Effects of oral estrogen on aortic ROS-generating and -scavenging enzymes and atherosclerosis in apoE-deficient mice

Experimental Biology and Medicine

Volumn 234, Issue 9, 2009, Pages 1037-1046

  Wing, Lih Yuh Chen ^a   Chen, Ya Chi ^a   Shih, Yu Yin ^a   Cheng, Jung Chien ^a   Lin, Yiu Jiuan ^b   Jiang, Meei Jyh ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b CHUNG HWA UNIVERSITY OF MEDICAL TECHNOLOGY   (Taiwan)

Author keywords

Atherosclerosis; NAD(P)H oxidase; Oral estrogen; Reactive oxygen species; ROS scavenging enzymes

Indexed keywords

APOENZYME; CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; ESTRADIOL; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MANGANESE SUPEROXIDE DISMUTASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA ROOT; ARTICLE; ATHEROSCLEROSIS; BLOOD LEVEL; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DRUG EFFECT; FEMALE; HORMONE SUBSTITUTION; INTIMA; MOUSE; NONHUMAN; OXIDATIVE STRESS; PERITONEUM MACROPHAGE; PROTEIN EXPRESSION; SMOOTH MUSCLE FIBER; UPREGULATION; UTERUS WEIGHT;

ADMINISTRATION, ORAL; ANIMALS; AORTA; APOLIPOPROTEINS E; ATHEROSCLEROSIS; CELLS, CULTURED; CHOLESTEROL, LDL; ESTRADIOL; ESTROGENS; MACROPHAGES, PERITONEAL; MICE; MICE, KNOCKOUT; MUSCLE CELLS; NADPH OXIDASE; SUPEROXIDE DISMUTASE; SUPEROXIDES;

ANIMALIA; MUS;

EID: 70349150593     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.3181/0811-RM-332     Document Type: Article

References (48)

