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Estrogen and estrogen receptors in cardiovascular oxidative stress

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Abstract

The cardiovascular system of a premenopausal woman is prepared to adapt to the challenges of increased cardiac output and work load that accompany pregnancy. Thus, it is tempting to speculate whether enhanced adaptability of the female cardiovascular system might be advantageous under conditions that promote cardiovascular disease. In support of this concept, 17β-estradiol as the major female sex hormone has been shown to confer protective cardiovascular effects in experimental studies. Mechanistically, these have been partially linked to the prevention and protection against oxidative stress. Current evidence indicates that estrogens attenuate oxidative stress at two levels: first, by preventing generation of reactive oxygen species (ROS) and, second, by scavenging ROS in the myocardium and in the vasculature. The purpose of this review is to give an overview on current concepts on conditions and mechanisms by which estrogens protect the cardiovascular system against ROS-mediated cellular injury.

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References

  1. Alderton WK, Cooper CE, Knowles RG (2001) Nitric oxide synthases: structure, function and inhibition. Biochem J 357(Pt 3):593–615

    Article  PubMed  CAS  Google Scholar 

  2. Altenhofer S, Kleikers PW, Radermacher KA, Scheurer P, Rob Hermans JJ, Schiffers P, Ho H, Wingler K, Schmidt HH (2012) The NOX toolbox: validating the role of NADPH oxidases in physiology and disease. Cell Mol Life Sci 69(14):2327–2343. doi:10.1007/s00018-012-1010-9

    Article  PubMed  Google Scholar 

  3. Arias-Loza PA, Hu K, Frantz S, Dienesch C, Bayer B, Wu R, Ertl G, Pelzer T (2011) Medroxyprogesterone acetate aggravates oxidative stress and left ventricular dysfunction in rats with chronic myocardial infarction. Toxicol Pathol 39(5):867–878. doi:10.1177/0192623311410441

    Article  PubMed  CAS  Google Scholar 

  4. Barbacanne MA, Rami J, Michel JB, Souchard JP, Philippe M, Besombes JP, Bayard F, Arnal JF (1999) Estradiol increases rat aorta endothelium-derived relaxing factor (EDRF) activity without changes in endothelial NO synthase gene expression: possible role of decreased endothelium-derived superoxide anion production. Cardiovasc Res 41(3):672–681

    Article  PubMed  CAS  Google Scholar 

  5. Baumer AT, Wassmann S, Ahlbory K, Strehlow K, Muller C, Sauer H, Bohm M, Nickenig G (2001) Reduction of oxidative stress and AT1 receptor expression by the selective oestrogen receptor modulator idoxifene. Br J Pharmacol 134(3):579–584. doi:10.1038/sj.bjp.0704299

    Article  PubMed  CAS  Google Scholar 

  6. Booth EA, Lucchesi BR (2007) Medroxyprogesterone acetate prevents the cardioprotective and anti-inflammatory effects of 17beta-estradiol in an in vivo model of myocardial ischemia and reperfusion. Am J Physiol Heart Circ Physiol 293(3):H1408–H1415. doi:10.1152/ajpheart.00993.2006

    Article  PubMed  CAS  Google Scholar 

  7. Borras C, Gambini J, Lopez-Grueso R, Pallardo FV, Vina J (2010) Direct antioxidant and protective effect of estradiol on isolated mitochondria. Biochim Biophys Acta 1802(1):205–211. doi:10.1016/j.bbadis.2009.09.007

    Article  PubMed  CAS  Google Scholar 

  8. Brilla CG, Weber KT (1992) Mineralocorticoid excess, dietary sodium, and myocardial fibrosis. J Lab Clin Med 120(6):893–901

    PubMed  CAS  Google Scholar 

  9. Busserolles J, Mazur A, Gueux E, Rock E, Rayssiguier Y (2002) Metabolic syndrome in the rat: females are protected against the pro-oxidant effect of a high sucrose diet. Exp Biol Med (Maywood) 227(9):837–842

    CAS  Google Scholar 

  10. Cavasin MA, Sankey SS, Yu AL, Menon S, Yang XP (2003) Estrogen and testosterone have opposing effects on chronic cardiac remodeling and function in mice with myocardial infarction. Am J Physiol Heart Circ Physiol 284(5):H1560–H1569. doi:10.1152/ajpheart.01087.2002

