Plastic changes in dendritic spines of hippocampal CA1 pyramidal neurons from ovariectomized rats after estradiol treatment

Brain Research

Volumn 1470, Issue , 2012, Pages 1-10

  Velázquez Zamora, Dulce A ^a,b   González Tapia, David ^a,b   González Ramírez, Myrna M ^a   Flores Soto, Mario E ^a   Vázquez Valls, Eduardo ^c   Cervantes, Miguel ^d   González Burgos, Ignacio ^a,b  

^a CENTRO DE INVESTIGACIÓN BIOMÉDICA DE OCCIDENTE   (Mexico)

^b UNIVERSITY OF GUADALAJARA   (Mexico)

^c INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

^d UNIVERSIDAD MICHOACANA DE SAN NICOLÁS DE HIDALGO   (Mexico)

Author keywords

CA1; Dendritic spine; Estrogen; Hippocampus; Plasticity; Synaptophysin

Indexed keywords

ESTRADIOL; SYNAPTOPHYSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DENSITY; CONTROLLED STUDY; DENDRITIC SPINE; FEMALE; HIPPOCAMPAL CA1 REGION; NERVE CELL PLASTICITY; NERVE SPROUTING; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT;

ANALYSIS OF VARIANCE; ANIMALS; CA1 REGION, HIPPOCAMPAL; DENDRITIC SPINES; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTRADIOL; ESTROGENS; FEMALE; GENE EXPRESSION REGULATION; OVARIECTOMY; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; SILVER STAINING; SYNAPTOPHYSIN;

ANIMALIA; BASIDIOMYCOTA; RATTUS;

EID: 84864631843     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2012.06.012     Document Type: Article

References (80)

