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Cognitive Effects of Aromatase and Possible Role in Memory Disorders 원문보기

Frontiers in Endocrinology, v.9, 2018년, pp.610 -   

Rosenfeld, Cheryl S. (Bond Life Sciences Center, University of Missouri , Columbia, MO , United States) ,  Shay, Dusti A. (Nutrition and Exercise Physiology, University of Missouri , Columbia, MO , United States) ,  Vieira-Potter, Victoria J. (Nutrition and Exercise Physiology, University of Missouri , Columbia, MO , United States)

Abstract AI-Helper 아이콘AI-Helper

Diverse cognitive functions in many vertebrate species are influenced by local conversion of androgens to 17β-estradiol (E2) by aromatase. This enzyme is highly expressed in various brain regions across species, with some inter-species variation in terms of regional brain expression. Since wome...

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참고문헌 (207)

  1. 1. Li R Cui J Shen Y . Brain sex matters: estrogen in cognition and Alzheimer's disease . Mol Cell Endocrinol. ( 2014 ) 389 : 13 – 21 . 10.1016/j.mce.2013.12.018 24418360 

  2. 2. Hara Y Waters EM McEwen BS Morrison JH . Estrogen effects on cognitive and synaptic health over the lifecourse . Physiol Rev. ( 2015 ) 95 : 785 – 807 . 10.1152/physrev.00036.2014 26109339 

  3. 3. Abu Hashim H . Potential role of aromatase inhibitors in the treatment of endometriosis . Int J Womens Health ( 2014 ) 6 : 671 – 80 . 10.2147/IJWH.S34684 25092998 

  4. 4. Franik S Kremer JA Nelen WL Farquhar C Aromatase inhibitors for subfertile women with polycystic ovary syndrome . Cochrane Database Syst Rev ( 2014 ). Cd010287 10.1002/14651858.CD010287.pub2 

  5. 5. Klement AH Casper RF . The use of aromatase inhibitors for ovulation induction . Curr Opin Obstet Gynecol. ( 2015 ) 27 : 206 – 9 . 10.1097/GCO.0000000000000163 25710389 

  6. 6. Roque M Tostes AC Valle M Sampaio M Geber S . Letrozole versus clomiphene citrate in polycystic ovary syndrome: systematic review and meta-analysis . Gynecol Endocrinol. ( 2015 ) 31 : 917 – 21 . 10.3109/09513590.2015.1096337 26479460 

  7. 7. Adhikari N Amin SA Saha A Jha T . Combating breast cancer with non-steroidal aromatase inhibitors (NSAIs): Understanding the chemico-biological interactions through comparative SAR/QSAR study . Eur J Med Chem. ( 2017 ) 137 : 365 – 438 . 10.1016/j.ejmech.2017.05.041 28622580 

  8. 8. Daldorff S Mathiesen RM Yri OE Odegard HP Geisler J . Cotargeting of CYP-19 (aromatase) and emerging, pivotal signalling pathways in metastatic breast cancer . Br J Cancer ( 2017 ) 116 : 10 – 20 . 10.1038/bjc.2016.405 27923036 

  9. 9. Goldvaser H Algorashi I Ribnikar D Seruga B Templeton AJ Ocana A . Efficacy of extended adjuvant therapy with aromatase inhibitors in early breast cancer among common clinicopathologically-defined subgroups: a systematic review and meta-analysis . Cancer Treat Rev. ( 2017 ) 60 : 53 – 9 . 10.1016/j.ctrv.2017.08.008 28881223 

  10. 10. Agrawal K Onami S Mortimer JE Pal SK . Cognitive changes associated with endocrine therapy for breast cancer . Maturitas ( 2010 ) 67 : 209 – 14 . 10.1016/j.maturitas.2010.07.004 20688441 

  11. 11. Bian C Zhao Y Guo Q Xiong Y Cai W Zhang J . Aromatase inhibitor letrozole downregulates steroid receptor coactivator-1 in specific brain regions that primarily related to memory, neuroendocrine and integration . J Steroid Biochem Mol Biol. ( 2014 ) 141 : 37 – 43 . 10.1016/j.jsbmb.2013.12.020 24434281 

  12. 12. Frank JS Vance DE Jukkala A Meneses KM . Attention and memory deficits in breast cancer survivors: implications for nursing practice and research . J Neurosci Nurs. ( 2014 ) 46 : 274 – 84 . 10.1097/JNN.0000000000000078 25099062 

  13. 13. Hurria A Patel SK Mortimer J Luu T Somlo G Katheria V . The effect of aromatase inhibition on the cognitive function of older patients with breast cancer . Clin Breast Cancer ( 2014 ) 14 : 132 – 40 . 10.1016/j.clbc.2013.10.010 24291380 

  14. 14. Bender CM Merriman JD Gentry AL Ahrendt GM Berga SL Brufsky AM . Patterns of change in cognitive function with anastrozole therapy . Cancer ( 2015 ) 121 : 2627 – 36 . 10.1002/cncr.29393 25906766 

  15. 15. Karatas F Akin S Babacan T Sever AR Altundag K . Can aromatase inhibitors cause forgetfulness in women with breast cancer? J BUON ( 2015 ) 20 : 935 . 26214652 

  16. 16. Beckwee D Leysen L Meuwis K Adriaenssens N . Prevalence of aromatase inhibitor-induced arthralgia in breast cancer: a systematic review and meta-analysis . Support Care Cancer ( 2017 ) 25 : 1673 – 86 . 10.1007/s00520-017-3613-z 28204994 

  17. 17. Chan A De Boer R Gan A Willsher P Martin R Zissiadis Y . Randomized phase II placebo-controlled study to evaluate the efficacy of topical pure emu oil for joint pain related to adjuvant aromatase inhibitor use in postmenopausal women with early breast cancer: JUST (Joints Under Study) . Support Care Cancer ( 2017 ) 25 : 3785 – 91 . 10.1007/s00520-017-3810-9 28691132 

  18. 18. Fontein DB Charehbili A Nortier JW Putter H Kranenbarg EM Kroep JR . Specific adverse events are associated with response to exemestane therapy in postmenopausal breast cancer patients: results from the TEAMIIA study (BOOG2006-04) . Eur J Surg Oncol. ( 2017 ) 43 : 619 – 24 . 10.1016/j.ejso.2016.07.146 28017458 

  19. 19. Duarte-Guterman P Yagi S Chow C Galea LA . Hippocampal learning, memory, and neurogenesis: effects of sex and estrogens across the lifespan in adults . Horm Behav. ( 2015 ) 74 : 37 – 52 . 10.1016/j.yhbeh.2015.05.024 26122299 

  20. 20. Newhouse P Dumas J . Estrogen-cholinergic interactions: implications for cognitive aging . Horm Behav. ( 2015 ) 74 : 173 – 85 . 10.1016/j.yhbeh.2015.06.022 26187712 

  21. 21. Ycaza Herrera A Mather M . Actions and interactions of estradiol and glucocorticoids in cognition and the brain: implications for aging women . Neurosci Biobehav Rev. ( 2015 ) 55 : 36 – 52 . 10.1016/j.neubiorev.2015.04.005 25929443 

  22. 22. Engler-Chiurazzi EB Brown CM Povroznik JM Simpkins JW . Estrogens as neuroprotectants: estrogenic actions in the context of cognitive aging and brain injury . Prog Neurobiol. ( 2016 ) 157 : 188 – 211 . 10.1016/j.pneurobio.2015.12.008 26891883 

  23. 23. Watson J Adkins-Regan E . Activation of sexual behavior by implantation of testosterone propionate and estradiol benzoate into the preoptic area of the male Japanese quail ( Coturnix japonica ) . Horm Behav. ( 1989 ) 23 : 251 – 68 . 10.1016/0018-506X(89)90065-2 2744741 

