Estrogen and aging affect the synaptic distribution of estrogen receptor beta-immunoreactivity in the CA1 region of female rat hippocampus

Brain Research

Volumn 1379, Issue , 2011, Pages 86-97

  Waters, Elizabeth M ^b   Yildirim, Murat ^a,b,e   Janssen, William G M ^a   Lou, W Y Wendy ^c   McEwen, Bruce S ^b   Morrison, John H ^a   Milner, Teresa A ^b,d  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

^e HACETTEPE UNIVERSITY   (Turkey)

Author keywords

Aging; Electron microscopy; Estrogen receptor beta; Estrogen treatment; Hippocampus; Immunocytochemistry; Ovariectomy; Rats; Synapses

Indexed keywords

CHOLESTEROL; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ELECTRON MICROSCOPY; EMBEDDING; ESTROGEN THERAPY; FEMALE; GROUPS BY AGE; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; MICROCAPSULE; NONHUMAN; OVARIECTOMY; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SYNAPTOGENESIS;

AGING; ANIMALS; CA1 REGION, HIPPOCAMPAL; ESTRADIOL; ESTROGEN RECEPTOR BETA; ESTROGENS; FEMALE; OVARIECTOMY; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES;

RATTUS;

EID: 79952312781     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.09.069     Document Type: Article

References (71)