1. T. Audesirk, L. Cabell, M. Kern, and G. Audesirk beta-estradiol influences differentiation of hippocampal neurons in vitro through an estrogen receptor-mediated process Neuroscience 121 2003 927 934 (Pubitemid 37324592)
2. M.E. Bailey, A.C. Wang, J. Hao, W.G. Janssen, Y. Hara, D. Dumitriu, P.R. Hof, and J.H. Morrison Interactive effects of age and estrogen on cortical neurons: implications for cognitive aging Neuroscience 191 2011 148 158
3. H.A. Bimonte, and V.H. Denenberg Estradiol facilitates performance as working memory load increases Psychoneuroendocrinology 24 1999 161 173 (Pubitemid 29125348)
4. J. Bourne, and K.M. Harris Do thin spines learn to be mushroom spines that remember? Curr. Opin. Neurobiol. 17 2007 1 6
5. W.G. Brake, S.E. Alves, J.C. Dunlop, S.J. Lee, K. Bullock, P.B. Allen, P. Greengard, and B.S. McEwen Novel target sites for estrogen action in the dorsal hippocampus: an examination of synaptic proteins Endocrinology 142 2001 1284 1289 (Pubitemid 32202840)
6. H.J. Carlisle, P. Manzerra, E. Marcora, and M.B. Kennedy SynGAP regulates steady-state and activity-dependent phosphorylation of cofilin J. Neurosci. 28 2008 13673 13683
7. S. Chamniansawat, and S. Chongthammakun Estrogen stimulates activity-regulated cytoskeleton associated protein (Arc) expression via the MAPK- and PI-3K-dependent pathways in SH-SY5Y cells Neurosci. Lett. 452 2009 130 135
8. R. Chindewa, S. Lapananstasin, Y. Sanvarinda, and S. Chongthammakun Pueraria mirifica, phytoestrogen-induced change in synaptophysin expression via estrogen receptor in rat hippocampal neuron J. Med. Assoc. Thailand 91 2008 208 214 (Pubitemid 351413681)
9. J.M. Daniel, S.L. Roberts, and G.P. Dohanich Effects of ovarian hormones and environment on radial maze and water maze performance Physiol. Behav. 66 1999 11 20 (Pubitemid 29155252)
10. 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 (Pubitemid 30183639)
11. S.J. Duff, and E. Hampson A beneficial effect of estrogen in working memory in postmenopausal women taking hormone replacement therapy Horm. Behav. 38 2000 262 276
12. A.J. Fader, P.E.M. Johnson, and G.P. Dohanich Estrogen improves working but not reference memory and prevents amnestic effects of scopolamine on a radial-arm maze Pharmacol. Biochem. Behav. 62 1999 711 717 (Pubitemid 29127176)
13. Feria-Velasco, A.; Del Angel-Meza, A.R.; González-Burgos, I.; 2002. Modification of dendritic development. In: Azmitia, E.C.; DeFelipe, J.; Jones, E.G.; Rakic, P.; Ribak, C.E. (Eds.), Changing Views of Cajal's Neuron. Progress in Brain Research Series, vol. 136, USA, pp. 135-143. (Pubitemid 35460974)
14. A. Feria-Velasco, and M.J. Karnovsky Optimal central nervous system preservation with glutaraldehyde perfusion for ultrastructural study Arch. Invest. Med. 1 1970 201 220
15. C.A. Frye Steroids, reproductive endocrine function, and cognition. A review Minerva Ginecol. 61 2009 563 585
16. I. González-Burgos Dendritic spines plasticity and learning/ memory processes: theory, evidence and perspectives L.R. Baylog, Dendritic Spines. Biochemistry, Modelling and Properties 2009 Nova Science Publishers, Inc. New York 163 186
17. I. González-Burgos, M. Alejandre-Gómez, and M. Cervantes Spine-type densities of hippocampal CA1 neurons vary in proestrus and estrus rats Neurosci. Lett. 379 2005 52 54 (Pubitemid 40462397)
18. González-Burgos, I.; Feria-Velasco, A. Psychobiological studies showing the serotonin involvement in the cognition-related behavioral performance. In: Gotsiridze-Columbus, N. (Ed.), Serotonin: Biosynthesis, Regulation and Health Implications. Nova Science Publishers, Inc.; New York, in press.
19. I. González-Burgos, D. González-Tapia, D.A. Velázquez Zamora, A. Feria-Velasco, and C. Beas-Zárate Guided motor training induces dendritic spine plasticity in adult rat cerebellar Purkinje cells Neurosci. Lett. 491 2011 216 220
20. I. González-Burgos, G. Tapia-Arizmendi, and A. Feria-Velasco Golgi method without osmium tetroxide for the study of the central nervous system Biotech. Histochem. 67 1992 288 296
