Learning and memory: Steroids and epigenetics

Journal of Steroid Biochemistry and Molecular Biology

Volumn 150, Issue , 2015, Pages 64-85

  Colciago, Alessandra ^a   Casati, Lavinia ^b   Negri Cesi, Paola ^a   Celotti, Fabio ^a  

^a Section of Biomedicine and Endocrinology   (Italy)

^b Department of Medical Biotechnologies and Translational Medicine ^*  (Italy)

Author keywords

Androgens; Corticosteroids; Epigenetics; Estrogens; Memory; Progesterone; Steroid receptors; Steroids

Indexed keywords

ANDROGEN; ESTROGEN; PRASTERONE; PROGESTERONE; STEROID; STEROID RECEPTOR; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR;

COGNITION; EPIGENETICS; GENETIC TRANSCRIPTION; HIPPOCAMPUS; HUMAN; LEARNING; LONG TERM DEPRESSION; MEMORY; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEUROTRANSMISSION; NONHUMAN; REVIEW; SEX DIFFERENCE; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; AMYGDALOID NUCLEUS; ANIMAL; GENETIC EPIGENESIS; GENETICS; METABOLISM; PHYSIOLOGY; SYNAPSE; TEMPORAL LOBE;

ANIMALIA;

AMYGDALA; ANDROGENS; ANIMALS; EPIGENESIS, GENETIC; ESTROGENS; GLUCOCORTICOIDS; HIPPOCAMPUS; HUMANS; MEMORY; NEURONAL PLASTICITY; PROGESTERONE; RECEPTORS, GLUCOCORTICOID; RECEPTORS, STEROID; SYNAPSES; TEMPORAL LOBE;

EID: 84925746116     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2015.02.008     Document Type: Review

References (280)