    PubMed  CAS  Google Scholar 

  11. Crabbe DL, Dipla K, Ambati S, Zafeiridis A, Gaughan JP, Houser SR, Margulies KB (2003) Gender differences in post-infarction hypertrophy in end-stage failing hearts. J Am Coll Cardiol 41(2):300–306

    Article  PubMed  Google Scholar 

  12. Dean SA, Tan J, White R, O'Brien ER, Leenen FH (2006) Regulation of components of the brain and cardiac renin-angiotensin systems by 17beta-estradiol after myocardial infarction in female rats. Am J Physiol Regul Integr Comp Physiol 291(1):R155–R162. doi:10.1152/ajpregu.00497.2005

    Article  PubMed  CAS  Google Scholar 

  13. Deschamps AM, Murphy E, Sun J (2010) Estrogen receptor activation and cardioprotection in ischemia reperfusion injury. Trends Cardiovasc Med 20(3):73–78. doi:10.1016/j.tcm.2010.05.001

    Article  PubMed  CAS  Google Scholar 

  14. Ejima K, Nanri H, Araki M, Uchida K, Kashimura M, Ikeda M (1999) 17Beta-estradiol induces protein thiol/disulfide oxidoreductases and protects cultured bovine aortic endothelial cells from oxidative stress. Eur J Endocrinol 140(6):608–613

    Article  PubMed  CAS  Google Scholar 

  15. Florian M, Freiman A, Magder S (2004) Treatment with 17-beta-estradiol reduces superoxide production in aorta of ovariectomized rats. Steroids 69(13–14):779–787. doi:10.1016/j.steroids.2004.09.008

    Article  PubMed  CAS  Google Scholar 

  16. Foryst-Ludwig A, Kintscher U (2010) Metabolic impact of estrogen signalling through ERalpha and ERbeta. J Steroid Biochem Mol Biol 122(1–3):74–81. doi:10.1016/j.jsbmb.2010.06.012

    Article  PubMed  CAS  Google Scholar 

  17. Furchgott RF (1999) Endothelium-derived relaxing factor: discovery, early studies, and identification as nitric oxide. Biosci Rep 19(4):235–251

    Article  PubMed  CAS  Google Scholar 

  18. Gragasin FS, Xu Y, Arenas IA, Kainth N, Davidge ST (2003) Estrogen reduces angiotensin II-induced nitric oxide synthase and NAD(P)H oxidase expression in endothelial cells. Arterioscler Thromb Vasc Biol 23(1):38–44

    Article  PubMed  CAS  Google Scholar 

  19. Griendling KK, FitzGerald GA (2003) Oxidative stress and cardiovascular injury: part I: basic mechanisms and in vivo monitoring of ROS. Circulation 108(16):1912–1916. doi:10.1161/01.CIR.0000093660.86242.BB

    Article  PubMed  Google Scholar 

  20. Griendling KK, Minieri CA, Ollerenshaw JD, Alexander RW (1994) Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res 74(6):1141–1148

    Article  PubMed  CAS  Google Scholar 

  21. Hayward CS, Kelly RP, Collins P (2000) The roles of gender, the menopause and hormone replacement on cardiovascular function. Cardiovasc Res 46(1):28–49

    Article  PubMed  CAS  Google Scholar 

  22. Hernandez I, Delgado JL, Diaz J, Quesada T, Teruel MJ, Llanos MC, Carbonell LF (2000) 17Beta-estradiol prevents oxidative stress and decreases blood pressure in ovariectomized rats. Am J Physiol Regul Integr Comp Physiol 279(5):R1599–R1605

    PubMed  CAS  Google Scholar 

  23. Javeshghani D, Schiffrin EL, Sairam MR, Touyz RM (2009) Potentiation of vascular oxidative stress and nitric oxide-mediated endothelial dysfunction by high-fat diet in a mouse model of estrogen deficiency and hyperandrogenemia. J Am Soc Hypertens 3(5):295–305. doi:10.1016/j.jash.2009.07.002

