Astrocyte-derived transforming growth factor-β mediates the neuroprotective effects of 17β-estradiol: Involvement of nonclassical genomic signaling pathways

Endocrinology

Volumn 146, Issue 6, 2005, Pages 2749-2759

  Dhandapani, Krishnan M ^a   Wade, F Marlene ^a   Mahesh, Virendra B ^a   Brann, Darrell W ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAMPTOTHECIN; ESTRADIOL; ESTROGEN RECEPTOR; FULVESTRANT; NEUROTROPIC AGENT; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B BETA; SELECTIVE ESTROGEN RECEPTOR MODULATOR; TAMOXIFEN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; CELL DEATH; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVATION; ENZYME INHIBITION; GENE EXPRESSION; GENOME; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ASTROCYTES; CELL LINE; CEREBRAL CORTEX; ESTRADIOL; GENE EXPRESSION; NEUROPROTECTIVE AGENTS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ESTROGEN; SELECTIVE ESTROGEN RECEPTOR MODULATORS; SIGNAL TRANSDUCTION; TAMOXIFEN; TRANSFORMING GROWTH FACTOR BETA;

EID: 18844376360     PISSN: 00137227     EISSN: None     Source Type: Journal    
DOI: 10.1210/en.2005-0014     Document Type: Article

References (65)

1. McEwen B 2002 Estrogen actions throughout the brain. Recent Prog Horm Res 57:357-384
2. McEwen B, Akama K, Alves S, Brake WG, Bulloch K, Lee S, Li C, Yuen G, Milner TA 2001 Tracking the estrogen receptor in neurons: implications for estrogen-induced synapse formation. Proc Natl Acad Sci USA 98:7093-7100
3. Wise PM, Dubal DB, Wilson ME, Rau SW, Bottner M 2002 Minireview: neuroprotective effects of estrogen: new insights into mechanisms of action. Endocrinology 142:969-973
4. Murphy S, McCullough L, Littleton-Kearney M, Hurn P 2003 Estrogen and selective estrogen receptor modulators: neuroprotection in the Women's Health Initiative era. Endocrine 21:17-26
5. Lonard DM, Smith CL 2002 Molecular perspectives on selective estrogen receptor modulators (SERMs): progress in understanding their tissue-specific agonist and antagonist actions. Steroids 67:15-24
6. Mehta S, Dhandapani KM, DeSevilla LM, Webb RC, Mahesh VB, Brann DW 2003 Tamoxifen, a selective estrogen receptor modulator, reduces ischemic damage caused by middle cerebral artery occlusion in the ovariectomized female rat. Neuroendocrinology 77:44-50
7. Mickley KR, Dluzen DE 2004 Dose-response effects of estrogen and tamoxifen upon methamphetamine-induced behavior responses and neurotoxicity of the nigrostriatal dopaminergic system in female mice. Neuroendocrinology 79:305-316
8. Kimelberg HK, Feustel PJ, Jin Y, Paquette J, Boulos A, Keller Jr RW, Tranmer BI 2000 Acute treatment with tamoxifen reduces ischemic damage following middle cerebral artery occlusion. Neuroreport 11:2675-2679
9. Silva I, Mello LE, Freymuller E, Haidar MA, Baracat EC 2000 Estrogen, progestogen, and tamoxifen increase synaptic density of the hippocampus of ovariectomized rats. Neurosci Lett 291:183-186
10. McMillan PL, LeMaster AM, Dorsa DM 2002 Tamoxifen enhances choline acetyltransferase mRNA expression in rat basal forebrain cholinergic neurons. Brain Res Mol Brain Res 103:140-145
11. Cyr M, Thibault C, Morissette M, Landry M, Di Paolo T 2001 Estrogen-like activity of tamoxifen and raloxifene on NMDA receptor binding and expression of its subunits in rat brain. Neuropsychopharmacology 25:242-257
12. Cyr M, Morissette M, Landry M, Di Paolo T 2001 Estrogenic activity of tamoxifen and raloxifene on rat brain AMPA receptors. Neuroreport 12:535-539
