Estrogen receptor alpha and beta are both involved in the cerebral VEGF/Akt/NO pathway and cerebral angiogenesis in female mice

Biomedical Research

Volumn 31, Issue 6, 2010, Pages 337-346

  Jesmin, Subrina ^a,b,d   Mowa, Chishimba N ^c   Sultana, Sayeeda Nusrat ^a,b   Mia, Sohag ^a,b   Islam, Reazul ^a,b   Zaedi, Sohel ^a,b   Sakuma, Ichiro ^d   Hattori, Yuichi ^d   Hiroe, Michiaki ^a,b   Yamaguchi, Naoto ^e  

^a NATIONAL CENTER FOR GLOBAL HEALTH AND MEDICINE   (Japan)

^b INTERNATIONAL CENTRE FOR DIARRHOEAL DISEASE RESEARCH   (Bangladesh)

^c APPALACHIAN STATE UNIVERSITY   (United States)

^d HOKKAIDO UNIVERSITY   (Japan)

^e IBARAKI PREFECTURAL UNIVERSITY OF HEALTH SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FIBROBLAST GROWTH FACTOR 2; NITRIC OXIDE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN KINASE B; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD VESSEL; BRAIN CAPILLARY; BRAIN LEVEL; CAPILLARY DENSITY; CONTROLLED STUDY; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PHOSPHORYLATION; FEMALE; FRONTAL CORTEX; GENE EXPRESSION REGULATION; GENE SILENCING; IMMUNOBLOTTING; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; WILD TYPE;

ANIMALS; BRAIN DISEASES; CAPILLARIES; CEREBRAL CORTEX; DOWN-REGULATION; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTROGENS; FEMALE; INBREEDING; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE SYNTHASE TYPE III; PREFRONTAL CORTEX; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

MUS; RATTUS;

EID: 78650851463     PISSN: 03886107     EISSN: 1880313X     Source Type: Journal    
DOI: 10.2220/biomedres.31.337     Document Type: Article

References (59)