1. M.G. Packard, and J. Goodman Factors that influence the relative use of multiple memory systems Hippocampus 23 2013 1044 1052
2. B.D. Murray, and E.A. Kensinger The effects of emotion and encoding strategy on associative memory Mem. Cognit. 40 2012 1056 1069
3. J.S. Kim, G. Vossel, and M. Gamer Effects of emotional context on memory for details: the role of attention PLoS One 8 2013 e77405
4. L.R. Squire Memory and brain systems: 1969-2009 J. Neurosci. 29 2009 12711 12716
5. L.R. Squire, and J.T. Wixted The cognitive neuroscience of human memory since H.M Annu. Rev. Neurosci. 34 2011 259 288
6. A.S. Kim, A. Vallesi, T.W. Picton, and E. Tulving Cognitive association formation in episodic memory: evidence from event-related potentials Neuropsychologia 47 2009 3162 3173
7. K. Henke A model for memory systems based on processing modes rather than consciousness Nat. Rev. Neurosci. 11 2010 523 532
8. P.J. Reber The neural basis of implicit learning and memory: a review of neuropsychological and neuroimaging research Neuropsychologia 51 2013 2026 2042
9. C. Ranganath, and M. Ritchey Two cortical systems for memory-guided behaviour Nat. Rev. Neurosci. 13 2012 713 726
10. S.F. Logue, and T.J. Gould The neural and genetic basis of executive function: attention, cognitive flexibility, and response inhibition Pharmacol. Biochem. Behav. 123 2013 45 54
11. A.A. Kehagia, G.K. Murray, and T.W. Robbins Learning and cognitive flexibility: frontostriatal function and monoaminergic modulation Curr. Opin. Neurobiol. 20 2010 199 204
12. R. Cabeza, E. Ciaramelli, and M. Moscovitch Cognitive contributions of the ventral parietal cortex: an integrative theoretical account Trends Cogn. Sci. 16 2012 338 352
13. B. Straube An overview of the neuro-cognitive processes involved in the encoding, consolidation, and retrieval of true and false memories Behav. Brain Funct. 8 2012 35
14. F.I. Craik, R. Govoni, M. Naveh-Benjamin, and N.D. Anderson The effects of divided attention on encoding and retrieval processes in human memory J. Exp. Psychol. Gen. 125 1996 159 180
15. E. Awh, E.K. Vogel, and S.H. Oh Interactions between attention and working memory Neuroscience 139 2006 201 208
16. L.S. Chau, and R. Galvez Amygdala's involvement in facilitating associative learning-induced plasticity: a promiscuous role for the amygdala in memory acquisition Front. Integr. Neurosci. 6 2012 92
17. G. Brod, M. Werkle-Bergner, and Y.L. Shing The influence of prior knowledge on memory: a developmental cognitive neuroscience perspective Front. Behav. Neurosci. 7 2013 139
18. S. Diekelmann, and J. Born The memory function of sleep Nat. Rev. Neurosci. 11 2010 114 126
19. M. Sehgal, C. Song, V.L. Ehlers, and J.R. Moyer Jr. Learning to learn-intrinsic plasticity as a metaplasticity mechanism for memory formation Neurobiol. Learn. Mem. 105 2013 186 199
20. A. Papoutsi, G. Kastellakis, M. Psarrou, S. Anastasakis, and P. Poirazi Coding and decoding with dendrites J. Physiol. Paris 108 1 2013 18 27
21. H.L. Atwood, and S. Karunanithi Diversification of synaptic strength: presynaptic elements Nat. Rev. Neurosci. 3 2002 497 516
22. M. Diaz-Rios, and M.W. Miller Target-specific regulation of synaptic efficacy in the feeding central pattern generator of Aplysia: potential substrates for behavioral plasticity? Biol. Bull. 210 2006 215 229
23. J. Cortes-Mendoza, S. Diaz de Leon-Guerrero, G. Pedraza-Alva, and L. Perez-Martinez Shaping synaptic plasticity: the role of activity-mediated epigenetic regulation on gene transcription Int. J. Dev. Neurosci. 31 2013 359 369
24. G.R. Owen, and E.A. Brenner Mapping molecular memory: navigating the cellular pathways of learning Cell. Mol. Neurobiol. 32 2012 919 941
25. S.J. Martin, and R.G. Morris New life in an old idea: the synaptic plasticity and memory hypothesis revisited Hippocampus 12 2002 609 636
26. R.A. Nicoll, and K.W. Roche Long-term potentiation: peeling the onion Neuropharmacology 74 2013 18 22
27. G. Neves, S.F. Cooke, and T.V. Bliss Synaptic plasticity, memory and the hippocampus: a neural network approach to causality Nat. Rev. Neurosci. 9 2008 65 75
28. S.J. Martin, P.D. Grimwood, and R.G. Morris Synaptic plasticity and memory: an evaluation of the hypothesis Annu. Rev. Neurosci. 23 2000 649 711
29. D.O. Hebb The Organization of Behavior; A Neuropsychological Theory 1949 Wiley New York
30. H.W. Kessels, and R. Malinow Synaptic AMPA receptor plasticity and behavior Neuron 61 2009 340 350
31. S. Asrar, and Z. Jia Molecular mechanisms coordinating functional and morphological plasticity at the synapse: role of GluA2/N-cadherin interaction-mediated actin signaling in mGluR-dependent LTD Cell. Signal. 25 2013 397 402
32. M. De Roo, P. Klauser, and D. Muller LTP promotes a selective long-term stabilization and clustering of dendritic spines PLoS Biol. 6 2008 e219
33. P.M. Steele, and M.D. Mauk Inhibitory control of LTP and LTD: stability of synapse strength J. Neurophysiol. 81 1999 1559 1566
34. G.L. Collingridge, S. Peineau, J.G. Howland, and Y.T. Wang Long-term depression in the CNS Nat. Rev. Neurosci. 11 2010 459 473
35. A.J. Heynen, W.C. Abraham, and M.F. Bear Bidirectional modification of CA1 synapses in the adult hippocampus in vivo Nature 381 1996 163 166
36. M.J. Palmer, A.J. Irving, G.R. Seabrook, D.E. Jane, and G.L. Collingridge The group I mGlu receptor agonist DHPG induces a novel form of LTD in the CA1 region of the hippocampus Neuropharmacology 36 1997 1517 1532
37. C. Bellone, C. Luscher, and M. Mameli Mechanisms of synaptic depression triggered by metabotropic glutamate receptors Cell. Mol. Life Sci. 65 2008 2913 2923
38. C. Romano, A.N. van den Pol, and K.L. O'Malley Enhanced early developmental expression of the metabotropic glutamate receptor mGluR5 in rat brain: protein, mRNA splice variants, and regional distribution J. Comp. Neurol. 367 1996 403 412
39. Y.M. Lu, Z. Jia, C. Janus, J.T. Henderson, R. Gerlai, J.M. Wojtowicz, and J.C. Roder Mice lacking metabotropic glutamate receptor 5 show impaired learning and reduced CA1 long-term potentiation (LTP) but normal CA3 LTP J. Neurosci. 17 1997 5196 5205
40. P.K. Stanton LTD, LTP, and the sliding threshold for long-term synaptic plasticity Hippocampus 6 1996 35 42
41. Z. Dong, Y. Bai, X. Wu, H. Li, B. Gong, J.G. Howland, Y. Huang, W. He, T. Li, and Y.T. Wang Hippocampal long-term depression mediates spatial reversal learning in the Morris water maze Neuropharmacology 64 2013 65 73
42. C. Menard, and R. Quirion Group 1 metabotropic glutamate receptor function and its regulation of learning and memory in the aging brain Front. Pharmacol. 3 2012 182
43. L.S. Lerea, and J.O. McNamara Ionotropic glutamate receptor subtypes activate c-fos transcription by distinct calcium-requiring intracellular signaling pathways Neuron 10 1993 31 41
44. M. Baudry, X. Bi, C. Gall, and G. Lynch The biochemistry of memory: the 26 year journey of a 'new and specific hypothesis' Neurobiol. Learn. Mem. 95 2011 125 133
45. Y.A. Barde, D. Edgar, and H. Thoenen Purification of a new neurotrophic factor from mammalian brain EMBO J. 1 1982 549 553
46. B. Lu, K.H. Wang, and A. Nose Molecular mechanisms underlying neural circuit formation Curr. Opin. Neurobiol. 19 2009 162 167
47. J.M. Conner, J.C. Lauterborn, Q. Yan, C.M. Gall, and S. Varon Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: evidence for anterograde axonal transport J. Neurosci. 17 1997 2295 2313
48. P. Bekinschtein, M. Cammarota, and J.H. Medina BDNF and memory processing Neuropharmacology 76 Pt C 2014 677 683