13. Wilson ME, Mook D, Graves F, Felger J, Bielsky IF, Wallen K 2003 Tamoxifen is an estrogen antagonist on gonadotropin secretion and responsiveness of the hypothalamic-pituitary-adrenal axis in female monkeys. Endocrine 22:305-315
14. Sanchez-Criado JE, Guelmes P, Bellido C, Gonzalez M, Hernandez G, Aguilar R, Garrido-Gracia JC, Bellow AR, Alonso R 2002 Tamoxifen but not other selective estrogen receptor modulators antagonizes estrogen actions on luteinizing hormone secretion while inducing gonadotropin-releasing hormone self-priming in the rat. Neuroendocrinology 76:203-213
15. Honda K, Shimohama S, Sawada H, Kihara T, Nakamizo T, Shibasaki H, Akaike A 2001 Nongenomic antiapoptotic signal transduction by estrogen in cultured cortical neurons. J Neurosci Res 64:466-475
16. Honda K, Sawada H, Kihara T, Urushitani M, Nakamizo T, Akaike A, Shimohama S 2000 Phosphatidylinositol-3-kinase mediates neuroprotection by estrogen in cultured cortical neurons. J Neurosci Res 60:321-327
17. Singer CA, Figueroa-Masot XA, Batchelor RH, Dorsa DM 1999 The mitogenactivated protein kinase pathway mediates estrogen neuroprotection after glutamate toxicity in primary cortical neurons. J Neurosci 19:2455-2463
18. Singer CA, Rogers KL, Strickland TM, Dorsa DM 1996 Estrogen protects primary cortical neurons from glutamate toxicity. Neurosci Lett 212:13-16
19. Bae YH, Hwang JY, Kim YH, Koh JY 2000 Anti-oxidant neuroprotection by estrogens in mouse cortical cultures. J Korean Med Sci 15:327-336
20. Moosmann B, Behl C 1999 The antioxidant neuroprotective effects of estrogens and phenolic compounds are independent from their estrogenic properties. Proc Natl Acad Sci USA 96:8867-8872
21. Regan RF, Guo Y 1997 Estrogens attenuate neuronal injury due to hemoglobin, chemical hypoxia, and excitatory amino acids in murine cortical cultures. Brain Res 764:133-140
22. Dhandapani KM, Brann DW 2003 Neuroprotective effects of estrogen and tamoxifen in vitro: a facilitative role for glia? Endocrine 21:59-66
23. Dhandapani KM, Brann DW 2002 Protective effects of estrogen and SERMs in the brain. Biol Reprod 67:1379-1385
24. 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. Mol Pharmacol 51:535-541
25. Wilson ME, Liu Y, Wise PM 2002 Estradiol enhances Akt activation in cortical explant cultures following neuronal injury. Brain Res Mol Brain Res 102:48-54
26. Wilson ME, Dubal DB, Wise PM 2000 Estradiol protects against injury-induced cell death in cortical explant cultures: a role for estrogen receptors. Brain Res 873:235-242
27. Sortino MA, Chisari M, Merlo S, Vancheri C, Caruso M, Nicoletti F, Canonico PL, Copani A 2004 Glia mediate the neuroprotective action of estradiol on β-amyloid-induced neuronal death. Endocrinology 145:5080-5086
28. Azcoitia I, Sierra A, Garcia-Segura LM 1999 Localization of estrogen receptor β-immunoreacrivity in astrocytes of the adult rat brain. Glia 26:260-267
29. Dhandapani KM, Wade FM, Mahesh VB, Brann DW 2002 Basic fibroblast growth factor induces TGF-β release in an isoform and glioma-specific manner. Neuroreport 13:239-241
30. McCarthy KD, de Vellis J 1979 The regulation of adenosine 3′:5′-cyclic monophosphate accumulation in glia by α-adrenergic agonists. Life Sci 24:639-649
31. Buchanan CD, Mahesh VB, Brann DW 2000 Estrogen-astrocyte-luteinizing hormone-releasing hormone signaling: a role for transforming growth factor-β1. Biol Reprod 62:1710-1721
32. Dalby B, Cateo S, Harris A, Ohki EC, Tilkins ML, Price PJ, Ciccarone VC 2004 Advanced transfection with Lipofectamine 2000 reagent: primary neurons, SiRNA, and high-throughput applications. Methods 33:95-103