  24. 24. Watson J Adkins-Regan E . Testosterone implanted in the preoptic area of male Japanese quail must be aromatized to activate copulation . Horm Behav. ( 1989 ) 23 : 432 – 47 . 10.1016/0018-506X(89)90055-X 2793083 

  25. 25. Bowers JM Waddell J McCarthy MM . A developmental sex difference in hippocampal neurogenesis is mediated by endogenous oestradiol . Biol Sex Differ. ( 2010 ) 1 : 8 . 10.1186/2042-6410-1-8 21208470 

  26. 26. Konkle AT McCarthy MM . Developmental time course of estradiol, testosterone, and dihydrotestosterone levels in discrete regions of male and female rat brain . Endocrinology ( 2011 ) 152 : 223 – 35 . 10.1210/en.2010-0607 21068160 

  27. 27. Arnold AP Breedlove SM . Organizational and activational effects of sex steroids on brain and behavior: a reanalysis . Horm Behav. ( 1985 ) 19 : 469 – 98 . 10.1016/0018-506X(85)90042-X 3910535 

  28. 28. Morris JA Jordan CL Breedlove SM . Sexual differentiation of the vertebrate nervous system . Nat Neurosci. ( 2004 ) 7 : 1034 – 9 . 10.1038/nn1325 15452574 

  29. 29. Fisher CR Graves KH Parlow AF Simpson ER . Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene . Proc Natl Acad Sci USA. ( 1998 ) 95 : 6965 – 70 . 10.1073/pnas.95.12.6965 9618522 

  30. 30. Nemoto Y Toda K Ono M Fujikawa-Adachi K Saibara T Onishi S . Altered expression of fatty acid-metabolizing enzymes in aromatase-deficient mice . J Clin Invest. ( 2000 ) 105 : 1819 – 25 . 10.1172/JCI9575 10862797 

  31. 31. Toda K Takeda K Okada T Akira S Saibara T Kaname T . Targeted disruption of the aromatase P450 gene (Cyp19) in mice and their ovarian and uterine responses to 17beta-oestradiol . J Endocrinol. ( 2001 ) 170 : 99 – 111 . 10.1677/joe.0.1700099 11431142 

  32. 32. Hill RA Boon WC . Estrogens, brain, and behavior: lessons from knockout mouse models . Semin Reprod Med. ( 2009 ) 27 : 218 – 28 . 10.1055/s-0029-1216275 19401953 

  33. 33. Daniel JM . Estrogens, estrogen receptors, and female cognitive aging: the impact of timing . Horm Behav. ( 2013 ) 63 : 231 – 7 . 10.1016/j.yhbeh.2012.05.003 22587940 

  34. 34. Korol DL Pisani SL . Estrogens and cognition: friends or foes? An evaluation of the opposing effects of estrogens on learning and memory . Horm Behav. ( 2015 ) 74 : 105 – 15 . 10.1016/j.yhbeh.2015.06.017 26149525 

  35. 35. Cornil CA . On the role of brain aromatase in females: why are estrogens produced locally when they are available systemically? J Comp Physiol A Neuroethol Sens Neural Behav Physiol. ( 2018 ) 204 : 31 – 49 . 10.1007/s00359-017-1224-2 29086012 

  36. 36. Naftolin F Ryan KJ Petro Z . Aromatization of androstenedione by limbic system tissue from human foetuses . J Endocrinol. ( 1971 ) 51 : 795 – 6 . 10.1677/joe.0.0510795 5138326 

  37. 37. Baum MJ Vreeburg JT . Copulation in castrated male rats following combined treatment with estradiol and dihydrotestosterone . Science ( 1973 ) 182 : 283 – 5 . 10.1126/science.182.4109.283 4742734 

  38. 38. Larsson K Sodersten P Beyer C . Induction of male sexual behaviour by oestradiol benzoate in combination with dihydrotestosterone . J Endocrinol. ( 1973 ) 57 : 563 – 4 . 10.1677/joe.0.0570563 4715730 

  39. 39. Lauber ME Lichtensteiger W . Pre- and postnatal ontogeny of aromatase cytochrome P450 messenger ribonucleic acid expression in the male rat brain studied by in situ hybridization . Endocrinology ( 1994 ) 135 : 1661 – 8 . 10.1210/endo.135.4.7925130 7925130 

  40. 40. Foidart A Reid J Absil P Yoshimura N Harada N Balthazart J Critical re-examination of the distribution of aromatase-immunoreactive cells in the quail forebrain using antibodies raised against human placental aromatase and against the recombinant quail, mouse or human enzyme . J Chem Neuroanat. ( 1995 ) 8 : 267 – 82 . 10.1016/0891-0618(95)00054-B 7669272 

  41. 41. Wagner CK Morrell JI . Distribution and steroid hormone regulation of aromatase mRNA expression in the forebrain of adult male and female rats: a cellular-level analysis using in situ hybridization . J Comp Neurol. ( 1996 ) 370 : 71 – 84 . 10.1002/(SICI)1096-9861(19960617)370:1 3.0.CO;2-I 8797158 

  42. 42. Roselli CE Stormshak F Resko JA . Distribution and regulation of aromatase activity in the ram hypothalamus and amygdala . Brain Res. ( 1998 ) 811 : 105 – 10 . 10.1016/S0006-8993(98)00995-0 9804911 

  43. 43. Saldanha CJ Tuerk MJ Kim YH Fernandes AO Arnold AP Schlinger BA . Distribution and regulation of telencephalic aromatase expression in the zebra finch revealed with a specific antibody . J Comp Neurol. ( 2000 ) 423 : 619 – 30 . 10.1002/1096-9861(20000807)423:4 3.0.CO;2-U 10880992 

  44. 44. Roselli CE Klosterman S Resko JA . Anatomic relationships between aromatase and androgen receptor mRNA expression in the hypothalamus and amygdala of adult male cynomolgus monkeys . J Comp Neurol. ( 2001 ) 439 : 208 – 23 . 10.1002/cne.1343 11596049 

  45. 45. Roselli CE Liu M Hurn PD . Brain aromatization: classic roles and new perspectives . Semin Reprod Med. ( 2009 ) 27 : 207 – 17 . 10.1055/s-0029-1216274 19401952 

  46. 46. Cisternas CD Tome K Caeiro XE Dadam FM Garcia-Segura LM Cambiasso MJ . Sex chromosome complement determines sex differences in aromatase expression and regulation in the stria terminalis and anterior amygdala of the developing mouse brain . Mol Cell Endocrinol. ( 2015 ) 414 : 99 – 110 . 10.1016/j.mce.2015.07.027 26231585 

  47. 47. Balthazart J Foidart A Surlemont C Harada N . Neuroanatomical specificity in the co-localization of aromatase and estrogen receptors . J Neurobiol. ( 1991 ) 22 : 143 – 57 . 10.1002/neu.480220205 2030339 

  48. 48. Veney SL Rissman EF . Co-localization of estrogen receptor and aromatase enzyme immunoreactivities in adult musk shrew brain . Horm Behav. ( 1998 ) 33 : 151 – 62 . 10.1006/hbeh.1998.1446 9698499 

  49. 49. Roselli CE Resko JA . Aromatase activity in the rat brain: hormonal regulation and sex differences . J Steroid Biochem Mol Biol. ( 1993 ) 44 : 499 – 508 . 10.1016/0960-0760(93)90254-T 8476764 

  50. 50. Roselli CE Resko JA . Sex differences in androgen-regulated expression of cytochrome P450 aromatase in the rat brain . J Steroid Biochem Mol Biol. ( 1997 ) 61 : 365 – 74 . 10.1016/S0960-0760(97)80034-9 9365212 

  51. 51. Boon WC Chow JD Simpson ER . The multiple roles of estrogens and the enzyme aromatase . Prog Brain Res. ( 2010 ) 181 : 209 – 32 . 10.1016/S0079-6123(08)81012-6 20478440 

