cetin T, Deniz G, Oral ET, Nutt DJ. Cytokine levels in euthymic bipolar patients. J Affect Disord 2010; 126: 458-462.
95. Brietzke E, Kauer-Sant'Anna M, Teixeira AL, Kapczinski F. Abnormalities in serum chemokine levels in euthymic patients with bipolar disorder. Brain Behav Immun 2009; 23: 1079-1082.
96. Padmos RC, Van Baal GC, Vonk R et al. Genetic and environmental influences on pro-inflammatory monocytes in bipolar disorder: a twin study. Arch Gen Psychiatry 2009; 66: 957-965.
97. Thomas AJ, Davis S, Ferrier IN, Kalaria RN, O'Brien JT. Elevation of cell adhesion molecule immunoreactivity in the anterior cingulate cortex in bipolar disorder. Biol Psychiatry 2004; 55: 652-655.
98. Rao JS, Harry GJ, Rapoport SI, Kim HW. Increased excitotoxicity and neuroinflammatory markers in postmortem frontal cortex from bipolar disorder patients. Mol Psychiatry 2010; 15: 384-392.
99. Foster R, Kandanearatchi A, Beasley C et al. Calprotectin in microglia from frontal cortex is up-regulated in schizophrenia: evidence for an inflammatory process? Eur J Neurosci 2006; 24: 3561-3566.
100. Brown CM, Mulcahey TA, Filipek NC, Wise PM. Production of proinflammatory cytokines and chemokines during neuroinflammation: novel roles for estrogen receptors alpha and beta. Endocrinology 2010; 151: 4916-4925.
101. Tapia-Gonzalez S, Carrero P, Pernia O, Garcia-Segura LM, Diz-Chaves Y. Selective oestrogen receptor (ER) modulators reduce microglia reactivity in vivo after peripheral inflammation: potential role of microglial ERs. J Endocrinol 2008; 198: 219-230.
102. Lewis DK, Johnson AB, Stohlgren S, Harms A, Sohrabji F. Effects of estrogen receptor agonists on regulation of the inflammatory response in astrocytes from young adult and middle-aged female rats. J Neuroimmunol 2008; 195: 47-59.
103. Tenenbaum M, Azab AN, Kaplanski J. Effects of estrogen against LPS-induced inflammation and toxicity in primary rat glial and neuronal cultures. J Endotoxin Res 2007; 13: 158-166.
104. Sunday L, Tran MM, Krause DN, Duckles SP. Estrogen and progestagens differentially modulate vascular proinflammatory factors. Am J Physiol Endocrinol Metab 2006; 291: E261-E267.
105. Dimayuga FO, Reed JL, Carnero GA et al. Estrogen and brain inflammation: effects on microglial expression of MHC, costimulatory molecules and cytokines. J Neuroimmunol 2005; 161: 123-136.
106. Baker AE, Brautigam VM, Watters JJ. Estrogen modulates microglial inflammatory mediator production via interactions with estrogen receptor beta. Endocrinology 2004; 145: 5021-5032.
107. Suuronen T, Nuutinen T, Huuskonen J, Ojala J, Thornell A, Salminen A. Anti-inflammatory effect of selective estrogen receptor modulators (SERMs) in microglial cells. Inflamm Res 2005; 54: 194-203.
108. Marriott LK, Hauss-Wegrzyniak B, Benton RS, Vraniak PD, Wenk GL. Long-term estrogen therapy worsens the behavioral and neuropathological consequences of chronic brain inflammation. Behav Neurosci 2002; 116: 902-911.
109. Morale MC, Serra PA, L'Episcopo F et al. Estrogen, neuroinflammation and neuroprotection in Parkinson's disease: glia dictates resistance versus vulnerability to neurodegeneration. Neuroscience 2006; 138: 869-878.
110. Saijo K, Collier JG, Li AC, Katzenellenbogen JA, Glass CK. An ADIOL-ERbeta-CtBP transrepression pathway negatively regulates microglia-mediated inflammation. Cell 2011; 145: 584-595.
111. Sárvári M, Hrabovszky E, Kalló I et al. Estrogens regulate neuroinflammatory genes via estrogen receptors alpha and beta in the frontal cortex of middle-aged female rats. J Neuroinflammation 2011; 8: 82.
112. Yildiz A, Guleryuz S, Ankerst DP, Ongur D, Renshaw PF. Protein kinase C inhibition in the treatment of mania: a double-blind, placebo-controlled trial of tamoxifen. Arch Gen Psychiatry 2008; 65: 255-263.
113. Amrollahi Z, Rezaei F, Salehi B et al. Double-blind, randomized, placebo-controlled 6-week study on the efficacy and safety of the tamoxifen adjunctive to lithium in acute bipolar mania. J Affect Disord 2011; 129: 327-331.
