Sex hormones regulate cytoskeletal proteins involved in brain plasticity

Frontiers in Psychiatry

Volumn 6, Issue NOV, 2015, Pages

  Hansberg Pastor, Valeria ^a   González Arenas, Aliesha ^a   Piña Medina, Ana Gabriela ^a   Camacho Arroyo, Ignacio ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Brain; Estradiol; Glial cells; Plasticity; Progesterone; Sex hormones

Indexed keywords

ACTIN; CYTOSKELETON PROTEIN; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GLIAL FIBRILLARY ACIDIC PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 2; PROGESTERONE; PROGESTERONE RECEPTOR A; PROGESTERONE RECEPTOR B; TAU PROTEIN;

BRAIN NERVE CELL; CELL COUNT; CELL SIZE; CELLULAR DISTRIBUTION; CYTOSKELETON; DENDRITIC SPINE; GLIA CELL; HIPPOCAMPUS; HORMONAL REGULATION; HUMAN; HYPOTHALAMUS; MENSTRUAL CYCLE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEUROMODULATION; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; STEROIDOGENESIS; SYNAPTOGENESIS; UPREGULATION;

EID: 84949755549     PISSN: None     EISSN: 16640640     Source Type: Journal    
DOI: 10.3389/fpsyt.2015.00165     Document Type: Review

References (184)

1. Parducz A, Hajszan T, Maclusky NJ, Hoyk Z, Csakvari E, Kurunczi A, et al. Synaptic remodeling induced by gonadal hormones: neuronal plasticity as a mediator of neuroendocrine and behavioral responses to steroids. Neuroscience (2006) 138:977-85. doi: 10.1016/j.neuroscience.2005.07.008
2. Gordon-Weeks PR, Fournier AE. Neuronal cytoskeleton in synaptic plasticity and regeneration. J Neurochem (2014) 129:206-12. doi:10.1111/jnc.12502
3. Chowen JA, Azcoitia I, Cardona-Gomez GP, Garcia-Segura LM. Sex steroids and the brain: lessons from animal studies. J Pediatr Endocrinol Metab (2000) 13:1045-66. doi:10.1515/JPEM.2000.13.8.1045
4. Garcia-Segura LM, Lorenz B, DonCarlos LL. The role of glia in the hypothalamus: implications for gonadal steroid feedback and reproductive neuroendocrine output. Reproduction (2008) 135:419-29. doi:10.1530/REP-07-0540
5. Kato A, Hojo Y, Higo S, Komatsuzaki Y, Murakami G, Yoshino H, et al. Female hippocampal estrogens have a significant correlation with cyclic fluctuation of hippocampal spines. Front Neural Circuits (2013) 7:149. doi:10.3389/fncir.2013.00149
6. Rhoda J, Corbier P, Roffi J. Gonadal steroid concentrations in serum and hypothalamus of the rat at birth: aromatization of testosterone to 17 β-estradiol. Endocrinology (1984) 114:1754-60. doi:10.1210/endo-114-5-1754
7. Konkle ATM, 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. doi:10.1210/en.2010-0607
8. Mellon SH, Vaudry H. Biosynthesis of neurosteroids and regulation of their synthesis. Int Rev Neurobiol (2001) 46:33-78. doi:10.1016/S0074-7742(01)46058-2
9. Mellon SH, Griffin LD, Compagnone NA. Biosynthesis and action of neurosteroids. Brain Res Brain Res Rev (2001) 37:3-12. doi:10.1016/S0165-0173(01)00109-6
10. Koenig HL, Schumacher M, Ferzaz B, Thi AN, Ressouches A, Guennoun R, et al. Progesterone synthesis and myelin formation by Schwann cells. Science (1995) 268:1500-3. doi:10.1126/science.7770777
11. Hojo Y, Hattori T-A, Enami T, Furukawa A, Suzuki K, Ishii H-T, et al. Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017alpha and P450 aromatase localized in neurons. Proc Natl Acad Sci U S A (2004) 101:865-70. doi:10.1073/pnas.2630225100
12. Ellmann S, Sticht H, Thiel F, Beckmann MW, Strick R, Strissel PL. Estrogen and progesterone receptors: from molecular structures to clinical targets. Cell Mol Life Sci (2009) 66:2405-26. doi:10.1007/s00018-009-0017-3
13. Sakuma Y. Gonadal steroid action and brain sex differentiation in the rat. J Neuroendocrinol (2009) 21:410-4. doi:10.1111/j.1365-2826.2009.01856.x
14. Carrillo-Martínez GE, Gómora-Arrati P, González-Arenas A, Roldán-Roldán G, González-Flores O, Camacho-Arroyo I. Effects of RU486 in the expression of progesterone receptor isoforms in the hypothalamus and the preoptic area of the rat during postpartum estrus. Neurosci Lett (2011) 504:127-30. doi:10.1016/j.neulet.2011.09.016
15. Guennoun R, Labombarda F, Gonzalez Deniselle MC, Liere P, De Nicola AF, Schumacher M. Progesterone and allopregnanolone in the central nervous system: response to injury and implication for neuroprotection. J Steroid Biochem Mol Biol (2015) 146C:48-61. doi:10.1016/j.jsbmb.2014.09.001
16. Waters EM, Thompson LI, Patel P, Gonzales AD, Ye HZ, Filardo EJ, et al. G-protein-coupled estrogen receptor 1 is anatomically positioned to modulate synaptic plasticity in the mouse hippocampus. J Neurosci (2015) 35:2384-97. doi:10.1523/JNEUROSCI.1298-14.2015