  52. 52. Konkle AT Balthazart J . Sex differences in the rapid control of aromatase activity in the quail preoptic area . J Neuroendocrinol. ( 2011 ) 23 : 424 – 34 . 10.1111/j.1365-2826.2011.02121.x 21366731 

  53. 53. Balthazart J Tlemcani O Harada N . Localization of testosterone-sensitive and sexually dimorphic aromatase-immunoreactive cells in the quail preoptic area . J Chem Neuroanat. ( 1996 ) 11 : 147 – 71 . 10.1016/0891-0618(96)00149-4 8906458 

  54. 54. Voigt C Ball GF Balthazart J . Neuroanatomical specificity of sex differences in expression of aromatase mRNA in the quail brain . J Chem Neuroanat. ( 2007 ) 33 : 75 – 86 . 10.1016/j.jchemneu.2006.12.004 17270396 

  55. 55. Peterson RS Yarram L Schlinger BA Saldanha CJ . Aromatase is pre-synaptic and sexually dimorphic in the adult zebra finch brain . Proc Biol Sci. ( 2005 ) 272 : 2089 – 96 . 10.1098/rspb.2005.3181 16191621 

  56. 56. Rohmann KN Schlinger BA Saldanha CJ . Subcellular compartmentalization of aromatase is sexually dimorphic in the adult zebra finch brain . Dev Neurobiol. ( 2007 ) 67 : 1 – 9 . 10.1002/dneu.20303 17443767 

  57. 57. Abdelgadir SE Roselli CE Choate JV Resko JA . Distribution of aromatase cytochrome P450 messenger ribonucleic acid in adult rhesus monkey brains . Biol Reprod. ( 1997 ) 57 : 772 – 7 . 10.1095/biolreprod57.4.772 9314579 

  58. 58. Dickens MJ Balthazart J Cornil CA . Brain aromatase and circulating corticosterone are rapidly regulated by combined acute stress and sexual interaction in a sex-specific manner . J Neuroendocrinol. ( 2012 ) 24 : 1322 – 34 . 10.1111/j.1365-2826.2012.02340.x 22612582 

  59. 59. Kadioglu P Oral G Sayitoglu M Erensoy N Senel B Gazioglu N . Aromatase cytochrome P450 enzyme expression in human pituitary . Pituitary ( 2008 ) 11 : 29 – 35 . 10.1007/s11102-007-0065-3 17703364 

  60. 60. Sasano H Takashashi K Satoh F Nagura H Harada N . Aromatase in the human central nervous system . Clin Endocrinol. ( 1998 ) 48 : 325 – 9 . 10.1046/j.1365-2265.1998.00390.x 9578823 

  61. 61. Roselli CE Horton LE Resko JA . Time-course and steroid specificity of aromatase induction in rat hypothalamus-preoptic area . Biol Reprod. ( 1987 ) 37 : 628 – 33 . 10.1095/biolreprod37.3.628 3676409 

  62. 62. Balthazart J Foidart A Hendrick JC . The induction by testosterone of aromatase activity in the preoptic area and activation of copulatory behavior . Physiol Behav. ( 1990 ) 47 : 83 – 94 . 10.1016/0031-9384(90)90045-6 2326347 

  63. 63. Balthazart J Schumacher M Evrard L . Sex differences and steroid control of testosterone-metabolizing enzyme activity in the quail brain . J Neuroendocrinol. ( 1990 ) 2 : 675 – 83 . 10.1111/j.1365-2826.1990.tb00464.x 19215405 

  64. 64. Tabatadze N Sato SM Woolley CS . Quantitative analysis of long-form aromatase mRNA in the male and female rat brain . PLoS ONE ( 2014 ) 9 : e100628 . 10.1371/journal.pone.0100628 25036039 

  65. 65. Schumacher M Balthazart J . Testosterone-induced brain aromatase is sexually dimorphic . Brain Res. ( 1986 ) 370 : 285 – 93 . 10.1016/0006-8993(86)90483-X 3708327 

  66. 66. Balthazart J Foidart A Harada N . Immunocytochemical localization of aromatase in the brain . Brain Res. ( 1990 ) 514 : 327 – 33 . 10.1016/0006-8993(90)91428-J 2357545 

  67. 67. Steimer T Hutchison JB . Is androgen-dependent aromatase activity sexually differentiated in the rat and dove preoptic area? J Neurobiol. ( 1990 ) 21 : 787 – 95 . 10.1002/neu.480210512 2394992 

  68. 68. Hutchison RE Wozniak AW Hutchison JB . Regulation of female brain aromatase activity during the reproductive cycle of the dove . J Endocrinol. ( 1992 ) 134 : 385 – 96 . 10.1677/joe.0.1340385 1402546 

  69. 69. Roselli CE Abdelgadir SE Jorgensen E Resko JA . Sex differences in androgen-regulated cytochrome P450 aromatase mRNA in the rat brain . Endocrine ( 1996 ) 5 : 59 – 65 . 10.1007/BF02738657 21153095 

  70. 70. Roselli CE Klosterman SA Fasasi TA . Sex differences in androgen responsiveness in the rat brain: regional differences in the induction of aromatase activity . Neuroendocrinology ( 1996 ) 64 : 139 – 45 . 10.1159/000127111 8857608 

  71. 71. Roselli CE Klosterman SA . Sexual differentiation of aromatase activity in the rat brain: effects of perinatal steroid exposure . Endocrinology ( 1998 ) 139 : 3193 – 201 . 10.1210/endo.139.7.6101 9645693 

  72. 72. Voigt C Ball GF Balthazart J . Effects of sex steroids on aromatase mRNA expression in the male and female quail brain . Gen Comp Endocrinol. ( 2011 ) 170 : 180 – 8 . 10.1016/j.ygcen.2010.10.003 20951703 

  73. 73. Balthazart J Baillien M Ball GF . Phosphorylation processes mediate rapid changes of brain aromatase activity . J Steroid Biochem Mol Biol. ( 2001 ) 79 : 261 – 77 . 10.1016/S0960-0760(01)00143-1 11850233 

  74. 74. Balthazart J Baillien M Charlier TD Cornil CA Ball GF . Multiple mechanisms control brain aromatase activity at the genomic and non-genomic level . J Steroid Biochem Mol Biol. ( 2003 ) 86 : 367 – 79 . 10.1016/S0960-0760(03)00346-7 14623533 

  75. 75. Hojo Y Hattori TA Enami T Furukawa A Suzuki K Ishii HT . Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017alpha and P450 aromatase localized in neurons . Proc Natl Acad Sci USA. ( 2004 ) 101 : 865 – 70 . 10.1073/pnas.2630225100 14694190 

  76. 76. Balthazart J Baillien M Ball GF . Rapid control of brain aromatase activity by glutamatergic inputs . Endocrinology ( 2006 ) 147 : 359 – 66 . 10.1210/en.2005-0845 16195408 

  77. 77. Remage-Healey L Maidment NT Schlinger BA . Forebrain steroid levels fluctuate rapidly during social interactions . Nat Neurosci. ( 2008 ) 11 : 1327 – 34 . 10.1038/nn.2200 18820691 

  78. 78. Balthazart J Charlier TD Cornil CA Dickens MJ Harada N Konkle AT . Sex differences in brain aromatase activity: genomic and non-genomic controls . Front Endocrinol. ( 2011 ) 2 : 34 . 10.3389/fendo.2011.00034 22645508 

  79. 79. Charlier TD Harada N Balthazart J Cornil CA . Human and quail aromatase activity is rapidly and reversibly inhibited by phosphorylating conditions . Endocrinology ( 2011 ) 152 : 4199 – 210 . 10.1210/en.2011-0119 21914772 

  80. 80. Remage-Healey L Dong S Maidment NT Schlinger BA . Presynaptic control of rapid estrogen fluctuations in the songbird auditory forebrain . J Neurosci. ( 2011 ) 31 : 10034 – 8 . 10.1523/JNEUROSCI.0566-11.2011 21734295 

  81. 81. Charlier TD Cornil CA Balthazart J . Rapid modulation of aromatase activity in the vertebrate brain . J Exp Neurosci. ( 2013 ) 7 : 31 – 7 . 10.4137/JEN.S11268 25157205 

  82. 82. Sato SM Woolley CS Acute inhibition of neurosteroid estrogen synthesis suppresses status epilepticus in an animal model . Elife ( 2016 ) 5 : e12917 10.7554/eLife.12917 27083045 

  83. 83. Gerlai R . Behavioral tests of hippocampal function: simple paradigms complex problems . Behav Brain Res. ( 2001 ) 125 : 269 – 77 . 10.1016/S0166-4328(01)00296-0 11682118 

  84. 84. Terry AV Jr Chapter 13: Spatial navigation (water maze) tasks . In: Methods of Behavior Analysis in Neuroscience. Buccafusco JJ editor. Boca Raton, FL : CRC Press; Taylor and Francis Taylor; Francis Group, LLC. ( 2009 ). 