1. Ross R. Atherosclerosis - an inflammatory disease. N Engl J Med 1340:115-126, 1999.
2. Pagano PJ, Ito Y, Tornheim K, Gallop PM, Tauber AI, Cohen RA. An NADPH oxidase superoxide-generating system in the rabbit aorta. Am J Physiol 1268:H2274-2280, 1995.
3. Sorescu D, Weiss D, Lassegue B, Clempus RE, Szocs K, Sorescu GP, Valppu L, Quinn MT, Lambeth JD, Vega JD, Taylor WR, Griendling KK. Superoxide production and expression of nox family proteins in human atherosclerosis. Circulation l105:1429-1435, 2002. (Pubitemid 34263273)
4. Warnholtz A, Nickenig G, Schulz E, Macharzina R, Brasen JH, Skatchkov M, Heitzer T, Stasch JP, Griendling KK, Harrison DG, Bohm M, Meinertz T, Munzel T. Increased NADH-oxidase-mediated superoxide production in the early stages of atherosclerosis: evidence for involvement of the renin-angiotensin system. Circulation l99:2027-2033, 1999. (Pubitemid 29183901)
5. Barry-Lane PA, Patterson C, van der Merwe M, Hu Z, Holland SM, Yeh ET, Runge MS. p47phox is required for atherosclerotic lesion progression in ApoE(-/-) mice. J Clin Invest l108:1513-1522, 2001. (Pubitemid 33091989)
6. Khatri JJ, Johnson C, Magid R, Lessner SM, Laude KM, Dikalov SI, Harrison DG, Sung HJ, Rong Y, Galis ZS. Vascular oxidant stress enhances progression and angiogenesis of experimental atheroma. Circulation l109:520-525, 2004. (Pubitemid 38168516)
7. Ballinger SW, Patterson C, Knight-Lozano CA, Burow DL, Conklin CA, Hu Z, Reuf J, Horaist C, Lebovitz R, Hunter GC, McIntyre K, Runge MS. Mitochondrial integrity and function in atherogenesis. Circulation 1106:544-549, 2002.
8. Yang H, Roberts LJ, Shi MJ, Zhou LC, Ballard BR, Richardson A, Guo ZM. Retardation of atherosclerosis by overexpression of catalase or both Cu/Zn-superoxide dismutase and catalase in mice lacking apolipoprotein E. Circ Res l95:1075-1081, 2004. (Pubitemid 39557894)
9. Fuster V. Epidemic of cardiovascular disease and stroke: the three main challenges. Presented at the 71st scientific sessions of the American Heart Association. Dallas, Texas. Circulation 199:1132-1137, 1999.
10. van der Schouw YT, van der Graaf Y, Steyerberg EW, Eijkemans JC, Banga JD. Age at menopause as a risk factor for cardiovascular mortality. Lancet l347:714-718, 1996. (Pubitemid 26085645)
11. Adams MR, Kaplan JR, Manuck SB, Koritnik DR, Parks JS, Wolfe MS, Clarkson TB. Inhibition of coronary artery atherosclerosis by 17-beta estradiol in ovariectomized monkeys. Lack of an effect of added progesterone. Arteriosclerosis 110:1051-1057, 1990.
12. Bourassa PA, Milos PM, Gaynor BJ, Breslow JL, Aiello RJ. Estrogen reduces atherosclerotic lesion development in apolipoprotein E-deficient mice. Proc Natl Acad Sci U S A l93:10022-10027, 1996. (Pubitemid 26314567)
13. Haarbo J, Christiansen C. The impact of female sex hormones on secondary prevention of atherosclerosis in ovariectomized cholesterol-fed rabbits. Atherosclerosis l123:139-144, 1996. (Pubitemid 26175072)
14. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SA, Howard BV, Johnson KC, Kotchen JM, Ockene J. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA l288:321-333, 2002. (Pubitemid 34761611)
15. Godsland IF. Effects of postmenopausal hormone replacement therapy on lipid, lipoprotein, and apolipoprotein (a) concentrations: analysis of studies published from 1974-2000. Fertil Steril 175:898-915, 2001.
16. Scarabin PY, Oger E, Plu-Bureau G. Differential association of oral and transdermal oestrogen-replacement therapy with venous thromboembolism risk. Lancet l362:428-432, 2003. (Pubitemid 36999704)
17. Post MS, Christella M, Thomassen LG, van der Mooren MJ, van Baal WM, Rosing J, Kenemans P, Stehouwer CD. Effect of oral and transdermal estrogen replacement therapy on hemostatic variables associated with venous thrombosis: a randomized, placebo-controlled study in postmenopausal women. Arterioscler Thromb Vasc Biol l23:1116-1121, 2003. (Pubitemid 36713570)
18. Miller AP, Chen YF, Xing D, Feng W, Oparil S. Hormone replacement therapy and inflammation: interactions in cardiovascular disease. Hypertension l42:657-663, 2003. (Pubitemid 37237305)
19. Sumino H, Ichikawa S, Kasama S, Takahashi T, Kumakura H, Takayama Y, Kanda T, Kurabayashi M. Different effects of oral conjugated estrogen and transdermal estradiol on arterial stiffness and vascular inflammatory markers in postmenopausal women. Atherosclerosis l189:436-442, 2006. (Pubitemid 44634490)
20. Schunkert H, Danser AH, Hense HW, Derkx FH, Kurzinger S, Riegger GA. Effects of estrogen replacement therapy on the renin-angiotensin system in postmenopausal women. Circulation l95:39-45, 1997. (Pubitemid 27029940)
21. Tsuda M, Iwai M, Li JM, Li HS, Min LJ, Ide A, Okumura M, Suzuki J, Mogi M, Suzuki H, Horiuchi M. Inhibitory effects of AT1 receptor blocker, olmesartan, and estrogen on atherosclerosis via anti-oxidative stress. Hypertension l45:545-551, 2005. (Pubitemid 40411257)
22. Strehlow K, Rotter S, Wassmann S, Adam O, Grohe C, Laufs K, Bohm M, Nickenig G. Modulation of antioxidant enzyme expression and function by estrogen. Circ Res l93:170-177, 2003. (Pubitemid 36919705)
23. Nakashima Y, Plump AS, Raines EW, Breslow JL, Ross R. ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler Thromb l14:133-140, 1994. (Pubitemid 24028177)
24. Zhang SH, Reddick RL, Piedrahita JA, Maeda N. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science 1258:468-471, 1992.
