Estrogen synthesis in the hippocampus

Cell and Tissue Research

Volumn 345, Issue 3, 2011, Pages 285-294

  Fester, Lars ^a   Prange Kiel, Janine ^b   Jarry, Hubertus ^c   Rune, Gabriele M ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Aromatase; Estrogen synthesis; Hippocampus; StAR; Synaptic plasticity

Indexed keywords

AROMATASE; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; GONADORELIN; LETROZOLE; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PRASTERONE; SMALL INTERFERING RNA; STEROIDOGENIC ACUTE REGULATORY PROTEIN;

BRAIN FUNCTION; CELL ACTIVITY; CELL FUNCTION; ENZYME ACTIVITY; ESTROGEN RELEASE; ESTROGEN RESPONSIVE ELEMENT; ESTROGEN SYNTHESIS; HIPPOCAMPUS; HORMONAL REGULATION; HORMONE DETERMINATION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NERVE CELL PLASTICITY; NEUROMODULATION; NEUROPROTECTION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

ANIMALS; AROMATASE; ESTROGENS; HIPPOCAMPUS; HUMANS; NEURONS;

EID: 80052736684     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-011-1221-7     Document Type: Review

References (92)

1. SE Abdelgadir JA Resko SR Ojeda ED Lephart MJ McPhaul CE Roselli 1994 Androgens regulate aromatase cytochrome P450 messenger ribonucleic acid in rat brain Endocrinology 135 395 401 8013375 10.1210/en.135.1.395 1:STN:280:DyaK2c3otlartA%3D%3D (Pubitemid 24203843)
2. MM Adams SE Fink WG Janssen RA Shah JH Morrison 2004 Estrogen modulates synaptic N-methyl-D-aspartate receptor subunit distribution in the aged hippocampus J Comp Neurol 474 419 426 15174084 10.1002/cne.20148 1:CAS:528:DC%2BD2cXlsFCmsLk%3D (Pubitemid 38720435)
3. MA Arevalo M Santos-Galindo MJ Bellini I Azcoitia LM Garcia-Segura 2010 Actions of estrogens on glial cells: implications for neuroprotection Biochim Biophys Acta 1800 1106 1112 19818384 1:CAS:528:DC%2BC3cXhtV2isbbF
4. I Azcoitia A Sierra LM Garcia-Segura 1999 Neuroprotective effects of estradiol in the adult rat hippocampus: interaction with insulin-like growth factor-I signalling J Neurosci Res 58 815 822 10583912 10.1002/(SICI)1097- 4547(19991215)58:6<815::AID-JNR8>3.0.CO;2-R 1:CAS:528:DyaK1MXnvF2gs7Y%3D
5. J Balthazart GF Ball 2006 Is brain estradiol a hormone or a neurotransmitter? Trends Neurosci 29 241 249 16580076 10.1016/j.tins.2006.03.004 1:CAS:528:DC%2BD28XktVehtLk%3D
6. J Balthazart M Baillien GF Ball 2001 Phosphorylation processes mediate rapid changes of brain aromatase activity J Steroid Biochem Mol Biol 79 261 277 11850233 10.1016/S0960-0760(01)00143-1 1:CAS:528:DC%2BD38XhtFylurs%3D (Pubitemid 34162529)
7. J Balthazart M Baillien TD Charlier GF Ball 2003 Calcium-dependent phosphorylation processes control brain aromatase in quail Eur J Neurosci 17 1591 1606 12752377 10.1046/j.1460-9568.2003.02598.x 1:STN:280: DC%2BD3s3jvFygug%3D%3D (Pubitemid 36628128)
8. J Balthazart M Baillien GF Ball 2005 Interactions between kinases and phosphatases in the rapid control of brain aromatase J Neuroendocrinol 17 553 559 16101893 10.1111/j.1365-2826.2005.01344.x 1:CAS:528:DC%2BD2MXpvFKktLg%3D (Pubitemid 41195408)