  85. 85. Vorhees CV Williams MT . Value of water mazes for assessing spatial and egocentric learning and memory in rodent basic research and regulatory studies . Neurotoxicol Teratol. ( 2014 ) 45 : 75 – 90 . 10.1016/j.ntt.2014.07.003 25116937 

  86. 86. Arakawa H Iguchi Y . Ethological and multi-behavioral analysis of learning and memory performance in laboratory rodent models . Neurosci Res. ( 2018 ) 135 : 1 – 12 . 10.1016/j.neures.2018.02.001 29432797 

  87. 87. Martin S Jones M Simpson E Van Den Buuse M . Impaired spatial reference memory in aromatase-deficient (ArKO) mice . Neuroreport ( 2003 ) 14 : 1979 – 82 . 10.1097/00001756-200310270-00020 14561933 

  88. 88. Boon WC Diepstraten J Van Der Burg J Jones ME Simpson ER Van Den Buuse M . Hippocampal NMDA receptor subunit expression and watermaze learning in estrogen deficient female mice . Brain Res Mol Brain Res. ( 2005 ) 140 : 127 – 32 . 10.1016/j.molbrainres.2005.07.004 16083992 

  89. 89. Rosenfeld CS Ferguson SA Barnes maze testing strategies with small and large rodent models . J Vis Exp. ( 2014 ) 84 : e51194 10.3791/51194 

  90. 90. Galea LA Kavaliers M Ossenkopp KP . Sexually dimorphic spatial learning in meadow voles Microtus pennsylvanicus and deer mice Peromyscus maniculatus . J Exp Biol. ( 1996 ) 199 : 195 – 200 . 8576690 

  91. 91. Jasarevic E Sieli PT Twellman EE Welsh TH Jr Schachtman TR Roberts RM . Disruption of adult expression of sexually selected traits by developmental exposure to bisphenol A . Proc Natl Acad Sci USA. ( 2011 ) 108 : 11715 – 20 . 10.1073/pnas.1107958108 21709224 

  92. 92. Jasarevic E Williams SA Vandas GM Ellersieck MR Liao C Kannan K . Sex and dose-dependent effects of developmental exposure to bisphenol A on anxiety and spatial learning in deer mice ( Peromyscus maniculatus bairdii) offspring . Horm Behav. ( 2013 ) 63 : 180 – 9 . 10.1016/j.yhbeh.2012.09.009 23051835 

  93. 93. Pierman S Sica M Allieri F Viglietti-Panzica C Panzica GC Bakker J . Activational effects of estradiol and dihydrotestosterone on social recognition and the arginine-vasopressin immunoreactive system in male mice lacking a functional aromatase gene . Horm Behav. ( 2008 ) 54 : 98 – 106 . 10.1016/j.yhbeh.2008.02.001 18346740 

  94. 94. Wesson DW Keller M Douhard Q Baum MJ Bakker J . Enhanced urinary odor discrimination in female aromatase knockout (ArKO) mice . Horm Behav. ( 2006 ) 49 : 580 – 6 . 10.1016/j.yhbeh.2005.12.013 16448653 

  95. 95. Brus M Trouillet AC Hellier V Bakker J . Estradiol-induced neurogenesis in the female accessory olfactory bulb is required for the learning of the male odor . J Neurochem. ( 2016 ) 138 : 457 – 68 . 10.1111/jnc.13677 27216894 

  96. 96. Zhou L Fester L Haghshenas S De Vrese X Von Hacht R Gloger S . Oestradiol-induced synapse formation in the female hippocampus: roles of oestrogen receptor subtypes . J Neuroendocrinol. ( 2014 ) 26 : 439 – 47 . 10.1111/jne.12162 24779550 

  97. 97. Bakker J Baum MJ Slob AK . Neonatal inhibition of brain estrogen synthesis alters adult neural Fos responses to mating and pheromonal stimulation in the male rat . Neuroscience ( 1996 ) 74 : 251 – 60 . 10.1016/0306-4522(96)00096-6 8843090 

  98. 98. Taylor GT Manzella FM Huffman J Cabrera OH Hoffman J . Cognition in female rats after blocking conversion of androgens to estrogens . Horm Behav. ( 2017 ) 90 : 84 – 9 . 10.1016/j.yhbeh.2017.02.011 28257758 

  99. 99. Alejandre-Gomez M Garcia-Segura LM Gonzalez-Burgos I . Administration of an inhibitor of estrogen biosynthesis facilitates working memory acquisition in male rats . Neurosci Res. ( 2007 ) 58 : 272 – 7 . 10.1016/j.neures.2007.03.011 17467093 

  100. 100. Moradpour F Naghdi N Fathollahi Y . Anastrozole improved testosterone-induced impairment acquisition of spatial learning and memory in the hippocampal CA1 region in adult male rats . Behav Brain Res. ( 2006 ) 175 : 223 – 32 . 10.1016/j.bbr.2006.08.037 17018237 

  101. 101. Zameer S Vohora D . Effect of aromatase inhibitors on learning and memory and modulation of hippocampal dickkopf-1 and sclerostin in female mice . Pharmacol Rep. ( 2017 ) 69 : 1300 – 7 . 10.1016/j.pharep.2017.06.002 29128813 

  102. 102. Meng FT Ni RJ Zhang Z Zhao J Liu YJ Zhou JN . Inhibition of oestrogen biosynthesis induces mild anxiety in C57BL/6J ovariectomized female mice . Neurosci Bull. ( 2011 ) 27 : 241 – 50 . 10.1007/s12264-011-1014-8 21788995 

  103. 103. Mennenga SE Koebele SV Mousa AA Alderete TJ Tsang CW Acosta JI Pharmacological blockade of the aromatase enzyme, but not the androgen receptor, reverses androstenedione-induced cognitive impairments in young surgically menopausal rats . Steroids ( 2015 ) 99 : 16 – 25 . 10.1016/j.steroids.2014.08.010 25159107 

  104. 104. Liu M Huangfu X Zhao Y Zhang D Zhang J . Steroid receptor coactivator-1 mediates letrozole induced downregulation of postsynaptic protein PSD-95 in the hippocampus of adult female rats . J Steroid Biochem Mol Biol. ( 2015 ) 154 : 168 – 75 . 10.1016/j.jsbmb.2015.07.011 26223010 

  105. 105. Tuscher JJ Szinte JS Starrett JR Krentzel AA Fortress AM Remage-Healey L . Inhibition of local estrogen synthesis in the hippocampus impairs hippocampal memory consolidation in ovariectomized female mice . Horm Behav. ( 2016 ) 83 : 60 – 7 . 10.1016/j.yhbeh.2016.05.001 27178577 