17. Guerra-Araiza C, Villamar-Cruz O, Gonzalez-Arenas A, Chavira R, Camacho-Arroyo I. Changes in progesterone receptor isoforms content in the rat brain during the oestrous cycle and after oestradiol and progesterone treatments. J Neuroendocrinol (2003) 15:984-90. doi:10.1046/j.1365-2826.2003.01088.x
18. Guerra-Araiza C, Cerbon MA, Morimoto S, Camacho-Arroyo I. Progesterone receptor isoforms expression pattern in the rat brain during the estrous cycle. Life Sci (2000) 66:1743-52. doi:10.1016/S0024-3205(00)00497-5
19. Helsen C, Claessens F. Looking at nuclear receptors from a new angle. Mol Cell Endocrinol (2013) 382:97-106. doi:10.1016/j.mce.2013.09.009
20. Schülke J-P, Wochnik GM, Lang-Rollin I, Gassen NC, Knapp RT, Berning B, et al. Differential impact of tetratricopeptide repeat proteins on the steroid hormone receptors. PLoS One (2010) 5:e11717. doi:10.1371/journal.pone.0011717
21. Cato L, Neeb A, Brown M, Cato ACB. Control of steroid receptor dynamics and function by genomic actions of the cochaperones p23 and Bag-1L. Nucl Recept Signal (2014) 12:e005. doi:10.1621/nrs.12005
22. Abdel-Hafiz HA, Horwitz KB. Post-translational modifications of the progesterone receptors. J Steroid Biochem Mol Biol (2014) 140:80-9. doi:10.1016/j.jsbmb.2013.12.008
23. Lange CA, Shen T, Horwitz KB. Phosphorylation of human progesterone receptors at serine-294 by mitogen-activated protein kinase signals their degradation by the 26S proteasome. Proc Natl Acad Sci U S A (2000) 97:1032-7. doi:10.1073/pnas.97.3.1032
24. Villamar-Cruz O, Manjarrez-Marmolejo J, Alvarado R, Camacho-Arroyo I. Regulation of the content of progesterone and estrogen receptors, and their cofactors SRC-1 and SMRT by the 26S proteasome in the rat brain during the estrous cycle. Brain Res Bull (2006) 69:276-81. doi:10.1016/j.brainresbull.2005.12.006
25. Deng H, Yin L, Zhang X-T, Liu L-J, Wang M-L, Wang Z-Y. ER-a variant ER-a36 mediates antiestrogen resistance in ER-positive breast cancer stem/progenitor cells. J Steroid Biochem Mol Biol (2014) 144(Pt B):417-26. doi:10.1016/j.jsbmb.2014.08.017
26. Garrido P, Salehzadeh F, Duque-Guimaraes DE, Al-Khalili L. Negative regulation of glucose metabolism in human myotubes by supraphysiological doses of 17β-estradiol or testosterone. Metabolism (2014) 63:1178-87. doi:10.1016/j.metabol.2014.06.003
27. González-Arenas A, Peña-Ortiz MA, Hansberg-Pastor V, Marquina-Sánchez B, Baranda-ávila N, Nava-Castro K, et al. PKCa and PKCd activation regulates transcriptional activity and degradation of progesterone receptor in human astrocytoma cells. Endocrinology (2015) 156:1010-22. doi:10.1210/en.2014-1137
28. Lishko PV, Botchkina IL, Kirichok Y. Progesterone activates the principal Ca2+ channel of human sperm. Nature (2011) 471:387-91. doi:10.1038/nature09767
29. Labombarda F, Ghoumari AM, Liere P, De Nicola AF, Schumacher M, Guennoun R. Neuroprotection by steroids after neurotrauma in organotypic spinal cord cultures: a key role for progesterone receptors and steroidal modulators of GABA(A) receptors. Neuropharmacology (2013) 71:46-55. doi:10.1016/j.neuropharm.2013.03.010
30. Micevych P, Christensen A. Membrane-initiated estradiol actions mediate structural plasticity and reproduction. Front Neuroendocrinol (2012) 33:331-41. doi:10.1016/j.yfrne.2012.07.003
31. Mueck AO, Ruan X, Seeger H, Fehm T, Neubauer H. Genomic and non-genomic actions of progestogens in the breast. J Steroid Biochem Mol Biol (2014) 142:62-7. doi:10.1016/j.jsbmb.2013.08.011
32. Levin ER. Extranuclear steroid receptors are essential for steroid hormone actions. Annu Rev Med (2015) 66:271-80. doi:10.1146/annurev-med-050913-021703
33. Chaudhri RA, Schwartz N, Elbaradie K, Schwartz Z, Boyan BD. Role of ERa36 in membrane-associated signaling by estrogen. Steroids (2014) 81:74-80. doi:10.1016/j.steroids.2013.10.020
34. Prossnitz ER, Hathaway HJ. What have we learned about GPER function in physiology and disease from knockout mice? J Steroid Biochem Mol Biol (2015) 153:114-26. doi:10.1016/j.jsbmb.2015.06.014
35. Nugent BM, Tobet SA, Lara HE, Lucion AB, Wilson ME, Recabarren SE, et al. Hormonal programming across the lifespan. Horm Metab Res (2012) 44:577-86. doi:10.1055/s-0032-1312593
36. Hillerer KM, Jacobs VR, Fischer T, Aigner L. The maternal brain: an organ with peripartal plasticity. Neural Plast (2014) 2014:574159. doi:10.1155/2014/574159
37. Kolb B, Gibb R. Brain plasticity and behaviour in the developing brain. J Can Acad Child Adolesc Psychiatry (2011) 20:265-76.