49. V. Lessmann, K. Gottmann, and M. Malcangio Neurotrophin secretion: current facts and future prospects Prog. Neurobiol. 69 2003 341 374
50. C. Cunha, R. Brambilla, and K.L. Thomas A simple role for BDNF in learning and memory? Front. Mol. Neurosci. 3 2010 1
51. W.J. Tyler, S.P. Perrett, and L.D. Pozzo-Miller The role of neurotrophins in neurotransmitter release Neuroscientist 8 2002 524 531
52. M. Zagrebelsky, A. Holz, G. Dechant, Y.A. Barde, T. Bonhoeffer, and M. Korte The p75 neurotrophin receptor negatively modulates dendrite complexity and spine density in hippocampal neurons J. Neurosci. 25 2005 9989 9999
53. C.S. Rex, C.Y. Lin, E.A. Kramar, L.Y. Chen, C.M. Gall, and G. Lynch Brain-derived neurotrophic factor promotes long-term potentiation-related cytoskeletal changes in adult hippocampus J. Neurosci. 27 2007 3017 3029
54. B. Lin, E.A. Kramar, X. Bi, F.A. Brucher, C.M. Gall, and G. Lynch Theta stimulation polymerizes actin in dendritic spines of hippocampus J. Neurosci. 25 2005 2062 2069
55. A. Thiele Muscarinic signaling in the brain Ann. Rev. Neurosci. 36 2013 271 294
56. T.L. Wallace, and D. Bertrand Importance of the nicotinic acetylcholine receptor system in the prefrontal cortex Biochem. Pharmacol. 85 2013 1713 1720
57. K.C. Chen, M.G. Baxter, and J.S. Rodefer Central blockade of muscarinic cholinergic receptors disrupts affective and attentional set-shifting Eur. J. Neurosci. 20 2004 1081 1088
58. B. Roozendaal, and J.L. McGaugh Memory modulation Behav. Neurosci. 125 2011 797 824
59. A. Cifariello, A. Pompili, and A. Gasbarri 5-HT(7) receptors in the modulation of cognitive processes Behav. Brain Res. 195 2008 171 179
60. H. Jeltsch-David, J. Koenig, and J.C. Cassel Modulation of cholinergic functions by serotonin and possible implications in memory: general data and focus on 5-HT(1A) receptors of the medial septum Behav. Brain Res. 195 2008 86 97
61. E.A. Kramar, A.H. Babayan, C.M. Gall, and G. Lynch Estrogen promotes learning-related plasticity by modifying the synaptic cytoskeleton Neuroscience 239 2013 3 16
62. B. Auyeung, M.V. Lombardo, and S. Baron-Cohen Prenatal and postnatal hormone effects on the human brain and cognition Pflugers Arch. 465 2013 557 571
63. S.A. Shumaker, C. Legault, L. Kuller, S.R. Rapp, L. Thal, D.S. Lane, H. Fillit, M.L. Stefanick, S.L. Hendrix, C.E. Lewis, K. Masaki, and L.H. Coker S. conjugated equine estrogens and incidence of probable dementia and mild cognitive impairment in postmenopausal women: Women's Health Initiative Memory Study JAMA 291 2004 2947 2958
64. S.A. Shumaker, C. Legault, S.R. Rapp, L. Thal, R.B. Wallace, J.K. Ockene, S.L. Hendrix, B.N. Jones III, A.R. Assaf, R.D. Jackson, J.M. Kotchen, S. Wassertheil-Smoller, J. Wactawski-Wende, and WHIMS Investigators Estrogen plus progestin and the incidence of dementia and mild cognitive impairment in postmenopausal women: The Women's Health Initiative Memory Study: a randomized controlled trial JAMA 289 2003 2651 2662
65. M.A. Espeland, S.R. Rapp, S.A. Shumaker, R. Brunner, J.E. Manson, B.B. Sherwin, J. Hsia, K.L. Margolis, P.E. Hogan, R. Wallace, M. Dailey, R. Freeman, and J. Hays Women's Health Initiative Memory, Conjugated equine estrogens and global cognitive function in postmenopausal women: Women's Health Initiative Memory Study JAMA 291 2004 2959 2968
66. P.M. Maki, and V.W. Henderson Hormone therapy, dementia, and cognition: the Women's Health Initiative 10 years on Climacteric 15 2012 256 262
67. B. Fischer, C. Gleason, and S. Asthana Effects of hormone therapy on cognition and mood Fertil. Steril. 101 2014 898 904
68. L.A. Bean, L. Ianov, and T.C. Foster Estrogen receptors, the hippocampus, and memory Neuroscientist 20 5 2014 534 545
69. G.E. Gillies, and S. McArthur Estrogen actions in the brain and the basis for differential action in men and women: a case for sex-specific medicines Pharmacol. Rev. 62 2010 155 198
70. G. Pelletier Steroidogenic enzymes in the brain: morphological aspects Prog. Brain Res. 181 2010 193 207
71. P. Negri-Cesi, A. Colciago, A. Pravettoni, L. Casati, L. Conti, and F. Celotti Sexual differentiation of the rodent hypothalamus: hormonal and environmental influences J. Steroid Biochem. Mol. Biol. 109 2008 294 299
72. Q.G. Zhang, R. Wang, H. Tang, Y. Dong, A. Chan, G.R. Sareddy, R.K. Vadlamudi, and D.W. Brann Brain-derived estrogen exerts anti-inflammatory and neuroprotective actions in the rat hippocampus Mol. Cell. Endocrinol. 389 1-2 2014 84 91
73. S. Grassi, A. Tozzi, C. Costa, M. Tantucci, E. Colcelli, M. Scarduzio, P. Calabresi, and V.E. Pettorossi Neural 17β-estradiol facilitates long-term potentiation in the hippocampal CA1 region Neuroscience 192 2011 67 73
74. D.P. Srivastava, K.M. Woolfrey, and P. Penzes Insights into rapid modulation of neuroplasticity by brain estrogens Pharmacol. Rev. 65 2013 1318 1350
75. M. Fiocchetti, P. Ascenzi, and M. Marino Neuroprotective effects of 17beta-estradiol rely on estrogen receptor membrane initiated signals Front. Physiol. 3 2012 73
76. J. Meitzen, J.I. Luoma, M.I. Boulware, V.L. Hedges, B.M. Peterson, K. Tuomela, K.A. Britson, and P.G. Mermelstein Palmitoylation of estrogen receptors is essential for neuronal membrane signaling Endocrinology 154 2013 4293 4304
77. S. Clark, J. Rainville, X. Zhao, B.S. Katzenellenbogen, D. Pfaff, and N. Vasudevan Estrogen receptor-mediated transcription involves the activation of multiple kinase pathways in neuroblastoma cells J. Steroid Biochem. Mol. Biol. 139 2014 45 53
78. P. Micevych, and R. Dominguez Membrane estradiol signaling in the brain Front. Neuroendocrinol. 30 2009 315 327
79. M.K. Osterlund, J.A. Gustafsson, E. Keller, and Y.L. Hurd Estrogen receptor beta (ERbeta) messenger ribonucleic acid (mRNA) expression within the human forebrain: distinct distribution pattern to ERalpha mRNA J. Clin. Endocrinol. Metab. 85 2000 3840 3846
80. C. Bodo, and E.F. Rissman New roles for estrogen receptor beta in behavior and neuroendocrinology Front. Neuroendocrinol. 27 2006 217 232
81. S. Szymczak, K. Kalita, J. Jaworski, B. Mioduszewska, A. Savonenko, A. Markowska, I. Merchenthaler, and L. Kaczmarek Increased estrogen receptor beta expression correlates with decreased spine formation in the rat hippocampus Hippocampus 16 2006 453 463
82. D.P. Srivastava, and P.D. Evans G-protein oestrogen receptor 1: trials and tribulations of a membrane oestrogen receptor J. Neuroendocrinol. 25 2013 1219 1230
83. J.L. Spencer, E.M. Waters, R.D. Romeo, G.E. Wood, T.A. Milner, and B.S. McEwen Uncovering the mechanisms of estrogen effects on hippocampal function Front. Neuroendocrinol. 29 2008 219 237
84. K.T. Akama, L.I. Thompson, T.A. Milner, and B.S. McEwen Post-synaptic density-95 (PSD-95) binding capacity of G-protein-coupled receptor 30 (GPR30), an estrogen receptor that can be identified in hippocampal dendritic spines J. Biol. Chem. 288 2013 6438 6450
85. A. Pompili, B. Arnone, and A. Gasbarri Estrogens and memory in physiological and neuropathological conditions Psychoneuroendocrinology 37 2012 1379 1396
86. H.N. Fugger, T.C. Foster, J. Gustafsson, and E.F. Rissman Novel effects of estradiol and estrogen receptor alpha and beta on cognitive function Brain Res. 883 2000 258 264
87. M.E. Rhodes, and C.A. Frye ERbeta-selective SERMs produce mnemonic-enhancing effects in the inhibitory avoidance and water maze tasks Neurobiol. Learn. Mem. 85 2006 183 191
88. L.C. Sheldahl, R.A. Shapiro, D.N. Bryant, I.P. Koerner, and D.M. Dorsa Estrogen induces rapid translocation of estrogen receptor beta but not estrogen receptor alpha, to the neuronal plasma membrane Neuroscience 153 2008 751 761
