Hetereogeneity of dose and time effects of estrogen on neuron-specific neuronal protein and phosphorylated cyclic AMP response element-binding protein in the hippocampus of ovariectomized rats

Journal of Neuroscience Research

Volumn 89, Issue 6, 2011, Pages 883-897

  Bakkum, Barclay W ^a,b   Fan, Lu ^a,c   Pandey, Subhash C ^a,c   Cohen, Rochelle S ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b ILLINOIS COLLEGE OF OPTOMETRY   (United States)

^c JESSE BROWN VA MEDICAL CENTER   (United States)

Author keywords

Estrogen; Hippocampus; NeuN; Phosphorylated CREB; Stereology

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; ESTRADIOL BENZOATE; ESTROGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; BRAIN REGION; CONCENTRATION RESPONSE; DENTATE GYRUS; HIPPOCAMPUS; NERVE CELL; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; STEREOLOGY;

ANALYSIS OF VARIANCE; ANIMALS; CELL COUNT; CREB-BINDING PROTEIN; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTRADIOL; ESTROGENS; FEMALE; GENE EXPRESSION REGULATION; HIPPOCAMPUS; NEURONS; ORGAN SIZE; OVARIECTOMY; PHOSPHOPYRUVATE HYDRATASE; PHOSPHORYLATION; RADIOIMMUNOASSAY; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS; UTERUS;

EID: 79954529408     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22601     Document Type: Article

References (71)