38. Maekawa F, Tsukahara S, Kawashima T, Nohara K, Ohki-Hamazaki H. The mechanisms underlying sexual differentiation of behavior and physiology in mammals and birds: relative contributions of sex steroids and sex chromosomes. Front Neurosci (2014) 8:242. doi:10.3389/fnins.2014.00242
39. Chung WCJ, Auger AP. Gender differences in neurodevelopment and epigenetics. Pflugers Arch (2013) 465:573-84. doi:10.1007/s00424-013-1258-4
40. Juraska JM, Sisk CL, DonCarlos LL. Sexual differentiation of the adolescent rodent brain: hormonal influences and developmental mechanisms. Horm Behav (2013) 64:203-10. doi:10.1016/j.yhbeh.2013.05.010
41. Farinetti A, Tomasi S, Foglio B, Ferraris A, Ponti G, Gotti S, et al. Testosterone and estradiol differentially affect cell proliferation in the subventricular zone of young adult gonadectomized male and female rats. Neuroscience (2015) 286:162-70. doi:10.1016/j.neuroscience.2014.11.050
42. Patel R, Moore S, Crawford DK, Hannsun G, Sasidhar MV, Tan K, et al. Attenuation of corpus callosum axon myelination and remyelination in the absence of circulating sex hormones. Brain Pathol (2013) 23:462-75. doi:10.1111/bpa.12029
43. Hasegawa Y, Hojo Y, Kojima H, Ikeda M, Hotta K, Sato R, et al. Estradiol rapidly modulates synaptic plasticity of hippocampal neurons: involvement of kinase networks. Brain Res (2015) 1621:147-61. doi:10.1016/j.brainres.2014.12.056
44. Schumacher M, Hussain R, Gago N, Oudinet J-P, Mattern C, Ghoumari AM. Progesterone synthesis in the nervous system: implications for myelination and myelin repair. Front Neurosci (2012) 6:10. doi:10.3389/fnins.2012.00010
45. Galea LA, Ormerod BK, Sampath S, Kostaras X, Wilkie DM, Phelps MT. Spatial working memory and hippocampal size across pregnancy in rats. Horm Behav (2000) 37:86-95. doi:10.1006/hbeh.1999.1560
46. Sandstrom NJ, Williams CL. Memory retention is modulated by acute estradiol and progesterone replacement. Behav Neurosci (2001) 115:384-93. doi:10.1037/0735-7044.115.2.384
47. Gould E, Woolley CS, Frankfurt M, McEwen BS. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci (1990) 10:1286-91.
48. Woolley CS, McEwen BS. Estradiol regulates hippocampal dendritic spine density via an N-methyl-D-aspartate receptor-dependent mechanism. J Neurosci (1994) 14:7680-7.
49. Fortress AM, Frick KM. Hippocampal Wnt signaling: memory regulation and hormone interactions. Neuroscientist (2015). doi:10.1177/1073858415574728
50. Garcia-Segura LM, Melcangi RC. Steroids and glial cell function. Glia (2006) 54:485-98. doi:10.1002/glia.20404
51. Barth C, Villringer A, Sacher J. Sex hormones affect neurotransmitters and shape the adult female brain during hormonal transition periods. Front Neurosci (2015) 9:37. doi:10.3389/fnins.2015.00037
52. González-Flores O, Gómora-Arrati P, García-Juárez M, Miranda-Martínez A, Armengual-Villegas A, Camacho-Arroyo I, et al. Progesterone receptor isoforms differentially regulate the expression of tryptophan and tyrosine hydroxylase and glutamic acid decarboxylase in the rat hypothalamus. Neurochem Int (2011) 59:671-6. doi:10.1016/j.neuint.2011.06.013
53. Sanchez AM, Flamini MI, Polak K, Palla G, Spina S, Mannella P, et al. Actin cytoskeleton remodelling by sex steroids in neurones. J Neuroendocrinol (2012) 24:195-201. doi:10.1111/j.1365-2826.2011.02258.x
54. Meisel RL, Luttrell VR. Estradiol increases the dendritic length of ventromedial hypothalamic neurons in female Syrian hamsters. Brain Res Bull (1990) 25:165-8. doi:10.1016/0361-9230(90)90269-6
55. Wong AM, Rozovsky I, Arimoto JM, Du Y, Wei M, Morgan TE, et al. Progesterone influence on neurite outgrowth involves microglia. Endocrinology (2009) 150:324-32. doi:10.1210/en.2008-0988
56. Garcia-Segura LM, Chowen JA, Parducz A, Naftolin F. Gonadal hormones as promoter of structural synaptic plasticity: cellular mechanisms. Prog Neurobiol (1994) 44:279-307. doi:10.1016/0301-0082(94)90042-6
57. García-López P, García-Marín V, Freire M. Three-dimensional reconstruction and quantitative study of a pyramidal cell of a Cajal histological preparation. J Neurosci (2006) 26:11249-52. doi:10.1523/JNEUROSCI.3543-06.2006
58. Ramóny Cajal S. Sur la structure de l'écorce cérébrale de quelques mammifères. La Cellule (1891) 7:125-76.
59. Nimchinsky EA, Sabatini BL, Svoboda K. Structure and function of dendritic spines. Annu Rev Physiol (2002) 64:313-53. doi:10.1146/annurev.physiol.64.081501.160008
60. Grienberger C, Chen X, Konnerth A. Dendritic function in vivo. Trends Neurosci (2015) 38:45-54. doi:10.1016/j.tins.2014.11.002
61. Hara Y, Waters EM, McEwen BS, Morrison JH. Estrogen effects on cognitive and synaptic health over the lifecourse. Physiol Rev (2015) 95:785-807. doi:10.1152/physrev.00036.2014
62. Hojo Y, Munetomo A, Mukai H, Ikeda M, Sato R, Hatanaka Y, et al. Estradiol rapidly modulates spinogenesis in hippocampal dentate gyrus: involvement of kinase networks. Horm Behav (2015) 74:149-56. doi:10.1016/j.yhbeh.2015.06.008
63. Murakami G, Hojo Y, Ogiue-Ikeda M, Mukai H, Chambon P, Nakajima K, et al. Estrogen receptor KO mice study on rapid modulation of spines and long-term depression in the hippocampus. Brain Res (2015) 1621:133-46. doi:10.1016/j.brainres.2014.12.002
64. Sellers K, Raval P, Srivastava DP. Molecular signature of rapid estrogen regulation of synaptic connectivity and cognition. Front Neuroendocrinol (2015) 36:72-89. doi:10.1016/j.yfrne.2014.08.001
65. Baudry M, Bi X, Aguirre C. Progesterone-estrogen interactions in synaptic plasticity and neuroprotection. Neuroscience (2013) 239:280-94. doi:10.1016/j.neuroscience.2012.10.051
66. 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. doi:10.3389/fncel.2015.00137
67. Bi R, Broutman G, Foy MR, Thompson RF, Baudry M. The tyrosine kinase and mitogen-activated protein kinase pathways mediate multiple effects of estrogen in hippocampus. Proc Natl Acad Sci U S A (2000) 97:3602-7. doi:10.1073/pnas.060034497
68. Bi R, Foy MR, Vouimba RM, Thompson RF, Baudry M. Cyclic changes in estradiol regulate synaptic plasticity through the MAP kinase pathway. Proc Natl Acad Sci U S A (2001) 98:13391-5. doi:10.1073/pnas.241507698
69. Sanchez AM, Flamini MI, Genazzani AR, Simoncini T. Effects of progesterone and medroxyprogesterone on actin remodeling and neuronal spine formation. Mol Endocrinol (2013) 27:693-702. doi:10.1210/me.2012-1278
70. Wessel L, Balakrishnan-Renuka A, Henkel C, Meyer HE, Meller K, Brand-Saberi B, et al. Long-term incubation with mifepristone (MLTI) increases the spine density in developing Purkinje cells: new insights into progesterone receptor mechanisms. Cell Mol Life Sci (2014) 71:1723-40. doi:10.1007/s00018-013-1448-4
71. Durand GM, Konnerth A. Long-term potentiation as a mechanism of functional synapse induction in the developing hippocampus. J Physiol Paris (1996) 90:313-5. doi:10.1016/S0928-4257(97)87905-3
72. Warren SG, Humphreys AG, Juraska JM, Greenough WT. LTP varies across the estrous cycle: enhanced synaptic plasticity in proestrus rats. Brain Res (1995) 703:26-30. doi:10.1016/0006-8993(95)01059-9
73. Yankova M, Hart SA, Woolley CS. Estrogen increases synaptic connectivity between single presynaptic inputs and multiple postsynaptic CA1 pyramidal cells: a serial electron-microscopic study. Proc Natl Acad Sci U S A (2001) 98:3525-30. doi:10.1073/pnas.051624598
74. Woolley CS, Gould E, Frankfurt M, McEwen BS. Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci (1990) 10:4035-9.