  106. 106. Nelson BS Black KL Daniel JM . Circulating Estradiol Regulates Brain-derived estradiol via actions at GnRH receptors to impact memory in ovariectomized rats . eNeuro ( 2016 ) 3 . 10.1523/ENEURO.0321-16.2016 28032117 

  107. 107. Phoenix CH Goy RW Gerall AA Young WC . Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig . Endocrinology ( 1959 ) 65 : 369 – 82 . 10.1210/endo-65-3-369 14432658 

  108. 108. Remage-Healey L Dong SM Chao A Schlinger BA . Sex-specific, rapid neuroestrogen fluctuations and neurophysiological actions in the songbird auditory forebrain . J Neurophysiol. ( 2012 ) 107 : 1621 – 31 . 10.1152/jn.00749.2011 22190616 

  109. 109. Bailey DJ Saldanha CJ . The importance of neural aromatization in the acquisition, recall, and integration of song and spatial memories in passerines . Horm Behav. ( 2015 ) 74 : 116 – 24 . 10.1016/j.yhbeh.2015.06.007 26122300 

  110. 110. Comito D Pradhan DS Karleen BJ Schlinger BA . Region-specific rapid regulation of aromatase activity in zebra finch brain . eNeuro ( 2015 ) 136 : 1177 – 85 . 10.1111/jnc.13513 26709964 

  111. 111. De Groof G Balthazart J Topography and lateralized effect of acute aromatase inhibition on auditory processing in a seasonal songbird . J Neurosci . ( 2017 ) 37 : 4243 – 4254 . 10.1523/JNEUROSCI.1961-16.2017 28314822 

  112. 112. Vahaba DM Macedo-Lima M . Sensory coding and sensitivity to local estrogens shift during critical period milestones in the auditory cortex of male songbirds . eNeuro ( 2017 ) 4 . 10.1523/ENEURO.0317-17.2017 29255797 

  113. 113. Yoder KM Lu K Vicario DS . Blocking estradiol synthesis affects memory for songs in auditory forebrain of male zebra finches . Neuroreport ( 2012 ) 23 : 922 – 6 . 10.1097/WNR.0b013e3283588b61 22955141 

  114. 114. Calisi RM Knudsen DP Krause JS Wingfield JC Gentner TQ . Estradiol differentially affects auditory recognition and learning according to photoperiodic state in the adult male songbird, European starling ( Sturnus vulgaris ) . PeerJ ( 2013 ) 1 : e150 . 10.7717/peerj.150 24058881 

  115. 115. Alward BA De Bournonville C Chan TT Balthazart J Cornil CA Ball GF . Aromatase inhibition rapidly affects in a reversible manner distinct features of birdsong . Sci Rep. ( 2016 ) 6 : 32344 . 10.1038/srep32344 27573712 

  116. 116. Fusani L Metzdorf R Hutchison JB Gahr M . Aromatase inhibition affects testosterone-induced masculinization of song and the neural song system in female canaries . J Neurobiol. ( 2003 ) 54 : 370 – 9 . 10.1002/neu.10141 12500312 

  117. 117. Merten MD Stocker-Buschina S . Fadrozole induces delayed effects on neurons in the zebra finch song system . Brain Res. ( 1995 ) 671 : 317 – 20 . 10.1016/0006-8993(94)01370-W 7743222 

  118. 118. Wade J Arnold AP Post-hatching inhibition of aromatase activity does not alter sexual differentiation of the zebra finch song system . Brain Res. ( 1994 ) 639 : 347 – 50 . 10.1016/0006-8993(94)91752-3 8205488 

  119. 119. Gong A Freking FW Wingfield J Schlinger BA Arnold AP . Effects of embryonic treatment with fadrozole on phenotype of gonads, syrinx, and neural song system in zebra finches . Gen Comp Endocrinol. ( 1999 ) 115 : 346 – 53 . 10.1006/gcen.1999.7318 10480985 

  120. 120. Bailey DJ Makeyeva YV Paitel ER Pedersen AL Hon AT Gunderson JA . Hippocampal aromatization modulates spatial memory and characteristics of the synaptic membrane in the male zebra finch . Endocrinology ( 2017 ) 158 : 852 – 9 . 10.1210/en.2016-1692 28324066 

  121. 121. Rensel MA Ellis JM Harvey B Schlinger BA . Sex, estradiol, and spatial memory in a food-caching corvid . Horm Behav. ( 2015 ) 75 : 45 – 54 . 10.1016/j.yhbeh.2015.07.022 26232613 

  122. 122. Rensel MA Salwiczek L Roth J Schlinger BA . Context-specific effects of estradiol on spatial learning and memory in the zebra finch . Neurobiol Learn Mem. ( 2013 ) 100 : 41 – 7 . 10.1016/j.nlm.2012.12.005 23257279 

  123. 123. Kravitz HM Meyer PM Seeman TE Greendale GA Sowers MR . Cognitive functioning and sex steroid hormone gene polymorphisms in women at midlife . Am J Med. ( 2006 ) 119 : S94 – 102 . 10.1016/j.amjmed.2006.07.030 16949394 

  124. 124. Chew SJ Mello C Nottebohm F Jarvis E Vicario DS . Decrements in auditory responses to a repeated conspecific song are long-lasting and require two periods of protein synthesis in the songbird forebrain . Proc Natl Acad Sci USA. ( 1995 ) 92 : 3406 – 10 . 10.1073/pnas.92.8.3406 7724575 

  125. 125. Mello C Nottebohm F Clayton D . Repeated exposure to one song leads to a rapid and persistent decline in an immediate early gene's response to that song in zebra finch telencephalon . J Neurosci. ( 1995 ) 15 : 6919 – 25 . 10.1523/JNEUROSCI.15-10-06919.1995 7472448 

  126. 126. Anthoni H Sucheston LE Lewis BA Tapia-Paez I Fan X Zucchelli M . The aromatase gene CYP19A1: several genetic and functional lines of evidence supporting a role in reading, speech and language . Behav Genet. ( 2012 ) 42 : 509 – 27 . 10.1007/s10519-012-9532-3 22426781 

  127. 127. Butler HT Warden DR Hogervorst E Ragoussis J Smith AD Lehmann DJ . Association of the aromatase gene with Alzheimer's disease in women . Neurosci Lett. ( 2010 ) 468 : 202 – 6 . 10.1016/j.neulet.2009.10.089 19879925 

  128. 128. Linardi A Damiani D Longui CA . The use of aromatase inhibitors in boys with short stature: what to know before prescribing? Arch Endocrinol Metab. ( 2017 ) 61 : 391 – 7 . 10.1590/2359-3997000000284 28977209 

  129. 129. Haas J Casper RF In vitro fertilization treatments with the use of clomiphene citrate or letrozole . Fertil Steril. ( 2017 ) 108 : 568 – 71 . 10.1016/j.fertnstert.2017.08.017 28965550 

  130. 130. Shippen ER West WJ Jr . Successful treatment of severe endometriosis in two premenopausal women with an aromatase inhibitor . Fertil Steril. ( 2004 ) 81 : 1395 – 8 . 10.1016/j.fertnstert.2003.11.027 15136110 

  131. 131. Biri A Korucuoglu U Zumrutbas N Tiras B Guner H . Intravenous leiomyomatosis treated with aromatase inhibitor therapy . Int J Gynaecol Obstet. ( 2008 ) 101 : 299 – 300 . 10.1016/j.ijgo.2007.12.002 18280477 

  132. 132. Mehta A Clearman T Paduch DA . Safety and efficacy of testosterone replacement therapy in adolescents with Klinefelter syndrome . J Urol. ( 2014 ) 191 : 1527 – 31 . 10.1016/j.juro.2013.09.015 24679877 

  133. 133. Hero M Maury S Luotoniemi E Service E Dunkel L . Cognitive effects of aromatase inhibitor therapy in peripubertal boys . Eur J Endocrinol. ( 2010 ) 163 : 149 – 55 . 10.1530/EJE-10-0040 20421333 