    Article  PubMed  Google Scholar 

  24. Jazbutyte V, Kehl F, Neyses L, Pelzer T (2009) Estrogen receptor alpha interacts with 17beta-hydroxysteroid dehydrogenase type 10 in mitochondria. Biochem Biophys Res Commun 384(4):450–454. doi:10.1016/j.bbrc.2009.04.139

    Article  PubMed  CAS  Google Scholar 

  25. Jeanes HL, Tabor C, Black D, Ederveen A, Gray GA (2008) Oestrogen-mediated cardioprotection following ischaemia and reperfusion is mimicked by an oestrogen receptor (ER)alpha agonist and unaffected by an ER beta antagonist. J Endocrinol 197(3):493–501. doi:10.1677/JOE-08-0071

    Article  PubMed  CAS  Google Scholar 

  26. Jeong EM, Liu M, Sturdy M, Gao G, Varghese ST, Sovari AA, Dudley SC Jr (2012) Metabolic stress, reactive oxygen species, and arrhythmia. J Mol Cell Cardiol 52(2):454–463. doi:10.1016/j.yjmcc.2011.09.018

    Article  PubMed  CAS  Google Scholar 

  27. Kannel WB, Hjortland MC, McNamara PM, Gordon T (1976) Menopause and risk of cardiovascular disease: the Framingham study. Ann Intern Med 85(4):447–452

    Article  PubMed  CAS  Google Scholar 

  28. Kauser K, Rubanyi GM (1994) Gender difference in bioassayable endothelium-derived nitric oxide from isolated rat aortae. Am J Physiol 267(6 Pt 2):H2311–H2317

    PubMed  CAS  Google Scholar 

  29. Kim JK, Pedram A, Razandi M, Levin ER (2006) Estrogen prevents cardiomyocyte apoptosis through inhibition of reactive oxygen species and differential regulation of p38 kinase isoforms. J Biol Chem 281(10):6760–6767. doi:10.1074/jbc.M511024200

    Article  PubMed  CAS  Google Scholar 

  30. Lagranha CJ, Deschamps A, Aponte A, Steenbergen C, Murphy E (2010) Sex differences in the phosphorylation of mitochondrial proteins result in reduced production of reactive oxygen species and cardioprotection in females. Circ Res 106(11):1681–1691. doi:10.1161/CIRCRESAHA.109.213645

    Article  PubMed  CAS  Google Scholar 

  31. Lam KK, Lee YM, Hsiao G, Chen SY, Yen MH (2006) Estrogen therapy replenishes vascular tetrahydrobiopterin and reduces oxidative stress in ovariectomized rats. Menopause 13(2):294–302. doi:10.1097/01.gme.0000182806.99137.5e

    Article  PubMed  Google Scholar 

  32. Lassegue B, San Martin A, Griendling KK (2012) Biochemistry, physiology, and pathophysiology of NADPH oxidases in the cardiovascular system. Circ Res 110(10):1364–1390. doi:10.1161/CIRCRESAHA.111.243972

    Article  PubMed  CAS  Google Scholar 

  33. Laufs U, Adam O, Strehlow K, Wassmann S, Konkol C, Laufs K, Schmidt W, Bohm M, Nickenig G (2003) Down-regulation of Rac-1 GTPase by estrogen. J Biol Chem 278(8):5956–5962. doi:10.1074/jbc.M209813200

    Article  PubMed  CAS  Google Scholar 

  34. Li L, Hisamoto K, Kim KH, Haynes MP, Bauer PM, Sanjay A, Collinge M, Baron R, Sessa WC, Bender JR (2007) Variant estrogen receptor-c-Src molecular interdependence and c-Src structural requirements for endothelial NO synthase activation. Proc Natl Acad Sci U S A 104(42):16468–16473. doi:10.1073/pnas.0704315104

    Article  PubMed  CAS  Google Scholar 

  35. Li JM, Shah AM (2004) Endothelial cell superoxide generation: regulation and relevance for cardiovascular pathophysiology. Am J Physiol Regul Integr Comp Physiol 287(5):R1014–R1030. doi:10.1152/ajpregu.00124.2004

    Article  PubMed  CAS  Google Scholar 

  36. McNeill AM, Kim N, Duckles SP, Krause DN, Kontos HA (1999) Chronic estrogen treatment increases levels of endothelial nitric oxide synthase protein in rat cerebral microvessels. Stroke 30(10):2186–2190