75. Amateau SK, Alt JJ, Stamps CL, McCarthy MM. Brain estradiol content in newborn rats: sex differences, regional heterogeneity, and possible de novo synthesis by the female telencephalon. Endocrinology (2004) 145:2906-17. doi:10.1210/en.2003-1363
76. Rasia-Filho AA, Dalpian F, Menezes IC, Brusco J, Moreira JE, Cohen RS. Dendritic spines of the medial amygdala: plasticity, density, shape, and subcellular modulation by sex steroids. Histol Histopathol (2012) 27:985-1011.
77. Rasia-Filho AA, Fabian C, Rigoti KM, Achaval M. Influence of sex, estrous cycle and motherhood on dendritic spine density in the rat medial amygdala revealed by the Golgi method. Neuroscience (2004) 126:839-47. doi:10.1016/j.neuroscience.2004.04.009
78. Fester L, Rune GM. Sexual neurosteroids and synaptic plasticity in the hippocampus. Brain Res (2015) 1621:162-9. doi:10.1016/j.brainres.2014.10.033
79. Kretz O, Fester L, Wehrenberg U, Zhou L, Brauckmann S, Zhao S, et al. Hippocampal synapses depend on hippocampal estrogen synthesis. J Neurosci (2004) 24:5913-21. doi:10.1523/JNEUROSCI.5186-03.2004
80. Maggi A, Perez J. Role of female gonadal hormones in the CNS: clinical and experimental aspects. Life Sci (1985) 37:893-906. doi:10.1016/0024-3205(85)90525-9
81. Sakamoto H, Ukena K, Tsutsui K. Dendritic spine formation in response to progesterone synthesized de novo in the developing Purkinje cell in rats. Neurosci Lett (2002) 322:111-5. doi:10.1016/S0304-3940(02)00077-0
82. Tournell CE, Bergstrom RA, Ferreira A. Progesterone-induced agrin expression in astrocytes modulates glia-neuron interactions leading to synapse formation. Neuroscience (2006) 141:1327-38. doi:10.1016/j.neuroscience.2006.05.004
83. Yuan A, Rao MV, Veeranna, Nixon RA. Neurofilaments at a glance. J Cell Sci (2012) 125:3257-63. doi:10.1242/jcs.104729
84. Sakakibara A, Ando R, Sapir T, Tanaka T. Microtubule dynamics in neuronal morphogenesis. Open Biol (2013) 3:130061. doi:10.1098/rsob.130061
85. Sergeant N, Buée L. Tau pathology. In: Nixon RA, Yuan A, editors. Cytoskeleton of the Nervous System. New York, NY: Springer (2011). p. 83-132.
86. Revenu C, Athman R, Robine S, Louvard D. The co-workers of actin filaments: from cell structures to signals. Nat Rev Mol Cell Biol (2004) 5:635-46. doi:10.1038/nrm1437
87. Ferri SL, Hildebrand PF, Way SE, Flanagan-Cato LM. Estradiol regulates markers of synaptic plasticity in the hypothalamic ventromedial nucleus and amygdala of female rats. Horm Behav (2014) 66:409-20. doi:10.1016/j.yhbeh.2014.06.016
88. Arevalo M-A, Santos-Galindo M, Bellini M-J, Azcoitia I, Garcia-Segura LM. Actions of estrogens on glial cells: implications for neuroprotection. Biochim Biophys Acta (2010) 1800:1106-12. doi:10.1016/j.bbagen.2009.10.002
89. Camacho-Arroyo I, Reyna-Neyra A, Mercado-Gómez O, Arias C. The role of estradiol and progesterone in the regulation of cytoskeletal proteins in the central nervous system. In: Pandala SG, editor. Recent Research Developments in Life Sciences. vol. 2, Kerala: Research Signpost (2004). p. 143-61.