9. J Balthazart M Baillien GF Ball 2006 Rapid control of brain aromatase activity by glutamatergic inputs Endocrinology 147 359 366 16195408 10.1210/en.2005-0845 1:CAS:528:DC%2BD28XptFCr (Pubitemid 43004289)
10. Barha CK, Brummelte S, Lieblich SE, Galea LAM (2010) Chronic restraint stress in adolescence differentially influences hypothalamic-pituitary-adrenal axis function and adult hippocampal neurogenesis in male and female rats. Hippocampus (Epub ahead of print)
11. EE Baulieu 1997 Neurosteroids: of the nervous system, by the nervous system, for the nervous system Recent Prog Horm Res 52 1 32 9238846 1:STN:280:DyaK2szotFKiuw%3D%3D (Pubitemid 127470204)
12. EE Baulieu P Robel 1990 Neurosteroids: a new brain function? J Steroid Biochem Mol Biol 37 395 403 2257243 10.1016/0960-0760(90)90490-C 1:CAS:528:DyaK3MXlsFygug%3D%3D
13. EE Baulieu P Robel 1998 Dehydroepiandrosterone (DHEA) and dehydroepiandrosterone sulfate (DHEAS) as neuroactive neurosteroids Proc Natl Acad Sci USA 95 4089 4091 9539693 10.1073/pnas.95.8.4089 1:CAS:528: DyaK1cXis1Ohsbk%3D (Pubitemid 28207868)
14. PP Bertrand UT Paranavitane C Chavez A Gogos M Jones M van den Buuse 2005 The effect of low estrogen state on serotonin transporter function in mouse hippocampus: a behavioral and electrochemical study Brain Res 1064 10 20 16298349 10.1016/j.brainres.2005.10.018 1:CAS:528:DC%2BD2MXhtlWqtbnK (Pubitemid 41774640)
15. C Beyer 1999 Estrogen and the developing mammalian brain Anat Embryol (Berl) 199 379 390 10.1007/s004290050236 1:STN:280:DyaK1M3js1Kgug%3D%3D (Pubitemid 29145836)
16. C Beyer R Tramonte RE Hutchison PJ Sharp PJ Barker NS Huskisson JB Hutchison 1994 Aromatase-immunoreactive neurons in the adult female chicken brain detected using a specific antibody Brain Res Bull 33 583 588 8187001 10.1016/0361-9230(94)90084-1 1:STN:280:DyaK2c3ktlOisQ%3D%3D (Pubitemid 24079476)
17. WC Boon J Diepstraten J van der Burg ME Jones ER Simpson M van den Buuse 2005 Hippocampal NMDA receptor subunit expression and watermaze learning in estrogen deficient female mice Brain Res Mol Brain Res 140 127 132 16083992 10.1016/j.molbrainres.2005.07.004 1:CAS:528:DC%2BD2MXhtFSisbjK (Pubitemid 41447489)
18. S Bourguiba S Lambard S Carreau 2003 Steroids control the aromatase gene expression in purified germ cells from the adult male rat J Mol Endocrinol 31 83 94 12914527 10.1677/jme.0.0310083 1:CAS:528:DC%2BD3sXntFejtb8%3D (Pubitemid 37063081)
19. DA Cordoba Montoya HF Carrer 1997 Estrogen facilitates induction of long term potentiation in the hippocampus of awake rats Brain Res 778 430 438 9459564 10.1016/S0006-8993(97)01206-7 1:CAS:528:DyaK2sXnvFGlsLY%3D (Pubitemid 28037427)
20. CA Cornil TD Charlier 2010 Rapid behavioural effects of oestrogens and fast regulation of their local synthesis by brain aromatase J Neuroendocrinol 22 664 673 20456609 1:CAS:528:DC%2BC3cXovFejs7k%3D
21. M Cyr F Calon M Morissette T Di Paolo 2002 Estrogenic modulation of brain activity: implications for schizophrenia and Parkinson's disease J Psychiatry Neurosci 27 12 27 11836973 (Pubitemid 34478366)