1. Ábrahám IM, Han S, Todman MG, Korach KS, Herbison AE. 2003. Estrogen receptor β mediates rapid estrogen actions on gonadotropin-releasing hormone neurons in vivo. J Neurosci 23: 5771-5777.
2. Barha CK, Dalton GL, Galea LA. 2009. Low doses of 17alpha-estradiol and 17beta-estradiol facilitate, whereas higher doses of estrone and 17alpha- and 17beta-estradiol impair, contextual fear conditioning in adult female rats. Neuropsychopharmacology 35: 547-59.
3. Barker JM, Galea LA. 2008. Repeated estradiol administration alters different aspects of neurogenesis and cell death in the hippocampus of female, but not male, rats. Neuroscience 52: 888-902.
4. Becker JB. 1999. Gender differences in dopaminergic function in striatum and nucleus accumbens. Pharmacol Biochem Behav 64: 803-812.
5. Bondar G, Kuo J, Micevych P. 2009. Estradiol-induced receptor-α trafficking. J Neurosci 29: 15323-15330.
6. Boulware MI, Weick JP, Becklund BR, Kuo SP, Groth RD, Mermelstein PG. 2005. Estradiol activates group I and II metabotropic glutamate receptor signaling, leading to opposing influences on cAMP response-element binding protein. J Neurosci 25: 5066-5078.
7. Boulware MI, Kordasiewicz H, Mermelstein PG. 2007. Calveolin proteins are essential for distinct effects of membrane estrogen receptors in neurons. J Neurosci 27: 9941-9950.
8. Brailou E, Dun SL, Brailou GC, Mizuo K, Sklar LA, Oprea TI, Prossnitz ER, Dun NJ. 2007. Distribution and characterization of estrogen G protein-coupled receptor 30 in the rat central nervous system. J Endocrinol 193: 311-321.
9. Carlstrom L, Ke ZJ, Unnerstall JR, Cohen RS, Pandey SC. 2001. Estrogen modulation of the cyclic AMP response element-binding protein pathway. Effects of long-term and acute treatments. Neuroendocrinology 74: 227-243.
10. Cohen RS, Pfaff DW. 1981. Ultrastructure of neurons in the ventromedial nucleus or the hypothalamus in ovariectomized rats with or without estrogen treatment. Cell Tissue Res 217: 451-470.
11. Dowsett M, Folkerd E. 2005. Deficits in plasma oestradiol measurements in studies and management of breast cancer. Breast Cancer Res 7: 1-4.
12. Fan L, Hanbury R, Pandey SC, Cohen RS. 2008a. Dose and time effects of estrogen on expression of neuron-specific protein and cyclic AMP response element-binding protein and brain region volume in the medial amygdala of ovariectomized rats. Neuroendocrinology 88: 111-126.
13. Fan L, Pandey SC, Cohen RS. 2008b. Estrogen affects levels of Bcl-2 protein and mRNA in medial amygdala of ovariectomized rats. J Neurosci Res 86: 3655-3664.
14. Galea LA, Uban KA, Epp JR, Brummelte S, Barha CK, Wilson WL, Lieblich SE, Pawluski JL. 2008. Endocrine regulation of cognition and neuroplasticity: our pursuit to unveil the complex interaction between hormones, the brain, and behaviour. Can J Exp Psychol 62: 247-260.
15. García-Ovejero D, Veiga S, García-Segura LM, DonCarlos LM. 2002. Glial expression of estrogen and androgen receptors after rat brain injury. J Comp Neurol 450: 256-271.
16. García-Segura LM, Cardona-Gomez P, Naftolin F, Chowen J. 1998. Estradiol upregulates Bcl-2 expression in adult brain neurons. Neuroendocrinology 9: 593-597.
17. Gibbs RB. 2000. Effects of gonadal hormone replacement on measures of basal forebrain cholinergic function. Neuroscience 101: 931-938.
18. Gingerich S, Kim GL, Chalmers JA, Koletar MM, Wang X, Wang Y, Belsham DD. 2010. Estrogen receptor alpha and G-protein coupled receptor 30 mediate the neuroprotective effects of 17β-estradiol in novel murine hippocampal cell models. Neurosciece 170: 54-66.
19. Goodman RL. 1978. A quantitative analysis of the physiological role of estradiol and progesterone in the control of tonic and surge secretion of luteinizing hormone in the rat. Endocrinology 102: 42-150.
20. Gu G, Rojo AA, Zee MC, Yu J, Simerly RB. 1996. Hormonal regulation of CREB phosphorylation in the anteroventral periventricular nucleus. J Neurosci 16: 3035-3044.
21. Gundersen HJ, Jensen EB, Kiêu K, Nielsen J. 1999. The efficiency of systematic sampling in stereology-reconsidered. J Microsc 193: 199-211.
22. Hanbury R, Pandey SC, Cohen RS. 2007. Strain-dependent differences in plasma steroid horone levels and in phosphorylated CREB (pCREB) levels in limbic brain areas of intact and ovariectomized (OVX) female rats. Soc Neurosci Abstr 729: 17.
23. Hoffman GE, Moore N, Fiskum G, Murphy AZ. 2003. Ovarian steroid modulation of seizure severity and hippocampal cell death after kainic acid treatment. Exp Neurol 182: 124-134.