89. T.C. Foster Role of estrogen receptor alpha and beta expression and signaling on cognitive function during aging Hippocampus 22 2012 656 669
90. X. Han, K.K. Aenlle, L.A. Bean, A. Rani, S.L. Semple-Rowland, A. Kumar, and T.C. Foster Role of estrogen receptor alpha and beta in preserving hippocampal function during aging J. Neurosci. 33 2013 2671 2683
91. K.K. Aenlle, and T.C. Foster Aging alters the expression of genes for neuroprotection and synaptic function following acute estradiol treatment Hippocampus 20 2010 1047 1060
92. R. Bi, M.R. Foy, R.M. Vouimba, R.F. Thompson, and M. Baudry Cyclic changes in estradiol regulate synaptic plasticity through the MAP kinase pathway Proc. Natl. Acad. Sci. U. S. A. 98 2001 13391 13395
93. M.R. Foy, M. Baudry, J.G. Foy, and R.F. Thompson 17beta-estradiol modifies stress-induced and age-related changes in hippocampal synaptic plasticity Behav. Neurosci. 122 2008 301 309
94. E.M. Waters, M. Yildirim, W.G. Janssen, W.Y. Lou, B.S. McEwen, J.H. Morrison, and T.A. Milner Estrogen and aging affect the synaptic distribution of estrogen receptor beta-immunoreactivity in the CA1 region of female rat hippocampus Brain Res. 1379 2011 86 97
95. M.I. Boulware, J.D. Heisler, and K.M. Frick The memory-enhancing effects of hippocampal estrogen receptor activation involve metabotropic glutamate receptor signaling J. Neurosci. 33 2013 15184 15194
96. H. Mukai, T. Tsurugizawa, G. Murakami, S. Kominami, H. Ishii, M. Ogiue-Ikeda, N. Takata, N. Tanabe, A. Furukawa, Y. Hojo, Y. Ooishi, J.H. Morrison, W.G. Janssen, J.A. Rose, P. Chambon, S. Kato, S. Izumi, T. Yamazaki, T. Kimoto, and S. Kawato Rapid modulation of long-term depression and spinogenesis via synaptic estrogen receptors in hippocampal principal neurons J. Neurochem. 100 2007 950 967
97. N.L. Desmond, D.X. Zhang, and W.B. Levy Estradiol enhances the induction of homosynaptic long-term depression in the CA1 region of the adult, ovariectomized rat Neurobiol. Learn. Mem. 73 2000 180 187
98. M. Morissette, M. Le Saux, and T. Di Paolo Effect of oestrogen receptor alpha and beta agonists on brain N-methyl-d-aspartate receptors J. Neuroendocrinol. 20 2008 1006 1014
99. K.M. Frick, S.M. Fernandez, and L.L. Harburger A new approach to understanding the molecular mechanisms through which estrogens affect cognition Biochim. Biophys. Acta 1800 2010 1045 1055
100. E.M. Waters, K. Mitterling, J.L. Spencer, S. Mazid, B.S. McEwen, and T.A. Milner Estrogen receptor alpha and beta specific agonists regulate expression of synaptic proteins in rat hippocampus Brain Res. 1290 2009 1 11
101. D.A. Velazquez-Zamora, D. Gonzalez-Tapia, M.M. Gonzalez-Ramirez, M.E. Flores-Soto, E. Vazquez-Valls, M. Cervantes, and I. Gonzalez-Burgos Plastic changes in dendritic spines of hippocampal CA1 pyramidal neurons from ovariectomized rats after estradiol treatment Brain Res. 1470 2012 1 10
102. L. Fester, L. Zhou, C. Voets, C. Ossig, E. Disteldorf, F. Blaute, J. Prange-Kiel, D. Dudzinski, H. Jarry, and G.M. Rune The opposing roles of estradiol on synaptic protein expression in hippocampal cultures Psychoneuroendocrinology 34 Suppl. 1 2009 S123 129
103. D.P. Srivastava, K.M. Woolfrey, and P.D. Evans Mechanisms underlying the interactions between rapid estrogenic and BDNF control of synaptic connectivity Neuroscience 239 2013 17 33
104. D.P. Srivastava, and P. Penzes Rapid estradiol modulation of neuronal connectivity and its implications for disease Front. Endocrinol. (Lausanne) 2 2011 77
105. A. Phan, C.S. Gabor, K.J. Favaro, S. Kaschack, J.N. Armstrong, N.J. MacLusky, and E. Choleris Low doses of 17beta-estradiol rapidly improve learning and increase hippocampal dendritic spines Neuropsychopharmacology 37 2012 2299 2309
106. S. Mortillo, A. Elste, Y. Ge, S.B. Patil, K. Hsiao, G.W. Huntley, R.L. Davis, and D.L. Benson Compensatory redistribution of neuroligins and N-cadherin following deletion of synaptic beta1-integrin J. Comp. Neurol. 520 2012 2041 2052
107. V. Luine, and M. Frankfurt Interactions between estradiol, BDNF and dendritic spines in promoting memory Neuroscience 239 2013 34 45
108. E. Gould, N. Vail, M. Wagers, and C.G. Gross Adult-generated hippocampal and neocortical neurons in macaques have a transient existence Proc. Natl. Acad. Sci. U. S. A. 98 2001 10910 10917
109. N.F. Ho, J.M. Hooker, A. Sahay, D.J. Holt, and J.L. Roffman In vivo imaging of adult human hippocampal neurogenesis: progress, pitfalls and promise Mol. Psychiatry 18 2013 404 416
110. K.K. Aenlle, A. Kumar, L. Cui, T.C. Jackson, and T.C. Foster Estrogen effects on cognition and hippocampal transcription in middle-aged mice Neurobiol. Aging 30 2009 932 945
111. C. Takeo, K. Ikeda, K. Horie-Inoue, and S. Inoue Identification of Igf2, Igfbp2 and Enpp2 as estrogen-responsive genes in rat hippocampus Endocr. J. 56 2009 113 120
112. A.S. Pechenino, and K.M. Frick The effects of acute 17beta-estradiol treatment on gene expression in the young female mouse hippocampus Neurobiol. Learn. Mem. 91 2009 315 322
113. J.S. Guan, S.J. Haggarty, E. Giacometti, J.H. Dannenberg, N. Joseph, J. Gao, T.J. Nieland, Y. Zhou, X. Wang, R. Mazitschek, J.E. Bradner, R.A. DePinho, R. Jaenisch, and L.H. Tsai HDAC2 negatively regulates memory formation and synaptic plasticity Nature 459 2009 55 60
114. N.J. MacLusky, T. Hajszan, J. Prange-Kiel, and C. Leranth Androgen modulation of hippocampal synaptic plasticity Neuroscience 138 2006 957 965
115. J.C. Carroll, and E.R. Rosario The potential use of hormone-based therapeutics for the treatment of Alzheimer's disease Curr. Alzheimer Res. 9 2012 18 34
116. F. Labrie, V. Luu-The, C. Labrie, A. Belanger, J. Simard, S.X. Lin, and G. Pelletier Endocrine and intracrine sources of androgens in women: inhibition of breast cancer and other roles of androgens and their precursor dehydroepiandrosterone Endocr. Rev. 24 2003 152 182
117. A. Colciago, F. Celotti, A. Pravettoni, O. Mornati, L. Martini, and P. Negri-Cesi Dimorphic expression of testosterone metabolizing enzymes in the hypothalamic area of developing rats Brain Res. Dev. Brain Res. 155 2005 107 116
118. L. Martini, R.C. Melcangi, and R. Maggi Androgen and progesterone metabolism in the central and peripheral nervous system J. Steroid Biochem. Mol. Biol. 47 1993 195 205
119. M. Ginsburg, N.J. Maclusky, I.D. Morris, and P.J. Thomas The specificity of oestrogen receptor in brain, pituitary and uterus Br. J. Pharmacol. 59 1977 397 402
120. R.C. Melcangi, F. Celotti, M. Ballabio, P. Castano, A. Poletti, S. Milani, and L. Martini Ontogenetic development of the 5 alpha-reductase in the rat brain: cerebral cortex, hypothalamus, purified myelin and isolated oligodendrocytes Brain Res. Dev. Brain Res. 44 1988 181 188
121. Y. Hojo, S. Higo, S. Kawato, Y. Hatanaka, Y. Ooishi, G. Murakami, H. Ishii, Y. Komatsuzaki, M. Ogiue-Ikeda, H. Mukai, and T. Kimoto Hippocampal synthesis of sex steroids and corticosteroids: essential for modulation of synaptic plasticity Front. Endocrinol. (Lausanne) 2 2011 43
122. C. Armoskus, D. Moreira, K. Bollinger, O. Jimenez, S. Taniguchi, and H.W. Tsai Identification of sexually dimorphic genes in the neonatal mouse cortex and hippocampus Brain Res. 1562 2014 23 38
123. C.J. Scott, I.J. Clarke, A. Rao, and A.J. Tilbrook Sex differences in the distribution and abundance of androgen receptor mRNA-containing cells in the preoptic area and hypothalamus of the ram and ewe J. Neuroendocrinol. 16 2004 956 963