1. Bar J, Tepper R, Fuchs J, Pardo Y, Goldberger S and Ovadia J (1993) The effect of estrogen replacement therapy on platelet aggregation and adenosine triphosphate release in post-menopausal women. Obstet Gynecol 81, 261-264.
2. Beldekas JC, Smith B, Gerstenfeld LC, Sonenshein GE and Franzblau C (1981) Effects of 17 beta-estradiol on the biosynthesis of collagen in cultured bovine aortic smooth muscle cells. Biochemistry 20, 2162-2167.
3. Cai J, Jiang WG, Grant MB and Boulton M (2006) Pigment epithelium-derived factor inhibits angiogenesis via regulated intracellular proteolysis of vascular endothelial growth factor receptor 1. J Biol Chem 281, 3604-3613.
4. Carolei A, Marini C, Ferranti E, Frontoni M, Prencipe M and Fieschi C (1993) A prospective study of cerebral ischemia in the young. Analysis of pathogenic determinants. The National Research Council Study Group. Stroke 24, 362-367.
5. Colditz GA, Willett WC, Stampfer MJ, Rosner B, Speizer FE and Hennekens CH (1987) Menopause and the risk of coronary heart disease in women. N Engl J Med 316, 1105-1110.
6. Croll SD, Ransohoff RM, Cai N, Zhang Q, Martin FJ, Wei T, Kasselman LJ, Kintner J, Murphy AJ, Yancopoulos GD and Wiegand SJ (2004) VEGF-mediated infammation precedes angiogenesis in adult brain. Exp Neurol 187, 388-402.
7. DonCarlos LL, Azcoitia I and Garcia-Segura LM (2009) Neuroprotective actions of selective estrogen receptor modulators. Psychoneuroendocrinology 34, Suppl 1, S113-122.
8. Farr TD, Carswell HV, Gsell W and Macrae IM (2007) Estrogen receptor beta agonist diarylpropiolnitrile (DPN) does not mediate neuroprotection in a rat model of permanent focal ischemia. Brain Res 1185, 275-282.
9. Grandien K (1996) Determination of transcription start sites in the human estrogen receptor gene and identifcation of a novel, tissue-specifc, estrogen receptor mRNA isoform. Mol Cell Endocrinol 116, 207-212.
10. Green PS and Simpkins JW (2000) Neuroprotective effects of estrogens: potential mechanisms of action. Int J Dev Neu-rosci 18, 347-358.
11. Gu JW and Adair TH (1997) Hypoxia-induced expression of VEGF is reversible in myocardial vascular smooth muscle cells. Am J Physiol 273, H628-H633.
12. Guo J, Krause DN, Horne J, Weiss JH, Li X and Duckles SP (2010) Estrogen-receptor-mediated protection of cerebral en-dothelial cell viability and mitochondrial function after isch-emic insult in vitro. J Cereb Blood Flow Metab 3, 545-554.
13. Hammes SR and Levin ER (2007) Extranuclear steroid receptors: nature and actions. Endocr Rev 7, 726-741.
14. Hulley S, Grady D, Bush T, Furberg C, Herrington D, Riggs B, Vittinghoff E and Heart & Estrogen/progestin Replacement Study (HERS) Research Group (1998) Randomized trial of estrogen plus progestin for secondary prevention of coronary heart disease in postmenopausal women. JAMA 280, 605- 613.
15. Jesmin S, Hattori Y, Sakuma I, Liu MY, Mowa CN and Kitabatake A (2003) Estrogen deprivation and replacement modulate cerebral capillary density with vascular expression of angiogenic molecules in middle-aged female rats. J Cereb Blood Flow Metab 23, 181-189.
16. Jesmin S, Sakuma I, Hattori Y and Kitabatake A (2004) Regulatory molecules for coronary expressions of VEGF and its angiogenic receptor KDR in hypoestrogenic middle-aged female rats. Mol Cell Biochem 259, 189-196.
17. Kannel WB, Hjortland MC, McNamara PM and Gordon T (1976) Menopause and risk of cardiovascular disease: the Framingham study. Ann Intern Med 85, 447-452.
18. Kawashima S and Takagi K (1994) Role of sex steroids on the survival, neuritic outgrowth of neurons, and dopamine neurons in cultured preoptic area and hypothalamus. Horm Behav 4, 305-312.
19. Kazi AA, Jones JM and Koos RD (2005) Chromatin immu-noprecipitation analysis of gene expression in the rat uterus in vivo: estrogen-induced recruitment of both estrogen receptor alpha and hypoxia-inducible factor 1 to the vascular en-dothelial growth factor promoter. Mol Endocrinol 19, 2006-2019
20. Kemp K, Hares K, Mallam E, Heesom KJ, Scolding N and Wilkins A (2010) Mesenchymal stem cell-secreted superox-ide dismutase promotes cerebellar neuronal survival. J Neu-rochem 10.1111/j, 1471-159.
21. Kliche S and Waltenberger J (2001) VEGF receptor signaling and endothelial function. IUBMB Life 52, 61-66.
22. Koike S, Sakai M and Muramatsu M (1987) Molecular cloning and characterization of rat estrogen receptor cDNA. Nucleic Acids Res 15, 2499-2513.
23. Krege JH, Hodgin JB, Couse JF, Enmark E, Warner M, Mahler JF, Sar M, Korach KS, Gustafsson JA and Smithies O (1998) Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc Natl Acad Sci USA 95, 15677-15682.
24. Kuiper GG, Carlsson B, Grandien K, Enmark E, Häggblad J, Nilsson S and Gustafsson JA (1997) Comparison of the li-gand binding specifcity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 138, 863- 870.
25. Kuiper GG, Enmark E, Pelto-Huikko M, Nilsson S and Gustafsson JA (1996) Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci USA 93, 5925- 5930.
26. Langer RD, Pradhan AD, Lewis CE, Manson JE, Rossouw JE, Hendrix SL, LaCroix AZ and Ridker PM (2005) Baseline associations between postmenopausal hormone therapy and infammatory, haemostatic, and lipid biomarkers of coronary heart disease. The Women's Health Initiative Observational Study. Thromb Haemost 93, 1108-1116.
27. Lee JE, Chung KW, Han W, Kim SW, Kim SW, Shin HJ, Bae JY and Noh DY (2004) Effect of estrogen, tamoxifen and epidermal growth factor on the transcriptional regulation of vascular endothelial growth factor in breast cancer cells. Anticancer Res 24, 3961-3964.
28. Levin ER (2005) Integration of the extranuclear and nuclear actions of estrogen. Mol Endocrinol 19, 1951-1959.