24. Hoffman GE, Le WW, Schulterbrandt T, Legan SJ. 2005. Estrogen and progesterone do not activate Fos in AVPV or LHRH neurons in male rats. Brain Res 1054: 116-124.
25. Kelly MJ, Rønnekleiv OK. 2009. Control of CNS neuronal excitability by estrogens via membrane initiated signaling. Mol Cell Endocrinol 308: 17-25.
26. Kow LM, Pfaff DW. 1975. Induction of lordosis in female rats: two models of estrogen action and the effect of adrenalectomy. Horm Behav 6: 259-276.
27. Kuo J, Hamid N, Bondar G, Prossnitz ER, Micevych P. 2010. Membrane estrogen receptors stimulate intracellular calcium release and progesterone synthesis in hypothalamic astrocytes. J Neurosci 30: 12950-12957.
28. Lauber AH, Mobbs CV, Muramatsu M, Pfaff DW. 1991. Estrogen receptor messenger RNA expression in rat hypothalamus as a function of genetic sex and estrogen dose. Endocrinology 129: 3180-3186.
29. Lee SJ, Campomanes CR, Sikat PT, Greenfield AT, Allen PB, McEwen BS. 2004a. Estrogen induces phosphorylation of cyclic AMP response element binding (pCREB) in primary hippocampal cells in a time-dependent manner. Neuroscience 124: 549-560.
30. Lee SJ, Romeo RD, Svenningsson P, Campomanes CR, Allen PB, Greengard P, McEwen BS. 2004b. Estradiol affects spinophilin protein differently in gonadectomized males and females. Neuroscience 127: 983-988.
31. Lister JP, Tonkiss J, Blatt GJ, Kemper TL, DeBassio WA, Galler JR, Rosene DL. 2006. Asymmetry of neuron numbers in the hippocampal formation of prenatally malnourished and normally nourished rats: a stereological investigation. Hippocampus 16: 946-958.
32. Lorenz B, García-Segura LM, DonCarlos LL. 2005. Cellular phenotype of androgen receptor-immunoreactive nuclei in the developing and adult rat brain J Comp Neurol 492: 456-468.
33. Luquin S, Naftolin F, García-Segura LM. 1993. Natural fluctuation and gonadal hormone regulation of astrocyte immunoreactivity in dentate gyrus. J Neurobiol 24: 913-924.
34. Lyck L, Jelsing J, Jensen PS, Lambertsen KL, Pakkenberg B, Finsen B. 2006. Immunohistochemical visualization of neurons and specific glial cells for stereological application in the porcine neocortex. J Neurosci Methods 152: 229-242.
35. Maggiolini M, Picard D. 2010. The unfolding stories of GPR30, a new membrane-bound estrogen receptor. J Endocrinol 204: 105-114.
36. Matsuda K, Sakamoto H, Mori H, Hosokawa K, Kawamura A, Itose M, Nishi M, Prossnitz ER, Kawata M. 2008. Expression and intracellular distribution of the G protein-coupled receptor 30 in rat hippocampal formation. Neurosci Lett 441: 94-99.
37. Medlock KL, Forrester TM, Sheehan DM. 1991a. Short-term effects of physiological and pharmacological doses of estradiol on estrogen receptor and uterine growth. J Recept Res 11: 743-756.
38. Medlock KL, Lyttle CR, Kelepouris N, Newman ED, Sheehan DM. 1991b. Estradiol down-regulation of the rat uterine estrogen receptor. Proc Soc Exp Biol Med 196: 293-300.
39. Mermelstein PG, Micevych PE. 2008. Nervous system physiology regulated by membrane estrogen receptors. Rev Neurosci 19: 423-424.
40. Micevych PE, Mermelstein PG. 2008. Membrane estrogen receptors acting through metabotropic glutamate receptors: an emerging mechanism of estrogen action in the brain. Mol Neurobiol 38: 66-67.
41. Milner TA, Ayoola K, Drake CT, Herrick SP, Tabori NE, McEwen BS, Warrier S, Alves SE. 2005. Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation. J Comp Neurol 491: 81-95.
42. Morris JA, Jordan CL, Dugger, BN, Breedlove SM. 2005. Partial demasculinization of several brain regions in adult male (XY) rats with a dysfunctional androgen receptor gene. J Comp Neurol 487: 217-226.
43. Mullen RJ, Buck CR, Smith AN. 1992. NeuN, a neuronal specific nuclear protein in vertebrates. Development 116: 201-211.
44. Musholt K, Cirillo G, CAvaliere C, Bianco MR, Bock J, Helmeke C, Braun K, Papa M. 2009. Neonatal separation stress reduces glial fibrillary acidic protein- and S100-immunoreactive astrocytes in rat medial precentral cortex. Dev Neurobiol 69: 203-211.
45. Nakagawa S, Kim JE, Lee R, Chen J, Fujioka T, Malberg J, Tsuji S, Duman RS. 2002. Localization of phosphorylated cAMP response element-binding protein in immature neurons of adult hippocampus. J Neurosci 22: 9868-9876.
46. Nakamura NH, Rosell DR, Akama KT, McEwen BS. 2004. Estrogen and ovariectomy regulate mRNA and protein of glutamic acid decarboxylases and cation-chloride cotransporters in the adult rat hippocampus. Neuroendocrinology 80: 308-323.