25. Plump AS, Smith JD, Hayek T, Aalto-Setala K, Walsh A, Verstuyft JG, Rubin EM, Breslow JL. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell 171:343-353, 1992.
26. Meir KS, Leitersdorf E. Atherosclerosis in the apolipoprotein-E-deficient mouse: a decade of progress. Arterioscler Thromb Vasc Biol l24:1006-1014, 2004. (Pubitemid 38737824)
27. Hodgin JB, Maeda N. Minireview: estrogen and mouse models of atherosclerosis. Endocrinology l143:4495-4501, 2002. (Pubitemid 35397587)
28. Freireich EJ, Gehan EA, Rall DP, Schmidt LH, Skipper HE. Quantitative comparison of toxicity of anticancer agents in mouse, rat, hamster, dog, monkey, and man. Cancer Chemother Rep 150:219-244, 1966.
29. Lo IC, Shih JM, Jiang MJ. Reactive oxygen species and ERK 1/2 mediate monocyte chemotactic protein-1-stimulated smooth muscle cell migration. J Biomed Sci 112:377-388, 2005.
30. Watanabe T, Akishita M, Nakaoka T, Kozaki K, Miyahara Y, He H, Ohike Y, Ogita T, Inoue S, Muramatsu M, Yamashita N, Ouchi Y. Estrogen receptor beta mediates the inhibitory effect of estradiol on vascular smooth muscle cell proliferation. Cardiovasc Res l59:734-744, 2003. (Pubitemid 38368690)
31. Zhang L, Fujii S, Kosaka H. Effect of oestrogen on reactive oxygen species production in the aortas of ovariectomized Dahl salt-sensitive rats. J Hypertens l25:407-414, 2007. (Pubitemid 46071939)
32. Ambasta RK, Kumar P, Griendling KK, Schmidt HH, Busse R, Brandes RP. Direct interaction of the novel Nox proteins with p22phox is required for the formation of a functionally active NADPH oxidase. J Biol Chem l279:45935-45941, 2004. (Pubitemid 39491586)
33. Gragasin FS, Xu Y, Arenas IA, Kainth N, Davidge ST. Estrogen reduces angiotensin II-induced nitric oxide synthase and NAD(P)H oxidase expression in endothelial cells. Arterioscler Thromb Vasc Biol l23:38-44, 2003. (Pubitemid 36091623)
34. Sumi D, Hayashi T, Matsui-Hirai H, Jacobs AT, Ignarro LJ, Iguchi A. 17beta-estradiol inhibits NADPH oxidase activity through the regulation of p47phox mRNA and protein expression in THP-1 cells. Biochim Biophys Acta l1640:113-118, 2003. (Pubitemid 36555697)
35. Laufs U, Adam O, Strehlow K, Wassmann S, Konkol C, Laufs K, Schmidt W, Bohm M, Nickenig G. Down-regulation of Rac-1 GTPase by estrogen. J Biol Chem 1278:5956-5962, 2003.
36. De Keulenaer GW, Alexander RW, Ushio-Fukai M, Ishizaka N, Griendling KK. Tumour necrosis factor alpha activates a p22phox-based NADH oxidase in vascular smooth muscle. Biochem J l329 (Pt 3):653-657, 1998. (Pubitemid 28055190)
37. Manea A, Manea SA, Gafencu AV, Raicu M, Simionescu M. AP-1-dependent transcriptional regulation of NADPH oxidase in human aortic smooth muscle cells: role of p22phox subunit. Arterioscler Thromb Vasc Biol l28:878-885, 2008. (Pubitemid 351544102)
38. Heumuller S, Wind S, Barbosa-Sicard E, Schmidt HH, Busse R, Schroder K, Brandes RP. Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant. Hypertension l51:211-217, 2008. (Pubitemid 351159930)
39. Stirone C, Duckles SP, Krause DN, Procaccio V. Estrogen increases mitochondrial efficiency and reduces oxidative stress in cerebral blood vessels. Mol Pharmacol l68:959-965, 2005. (Pubitemid 41345787)
40. Grodstein F, Manson JE, Colditz GA, Willett WC, Speizer FE, Stampfer MJ. A prospective, observational study of postmenopausal hormone therapy and primary prevention of cardiovascular disease. Ann Intern Med l133:933-941, 2000. (Pubitemid 32003509)
41. Villablanca AC, Lewis KA, Tham D, Rutledge JC. Differential regulation of gene expression by ovariectomy in mouse aorta. Physiol Genomics l12:175-185, 2003. (Pubitemid 37139697)
42. Grasso P, Reichert LE Jr. In vivo effects of follicle-stimulating hormone-related synthetic peptides on the mouse estrous cycle. Endocrinology 1137:5370-5375, 1996.
43. Walmer DK, Wrona MA, Hughes CL, Nelson KG. Lactoferrin expression in the mouse reproductive tract during the natural estrous cycle: correlation with circulating estradiol and progesterone. Endocrinology 1131:1458-1466, 1992.
44. Anderson GL, Limacher M, Assaf AR, Bassford T, Beresford 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. Effects of conjugated equine estrogen in postmenopausal women with hysterectomy: the Women's Health Initiative randomized controlled trial. JAMA l291:1701-1712, 2004. (Pubitemid 38489892)
45. Rosano GM, Maffei S, Andreassi MG, Vitale C, Vassalle C, Gambacciani M, Stramba-Badiale M, Mercuro G. Hormone replacement therapy and cardioprotection: a new dawn? A statement of the Study Group on Cardiovascular Disease in Women of the Italian Society of Cardiology on hormone replacement therapy in postmenopausal women. J Cardiovasc Med (Hagerstown) 110:85-92, 2009.
46. Grodstein F, Manson JE, Stampfer MJ. Hormone therapy and coronary heart disease: the role of time since menopause and age at hormone initiation. J Womens Health (Larchmt) l15:35-44, 2006. (Pubitemid 43192860)
47. Clarkson TB, Appt SE. Controversies about HRT - lessons from monkey models. Maturitas 151:64-74, 2005.
48. Rosenfeld ME, Kauser K, Martin-McNulty B, Polinsky P, Schwartz SM, Rubanyi GM. Estrogen inhibits the initiation of fatty streaks throughout the vasculature but does not inhibit intra-plaque hemorrhage and the progression of established lesions in apolipoprotein E deficient mice. Atherosclerosis l164:251-259, 2002. (Pubitemid 35223074)