Estrogen receptor agonists alleviate cardiac and renal oxidative injury in rats with renovascular hypertension

References

• Chobanian AV, Bakris GL, Black HR, et al. The seventh report of the joint national committee on prevention, detection, evaluation, and treatment of high blood pressure: the JNC 7 report. JAMA 2003;289:2560–572.
   Google Scholar
• August P. Hypertension in women. Adv Chronic Kidney Dis 2013;20:396–401.
   PubMed Web of Science ®Google Scholar
• Hall PM. Hypertension in women. Cardiology 1990;77(Suppl 2):25–30.
   PubMed Web of Science ®Google Scholar
• Mendonca LS, Fernandes-Santos C, Mandarim-de-Lacerda CA. Cardiac and aortic structural alterations due to surgically-induced menopause associated with renovascular hypertension in rats. Int J Exp Pathol 2007;88:301–9.
   PubMed Web of Science ®Google Scholar
• Mendelsohn ME, Karas RH. The protective effects of estrogen on the cardiovascular system. N Engl J Med 1999;340:1801–11.
   PubMed Web of Science ®Google Scholar
• Stampfer MJ, Colditz GA, Willett WC, et al. Postmenopausal estrogen therapy and cardiovascular disease. Ten-year follow-up from the nurses’ health study. N Engl J Med 1991;325:756–62.
   PubMed Web of Science ®Google Scholar
• Wang Y, Shoemaker R, Thatcher SE, et al. Administration of 17beta-estradiol to ovariectomized obese female mice reverses obesity-hypertension through an ACE2-dependent mechanism. Am J Physiol Endocrinol Metab 2015;308:E1066–75.
   PubMed Web of Science ®Google Scholar
• Campos C, Sartorio CL, Casali KR, et al. Low-dose estrogen is as effective as high-dose treatment in rats with postmenopausal hypertension. J Cardiovasc Pharmacol 2014;63:144–151.
   PubMed Web of Science ®Google Scholar
• Barrett-Connor E, Bush TL. Estrogen and coronary heart disease in women. JAMA 1991;265:1861–7.
   PubMed Web of Science ®Google Scholar
• Grodstein F, Chen J, Pollen DA, et al. Postmenopausal hormone therapy and cognitive function in healthy older women. J Am Geriatr Soc 2000;48:746–52.
   PubMed Web of Science ®Google Scholar
• Pinto S, Virdis A, Ghiadoni L, et al. Endogenous estrogen and acetylcholine-induced vasodilation in normotensive women. Hypertension 1997;29:268–73.
   PubMed Web of Science ®Google Scholar
• Hulley S, Grady D, Bush T, et al. Randomized trial of estrogen plus progestin for secondary prevention of coronary heart disease in postmenopausal women. heart and estrogen/progestin replacement study (HERS) research group. JAMA 1998;280:605–613.
   PubMed Web of Science ®Google Scholar
• Sun J, Meyers MJ, Fink BE, et al. Novel ligands that function as selective estrogens or antiestrogens for estrogen receptor-alpha or estrogen receptor-beta. Endocrinology 1999;140:800–4.
   PubMed Web of Science ®Google Scholar
• Hall JM. Responses of adults in the southeast to events of September 11: six months later. Issues Ment Health Nurs 2005;26:415–32.
   PubMedGoogle Scholar
• Revankar CM, Cimino DF, Sklar LA, et al. A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 2005;307:1625–30.
   PubMed Web of Science ®Google Scholar
• Booth EA, Obeid NR, Lucchesi BR. Activation of estrogen receptor-alpha protects the in vivo rabbit heart from ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 2005;289:H2039–47.
   PubMed Web of Science ®Google Scholar
• Huang C, Gu H, Wang Y, Wang M. Estrogen-induced SDF-1 production is mediated by estrogen receptor-alpha in female hearts after acute ischemia and reperfusion. Surgery 2011;150:197–203.
   PubMed Web of Science ®Google Scholar
• Hutchens MP, Fujiyoshi T, Komers R, et al. Estrogen protects renal endothelial barrier function from ischemia-reperfusion in vitro and in vivo. Am J Physiol Renal Physiol 2012;303:F377–F385.