29. Liu W, Ahmad SA, Reinmuth N, Shaheen RM, Jung YD, Fan F and Ellis LM (2000) Endothelial cell survival and apoptosis in the tumor vasculature. Apoptosis 5, 323-328.
30. Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS and Smithies O (1993) Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci USA 90, 11162-11166.
31. Martinou JC, Desagher S and Antonsson B (2000) Cyto-chrome c release from mitochondria: all or nothing. Nat Cell Biol 2, E41-E43.
32. Matsumoto T and Claesson-Welsh L (2001) VEGF receptor signal transduction. Science's STKE 112, RE21.
33. Mueller MD, Vigne JL, Minchenko A, Lebovic DI, Leitman DC and Taylor RN (2000) Regulation of vascular endothelial growth factor (VEGF) gene transcription by estrogen receptors alpha and beta. Proc Natl Acad Sci USA 97, 10972-10977.
34. Nuedling S, Kahlert S, Loebbert K, Doevendans PA, Meyer R, Vetter H and Grohe C (1999) 17 Beta-estradiol stimulates expression of endothelial and inducible NO synthase in rat myocardium in-vitro and in-vivo. Cardiovasc Res 43, 666- 674.
35. Orshal JM and Khalil RA (2004) Gender, sex hormones, and vascular tone. Am J Physiol 286, R233-R249.
36. Prencipe M, Ferretti C, Casini AR, Santini M, Giubilei F and Culasso F (1997) Stroke, disability, and dementia: results of a population survey. Stroke 28, 531-536.
37. Razmara A, Sunday L, Stirone C, Wang XB, Krause DN, Duckles SP and Procaccio V (2008) Mitochondrial effects of estrogen are mediated by estrogen receptor alpha in brain en-dothelial cells. J Pharmacol Exp Ther 325, 782-790.
38. Reckelhoff JF, Zhang H and Srivastava K (2000) Gender differences in development of hypertension in spontaneously hypertensive rats: role of the renin-angiotensin system. Hypertension 35, 480-483.
39. Rifci VA and Khachadurian AK (1992) The inhibition of low-density lipoprotein oxidation by 17-beta estradiol. Metabolism 41, 1110-1114.
40. Rosamond WD, Folsom AR, Chambless LE, Wang CH, McGovern PG, Howard G, Copper LS and Shahar E (1999) Stroke incidence and survival among middle-aged adults. Stroke 30, 736-743.
41. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SA, Howard BV, Johnson KC, Kotchen JM and Ockene J (2002) Risks and benefts of estrogen plus progestin in healthy post-menopausal women principal results from the Women's Health Initiative randomized controlled trial. JAMA 288, 321-333.
42. Rubanyi GM, Johns A and Kauser K (2002) Effect of estrogen on endothelial function and angiogenesis. Vascul Pharmacol 38, 89-98.
43. Rubanyi GM, Kauser K and Johns A (2002) Role of estrogen receptors in the vascular system. Vascul Pharmacol 38, 81- 88.
44. Saunders PT, Maguire SM, Gaughan J and Millar MR (1997) Expression of oestrogen receptor beta (ER beta) in multiple rat tissues visualised by immunohistochemistry. J Endocrinol 154, R13-R16.
45. Shughrue PJ, Lane MV and Merchenthaler I (1997) Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J Comp Neurol 388, 507- 525.
46. Stell A, Belcredito S, Ciana P and Maggi A (2008) Molecular imaging provides novel insights on estrogen receptor activity in mouse brain. Mol Imaging 7, 283-292.
47. Stevenson JC (2004) Hormone replacement therapy: review, update, and remaining questions after the Women's Health Initiative Study. Curr Osteoporos Rep 2, 12-16.
48. Sudlow CL and Warlow CP (1997) Comparable studies of the incidence of stroke and its pathological types: results from an international collaboration. International Stroke Incidence Collaboration. Stroke 28, 491-499.
49. Sundner P, Wolf K, Bergmaier U, Gess B and Kurtz A (1997) Hypoxia and cobalt stimulate vascular endothelial growth factor receptor gene expression in rats. Pfügers Archiv 433, 803-808.
50. Toi M, Inada K, Hoshina S, Suzuki H, Kondo S and Tominaga T (1995) Vascular endothelial growth factor and platelet-derived endothelial cell growth factor are frequently coex-pressed in highly vascularized human breast cancer. Clin Cancer Res 1, 961-964.
51. Tsai MJ, Chen YMA, Weng CF, Liou DY, Yang HC, Chen CH, Liao RH, Kuo FS, Chiu CW, Kuo HS, Huang MC and Li YL (2010) Enhanced expression of glycine N-methyltrans-ferase by adenovirus-mediated gene transfer in CNS culture is neuroprotective. Ann N Y Acad Sci 1199, 194-203.
52. Vasudevan N and Pfaff DW (2008) Non-genomic actions of estrogens and their interaction with genomic actions in the brain. Front Neuroendocrinol 29, 238-257.
53. Walter P, Green S, Green G, Krust A, Bornert JM, Jeltsch JM, Staub A, Jensen E, Scrace G and Waterfeld M (1985) Cloning of the human estrogen receptor cDNA. Proc Natl Acad Sci USA 82, 7889-7893.
54. Wenger NK (2005) Menopausal hormone therapy: currently no evidence for cardiac protection. Pediatr Blood Cancer 44, 625-629.
55. Williams JK and Suparto I (2004) Hormone replacement therapy and cardiovascular disease: lessons from a monkey model of postmenopausal women. ILAR J 45, 139-146.
56. Writing Group Members, Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, Simone GD, Ferguson TB, Ford E, Furie K, et al. (2010) Heart disease and stroke statistics- 2010 update: a report from the American Heart Association. Circulation 121, e46-e215.
57. The Writing Group for the PEPI Trial, et al. (1995) Effects of estrogen or estrogen/progestin regimens on heart disease risk factors in postmenopausal women. The Postmenopausal Estrogen/Progestin Interventions (PEPI) Trial. JAMA 273, 199-208.
58. Yatsuya H, Folsom AR, Yamagishi K, North KE, Brancati FL, Stevens J, and for the ARIC Study Investigators (2010) Race- and sex-specifc associations of obesity measures with ischemic stroke incidence in the Atherosclerosis Risk in Communities (ARIC) study. Stroke 41, 417-425.
59. Zachary I (2003) VEGF signaling: integration and multi-tasking in endothelial cell biology. Biochem Soc Trans 31, 1171-1177.