22. C Dalla K Antoniou Z Papadopoulou-Daifoti J Balthazart J Bakker 2004 Oestrogen-deficient female aromatase knockout (ArKO) mice exhibit depressive-like symptomatology Eur J Neurosci 20 217 228 15245494 10.1111/j.1460-9568.2004.03443.x 1:STN:280:DC%2BD2czktlSqtA%3D%3D (Pubitemid 38932142)
23. EE Daniel G Bodie M Mannarino G Boddy WJ Cho 2004 Changes in membrane cholesterol affect caveolin-1 localization and ICC-pacing in mouse jejunum Am J Physiol Gastrointest Liver Physiol 287 G202 G210 14977635 10.1152/ajpgi.00356. 2003 1:CAS:528:DC%2BD2cXlvFOgs7k%3D (Pubitemid 38802134)
24. S Daniel AJ Diaz KM Martinez BJ Bench F Albertorio PS Cremer 2007 Separation of membrane-bound compounds by solid-supported bilayer electrophoresis J Am Chem Soc 129 8072 8073 17564451 10.1021/ja0720816 1:CAS:528:DC%2BD2sXmt12gsLo%3D (Pubitemid 47035112)
25. JL Do Rego JY Seong D Burel J Leprince V Luu-The K Tsutsui MC Tonon G Pelletier H Vaudry 2009 Neurosteroid biosynthesis: enzymatic pathways and neuroendocrine regulation by neurotransmitters and neuropeptides Front Neuroendocrinol 30 259 301 19505496 10.1016/j.yfrne.2009.05.006 1:CAS:528:DC%2BD1MXptl2itbw%3D
26. SV Fernandez J Russo 2010 Estrogen and xenoestrogens in breast cancer Toxicol Pathol 38 110 122 19933552 10.1177/0192623309354108 1:CAS:528: DC%2BC3cXjt1ajtb8%3D
27. L Fester V Ribeiro-Gouveia J Prange-Kiel C von Schassen M Bottner H Jarry GM Rune 2006 Proliferation and apoptosis of hippocampal granule cells require local oestrogen synthesis J Neurochem 97 1136 1144 16579833 10.1111/j.1471-4159. 2006.03809.x 1:CAS:528:DC%2BD28XlsVOnt7k%3D
28. MR Foy 2001 17beta-estradiol: effect on CA1 hippocampal synaptic plasticity Neurobiol Learn Mem 76 239 252 11726235 10.1006/nlme.2001.4018 1:CAS:528:DC%2BD3MXos1amt7Y%3D (Pubitemid 34001400)
29. MR Foy J Xu X Xie RD Brinton RF Thompson TW Berger 1999 17beta-estradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation J Neurophysiol 81 925 929 10036289 1:CAS:528:DyaK1MXhslOltrc%3D (Pubitemid 29264535)
30. A Furukawa A Miyatake T Ohnishi Y Ichikawa 1998 Steroidogenic acute regulatory protein (StAR) transcripts constitutively expressed in the adult rat central nervous system: colocalization of StAR, cytochrome P-450SCC (CYP XIA1), and 3beta-hydroxysteroid dehydrogenase in the rat brain J Neurochem 71 2231 2238 9832120 10.1046/j.1471-4159.1998.71062231.x 1:CAS:528:DyaK1cXns1eisbc%3D (Pubitemid 28531232)
31. LM Garcia-Segura 2008 Aromatase in the brain: not just for reproduction anymore J Neuroendocrinol 20 705 712 18601693 10.1111/j.1365-2826.2008.01713.x 1:CAS:528:DC%2BD1cXnt1Cjtbk%3D (Pubitemid 351858721)
32. LM Garcia-Segura A Wozniak I Azcoitia JR. Rodriguez RE Hutchison JB Hutchison 1999 Aromatase expression by astrocytes after brain injury: implications for local estrogen formation in brain repair Neuroscience 89 567 578 10077336 10.1016/S0306-4522(98)00340-6 1:CAS:528:DyaK1MXnsVeitA%3D%3D (Pubitemid 29044337)
33. M Good M Day JL Muir 1999 Cyclical changes in endogenous levels of oestrogen modulate the induction of LTD and LTP in the hippocampal CA1 region Eur J Neurosci 11 4476 4480 10594677 10.1046/j.1460-9568.1999.00920.x 1:STN:280:DC%2BD3c%2Fmt1Giug%3D%3D (Pubitemid 30009282)