114. Kulkarni J, Garland KA, Scaffidi A et al. A pilot study of hormone modulation as a new treatment for mania in women with bipolar affective disorder. Psychoneuroendocrinology 2006; 31: 543-547.
115. Frey BN, Macritchie KA, Soares CN, Steiner M. Bipolar disorder in women. In: Yatham LN, Maj M eds. Bipolar Disorder: Clinical and Neurobiological Foundations. West Sussex, UK: John Wiley & Sons, 2010: 463-476.
116. Galimberti CA, Magri F, Copello F et al. Changes in sex steroid levels in women with epilepsy on treatment: relationship with antiepileptic therapies and seizure frequency. Epilepsia 2009; 50 (Suppl. 1): 28-32.
117. Joffe H, Cohen LS, Suppes T et al. Valproate is associated with new-onset oligoamenorrhea with hyperandrogenism in women with bipolar disorder. Biol Psychiatry 2006; 59: 1078-1086.
118. Gosselin D, Rivest S. Estrogen receptor transrepresses brain inflammation. Cell 2011; 145: 495-497.
119. Deurveilher S, Rusak B, Semba K. Estradiol and progesterone modulate spontaneous sleep patterns and recovery from sleep deprivation in ovariectomized rats. Sleep 2009; 32: 865-877.
120. Nakamura TJ, Sellix MT, Menaker M, Block GD. Estrogen directly modulates circadian rhythms of PER2 expression in the uterus. Am J Physiol Endocrinol Metab 2008; 295: E1025-E1031.
121. Zeidan MA, Igoe SA, Linnman C et al. Estradiol modulates medial prefrontal cortex and amygdala activity during fear extinction in women and female rats. Biol Psychiatry 2011; 70: 920-927.
122. Johansson AG, Nikamo P, Schalling M, Landen M. Polymorphisms in AKR1C4 and HSD3B2 and differences in serum DHEAS and progesterone are associated with paranoid ideation during mania or hypomania in bipolar disorder. Eur Neuropsychopharmacol 2012; 22: 632-640.
123. Johansson AG, Nikamo P, Schalling M, Landen M. AKR1C4 gene variant associated with low euthymic serum progesterone and a history of mood irritability in males with bipolar disorder. J Affect Disord 2011; 133: 346-351.
124. El Kihel L. Oxidative metabolism of dehydroepiandrosterone (DHEA) and biologically active oxygenated metabolites of DHEA and epiandrosterone (EpiA)-recent reports. Steroids 2012; 77: 10-26.
125. Gallagher P, Watson S, Smith MS, Young AH, Ferrier IN. Plasma cortisol-dehydroepiandrosterone (DHEA) ratios in schizophrenia and bipolar disorder. Schizophr Res 2007; 90: 258-265.
126. Morfin R, Starka L. Neurosteroid 7-hydroxylation products in the brain. Int Rev Neurobiol 2001; 46: 79-95.
127. Juhasz-Vedres G, Rozsa E, Rakos G et al. Dehydroepiandrosterone sulfate is neuroprotective when administered either before or after injury in a focal cortical cold lesion model. Endocrinology 2006; 147: 683-686.
128. Zheng P. Neuroactive steroid regulation of neurotransmitter release in the CNS: action, mechanism and possible significance. Prog Neurobiol 2009; 89: 134-152.
129. Gottfried-Blackmore A, Sierra A, Jellinck PH, McEwen BS, Bulloch K. Brain microglia express steroid-converting enzymes in the mouse. J Steroid Biochem Mol Biol 2008; 109: 96-107.
130. Chakraborti A, Gulati K, Ray A. Involvement of nitric oxide in the protective effects of dehydroepiandrosterone sulphate on stress induced neurobehavioral suppression and brain oxidative injury in rats. Eur J Pharmacol 2011; 652: 55-59.
131. Pluchino N, Russo M, Santoro AN, Litta P, Cela V, Genazzani AR. Steroid hormones and BDNF. Neuroscience 2013; 239: 271-279.
132. Pompili M, Gibiino S, Innamorati M et al. Prolactin and thyroid hormone levels are associated with suicide attempts in psychiatric patients. Psychiatry Res 2012; 200: 389-394.
133. Sosa L, Gutierrez S, Petiti JP et al. 17beta-Estradiol modulates the prolactin secretion induced by TRH through membrane estrogen receptors via PI3K/Akt in female rat anterior pituitary cell culture. Am J Physiol Endocrinol Metab 2012; 302: E1189-E1197.
134. Hardoy MC, Serra M, Carta MG, Contu P, Pisu MG, Biggio G. Increased neuroactive steroid concentrations in women with bipolar disorder or major depressive disorder. J Clin Psychopharmacol 2006; 26: 379-384.
135. Bäckström T, Haage D, Löfgren M et al. Paradoxical effects of GABA-A modulators may explain sex steroid induced negative mood symptoms in some persons. Neuroscience 2011; 191: 46-54.