90. Pollard TD, Borisy GG. Cellular motility driven by assembly and disassembly of actin filaments. Cell (2003) 112:453-65. doi:10.1016/S0092-8674(03)00120-X
91. Kaech S, Parmar H, Roelandse M, Bornmann C, Matus A. Cytoskeletal microdifferentiation: a mechanism for organizing morphological plasticity in dendrites. Proc Natl Acad Sci U S A (2001) 98:7086-92. doi:10.1073/pnas.111146798
92. Sekino Y, Kojima N, Shirao T. Role of actin cytoskeleton in dendritic spine morphogenesis. Neurochem Int (2007) 51:92-104. doi:10.1016/j.neuint.2007.04.029
93. Shirao T, González-Billault C. Actin filaments and microtubules in dendritic spines. J Neurochem (2013) 126:155-64. doi:10.1111/jnc.12313
94. Jan Y-N, Jan LY. Branching out: mechanisms of dendritic arborization. Nat Rev Neurosci (2010) 11:316-28. doi:10.1038/nrn2836
95. Gonzalez-Billault C, Muñoz-Llancao P, Henriquez DR, Wojnacki J, Conde C, Caceres A. The role of small GTPases in neuronal morphogenesis and polarity. Cytoskeleton (Hoboken) (2012) 69:464-85. doi:10.1002/cm.21034
96. De Pittà M, Brunel N, Volterra A. Astrocytes: orchestrating synaptic plasticity? Neuroscience (2015). doi:10.1016/j.neuroscience.2015.04.001
97. Bernardinelli Y, Muller D, Nikonenko I. Astrocyte-synapse structural plasticity. Neural Plast (2014) 2014:232105. doi:10.1155/2014/232105
98. Middeldorp J, Hol EM. GFAP in health and disease. Prog Neurobiol (2011) 93:421-43. doi:10.1016/j.pneurobio.2011.01.005
99. Doherty GJ, McMahon HT. Mediation, modulation, and consequences of membrane-cytoskeleton interactions. Annu Rev Biophys (2008) 37:65-95. doi:10.1146/annurev.biophys.37.032807.125912
100. Dominguez R, Holmes KC. Actin structure and function. Annu Rev Biophys (2011) 40:169-86. doi:10.1146/annurev-biophys-042910-155359
101. Cohen RS, Chung SK, Pfaff DW. Immunocytochemical localization of actin in dendritic spines of the cerebral cortex using colloidal gold as a probe. Cell Mol Neurobiol (1985) 5:271-84. doi:10.1007/BF00711012
102. Fischer M, Kaech S, Wagner U, Brinkhaus H, Matus A. Glutamate receptors regulate actin-based plasticity in dendritic spines. Nat Neurosci (2000) 3:887-94. doi:10.1038/78791
103. Simoncini T, Scorticati C, Mannella P, Fadiel A, Giretti MS, Fu XD, et al. Estrogen receptor alpha interacts with Galpha13 to drive actin remodeling and endothelial cell migration via the RhoA/Rho kinase/moesin pathway. Mol Endocrinol (2006) 20:1756-71. doi:10.1210/me.2005-0259
104. Fu XD, Giretti MS, Baldacci C, Garibaldi S, Flamini M, Sanchez AM, et al. Extra-nuclear signaling of progesterone receptor to breast cancer cell movement and invasion through the actin cytoskeleton. PLoS One (2008) 3:e2790. doi:10.1371/journal.pone.0002790
105. Flamini MI, Sanchez AM, Goglia L, Tosi V, Genazzani AR, Simoncini T. Differential actions of estrogen and SERMs in regulation of the actin cytoskeleton of endometrial cells. Mol Hum Reprod (2009) 15:675-85. doi:10.1093/molehr/gap045
106. Giretti MS, Fu XD, De Rosa G, Sarotto I, Baldacci C, Garibaldi S, et al. Extra-nuclear signalling of estrogen receptor to breast cancer cytoskeletal remodelling, migration and invasion. PLoS One (2008) 3:e2238. doi:10.1371/journal.pone.0002238
107. Suetsugu S, Hattori M, Miki H, Tezuka T, Yamamoto T, Mikoshiba K, et al. Sustained activation of N-WASP through phosphorylation is essential for neurite extension. Dev Cell (2002) 3:645-58.
108. Kim Y, Sung JY, Ceglia I, Lee KW, Ahn JH, Halford JM, et al. Phosphorylation of WAVE1 regulates actin polymerization and dendritic spine morphology. Nature (2006) 442:814-17.
109. Sánchez AM, Flamini MI, Fu XD, Mannella P, Giretti MS, Goglia L, et al. Rapid signaling of estrogen to WAVE1 and moesin controls neuronal spine formation via the actin cytoskeleton. Mol Endocrinol (2009) 23:1193-202. doi:10.1210/me.2008-0408
110. Tsukita S, Yonemura S. Cortical actin organization: lessons from ERM (ezrin/radixin/moesin) proteins. J Biol Chem (1999) 274:34507-10. doi:10.1074/jbc.274.49.34507
111. Louvet-Vallee S. ERM proteins: from cellular architecture to cell signaling. Biol Cell (2000) 92:305-16. doi:10.1016/S0248-4900(00)01078-9
112. Babayan AH, Kramár EA. Rapid effects of oestrogen on synaptic plasticity: interactions with actin and its signalling proteins. J Neuroendocrinol (2013) 25:1163-72. doi:10.1111/jne.12108
113. Vierk R, Brandt N, Rune GM. Hippocampal estradiol synthesis and its significance for hippocampal synaptic stability in male and female animals. Neuroscience (2014) 274:24-32. doi:10.1016/j.neuroscience.2014.05.003
114. Srivastava DP, Woolfrey KM, Woolfrey K, Jones KA, Shum CY, Lash LL, et al. Rapid enhancement of two-step wiring plasticity by estrogen and NMDA receptor activity. Proc Natl Acad Sci U S A (2008) 105:14650-5. doi:10.1073/pnas.0801581105
115. Olbrich L, Wessel L, Balakrishnan-Renuka A, Boing M, Brand-Saberi B, Theiss C. Rapid impact of progesterone on the neuronal growth cone. Endocrinology (2013) 154:3784-95. doi:10.1210/en.2013-1175
116. Brouhard GJ, Rice LM. The contribution of aβ-tubulin curvature to microtubule dynamics. J Cell Biol (2014) 207:323-34. doi:10.1083/jcb.201407095
117. Halpain S, Dehmelt L. The MAP1 family of microtubule-associated proteins. Genome Biol (2006) 7:224. doi:10.1186/gb-2006-7-6-224
118. Sergeant N, Buée L. Cytoskeleton of the nervous system. Neurobiology (2011) 3:83-132. doi:10.1007/978-1-4419-6787-9
119. Hanger DP, Anderton BH, Noble W. Tau phosphorylation: the therapeutic challenge for neurodegenerative disease. Trends Mol Med (2009) 15:112-9. doi:10.1016/j.molmed.2009.01.003
120. Harada A, Teng J, Takei Y, Oguchi K, Hirokawa N. MAP2 is required for dendrite elongation, PKA anchoring in dendrites, and proper PKA signal transduction. J Cell Biol (2002) 158:541-9. doi:10.1083/jcb.200110134
121. Dehmelt L, Halpain S. The MAP2/Tau family of microtubule-associated proteins. Genome Biol (2005) 6:204. doi:10.1186/gb-2004-6-1-204
122. Murakami K, Fellous A, Baulieu EE, Robel P. Pregnenolone binds to microtubule-associated protein 2 and stimulates microtubule assembly. Proc Natl Acad Sci U S A (2000) 97:3579-84. doi:10.1073/pnas.97.7.3579
123. Reyna-Neyra A, Camacho-Arroyo I, Ferrera P, Arias C. Estradiol and progesterone modify microtubule associated protein 2 content in the rat hippocampus. Brain Res Bull (2002) 58:607-12. doi:10.1016/S0361-9230(02)00829-8
124. Reyna-Neyra A, Arias C, Ferrera P, Morimoto S, Camacho-Arroyo I. Changes in the content and distribution of microtubule associated protein 2 in the hippocampus of the rat during the estrous cycle. J Neurobiol (2004) 60:473-80. doi:10.1002/neu.20042
125. Ferreira A, Caceres A. Estrogen-enhanced neurite growth: evidence for a selective induction of tau and stable microtubules. J Neurosci (1991) 11:392-400.
