β-Estradiol influences differentiation of hippocampal neurons in vitro through an estrogen receptor-mediated process

Neuroscience

Volumn 121, Issue 4, 2003, Pages 927-934

  Audesirk, T ^a   Cabell, L ^a   Kern, M ^a   Audesirk, G ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Raloxifene; Selective estrogen receptor modulators; SERMS

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FULVESTRANT; RALOXIFENE; SELECTIVE ESTROGEN RECEPTOR MODULATOR;

AGING; ANIMAL CELL; ARTICLE; BRAIN DEVELOPMENT; COGNITION; CONTROLLED STUDY; DENDRITE; DRUG EFFECT; DRUG RECEPTOR BINDING; EMBRYO; FEMALE; HIPPOCAMPUS; IN VITRO STUDY; LEARNING; MEMORY; NERVE CELL DIFFERENTIATION; NERVE CELL GROWTH; NERVE CELL PLASTICITY; NERVE FIBER; NEURITE; NONHUMAN; PRIORITY JOURNAL; RAT; SEX DIFFERENCE; WESTERN BLOTTING;

EID: 0142216502     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(03)00294-X     Document Type: Article

References (68)

1. Audesirk T., Audesirk G., Ferguson C., Shugarts D. Effects of inorganic lead on the differentiation and growth of cultured hippocampal and neuroblastoma cells. Neurotoxicology. 12:1991;519-528.
2. Audesirk G., Cabell L., Kern M. Modulation of neurite branching by protein phosphorylation in cultured hippocampal neurons. Dev Brain Res. 102:1997;247-260.
3. Barkhem T., Carlsson B., Nilsson Y., Enmark E., Gustafsson J.- A.̊, Nilsson S. Differential response of estrogen receptor α and estrogen receptor β to partial estrogen agonists/antagonists. Am Soc Pharm Exp Ther. 54:1998;105-112.
4. Barrett-Connor E., Cox D.A., Anderson P.W. The potential of SERMs for reducing the risk of coronary heart disease. Trends Endocrinol Metab. 10:1999;320-325.
5. Behl C., Manthey D. Neuroprotective activities of estrogen an update . J Neurocytol. 29:2000;351-358.
6. Beyer C. Estrogen and the developing brain. Anat Embryol. 199:1999;379-390.
7. Beyer C., Ivanova T., Karolczak M., Küppers E. Cell type-specificity of nonclassical estrogen signaling in the developing midbrain. J Steroid Biochem Mol Biol. 81:2002;319-325.
8. Beyer C., Karolczak M. Estrogenic stimulation of neurite growth in midbrain dopaminergic neurons depends on cAMP/protein kinase A signaling. J Neurosci. 59:2000;107-116.
9. Beyer C., Raab H. Nongenomic effects of oestrogen embryonic mouse midbrain neurones respond with a rapid release of calcium from intracellular stores . Eur J Neurosci. 10:1998;255-262.
10. Blanco G., Diaz H., Carrer H.F., Beauge L. Differentiation of rat hippocampal neurons induced by estrogen in vitro effects on neuritogenesis and Na, K-ATPase activity . J Neurosci Res. 27:1990;47-54.
11. Brinton R.D. Cellular and molecular mechanisms of estrogen regulation of memory function and neuroprotection against Alzheimer's disease recent insights and remaining challenges . Learn Mem. 8:2001;121-133.
12. Brinton R.D., Tran J., Proffitt P., Montoya M. 17 β-Estradiol enhances the outgrowth and survival of neocortical neurons in culture. Neurochem Res. 22:1997;1339-1351.
13. Brubaker K.D., Gay C.V. Evidence for plasma membrane-mediated effects of estrogen. Calcif Tissue Int. 64:1999;459-462.
14. Cambiasso M.J., Carrer H.F. Nongenomic mechanism mediates estradiol stimulation of axon growth in male rat hypothalamic neurons in vitro. J Neurosci Res. 66:2001;475-481.
15. Clarke C.H., Norfleet A.M., Clarke M.S., Watson C.S., Cunningham K.A., Thomas M.L. Perimembrane localization of the estrogen receptor alpha protein in neuronal processes of cultured hippocampal neurons. Neuroendocrinology. 71:2000;34-42.
16. Cordoba Montoya D.A., Carrer H.F. Estrogen facilitates induction of long term potentiation in the hippocampus of awake rats. Brain Res. 778:1997;430-438.
17. Cosman F., Lindsay R. Selective estrogen receptor modulators clinical spectrum . Endocrinol Rev. 20:1999;418-434.
18. Enmark E., Gustafsson J.A. Oestrogen receptors an overview . J Intern Med. 246:1999;133-138.
19. Ferreira A., Caceres A. Estrogen-enhanced neurite growth evidence for a selective induction of tau and stable microtubules . J Neurosci. 11:1991;392-400.