34. E Gould CS Woolley M Frankfurt BS McEwen 1990 Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood J Neurosci 10 1286 1291 2329377 1:CAS:528:DyaK3cXit12rtbc%3D
35. C Gundlah SG Kohama SJ Mirkes VT Garyfallou HF Urbanski CL Bethea 2000 Distribution of estrogen receptor beta (ER[beta]) mRNA in hypothalamus, midbrain and temporal lobe of spayed macaque: continued expression with hormone replacement Mol Brain Res 76 191 204 10762694 10.1016/S0006-8993(99)02475-0 1:CAS:528:DC%2BD3cXitlOls7c%3D (Pubitemid 30179755)
36. N Harada S Abe-Dohmae R Loeffen A Foidart J Balthazart 1993 Synergism between androgens and estrogens in the induction of aromatase and its messenger RNA in the brain Brain Res 622 243 256 8242362 10.1016/0006-8993(93)90825-8 1:CAS:528:DyaK3sXlvFGqu78%3D (Pubitemid 23264971)
37. BL Hart 2001 Effect of gonadectomy on subsequent development of age-related cognitive impairment in dogs J Am Vet Med Assoc 219 51 56 11439769 10.2460/javma.2001.219.51 1:CAS:528:DC%2BD3MXlt1eit78%3D (Pubitemid 33611602)
38. RA Hill HK Chua ME Jones ER Simpson WC Boon 2009 Estrogen deficiency results in apoptosis in the frontal cortex of adult female aromatase knockout mice Mol Cell Neurosci 41 1 7 19185610 10.1016/j.mcn.2008.12.009 1:CAS:528:DC%2BD1MXltVyru74%3D
39. Y Hojo TA Hattori T Enami A Furukawa K Suzuki HT Ishii H Mukai JH Morrison WG Janssen S Kominami N Harada T Kimoto S Kawato 2004 Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017alpha and P450 aromatase localized in neurons Proc Natl Acad Sci USA 101 865 870 14694190 10.1073/pnas.2630225100 1:CAS:528:DC%2BD2cXhsVWgsr0%3D (Pubitemid 38121049)
40. E Hosli L Hosli 1999 Cellular localization of estrogen receptors on neurones in various regions of cultured rat CNS: coexistence with cholinergic and galanin receptors Int J Dev Neurosci 17 317 330 10479067 10.1016/S0736-5748(99)00038-6 1:CAS:528:DyaK1MXlvVClu7k%3D (Pubitemid 29356002)
41. S Iivonen T Heikkinen J Puolivali S Helisalmi M Hiltunen H Soininen H Tanila 2006 Effects of estradiol on spatial learning, hippocampal cytochrome P450 19, and estrogen alpha and beta mRNA levels in ovariectomized female mice Neuroscience 137 1143 1152 16326017 10.1016/j.neuroscience.2005.10.023 1:CAS:528:DC%2BD28Xos1emtg%3D%3D (Pubitemid 43133140)
42. T Ikeda N Matsuki MK Yamada 2006 Estrogen produced in cultured hippocampal neurons is a functional regulator of a GABAergic machinery J Neurosci Res 84 1771 1777 17044036 10.1002/jnr.21083 1:CAS:528: DC%2BD28XhtlGqs7zJ (Pubitemid 44892610)
43. TA Ishunina DF Fischer DF Swaab 2007 Estrogen receptor alpha and its splice variants in the hippocampus in aging and Alzheimer's disease Neurobiol Aging 28 1670 1681 17010478 10.1016/j.neurobiolaging.2006.07.024 1:CAS:528:DC%2BD2sXhtVCmt7nK (Pubitemid 47384954)
44. RL Jakab TL Horvath C Leranth N Harada F Naftolin 1993 Aromatase immunoreactivity in the rat brain: gonadectomy-sensitive hypothalamic neurons and an unresponsive "limbic ring" of the lateral septum-bed nucleus-amygdala complex J Steroid Biochem Mol Biol 44 481 498 8476763 10.1016/0960-0760(93)90253-S 1:CAS:528:DyaK3sXktVGms74%3D (Pubitemid 23126620)