126. Lorenzo A, Díaz H, Carrer H, Cáceres A. Amygdala neurons in vitro: neurite growth and effects of estradiol. J Neurosci Res (1992) 33:418-35. doi:10.1002/jnr.490330308
127. Diaz H, Lorenzo A, Carrer HF, Caceres A. Time lapse study of neurite growth in hypothalamic dissociated neurons in culture: sex differences and estrogen effects. J Neurosci Res (1992) 33:266-81. doi:10.1002/jnr.490330210
128. Camacho-Arroyo I, Gonzalez-Arenas A, Espinosa-Raya J, Pina-Medina AG, Picazo O. Short-and long-term treatment with estradiol or progesterone modifies the expression of GFAP, MAP2 and Tau in prefrontal cortex and hippocampus. Life Sci (2011) 89:123-8. doi:10.1016/j.lfs.2011.05.008
129. Guerra-Araiza C, Amorim MA, Camacho-Arroyo I, Garcia-Segura LM. Effects of progesterone and its reduced metabolites, dihydroprogesterone and tetrahydroprogesterone, on the expression and phosphorylation of glycogen synthase kinase-3 and the microtubule-associated protein tau in the rat cerebellum. Dev Neurobiol (2007) 67:510-20. doi:10.1002/dneu.20383
130. González SL, López-Costa JJ, Labombarda F, Deniselle MCG, Guennoun R, Schumacher M, et al. Progesterone effects on neuronal ultrastructure and expression of microtubule-associated protein 2 (MAP2) in bats with acute spinal cord injury. Cell Mol Neurobiol (2009) 29:27-39. doi:10.1007/s10571-008-9291-0
131. Bridges RS. A quantitative analysis of the roles of dosage, sequence, and duration of estradiol and progesterone exposure in the regulation of maternal behavior in the rat. Endocrinology (1984) 114:930-40. doi:10.1210/endo-114-3-930
132. González-Arenas A, Piña-Medina AG, González-Flores O, Galván-Rosas A, Gómora-Arrati P, Camacho-Arroyo I. Sex hormones and expression pattern of cytoskeletal proteins in the rat brain throughout pregnancy. J Steroid Biochem Mol Biol (2014) 139:154-8. doi:10.1016/j.jsbmb.2013.01.005
133. Bridges RS, Hammer RP Jr. Parity-associated alterations of medial preoptic opiate receptors in female rats. Brain Res (1992) 578:269-74. doi:10.1016/0006-8993(92)90257-A
134. Keyser-Marcus L, Stafisso-Sandoz G, Gerecke K, Jasnow A, Nightingale L, Lambert KG, et al. Alterations of medial preoptic area neurons following pregnancy and pregnancy-like steroidal treatment in the rat. Brain Res Bull (2001) 55:737-45. doi:10.1016/S0361-9230(01)00554-8
135. González-Arenas A, Piña-Medina AG, González-Flores O, Gómora-Arrati P, Carrillo-Martínez GE, Balandrán-Ruíz MA, et al. Expression pattern of tau in the rat brain during pregnancy and the beginning of lactation. Brain Res Bull (2012) 89:108-14. doi:10.1016/j.brainresbull.2012.07.011
136. Evans DB, Rank KB, Bhattacharya K, Thomsen DR, Gurney ME, Sharma SK. Tau phosphorylation at serine 396 and serine 404 by human recombinant tau protein kinase II inhibits tau's ability to promote microtubule assembly. J Biol Chem (2000) 275:24977-83. doi:10.1074/jbc.M000808200
137. Regan P, Piers T, Yi J-H, Kim D-H, Huh S, Park SJ, et al. Tau phosphorylation at serine 396 residue is required for hippocampal LTD. J Neurosci (2015) 35:4804-12. doi:10.1523/JNEUROSCI.2842-14.2015
138. Nicholls RE, Alarcon JM, Malleret G, Carroll RC, Grody M, Vronskaya S, et al. Transgenic mice lacking NMDAR-dependent LTD exhibit deficits in behavioral flexibility. Neuron (2008) 58:104-17. doi:10.1016/j.neuron.2008.01.039
139. Kang H-S, Lee C-K, Kim J-R, Yu S-J, Kang S-G, Moon D-H, et al. Gene expression analysis of the pro-oestrous-stage rat uterus reveals neuroligin 2 as a novel steroid-regulated gene. Reprod Fertil Dev (2004) 16:763-72. doi:10.1071/RD04040
140. Akama KT, McEwen BS. Estrogen stimulates postsynaptic density-95 rapid protein synthesis via the Akt/protein kinase B pathway. J Neurosci (2003) 23:2333-9.