  134. 134. Gerard C Brown KA . Obesity and breast cancer - Role of estrogens and the molecular underpinnings of aromatase regulation in breast adipose tissue . Mol Cell Endocrinol . ( 2017 ) 466 : 15 – 30 . 10.1016/j.mce.2017.09.014 28919302 

  135. 135. Wang X Simpson ER Brown KA . Aromatase overexpression in dysfunctional adipose tissue links obesity to postmenopausal breast cancer . J Steroid Biochem Mol Biol. ( 2015 ) 153 : 35 – 44 . 10.1016/j.jsbmb.2015.07.008 26209254 

  136. 136. Simpson ER Brown KA . Obesity and breast cancer: role of inflammation and aromatase . J Mol Endocrinol. ( 2013 ) 51 : T51 – 9 . 10.1210/me.2013-1011 24163427 

  137. 137. Ioannides SJ Barlow PL Elwood JM Porter D . Effect of obesity on aromatase inhibitor efficacy in postmenopausal, hormone receptor-positive breast cancer: a systematic review . Breast Cancer Res Treat. ( 2014 ) 147 : 237 – 48 . 10.1007/s10549-014-3091-7 25119728 

  138. 138. Gallicchio L Calhoun C Helzlsouer K . A prospective study of aromatase inhibitor therapy initiation and self-reported side effects . Support Care Cancer ( 2017 ) 25 : 2697 – 705 . 10.1007/s00520-017-3678-8 28341972 

  139. 139. Le Rhun E Delbeuck X Lefeuvre-Plesse C Kramar A Skrobala E Pasquier F . A phase III randomized multicenter trial evaluating cognition in post-menopausal breast cancer patients receiving adjuvant hormonotherapy . Breast Cancer Res Treat. ( 2015 ) 152 : 569 – 80 . 10.1007/s10549-015-3493-1 26160250 

  140. 140. Hertz DL Henry NL Rae JM . Germline genetic predictors of aromatase inhibitor concentrations, estrogen suppression and drug efficacy and toxicity in breast cancer patients . Pharmacogenomics ( 2017 ) 18 : 481 – 99 . 10.2217/pgs-2016-0205 28346074 

  141. 141. Schilder CM Eggens PC Seynaeve C Linn SC Boogerd W Gundy CM . Neuropsychological functioning in postmenopausal breast cancer patients treated with tamoxifen or exemestane after AC-chemotherapy: cross-sectional findings from the neuropsychological TEAM-side study . Acta Oncol. ( 2009 ) 48 : 76 – 85 . 10.1080/02841860802314738 18777410 

  142. 142. Phillips KA Aldridge J Ribi K Sun Z Thompson A Harvey V Cognitive function in postmenopausal breast cancer patients one year after completing adjuvant endocrine therapy with letrozole and/or tamoxifen in the BIG 1-98 trial . Breast Cancer Res Treat. ( 2011 ) 126 : 221 – 6 . 10.1007/s10549-010-1235-y 21046229 

  143. 143. Ganz PA Petersen L Bower JE Crespi CM . Impact of adjuvant endocrine therapy on quality of lLife and symptoms: observational data over 12 months from the mind-body study . J Clin Oncol. ( 2016 ) 34 : 816 – 24 . 10.1200/JCO.2015.64.3866 26786934 

  144. 144. Shah S Bell RJ Savage G Goldstat R Papalia MA Kulkarni J . Testosterone aromatization and cognition in women: a randomized, placebo-controlled trial . Menopause ( 2006 ) 13 : 600 – 8 . 10.1097/01.gme.0000227333.50867.4e 16837882 

  145. 145. Kwan ML Roh JM Laurent CA Lee J Tang L Hershman D . Patterns and reasons for switching classes of hormonal therapy among women with early-stage breast cancer . Cancer Causes Control ( 2017 ) 28 : 557 – 62 . 10.1007/s10552-017-0888-9 28349440 

  146. 146. Underwood EA Rochon PA Moineddin R Lee PE Wu W Pritchard KI . Cognitive sequelae of endocrine therapy in women treated for breast cancer: a meta-analysis . Breast Cancer Res Treat . ( 2018 ) 168 : 299 – 310 . 10.1007/s10549-017-4627-4 29264751 

  147. 147. Shilling V Jenkins V Fallowfield L Howell T . The effects of hormone therapy on cognition in breast cancer . J Steroid Biochem Mol Biol. ( 2003 ) 86 : 405 – 12 . 10.1016/j.jsbmb.2003.07.001 14623538 

  148. 148. Jenkins V Shilling V Fallowfield L Howell A Hutton S . Does hormone therapy for the treatment of breast cancer have a detrimental effect on memory and cognition? A pilot study . Psychooncology ( 2004 ) 13 : 61 – 6 . 10.1002/pon.709 14745746 

  149. 149. Rocha-Cadman X Massie MJ Du Hamel K . Aromatase inhibitors and mood disturbances . Palliat Support Care ( 2012 ) 10 : 225 – 7 . 10.1017/S1478951512000636 22677000 

  150. 150. Jenkins VA Ambroisine LM Atkins L Cuzick J Howell A Fallowfield LJ . Effects of anastrozole on cognitive performance in postmenopausal women: a randomised, double-blind chemoprevention trial (IBIS II) . Lancet Oncol. ( 2008 ) 9 : 953 – 61 . 10.1016/S1470-2045(08)70207-9 18768369 

  151. 151. Li C Zhou C Li R . Can exercise ameliorate aromatase inhibitor-induced cognitive decline in breast cancer pPatients? Mol Neurobiol. ( 2016 ) 53 : 4238 – 46 . 10.1007/s12035-015-9341-9 26223800 

  152. 152. Barha CK Falck RS Davis JC Nagamatsu LS Liu-Ambrose T . Sex differences in aerobic exercise efficacy to improve cognition: a systematic review and meta-analysis of studies in older rodents . Front Neuroendocrinol. ( 2017 ) 46 : 86 – 105 . 10.1016/j.yfrne.2017.06.001 28614695 

  153. 153. Brown JC Mao JJ Stricker C Hwang WT Tan KS Schmitz KH . Aromatase inhibitor associated musculoskeletal symptoms are associated with reduced physical activity among breast cancer survivors . Breast J. ( 2014 ) 20 : 22 – 8 . 10.1111/tbj.12202 24165356 

  154. 154. Evrard HC Balthazart J . Rapid regulation of pain by estrogens synthesized in spinal dorsal horn neurons . J Neurosci. ( 2004 ) 24 : 7225 – 9 . 10.1523/JNEUROSCI.1638-04.2004 15317848 

  155. 155. Ghorbanpoor S Garcia-Segura LM Haeri-Rohani A Khodagholi F Jorjani M . Aromatase inhibition exacerbates pain and reactive gliosis in the dorsal horn of the spinal cord of female rats caused by spinothalamic tract injury . Endocrinology ( 2014 ) 155 : 4341 – 55 . 10.1210/en.2014-1158 25105782 

  156. 156. O'brien EE Smeester BA Michlitsch KS Lee JH Beitz AJ . Colocalization of aromatase in spinal cord astrocytes: differences in expression and relationship to mechanical and thermal hyperalgesia in murine models of a painful and a non-painful bone tumor . Neuroscience ( 2015 ) 301 : 235 – 45 . 10.1016/j.neuroscience.2015.06.009 26071956 

  157. 157. Choi HS Lee MJ Choi SR Smeester BA Beitz AJ Lee JH . Spinal sigma-1 receptor-mediated dephosphorylation of astrocytic aromatase plays a key role in formalin-induced inflammatory nociception . Neuroscience ( 2018 ) 372 : 181 – 91 . 10.1016/j.neuroscience.2017.12.031 29289721 