20. Filit H.M. The role of hormone replacement therapy in the prevention of Alzheimer's disease. Arch Int Med. 162:2002;1934-1942.
21. Garcia-Segura L.M., Azcoitia I., DonCarlos L.L. Neuroprotection by estradiol. Prog Neurobiol. 63:2001;29-60.
22. Gibbs R.B., Aggarwal P. Estrogen and basal forebrain cholinergic neurons implications for brain aging and Alzheimer's disease-related cognitive decline . Horm Behav. 34:1998;98-111.
23. Henderson V.W., Watt L., Buckwalter J.G. Cognitive skills associated with estrogen replacement in women with Alzheimer's disease. Psychoneuroendocrinology. 21:1996;421-430.
24. Hosli E., Hosli L. Cellular localization of estrogen receptors on neurones in various regions of cultured rat CNS coexistence with cholinergic and galanin receptors . Int J Dev Neurosci. 17:1999;317-330.
25. Hubert J.F., Vincent A., Labrie F. Estrogenic activity of phenol red in rat anterior pituitary cells in culture. Biochem Biophys Res Commun. 141:1986;885-891.
26. Jacobs D.M., Tang M.X., Stern Y., Sano M., Marder K., Bell K.L., Schofield P., Dooneief G., Gurland B., Mayeux R. Cognitive function in nondemented older women who took estrogen after menopause. Neurology. 50:1998;368-373.
27. Jordan V.C. Antiestrogenic action of raloxifene and tamoxifen today and tomorrow . J Nat Cancer Inst. 90:1998;967-971.
28. Kamden D.L., Sherwin B.B. Estrogen use and verbal memory in healthy menopausal women. Obstet Gynecol. 83:1994;979-983.
29. Kern M., Audesirk G. Inorganic lead may inhibit neurite development in hippocampal neurons through hyperphosphorylation. Toxicol Appl Pharmacol. 134:1995;111-123.
30. Levin E.R. Cellular functions of the plasma membrane estrogen receptor. T. E. M. 10:1999;374-377.
31. Lorenzo A., Diaz H., Carrer H., Caceres A. Amygdala neurons in vitro neurite growth and effects of estradiol . J Neurosci Res. 33:1992;418-435.
32. Lustig R.H., Hua P., Yu W., Ahmad F.J., Baas P.W. An in vitro model for the effects of estrogen on neurons employing estrogen receptor-transfected PC12 cells. J Neurosci. 14:1994;3945-3957.
33. Manly J.J., Merchant C.A., Jacobs D.M., Small S.A., Bell K., Ferin M., Mayeux R. Endogenous estrogen levels and Alzheimer's disease among postmenopausal women. Neurology. 54:2000;833-837.
34. Mattson M.P., Kater S.B. Isolated hippocampal neurons in cryopreserved long-term cultures development of neuroarchitecture and sensitivity to NMDA . Int J Dev Neurosci. 6:1988;439-452.
35. McDonnell D.P. The molecular pharmacology of SERMs. Trends Endocrinol Metab. 10:1999;301-311.
36. McEwen B.S. Estrogen actions throughout the brain. Recent Prog Horm Res. 57:2002;357-384.
37. McEwen B.S., Alves S.E. Estrogen actions in the central nervous system. Endocr Rev. 20:1999;279-307.
38. McEwen B.S., Tanapat P., Weiland N.G. Inhibition of dendritic spine induction on hippocampal CA1 pyramidal neurons by a nonsteroidal estrogen antagonist in female rats. Endocrinol. 140:1999;1044-1047.
39. Moore F.L., Evans S.J. Steroid hormones use non-genomic mechanisms to control brain functions and behaviors a review of evidence . Brain Behav Evol. 54:1999;41-50.
40. Murphy D.D., Andrews B. Culture models for the study of estradiol-induced synaptic plasticity. J Neurocytol. 29:2000;411-417.
41. Murphy D.D., Segal M. Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones. J Neurosci. 16:1996;4059-4068.
42. Nilsen J., Mor G., Naftolin F. Raloxifene induces neurite outgrowth in estrogen receptor positive PC12 cells. Menopause. 5:1998;211-216.
43. Nickelsen T., Lufkin E.G., Riggs B.L., Cox D.A., Crook T.H. Raloxifene hydrochloride, a selective estrogen receptor modulator safety assessment of effects on cognitive function and mood in postmenopausal women . Psychoneuroendocrinology. 24:1999;115-128.
44. Patrone C., Pollio G., Vegeto E., Enmar E., deCurtis I., Gufstafsson J.-A., Maggi A. Estradiol induces differential neuronal phenotypes by activating estrogen receptor α or β Endocrinol. 141:2000;1839-1845.
45. Phillips S.M., Sherwin B.B. Effects of estrogen on memory function in surgically menopausal women. Psychoneuroendocrinology. 17:1992;485-495.