124. S. Beyenburg, M. Watzka, H. Clusmann, I. Blumcke, F. Bidlingmaier, C.E. Elger, and B. Stoffel-Wagner Androgen receptor mRNA expression in the human hippocampus Neurosci. Lett. 294 2000 25 28
125. J.E. Kerr, R.J. Allore, S.G. Beck, and R.J. Handa Distribution and hormonal regulation of androgen receptor (AR) and AR messenger ribonucleic acid in the rat hippocampus Endocrinology 136 1995 3213 3221
126. H. Tohgi, K. Utsugisawa, M. Yamagata, and M. Yoshimura Effects of age on messenger RNA expression of glucocorticoid, thyroid hormone, androgen, and estrogen receptors in postmortem human hippocampus Brain Res. 700 1995 245 253
127. P. Negri-Cesi, A. Colciago, F. Celotti, and M. Motta Sexual differentiation of the brain: role of testosterone and its active metabolites J. Endocrinol. Invest. 27 2004 120 127
128. S.D. Moffat, A.B. Zonderman, E.J. Metter, C. Kawas, M.R. Blackman, S.M. Harman, and S.M. Resnick Free testosterone and risk for Alzheimer disease in older men Neurology 62 2004 188 193
129. R.L. Roof, and M.D. Havens Testosterone improves maze performance and induces development of a male hippocampus in females Brain Res. 572 1992 310 313
130. J.F. Flood, J.E. Morley, and E. Roberts Memory-enhancing effects in male mice of pregnenolone and steroids metabolically derived from it Proc. Natl. Acad. Sci. U. S. A. 89 1992 1567 1571
131. J.S. Janowsky, S.K. Oviatt, and E.S. Orwoll Testosterone influences spatial cognition in older men Behav. Neurosci. 108 1994 325 332
132. C.W. Harley, C.W. Malsbury, A. Squires, and R.A. Brown Testosterone decreases CA1 plasticity in vivo in gonadectomized male rats Hippocampus 10 2000 693 697
133. P.C. Hebbard, R.R. King, C.W. Malsbury, and C.W. Harley Two organizational effects of pubertal testosterone in male rats: transient social memory and a shift away from long-term potentiation following a tetanus in hippocampal CA1 Exp. Neurol. 182 2003 470 475
134. V.E. Pettorossi, M. Di Mauro, M. Scarduzio, R. Panichi, A. Tozzi, P. Calabresi, and S. Grassi Modulatory role of androgenic and estrogenic neurosteroids in determining the direction of synaptic plasticity in the CA1 hippocampal region of male rats Physiol. Rep. 1 2013 e00185
135. S. Grassi, A. Frondaroli, C. Dieni, and M. Scarduzio Effects of 17beta-estradiol on synaptic plasticity in the rat medial vestibular nuclei Acta Otolaryngol. 129 2009 390 394
136. S. Li, L. Kang, C. Zhang, G. Xie, N. Li, Y. Zhang, J. Du, and H. Cui Effects of dihydrotestosterone on synaptic plasticity of hippocampus in male SAMP8 mice Exp. Gerontol. 48 2013 778 785
137. T.J. McHugh, K.I. Blum, J.Z. Tsien, S. Tonegawa, and M.A. Wilson Impaired hippocampal representation of space in CA1-specific NMDAR1 knockout mice Cell 87 1996 1339 1349
138. D.J. Selkoe Alzheimer's disease is a synaptic failure Science 298 2002 789 791
139. C.S. Woolley, and B.S. McEwen Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat J. Neurosci. 12 1992 2549 2554
140. C.C. Wimer, and R.E. Wimer On the sources of strain and sex differences in granule cell number in the dentate area of house mice Brain Res. Dev. Brain Res. 48 1989 167 176
141. A. Parducz, and L.M. Garcia-Segura Sexual differences in the synaptic connectivity in the rat dentate gyrus Neurosci. Lett. 161 1993 53 56
142. T.J. Shors, C. Chua, and J. Falduto Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus J. Neurosci. 21 2001 6292 6297
143. R. Yuste, and T. Bonhoeffer Morphological changes in dendritic spines associated with long-term synaptic plasticity Annu. Rev. Neurosci. 24 2001 1071 1089
144. M. Li, M. Masugi-Tokita, K. Takanami, S. Yamada, and M. Kawata Testosterone has sublayer-specific effects on dendritic spine maturation mediated by BDNF and PSD-95 in pyramidal neurons in the hippocampus CA1 area Brain Res. 1484 2012 76 84
145. X. Gao, G.M. Smith, and J. Chen Impaired dendritic development and synaptic formation of postnatal-born dentate gyrus granular neurons in the absence of brain-derived neurotrophic factor signaling Exp. Neurol. 215 2009 178 190
146. A.L. Mendell, K. Szigeti-Buck, N.J. MacLusky, and C. Leranth Orchidectomy does not significantly affect spine synapse density in the CA3 hippocampal subfield in St. Kitts vervet monkeys (Chlorocebus aethiops sabaeus) Neurosci. Lett. 559 2014 189 192
147. V.A. Skucas, A.M. Duffy, L.C. Harte-Hargrove, A. Magagna-Poveda, T. Radman, G. Chakraborty, C.E. Schroeder, N.J. MacLusky, and H.E. Scharfman Testosterone depletion in adult male rats increases mossy fiber transmission, LTP, and sprouting in area CA3 of hippocampus J. Neurosci. 33 2013 2338 2355
148. R.M. Goel, and A.R. Cappola Dehydroepiandrosterone sulfate and postmenopausal women Curr. Opin. Endocrinol. Diabetes Obes. 18 2011 171 176
149. I.H. Zwain, and S.S. Yen Dehydroepiandrosterone: biosynthesis and metabolism in the brain Endocrinology 140 1999 880 887
150. P.H. Jellinck, M. Kaufmann, A. Gottfried-Blackmore, B.S. McEwen, G. Jones, and K. Bulloch Selective conversion by microglia of dehydroepiandrosterone to 5-androstenediol-A steroid with inherent estrogenic properties J. Steroid Biochem. Mol. Biol. 107 2007 156 162
151. P.H. Jellinck, G. Croft, B.S. McEwen, A. Gottfried-Blackmore, G. Jones, V. Byford, and K. Bulloch Metabolism of dehydroepiandrosterone by rodent brain cell lines: relationship between 7-hydroxylation and aromatization J. Steroid Biochem. Mol. Biol. 93 2005 81 86
152. L. Starka, M. Duskova, and M. Hill Dehydroepiandrosterone: a neuroactive steroid J. Steroid Biochem. Mol. Biol. 145 2014 254 260
153. H.F. Sakr, K.I. Khalil, A.M. Hussein, M.S. Zaki, R.A. Eid, and M. Alkhateeb Effect of dehydroepiandrosterone (DHEA) on memory and brain derived neurotrophic factor (BDNF) in a rat model of vascular dementia J. Physiol. Pharmacol. 65 2014 41 53
154. J.R. Chen, G.F. Tseng, Y.J. Wang, and T.J. Wang Exogenous dehydroisoandrosterone sulfate reverses the dendritic changes of the central neurons in aging male rats Exp. Gerontol. 57C 2014 191 202
155. H. Mukai, T. Tsurugizawa, M. Ogiue-Ikeda, G. Murakami, Y. Hojo, H. Ishii, T. Kimoto, and S. Kawato Local neurosteroid production in the hippocampus: influence on synaptic plasticity of memory Neuroendocrinology 84 2006 255 263
156. N. Samaras, D. Samaras, E. Frangos, A. Forster, and J. Philippe A review of age-related dehydroepiandrosterone decline and its association with well-known geriatric syndromes: is treatment beneficial? Rejuvenation Res. 16 2013 285 294
157. M. Singh, and C. Su Progesterone-induced neuroprotection: factors that may predict therapeutic efficacy Brain Res. 1514 2013 98 106
158. M. Singh, C. Su, and S. Ng Non-genomic mechanisms of progesterone action in the brain Front. Neurosci. 7 2013 159
159. M. Schumacher, C. Mattern, A. Ghoumari, J.P. Oudinet, P. Liere, F. Labombarda, R. Sitruk-Ware, A.F. De Nicola, and R. Guennoun Revisiting the roles of progesterone and allopregnanolone in the nervous system: resurgence of the progesterone receptors Prog. Neurobiol. 113 2014 6 39
160. E. Vegeto, M.M. Shahbaz, D.X. Wen, M.E. Goldman, B.W. O'Malley, and D.P. McDonnell Human progesterone receptor A form is a cell-and promoter-specific repressor of human progesterone receptor B function Mol. Endocrinol. 7 1993 1244 1255
161. V. Boonyaratanakornkit, M.P. Scott, V. Ribon, L. Sherman, S.M. Anderson, J.L. Maller, W.T. Miller, and D.P. Edwards Progesterone receptor contains a proline-rich motif that directly interacts with SH3 domains and activates c-Src family tyrosine kinases Mol. Cell 8 2001 269 280
