Estrogen receptor alpha mediates neuronal differentiation and neuroprotection in PC12 cells: Critical role of the A/B domain of the receptor

Journal of Molecular Endocrinology

Volumn 35, Issue 2, 2005, Pages 257-267

  Mérot, Yohann ^b   Ferrière, François ^b   Debroas, Edith ^a   Flouriot, Gilles ^b   Duval, Dominique ^a   Saligaut, Christian ^b  

^a UNIVERSITÉ DE CAEN   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA; GLUTATHIONE; NERVE GROWTH FACTOR;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL STRAIN; CONTROLLED STUDY; GENE ACTIVATION; GENE TARGETING; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PHEOCHROMOCYTOMA CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; RAT; REPORTER GENE;

ANIMALS; BUTHIONINE SULFOXIMINE; CELL DIFFERENTIATION; ENZYME INHIBITORS; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; GENE EXPRESSION REGULATION; GENES, REPORTER; HUMANS; NEURONS; NEUROPROTECTIVE AGENTS; PC12 CELLS; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; RATS; TRANSCRIPTION, GENETIC;

EID: 27644508001     PISSN: 09525041     EISSN: None     Source Type: Journal    
DOI: 10.1677/jme.1.01826     Document Type: Article

References (59)

1. Abraham IM, Todman MG, Korach KS & Herbison AE 2004 Critical in vivo roles for classical estrogen receptors in rapid estrogen actions on intracellular signaling in mouse brain. Endocrinology 145 3055-3061.
2. Beato M 1989 Gene regulation by steroid hormones. Cell 56 335-344.
3. Behl C 2002 Oestrogen as a neuroprotective hormone. Nature Reviews Neuroscience 3 433-442.
4. Behl C, Skutella T, Lezoualc'h F, Post A, Widmann M, Newton CJ & Holsboer F 1997 Neuroprotection against oxidative stress by estrogens: structure-activity relationship. Molecular Pharmacology 51 535-541.
5. Berry M, Metzger D & Chambon P 1990 Role of the two activating domains of the estrogen receptor in the cell-type and promoter-context dependent agonistic activity of the anti-estrogen 4-hydroxytamoxifen. EMBO Journal 9 2811-2818.
6. Couse JF, Curtis SW, Washburn TF, Lindzey J, Golding TS, Lubahn D, Smithies O & Korach KS 1995 Analysis of transcription and estrogen insensitivity in the female mouse after targeted disruption of the estrogen receptor gene. Molecular Endocrinology 9 1441-1454.
7. Dominguez R, Jalali C & De Lacalle S. 2004 Morphological effects of estrogen on cholinergic neurons in vitro involves activation of extracellular signal-regulated kinases. Journal of Neuroscience 24 982-990.
8. Dubal DB, Shughrue PJ, Wilson ME, Merchenthaler I & Wise PM 1999 Estradiol modulates bcl-2 in cerebral ischemia: a potential role for estrogen receptors. Journal of Neuroscience 19 6385-6393.
9. Dubal DB, Zhu H, Yu J, Rau SW, Shughrue PJ, Merchenthaler I, Kindy MS & Wise PM 2001 Estrogen receptor alpha, not beta, is a critical link in estradiol-mediated protection against brain injury. PNAS 98 1952-1957.
10. Edwards DP 2005 Regulation of signal transduction pathway by estrogen and progesterone. Annual Review of Physiology 67 335-376.
11. Evans RM 1988 The steroid and thyroid hormone receptor superfamily. Science 240 889-895.
12. Ferreira A & Caceres A 1991 Estrogen-enhanced neurite growth: evidence for a selective induction of Tau and stable microtubules. Journal of Neuroscience 11 392-400.
13. Figtree GA, McDonald D, Watkins H & Channon KM 2002 Truncated estrogen receptor α 46-kDa isoform in human endothelial cells; relation to acute activation of nitric oxide synthase. Circulation 107 120-126.
14. Fitzpatrick JL, Mize AL, Wade CB, Harris JA, Shapiro RA & Dorsa DM 2002 Estrogen-mediated neuroprotection against β-amyloid toxicity requires expression of estrogen receptor α or β and activation of the MAPK pathway. Journal of Neurochemistry 82 674-682.
15. Flouriot G, Brand H, Denger S, Métivier R, Kos M, Reid G, Sonntag-Buck V & Gannon F 2000 Identification of a new isoform of the human estrogen receptor-alpha (hER-α) that is encoded by distinct transcripts and that is able to repress hER-α activation function 1. EMBO Journal 19 4688-4700.
16. Froissard P, Monrocq H & Duval D 1997 Glutamate-induced programmed cell death in neuronal-like PC12 cells is mediated through an inhibition of glutathione metabolism. European Journal of Pharmacology 326 93-99.
