Estrogen receptor α and β differentially regulate intracellular Ca2+ dynamics leading to ERK phosphorylation and estrogen neuroprotection in hippocampal neurons

Brain Research

Volumn 1172, Issue 1, 2007, Pages 48-59

  Zhao, Liqin ^a   Brinton, Roberta Diaz ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

17 estradiol; DPN; Estrogen receptor; Hippocampal neuron; ICI 182,780; PPT

Indexed keywords

1,3,5 TRIS(4 HYDROXYPHENYL) 4 PROPYL 1H PYRAZOLE; 2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2,3 BIS(4 HYDROXYPHENYL)PROPIONITRILE; CALCIUM; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GLUTAMIC ACID; HORMONE RECEPTOR STIMULATING AGENT; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN BCL 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CELL FUNCTION; CONTROLLED STUDY; DRUG ANTAGONISM; DRUG EFFICACY; DRUG MECHANISM; EMBRYO; ENZYME PHOSPHORYLATION; EXCITOTOXICITY; HIPPOCAMPUS; MOLECULAR DYNAMICS; NERVE CELL; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM; CALCIUM CHANNEL BLOCKERS; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; EMBRYO, MAMMALIAN; ENZYME INHIBITORS; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTROGENS; GLUTAMIC ACID; HIPPOCAMPUS; MITOGEN-ACTIVATED PROTEIN KINASE 1; NEURONS; NIFEDIPINE; PHENOLS; PHOSPHORYLATION; PYRAZOLES; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

EID: 34548681666     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2007.06.092     Document Type: Article

References (50)