162. C.R. Hagan, A.R. Daniel, G.E. Dressing, and C.A. Lange Role of phosphorylation in progesterone receptor signaling and specificity Mol. Cell. Endocrinol. 357 2012 43 49
163. A. Poletti, A. Coscarella, P. Negri-Cesi, A. Colciago, F. Celotti, and L. Martini 5α-reductase isozymes in the central nervous system Steroids 63 1998 246 251
164. M. Wang Neurosteroids and GABA-A receptor function Front. Endocrinol. (Lausanne) 2 2011 44
165. C.J. Koonce, and C.A. Frye Progesterone facilitates exploration affective and social behaviors among wildtype, but not 5alpha-reductase Type 1 mutant, mice Behav. Brain Res. 253 2013 232 239
166. C.A. Frye, C.J. Koonce, and A.A. Walf Progesterone compared to medroxyprogesterone acetate, to C57BL/6, but not 5alpha-reductase mutant, mice enhances object recognition and placement memory and is associated with higher BDNF levels in the hippocampus and cortex Neurosci. Lett. 551 2013 53 57
167. M.R. Foy, G. Akopian, and R.F. Thompson Progesterone regulation of synaptic transmission and plasticity in rodent hippocampus Learn. Mem. 15 2008 820 822
168. M.B. Herd, A.R. Haythornthwaite, T.W. Rosahl, K.A. Wafford, G.E. Homanics, J.J. Lambert, and D. Belelli The expression of GABAA beta subunit isoforms in synaptic and extrasynaptic receptor populations of mouse dentate gyrus granule cells J. Physiol. 586 2008 989 1004
169. C.A. Shively, and C.L. Bethea Cognition, mood disorders, and sex hormones ILAR J. 45 2004 189 199
170. K. Ito, K.L. Skinkle, and T.P. Hicks Age-dependent, steroid-specific effects of oestrogen on long-term potentiation in rat hippocampal slices J. Physiol. 515 Pt 1 1999 209 220
171. B.S. McEwen, and C.S. Woolley Estradiol and progesterone regulate neuronal structure and synaptic connectivity in adult as well as developing brain Exp. Gerontol. 29 1994 431 436
172. C.S. Woolley, and B.S. McEwen Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat J. Comp. Neurol. 336 1993 293 306
173. I. Ciriza, P. Carrero, C.A. Frye, and L.M. Garcia-Segura Reduced metabolites mediate neuroprotective effects of progesterone in the adult rat hippocampus. The synthetic progestin medroxyprogesterone acetate (Provera) is not neuroprotective J. Neurobiol. 66 2006 916 928
174. E.W. Freeman, L. Weinstock, K. Rickels, S.J. Sondheimer, and C. Coutifaris A placebo-controlled study of effects of oral progesterone on performance and mood Br. J. Clin. Pharmacol. 33 1992 293 298
175. G. van Wingen, F. van Broekhoven, R.J. Verkes, K.M. Petersson, T. Backstrom, J. Buitelaar, and G. Fernandez How progesterone impairs memory for biologically salient stimuli in healthy young women J. Neurosci. 27 2007 11416 11423
176. M. Sofuoglu, M. Mouratidis, and M. Mooney Progesterone improves cognitive performance and attenuates smoking urges in abstinent smokers Psychoneuroendocrinology 36 2011 123 132
177. I.M. Johansson, V. Birzniece, C. Lindblad, T. Olsson, and T. Backstrom Allopregnanolone inhibits learning in the Morris water maze Brain Res. 934 2002 125 131
178. A. Rabinowitz, S.J. Cohen, D.A. Finn, and R.W. Stackman Jr. The neurosteroid allopregnanolone impairs object memory and contextual fear memory in male C57BL/6J mice Horm. Behav. 66 2014 238 246
179. S.K. Bengtsson, M. Johansson, T. Backstrom, and M. Wang Chronic allopregnanolone treatment accelerates Alzheimer's disease development in AbetaPP(Swe)PSEN1(DeltaE9) mice J. Alzheimers Dis. 31 2012 71 84
180. S.K. Bengtsson, M. Johansson, T. Backstrom, R.M. Nitsch, and M. Wang Brief but chronic increase in allopregnanolone cause accelerated AD pathology differently in two mouse models Curr. Alzheimer Res. 10 2013 38 47
181. R.W. Irwin, and R.D. Brinton Allopregnanolone as regenerative therapeutic for Alzheimer's disease: translational development and clinical promise Prog. Neurobiol. 113 2014 40 55
182. J.M. Wang, C. Singh, L. Liu, R.W. Irwin, S. Chen, E.J. Chung, R.F. Thompson, and R.D. Brinton Allopregnanolone reverses neurogenic and cognitive deficits in mouse model of Alzheimer's disease Proc. Natl. Acad. Sci. U. S. A. 107 2010 6498 6503
183. C. Singh, L. Liu, J.M. Wang, R.W. Irwin, J. Yao, S. Chen, S. Henry, R.F. Thompson, and R.D. Brinton Allopregnanolone restores hippocampal-dependent learning and memory and neural progenitor survival in aging 3xTgAD and nonTg mice Neurobiol. Aging 33 2012 1493 1506
184. V.S. Chin, C.E. Van Skike, R.B. Berry, R.E. Kirk, J. Diaz-Granados, and D.B. Matthews Effect of acute ethanol and acute allopregnanolone on spatial memory in adolescent and adult rats Alcohol 45 2011 473 483
185. M. Singh, E.M. Meyer, and J.W. Simpkins The effect of ovariectomy and estradiol replacement on brain-derived neurotrophic factor messenger ribonucleic acid expression in cortical and hippocampal brain regions of female Sprague-Dawley rats Endocrinology 136 1995 2320 2324
186. P. Kaur, P.K. Jodhka, W.A. Underwood, C.A. Bowles, N.C. de Fiebre, C.M. de Fiebre, and M. Singh 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. 85 2007 2441 2449
187. M.C. Gonzalez Deniselle, L. Garay, S. Gonzalez, F. Saravia, F. Labombarda, R. Guennoun, M. Schumacher, and A.F. De Nicola Progesterone modulates brain-derived neurotrophic factor and choline acetyltransferase in degenerating Wobbler motoneurons Exp. Neurol. 203 2007 406 414
188. C.C. Aguirre, and M. Baudry Progesterone reverses 17beta-estradiol-mediated neuroprotection and BDNF induction in cultured hippocampal slices Eur. J. Neurosci. 29 2009 447 454
189. P.K. Jodhka, P. Kaur, W. Underwood, J.P. Lydon, and M. Singh The differences in neuroprotective efficacy of progesterone and medroxyprogesterone acetate correlate with their effects on brain-derived neurotrophic factor expression Endocrinology 150 2009 3162 3168
190. C. Su, R.L. Cunningham, N. Rybalchenko, and M. Singh Progesterone increases the release of brain-derived neurotrophic factor from glia via progesterone receptor membrane component 1 (Pgrmc1)-dependent ERK5 signaling Endocrinology 153 2012 4389 4400
191. H.A. Bimonte-Nelson, K.R. Francis, C.D. Umphlet, and A.C. Granholm Progesterone reverses the spatial memory enhancements initiated by tonic and cyclic oestrogen therapy in middle-aged ovariectomized female rats Eur. J. Neurosci. 24 2006 229 242
192. M. Baudry, X. Bi, and C. Aguirre Progesterone-estrogen interactions in synaptic plasticity and neuroprotection Neuroscience 239 2013 280 294
193. C.K. McIntyre, J.L. McGaugh, and C.L. Williams Interacting brain systems modulate memory consolidation Neurosci. Biobehav. Rev. 36 2012 1750 1762
194. E.R. de Kloet, M. Joels, and F. Holsboer Stress and the brain: from adaptation to disease Nat. Rev. Neurosci. 6 2005 463 475
195. F.L. Groeneweg, H. Karst, E.R. de Kloet, and M. Joels Mineralocorticoid and glucocorticoid receptors at the neuronal membrane, regulators of nongenomic corticosteroid signalling Mol. Cell. Endocrinol. 350 2012 299 309
196. S. Yang, F. Roselli, A.V. Patchev, S. Yu, and O.F. Almeida Non-receptor-tyrosine kinases integrate fast glucocorticoid signaling in hippocampal neurons J. Biol. Chem. 288 2013 23725 23739
197. J. Stromberg, T. Backstrom, and P. Lundgren Rapid non-genomic effect of glucocorticoid metabolites and neurosteroids on the γ-aminobutyric acid-A receptor Eur. J. Neurosci. 21 2005 2083 2088
198. Y. Matsusue, N. Horii-Hayashi, T. Kirita, and M. Nishi Distribution of corticosteroid receptors in mature oligodendrocytes and oligodendrocyte progenitors of the adult mouse brain J. Histochem. Cytochem. 62 2014 211 226
