Estrogen receptor-α overexpression suppresses 17β-estradiol- mediated vascular endothelial growth factor expression and activation of survival kinases

Endocrinology

Volumn 149, Issue 8, 2008, Pages 3881-3889

  Bake, Shameena ^a   Ma, Lijiang ^a   Sohrabji, Farida ^a  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOXYCYCLINE; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; PYRAZOLE DERIVATIVE; TRANSCRIPTION FACTOR PITX2; VASCULOTROPIN;

ARTICLE; CELL LINE; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN SYNTHESIS; REGULATORY MECHANISM;

APOPTOSIS REGULATORY PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; DOXYCYCLINE; ENZYME ACTIVATION; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION; GENES, REPORTER; HELA CELLS; HUMANS; ONCOGENE PROTEIN V-AKT; TRANSFECTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 47949123625     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2008-0288     Document Type: Article

References (75)

1. Simpkins JW, Singh M, Bishop J 1994 The potential role for estrogen replacement therapy in the treatment of the cognitive decline and neurodegeneration associated with Alzheimer's disease. Neurobiol Aging 2:S195-S197
2. 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
3. Sitges M, Leivas A, Heras M, Ferrer E, Roque M, Viles D, Roig E, Rivera F, Sanz G 2005 Short-term transdermal estradiol enhances nitric oxide synthase III and estrogen receptor mRNA expression in arteries of women with coronary artery disease. Int J Cardiol 105:74-79
4. Singh M, Meyer EM, Millard WJ, Simpkins JW 1994 Ovarian steroid deprivation results in a reversible learning impairment and compromised cholinergic function in female Sprague-Dawley rats. Brain Res 644:305-312
5. Nelson HD, Rizzo J, Harris E, Cauley J, Ensrud K, Bauer DC, Orwoll E 2002 Osteoporosis and fractures in postmenopausal women using estrogen. Arch Int Med 162:2278-2284
6. Green S, Walter P, Kumar V, Krust A, Bornert JM, Argos P, Chambon P 1986 Human oestrogen receptor cDNA: sequence, expression and homology to v-erb-A. Nature 320:134-139
7. Kuiper GGJM, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, Gustafsson J-A 1997 Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors α and β. Endocrinology 3:863-870
8. Friend KE, Ang LW, Shupnik MA 1995 Estrogen regulates the expression of several different estrogen receptor mRNA isoforms in rat pituitary. Proc Natl Acad Sci USA 92:4367-4371
9. Peng B, Lu B, Leygue E, Murphy LC 2003 Putative functional characteristics of human estrogen receptor-β isoforms. J Mol Endocrinol 30:13-29
10. Sohrabji F, Miranda RC, Toran-Allerand CD 1994 Estrogen differentially regulates estrogen and nerve growth factor receptor mRNAs in adult sensory neurons. J Neurosci 14:459-471
11. Toran-Allerand CD 1984 Gonadal hormones and brain development: implications for the genesis of sexual differentiation. Ann NY Acad Sci 435:101-111
12. Toran-Allerand CD 1980 Sex steroids and the development of the newborn mouse hypothalamus and preoptic area in vitro. II. Morphological correlates and hormonal specificity. Brain Res 189:413-427
13. Lustig RH, Sudol M, Pfaff DW, Federoff HJ 1991 Estrogenic regulation and sex dimorphism of growth-associated protein 43 kDa (GAP-43) messenger RNA in the rat. Brain Res 11:125-132
14. Nishizuka M, Arai Y 1981 Organizational action of estrogen on synaptic pattern in the amygdala: implications for sexual differentiation of the brain. Brain Res 213:422-426
15. Stanley HF, Curtis A, Sheward WJ, Roberts JL, Fink G 1986 Prolactin messenger ribonucleic acid levels in the normal and hypogonadal mouse pituitary gland. Endocrinology 119:2422-2426
16. Singh M, Meyer EM, Simpkins JW 1995 The effect of ovariectomy and estradiol replacement on brain-derived neurotrophic factor messenger ribonucleic acid expression in cortical and hippocampal brain regions of female Sprague-Dawley rats. Endocrinology 136:2320-2324
17. Sohrabji F, Miranda RCG, 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
