17ß-Estradiol Antagonizes the Down-Regulation of ERα/NOS-3 Signaling in Vascular Endothelial Dysfunction of Female Diabetic Rats

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Han, Yi ^a   Li, Xiaozhen ^b   Zhou, Suming ^a   Meng, Guoliang ^b   Xiao, Yujiao ^b   Zhang, Wen ^b   Wang, Zhuoying ^b   Xie, Liping ^b   Liu, Zhen ^b   Lu, Hui ^b   Ji, Yong ^b  

^a THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

^b NANJING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; GELATINASE B; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; TISSUE INHIBITOR OF METALLOPROTEINASE 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY CONSTRICTION; ARTERY DILATATION; ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; DOWN REGULATION; DRUG EFFECT; DRUG MECHANISM; ENDOTHELIAL DYSFUNCTION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME SYNTHESIS; FEMALE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM;

ANIMALS; AORTA; CELL LINE; CYCLIC GMP; DIABETES MELLITUS, EXPERIMENTAL; DOWN-REGULATION; ENDOTHELIUM, VASCULAR; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGENS; ETHIDIUM; EXTRACELLULAR MATRIX; FEMALE; MATRIX METALLOPROTEINASE 9; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; TISSUE INHIBITOR OF METALLOPROTEINASE-1; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

ANIMALIA; RATTUS;

EID: 84870505790     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050402     Document Type: Article

References (47)