199. A.E. Wurmser, T.D. Palmer, and F.H. Gage Neuroscience. Cellular interactions in the stem cell niche Science 304 2004 1253 1255
200. D.J. Saaltink, and E. Vreugdenhil Stress, glucocorticoid receptors, and adult neurogenesis: a balance between excitation and inhibition? Cell. Mol. Life Sci. 71 13 2014 2499 2515
201. N.A. Datson, M.C. Morsink, O.C. Meijer, and E.R. de Kloet Central corticosteroid actions: search for gene targets Eur. J. Pharmacol. 583 2008 272 289
202. F.L. Groeneweg, H. Karst, E.R. de Kloet, and M. Joels Rapid non-genomic effects of corticosteroids and their role in the central stress response J. Endocrinol. 209 2011 153 167
203. P. Atsak, B. Roozendaal, and P. Campolongo Role of the endocannabinoid system in regulating glucocorticoid effects on memory for emotional experiences Neuroscience 204 2012 104 116
204. D.J. de Quervain, A. Aerni, G. Schelling, and B. Roozendaal Glucocorticoids and the regulation of memory in health and disease Front. Neuroendocrinol. 30 2009 358 370
205. B.S. McEwen Plasticity of the hippocampus: adaptation to chronic stress and allostatic load Ann. N. Y. Acad. Sci. 933 2001 265 277
206. H.C. Abercrombie, N.S. Speck, and R.M. Monticelli Endogenous cortisol elevations are related to memory facilitation only in individuals who are emotionally aroused Psychoneuroendocrinology 31 2006 187 196
207. C. Finsterwald, and C.M. Alberini Stress and glucocorticoid receptor-dependent mechanisms in long-term memory: From adaptive responses to psychopathologies Neurobiol. Learn. Mem. 112 2013 17 29
208. J.D. Gray, T.A. Milner, and B.S. McEwen Dynamic plasticity: the role of glucocorticoids, brain-derived neurotrophic factor and other trophic factors Neuroscience 239 2013 214 227
209. J.L. McGaugh The amygdala modulates the consolidation of memories of emotionally arousing experiences Ann. Rev. Neurosci. 27 2004 1 28
210. T. Canli, Z. Zhao, J. Brewer, J.D. Gabrieli, and L. Cahill Event-related activation in the human amygdala associates with later memory for individual emotional experience J. Neurosci. 20 2000 RC99
211. R. Adolphs, L. Cahill, R. Schul, and R. Babinsky Impaired declarative memory for emotional material following bilateral amygdala damage in humans Learn. Mem. 4 1997 291 300
212. D.J. de Quervain, B. Roozendaal, R.M. Nitsch, J.L. McGaugh, and C. Hock Acute cortisone administration impairs retrieval of long-term declarative memory in humans Nat. Neurosci. 3 2000 313 314
213. S. Kuhlmann, M. Piel, and O.T. Wolf Impaired memory retrieval after psychosocial stress in healthy young men J. Neurosci. 25 2005 2977 2982
214. R.M. Sapolsky, L.C. Krey, and B.S. McEwen The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis Endocr. Rev. 7 1986 284 301
215. C.D. Conrad Chronic stress-induced hippocampal vulnerability: the glucocorticoid vulnerability hypothesis Rev. Neurosci. 19 2008 395 411
216. D. Suri, and V.A. Vaidya Glucocorticoid regulation of brain-derived neurotrophic factor: relevance to hippocampal structural and functional plasticity Neuroscience 239 2013 196 213
217. J. Wei, E.Y. Yuen, W. Liu, X. Li, P. Zhong, I.N. Karatsoreos, B.S. McEwen, and Z. Yan Estrogen protects against the detrimental effects of repeated stress on glutamatergic transmission and cognition Mol. Psychiatry 19 5 2013 588 598
218. F. Crick Memory and molecular turnover Nature 312 1984 101
219. J.J. Day, and J.D. Sweatt DNA methylation and memory formation Nat. Neurosci. 13 2010 1319 1323
220. J.J. Day, and J.D. Sweatt Epigenetic mechanisms in cognition Neuron 70 2011 813 829
221. T.L. Roth, and J.D. Sweatt Regulation of chromatin structure in memory formation Curr. Opin. Neurobiol. 19 2009 336 342
222. C.A. Miller, S.L. Campbell, and J.D. Sweatt DNA methylation and histone acetylation work in concert to regulate memory formation and synaptic plasticity Neurobiol. Learn. Mem. 89 2008 599 603
223. A. Fischer, F. Sananbenesi, X. Wang, M. Dobbin, and L.H. Tsai Recovery of learning and memory is associated with chromatin remodelling Nature 447 2007 178 182
224. R.G. Hunter, K.J. McCarthy, T.A. Milne, D.W. Pfaff, and B.S. McEwen Regulation of hippocampal H3 histone methylation by acute and chronic stress Proc. Natl. Acad. Sci. U. S. A. 106 2009 20912 20917
225. Z. Zhao, L. Fan, and K.M. Frick Epigenetic alterations regulate estradiol-induced enhancement of memory consolidation Proc. Natl. Acad. Sci. U. S. A. 107 2010 5605 5610
226. C.A. Miller, C.F. Gavin, J.A. White, R.R. Parrish, A. Honasoge, C.R. Yancey, I.M. Rivera, M.D. Rubio, G. Rumbaugh, and J.D. Sweatt Cortical DNA methylation maintains remote memory Nat. Neurosci. 13 2010 664 666
227. S.A. Maddox, C.S. Watts, and G.E. Schafe p300/CBP histone acetyltransferase activity is required for newly acquired and reactivated fear memories in the lateral amygdala Learn. Mem. 20 2013 109 119
228. M.W. Swank, and J.D. Sweatt Increased histone acetyltransferase and lysine acetyltransferase activity and biphasic activation of the ERK/RSK cascade in insular cortex during novel taste learning J. Neurosci. 21 2001 3383 3391
229. R. Metivier, R. Gallais, C. Tiffoche, C. Le Peron, R.Z. Jurkowska, R.P. Carmouche, D. Ibberson, P. Barath, F. Demay, G. Reid, V. Benes, A. Jeltsch, F. Gannon, and G. Salbert Cyclical DNA methylation of a transcriptionally active promoter Nature 452 2008 45 50
230. R.M. Kohli, and Y. Zhang TET enzymes, TDG and the dynamics of DNA demethylation Nature 502 2013 472 479
231. D.K. Ma, M.H. Jang, J.U. Guo, Y. Kitabatake, M.L. Chang, N. Pow-Anpongkul, R.A. Flavell, B. Lu, G.L. Ming, and H. Song Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis Science 323 2009 1074 1077
232. K.D. Robertson DNA methylation and human disease Nat. Rev. Genet. 6 2005 597 610
233. M. Chahrour, S.Y. Jung, C. Shaw, X. Zhou, S.T. Wong, J. Qin, and H.Y. Zoghbi MeCP2 a key contributor to neurological disease, activates and represses transcription Science 320 2008 1224 1229
234. H. Denis, M.N. Ndlovu, and F. Fuks Regulation of mammalian DNA methyltransferases: a route to new mechanisms EMBO Rep. 12 2011 647 656
235. M. Okano, D.W. Bell, D.A. Haber, and E. Li DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development Cell 99 1999 247 257
236. J. Feng, Y. Zhou, S.L. Campbell, T. Le, E. Li, J.D. Sweatt, A.J. Silva, and G. Fan Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons Nat. Neurosci. 13 2010 423 430
237. J.M. Levenson, T.L. Roth, F.D. Lubin, C.A. Miller, I.C. Huang, P. Desai, L.M. Malone, and J.D. Sweatt Evidence that DNA (cytosine-5) methyltransferase regulates synaptic plasticity in the hippocampus J. Biol. Chem. 281 2006 15763 15773
238. J.U. Guo, Y. Su, C. Zhong, G.L. Ming, and H. Song Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain Cell 145 2011 423 434
239. F.D. Lubin, T.L. Roth, and J.D. Sweatt Epigenetic regulation of BDNF gene transcription in the consolidation of fear memory J. Neurosci. 28 2008 10576 10586
240. B.H. Miller, Z. Zeier, L. Xi, T.A. Lanz, S. Deng, J. Strathmann, D. Willoughby, P.J. Kenny, J.D. Elsworth, M.S. Lawrence, R.H. Roth, D. Edbauer, R.J. Kleiman, and C. Wahlestedt MicroRNA-132 dysregulation in schizophrenia has implications for both neurodevelopment and adult brain function Proc. Natl. Acad. Sci. U. S. A. 109 2012 3125 3130
241. C.A. Miller, and J.D. Sweatt Covalent modification of DNA regulates memory formation Neuron 53 2007 857 869
242. V. Coskun, R. Tsoa, and Y.E. Sun Epigenetic regulation of stem cells differentiating along the neural lineage Curr. Opin. Neurobiol. 22 2012 762 767
243. M. Szyf DNA methylation, behavior and early life adversity J. Genet. Genomics 40 2013 331 338