    Article  PubMed  CAS  Google Scholar 

  37. Mendelsohn ME, Karas RH (1999) The protective effects of estrogen on the cardiovascular system. N Engl J Med 340(23):1801–1811. doi:10.1056/NEJM199906103402306

    Article  PubMed  CAS  Google Scholar 

  38. Mendelsohn ME, Karas RH (2005) Molecular and cellular basis of cardiovascular gender differences. Science 308(5728):1583–1587. doi:10.1126/science.1112062

    Article  PubMed  CAS  Google Scholar 

  39. Moreau KL, Meditz A, Deane KD, Kohrt WM (2012) Tetrahydrobiopterin improves endothelial function and decreases arterial stiffness in estrogen-deficient postmenopausal women. Am J Physiol Heart Circ Physiol 302(5):H1211–H1218. doi:10.1152/ajpheart.01065.2011

    Article  PubMed  CAS  Google Scholar 

  40. Muehlfelder M, Arias-Loza PA, Fritzemeier KH, Pelzer T (2012) Both estrogen receptor subtypes, ERalpha and ERbeta, prevent aldosterone-induced oxidative stress in VSMC via increased NADPH bioavailability. Biochem Biophys Res Commun 423(4):850–856. doi:10.1016/j.bbrc.2012.06.053

    Article  PubMed  CAS  Google Scholar 

  41. Murase T, Hattori T, Ohtake M, Nakashima C, Takatsu M, Murohara T, Nagata K (2012) Effects of estrogen on cardiovascular injury in ovariectomized female DahlS.Z-Lepr(fa)/Lepr(fa) rats as a new animal model of metabolic syndrome. Hypertension 59(3):694–704. doi:10.1161/HYPERTENSIONAHA.111.180976

    Article  PubMed  CAS  Google Scholar 

  42. Nickenig G, Baumer AT, Grohe C, Kahlert S, Strehlow K, Rosenkranz S, Stablein A, Beckers F, Smits JF, Daemen MJ, Vetter H, Bohm M (1998) Estrogen modulates AT1 receptor gene expression in vitro and in vivo. Circulation 97(22):2197–2201

    Article  PubMed  CAS  Google Scholar 

  43. Ortmann J, Veit M, Zingg S, Di Santo S, Traupe T, Yang Z, Volzmann J, Dubey RK, Christen S, Baumgartner I (2011) Estrogen receptor-alpha but not -beta or GPER inhibits high glucose-induced human VSMC proliferation: potential role of ROS and ERK. J Clin Endocrinol Metab 96(1):220–228. doi:10.1210/jc.2010-0943

    Article  PubMed  Google Scholar 

  44. Paravicini TM, Touyz RM (2008) NADPH oxidases, reactive oxygen species, and hypertension: clinical implications and therapeutic possibilities. Diabetes Care 31(Suppl 2):S170–S180. doi:10.2337/dc08-s247

    Article  PubMed  CAS  Google Scholar 

  45. Perjes A, Kubin AM, Konyi A, Szabados S, Cziraki A, Skoumal R, Ruskoaho H, Szokodi I (2012) Physiological regulation of cardiac contractility by endogenous reactive oxygen species. Acta Physiol (Oxf) 205(1):26–40. doi:10.1111/j.1748-1716.2012.02391.x

    Article  CAS  Google Scholar 

  46. Poornima IG, Parikh P, Shannon RP (2006) Diabetic cardiomyopathy: the search for a unifying hypothesis. Circ Res 98(5):596–605. doi:10.1161/01.RES.0000207406.94146.c2

    Article  PubMed  CAS  Google Scholar 

  47. Raedschelders K, Ansley DM, Chen DD (2012) The cellular and molecular origin of reactive oxygen species generation during myocardial ischemia and reperfusion. Pharmacol Ther 133(2):230–255. doi:10.1016/j.pharmthera.2011.11.004

    Article  PubMed  CAS  Google Scholar 

  48. Razmara A, Sunday L, Stirone C, Wang XB, Krause DN, Duckles SP, Procaccio V (2008) Mitochondrial effects of estrogen are mediated by estrogen receptor alpha in brain endothelial cells. J Pharmacol Exp Ther 325(3):782–790. doi:10.1124/jpet.107.134072