45. RM Janssens L Brus DJ Cahill JA Huirne J Schoemaker CB Lambalk 2000 Direct ovarian effects and safety aspects of GnRH agonists and antagonists Hum Reprod Update 6 505 518 11045881 10.1093/humupd/6.5.505 1:CAS:528: DC%2BD3cXnvV2qsrw%3D
46. KB Jelks R Wylie CL Floyd AK McAllister P Wise 2007 Estradiol targets synaptic proteins to induce glutamatergic synapse formation in cultured hippocampal neurons: critical role of estrogen receptor-alpha J Neurosci 27 6903 6913 17596438 10.1523/JNEUROSCI.0909-07.2007 1:CAS:528:DC%2BD2sXnsVyjtro%3D (Pubitemid 47015894)
47. V Jenkins V Shilling G Deutsch D Bloomfield R Morris S Allan H Bishop N Hodson S Mitra G Sadler E Shah R Stein S Whitehead J Winstanley 2006 A 3-year prospective study of the effects of adjuvant treatments on cognition in women with early stage breast cancer Br J Cancer 94 828 834 16523200 10.1038/sj.bjc.6603029 1:CAS:528:DC%2BD28Xis1Gktbw%3D
48. L Jennes B Brame A Centers JA Janovick PM Conn 1995 Regulation of hippocampal gonadotropin releasing hormone (GnRH) receptor mRNA and GnRH-stimulated inositol phosphate production by gonadal steroid hormones Brain Res Mol Brain Res 33 104 110 8774951 10.1016/0169-328X(95)00113-7 1:CAS:528:DyaK2MXotVaqsbo%3D
49. K Kalita S Szymczak L Kaczmarek 2005 Non-nuclear estrogen receptor beta and alpha in the hippocampus of male and female rats Hippocampus 15 404 412 15669092 10.1002/hipo.20066 1:CAS:528:DC%2BD2MXksVynu7k%3D (Pubitemid 40668359)
50. CM Klinge SC Jernigan SL Smith VV Tyulmenkov PC Kulakosky 2001 Estrogen response element sequence impacts the conformation and transcriptional activity of estrogen receptor alpha Mol Cell Endocrinol 174 151 166 11306182 10.1016/S0303-7207(01)00382-3 1:CAS:528:DC%2BD3MXisF2ktLs%3D (Pubitemid 32288879)
51. O Kretz L Fester U Wehrenberg L Zhou S Brauckmann S Zhao J Prange-Kiel T Naumann H Jarry M Frotscher GM Rune 2004 Hippocampal synapses depend on hippocampal estrogen synthesis J Neurosci 24 5913 5921 15229239 10.1523/JNEUROSCI.5186-03.2004 1:CAS:528:DC%2BD2cXlsleltLg%3D (Pubitemid 38859389)
52. C Leranth T Hajszan NJ MacLusky 2004 Androgens increase spine synapse density in the CA1 hippocampal subfield of ovariectomized female rats J Neurosci 24 495 499 14724248 10.1523/JNEUROSCI.4516-03.2004 1:CAS:528: DC%2BD2cXpvVyjtg%3D%3D (Pubitemid 38112381)
53. YP Lu M Zeng DF Swaab R Ravid JN Zhou 2004 Colocalization and alteration of estrogen receptor-alpha and -beta in the hippocampus in Alzheimer's disease Hum Pathol 35 275 280 15017582 10.1016/j.humpath.2003.11.004 1:CAS:528:DC%2BD2cXitFKntbc%3D (Pubitemid 38339600)
54. VN Luine 2008 Sex steroids and cognitive function J Neuroendocrinol 20 866 872 18513207 10.1111/j.1365-2826.2008.01710.x 1:CAS:528:DC%2BD1cXnt1Cis7o%3D (Pubitemid 351858740)
55. NJ MacLusky F Naftolin PS Goldman-Rakic 1986 Estrogen formation and binding in the cerebral cortex of the developing rhesus monkey Proc Natl Acad Sci USA 83 513 516 3455786 10.1073/pnas.83.2.513 1:CAS:528:DyaL28Xot1amsg%3D%3D (Pubitemid 16080044)
56. NJ MacLusky MJ Walters AS Clark CD Toran-Allerand 1994 Aromatase in the cerebral cortex, hippocampus, and mid-brain: ontogeny and developmental implications Mol Cell Neurosci 5 691 698 7704444 10.1006/mcne.1994.1083 1:CAS:528:DyaK2MXjt1egs7c%3D