244. C. Zhao, W. Deng, and F.H. Gage Mechanisms and functional implications of adult neurogenesis Cell 132 2008 645 660
245. J.B. Aimone, W. Deng, and F.H. Gage Resolving new memories: a critical look at the dentate gyrus, adult neurogenesis, and pattern separation Neuron 70 2011 589 596
246. R. Faigle, and H. Song Signaling mechanisms regulating adult neural stem cells and neurogenesis Biochim. Biophys. Acta 1830 2013 2435 2448
247. I.C. Weaver, J. Diorio, J.R. Seckl, M. Szyf, and M.J. Meaney Early environmental regulation of hippocampal glucocorticoid receptor gene expression: characterization of intracellular mediators and potential genomic target sites Ann. N. Y. Acad. Sci. 1024 2004 182 212
248. P.O. McGowan, A. Sasaki, A.C. D'Alessio, S. Dymov, B. Labonte, M. Szyf, G. Turecki, and M.J. Meaney Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse Nat. Neurosci. 12 2009 342 348
249. M. Suderman, P.O. McGowan, A. Sasaki, T.C. Huang, M.T. Hallett, M.J. Meaney, G. Turecki, and M. Szyf Conserved epigenetic sensitivity to early life experience in the rat and human hippocampus Proc. Natl. Acad. Sci. U. S. A. 210 Suppl. 2 2012 17266 17272
250. A.M. Fortress, and K.M. Frick Epigenetic regulation of estrogen-dependent memory Front. Neuroendocrinol. 35 4 2014 530 549
251. J.S. Guan, H. Xie, and X. Ding The role of epigenetic regulation in learning and memory Exp. Neurol. 2014 10.1016/j.expneurol.2014.05.006
252. K.M. Frick Epigenetics, oestradiol and hippocampal memory consolidation J. Neuroendocrinol. 25 2013 1151 1162
253. E. Korzus, M.G. Rosenfeld, and M. Mayford CBP histone acetyltransferase activity is a critical component of memory consolidation Neuron 42 2004 961 972
254. M.A. Wood, M.A. Attner, A.M. Oliveira, P.K. Brindle, and T. Abel A transcription factor-binding domain of the coactivator CBP is essential for long-term memory and the expression of specific target genes Learn. Mem. 13 2006 609 617
255. A.M. Oliveira, M.A. Wood, C.B. McDonough, and T. Abel Transgenic mice expressing an inhibitory truncated form of p300 exhibit long-term memory deficits Learn. Mem. 14 2007 564 572
256. J.M. Alarcon, G. Malleret, K. Touzani, S. Vronskaya, S. Ishii, E.R. Kandel, and A. Barco Chromatin acetylation, memory, and LTP are impaired in CBP+/-mice: a model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration Neuron 42 2004 947 959
257. T.W. Bredy, and M. Barad The histone deacetylase inhibitor valproic acid enhances acquisition, extinction, and reconsolidation of conditioned fear Learn. Mem. 15 2008 39 45
258. C.G. Vecsey, J.D. Hawk, K.M. Lattal, J.M. Stein, S.A. Fabian, M.A. Attner, S.M. Cabrera, C.B. McDonough, P.K. Brindle, T. Abel, and M.A. Wood Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB:CBP-dependent transcriptional activation J. Neurosci. 27 2007 6128 6140
259. J. Gao, W.Y. Wang, Y.W. Mao, J. Graff, J.S. Guan, L. Pan, G. Mak, D. Kim, S.C. Su, and L.H. Tsai A novel pathway regulates memory and plasticity via SIRT1 and miR-134 Nature 466 2010 1105 1109
260. M.S. Kim, M.W. Akhtar, M. Adachi, M. Mahgoub, R. Bassel-Duby, E.T. Kavalali, E.N. Olson, and L.M. Monteggia An essential role for histone deacetylase 4 in synaptic plasticity and memory formation J. Neurosci. 32 2012 10879 10886
261. J.M. Levenson, K.J. O'Riordan, K.D. Brown, M.A. Trinh, D.L. Molfese, and J.D. Sweatt Regulation of histone acetylation during memory formation in the hippocampus J. Biol. Chem. 279 2004 40545 40559
262. D.P. Stefanko, R.M. Barrett, A.R. Ly, G.K. Reolon, and M.A. Wood Modulation of long-term memory for object recognition via HDAC inhibition Proc. Natl. Acad. Sci. U. S. A. 106 2009 9447 9452
263. S. Gupta, S.Y. Kim, S. Artis, D.L. Molfese, A. Schumacher, J.D. Sweatt, R.E. Paylor, and F.D. Lubin Histone methylation regulates memory formation J. Neurosci. 30 2010 3589 3599
264. S. Gupta-Agarwal, A.V. Franklin, T. Deramus, M. Wheelock, R.L. Davis, L.L. McMahon, and F.D. Lubin G9a/GLP histone lysine dimethyltransferase complex activity in the hippocampus and the entorhinal cortex is required for gene activation and silencing during memory consolidation J. Neurosci. 32 2012 5440 5453
265. W.B. Chwang, K.J. O'Riordan, J.M. Levenson, and J.D. Sweatt ERK/MAPK regulates hippocampal histone phosphorylation following contextual fear conditioning Learn. Mem. 13 2006 322 328
266. J.M. Reul Making memories of stressful events: a journey along epigenetic, gene transcription, and signaling pathways Front. Psychiatry 5 2014 5
267. B.R. Selvi, J.C. Cassel, T.K. Kundu, and A.L. Boutillier Tuning acetylation levels with HAT activators: therapeutic strategy in neurodegenerative diseases Biochim. Biophys. Acta 1799 2010 840 853
268. B. Roozendaal, A. Hernandez, S.M. Cabrera, R. Hagewoud, M. Malvaez, D.P. Stefanko, J. Haettig, and M.A. Wood Membrane-associated glucocorticoid activity is necessary for modulation of long-term memory via chromatin modification J. Neurosci. 30 2010 5037 5046
269. J.M. Daniel Effects of oestrogen on cognition: what have we learned from basic research? J. Neuroendocrinol. 18 2006 787 795
270. V.N. Luine, L.F. Jacome, and N.J. Maclusky Rapid enhancement of visual and place memory by estrogens in rats Endocrinology 144 2003 2836 2844
271. C.A. Frye, C.K. Duffy, and A.A. Walf Estrogens and progestins enhance spatial learning of intact and ovariectomized rats in the object placement task Neurobiol. Learn. Mem. 88 2007 208 216
272. J.E. Gresack, and K.M. Frick Post-training estrogen enhances spatial and object memory consolidation in female mice Pharmacol. Biochem. Behav. 84 2006 112 119
273. J.C. Blanco, S. Minucci, J. Lu, X.J. Yang, K.K. Walker, H. Chen, R.M. Evans, Y. Nakatani, and K. Ozato The histone acetylase PCAF is a nuclear receptor coactivator Genes Dev. 12 1998 1638 1651
274. M. Kishimoto, R. Fujiki, S. Takezawa, Y. Sasaki, T. Nakamura, K. Yamaoka, H. Kitagawa, and S. Kato Nuclear receptor mediated gene regulation through chromatin remodeling and histone modifications Endocr. J. 53 2006 157 172
275. S.M. Fernandez, M.C. Lewis, A.S. Pechenino, L.L. Harburger, P.T. Orr, J.E. Gresack, G.E. Schafe, and K.M. Frick Estradiol-induced enhancement of object memory consolidation involves hippocampal extracellular signal-regulated kinase activation and membrane-bound estrogen receptors J. Neurosci. 28 2008 8660 8667
276. L. Fan, Z. Zhao, P.T. Orr, C.H. Chambers, M.C. Lewis, and K.M. Frick Estradiol-induced object memory consolidation in middle-aged female mice requires dorsal hippocampal extracellular signal-regulated kinase and phosphatidylinositol 3-kinase activation J. Neurosci. 30 2010 4390 4400
277. P. Mannella, and R.D. Brinton Estrogen receptor protein interaction with phosphatidylinositol 3-kinase leads to activation of phosphorylated Akt and extracellular signal-regulated kinase 1/2 in the same population of cortical neurons: a unified mechanism of estrogen action J. Neurosci. 26 2006 9439 9447
278. C.B. Wade, and D.M. Dorsa Estrogen activation of cyclic adenosine 5′-monophosphate response element-mediated transcription requires the extracellularly regulated kinase/mitogen-activated protein kinase pathway Endocrinology 144 2003 832 838
279. K.M. Frick, Z. Zhao, and L. Fan The epigenetics of estrogen: epigenetic regulation of hormone-induced memory enhancement Epigenetics 6 2011 675 680
280. K.C. Lakshmaiah, L.A. Jacob, S. Aparna, D. Lokanatha, and S.C. Saldanha Epigenetic therapy of cancer with histone deacetylase inhibitors J. Cancer Res. Ther. 10 2014 469 478