33. Simpkins JW, Rajakumar G, Zhang YQ, Simpkins CE, Grenwald D, Yu CJ, Bodor N, Day AL 1997 Estrogens may reduce mortality and ischemic damage caused by middle cerebral artery occlusion in the female rat. J Neurosurg 87:724-730
34. Rusa R, Alkayed NJ, Crain BJ, Traystman RJ, Kimes AS, London ED, Klaus JA, Hurn PD 1999 17β-Estradiol reduces stroke injury in estrogen-deficient female animals. Stroke 30:1665-1670
35. Dubal DB, Kashon ML, Pettigrew LC, Ren JM, Finklestein SP, Rau SW, Wise PM 1998 Estradiol protects against ischemic injury. J Cereb Blood Flow Metab 18:1253-1258
36. Alkayed NJ, Murphy SJ, Traystman RJ, Hum PD, Miller VM 2000 Neuroprotective effects of female gonadal steroids in reproductively senescent female rats. Stroke 31:161-168
37. Dubal DB, Wise PM 2001 Neuroprotective effects of estradiol in middle-aged female rats. Endocrinology 142:43-48
38. Cholerton B, Gleason CE, Baker LD, Asthana S 2002 Estrogen and Alzheimer's disease: the story so far. Drugs Aging 19:405-427
39. Chaban VV, Lakhter AJ, Micevych P 2004 A membrane estrogen receptor mediates intracellular calcium release in astrocytes. Endocrinology 145:3788-3795
40. Lu YP, Zeng M, Hu XY, Xu H, Swaab DF, Ravid R, Zhou JN 2003 Estrogen receptor α-immunoreactive astrocytes are increased in the hippocampus in Alzheimer's disease. Exp Neurol 183:482-488
41. Garcia-Ovejero D, Veiga S, Garcia-Segura LM, Doncarlos LL 2002 Glial expression of estrogen and androgen receptors after rat brain injury. J Comp Neurol 450:256-271
42. Blurton-Jones M, Tuszynski MH 2001 Reactive astrocytes express estrogen receptors in the injured primate brain. J Comp Neurol 433:115-123
43. Zhang JQ, Cai WQ, Zhou de S, Su BY 2002 Distribution and differences of estrogen receptor β immunoreactiviry in the brain of adult male and female rats. Brain Res 935:73-80
44. Deitch HR, Mershon JL, Clark KE 2001 Estrogen receptor β is the predominant isoform expressed in the brain of adult and fetal sheep. Am J Obstet Gynecol 184:1077-1079
45. Shughrue PJ, Lane MV, Merchenthaler I 1997 Comparative distribution of estrogen receptor-α and -β mRNA in the rat central nervous system. J Comp Neurol 388:507-525
46. Dhandapani KM, Brann DW 2002 Estrogen-astrocyte interactions: implications for neuroprotection. BMC Neurosci 3:6
47. Zwain IH, Arroyo A, Amato P, Yen SS 2002 A role for hypothalamic astrocytes in dehydroepiandrosterone and estradiol regulation of gonadotropin-releasing hormone (GnRH) release by GnRH neurons. Neuroendocrinology 75:375-383
48. Dhandapani KM, Hadman M, De Sevilla LM, Wade MF, Mahesh VB, Brann DW 2003 Astrocyte protection of neurons: role of TGF-β signaling via a c-Jun-AP-1 protective pathway. J Biol Chem 278:43329-43339
49. Dhandapani KM, Brann DW 2003 TGF-β: a neuroprotective factor in cerebral ischemia. Cell Biochem Biophys 39:13-22
50. Ruocco A, Nicole O, Docagne F, Ali C, Chazalviel L, Komesli S, Yablonsky F, Roussel S, MacKenzie ET, Vivien D, Buisson A 1999 A transforming growth factor-β antagonist unmasks the neuroprotective role of this endogenous cytokine in excitotoxic and ischemic brain injury. J Cereb Blood Flow Metab 19:1345-1353
51. Bruno V, Battaglia G, Casabona G, Copani A, Caciagli F, Nicoletti F 1998 Neuroprotection by glial metabotropic glutamate receptors is mediated by transforming factor-β. J Neurosci 38:9594-9600