57. S Martin M Jones E Simpson M van den Buuse 2003 Impaired spatial reference memory in aromatase-deficient (ArKO) mice Neuroreport 14 1979 1982 14561933 10.1097/00001756-200310270-00020 1:CAS:528:DC%2BD3sXotFWlsrc%3D (Pubitemid 38339773)
58. CA McArdle J Franklin L Green JN Hislop 2002 Signalling, cycling and desensitisation of gonadotrophin-releasing hormone receptors J Endocrinol 173 1 11 11927379 10.1677/joe.0.1730001 1:CAS:528:DC%2BD38Xjt1ejsLk%3D (Pubitemid 34428886)
59. B McEwen 2002 Estrogen actions throughout the brain Recent Prog Horm Res 57 357 384 12017552 10.1210/rp.57.1.357 1:CAS:528:DC%2BD38Xjt1WqtLY%3D
60. SH Mellon LD Griffin 2002 Neurosteroids: biochemistry and clinical significance Trends Endocrinol Metab 13 35 43 11750861 10.1016/S1043-2760(01) 00503-3 1:CAS:528:DC%2BD3MXpt1anu7w%3D (Pubitemid 36734014)
61. H Mukai T Tsurugizawa G Murakami S Kominami H Ishii M Ogiue-Ikeda N Takata N Tanabe A Furukawa Y Hojo Y Ooishi JH Morrison WG Janssen JA Rose P Chambon S Kato S Izumi T Yamazaki T Kimoto S Kawato 2007 Rapid modulation of long-term depression and spinogenesis via synaptic estrogen receptors in hippocampal principal neurons J Neurochem 100 950 967 17266735 10.1111/j.1471-4159.2006.04264.x 1:CAS:528:DC%2BD2sXisFGnurc%3D (Pubitemid 46213921)
62. T Murata K Narita K Honda S Matsukawa T Higuchi 2003 Differential regulation of estrogen receptor alpha and beta mRNAs in the rat uterus during pregnancy and labor: possible involvement of estrogen receptors in oxytocin receptor regulation Endocr J 50 579 587 14614214 10.1507/endocrj.50.579 1:CAS:528:DC%2BD2cXmt1Gqsw%3D%3D (Pubitemid 37448518)
63. M Osterlund GG Kuiper JA Gustafsson YL Hurd 1998 Differential distribution and regulation of estrogen receptor-alpha and -beta mRNA within the female rat brain Brain Res Mol Brain Res 54 175 180 9526077 10.1016/S0169-328X(97)00351-3 1:CAS:528:DyaK1cXhsFehtrg%3D (Pubitemid 28119175)
64. G Pelletier 2010 Steroidogenic enzymes in the brain: morphological aspects Prog Brain Res 181 193 207 20478439 10.1016/S0079-6123(08)81011-4 1:CAS:528:DC%2BC3cXhtVajtb%2FN
65. SB Pillai JM Jones RD Koos 2002 Treatment of rats with 17beta-estradiol or relaxin rapidly inhibits uterine estrogen receptor beta1 and beta2 messenger ribonucleic acid levels Biol Reprod 67 1919 1926 12444070 10.1095/biolreprod. 102.003392 1:CAS:528:DC%2BD38XptVeltr8%3D (Pubitemid 35388023)
66. J Prange-Kiel GM Rune 2006 Direct and indirect effects of estrogen on rat hippocampus Neuroscience 138 765 772 16324798 10.1016/j.neuroscience.2005.05. 061 1:CAS:528:DC%2BD28XitVGjsb0%3D
67. J Prange-Kiel U Wehrenberg H Jarry GM Rune 2003 Para/autocrine regulation of estrogen receptors in hippocampal neurons Hippocampus 13 226 234 12699330 10.1002/hipo.10075 1:CAS:528:DC%2BD3sXjt1Wqurw%3D (Pubitemid 36503535)
68. J Prange-Kiel H Jarry M Schoen P Kohlmann C Lohse L Zhou GM Rune 2008 Gonadotropin-releasing hormone regulates spine density via its regulatory role in hippocampal estrogen synthesis J Cell Biol 180 417 426 18227283 10.1083/jcb.200707043 1:CAS:528:DC%2BD1cXhsFOntbo%3D (Pubitemid 351185925)