47. Olde B, Leeb-Lundberg LMF. 2009. GRP30/GPER1: searching for a role in estrogen physiology. Trends Endocrinol Metab 20: 409-416.
48. Pandey SC, Zhang H, Roy A, Xu T. 2005. Deficits in amygdaloid cAMP-responsive element-binding protein signaling play a role in genetic predisposition to anxiety and alcoholism. J Clin Invest 115: 2762-2773.
49. Paxinos G, Watson C. 1998. The rat brain in stereotaxic coordinates. San Diego: Academic Press.
50. Porte Y, Buhot MC, Mons NE. 2008. Spatial memory in the Morris water maze and activation of cyclic AMP response element-binding (CREB) protein within the mouse hippocampus. Learn Mem 15: 885-894.
51. Raval AP, Saul I, Defazio KR, Perez-Pinzon MA, Bramlett H. 2009. Pretreatment with a single estradiol-17β bolus activates cyclic-AMP response element binding protein and protects CA1 neurons against global cerebral ischemia. Neuroscience 160: 307-318.
52. Reimers TJ, Lamb SV, Bartlett SA, Matamoros RA, Cowan RG, Engel JS. 1991. Effects of hemolysis and storage on quantification of hormones in blood samples from dogs, cattle, and horse. Am J Vet Res 7: 1075-1080.
53. Rønnekleiv OK, Malyala A, Kelly MJ. 2007. Membrane-initiated signaling of estrogen in the brain. Semin Reprod Med 25: 165-177.
54. Schumann CM, Amaral DG. 2005. Stereological estimation of the number of neurons in the human amygdaloid complex. J Comp Neurol 491: 320-329.
55. Shors TJ, Leuner B. 2003. Estrogen-mediated effects on depression and memory formation in females. J Affect Disord 74: 85-96.
56. Shughrue PJ, Lane MV, Merchenthaler I. 1997. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J Comp Neurol 388: 507-525.
57. Struble RG, Afridi S, Beckman-Randall S, Li M, Cady C, Nathan B, McAey ME. 2006. Neocortical and hippocampal glial fibrillary acidic protein immunoreactivity shows region-specific variation during the mouse estrous cycle. Neuroendocrinology 83: 325-335.
58. Szegö EM, Barabas K, Balog J, Szilagyi N, Korach KS, Juhasz G, Ábrahám IM. 2006. Estrogen induces estrogen receptor α-dependent cAMP response element-binding protein phosphorylation via mitogen activated protein kinase pathway in basal forebrain cholinergic neurons in vivo. J Neurosci 26: 4104-4110.
59. Takuma K, Matsuo A, Himeno Y, Hoshina Y, Ohno Y, Funatsu Y, Arai S, Kamei H, Mizoguchi H, Nagai T, Koike K, Inoue M, Yamada K. 2007. 17Beta-estradiol attenuates hippocampal neuronal loss and cognitive dysfunction induced by chronic restraint stress in ovariectomized rats. Neuroscience 146: 60-68.
60. Tanapat P, Hastings NB, Gould E. 2005. Ovarian steroids influence cell proliferation in the dentate gyrus of the adult female rat in a dose- and time-dependent manner. J Comp Neurol 481: 252-65.
61. Toran-Allerand CD. 2005. Estrogen and the brain. Beyond ER-α, ER-β and 17β-estradiol. Ann N Y Acad Sci 1052: 136-144.
62. Walf AA, Frye CA. 2009. Effects of two estradiol regimens on anxiety and depressive behaviors and trophic effects in peripheral tissues in a rodent model. Gen Med 6: 300-311.
63. Weiland NG, Orikasa C, Hayashi S, McEwen BS. 1997. Distribution and hormone regulation of estrogen receptor immunoreactive cells in the hippocampus of male and female rats. J Comp Neurol 388: 603-612.
64. Willard SL, Friedman DP, Henkel CK, Shively CA. 2009. Anterior hippocampal volume is reduced in behaviorally depressed female cynomolgus macaques. Psychoneuroendocrinology 34: 1469-1475.
65. Woolley CS. 1998. Estrogen-mediated structural and functional synaptic plasticity in the female rat hippocampus. Horm Behav 34: 140-148.
66. Young KA, Holcomb LA, Yazdani U, Hicks PB, German DC. 2004. Elevated neuron number in the limbic thalamus in major depression. Am J Psychiatry 161: 1270-1277.
67. Zhao H, Tian Z, Hao J, Chen B. 2005. Extragonadal aromatization increases with time after ovariectomy in rats. Reprod Biol Endocrinol 3: 6.
68. 2+/calmodulin-dependent protein kinase IV in amygdala. Neuroreport 12: 2987-2990.
69. Zhou J, Pandey SC, Cohen RS. 2004. Estrogen decreases levels of calcineurin in rat amygdala and hippocampus. Neuroreport 15: 2437-2440.
70. Zhou J, Zhang H, Cohen RS, Pandey SC. 2005. Effects of estrogen treatment on expression of brain-derived neurotrophic factor and cAMP response element-binding protein expression and phosphorylation in rat amygdaloid and hippocampal structures. Neuroendocrinology 81: 294-310.
71. Zhou Y, Watters J, Dorsa D. 1996. Estrogen rapidly induces the phosphorylation of the cAMP response element binding protein in rat brain. Endocrinology 137: 2163-2166.