1. Felaco M, Grilli A, De Lutiis MA, Patruno A, Libertini N, et al. (2001) Endothelial nitric oxide synthase (eNOS) expression and localization in healthy and diabetic rat hearts. Ann Clin Lab Sci 31: 179-186.
2. Xu B, Chibber R, Ruggiero D, Kohner E, Ritter J, et al. (2003) Impairment of vascular endothelial nitric oxide synthase activity by advanced glycation end products. FASEB J 17: 1289-1291.
3. Xu B, Ji Y, Yao K, Cao YX, Ferro A, (2005) Inhibition of human endothelial cell nitric oxide synthesis by advanced glycation end-products but not glucose: relevance to diabetes. Clin Sci (Lond) 109: 439-446.
4. Brouchet L, Krust A, Dupont S, Chambon P, Bayard F, et al. (2001) Estradiol accelerates reendothelialization in mouse carotid artery through estrogen receptor-alpha but not estrogen receptor-beta. Circulation 103: 423-428.
5. Toutain CE, Filipe C, Billon A, Fontaine C, Brouchet L, et al. (2009) Estrogen receptor alpha expression in both endothelium and hematopoietic cells is required for the accelerative effect of estradiol on reendothelialization. Arterioscler Thromb Vasc Biol 29: 1543-1550.
6. Bernier SG, Haldar S, Michel T, (2000) Bradykinin-regulated interactions of the mitogen-activated protein kinase pathway with the endothelial nitric-oxide synthase. J Biol Chem 275: 30707-30715.
7. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, et al. (1999) Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399: 601-605.
8. Haynes MP, Sinha D, Russell KS, Collinge M, Fulton D, et al. (2000) Membrane estrogen receptor engagement activates endothelial nitric oxide synthase via the PI3-kinase-Akt pathway in human endothelial cells. Circ Res 87: 677-682.
9. Hisamoto K, Ohmichi M, Kanda Y, Adachi K, Nishio Y, et al. (2001) Induction of endothelial nitric-oxide synthase phosphorylation by the raloxifene analog LY117018 is differentially mediated by Akt and extracellular signal-regulated protein kinase in vascular endothelial cells. J Biol Chem 276: 47642-47649.
10. Tronc F, Wassef M, Esposito B, Henrion D, Glagov S, et al. (1996) Role of NO in flow-induced remodeling of the rabbit common carotid artery. Arterioscler Thromb Vasc Biol 16: 1256-1262.
11. Vasudevan H, Xiang H, McNeill JH, (2005) Differential regulation of insulin resistance and hypertension by sex hormones in fructose-fed male rats. Am J Physiol Heart Circ Physiol 289: H1335-1342.
12. Ordóñez P, Moreno M, Alonso A, Llaneza P, Díaz F, et al. (2008) 17beta-estradiol and/or progesterone protect from insulin resistance in STZ-induced diabetic rats. J Steroid Biochem Mol Biol 111: 287-294.
13. De Vriese AS, Verbeuren TJ, Van de Voorde J, Lameire NH, Vanhoutte PM, (2000) Endothelial dysfunction in diabetes. Br J Pharmacol 130: 963-974.
14. Belin de Chantemèle EJ, Vessières E, Guihot AL, Toutain B, Maquignau M, et al. (2009) Type 2 diabetes severely impairs structural and functional adaptation of rat resistance arteries to chronic changes in blood flow. Cardiovasc Res 81: 788-796.
15. Tan J, Hua Q, Xing X, Wen J, Liu R, et al. (2007) Impact of the metalloproteinase-9/tissue inhibitor of metalloproteinase-1 system on large arterial stiffness in patients with essential hypertension. Hypertens Res 30: 959-963.
16. Yasmin, McEniery CM, Wallace S, Dakham Z, Pulsalkar P, et al. (2005) Matrix metalloproteinase-9 (MMP-9), MMP-2, and serum elastase activity are associated with systolic hypertension and arterial stiffness. Arterioscler Thromb Vasc Biol 25: 372-378.
17. Kielstein JT, Impraim B, Simmel S, Bode-Böger SM, Tsikas D, et al. (2004) Cardiovascular effects of systemic nitric oxide synthase inhibition with asymmetrical dimethylarginine in humans. Circulation 109: 172-177.
18. Miyazaki-Akita A, Hayashi T, Ding QF, Shiraishi H, Nomura T, et al. (2007) 17beta-estradiol antagonizes the down-regulation of endothelial nitric-oxide synthase and GTP cyclohydrolase I by high glucose: relevance to postmenopausal diabetic cardiovascular disease. J Pharmacol Exp Ther 320: 591-598.
19. Chung AW, Yang HH, Sigrist MK, Brin G, Chum E, et al. (2009) Matrix metalloproteinase-2 and-9 exacerbate arterial stiffening and angiogenesis in diabetes and chronic kidney disease. Cardiovasc Res 84: 494-504.
20. Tayebjee MH, Lim HS, MacFadyen RJ, Lip GY, (2004) Matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 and-2 in type 2 diabetes: effect of 1 year's cardiovascular risk reduction therapy. Diabetes Care 27: 2049-2051.
21. Davis BJ, Xie Z, Viollet B, Zou MH, (2006) Activation of the AMP-activated kinase by antidiabetes drug metformin stimulates nitric oxide synthesis in vivo by promoting the association of heat shock protein 90 and endothelial nitric oxide synthase. Diabetes 55: 496-505.
22. Baba T, Shimizu T, Suzuki Y, Ogawara M, Isono K, et al. (2005) Estrogen, insulin, and dietary signals cooperatively regulate longevity signals to enhance resistance to oxidative stress in mice. J Biol Chem 280: 16417-16426.