18. Gibbs RB, Pfaff DW 1992 Effects of estrogen and fimbria/fornix transection on p75NGFR and ChAT expression in the medial septum and diagonal band of Broca. Exp Neurol 116:23-39
19. Lapchak PA, Araujo DM, Quirion R, Beaudet A 1990 Neurotensin regulation of endogenous acetylcholine release from rat cerebral cortex: effect of quinolinic acid lesions of the basal forebrain. J Neurochem 55:1397-1403
20. Luine VN 1985 Estradiol increases choline acetyltransferase activity in specific basal forebrain nuclei and projection areas of female rats. Exp Neurol 89:484-490
21. Frick KM, Fernandez SM, Bulinski SC 2002 Estrogen replacement improves spatial reference memory and increases hippocampal synaptophysin in aged female mice. Neuroscience 115:547-558
22. Daniel JM, Dohanich GP 2001 Acetylcholine mediates the estrogen-induced increase in NMDA receptor binding in CA1 of the hippocampus and the associated improvement in working memory. J Neurosci 21:6949-6956
23. Lacreuse A, Wilson ME, Herndon JG 2002 Estradiol, but not raloxifene, improves aspects of spatial working memory in aged ovariectomized rhesus monkeys. Neurobiol Aging 23:589-600
24. Zhang Y-Q, Shi J, Rajakumar G, Day AL, Simpkins JW 1998 Effects of gender and estradiol treatment on focal brain ischemia. Brain Res 784:321-324
25. Sohrabji F, Peeples KW, Marroquin OA 2000 Local and cortical effects of olfactory bulb lesions on trophic support and cholinergic function and their modulation by estrogen. J Neurobiol 45:61-74
26. Ritz MF, Schmidt P, Mendelowitsch A 2002 17β-Estradiol effect on the extracellular concentration of amino acids in the glutamate excitotoxicity model in the rat. Neurochem Res 27:1677-1683
27. Mendez P, Azcoitia I, Garcia-Segura LM 2005 Interdependence of oestrogen and insulin-like growth factor-I in the brain: potential for analysing neuroprotective mechanisms. J Endocrinol 185:11-17
28. Migliaccio A, Castoria G, Di Domenico M, de Falco A, Bilancio A, Lombardi M, Bottero D, Varricchio L, Nanayakkara M, Rotondi A, Auricchio F 2002 Sex steroid hormones act as growth factors. J Steroid Biochem Mol Biol 83:31-35
29. Gibbs RB 1999 Treatment with estrogen and progesterone affects relative levels of brain-derived neurotrophic factor mRNA and protein in different regions of the adult rat brain. Brain Res 844:20-27
30. Jezierski MK, Sohrabji F 2000 Region- and peptide-specific regulation of the neurotrophins by estrogen. Mol Brain Res 85:77-84
31. Berchtold NC, Kesslak JP, Pike CJ, Adlard PA, Cotman CW 2001 Estrogen and exercise interact to regulate brain-derived neurotrophic factor mRNA and protein expression in the hippocampus. Eur J Neurosci 14:1992-2002
32. Solum DT, Handa RJ 2002 Estrogen regulates the development of brain-derived neurotrophic factor mRNA and protein in the rat hippocampus. Eur J Neurosci 22:2650-2659
33. Jezierski MK, Sohrabji F 2001 Neurotrophin expression in the reproductively senescent forebrain is refractory to estrogen stimulation. Neurobiol Aging 22:311-321
34. Vegeto E, Belcredito S, Etteri S, Ghisletti S, Brusadelli A, Meda C, Krust A, Dupont S, Ciana P, Chambon P, Maggi A 2003 Estrogen receptor-α mediates the brain antiinflammatory activity of estradiol. Proc Natl Acad Sci USA 100:9614-9619
35. Nordell VL, Scarborough MM, Buchanan AK, Sohrabji F 2003 Differential effects of estrogen in the injured forebrain of young adult and reproductive senescent animals. Neurobiol Aging 24:733-743
36. Chakraborty TR, Hof PR, Ng L, Gore AC 2003 Stereologic analysis of estrogen receptor α (ERα) expression in rat hypothalamus and its regulation by aging and estrogen. J Comp Neurol 466:409-421
37. Nordell VL, Lewis DK, Bake S, Sohrabji F 2005 The neurotrophin receptor p75NTR mediates early anti-inflammatory effects of estrogen in the forebrain of young adult rats. BMC Neurosci 6:58
38. Yun H, Lee M, Kim S-S, Ha J 2005 Glucose deprivation increases mRNA stability of vascular endothelial growth factor through activation of AMP-activated protein kinase in DU145 prostate carcinoma. J Biol Chem 280:9963-9972
