The ability of oestradiol administration to regulate protein levels of oestrogen receptor alpha in the hippocampus and prefrontal cortex of middle-aged rats is altered following long-term ovarian hormone deprivation

Journal of Neuroendocrinology

Volumn 21, Issue 7, 2009, Pages 640-647

  Bohacek, J ^a   Daniel, Jill M ^a  

^a TULANE UNIVERSITY   (United States)

Author keywords

Oestradiol; Oestrogen receptor; Oestrogens; Ovariectomy; SRC 1

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; STEROID RECEPTOR COACTIVATOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITION; CONTROLLED STUDY; DRUG CAPSULE; DRUG EFFICACY; DRUG IMPLANTATION; ELECTROPHORESIS; FEMALE; HELA CELL; HIPPOCAMPUS; HORMONAL REGULATION; HORMONE SUBSTITUTION; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; LONG EVANS RAT; NONHUMAN; OVARIECTOMY; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RAT; SHAM PROCEDURE; UTERUS WEIGHT; WEIGHT REDUCTION; WESTERN BLOTTING;

AGING; ANIMALS; BLOTTING, WESTERN; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTROGENS; FEMALE; HIPPOCAMPUS; HISTONE ACETYLTRANSFERASES; OVARIECTOMY; PREFRONTAL CORTEX; RATS; RATS, LONG-EVANS; TIME FACTORS; TRANSCRIPTION FACTORS;

EID: 67149101022     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2009.01882.x     Document Type: Article

References (44)