21. E. Gould, C.S. Woolley, M. Frankfurt, and B. McEwen Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood J. Neurosci. 10 1990 1286 1291
22. G.D. Griffin, and L.M. Flanagan-Cato Estradiol and progesterone differentially regulate the dendritic arbor of neurons in the hypothalamic ventromedial nucleus of the female rat (Rattus norvegicus) J. Comp. Neurol. 510 2008 631 640
23. T. Hajszan, K. Szigeti-Buck, N.L. Sallam, J. Bober, A. Parducz, N.J. Maclusky, C. Leranth, and R.S. Duman Effects of estradiol on learned helplessness and associated remodeling of hippocampal spine synapses in female rats Biol. Psychiatry 67 2010 168 174
24. J. Hao, P.R. Rapp, W.G. Janssen, W. Lou, B.L. Lasley, P.R. Hof, and J.H. Morrison Interactive effects of age and estrogen on cognition and pyramidal neurons in monkey prefrontal cortex Proc. Natl. Acad. Sci. U.S.A. 104 2007 11465 11470 (Pubitemid 47175163)
25. K.M. Harris, F.E. Jensen, and B.H. Tsao Ultraestructure, development and plasticity of dendritic spine synapses in area CA1 of the rat hippocampus: extending our vision with serial electron microscopy and three-dimensional analyses V. Chan-Palay, Ch. Kôhler, The Hippocampus - New Vistas 1989 Alan R. Liss New York 33 52
26. K. Hayashi, and T. Shirao Change in the shape of dendritic spines caused by overexpression of drebrin in cultured cortical neurons J. Neurosci. 19 1999 3918 3925 (Pubitemid 29222266)
27. H. Hering, and M. Sheng Dendritic spines: structure, dynamics and regulation Nat. Rev. Neurosci. 2 2001 880 888 (Pubitemid 33674075)
28. J. Hongpaisan, and D.L. Alkon A structural basis for enhancement of long-term associative memory in single dendritic spines regulated by PKC Proc. Natl. Acad. Sci. U.S.A. 104 2007 19571 19576
29. H. Kasai, M. Matsuzaki, J. Noguchi, N. Yasumatsu, and H. Nakahara Structure-stability-function relationships of dendritic spines Trends Neurosci. 26 2003 360 368 (Pubitemid 36794552)
30. P.A. Keenan, W.H. Ezzat, K. Ginsburg, and G.J. Moore Prefrontal cortex as the site of estrogen's effect on cognition Psychoneuroendocrinology 26 2001 577 590 (Pubitemid 32524188)
31. C. Koch, and A. Zador The function of dendritic spines: devices subserving biochemical rather than electrical compartmentalization J. Neurosci. 13 1993 413 422 (Pubitemid 23045128)
32. C. Koch, A. Zador, and T.H. Brown Dendritic spines: convergence of theory and experiment Science 256 1992 973 974
33. N. Kojima, and T. Shirao Synaptic dysfunction and disruption of postsynaptic drebrin-actin complex: a study of neurological disorders accompanied by cognitive deficits Neurosci. Res. 58 2007 1 5 (Pubitemid 46678494)
34. E.A. Kramár, L.Y. Chen, N.J. Brandon, C.S. Rex, F. Liu, C.M. Gall, and G. Lynch Cytoskeletal changes underlie estrogen's acute effects on synaptic transmission and plasticity J. Neurosci. 29 2009 12982 12993
35. R. Krug, J. Born, and B. Rasch A 3-day estrogen treatment improves prefrontal cortex-dependent cognitive function in postmenopausal women Psychoneuroendocrinology 31 2006 965 975 (Pubitemid 44148914)
36. K.J. Lee, H. Kim, and I.J. Rhyu The roles of dendritic spine shapes in Purkinje cells Cerebellum 4 2005 97 104 (Pubitemid 40943006)
37. A. Lethaby, E. Hogervorst, M. Richards, A. Yesufu, and K. Yaffe Hormone replacement therapy for cognitive function in postmenopausal women Cochrane Database Syst. Rev. 2008 23
38. Ch. Li, W.G. Brake, R.D. Romeo, J.C. Dunlop, M. Gordon, R. Buzescu, A.M. Magarinos, P.B. Allen, P.B. Greengard, V. Luine, and B. McEwen Estrogen alters hippocampal dendritic spine shape and enhances synaptic protein immunoreactivity and spatial memory in female mice Proc. Natl. Acad. Sci. U.S.A. 101 2004 2185 2190 (Pubitemid 38229036)