1. Baldereschi M., Di Carlo A., Lepore V., Bracco L., Maggi S., Grigoletto F., Scarlato G., and Amaducci L. Estrogen-replacement therapy and Alzheimer's disease in the Italian Longitudinal Study on Aging. Neurology 50 (1998) 996-1002
2. Behl C., Skutella T., Lezoualc'h F., Post A., Widmann M., Newton C.J., and Holsboer F. Neuroprotection against oxidative stress by estrogens: structure-activity relationship. Mol. Pharmacol. 51 (1997) 535-541
3. 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
4. Brinton R.D. Estrogen therapy for prevention of Alzheimer's disease not for rehabilitation following onset of disease: the healthy cell bias of estrogen action. In: Baudry M., Bi R., and Schreiber S.S. (Eds). Synaptic Plasticity: Basic Mechanisms to Clinical Applications (2004), Taylor and Francis Group, New York 131-157
5. Brinton R.D. Impact of estrogen therapy on Alzheimer's disease: a fork in the road?. CNS Drugs 18 (2004) 405-422
6. Cordey M., and Pike C.J. Neuroprotective properties of selective estrogen receptor agonists in cultured neurons. Brain Res. 1045 (2005) 217-223
7. Dauvois S., White R., and Parker M.G. The antiestrogen ICI 182780 disrupts estrogen receptor nucleocytoplasmic shuttling. J. Cell Sci. 106 (1993) 1377-1388
8. Espeland M.A., Rapp S.R., Shumaker S.A., Brunner R., Manson J.E., Sherwin B.B., Hsia J., Margolis K.L., Hogan P.E., Wallace R., Dailey M., Freeman R., and Hays J. Conjugated equine estrogens and global cognitive function in postmenopausal women: Women's Health Initiative Memory Study. JAMA 291 (2004) 2959-2968
9. Fawell S.E., White R., Hoare S., Sydenham M., Page M., and Parker M.G. Inhibition of estrogen receptor-DNA binding by the "pure" antiestrogen ICI 164,384 appears to be mediated by impaired receptor dimerization. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 6883-6887
10. Foster T.C., and Kumar A. Calcium dysregulation in the aging brain. Neuroscientist 8 (2002) 297-301
11. Grady D., Yaffe K., Kristof M., Lin F., Richards C., and Barrett-Connor E. Effect of postmenopausal hormone therapy on cognitive function: the Heart and Estrogen/progestin Replacement Study. Am. J. Med. 113 (2002) 543-548
12. Green P.S., and Simpkins J.W. Estrogens and estrogen-like non-feminizing compounds. Their role in the prevention and treatment of Alzheimer's disease. Ann. N. Y. Acad. Sci. 924 (2000) 93-98
13. Green P.S., Gordon K., and Simpkins J.W. Phenolic A ring requirement for the neuroprotective effects of steroids. J. Steroid Biochem. Mol. Biol. 63 (1997) 229-235
14. Gustafsson J.A. What pharmacologists can learn from recent advances in estrogen signaling. Trends Pharmacol. Sci. 24 (2003) 479-485
15. Henderson V.W., Paganini-Hill A., Miller B.L., Elble R.J., Reyes P.F., Shoupe D., McCleary C.A., Klein R.A., Hake A.M., and Farlow M.R. Estrogen for Alzheimer's disease in women: randomized, double-blind, placebo-controlled trial. Neurology 54 (2000) 295-301
16. Jacobs D.M., Tang M.X., Stern Y., Sano M., Marder K., Bell K.L., Schofield P., Dooneief G., Gurland B., and Mayeux R. Cognitive function in nondemented older women who took estrogen after menopause. Neurology 50 (1998) 368-373
17. Kumar V., and Chambon P. The estrogen receptor binds tightly to its responsive element as a ligand-induced homodimer. Cell 55 (1988) 145-156
18. LaFerla F.M. Calcium dyshomeostasis and intracellular signalling in Alzheimer's disease. Nat. Rev., Neurosci. 3 (2002) 862-872
19. 2+ channel activity in brain aging and dementia. Hormonal and pharmacologic modulation. Ann. N. Y. Acad. Sci. 747 (1994) 351-364
20. Mannella P., and Brinton R.D. Estrogen receptor protein interaction with phosphatidylinositol 3-kinase leads to activation of phosphorylated Akt and extracellular signal-regulated kinase 1/2 in the same population of cortical neurons: a unified mechanism of estrogen action. J. Neurosci. 26 (2006) 9439-9447
21. Matthews K., Cauley J., Yaffe K., and Zmuda J.M. Estrogen replacement therapy and cognitive decline in older community women. J. Am. Geriatr. Soc. 47 (1999) 518-523
22. 2+ homeostasis in Alzheimer's disease. Trends Neurosci. 16 (1993) 409-414
23. Mattson M.P., LaFerla F.M., Chan S.L., Leissring M.A., Shepel P.N., and Geiger J.D. Calcium signaling in the ER: its role in neuronal plasticity and neurodegenerative disorders. Trends Neurosci. 23 (2000) 222-229
24. Meyers M.J., Sun J., Carlson K.E., Marriner G.A., Katzenellenbogen B.S., and Katzenellenbogen J.A. Estrogen receptor-beta potency-selective ligands: structure-activity relationship studies of diarylpropionitriles and their acetylene and polar analogues. J. Med. Chem. 44 (2001) 4230-4251
25. Mulnard R.A., Cotman C.W., Kawas C., van Dyck C.H., Sano M., Doody R., Koss E., Pfeiffer E., Jin S., Gamst A., Grundman M., Thomas R., and Thal L.J. Estrogen replacement therapy for treatment of mild to moderate Alzheimer disease: a randomized controlled trial. Alzheimer's Disease Cooperative Study. JAMA 283 (2000) 1007-1015
26. Nilsen J., and Brinton R.D. Mechanism of estrogen-mediated neuroprotection: regulation of mitochondrial calcium and Bcl-2 expression. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 2842-2847
27. Nilsen J., and Brinton R.D. Mechanism of estrogen-mediated neuroprotection: regulation of mitochondrial calcium and Bcl-2 expression. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 2842-2847
28. Nilsen J., and Brinton R.D. Mitochondria as therapeutic targets of estrogen action in the central nervous system. Curr. Drug Targets CNS Neurol. Disord. 3 (2004) 297-313