   PubMed Web of Science ®Google Scholar
• Meyer MR, Prossnitz ER, M. Barton The G protein-coupled estrogen receptor GPER/GPR30 as a regulator of cardiovascular function. Vascul Pharmacol 2011;55:17–25.
   PubMed Web of Science ®Google Scholar
• Gunal O, Oktar BK, Ozcinar E, et al. Estradiol treatment ameliorates acetic acid-induced gastric and colonic injuries in rats. Inflammation 2003;27:351–359.
   PubMed Web of Science ®Google Scholar
• Kasimay O, Sener G, Cakir B, et al. Estrogen protects against oxidative multiorgan damage in rats with chronic renal failure. Ren Fail 2009;31:711–25.
   PubMed Web of Science ®Google Scholar
• Ozveri ES, Bozkurt A, Haklar G, et al. Estrogens ameliorate remote organ inflammation induced by burn injury in rats. Inflamm Res 2001;50:585–91.
   PubMed Web of Science ®Google Scholar
• Sener G, Arbak S, Kurtaran P, et al. Estrogen protects the liver and intestines against sepsis-induced injury in rats. J Surg Res 2005;128:70–8.
   PubMed Web of Science ®Google Scholar
• Kumral ZN, Memi G, Ercan F, Yegen BC. Estrogen alleviates acetic acid-induced gastric or colonic damage via both ERalpha- and ERbeta-mediated and direct antioxidant mechanisms in rats. Inflammation 2014;37:694–705.
   PubMed Web of Science ®Google Scholar
• Ploth DW. Angiotensin-dependent renal mechanisms in two-kidney, one-clip renal vascular hypertension. Am J Physiol 1983;245:F131–41.
   PubMed Web of Science ®Google Scholar
• Baradaran A, Nasri H, Rafieian-Kopaei M. Oxidative stress and hypertension: Possibility of hypertension therapy with antioxidants. J Res Med Sci 2014;19:358–67.
   PubMed Web of Science ®Google Scholar
• Goldblatt H, Lynch J, Hanzal RF, Summerville WW. Studies on experimental hypertension: I. The production of persistent elevation of systolic blood pressure by means of renal ischemia. J Exp Med 1934;59:347–79.
   PubMedGoogle Scholar
• Navar LG, Harrison-Bernard LM, Nishiyama A, Kobori H. Regulation of intrarenal angiotensin II in hypertension. Hypertension 2002;39:316–22.
   PubMed Web of Science ®Google Scholar
• Cevik O, Akpinar H, Oba R, et al. The effect of Momordica charantia intake on the estrogen receptors ESRalpha/ESRbeta gene levels and apoptosis on uterine tissue in ovariectomy rats. Mol Biol Rep 2015;42:167–77.
   PubMed Web of Science ®Google Scholar
• Sener G, Paskaloglu K, Toklu H, et al. Melatonin ameliorates chronic renal failure-induced oxidative organ damage in rats. J Pineal Res 2004;36:232–41.
   PubMed Web of Science ®Google Scholar
• Buege JA, Aust SD. Microsomal lipid peroxidation. Methods Enzymol 1978;52:302–310.
   PubMedGoogle Scholar
• Aykac G, Uysal M, Yalcin AS, et al. The effect of chronic ethanol ingestion on hepatic lipid peroxide, glutathione, glutathione peroxidase and glutathione transferase in rats. Toxicology 1985;36:71–6.
   PubMed Web of Science ®Google Scholar
• Bradley PP, Priebat DA, Christensen RD, Rothstein G. Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. J Invest Dermatol 1982;78:206–9.
   PubMed Web of Science ®Google Scholar
• Mylroie AA, Collins H, Umbles C, Kyle J. Erythrocyte superoxide dismutase activity and other parameters of copper status in rats ingesting lead acetate. Toxicol Appl Pharmacol 1986;82:512–520.
   PubMed Web of Science ®Google Scholar
• Aebi H. Catalase in vitro. Methods Enzymol 1984;105:121–6.
   PubMed Web of Science ®Google Scholar
• Taussky HH. A procedure increasing the specificity of the Jaffe reaction for the determination of creatine and creatinine in urine and plasma. Clin Chim Acta 1956;1:210–24.