69. Reddy D (2010) Neurosteroids: endogenous role in the human brain and therapeutic potentials. Prog Brain Res 113-137
70. CE Roselli LE Horton JA Resko 1985 Distribution and regulation of aromatase activity in the rat hypothalamus and limbic system Endocrinology 117 2471 2477 4065042 10.1210/endo-117-6-2471 1:CAS:528:DyaL28XhsFegtw%3D%3D (Pubitemid 16194078)
71. CE Roselli RL Salisbury JA Resko 1987 Genetic evidence for androgen-dependent and independent control of aromatase activity in the rat brain Endocrinology 121 2205 2210 3678147 10.1210/endo-121-6-2205 1:CAS:528:DyaL1cXjt1Wqsw%3D%3D (Pubitemid 18016995)
72. C Roselli A Boussac TA Mattioli 1994 Direct vibrational structure of protein metal-binding sites from near-infrared Yb3+ vibronic side band spectroscopy Proc Natl Acad Sci USA 91 12897 12901 7809143 10.1073/pnas.91.26. 12897 1:CAS:528:DyaK2MXivVCqs7Y%3D
73. GM Rune M Frotscher 2005 Neurosteroid synthesis in the hippocampus: role in synaptic plasticity Neuroscience 136 833 842 16344155 10.1016/j.neuroscience. 2005.03.056 1:CAS:528:DC%2BD2MXhtlaiurjP (Pubitemid 41774728)
74. GM Rune U Wehrenberg J Prange-Kiel L Zhou G Adelmann M Frotscher 2002 Estrogen up-regulates estrogen receptor alpha and synaptophysin in slice cultures of rat hippocampus Neuroscience 113 167 175 12123695 10.1016/S0306-4522(02)00152-5 1:CAS:528:DC%2BD38Xlt1Oitbs%3D (Pubitemid 34786022)
75. MK Sanghera ER Simpson MJ McPhaul G Kozlowski AJ Conley ED Lephart 1991 Immunocytochemical distribution of aromatase cytochrome P450 in the rat brain using peptide-generated polyclonal antibodies Endocrinology 129 2834 2844 1954870 10.1210/endo-129-6-2834 1:CAS:528:DyaK38XhvVOgsw%3D%3D
76. DA Schreihofer MH Stoler MA Shupnik 2000 Differential expression and regulation of estrogen receptors (ERs) in rat pituitary and cell lines: estrogen decreases ERalpha protein and estrogen responsiveness Endocrinology 141 2174 2184 10830306 10.1210/en.141.6.2174 1:CAS:528:DC%2BD3cXlt1WmsL8%3D (Pubitemid 32279622)
77. K Shibuya N Takata Y Hojo A Furukawa N Yasumatsu T Kimoto T Enami K Suzuki N Tanabe H Ishii H Mukai T Takahashi TA Hattori S Kawato 2003 Hippocampal cytochrome P450s synthesize brain neurosteroids which are paracrine neuromodulators of synaptic signal transduction Biochim Biophys Acta 1619 301 316 12573490 1:CAS:528:DC%2BD3sXovFGrug%3D%3D (Pubitemid 36160608)
78. PJ Shughrue I Merchenthaler 2000 Evidence for novel estrogen binding sites in the rat hippocampus Neuroscience 99 605 612 10974424 10.1016/S0306-4522(00)00242-6 1:CAS:528:DC%2BD3cXmtF2hsrg%3D
79. T Smejkalova CS Woolley 2010 Estradiol acutely potentiates hippocampal excitatory synaptic transmission through a presynaptic mechanism J Neurosci 30 16137 16148 21123560 10.1523/JNEUROSCI.4161-10.2010 1:CAS:528:DC%2BC3cXhs1SlurvI
80. CC Smith LL McMahon 2006 Estradiol-induced increase in the magnitude of long-term potentiation is prevented by blocking NR2B-containing receptors J Neurosci 26 8517 8522 16914677 10.1523/JNEUROSCI.5279-05.2006 1:CAS:528:DC%2BD28Xpt1Cks7o%3D (Pubitemid 44316180)