39. Wei Q, Adelstein RS 2002 Pitx2a expression alters actin-myosin cytoskeleton and migration of HeLa cells through Rho GTPase signaling. Mol Biol Cell 13:683-697
40. Sun J, Huang YR, Harrington WR, Sheng S, Katzenellenbogen JA, Katzenellenbogen BS 2002 Antagonists selective for estrogen receptor α. Endocrinology 143:941-947
41. Sohrabji F 2005 Estrogen: a neuroprotective or proinflammatory hormone? Emerging evidence from reproductive aging models. Ann NY Acad Sci 1052:75-90
42. Sohrabji F, Bake S 2006 Age-related changes in neuroprotection: is estrogen pro-inflammatory for the reproductive senescent brain? Endocrine 29:191-197
43. Ishunina TA, Swaab DF 2003 Increased neuronal metabolic activity and estrogen receptors in the vertical limb of the diagonal band of broca in Alzheimer's disease: relation to sex and aging. Exp Neurol 183:159-172
44. Hestiantoro A, Swaab DF 2004 Changes in estrogen receptor-α and -β in the infundibular nucleus of the human hypothalamus are related to the occurrence of Alzheimer's disease neuropathology. J Clin Endocrinol Metab 89:1912-1925
45. Mahmoodzadeh S, Eder S, Nordmeyer J, Ehler E, Huber O, Martus P, Weiske J, Pregla R, Hetzer R, Regitz-Zagrosek V 2006 Estrogen receptor α up-regulation and redistribution in human heart failure. FASEB J 20:926-934
46. Kalesnykas G, Roschier U, Puolivali J, Wang J, Miettinen R 2005 The effect of aging on the subcellular distribution of estrogen receptor-α in the cholinergic neurons of transgenic and wild-type mice. Eur J Neurosci 21:1437-1442
47. Ankrom MA, Patterson JA, d'Avis PY, Vetter UK, Blackman MR, Sponseller PD, Tayback M, Robey PG, Shapiro JR, Fedarko NS 1998 Age-related changes in human oestrogen receptor α function and levels in osteoblasts. Biochem J 333(Pt 3):787-794
48. Sharma PK, Thakur MK 2004 Estrogen receptor α expression in mice kidney shows sex differences during aging. Biogerontology 5:375-381
49. Maminta ML, Molteni A, Rosen ST 1991 Stable expression of the human estrogen receptor in HeLa cells by infection: effect of estrogen on cell proliferation and c-myc expression. Mol Cell Endocrinol 78:61-69
50. Lazennec G, Katzenellenbogen BS 1999 Expression of human estrogen receptor using an efficient adenoviral gene delivery system is able to restore hormone-dependent features to estrogen receptor-negative breast carcinoma cells. Mol Cell Endocrinol 149:93-105
51. Garcia M, Derocq D, Freiss G, Rochefort H 1992 Activation of estrogen receptor transfected into a receptor-negative breast cancer cell line decreases the metastatic and invasive potential of the cells. Proc Nat Acad Sci USA 89:11538-11542
52. Upla P, Marjomaki V, Kankaanpaa P, Ivaska J, Hyypia T, van der Goot FG, Heino J 2004 Clustering induces a lateral redistribution of α2β1 integrin from membrane rafts to caveolae and subsequent protein kinase C-dependent internalization. Mol Biol Cell 15:625-636
53. Milner TA, McEwen BS, Hayashi S, Li CJ, Reagan LP, Alves SE 2001 Ultrastructural evidence that hippocampal α estrogen receptors are located at extranuclear sites. J Comp Neurol 429:355-371
54. Hyder SM, Nawaz Z, Chiappetta C, Stancel GM 2000 Identification of functional estrogen response elements in the gene coding for the potent angiogenic factor vascular endothelial growth factor. Cancer Res 60:3183-3190
55. Charnock-Jones DS, Sharkey AM, Rajput-Williams J, Burch D, Schofield JP, Fountain SA, Boocock CA, Smith SK 1993 Identification and localization of alternately spliced mRNAs for vascular endothelial growth factor in human uterus and estrogen regulation in endometrial carcinoma cell lines. Biol Reprod 48:1120-1128
56. Shifren JL, Tseng JF, Zaloudek CJ, Ryan IP, Meng YG, Ferrara N, Jaffe RB, Taylor RN 1996 Ovarian steroid regulation of vascular endothelial growth factor in the human endometrium: implications for angiogenesis during the menstrual cycle and in the pathogenesis of endometriosis. J Clin Endocrinol Metab 81:1120-1128
57. Giuliani N, Lunghi P, Morandi F, Colla S, Bonomini S, Hojden M, Rizzoli V, Bonati A 2004 Downmodulation of ERK protein kinase activity inhibits VEGF secretion by human myeloma cells and myeloma-induced angiogenesis. Leukemia 18:628-635