   PubMed Web of Science ®Google Scholar
• Toklu HZ, Sehirli O, Ersahin M, et al. Resveratrol improves cardiovascular function and reduces oxidative organ damage in the renal, cardiovascular and cerebral tissues of two-kidney, one-clip hypertensive rats. J Pharm Pharmacol 2010;62:1784–93.
   PubMed Web of Science ®Google Scholar
• Kim YK, Lee SH, Goldinger JM, Hong SK. Effect of ethanol on organic ion transport in rabbit kidney. Toxicol Appl Pharmacol 1986;86:411–20.
   PubMed Web of Science ®Google Scholar
• Reading HW, Isbir T. The role of cation-activated ATPases in transmitter release from the rat iris. Q J Exp Physiol Cogn Med Sci 1980;65:105–16.
   PubMedGoogle Scholar
• Fiske CH, Subbarow Y. Phosphorus compounds of muscle and liver. Science 1929;70:381–382.
   PubMedGoogle Scholar
• Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265–75.
   PubMed Web of Science ®Google Scholar
• Conlon PJ, Little MA, Pieper K, Mark DB. Severity of renal vascular disease predicts mortality in patients undergoing coronary angiography. Kidney Int 2001;60:1490–1497.
   PubMed Web of Science ®Google Scholar
• Lerman LO, Textor SC, Grande JP. Mechanisms of tissue injury in renal artery stenosis: ischemia and beyond. Prog Cardiovasc Dis 2009;52:196–203.
   PubMed Web of Science ®Google Scholar
• Manjunath G, Tighiouart H, Ibrahim H, et al. Level of kidney function as a risk factor for atherosclerotic cardiovascular outcomes in the community. J Am Coll Cardiol 2003;41:47–55.
   PubMed Web of Science ®Google Scholar
• Higashi Y, Sasaki S, Nakagawa K, et al. Endothelial function and oxidative stress in renovascular hypertension. N Engl J Med 2002;346:1954–1962.
   PubMed Web of Science ®Google Scholar
• Oliveira-Sales EB, Dugaich AP, Carillo BA, et al. Oxidative stress contributes to renovascular hypertension. Am J Hypertens 2008;21:98–104.
   PubMed Web of Science ®Google Scholar
• Schnackenberg CG. Physiological and pathophysiological roles of oxygen radicals in the renal microvasculature. Am J Physiol Regul Integr Comp Physiol 2002;282:R335–R342.
   Google Scholar
• Cohuet G, Struijker-Boudier H. Mechanisms of target organ damage caused by hypertension: therapeutic potential. Pharmacol Ther 2006;111:81–98.
   PubMed Web of Science ®Google Scholar
• Swei A, Lacy F, Delano FA, et al. A mechanism of oxygen free radical production in the Dahl hypertensive rat. Microcirculation 1999;6:179–187.
   PubMed Web of Science ®Google Scholar
• Rappelli A. Hypertension and obesity after the menopause. J Hypertens Suppl 2002;20:S26–S28.
   Google Scholar
• Reckelhoff JF, Fortepiani LA. Novel mechanisms responsible for postmenopausal hypertension. Hypertension 2004;43:918–23.
   PubMed Web of Science ®Google Scholar
• Coylewright M, Reckelhoff JF, Ouyang P. Menopause and hypertension: an age-old debate. Hypertension 2008;51:952–959.
   PubMed Web of Science ®Google Scholar
• Schulman IH, Aranda P, Raij L, et al. Surgical menopause increases salt sensitivity of blood pressure. Hypertension 2006;47:1168–74.
   PubMed Web of Science ®Google Scholar
• Barp J, Sartorio CL, Campos C, et al. Influence of ovariectomy on cardiac oxidative stress in a renovascular hypertension model. Can J Physiol Pharmacol 2012;90:1229–34.
   PubMed Web of Science ®Google Scholar
• Maranon R, Reckelhoff JF. Sex and gender differences in control of blood pressure. Clin Sci (Lond) 2013;125:311–318.
   PubMed Web of Science ®Google Scholar
• Sandberg K, Ji H. Sex differences in primary hypertension. Biol Sex Differ 2012;3:7.
   PubMed Web of Science ®Google Scholar
• Chappell MC, Gallagher PE, Averill DB, et al. Estrogen or the AT1 antagonist olmesartan reverses the development of profound hypertension in the congenic mRen2. Lewis rat. Hypertension 2003;42:781–786.