    Article  PubMed  CAS  Google Scholar 

  49. Schramm A, Matusik P, Osmenda G, Guzik TJ (2012) Targeting NADPH oxidases in vascular pharmacology. Vascul Pharmacol 56(5–6):216–231. doi:10.1016/j.vph.2012.02.012

    Article  PubMed  CAS  Google Scholar 

  50. Smith PJ, Ornatsky O, Stewart DJ, Picard P, Dawood F, Wen WH, Liu PP, Webb DJ, Monge JC (2000) Effects of estrogen replacement on infarct size, cardiac remodeling, and the endothelin system after myocardial infarction in ovariectomized rats. Circulation 102(24):2983–2989

    Article  PubMed  CAS  Google Scholar 

  51. Sovershaev MA, Egorina EM, Andreasen TV, Jonassen AK, Ytrehus K (2006) Preconditioning by 17beta-estradiol in isolated rat heart depends on PI3-K/PKB pathway, PKC, and ROS. Am J Physiol Heart Circ Physiol 291(4):H1554–H1562. doi:10.1152/ajpheart.01171.2005

    Article  PubMed  CAS  Google Scholar 

  52. Stirone C, Boroujerdi A, Duckles SP, Krause DN (2005) Estrogen receptor activation of phosphoinositide-3 kinase, akt, and nitric oxide signaling in cerebral blood vessels: rapid and long-term effects. Mol Pharmacol 67(1):105–113. doi:10.1124/mol.104.004465

    Article  PubMed  CAS  Google Scholar 

  53. Stirone C, Chu Y, Sunday L, Duckles SP, Krause DN (2003) 17 Beta-estradiol increases endothelial nitric oxide synthase mRNA copy number in cerebral blood vessels: quantification by real-time polymerase chain reaction. Eur J Pharmacol 478(1):35–38

    Article  PubMed  CAS  Google Scholar 

  54. Strehlow K, Rotter S, Wassmann S, Adam O, Grohe C, Laufs K, Bohm M, Nickenig G (2003) Modulation of antioxidant enzyme expression and function by estrogen. Circ Res 93(2):170–177. doi:10.1161/01.RES.0000082334.17947.11

    Article  PubMed  CAS  Google Scholar 

  55. Szabo C (2003) Multiple pathways of peroxynitrite cytotoxicity. Toxicol Lett 140–141:105–112

    Article  PubMed  Google Scholar 

  56. Timmermans PB, Wong PC, Chiu AT, Herblin WF, Benfield P, Carini DJ, Lee RJ, Wexler RR, Saye JA, Smith RD (1993) Angiotensin II receptors and angiotensin II receptor antagonists. Pharmacol Rev 45(2):205–251

    PubMed  CAS  Google Scholar 

  57. Tomaschitz A, Pilz S, Ritz E, Meinitzer A, Boehm BO, Marz W (2010) Plasma aldosterone levels are associated with increased cardiovascular mortality: the Ludwigshafen Risk and Cardiovascular Health (LURIC) study. Eur Heart J 31(10):1237–1247. doi:10.1093/eurheartj/ehq019

    Article  PubMed  CAS  Google Scholar 

  58. Tschudi MR, Mesaros S, Luscher TF, Malinski T (1996) Direct in situ measurement of nitric oxide in mesenteric resistance arteries. Increased decomposition by superoxide in hypertension. Hypertension 27(1):32–35

    Article  PubMed  CAS  Google Scholar 

  59. Urata Y, Ihara Y, Murata H, Goto S, Koji T, Yodoi J, Inoue S, Kondo T (2006) 17Beta-estradiol protects against oxidative stress-induced cell death through the glutathione/glutaredoxin-dependent redox regulation of Akt in myocardiac H9c2 cells. J Biol Chem 281(19):13092–13102. doi:10.1074/jbc.M601984200

    Article  PubMed  CAS  Google Scholar 

  60. Vasquez-Vivar J, Kalyanaraman B, Martasek P, Hogg N, Masters BS, Karoui H, Tordo P, Pritchard KA Jr (1998) Superoxide generation by endothelial nitric oxide synthase: the influence of cofactors. Proc Natl Acad Sci U S A 95(16):9220–9225