46. 2+ transients in spines of CA1 pyramidal neurons from hippocampal slices. J Neurophysiol. 81:1999;1404-1411.
47. Robinson D., Friedman L., Marcus R., Tinklenberg J., Yesavage J. Estrogen replacement therapy and memory in older women. J Am Geriatr Soc. 42:1994;919-922.
48. Resnick S.M., Maki P.M., Golski S., Kraut M.A., Zonderman A.B. Effects of estrogen replacement therapy on PET cerebral blood flow and neuropsychological performance. Horm Behav. 34:1998;171-182.
49. Russell K.S., Haynes M.P., Sinha D., Clerisme E., Bender J.R. Human vascular endothelial cells contain membrane binding sites for estradiol, which mediate rapid intracellular signaling. Proc Natl Acad Sci USA. 97:2000;5930-5935.
50. Schmidt B.M.W., Gerdes D., Feuring M., Falkenstein E., Christ M., Wehling M. Rapid, nongenomic steroid actions a new age? Front Neuroendocrinol. 21:2000;57-94.
51. Sherwin B.B. Can estrogen keep you smart? evidence from clinical studies. J Psychiatry Neurosci. 24:1999;315-321.
52. Skoog I., Gustafson D. HRT and dementia. J Epidemiol Biostat. 4:1999;227-251.
53. Slooter A.J., Bronzova J., Witteman J.C., Van Broeckhoven C., Hofman A., van Duijn C.M. Estrogen use and early onset Alzheimer's disease a population-based study . J Neurol Neurosurg Psychiatry. 67:1999;779-781.
54. Su J.-D., Qiu J., Zhong Y.-P., Li X.-Y., Wang J.-W., Chen Y.-Z. Expression of estrogen receptor (ER)-α and -β immunoreactivity in hippocampal cell cultures with special attention to GABAergic neurons. J Neurosci Res. 65:2001;396-402.
55. Toran-Allerand C.D., Singh M., Setalo G. Jr. Novel mechanisms of estrogen action in the brain new players in an old story . Front Neuroendocrinol. 20:1999;97-121.
56. Waring S.C., Rocca W.A., Petersen R.C., O'Brien P.C., Tangalos E.G., Kokmen E. Postmenopausal estrogen replacement therapy and risk of AD a population-based study . Neurology. 52:1999;965-970.
57. Warren S.G., Humphreys A.G., Juraska J.M., Greenough W.T. LTP varies across the estrous cycle enhanced synaptic plasticity in proestrus rats . Brain Res. 703:1995;26-30.
58. Wijayaratne A.L., McDonnell D.P. The estrogen receptor-alpha is a ubiquinated protein whose stability is affected differentially by agonists, antagonists and selective estrogen receptor modulators. J Biol Chem. 276:2001;35684-35692.
59. Wise P.M., Dubal D.B., Wilson M.E., Rau S.W., Böttner M. Minireview neuroprotective effects of estrogen: new insights into mechanisms of action . Endocrinology. 142:2001;969-973.
60. Wise P.M., Dubal D.B., Wilson M.E., Rau S.W., Ying L. Estrogens trophic and protective factors in the adult brain . Front Neuroendocrinol. 22:2001;33-66.
61. Woolley C.S. Effects of estrogen in the CNS. Curr Opin Neurobiol. 9:1999;349-354.
62. Woolley C.S. Electrophysiological and cellular effects of estrogen on neuronal function. Crit Rev Neurobiol. 13:1999;1-20.
63. Woolley C.S., McEwen B.S. Estradiol regulates hippocampal dendritic spine density via an N-methyl-D-aspartate receptor-dependent mechanism. J Neurosci. 14:1994;7680-7687.
64. Woolley C.S., Gould E., Frankfurt M., McEwen B.S. Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci. 12:1990;4035-4039.
65. Wong M., Thompson T.L., Moss R.L. Nongenomic actions of estrogen in the brain physiological significance and cellular mechanisms . Crit Rev Neurobiol. 10:1996;189-203.
66. Wu X., Glinn M.A., Ostrowski N.L., Su Y., Ni B., Cole H.W., Bryant H.U., Paul S.M. Raloxifene and estradiol benzoate both fully restore hippocampal choline acetyltransferase activity in ovariectomized rats. Brain Res. 847:1999;98-104.
67. Yaffe K., Krueger K., Sarkar S., Grady D., Barrett-Connor E., Cox D.A., Nickelsen T. Cognitive function in postmenopausal women treated with raloxifene. N Engl J Med. 344:2001;1207-1213.
68. Zhang L., Chang Y.H., Barker J.L., Hu Q., Zhang L., Maric D., Li B.-S., Rubinow D.R. Testosterone and estrogen affect neuronal differentiation but not proliferation in early embryonic cortex of the rat the possible roles of androgen and estrogen receptors . Neurosci Lett. 281:2000;57-60.