1. Adams, M.M., Morrison, J.H., Gore, A.C., 2001a. N-methyl-Daspartate receptor mRNA levels change during reproductive senescence in the hippocampus of female rats. Exp. Neurol. 170, 171-179.
2. Adams, M.M., Oung, T., Morrison, J.H., Gore, A.C., 2001b. Length of postovariectomy interval and age, but not estrogen replacement, regulate N-methyl-D-aspartate receptor mRNA levels in the hippocampus of female rats. Exp. Neurol. 170, 345-356.
3. Adams, M.M., Shah, R.A., Janssen, W.G., Morrison, J.H., 2001c. Different modes of hippocampal plasticity in response to estrogeninyoung and aged female rats. Proc. Natl Acad. Sci. USA 98, 8071-8076.
4. Adams, M.M., Fink, S.E., Janssen, W.G., Shah, R.A., Morrison, J.H., 2004. Estrogen modulates synaptic N-methyl-D-aspartate receptor subunit distribution in the aged hippocampus. J. Comp. Neurol. 474, 419-426.
5. Adams, M.M., Fink, S.E., Shah, R.A., Janssen, W.G., Hayashi, S., Milner, T.A., McEwen, B.S., Morrison, J.H., 2002. Estrogen and aging affect the subcellular distribution of estrogen receptor-alpha in the hippocampus of female rats. J. Neurosci. 22, 3608-3614. (Pubitemid 37465765)
6. Alonso-Magdalena, P., Ropero, A.B., Carrera, M.P., Cederroth, C.R., Baquié, M., Gauthier, B.R., Nef, S., Stefani, E., Nadal, A., 2008. Pancreatic insulin content regulation by the estrogen receptor ER alpha. PLoS ONE 3, e2069.
7. Becker, J.B., 1990. Direct effect of 17 beta-estradiol on striatum: sex differences in dopamine release. Synapse 5 (2), 157-164. (Pubitemid 20095108)
8. Bi, R., Broutman, G., Foy, M.R., Thompson, R.F., Baudry, M., 2000. The tyrosine kinase and mitogen-activated protein kinase pathways mediate multiple effects of estrogen in hippocampus. Proc. Natl Acad. Sci. USA 97, 3602-3607.
9. Brake, W.G., Alves, S.E., Dunlop, J.C., Lee, S.J., Bulloch, K., Allen, P.B., Greengard, P., McEwen, B.S., 2001. Novel target sites for estrogen action in the dorsal hippocampus: an examination of synaptic proteins. Endocrinology 142, 1284-1289. (Pubitemid 32202840)
10. Burke, S.N., Barnes, C.A., 2010. Senescent synapses and hippocampal circuit dynamics. Trends Neurosci. 33, 153-161.
11. Dubal, D.B., Zhu, H., Yu, J., Rau, S.W., Shughrue, P.J., Merchenthaler, I., Kindy, M.S., Wise, P.M., 2001. Estrogen receptor alpha, not beta, is a critical link in estradiol-mediated protection against brain injury. Proc. Natl Acad. Sci. USA 98, 1952-1957.
12. Elste, A.M., Benson, D.L., 2006. Structural basis for developmentally regulated changes in cadherin function at synapses. J. Comp. Neurol. 495, 324-335.
13. Fan, L., Zhao, Z., Orr, P.T., Chambers, C.H., Lewis, M.C., Frick, K.M., 2010. 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, 4390-4400.
14. Fernandez, S.M., Lewis, M.C., Pechenino, A.S., Harburger, L.L., Orr, P.T., Gresack, J.E., Schafe, G.E., Frick, K.M., 2008. Estradiol-mediated enhancement of object memory consolidation involves hippocampal extracellular signal-regulated kinase activation and membrane-bound estrogen receptors. J. Neurosci. 28, 8660-8667.
15. Foy, M.R., Xu, J., Xie, X., Brinton, R.D., Thompson, R.F., Berger, T.W., 1999. 17beta-Estradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation. J. Neurophysiol. 81, 925-929. (Pubitemid 29264535)
16. Funabashi, T., Kleopoulos, S.P., Kimura, F., Mobbs, C.V., 1998. Changes in neurotensin mRNA expression by estrogen in the female rat preoptic are during aging: an in situ hybridization histochemistry study. Gen. Comp. Endocrinol. 112, 364-371.
17. Gould, E., Woolley, C.S., Frankfurt, M., McEwen, B.S., 1990. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J. Neurosci. 10, 1286-1291.
18. Ishunina, T.A., Swaab, D.F., 2001. Increased expression of estrogen receptor alpha and beta in the nucleus basalis of Meynert in Alzheimer's disease. Neurobiol. Aging 22, 417-426. (Pubitemid 32510914)