81. M Tena-Sempere VM Navarro A Mayen C Bellido JE Sanchez-Criado 2004 Regulation of estrogen receptor (ER) isoform messenger RNA expression by different ER ligands in female rat pituitary Biol Reprod 70 671 678 14613904 10.1095/biolreprod.103.021378 1:CAS:528:DC%2BD2cXhs1ChsL8%3D (Pubitemid 38233705)
82. C von Schassen L Fester J Prange-Kiel C Lohse C Huber M Bottner GM Rune 2006 Oestrogen synthesis in the hippocampus: role in axon outgrowth J Neuroendocrinol 18 847 856 10.1111/j.1365-2826.2006.01484.x (Pubitemid 44501989)
83. SG Warren AG Humphreys JM Juraska WT Greenough 1995 LTP varies across the estrous cycle: enhanced synaptic plasticity in proestrus rats Brain Res 703 26 30 8719612 10.1016/0006-8993(95)01059-9 1:CAS:528:DyaK2MXhtVSksrzF
84. U Wehrenberg J Prange-Kiel GM Rune 2001 Steroidogenic factor-1 expression in marmoset and rat hippocampus: co-localization with StAR and aromatase J Neurochem 76 1879 1886 11259506 10.1046/j.1471-4159.2001.00207.x 1:CAS:528:DC%2BD3MXitlSktLw%3D (Pubitemid 32221128)
85. CS Woolley E Gould M Frankfurt BS McEwen 1990 Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons J Neurosci 10 4035 4039 2269895 1:STN:280:DyaK3M7gtFSmtQ%3D%3D
86. CW Xiao AK Goff 1999 Hormonal regulation of oestrogen and progesterone receptors in cultured bovine endometrial cells J Reprod Fertil 115 101 109 10341728 10.1530/Jr.f.0.1150101 1:CAS:528:DyaK1MXhs12is7g%3D
87. JG Yague A Munoz P de Monasterio-Schrader J Defelipe LM Garcia-Segura I Azcoitia 2006 Aromatase expression in the human temporal cortex Neuroscience 138 389 401 16426763 10.1016/j.neuroscience.2005.11.054 1:CAS:528: DC%2BD28XhvVWrs7Y%3D (Pubitemid 43255552)
88. JG Yague AC Wang WG Janssen PR Hof LM Garcia-Segura I Azcoitia JH Morrison 2008 Aromatase distribution in the monkey temporal neocortex and hippocampus Brain Res 1209 115 127 18402929 10.1016/j.brainres.2008.02.061 1:CAS:528:DC%2BD1cXlsFyjsLg%3D
89. MB Yilmaz A Wolfe YH Cheng C Glidewell-Kenney JL Jameson SE Bulun 2009 Aromatase promoter I.f is regulated by estrogen receptor alpha (ESR1) in mouse hypothalamic neuronal cell lines Biol Reprod 81 956 965 19605792 10.1095/biolreprod.109.077206 1:CAS:528:DC%2BD1MXhtlWrtrzK
90. C Zhao R Fujinaga A Yanai K Kokubu Y Takeshita Y Watanabe K Shinoda 2008 Sex-steroidal regulation of aromatase mRNA expression in adult male rat brain: a quantitative non-radioactive in situ hybridization study Cell Tissue Res 332 381 391 18401595 10.1007/s00441-008-0606-8 1:CAS:528:DC%2BD1cXls1Krt7w%3D
91. L Zhou N Lehan U Wehrenberg E Disteldorf R von Lossow U Mares H Jarry GM Rune 2007 Neuroprotection by estradiol: a role of aromatase against spine synapse loss after blockade of GABA(A) receptors Exp Neurol 203 72 81 17005180 10.1016/j.expneurol.2006.07.020 1:CAS:528:DC%2BD28Xht1Krt7rO (Pubitemid 44821165)
92. L Zhou L Fester B von Blittersdorff B Hassu H Nogens J Prange-Kiel H Jarry K Wegscheider GM Rune 2010 Aromatase inhibitors induce spine synapse loss in the hippocampus of ovariectomized mice Endocrinology 151 1153 1160 20097718 10.1210/en.2009-0254 1:CAS:528:DC%2BC3cXjvVKqtr0%3D