17. Fujita T, Kobayashi Y, Wada O, Tateishi Y, Kitada L, Yamamoto Y, Takashima H, Murayama A, Yano T, Baba T, Kawabe Y & Yanagisawa J 2003 Full activation of estrogen receptor alpha activation function-1 induces proliferation of breast cancer cells. Journal of Biological Chemistry 278 26704-26714.
18. Gerlach JL, McEwen BS, Toran-Allerand CD & Friedman WJ 1983 Perinatal development of estrogen receptors in mouse brain assessed by radioautography, nuclear isolation and receptor assay. Brain Research 313 7-18.
19. Gollapudi L & Oblinger MM 1999a Stable transfection of PC12 cells with estrogen receptor (ERα): protective effects of estrogen on cell survival after serum deprivation. Journal of Neuroscience Research 56 99-108.
20. Gollapudi L & Oblinger MM 1999b Estrogen and NGF synergistically protect terminally differentiated, ERα-transfected PC12 cells from apoptosis. Journal of Neuroscience Research 56 471-481.
21. Gollapudi L & Oblinger MM 2001 Estrogen effects on neurite outgrowth and cytoskeletal gene expression in ERα-transfected PC12 cell lines. Experimental Neurology 171 308-316.
22. Green PS, Gridley KE & Simpkins JW 1998 Nuclear estrogen receptor-independent neuroprotection by estratrienes: a novel interaction with glutathione. Neuroscience 84 7-10.
23. Green S, Kumar V, Theulaz I, Wahli W & Chambon P 1988 The N-terminal DNA-binding 'zinc finger' of the estrogen and glucocorticoid receptors determines target gene specificity. EMBO Journal 7 3037-3044.
24. Griffith OW & Meister A 1979a Potent and specific inhibition of glutathione synthesis by buthionine sulfoximine (S-n-butylhomocysteine sulfoximine). Journal of Biological Chemistry 254 7558-7560.
25. Griffith OW & Meister A 1979b Glutathione: interorgan translocation, turnover, and metabolism. PNAS 76 5606-5610.
26. Higuchi Y & Matsukawa S 1999 Glutathione depletion induces giant DNA and high-molecular-weight DNA fragmentation associated with apoptosis through lipid peroxidation and protein kinase C activation in C6 glioma cells. Archives of Biochemistry and Biophysics 363 33-42.
27. Ho KJ & Liao JK 2002 Non-nuclear actions of estrogen: new targets for prevention and treatment of cardiovascular disease. Molecular Interventions 2 219-228.
28. Kousteni S, Bellido T, Plotkin LI, O'Brien CA, Bodenner DL, Han L, Han K, DiGregorio GB, Katzenellenbogen JA, Katzenellenbogen BS, Roberson PK, Weinstein RS, Jilka RL & Manolagas SC 2001 Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity. Cell 104 719-730.
29. Kuroki Y, Fukushima K, Kanda Y, Mizuno K & Watanabe Y 2001 Neuroprotection by estrogen via extracellular signal-regulated kinase against quinolinic acid-induced cell death in the rat hippocampus. European Journal of Neuroscience 13 472-476.
30. Le Foll I & Duval D 2001 Programmed cell death induced by glutathione depletion in PC12 cells is blocked by inhibitors of 12 lipoxygenase, but does not appear to be mediated through the formation of 12 HETE derivatives. Free Radical Biology and Medicine 30 793-802.
31. Leon A, Le Foll I, Charriault-Marlangue C, Leprince J, Vaudry H, Gabriel C & Duval D 2003 The level of heme oxygenase does not obligatorily reflect the sensitivity of PC12 cells to an oxidative shock induced by glutathione depletion. Journal of Neurochemistry 84 459-470.
32. McEwen BS 2002 Estrogen actions throughout the brain. Recent Progress in Hormone Research 57 357-384.
33. Maggi A, Ciana P, Belcredito S & Vegeto E 2004 Estrogens in the nervous system: mechanisms and nonreproductive functions. Annual Review of Physiology 66 291-313.
34. Mérot Y, Métivier R, Penot G, Mann D, Saligaut C, Gannon F, Pakdel F, Kah O & Flouriot G 2004 The relative contribution exerted by AF-1 and AF-2 transactivation functions in estrogen receptor alpha (ERα) transcriptional activity depends upon the differentiation stage of the cell. Journal of Biological Chemishy 279 26184-26191.
35. Métivier R, Penot G, Flouriot G & Pakdel F 2001 Synergism between ERalpha transactivation function 1 (AF-1) and AF-2 mediated by steroid receptor coactivator protein-1: requirement for the AF-1 alpha-helical core and for a direct interaction between the N- and C-terminal domains. Molecular Endocrinology 15 1953-1970.