1. Sherwin BB. Estrogen and cognitive aging in women. Trends Pharmacol Sci 2002; 23: 527-534.
2. Espeland MA, Rapp SR, Shumaker SA, Brunner R, Manson JE, Sherwin BB, Hsia J, Margolis KL, Hogan PE, Wallace R, Dailey M, Freeman R, Hays J. Conjugated equine estrogens and global cognitive function in postmenopausal women: Women's Health Initiative Memory Study. J Am Med Assoc 2004; 291: 2959-2968.
3. Shumaker SA, Legault C, Kuller L, Rapp SR, Thal L, Lane DS, Fillit H, Stefanick ML, Hendrix SL, Lewis CE, Masaki K, Coker LH, for the Women's Health Initiative Memory Study. Conjugated equine estrogens and incidence of probable dementia and mild cognitive impairment in postmenopausal women: Women's Health Initiative Memory Study. JAMA 2004; 291: 2947-2958.
4. Resnick SM, Henderson VW. Hormone therapy and risk of Alzheimer disease: a critical time. JAMA 2002; 288: 2170-2172.
5. Sherwin BB. The critical period hypothesis: Can it explain discrepancies in the oestrogen-cognition literature? J Neuroendocrinol 2007; 19: 77-81.
6. Zandi PP, Carlson MC, Plassman BL, Welsh-Bohmer KA, Mayer LS, Steffens DC, Breitner JC. Hormone replacement therapy and incidence of Alzheimer disease in older women: The Cache County Study. JAMA 2002; 288: 2123-2129.
7. MacLennan AHM, Henderson VWM, Paine BJB, Mathias JP, Ramsay ENB, Ryan PMBBF, Stocks NPM, Taylor AWM. Hormone therapy, timing of initiation, and cognition in women aged older than 60years: The REMEMBER pilot study. Menopause 2006; 13: 28-36.
8. Dumas J, Hancur-Bucci C, Naylor M, Sites C, Newhouse P. Estradiol interacts with the cholinergic system to affect verbal memory in postmenopausal women: Evidence for the critical period hypothesis. Horm Behav 2008; 53: 159-169.
9. Henderson VW, Benke KS, Green RC, Cupples LA, Farrer LA. Postmenopausal hormone therapy and Alzheimer's disease risk: Interaction with age. J Neurol Neurosurg Psychiatry 2005; 76: 103-105.
10. Talboom JS, Williams BJ, Baxley ER, West SG, Bimonte-Nelson HA. Higher levels of estradiol replacement correlate with better spatial memory in surgically menopausal young and middle-aged rats. Neurobiol Learn Mem 2008; 90: 155-163.
11. Gibbs RB. Long-term treatment with estrogen and progesterone enhances acquisition of a spatial memory task by ovariectomized aged rats. Neurobiol Aging 2000; 21: 107-116.
12. Daniel JM, Hulst JL, Berbling JL. Estradiol replacement enhances working memory in middle-aged rats when initiated immediately after ovariectomy but not after a long-term period of ovarian hormone deprivation. Endocrinology 2006; 147: 607-614.
13. Gibbs RB, Aggarwal P. Estrogen and basal forebrain cholinergic neurons: implications for brain aging and Alzheimer's disease-related cognitive decline. Horm Behav 1998; 34: 98-111.
14. Spencer JL, Waters EM, Romeo RD, Wood GE, Milner TA, McEwen BS. Uncovering the mechanisms of estrogen effects on hippocampal function. Front Neuroendocrinol 2008; 29: 219-237.
15. Rudick CN, Gibbs RB, Woolley CS. A role for the basal forebrain cholinergic system in estrogen-induced disinhibition of hippocampal pyramidal cells. J Neurosci 2003; 23: 4479-4490.
16. Lam TT, Leranth C. Role of the medial septum diagonal band of Broca cholinergic neurons in oestrogen-induced spine synapse formation on hippocampal CA1 pyramidal cells of female rats. Eur J Neurosci 2003; 17: 1997-2005.
17. Daniel JM, Dohanich GP. Acetylcholine mediates the estrogen-induced increase in NMDA receptor binding in CA1 of the hippocampus and the associated improvement in working memory. J Neurosci 2001; 21: 6949-6956.
18. Daniel JM, Hulst JL, Lee CD. Role of hippocampal M2 muscarinic receptors in the estrogen-induced enhancement of working memory. Neuroscience 2005; 132: 57-64.
19. Bohacek J, Bearl AM, Daniel JM. Long-term ovarian hormone deprivation alters the ability of subsequent oestradiol replacement to regulate choline acetyltransferase protein levels in the hippocampus and prefrontal cortex of middle-aged rats. J Neuroendocrinol 2008; 20: 1023-1027.
20. McEwen BS, Alves SE. Estrogen actions in the central nervous system. Endocr Rev 1999; 20: 279-307.
21. Spencer TE, Jenster G, Burcin MM, Allis CD, Zhou J, Mizzen CA, McKenna NJ, Onate SA, Tsai SY, Tsai MJ, O'Malley BW. Steroid receptor coactivator-1 is a histone acetyltransferase. Nature 1997; 389: 194-198.
22. Jezierski MK, Sohrabji F. Neurotrophin expression in the reproductively senescent forebrain is refractory to estrogen stimulation. Neurobiol Aging 2001; 22: 311-321.
23. Gallagher M, Rapp PR. The use of animal models to study the effects of aging on cognition. Annu Rev Psychol 1997; 48: 339-370.
24. Dohanich GP. Gonadal steroids, learning and memory. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, eds. Hormones, Brain and Behavior. San Diego, CA: Academic Press, 2002: 265-327.
25. Keenan PA, Ezzat WH, Ginsburg K, Moore GJ. Prefrontal cortex as the site of estrogen's effect on cognition. Psychoneuroendocrinology 2001; 26: 577-590.
26. Miller NR, Jover T, Cohen HW, Zukin RS, Etgen AM. Estrogen can act via estrogen receptor alpha and beta to protect hippocampal neurons against global ischemia-induced cell death. Endocrinology 2005; 146: 3070-3079.
27. Jin M, Jin F, Zhang L, Chen Z, Huang H. Two estrogen replacement therapies differentially regulate expression of estrogen receptors alpha and beta in the hippocampus and cortex of ovariectomized rat. Brain Res Mol Brain Res 2005; 142: 107-114.
28. Maffucci JA, Gore AC. Age-related changes in hormones and their receptors in animal models of female reproductive senescence. In: Conn PM, ed. Handbood of models for human aging. New York, NY: Elsevier, 2006: 533-552.
29. Morrison JH, Brinton RD, Schmidt PJ, Gore AC. Estrogen, menopause, and the aging brain: How basic neuroscience can inform hormone therapy in women. J Neurosci 2006; 26: 10332-10348.
30. Bohacek J, Daniel JM. Increased daily handling of ovariectomized rats enhances performance on a radial-maze task and obscures effects of estradiol replacement. Horm Behav 2007; 52: 237-243.
31. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. San Diego, CA: Academic, 1998.
32. Song RX, Barnes CJ, Zhang Z, Bao Y, Kumar R, Santen RJ. The role of Shc and insulin-like growth factor 1 receptor in mediating the translocation of estrogen receptor α to the plasma membrane. Proc Natl Acad Sci USA 2004; 101: 2076-2081.
33. Scott MB, Xiaolan M, Hoa HL. Blockade of estrogen receptor signaling inhibits growth and migration of medulloblastoma. Endocrinology 2009; 150: 1112-1121.
34. Macbeth AH, Scharfman HE, MacLusky NJ, Gautreaux C, Luine VN. Effects of multiparity on recognition memory, monoaminergic neurotransmitters, and brain-derived neurotrophic factor (BDNF). Horm Behav 2008; 54: 7-17.
35. Frick KM. Estrogens and age-related memory decline in rodents: What have we learned and where do we go from here? Horm Behav 2009; 55: 2-23.
36. Frye CA, Duffy CK, Walf AA. Estrogens and progestins enhance spatial learning of intact and ovariectomized rats in the object placement task. Neurobiol Learn Mem 2007; 88: 208-216.
37. Fugger HN, Foster TC, Gustafsson J, Rissman EF. Novel effects of estradiol and estrogen receptor alpha and beta on cognitive function. Brain Res 2000; 883: 258-264.
38. Foster TC, Rani A, Kumar A, Cui L, Semple-Rowland SL. Viral vector-mediated delivery of estrogen receptor-alpha to the hippocampus improves spatial learning in estrogen receptor-alpha knockout mice. Mol Ther 2008; 16: 1587-1593.
39. Adams MM, Fink SE, Shah RA, Janssen WG, Hayashi S, Milner TA, McEwen BS, Morrison JH. Estrogen and aging affect the subcellular distribution of estrogen receptor-alpha in the hippocampus of female rats. J Neurosci 2002; 22: 3608-3614.
40. Adams MM, Shah RA, Janssen WGM, Morrison JH. Different modes of hippocampal plasticity in response to estrogen in young and aged female rats. PNAS 2001; 98: 8071-8076.
41. McLaughlin KJ, Bimonte-Nelson H, Neisewander JL, Conrad CD. 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 2008; 54: 386-395.
42. Gibbs RB. Expression of estrogen receptor-like immunoreactivity by different subgroups of basal forebrain cholinergic neurons in gonadectomized male and female rats. Brain Res 1996; 720: 61-68.
43. Towart LA, Alves SE, Znamensky V, Hayashi S, McEwen BS, Milner TA. Subcellular relationships between cholinergic terminals and estrogen receptor-alpha in the dorsal hippocampus. J Comp Neurol 2003; 463: 390-401.
44. Bake S, Ma L, Sohrabji F. Estrogen receptor-alpha overexpression suppresses 17beta-estradiol-mediated vascular endothelial growth factor expression and activation of survival kinases. Endocrinology 2008; 149: 3881-3889.