39. F. Liu, M. Day, L.C. Muñiz, D. Bitran, R. Arias, R. Revilla-Sanchez, S. Grauer, G. Zhang, C. Kelley, V. Pulito, A. Sung, R.F. Mervis, R. Navarra, W.D. Hirst, P.H. Reinhart, K.L. Marquis, S.J. Moss, M.N. Pangalos, and N.J. Brandon Activation of estrogen receptor-beta regulates hippocampal synaptic plasticity and improves memory Nat. Neurosci. 11 2008 334 343 (Pubitemid 351311804)
40. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and R.J. Randall Protein measurement with the Folin phenol reagent J. Biol. Chem. 193 1951 265 275
41. M.A. López-Vázquez, M.E. Olvera-Cortés, and I. González-Burgos Multiunitary activity of prefrontal pyramidal neurons increases during spatial working memory performance, after serotonin depletion Int. J. Dev. Neurosci. 24 2006 502 503
42. V.N. Luine, S.T. Richards, V.Y. Wu, and K.D. Beck Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters Horm. Behav. 34 1998 149 162 (Pubitemid 28541756)
43. X.M. Ma, D.D. Kiraly, E.D. Gaier, Y. Wang, E.J. Kim, E.S. Levine, B.A. Eipper, and R.E. Mains Kalirin-7 is required for synaptic structure and function J. Neurosci. 28 2008 12368 12382
44. M. Matsuzaki, N. Honkura, G.C.R. Ellis-Davies, and H. Kasai Structural basis of long-term potentiation in single dendritic spines Nature 429 2004 761 766 (Pubitemid 38833127)
45. K.J. McLaughlin, H. Bimonte-Nelson, J.L. Neisewander, and C.D. Conrad Assessment of estradiol influence on spatial tasks and hippocampal CA1 spines: evidence that the duration of hormone deprivation after ovariectomy compromises 17beta-estradiol effectiveness in altering CA1 spines Horm. Behav. 54 2008 386 395
46. R.L. Meisel, and V.R. Luttrell Estradiol increases the dendritic length of ventromedial hypothalamic neurons in female Syrian hamsters Brain Res. Bull. 25 1990 165 168 (Pubitemid 20246631)
47. P. Mendez, L.M. GarciaSegura, and D. Muller Estradiol promotes spine growth and synapse formation without affecting pre-established networks Hippocampus 21 2011 1263 1267
48. 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 (Pubitemid 46213921)
49. D.D. Murphy, and M. Segal Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormons J. Neurosci. 16 1996 4059 4068 (Pubitemid 26192402)
50. M.K. Osterlund, and Y.L. Hurd Estrogen receptors in the human forebrain and in relation to neuropsychiatric disorders Prog. Neurobiol. 64 2001 251 267 (Pubitemid 32194454)
51. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordenates 1986 Academic Press New York
52. G. Pelletier, C. Labrie, C. Martel, S. Li, and F. Labrie Role of extraovarian estrogens in the regulation of gonadotropin releasing hormone mRNA expression in the brain J. Neuroendocrinol. 13 2001 678 682 (Pubitemid 32725575)
53. P. Penzes, and K.A. Jones Dendritic spine dynamics - a key role for kalirin-7 Trends Neurosci. 31 2008 419 427
54. M.I. Pérez-Vega, A. Feria-Velasco, and I. González-Burgos Prefrontocortical serotonin depletion results in plastic changes of prefrontocortical pyramidal neurons, underlying a greater efficiency of short-term memory Brain Res. Bull. 53 2000 291 300
55. C.G. Pontrello, M.Y. Sun, A. Lin, T.A. Fiacco, K.A. DeFea, and I.M. Ethell Cofilin under control of β-arrestin-2 in NMDA-dependent dendritic spine plasticity, long-term depression (LTD), and learning Proc. Natl. Acad. Sci. U.S.A. 109 2012 E442 E451
56. V.I. Popov, N.I. Medvedev, I.V. Patrushev, D.A. Ignat'ev, E.D. Morenkov, and M.G. Stewart Reversible reduction in dendritic spines in CA1 of rat and ground squirrel subjected to hypothermia-normothermia in vivo: a three-dimensional electron microscope study Neuroscience 149 2007 549 560 (Pubitemid 47633024)
57. J. Prange-Kiel, H. Jarry, M. Schoen, P. Kohlmann, C. Lohse, L. Zhou, and G.M. Rune Gonadotropin-release hormone regulates spine density via its regulatory role in hippocampal estrogen synthesis J. Cell Biol. 180 2008 417 426 (Pubitemid 351185925)
58. J. Prange-Kiel, L. Fester, L. Zhou, H. Jarry, and G.M. Rune Estrus cyclicity of spinogenesis: underlying mechanisms J. Neural Transm. 116 2009 1417 1425
59. J. Prange-Kiel, and G.M. Rune Direct and indirect effects of estrogen on rat hippocampus Neuroscience 138 2006 765 772