52. D'Onofrio M, Cuomo L, Battaglia G, Ngomba RT, Storto M, Kingston AE, Orzi F, De Blasi A, Di Iorio P, Nicoletti F, Bruno V 2001 Neuroprotection mediated by glial group-II metabotropic glutamate receptors requires the activation of the MAP kinase and the phosphatidylinositol-3-kinase pathways. J Neurochem 78:435-445
53. Docagne F, Nicole O, Gabriel C, Fernandez-Monreal M, Lesne S, Ali C, Plawinski L, Carmeliet P, MacKenzie ET, Buisson A, Vivien D 2002 Smad3-dependent induction of plasminogen activator inhibitor-1 in astrocytes mediates neuroprotective activity of transforming growth factor-β1 against NMDA-induced necrosis. Mol Cell Neurosci 21:634-644
54. Gabriel C, Ali C, Lesne S, Fernandez-Monreal M, Docagne F, Plawinski L, MacKenzie ET, Buisson A, Vivien D 2003 Transforming growth factor α-induced expression of type 1 plasminogen activator inhibitor in astrocytes rescues neurons from excitotoxicity. FASEB J 17:277-279
55. Treichel JA, Reddington M, Kreutzberg GW 1998 Regulation of plasminogen activator inhibitor-1 mRNA accumulation by basic fibroblast growth factor and transforming growth factor-β1 in cultured rat astrocytes. J Neurochem 71:1944-1952
56. Lesne S, Blanchet S, Docagne F, Liot G, Plawinski L, MacKenzie ET, Auffray C, Buisson A, Pietu G, Vivien D 2002 Transforming growth factor-β1-modulated cerebral gene expression. J Cereb Blood Flow Metab 22:1114-1123
57. Sohrabji F, Miranda RC, Toran-Allerand CD 1995 Identification of a putative estrogen response element in the gene encoding brain-derived neurotrophic factor. Proc Natl Acad Sci USA 92:11110-11114
58. Solum DJ, Handa RJ 2002 Estrogen regulates the development of brain-derived neurotrophic factor mRNA and protein in the rat hippocampus. J Neurosci 22:2650-2659
59. Zafra F, Lindholm D, Castren E, Hartikka J, Thoenen H 1992 Regulation of brain-derived neurotrophic factor and nerve growth factor mRNA in primary cultures of hippocampal neurons and astrocytes. J Neurosci 12:4793-4799
60. Abraham IM, Han SK, 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
61. 2+, ErbB3, and phosphoinositide 3-kinase in 1321N1 astrocytoma cells. J Biol Chem 277:338-344
62. Carswell HW, Macrae IN, Gallagher L, Harrop E, Horsburgh KJ 2004 Neuroprotecrion by a selective oestrogen receptor b agonist in a mouse model of global ischemia. Am J Physiol 287:H1501-H1504
63. Wassertheil-Smoller S, Hendriz SL, Limacher M, Heiss G, Kooperberg C, Baird A, Kotchen T, Curb JD, Black H, Rossouw JE, Aragaki A, Safford M, Stein E, Laowattana S, Mysiw WJ, WHI Investigators 2003 Effect of estrogen plus progestin on stroke in postmenopausal women: the Women's Health Initiative: a randomized trial. J Am Med Assoc 289:2673-2684
64. Anderson GL, Limacher M, Assaf AR, Bassford T, Beresfold SA, Black H, Bonds D, Brunner R, Brzyski R, Caan B, Chlebowski R, Curb D, Gass M, Hays J, Heiss G, Hendrix S, Howard BV, Hsia J, Hubbell A, Jackson R, Johnson KC, Judd H, Kotchen JM, Kuller L, LaCroix AZ, Lane D, Langer RD, Lasser N, Lewis CE, Manson J, Margolis K, Ockene J, O'Sullivan MJ, Phillips L, Prentice RL, Ritenbaugh C, Robbins J, Rossouw JE, Sarto G, Stefanick ML, Van Horn L, Wactawski-Wende J, Wallace R, Wassertheil-Smoller S, Women Health Initiative Steering Committee 2004 Effects of conjugated equine estrogen in postmenopausal women with hysterectomy: the Women's Health Initiative randomized controlled trial. J Am Med Assoc 291:1701-1712
65. Rossberg MI, Murphy SJ, Traystman RJ, Hum PD 2000 LY353381.HCl, a selective estrogen receptor modulator, and experimental stroke. Stroke 31:3041-3046