    Article  PubMed  CAS  Google Scholar 

  61. Wagner AH, Schroeter MR, Hecker M (2001) 17beta-estradiol inhibition of NADPH oxidase expression in human endothelial cells. FASEB J 15(12):2121–2130. doi:10.1096/fj.01-0123com

    Article  PubMed  CAS  Google Scholar 

  62. Wassmann S, Laufs U, Stamenkovic D, Linz W, Stasch JP, Ahlbory K, Rosen R, Bohm M, Nickenig G (2002) Raloxifene improves endothelial dysfunction in hypertension by reduced oxidative stress and enhanced nitric oxide production. Circulation 105(17):2083–2091

    Article  PubMed  CAS  Google Scholar 

  63. Wing LY, Chen YC, Shih YY, Cheng JC, Lin YJ, Jiang MJ (2009) Effects of oral estrogen on aortic ROS-generating and-scavenging enzymes and atherosclerosis in apoE-deficient mice. Exp Biol Med (Maywood) 234(9):1037–1046. doi:10.3181/0811-RM-332

    Article  CAS  Google Scholar 

  64. Wong CM, Yung LM, Leung FP, Tsang SY, Au CL, Chen ZY, Yao X, Cheng CH, Lau CW, Gollasch M, Huang Y (2008) Raloxifene protects endothelial cell function against oxidative stress. Br J Pharmacol 155(3):326–334. doi:10.1038/bjp.2008.262

    Article  PubMed  CAS  Google Scholar 

  65. Yang SH, Liu R, Perez EJ, Wen Y, Stevens SM Jr, Valencia T, Brun-Zinkernagel AM, Prokai L, Will Y, Dykens J, Koulen P, Simpkins JW (2004) Mitochondrial localization of estrogen receptor beta. Proc Natl Acad Sci U S A 101(12):4130–4135. doi:10.1073/pnas.0306948101

    Article  PubMed  CAS  Google Scholar 

  66. Yung LM, Wong WT, Tian XY, Leung FP, Yung LH, Chen ZY, Yao X, Lau CW, Huang Y (2011) Inhibition of renin-angiotensin system reverses endothelial dysfunction and oxidative stress in estrogen deficient rats. PLoS One 6(3):e17437. doi:10.1371/journal.pone.0017437

    Article  PubMed  CAS  Google Scholar 

  67. Zhang L, Fujii S, Kosaka H (2007) Effect of oestrogen on reactive oxygen species production in the aortas of ovariectomized Dahl salt-sensitive rats. J Hypertens 25(2):407–414. doi:10.1097/HJH.0b013e328010beee

    Article  PubMed  CAS  Google Scholar 

  68. Zhang Y, Tocchetti CG, Krieg T, Moens AL (2012) Oxidative and nitrosative stress in the maintenance of myocardial function. Free Radic Biol Med 53(8):1531–1540. doi:10.1016/j.freeradbiomed.2012.07.010

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

T.P. received support from the Interdisciplinary Center for Clinical Research Würzburg (Z-2/21 and F-144) and the Comprehensive Heart Failure Center Würzburg (CHFC D-5).

Conflict of interest

T.P. has received financial support from the Bayer Pharma AG Berlin that relates to the evaluation of novel steroid hormone receptor ligands.

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Authors and Affiliations

  1. Department of Internal Medicine I, University Hospital of Würzburg, Würzburg, Germany

    Paula-Anahi Arias-Loza, Melanie Muehlfelder & Theo Pelzer

  2. Department of Medicine I—Cardiology and Pneumology (ZIM), University Hospital of Würzburg, Oberduerrbacher Str. 6, 97080, Würzburg, Germany

    Theo Pelzer

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  1. Paula-Anahi Arias-Loza
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Correspondence to Theo Pelzer.

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This article is published as part of the special issue on “Sex differences in health and disease: brain and heart connections.”

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Arias-Loza, PA., Muehlfelder, M. & Pelzer, T. Estrogen and estrogen receptors in cardiovascular oxidative stress. Pflugers Arch - Eur J Physiol 465, 739–746 (2013). https://doi.org/10.1007/s00424-013-1247-7

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