141. Rasooli-Nejad S, Palygin O, Lalo U, Pankratov Y. Cannabinoid receptors contribute to astroglial Ca(2)(+)-signalling and control of synaptic plasticity in the neocortex. Philos Trans R Soc Lond B Biol Sci (2014) 369:20140077. doi:10.1098/rstb.2014.0077
142. Elobeid A, Bongcam-Rudloff E, Westermark B, Nister M. Effects of inducible glial fibrillary acidic protein on glioma cell motility and proliferation. J Neurosci Res (2000) 60:245-56. doi:10.1002/(SICI)1097-4547(20000415)60:2<245::AID-JNR14>3.0.CO;2-1
143. Toda M, Miura M, Asou H, Sugiyama I, Kawase T, Uyemura K. Suppression of glial tumor growth by expression of glial fibrillary acidic protein. Neurochem Res (1999) 24:339-43. doi:10.1023/A:1022538810581
144. Potokar M, Kreft M, Li L, Daniel Andersson J, Pangrsic T, Chowdhury HH, et al. Cytoskeleton and vesicle mobility in astrocytes. Traffic (2007) 8:12-20. doi:10.1111/j.1600-0854.2006.00509.x
145. Liedtke W, Edelmann W, Bieri PL, Chiu FC, Cowan NJ, Kucherlapati R, et al. GFAP is necessary for the integrity of CNS white matter architecture and long-term maintenance of myelination. Neuron (1996) 17:607-15. doi:10.1016/S0896-6273(00)80194-4
146. Eddleston M, Mucke L. Molecular profile of reactive astrocytes - implications for their role in neurologic disease. Neuroscience (1993) 54:15-36. doi:10.1016/0306-4522(93)90380-X
147. Otani N, Nawashiro H, Fukui S, Ooigawa H, Ohsumi A, Toyooka T, et al. Enhanced hippocampal neurodegeneration after traumatic or kainate excitotoxicity in GFAP-null mice. J Clin Neurosci (2006) 13:934-8. doi:10.1016/j.jocn.2005.10.018
148. Day JR, Laping NJ, Lampert-Etchells M, Brown SA, O'Callaghan JP, McNeill TH, et al. Gonadal steroids regulate the expression of glial fibrillary acidic protein in the adult male rat hippocampus. Neuroscience (1993) 55:435-43. doi:10.1016/0306-4522(93)90512-E
149. Conejo NM, Gonzalez-Pardo H, Cimadevilla JM, Arguelles JA, Diaz F, Vallejo-Seco G, et al. Influence of gonadal steroids on the glial fibrillary acidic protein-immunoreactive astrocyte population in young rat hippocampus. J Neurosci Res (2005) 79:488-94. doi:10.1002/jnr.20372
150. Del Cerro S, Garcia-Estrada J, Garcia-Segura LM. Neuroactive steroids regulate astroglia morphology in hippocampal cultures from adult rats. Glia (1995) 14:65-71. doi:10.1002/glia.440140109
151. Storer PD, Jones KJ. Glial fibrillary acidic protein expression in the hamster red nucleus: effects of axotomy and testosterone treatment. Exp Neurol (2003) 184:939-46. doi:10.1016/S0014-4886(03)00339-X
152. Nilsson M, Pekny M. Enriched environment and astrocytes in central nervous system regeneration. J Rehabil Med (2007) 39:345-52. doi:10.2340/16501977-0084
153. Arias C, Zepeda A, Hernández-Ortega K, Leal-Galicia P, Lojero C, Camacho-Arroyo I. Sex and estrous cycle-dependent differences in glial fibrillary acidic protein immunoreactivity in the adult rat hippocampus. Horm Behav (2009) 55:257-63. doi:10.1016/j.yhbeh.2008.10.016
154. Gómora-Arrati P, González-Arenas A, Balandrán-Ruiz MA, Mendoza-Magaña ML, González-Flores O, Camacho-Arroyo I. Changes in the content of GFAP in the rat brain during pregnancy and the beginning of lactation. Neurosci Lett (2010) 484:197-200. doi:10.1016/j.neulet.2010.08.052
155. Garcia-Segura LM, McCarthy MM. Minireview: role of glia in neuroendocrine function. Endocrinology (2004) 145:1082-6. doi:10.1210/en.2003-1383
156. Mong JA, Blutstein T. Estradiol modulation of astrocytic form and function: implications for hormonal control of synaptic communication. Neuroscience (2006) 138:967-75. doi:10.1016/j.neuroscience.2005.10.017
157. Rozovsky I, Wei M, Stone DJ, Zanjani H, Anderson CP, Morgan TE, et al. Estradiol (E2) enhances neurite outgrowth by repressing glial fibrillary acidic protein expression and reorganizing laminin. Endocrinology (2002) 143:636-46. doi:10.1210/endo.143.2.8615
158. Cervantes M, González-Vidal MD, Ruelas R, Escobar A, Moralí G. Neuroprotective effects of progesterone on damage elicited by acute global cerebral ischemia in neurons of the caudate nucleus. Arch Med Res (2002) 33:6-14. doi:10.1016/S0188-4409(01)00347-2
159. Hoffman GE, Merchenthaler I, Zup SL. Neuroprotection by ovarian hormones in animal models of neurological disease. Endocrine (2006) 29(2):217. doi:10.1385/ENDO:29:2:217
160. Nilsen J, Brinton RD. Impact of progestins on estrogen-induced neuroprotection: synergy by progesterone and 19-norprogesterone and antagonism by medroxyprogesterone acetate. Endocrinology (2002) 143:205-12. doi:10.1210/en.143.1.205
161. Singh M, Su C. Progesterone-induced neuroprotection: factors that may predict therapeutic efficacy. Brain Res (2013) 1514:98-106. doi:10.1016/j.brainres.2013.01.027
162. Opendak M, Gould E. Adult neurogenesis: a substrate for experience-dependent change. Trends Cogn Sci (2015) 19:151-61. doi:10.1016/j.tics.2015.01.001