   PubMedGoogle Scholar
• Wang H, Jessup JA, Lin MS, et al. Activation of GPR30 attenuates diastolic dysfunction and left ventricle remodelling in oophorectomized mRen2.Lewis rats. Cardiovasc Res 2012;94:96–104.
   PubMed Web of Science ®Google Scholar
• Effects of estrogen or estrogen/progestin regimens on heart disease risk factors in postmenopausal women. The Postmenopausal Estrogen/Progestin Interventions (PEPI) Trial. The Writing Group for the PEPI Trial. JAMA 1995;273:199–208.
   PubMed Web of Science ®Google Scholar
• Wassertheil-Smoller S, Anderson G, Psaty BM, et al. Hypertension and its treatment in postmenopausal women: baseline data from the Women’s Health Initiative. Hypertension 2000;36:780–789.
   PubMed Web of Science ®Google Scholar
• Caroccia B, Seccia TM, Campos AG, et al. GPER-1 and estrogen receptor-beta ligands modulate aldosterone synthesis. Endocrinology 2014;155:4296–304.
   PubMed Web of Science ®Google Scholar
• Shih CD. Activation of estrogen receptor beta-dependent nitric oxide signaling mediates the hypotensive effects of estrogen in the rostral ventrolateral medulla of anesthetized rats. J Biomed Sci 2009;16:60.
   PubMed Web of Science ®Google Scholar
• Pare G, Krust A, Karas RH, et al. Estrogen receptor-alpha mediates the protective effects of estrogen against vascular injury. Circ Res 2002;90:1087–92.
   PubMed Web of Science ®Google Scholar
• Zhu Y, Bian Z, Lu P, et al. Abnormal vascular function and hypertension in mice deficient in estrogen receptor beta. Science 2002;295:505–8.
   PubMed Web of Science ®Google Scholar
• Iafrati MD, Karas RH, Aronovitz M, et al. Estrogen inhibits the vascular injury response in estrogen receptor alpha-deficient mice. Nat Med 1997;3:545–8.
   PubMed Web of Science ®Google Scholar
• Karas RH, Hodgin JB, Kwoun M, et al. Estrogen inhibits the vascular injury response in estrogen receptor beta-deficient female mice. Proc Natl Acad Sci U S A 1999;96:15133–6.
   PubMed Web of Science ®Google Scholar
• Petrie WK, Dennis MK, Hu C, et al. G protein-coupled estrogen receptor-selective ligands modulate endometrial tumor growth. Obstet Gynecol Int 2013;2013:472720.
   PubMedGoogle Scholar
• Pijacka W, Clifford B, Tilburgs C, et al. Protective role of female gender in programmed accelerated renal aging in the rat. Physiological Reports. 2015;3(4):e12342.
   Google Scholar
• Chade AR, Rodriguez-Porcel M, Herrmann J, et al. Antioxidant intervention blunts renal injury in experimental renovascular disease. J Am Soc Nephrol 2004;15:958–66.
   PubMed Web of Science ®Google Scholar
• Dantas AP, Tostes RC, Fortes ZB, et al. In vivo evidence for antioxidant potential of estrogen in microvessels of female spontaneously hypertensive rats. Hypertension 2002;39:405–11.
   PubMed Web of Science ®Google Scholar
• Ji H, Menini S, Mok K, et al. Gonadal steroid regulation of renal injury in renal wrap hypertension. Am J Physiol Renal Physiol 2005;288:F513–20.
   Google Scholar
• Mankhey RW, Bhatti F, Maric C. 17beta-Estradiol replacement improves renal function and pathology associated with diabetic nephropathy. Am J Physiol Renal Physiol 2005;288:F399–405.
   PubMed Web of Science ®Google Scholar
• Hutchens MP, Nakano T, Kosaka Y, et al. Estrogen is renoprotective via a nonreceptor-dependent mechanism after cardiac arrest in vivo. Anesthesiology 2010;112:395–405.
   PubMed Web of Science ®Google Scholar
• Brown NJ, Abbas A, Byrne D, et al. Comparative effects of estrogen and angiotensin-converting enzyme inhibition on plasminogen activator inhibitor-1 in healthy postmenopausal women. Circulation 2002–22;105:304–9.
   PubMed Web of Science ®Google Scholar