19. Ishunina, T.A., Kruijver, F.P., Balesar, R., Swaab, D.F., 2000. Differential expression of estrogen receptor alpha and beta immunoreactivity in the human supraoptic nucleus in relation to sex and aging. J. Clin. Endocrinol. Metab. 83, 3283-3291.
20. Janssen, W.G., Vissavajjhala, P., Andrews, G., Moran, T., Hof, P.R., Morrison, J.H., 2005. Cellular and synaptic distribution of NR2A and NR2B in macaque monkey and rat hippocampus as visualized with subunit-specific monoclonal antibodies. Exp. Neurol. 191 (Suppl 1), S28-S44.
21. Kelly, M.J., Ronnekleiv, O.K., 2009. Control of CNS neuronal excitability by estrogens via membrane-initiated signaling. Mol. Cell. Endocrinol. 308, 17-25.
22. Korol, D.L., Kolo, L.L., 2002. Estrogen-induced changes in place and response learning in young adult female rats. Behav. Neurosci. 116, 411-420.
23. Kramar, E.A., Chen, L.Y., Brandon, N.J., Rex, C.S., Liu, F., Gall, C.M., Lynch, G., 2009. Cytoskeletal changes underlie estrogen's acute effects on synaptic transmission and plasticity. J. Neurosci. 29, 12982-12993.
24. Lauber, A.H., Romano, G.J., Mobbs, C.V., Howells, R.D., Pfaff, D.W., 1990. Estradiol induction of proenkephalin messenger RNA in the hypothalamus: dose-response and relation to reproductive behavior in the female rat. Brain Res. Mol. Brain Res. 8, 47-54.
25. Levin, E.R., 2001. Cell localization, physiology, and nongenomic actions of estrogen receptors. J. Appl. Physiol. 91, 1860-1867.
26. Lindberg, M.K., Moverare, S., Skrtic, S., Gao, H., Dahlman-Wright, K., Gustafsson, J.A., Ohlsson, C., 2003. Estrogen receptor (ER)-beta reduces ERalpha-regulated gene transcription, supporting a "ying yang" relationship between ERalpha and ERbeta in mice. Mol. Endocrinol. 17, 203-208.
27. Liu, F., Day, M., Muniz, L.C., Bitran, D., Arias, R., Revilla-Sanchez, R., Grauer, S., Zhang, G., Kelley, C., Pulito, V., Sung, A., Mervis, R.F., Navarra, R., Hirst, W.D., Reinhart, P.H., Marquis, K.L., Moss, S.J., Pangalos, M.N., Brandon, N.J., 2008. Activation of estrogen receptor-beta regulates hippocampal synaptic plasticity and improves memory. Nat. Neurosci. 11, 334-343.
28. Luine, V.N., Jacome, L.F., Maclusky, N.J., 2003. Rapid enhancement of visual and place memory by estrogens in rats. Endocrinology 144, 2836-2844. (Pubitemid 36819884)
29. McEwen, B., Akama, K., Alves, S., Brake, W.G., Bulloch, K., Lee, S., Li, C., Yuen, G., Milner, T.A., 2001. Tracking the estrogen receptor in neurons: implications for estrogen-induced synapse formation. Proc. Natl Acad. Sci. USA 98, 7093-7100.
30. Mehra, R.D., Sharma, K., Nyakas, C., Vij, U., 2005. Estrogen receptor alpha and beta immunoreactive neurons in normal adult and aged female rat hippocampus: a qualitative and quantitative study. Brain Res. 1056, 22-35. (Pubitemid 41219354)
31. Miller, N.R., Jover, T., Cohen, H.W., Zukin, R.S., Etgen, A.M., 2005. Estrogen can act via estrogen receptor alpha and beta to protect hippocampal neurons against global ischemia-induced cell death. Endocrinology 146, 3070-3079. (Pubitemid 41002816)
32. Milner, T.A., Lubbers, L.S., Alves, S.E., McEwen, B.S., 2008. Nuclear and extranuclear estrogen binding sites in the rat forebrain and autonomic medullary areas. Endocrinology 149, 3306-3312. (Pubitemid 351919599)
33. Milner, T.A., McEwen, B.S., Hayashi, S., Li, C.J., Reagan, L.P., Alves, S.E., 2001. Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites. J. Comp. Neurol. 429, 355-371.
34. Milner, T.A., Ayoola, K., Drake, C.T., Herrick, S.P., Tabori, N.E., McEwen, B.S., Warrier, S., Alves, S.E., 2005. Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation. J. Comp. Neurol. 491, 81-95.
35. Miranda, P., Williams, C.L., Einstein, G., 1999. Granule cells in aging rats are sexually dimorphic in their response to estradiol. J. Neurosci. 19, 3316-3325. (Pubitemid 29203111)