163. Duarte-Guterman P, Yagi S, Chow C, Galea LAM. Hippocampal learning, memory, and neurogenesis: effects of sex and estrogens across the lifespan in adults. Horm Behav (2015) 74:37-52. doi:10.1016/j.yhbeh.2015.05.024
164. Chan M, Chow C, Hamson DK, Lieblich SE, Galea LAM. Effects of chronic oestradiol, progesterone and medroxyprogesterone acetate on hippocampal neurogenesis and adrenal mass in adult female rats. J Neuroendocrinol (2014) 26:386-99. doi:10.1111/jne.12159
165. Zheng J, Zhang P, Li X, Lei S, Li W, He X, et al. Post-stroke estradiol treatment enhances neurogenesis in the subventricular zone of rats after permanent focal cerebral ischemia. Neuroscience (2013) 231:82-90. doi:10.1016/j.neuroscience.2012.11.042
166. Li J, Siegel M, Yuan M, Zeng Z, Finnucan L, Persky R, et al. Estrogen enhances neurogenesis and behavioral recovery after stroke. J Cereb Blood Flow Metab (2011) 31:413-25. doi:10.1038/jcbfm.2010.181
167. Suzuki S, Gerhold LM, Böttner M, Rau SW, Dela Cruz C, Yang E, et al. Estradiol enhances neurogenesis following ischemic stroke through estrogen receptors a and β. J Comp Neurol (2007) 500:1064-75. doi:10.1002/cne.21240
168. Li Z, Wang B, Kan Z, Zhang B, Yang Z, Chen J, et al. Progesterone increases circulating endothelial progenitor cells and induces neural regeneration after traumatic brain injury in aged rats. J Neurotrauma (2012) 29:343-53. doi:10.1089/neu.2011.1807
169. Stiess M, Bradke F. Neuronal polarization: the cytoskeleton leads the way. Dev Neurobiol (2011) 71:430-44. doi:10.1002/dneu.20849
170. Sudo S, Wen TC, Desaki J, Matsuda S, Tanaka J, Arai T, et al. β-Estradiol protects hippocampal CA1 neurons against transient forebrain ischemia in gerbil. Neurosci Res (1997) 29:345-54. doi:10.1016/S0168-0102(97)00106-5
171. Espinosa-García C, Aguilar-Hernández A, Cervantes M, Moralí G. Effects of progesterone on neurite growth inhibitors in the hippocampus following global cerebral ischemia. Brain Res (2014) 1545:23-34. doi:10.1016/j.brainres.2013.11.030
172. Shi J, Panickar KS, Yang SH, Rabbani O, Day AL, Simpkins JW. Estrogen attenuates over-expression of beta-amyloid precursor protein messager RNA in an animal model of focal ischemia. Brain Res (1998) 810:87-92. doi:10.1016/S0006-8993(98)00888-9
173. Simpkins JW, Singh M. More than a decade of estrogen neuroprotection. Alzheimers Dement (2008) 4:S131-6. doi:10.1016/j.jalz.2007.10.009
174. Petanceska SS, Nagy V, Frail D, Gandy S. Ovariectomy and 17beta-estradiol modulate the levels of Alzheimer's amyloid beta peptides in brain. Exp Gerontol (2000) 35:1317-25. doi:10.1016/S0531-5565(00)00157-1
175. Hampl R, Bicíková M. Neuroimmunomodulatory steroids in Alzheimer dementia. J Steroid Biochem Mol Biol (2010) 119:97-104. doi:10.1016/j.jsbmb.2010.02.007
176. Alvarez-de-la-Rosa M, Silva I, Nilsen J, Pérez MM, García-Segura LM, Avila J, et al. Estradiol prevents neural tau hyperphosphorylation characteristic of Alzheimer's disease. Ann N Y Acad Sci (2005) 1052:210-24. doi:10.1196/annals.1347.016
177. Paganini-Hill A, Henderson VW. Estrogen replacement therapy and risk of Alzheimer disease. Arch Intern Med (1996) 156:2213-7. doi:10.1001/archinte.1996.00440180075009
178. Wang Q, Santizo R, Baughman VL, Pelligrino DA, Iadecola C. Estrogen provides neuroprotection in transient forebrain ischemia through perfusion-independent mechanisms in rats. Stroke (1999) 30:630-7. doi:10.1161/01.STR.30.3.630
179. Regan RF, Guo Y. Estrogens attenuate neuronal injury due to hemoglobin, chemical hypoxia, and excitatory amino acids in murine cortical cultures. Brain Res (1997) 764:133-40. doi:10.1016/S0006-8993(97)00437-X
180. Bonnefont AB, Muñoz FJ, Inestrosa NC. Estrogen protects neuronal cells from the cytotoxicity induced by acetylcholinesterase-amyloid complexes. FEBS Lett (1998) 441:220-4. doi:10.1016/S0014-5793(98)01552-X
181. Guennoun R, Benmessahel Y, Delespierre B, Gouézou M, Rajkowski KM, Baulieu EE, et al. Progesterone stimulates Krox-20 gene expression in Schwann cells. Mol Brain Res (2001) 90:75-82. doi:10.1016/S0169-328X(01)00094-8
182. Sereda MW, Meyer zu Hörste G, Suter U, Uzma N, Nave K-A. Therapeutic administration of progesterone antagonist in a model of Charcot-Marie-Tooth disease (CMT-1A). Nat Med (2003) 9:1533-7. doi:10.1038/nm957
183. Jung-Testas I, Schumacher M, Robel P, Baulieu EE. Actions of steroid hormones-and growth factors on glial cells of the central and peripheral nervous system. J Steroid Biochem Mol Biol (1994) 48:145-54. doi:10.1016/0960-0760(94)90261-5
184. Baulieu E, Schumacher M. Progesterone as a neuroactive neurosteroid, with special reference to the effect of progesterone on myelination. Steroids (2000) 65:605-12. doi:10.1016/S0039-128X(00)00173-2