  158. 158. Fusi C Materazzi S Benemei S Coppi E Trevisan G Marone IM . Steroidal and non-steroidal third-generation aromatase inhibitors induce pain-like symptoms via TRPA1 . Nat Commun. ( 2014 ) 5 : 5736 . 10.1038/ncomms6736 25484020 

  159. 159. Robarge JD Duarte DB Shariati B Wang R Flockhart DA Vasko MR . Aromatase inhibitors augment nociceptive behaviors in rats and enhance the excitability of sensory neurons . Exp Neurol. ( 2016 ) 281 : 53 – 65 . 10.1016/j.expneurol.2016.04.006 27072527 

  160. 160. Xu P Cao X He Y Zhu L Yang Y Saito K . Estrogen receptor-alpha in medial amygdala neurons regulates body weight . J Clin Invest. ( 2015 ) 125 : 2861 – 76 . 10.1172/JCI80941 26098212 

  161. 161. Giles ED Jackman MR Johnson GC Schedin PJ Houser JL MacLean PS . Effect of the estrous cycle and surgical ovariectomy on energy balance, fuel utilization, and physical activity in lean and obese female rats . Am J Physiol Regul Integr Comp Physiol. ( 2010 ) 299 : R1634 – 1642 . 10.1152/ajpregu.00219.2010 20926768 

  162. 162. Bowen RS Ferguson DP Lightfoot JT . Effects of aromatase inhibition on the physical activity levels of male mice . J Steroids Horm Sci. ( 2011 ) 1 : 1 – 7 . 10.4172/2157-7536.S1-001 23483029 

  163. 163. Jones ME Thorburn AW Britt KL Hewitt KN Wreford NG Proietto J . Aromatase-deficient (ArKO) mice have a phenotype of increased adiposity . Proc Natl Acad Sci USA. ( 2000 ) 97 : 12735 – 40 . 10.1073/pnas.97.23.12735 11070087 

  164. 164. De Paulo TRS Viezel J Aro BL Seidinger SC Trindade A Christofaro DGD Relationship between physical activity practice and metabolic profile of postmenopausal women under treatment with aromatase inhibitors for breast cancer . Eur J Obstet Gynecol Reprod Biol. ( 2017 ) 216 : 33 – 7 . 10.1016/j.ejogrb.2017.07.003 28700959 

  165. 165. Raichlen DA Alexander GE . Adaptive capacity: an evolutionary neuroscience model linking exercise, cognition, and brain health . Trends Neurosci. ( 2017 ) 40 : 408 – 21 . 10.1016/j.tins.2017.05.001 28610948 

  166. 166. Nichol K Deeny SP Seif J Camaclang K Cotman CW . Exercise improves cognition and hippocampal plasticity in APOE epsilon4 mice . Alzheimers Dement. ( 2009 ) 5 : 287 – 94 . 10.1016/j.jalz.2009.02.006 19560099 

  167. 167. Lafenetre P Leske O Ma-Hogemeie Z Haghikia A Bichler Z Wahle P . Exercise can rescue recognition memory impairment in a model with reduced adult hippocampal neurogenesis . Front Behav Neurosci. ( 2010 ) 3 : 34 . 10.3389/neuro.08.034.2009 20204139 

  168. 168. Kobilo T Yuan C Van Praag H . Endurance factors improve hippocampal neurogenesis and spatial memory in mice . Learn Mem. ( 2011 ) 18 : 103 – 7 . 10.1101/lm.2001611 21245211 

  169. 169. 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 – 20 . 10.1016/j.brainres.2007.02.093 17433270 

  170. 170. Sellers KJ Erli F Raval P Watson IA Chen D Srivastava DP . Rapid modulation of synaptogenesis and spinogenesis by 17β-estradiol in primary cortical neurons . Front Cell Neurosci. ( 2015 ) 9 : 137 . 10.3389/fncel.2015.00137 25926772 

  171. 171. McEwen BS . Sex, stress and the brain: interactive actions of hormones on the developing and adult brain . Climacteric ( 2014 ) 17 ( Suppl. 2 ): 18 – 25 . 10.3109/13697137.2014.949662 25225752 

  172. 172. Dominguez R Zitting M Liu Q Patel A Babadjouni R Hodis DM . Estradiol protects white matter of male C57BL6J mice against experimental chronic cerebral hypoperfusion . J Stroke Cerebrovasc Dis. ( 2018 ) 27 : 1743 – 51 . 10.1016/j.jstrokecerebrovasdis.2018.01.030 29602614 

  173. 173. Kretz O Fester L Wehrenberg U Zhou L Brauckmann S Zhao S . Hippocampal synapses depend on hippocampal estrogen synthesis . J Neurosci. ( 2004 ) 24 : 5913 – 21 . 10.1523/JNEUROSCI.5186-03.2004 15229239 

  174. 174. Prange-Kiel J Rune GM . Direct and indirect effects of estrogen on rat hippocampus . Neuroscience ( 2006 ) 138 : 765 – 72 . 10.1016/j.neuroscience.2005.05.061 16324798 

  175. 175. Fester L Brandt N Windhorst S Prols F Blaute C Rune GM . Control of aromatase in hippocampal neurons . J Steroid Biochem Mol Biol. ( 2016 ) 160 : 9 – 14 . 10.1016/j.jsbmb.2015.10.009 26472556 

  176. 176. Bauml J Chen L Chen J Boyer J Kalos M Li SQ . Arthralgia among women taking aromatase inhibitors: is there a shared inflammatory mechanism with co-morbid fatigue and insomnia? Breast Cancer Res. ( 2015 ) 17 : 89 . 10.1186/s13058-015-0599-7 26126656 

  177. 177. Hershman DL Loprinzi C Schneider BP . Symptoms: Aromatase inhibitor induced arthralgias . Adv Exp Med Biol. ( 2015 ) 862 : 89 – 100 . 10.1007/978-3-319-16366-6_7 26059931 

  178. 178. Irwin ML Cartmel B Gross CP Ercolano E Li F Yao X . Randomized exercise trial of aromatase inhibitor-induced arthralgia in breast cancer survivors . J Clin Oncol. ( 2015 ) 33 : 1104 – 11 . 10.1200/JCO.2014.57.1547 25452437 

  179. 179. Thomas GA Cartmel B Harrigan M Fiellin M Capozza S Zhou Y . The effect of exercise on body composition and bone mineral density in breast cancer survivors taking aromatase inhibitors . Obesity ( 2017 ) 25 : 346 – 51 . 10.1002/oby.21729 28026901 

  180. 180. Gentry AL Erickson KI Sereika SM Casillo FE Crisafio ME Donahue PT . Protocol for exercise program in cancer and cognition (EPICC): a randomized controlled trial of the effects of aerobic exercise on cognitive function in postmenopausal women with breast cancer receiving aromatase inhibitor therapy . Contemp Clin Trials ( 2018 ) 67 : 109 – 15 . 10.1016/j.cct.2018.02.012 29501739 

  181. 181. Janicki SC Park N Cheng R Schupf N Clark LN Lee JH . Aromatase variants modify risk for Alzheimer's disease in a multiethnic female cohort . Dement Geriatr Cogn Disord. ( 2013 ) 35 : 340 – 6 . 10.1159/000343074 23635391 

  182. 182. Iivonen S Corder E Lehtovirta M Helisalmi S Mannermaa A Vepsalainen S . Polymorphisms in the CYP19 gene confer increased risk for Alzheimer disease . Neurology ( 2004 ) 62 : 1170 – 6 . 10.1212/01.WNL.0000118208.16939.60 15079018 

  183. 183. Combarros O Riancho JA Infante J Sanudo C Llorca J Zarrabeitia MT . Interaction between CYP19 aromatase and butyrylcholinesterase genes increases Alzheimer's disease risk . Dement Geriatr Cogn Disord. ( 2005 ) 20 : 153 – 7 . 10.1159/000087065 16020944 