58. Wade CB, Dorsa DM 2003 Estrogen activation of cyclic adenosine 5′-monophosphate response element-mediated transcription requires the extracellularly regulated kinase/mitogen-activated protein kinase pathway. Endocrinology 144:832-838
59. Singh M, Setalo Jr G, Guan X, Warren M, Toran-Allerand CD 1999 Estrogen-induced activation of mitogen-activated protein kinase in cerebral cortical explants: convergence of estrogen and neurotrophin signaling pathways. J Neurosci 19:1179-1188
60. Singh M, Setalo Jr G, Guan X, Frail DE, Toran-Allerand CD 2000 Estrogen-induced activation of the mitogen-activated protein kinase cascade in the cerebral cortex of estrogen receptor-α knock-out mice. J Neurosci 20:1694-1700
61. Pedram A, Razandi M, Levin ER 1998 Extracellular signal-regulated protein kinase/Jun kinase cross-talk underlies vascular endothelial cell growth factor-induced endothelial cell proliferation. J Biol Chem 273:26722-26728
62. Carmeliet P, Lampugnani MG, Moons L, Breviario F, Compernolle V, Bono F, Balconi G, Spagnuolo R, Oostuyse B, Dewerchin M, Zanetti A, Angellilo A, Mattot V, Nuyens D, Lutgens E, Clotman F, de Ruiter MC, Gittenberger-de Groot A, Poelmann R, Lupu F, Herbert JM, Collen D, Dejana E 1999 Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 98:147-157
63. Simoncini T, Mannella P, Fornari L, Caruso A, Varone G, Genazzani AR 2004 Genomic and non-genomic effects of estrogens on endothelial cells. Steroids 69:537-542
64. Bryant DN, Sheldahl LC, Marriott LK, Shapiro RA, Dorsa DM 2006 Multiple pathways transmit neuroprotective effects of gonadal steroids. Endocrine 29:199-207
65. Rosenstein JM, Mani N, Khaibullina A, Krum JM 2003 Neurotrophic effects of vascular endothelial growth factor on organotypic cortical explants and primary cortical neurons. J Neurosci 23:11036-11044
66. Zhao H, Shimohata T, Wang JQ, Sun G, Schaal DW, Sapolsky RM, Steinberg GK 2005 Akt contributes to neuroprotection by hypothermia against cerebral ischemia in rats. J Neurosci 27:9794-9806
67. Frago LM, Paneda C, Argente J, Chowen JA 2005 Growth hormone-releasing peptide-6 increases insulin-like growth factor-I mRNA levels and activates Akt in RCA-6 cells as a model of neuropeptide Y neurones. J Neuroendocrinol 17:701-710
68. Kilic E, Kilic U, Soliz J, Bassetti CL, Gassmann M, Hermann DM 2005 Brain-derived erythropoietin protects from focal cerebral ischemia by dual activation of ERK-1/-2 and Akt pathways. FASEB J 19:2026-2028
69. Jin KL, Mao XO, Greenberg DA 2000 Vascular endothelial growth factor rescues HN33 neural cells from death induced by serum withdrawal. J Mol Neurosci 14:197-203
70. Kanda S, Miyata Y, Kanetake H 2004 Fibroblast growth factor-2-mediated capillary morphogenesis of endothelial cells requires signals via Flt-1/vascular endothelial growth factor receptor-1: possible involvement of c-Akt. J Biol Chem 279:4007-4016
71. Kazi AA, Koos RD 2007 Estrogen-induced activation of hypoxia-inducible factor-1α, vascular endothelial growth factor expression, and edema in the uterus are mediated by the phosphatidylinositol 3-kinase/Akt pathway. Endocrinology 148:2363-2374
72. Chambliss KL, Yuhanna IS, Mineo C, Liu P, German Z, Sherman TS, Mendelsohn ME, Anderson RGW, Shaul PW 2000 Estrogen receptor α and endothelial nitric oxide synthase are organized into a functional signaling module in caveolae. Circulation Res 87:44-52
73. Turi A, Kiss AL, Mullner N 2001 Estrogen down-regulates the number of caveolae and the level of caveolin in uterine smooth muscle. Cell Biol Int 25:785-794
74. Toran-Allerand CD, Guan X, MacLusky NJ, Horvath TL, Diano S, Singh M, Connolly Jr ES, Nethrapalli IS, Tinnikov AA 2002 ER-X: a novel, plasma membrane-associated, putative estrogen receptor that is regulated during development and after ischemic brain injury. J Neurosci 22:8391-8401
75. Boulware MI, Kordasiewicz H, Mermelstein PG 2007 Caveolin proteins are essential for distinct effects of membrane estrogen receptors in neurons. J Neurosci 27:9941-9950