36. Migliaccio A, Piccolo D, Castoria G, Di Domenico M, Bilancio A, Lombardi M, Gong W, Beato M & Auricchio F 1998 Activation of the Src/p21 ras/Erk pathway by progesterone receptor via cross-talk with estrogen receptor. EMBO Journal 17 2008-2018.
37. Mize AL, Shapiro RA & Dorsa DM 2003 Estrogen receptor-mediated neuroprotection from oxidative stress requires activation of the mitogen-activated protein kinase pathway. Endocrinology 144 306-312.
38. Nethrapalli IS, Singh M, Guan X, Guo Q, Lubahn DB, Korach KS & Toran-Allerand CD 2001 Estradiol (E2) elicits SRC phosphorylation in the mouse neocortex: the initial event in E2 activation of the MAPK cascade? Endocrinology 142 5145-5148.
39. Norris JD, Fan D, Kerner SA & McDonnell DP 1997 Identification of a third autonomous activation domain within the human estrogen receptor. Molecular Endocrinology 11 747-754.
40. Parker MG 1995 Structure and function of estrogen receptors. Vitamins and Hormones 51 267-287.
41. Pendaries C, Darblade B, Rochaix P, Krust A, Chambon P, Korach KS, Bayard F & Arnal JF 2002 The AF-1 activation-function of ERalpha may be dispensable to mediate the effects of estradiol on endothelial NO production in mice. PNAS 99 2205-2210.
42. Pike CJ 1999 Estrogen modulates neuronal Bcl-xL expression and beta-amyloid-induced apoptosis: relevance to Alzheimer's disease. Journal of Neurochemistry 72 1552-1563.
43. Sawada H, Ibi M, Kihara T, Urushitani M, Honda K, Nakanishi M, Akaike A & Shimohama S 2000 Mechanisms of antiapoptotic effects of estrogens in nigral dopaminergic neurons. FASEB Journal 14 1202-1214.
44. Serghini R, Froissard P, Sola B & Duval D 1994 Cycloheximide and actinomycin D block the toxic effect of glutamic acid on PC12 cells. Neuroreport 6 29-32.
45. Shughrue PJ & Dorsa DM 1993 Estrogen modulates the growth-associated protein GAP-43 (neuromodulin) mRNA in the rat preoptic area and basal hypothalamus. Neuroendocrinology 57 439-447.
46. Singer CA, Figueroa-Masot XA, Batchelor RH & Dorsa DM 1999 The mitogen-activated protein kinase pathway mediates estrogen neuroprotection after glutamate toxicity in primary cortical neurons. Journal of Neuroscience 19 2455-2463.
47. Sohrabji F, Greene LA, Miranda RC & Toran-Allerand CD 1994 Reciprocal regulation of estrogen and NGF receptors by their ligands in PC12 cells. Journal of Neurobiology 25 974-988.
48. Sohrabji F, Miranda RC & Toran-Allerand CD 1995 Identification of a putative estrogen response element in the gene encoding brain-derived neurotrophic factor. PNAS 92 11110-11114.
49. Sugioka K, Shimosegawa Y & Nakano M 1987 Estrogens as natural antioxidants of membrane phospholipid peroxidation. FEBS Letters 210 37-39.
50. Tietze F 1969 Enzymatic method for quantitative determination of total and oxidized glutathione. Analytical Biochemistry 27 507-522.
51. Toran-Allerand CD 1996 Mechanisms of estrogen action during neural development: mediation by interactions with the neurotrophins and their receptors? Journal of Steroid Biochemistry and Molecular Biology 56 169-178.
52. Toran-Allerand CD 2004 A plethora of estrogen receptors in the brain: where will it end? Endocrinology 145 1069-1074.
53. Toran-Allerand CD, Singh M & Setalo G Jr 1999 Novel mechanisms of estrogen action in the brain: new players in an old story. Frontiers in Neuroendocrinology 20 97-121.
54. Vasudevan N, Kow LM & Pfaff DW 2001 Early membrane estrogenic effects required for full expression of slower genomic actions in a nerve cell line. PNAS 98 12267-12271.
55. Wilson ME, Dubai DB & Wise PM 2000 Estradiol protects against injury-induced cell death in cortical explant cultures: a role for estrogen receptors. Brain Research 873 235-242.
56. Wise PM 2003 Estrogens: protective or risk factors in brain function? Progress in Neurobiology 69 181-191.
57. Wise PM, Dubai DB, Wilson ME, Rau SW & Liu Y 2001 Estrogens: trophic and protective factors in the adult brain. Frontiers in Neuroendocrinology 22 33-66.
58. Zhang L, Rubinow DR, Xaing G, Li BS, Chang YH, Maric D, Barker JL & Ma W 2001 Estrogen protects against beta-amyloid-induced neurotoxicity in rat hippocampal neurons by activation of Akt. Neuroreport 12 1919-1923.
59. Zhao L, Wu TW & Brinton RD 2004 Estrogen receptor subtypes alpha and beta contribute to neuroprotection and increased Bcl-2 expression in primary hippocampal neurons. Brain Research 1010 22-34.