36. Mitterling, K.L., Spencer, J.L., Dziedzic, N., Shenoy, S., McCarthy, K., Waters, E.M., McEwen, B.S., Milner, T.A., 2010. Cellular and subcellular localization of estrogen and progestin receptor in the mouse hippocampus. J. Comp. Neurol. 518, 2729-2743.
37. McEwen, B.S., Alves, S.E., 1999. Estrogen actions in the central nervous system. Endocr. Rev. 20 (3), 279-307.
38. Monroe, D.G., Johnsen, S.A., Subramaniam, M., Getz, B.J., Khosla, S., Riggs, B.L., Spelsberg, T.C., 2003. Mutual antagonism of estrogen receptors alpha and beta and their preferred interactions with steroid receptor coactivators in human osteoblastic cell lines. J. Endocrinol. 176, 349-357. (Pubitemid 36416546)
39. Nealen, M.L., Vijayan, K.V., Bolton, E., Bray, P.F., 2001. Human platelets contain a glycosylated estrogen receptor beta. Circ. Res. 88, 438-442.
40. O'Malley, C.A., Hautamaki, R.D., Kelley, M., Meyer, E.M., 1987. Effects of ovariectomy and estradiol benzoate on high affinity choline uptake, ACh synthesis, and release from rat cerebral cortical synaptosomes. Brain Research 403 (2), 389-392.
41. Packard, M.G., Teather, L.A., 1997. Intra-hippocampal estradiol infusion enhances memory in ovariectomized rats. NeuroReport 8, 3009-3013. (Pubitemid 27421724)
42. Paech, K., Webb, P., Kuiper, G.G., Nilsson, S., Gustafsson, J., Kushner, P.J., Scanlan, T.S., 1997. Differential ligand activation of estrogen receptors ERalpha and ERbeta at AP1 sites. Science 277, 1508-1510. (Pubitemid 27449239)
43. Razandi, M., Pedram, A., Merchenthaler, I., Greene, G.L., Levin, E.R., 2004. Plasma membrane estrogen receptors exist and functions as dimers. Mol. Endocrinol. 18, 2854-2865.
44. Rhodes, M.E., Frye, C.A., 2006. ERbeta-selective SERMs produce mnemonic-enhancing effects in the inhibitory avoidance and water maze tasks. Neurobiol. Learn. Mem. 85, 183-191.
45. Rissman, E.F., Heck, A.L., Leonard, J.E., Shupnik, M.A., Gustafsson, J.A., 2002. Disruption of estrogen receptor beta gene impairs spatial learning in female mice. Proc. Natl Acad. Sci. USA 99, 3996-4001.
46. Rizzoli, S.O., Betz, W.J., 2005. Synaptic vesicle pools. Nat. Rev. Neurosci. 6, 389-394.
47. Roger, C., Lambard, S., Bouskine, A., Mograbi, B., Chevallier, D., Nebout, M., Pointis, G., Carreau, S., Fenichel, P., 2005. Estrogen-induced growth inhibition of human seminoma cells expressing estrogen receptor beta and aromatase. J. Mol. Endocrinol. 35, 191-199.
48. Roger, P., Sahla, M.E., Makela, S., Gustafsson, J.A., Baldet, P., Rochefort, H., 2001. Decreased expression of estrogen receptor beta protein in proliferative preinvasive mammary tumors. Cancer Res. 61, 2537-2541. (Pubitemid 32685835)
49. Royuela, M., de Miguel, M.P., Bethencourt, F.R., Sancherz-Chapado, M., Fraile, B., Arenas, M.I., Paniagua, R., 2001. Estrogen receptors alpha and beta in the normal, hyperplastic and carcinomatous human prostate. J. Neuroendocrinol. 168, 447-454. (Pubitemid 32241889)
50. Ruud, H.K., Blackstad, T.W., 1999. PALIREL, a computer program for analyzing particle-to-membrane relations, with emphasis on electron micrographs of immunocytochemical preparations and gold labeled molecules. Comput. Biomed. Res. 32, 93-122.
51. Sandstrom, N.J., Williams, C.L., 2001. Memory retention is modulated by acute estradiol and progesterone replacement. Behav. Neurosci. 115, 384-393.
52. Sandstrom, N.J., Williams, C.L., 2004. Spatial memory retention is enhanced by acute and continuous estradiol replacement. Horm. Behav. 45, 128-135.
53. Saneyorshi, T., Fortin, D.A., Soderling, T.R., 2010. Regulation of spine and synapse formation by activity-dependent intracellular signaling pathways. Curr. Opin. Neurobiol. 20, 108-115.
54. Shughrue, P.J., Lane, M.V., Merchenthaler, I., 1997. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J. Comp. Neurol. 388, 507-525.