60. B. Racz, and R.J. Weinberg Spatial organization of cofilin in dendritic spines Neuroscience 138 2006 447 456 (Pubitemid 43255557)
61. A. Reyna-Neyra, I. Camacho-Arroyo, P. Ferrera, and C. Arias Estradiol and progesterone modify microtubule associated protein 2 content in the rat hippocampus Brain Res. Bull. 58 2002 607 612
62. C.N. Rudick, and C.S. Woolley Estrogen regulates functional inhibition of hippocampal CA1 pyramidal cells in the adult female rat J. Neurosci. 21 2001 6532 6543 (Pubitemid 32781097)
63. G.M. Rune, U. Wehrenberg, J. Prange-Kiel, L. Zhou, G. Adelmann, and M. Frotscer Estrogen up-regulates estrogen receptor alpha and synaptophysin in slice cultures of rat hippocampus Neuroscience 113 2002 167 175 (Pubitemid 34786022)
64. N.J. Sandstrom, and Ch.L. Williams Spatial memory retention is enhanced by acute and continuous estradiol replacement Horm. Behav. 45 2004 128 135 (Pubitemid 38326869)
65. M. Segal, and P. Andersen Dendritic spines shaped by synaptic activity Curr. Opin. Neurobiol. 10 2000 582 586
66. B.B. Sherwin Estrogen and cognitive functioning in women: lessons we have learned Behav. Neurosci. 126 2012 123 127
67. CC Smith, LC Vedder, and LL. McMahon Estradiol and the relationship between dendritic spines, NR2B containing NMDA receptors, and the magnitude of long-term potentiation at hippocampal CA3-CA1 synapses Psychoneuroendocrinology 34 Suppl. 1 2009 S130 S142
68. K.E. Sorra, and K.M. Harris Overview on the structure, composition, function, development, and plasticity of hippocampal dendritic spines Hippocampus 10 2000 501 511
69. L. Tarelo-Acuña, E. Olvera-Cortés, and I. González-Burgos Prenatal and postnatal exposure to ethanol induces changes in the shape of the dendritic spines from hippocampal CA1 pyramidal neurons of the rat Neurosci. Lett. 286 2000 13 16 (Pubitemid 30259109)
70. D.A. Velázquez-Zamora, M.M. González-Ramírez, C. Beas-Zárate, and I. González-Burgos Egocentric working memory impairment and dendritic spine plastic changes in prefrontal neurons after NMDA receptor blockade, in rats Brain Res. 1402 2011 101 108
71. D.A. Velázquez-Zamora, M. Martínez-Degollado, and I. González-Burgos Morphological development of dendritic spines on rat cerebellar Purkinje cells Int. J. Dev. Neurosci. 29 2011 515 520
72. S.G. Warren, and J.M. Juraska Spatial and nonspatial learning across the rat estrous cycle Behav. Neurosci. 111 1997 259 266 (Pubitemid 27169317)
73. C.S. Woolley, E. Gould, M. Frankfurt, and B. McEwen Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons J. Neurosci. 10 1990 4035 4039
74. C.S. Woolley, and B. McEwen Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat J. Neurosci. 12 1992 2549 2554
75. C.S. Woolley, and B. 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 296 306
76. C.S. Woolley, and B. McEwen Estradiol regulates hippocampal dendritic spine density via an N-methyl-d-aspartate receptor-dependent mechanism J. Neurosci. 14 1994 7680 7687
77. C.S. Woolley, H.J. Wenzel, and P.A. Schwartzkroin Estradiol increases the frequency of multiple synapse boutons in the hippocampal CA1 region of the adult female rat J. Comp. Neurol. 373 1996 108 117 (Pubitemid 26292122)
78. Z. Xie, H. Photowala, M.E. Cahill, D.P. Srivastava, K.M. Woolfrey, C.Y. Shum, R.L. Huganir, and P. Penzes Coordination of synaptic adhesion with dendritic spine remodeling by AF-6 and kalirin-7 J. Neurosci. 28 2008 6079 6091
79. Z. Xie, D.P. Srivastava, H. Photowala, L. Kai, M.E. Cahill, K.M. Woolfrey, C.Y. Shum, D.J. Surmeier, and P. Penzes Kalirin-7 controls activity-dependent structural and functional plasticity of dendritic spines Neuron 56 2007 640 656 (Pubitemid 350102031)
80. L. Zhou, L. Fester, B. von Blittersdorff, B. Hassu, H. Nogens, J. Prange-Kiel, H. Jarry, K. Wegscheider, and G.M. Rune Aromatase inhibitors induce spine synapse loss in the hippocampus of ovariectomized mice Endocrinology 151 2010 1153 1160