29. Nilsen J., Chen S., and Brinton R.D. Dual action of estrogen on glutamate-induced calcium signaling: mechanisms requiring interaction between estrogen receptors and src/mitogen activated protein kinase pathway. Brain Res. 930 (2002) 216-234
30. Rapp S.R., Espeland M.A., Shumaker S.A., Henderson V.W., Brunner R.L., Manson J.E., Gass M.L., Stefanick M.L., Lane D.S., Hays J., Johnson K.C., Coker L.H., Dailey M., and Bowen D. Effect of estrogen plus progestin on global cognitive function in postmenopausal women: the Women's Health Initiative Memory Study: a randomized controlled trial. JAMA 289 (2003) 2663-2672
31. Rissman E.F., Heck A.L., Leonard J.E., Shupnik M.A., and Gustafsson J.A. Disruption of estrogen receptor beta gene impairs spatial learning in female mice. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 3996-4001
32. Shumaker S.A., Legault C., Rapp S.R., Thal L., Wallace R.B., Ockene J.K., Hendrix S.L., Jones B.N., Assaf A.R., Jackson R.D., Kotchen J.M., Wassertheil-Smoller S., and Wactawski-Wende J. Estrogen plus progestin and the incidence of dementia and mild cognitive impairment in postmenopausal women: the Women's Health Initiative Memory Study: a randomized controlled trial. JAMA 289 (2003) 2651-2662
33. Shumaker S.A., Legault C., Kuller L.H., Rapp S.R., Thal L., Lane D.S., Fillit H., Stefanick M.L., Hendrix S.L., Lewis C.E., Masaki K., and Coker L.H. Conjugated equine estrogens and incidence of probable dementia and mild cognitive impairment in postmenopausal women: Women's Health Initiative Memory Study. JAMA 291 (2004) 2947-2958
34. Stauffer S.R., Coletta C.J., Tedesco R., Nishiguchi G., Carlson K., Sun J., Katzenellenbogen B.S., and Katzenellenbogen J.A. Pyrazole ligands: structure-affinity/activity relationships and estrogen receptor-alpha-selective agonists. J. Med. Chem. 43 (2000) 4934-4947
35. Steffens D.C., Norton M.C., Plassman B.L., Tschanz J.T., Wyse B.W., Welsh-Bohmer K.A., Anthony J.C., and Breitner J.C. Enhanced cognitive performance with estrogen use in nondemented community-dwelling older women. J. Am. Geriatr. Soc. 47 (1999) 1171-1175
36. Thibault O., Porter N.M., Chen K.C., Blalock E.M., Kaminker P.G., Clodfelter G.V., Brewer L.D., and Landfield P.W. Calcium dysregulation in neuronal aging and Alzheimer's disease: history and new directions. Cell Calcium 24 (1998) 417-433
37. Tora L., White J., Brou C., Tasset D., Webster N., Scheer E., and Chambon P. The human estrogen receptor has two independent nonacidic transcriptional activation functions. Cell 59 (1989) 477-487
38. Wang P.N., Liao S.Q., Liu R.S., Liu C.Y., Chao H.T., Lu S.R., Yu H.Y., Wang S.J., and Liu H.C. Effects of estrogen on cognition, mood, and cerebral blood flow in AD: a controlled study. Neurology 54 (2000) 2061-2066
39. Wang L., Andersson S., Warner M., and Gustafsson J.A. Morphological abnormalities in the brains of estrogen receptor beta knockout mice. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 2792-2796
40. Wang L., Andersson S., Warner M., and Gustafsson J.A. Estrogen receptor (ER)beta knockout mice reveal a role for ERbeta in migration of cortical neurons in the developing brain. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 703-708
41. Waring S.C., Rocca W.A., Petersen R.C., O'Brien P.C., Tangalos E.G., and Kokmen E. Postmenopausal estrogen replacement therapy and risk of AD: a population-based study. Neurology 52 (1999) 965-970
42. West A.E., Chen W.G., Dalva M.B., Dolmetsch R.E., Kornhauser J.M., Shaywitz A.J., Takasu M.A., Tao X., and Greenberg M.E. Calcium regulation of neuronal gene expression. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 11024-11031
43. White R.J., and Reynolds I.J. Mitochondrial depolarization in glutamate-stimulated neurons: an early signal specific to excitotoxin exposure. J. Neurosci. 16 (1996) 5688-5697
44. Woolley C.S., and McEwen B.S. Estradiol regulates hippocampal dendritic spine density via an N-methyl-d-aspartate receptor-dependent mechanism. J. Neurosci. 14 (1994) 7680-7687
45. 2+ influx via L-type calcium channels activates the Src/ERK/cyclic-AMP response element binding protein signal pathway and BCL-2 expression in rat hippocampal neurons: a potential initiation mechanism for estrogen-induced neuroprotection. Neuroscience 135 (2005) 59-72
46. Zandi P.P., Carlson M.C., Plassman B.L., Welsh-Bohmer K.A., Mayer L.S., Steffens D.C., and Breitner J.C. Hormone replacement therapy and incidence of Alzheimer disease in older women: the Cache County Study. JAMA 288 (2002) 2123-2129
47. Zhao L., Wu T.-W., and Brinton R.D. Estrogen receptor subtypes alpha and beta contribute to neuroprotection and increased Bcl-2 expression in primary hippocampal neurons. Brain Res. 1010 (2004) 22-34
48. 2+ rise and subsequent cyclic AMP response element-binding protein activation in hippocampal neurons: a potential initiation mechanism for estrogen neurotrophism. Neuroscience 132 (2005) 299-311
49. Zhao L., O'Neill K., and Brinton R.D. Selective estrogen receptor modulators (SERMs) for the brain: current status and remaining challenges for developing NeuroSERMs. Brain Res. Brain Res. Rev. 49 (2005) 472-493
50. Zhao L., O'Neill K., and Brinton R.D. Estrogenic agonist activity of ICI 182,780 (Faslodex) in hippocampal neurons: implications for basic science understanding of estrogen signaling and development of estrogen modulators with a dual therapeutic profile. J. Pharmacol. Exp. Ther. 319 (2006) 1124-1132