55. Snyder, M.A., Smejkalova, T., Forlano, P.M., Woolley, C.S., 2010. Multiple ERbeta antisera label in ERbeta knockout and null mouse tissues. J. Neurosci. Methods.
56. Speir, E., Yu, Z.X., Takeda, K., Ferrans, V.J., ROr, Cannon, 2000. Competition for p300 regulates transcription of estrogen receptors and nuclear factor-kappaB in human coronary smooth muscle cells. Circ. Res. 87, 1006-1011.
57. Spencer, J.L., Waters, E.M., Milner, T.A., McEwen, B.S., 2008. Estrous cycle regulates activation of hippocampal Akt, LIM kinase, and neurotrophin receptors in C57BL/6 mice. Neuroscience 155, 1106-1119.
58. Szymczak, S., Kalita, K., Jaworski, J., Mioduszewska, B., Savonenko, A., Markowska, A., Merchenthaler, I., Kaczmarek, L., 2006. Increased estrogen receptor beta expression correlates with decreased spine formation in the rat hippocampus. Hippocampus 16, 453-463. (Pubitemid 44712069)
59. Tetel, M.J., Pfaff, D.W., 2010. Contributions of estrogen receptor-alpha and estrogen receptor-beta to the regulation of behavior. Biochem Biophys Acta.
60. Torres-Reveron, A., Khalid, S., Williams, T.J., Waters, E.M., Jacome, L.F., Luine, V.N., Drake, C.T., McEwen, B.S., Milner, T.A., 2009. Hippocampal dynorphin immunoreactivity increases in response to gonadal steroids and is positioned for direct modulation by ovarian steroid receptors. Neuroscience 159, 204-216.
61. Towart, L.A., Alves, S.E., Znamensky, V., Hayashi, S., McEwen, B.S., Milner, T.A., 2003. Subcellular relationships between cholinergic terminals and estrogen receptor-alpha in the dorsal hippocampus. J. Comp. Neurol. 463, 390-401.
62. van Lookeren, Campagne M., Oestreicher, A.B., van der Krift, T.P., Gispen, W.H., Verkleij, A.J., 1991. Freeze-substitution and Lowicryl HM20 embedding of fixed rat brain: suitability for immunogold ultrastructural localization of neural antigens. J. Histochem. Cytochem. 39, 1267-1279.
63. Walf, A.A., Koonce, C., Manley, K., Frye, C.A., 2009. Proestrous compared to diestrous wildtype, but not estrogen receptor beta knockout, mice have better performance in the spontaneous alternation and object recognition tasks and reduced anxiety-like behavior in the elevated plus and mirror maze. Behavioral Brain Research 196, 254-260.
64. Waters, E.M., Mitterling, K.L., Spencer, J.L., Mazid, S., McEwen, B.S., Milner, T.A., 2009. Estrogen receptor alpha and beta specific agonists regulate expression of synaptic proteins in rat hippocampus. Brain Res. 1290, 1-11.
65. Woolley, C.S., McEwen, B.S., 1992. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J. Neurosci. 12, 2549-2554.
66. Woolley, C.S., McEwen, B.S., 1993. Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J. Comp. Neurol. 336, 293-306.
67. Woolley, C.S., Gould, E., Frankfurt, M., McEwen, B.S., 1990. Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J. Neurosci. 10, 4035-4039.
68. Yildirim, M., Janssen, W.G., Lou, W.Y., Akama, K.T., McEwen, B.S., Milner, T.A., Morrison, J.H., 2011. Effects of estrogen and aging on the synaptic distribution of phosphorylated Akt-immunoreactivity in the CA1 region of the female rat hippocampus. Brain Res. 1379, 98-108.
69. Yildirim, M., Janssen, W.G., Tabori, N.E., Adams, M.M., Yuen, G.S., Akama, K.T., McEwen, B.S., Milner, T.A., Morrison, J. H., 2008. Estrogen and aging affect synaptic distribution of phosphorylated LIM kinase (pLIMK) in the CA1 region of the female rat hippocampus. Neuroscience 152, 360-370.
70. Zadran, S., Qin, Q., Bi, X., Kim, Y., Foy, M.R., Thompson, R., Baudry, M., 2009. 17-Beta-estradiol increases neuronal excitability through MAP kinase-induced calpain activation. Proc. Natl Acad. Sci. USA 106, 21936-21941.
71. Zhang, Q.H., Huang, Y.H., Hu, Y.Z., Wei, G.Z., Han, X.F., Lu, S.Y., Zhao, Y.F., 2004. Disruption of estrogen receptor beta in mice brain results in pathological alterations resembling Alzheimer disease. Acta Pharmacol. Sin. 25, 452-457.