  184. 184. Huang R Poduslo SE . CYP19 haplotypes increase risk for Alzheimer's disease . J Med Genet. ( 2006 ) 43 : e42 . 10.1136/jmg.2005.039461 16882736 

  185. 185. Combarros O Sanchez-Juan P Riancho JA Mateo I Rodriguez-Rodriguez E Infante J . Aromatase and interleukin-10 genetic variants interactively modulate Alzheimer's disease risk . J Neural Transm. ( 2008 ) 115 : 863 – 7 . 10.1007/s00702-008-0028-5 18299793 

  186. 186. Corbo RM Gambina G Ulizzi L Moretto G Scacchi R . Genetic variation of CYP19 (aromatase) gene influences age at onset of Alzheimer's disease in women . Dement Geriatr Cogn Disord. ( 2009 ) 27 : 513 – 8 . 10.1159/000221832 19478482 

  187. 187. Chace C Pang D Weng C Temkin A Lax S Silverman W . Variants in CYP17 and CYP19 cytochrome P450 genes are associated with onset of Alzheimer's disease in women with down syndrome . J Alzheimers Dis. ( 2012 ) 28 : 601 – 12 . 10.3233/JAD-2011-110860 22057025 

  188. 188. Medway C Combarros O Cortina-Borja M Butler HT Ibrahim-Verbaas CA De Bruijn RF . The sex-specific associations of the aromatase gene with Alzheimer's disease and its interaction with IL10 in the Epistasis Project . Eur J Hum Genet. ( 2014 ) 22 : 216 – 20 . 10.1038/ejhg.2013.116 23736221 

  189. 189. Zheng J Yan H Shi L Kong Y Zhao Y Xie L . The CYP19A1 rs3751592 variant confers susceptibility to Alzheimer disease in the Chinese Han population . Medicine ( 2016 ) 95 : e4742 . 10.1097/MD.0000000000004742 27583919 

  190. 190. Prange-Kiel J Dudzinski DA Prols F Glatzel M Matschke J Rune GM . Aromatase expression in the hippocampus of AD patients and 5xFAD mice . Neural Plast. ( 2016 ) 2016 : 11 . 10.1155/2016/9802086 27298742 

  191. 191. Overk CR Lu PY Wang YT Choi J Shaw JW Thatcher GR . Effects of aromatase inhibition versus gonadectomy on hippocampal complex amyloid pathology in triple transgenic mice . Neurobiol Dis. ( 2012 ) 45 : 479 – 87 . 10.1016/j.nbd.2011.08.035 21945538 

  192. 192. Prat A Behrendt M Marcinkiewicz E Boridy S Sairam RM Seidah NG . A novel mouse model of Alzheimer's disease with chronic estrogen deficiency leads to glial cell activation and hypertrophy . J Aging Res. ( 2011 ) 2011 : 251517 . 10.4061/2011/251517 21969914 

  193. 193. Yue X Lu M Lancaster T Cao P Honda S Staufenbiel M . Brain estrogen deficiency accelerates Abeta plaque formation in an Alzheimer's disease animal model . Proc Natl Acad Sci USA. ( 2005 ) 102 : 19198 – 203 . 10.1073/pnas.0505203102 16365303 

  194. 194. Li R He P Cui J Staufenbiel M Harada N Shen Y . Brain endogenous estrogen levels determine responses to estrogen replacement therapy via regulation of BACE1 and NEP in female Alzheimer's transgenic mice . Mol Neurobiol. ( 2013 ) 47 : 857 – 67 . 10.1007/s12035-012-8377-3 23180279 

  195. 195. McAllister C Long J Bowers A Walker A Cao P Honda S . Genetic targeting aromatase in male amyloid precursor protein transgenic mice down-regulates beta-secretase (BACE1) and prevents Alzheimer-like pathology and cognitive impairment . J Neurosci. ( 2010 ) 30 : 7326 – 34 . 10.1523/JNEUROSCI.1180-10.2010 20505099 

  196. 196. Clarke R Smith AD Jobst KA Refsum H Sutton L Ueland PM . Folate, vitamin B12, and serum total homocysteine levels in confirmed Alzheimer disease . Arch Neurol. ( 1998 ) 55 : 1449 – 55 . 10.1001/archneur.55.11.1449 9823829 

  197. 197. Ishunina TA Van Beurden D Van Der Meulen G Unmehopa UA Hol EM Huitinga I Diminished aromatase immunoreactivity in the hypothalamus, but not in the basal forebrain nuclei in Alzheimer's disease . Neurobiol Aging ( 2005 ) 26 : 173 – 94 . 10.1016/j.neurobiolaging.2004.03.010 15582747 

  198. 198. Ishunina TA Fischer DF Swaab DF . Estrogen receptor alpha and its splice variants in the hippocampus in aging and Alzheimer's disease . Neurobiol Aging ( 2007 ) 28 : 1670 – 81 . 10.1016/j.neurobiolaging.2006.07.024 17010478 

  199. 199. Wozniak A Hutchison RE Morris CM Hutchison JB . Neuroblastoma and Alzheimer's disease brain cells contain aromatase activity . Steroids ( 1998 ) 63 : 263 – 7 . 10.1016/S0039-128X(98)00029-4 9618782 

  200. 200. Luchetti S Bossers K Van De Bilt S Agrapart V Morales RR Frajese GV . Neurosteroid biosynthetic pathways changes in prefrontal cortex in Alzheimer's disease . Neurobiol Aging ( 2011 ) 32 : 1964 – 76 . 10.1016/j.neurobiolaging.2009.12.014 20045216 

  201. 201. Honda S Harada N Ito S Takagi Y Maeda S . Disruption of sexual behavior in male aromatase-deficient mice lacking exons 1 and 2 of the cyp19 gene . Biochem Biophys Res Commun. ( 1998 ) 252 : 445 – 9 . 10.1006/bbrc.1998.9672 9826549 

  202. 202. Bakker J Honda S Harada N Balthazart J . Restoration of male sexual behavior by adult exogenous estrogens in male aromatase knockout mice . Horm Behav. ( 2004 ) 46 : 1 – 10 . 10.1016/j.yhbeh.2004.02.003 15215036 

  203. 203. Farman HH Windahl SH Westberg L Isaksson H Egecioglu E Schele E . Female mice lacking estrogen receptor-alpha in hypothalamic proopiomelanocortin (POMC) neurons display enhanced estrogenic response on cortical bone mass . Endocrinology ( 2016 ) 157 : 3242 – 52 . 10.1210/en.2016-1181 27254004 

  204. 204. Nakata M Sano K Musatov S Yamaguchi N Sakamoto T Ogawa S . Effects of prepubertal or adult site-specific knockdown of estrogen receptor β in the medial preoptic area and medial amygdala on social behaviors in male mice . eNeuro ( 2016 ) 3 . 10.1523/ENEURO.0155-15.2016 27066533 

  205. 205. Sano K Nakata M Musatov S Morishita M Sakamoto T Tsukahara S . Pubertal activation of estrogen receptor alpha in the medial amygdala is essential for the full expression of male social behavior in mice . Proc Natl Acad Sci USA. ( 2016 ) 113 : 7632 – 7 . 10.1073/pnas.1524907113 27325769 

  206. 206. Kesslak JP Can estrogen play a significant role in the prevention of Alzheimer's disease? J Neural Transm Suppl. ( 2002 ) 62 : 227 – 39 . 10.1007/978-3-7091-6139-5_21 

  207. 207. Garcia-Segura LM Wozniak A Azcoitia I Rodriguez JR Hutchison RE Hutchison JB . Aromatase expression by astrocytes after brain injury: implications for local estrogen formation in brain repair . Neuroscience ( 1999 ) 89 : 567 – 78 . 10.1016/S0306-4522(98)00340-6 10077336 

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