23. Stirone C, Duckles SP, Krause DN, Procaccio V, (2005) Estrogen increases mitochondrial efficiency and reduces oxidative stress in cerebral blood vessels. Mol Pharmacol 68: 959-965.
24. Kanaya AM, Herrington D, Vittinghoff E, Lin F, Grady D, et al. (2003) Glycemic effects of postmenopausal hormone therapy: the Heart and Estrogen/progestin Replacement Study. A randomized, double-blind, placebo-controlled trial. Ann Intern Med 138: 1-9.
25. Margolis KL, Bonds DE, Rodabough RJ, Tinker L, Phillips LS, et al. (2004) Effect of oestrogen plus progestin on the incidence of diabetes in postmenopausal women: results from the Women's Health Initiative Hormone Trial. Diabetologia 47: 1175-1187.
26. Dumont O, Loufrani L, Henrion D, (2007) Key role of the NO-pathway and matrix metalloprotease-9 in high blood flow-induced remodeling of rat resistance arteries. Arterioscler Thromb Vasc Biol 27: 317-324.
27. Denizalti M, Bozkurt TE, Akpulat U, Sahin-Erdemli I, Abaci{dotless}oǧlu N, (2011) The vasorelaxant effect of hydrogen sulfide is enhanced in streptozotocin-induced diabetic rats. Naunyn. Schmiedeberqs. Arch Pharmacol 383: 509-517.
28. Csanyi G, Lepran I, Flesch T, Telegdy G, Szabo G, et al. (2007) Lack of endothelium-derived hyperpolarizing factor (EDHF) up-regulation in endothelial dysfunction in aorta in diabetic rats. Pharmacol Rep 59: 447-455.
29. Woodman OL, Malakul W, (2009) 3′,4′-Dihydroxyflavonol prevents diabetes-induced endothelial dysfunction in rat aorta. Life Sci 85: 54-59.
30. Paul RJ, Bowman PS, Johnson J, Martin AF, (2007) Effects of sex and estrogen on myosin COOH-terminal isoforms and contractility in rat aorta. Am J Physiol Regul Integr Comp Physiol 292: R751-757.
31. Abebe W, Mozaffari MS, (2007) Vascular reactivity changes in glucose-intolerant rat. J Cardiovasc Pharmacol 50: 590-597.
32. Kobayashi T, Hayashi Y, Taguchi K, Matsumoto T, Kamata K, (2006) ANG II enhances contractile responses via PI3-kinase p110 delta pathway in aortas from diabetic rats with systemic hyperinsulinemia. Am J Physiol Heart Circ Physiol 291: H846-853.
33. Song D, Hutchings SR, Pang CC, (2006) Impaired in vivo venous constriction in conscious obese Zucker rats with metabolic syndrome. Naunyn. Schmiedebergs. Arch Pharmacol 373: 451-456.
34. Cheng X, Leung SW, Lim SL, Pang CC, (2003) Attenuated arterial and venous constriction in conscious rats with streptozotocin-induced diabetes. Eur J Pharmaco 458: 299-304.
35. Kobayashi T, Taguchi K, Nemoto S, Nogami T, Matsumoto T, et al. (2009) Activation of the PDK-1/Akt/eNOS pathway involved in aortic endothelial function differs between hyperinsulinemic and insulin-deficient diabetic rats. Am J Physiol Heart Circ Physiol 297: H1767-1775.
36. Darblade B, Pendaries C, Krust A, Dupont S, Fouque MJ, et al. (2002) Estradiol alters nitric oxide production in the mouse aorta through the alpha-, but not beta-, estrogen receptor. Circ Res 90: 413-419.
37. Gavin KM, Seals DR, Silver AE, Moreau KL, (2009) Vascular endothelial estrogen receptor alpha is modulated by estrogen status and related to endothelial function and endothelial nitric oxide synthase in healthy women. J Clin Endocrinol Metab 94: 3513-3520.
38. Pinna C, Cignarella A, Sanvito P, Pelosi V, Bolego C, (2008) Prolonged ovarian hormone deprivation impairs the protective vascular actions of estrogen receptor alpha agonists. Hypertension 51: 1210-1217.
39. Kim KH, Bender JR, (2009) Membrane-initiated actions of estrogen on the endothelium. Mol Cell Endocrinol 308: 3-8.
40. Kim KH, Moriarty K, Bender JR, (2008) Vascular cell signaling by membrane estrogen receptors. Steroids 73: 864-869.
41. Li L, Hisamoto K, Kim KH, Haynes MP, Bauer PM, et al. (2007) Variant estrogen receptor-c-Src molecular interdependence and c-Src structural requirements for endothelial NO synthase activation. Proc Natl Acad Sci USA 104: 16468-16473.
42. Kleinert H, Wallerath T, Euchenhofer C, Ihrig-Biedert I, Li H, et al. (1998) Estrogens increase transcription of the human endothelial NO synthase gene: analysis of the transcription factors involved. Hypertension 31: 582-588.
43. Creager MA, Lüscher TF, Cosentino F, Beckman JA, (2003) Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: Part I. Circulation. 108: 1527-1532.
44. Albrecht EW, Stegeman CA, Heeringa P, Henning RH, van Goor H, (2003) Protective role of endothelial nitric oxide synthase. J Pathol 199: 8-17.
45. Bracamonte MP, Miller VM, (2001) Vascular effects of estrogens: arterial protection versus venous thrombotic risk. Trends Endocrinol Metab 12: 204-209.
46. Tamura K, Yamaguchi K, Kogo H, (2000) 17 Beta-estradiol inhibits ovariectomy-induced expression of inducible nitric oxide synthase in rat aorta in vivo. Life Sci 66: PL259-264.
47. Favre J, Gao J, Henry JP, Remy-jouet I, Fourquaux I, et al. (2010) Endothelial Estrogen Receptor α Plays an Essential Role in the Coronary and Myocardial Protective Effects of Estradiol in Ischemia/Reperfusion. Arterioscler Thromb Vasc Biol 30: 2562-2567.