Myocardial ischemia-reperfusion injury in estrogen receptor-α knockout and wild-type mice

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 278, Issue 5 47-5, 2000, Pages

  Zhai, Peiyong ^a   Eurell, Thomas E ^a   Cooke, Paul S ^a   Lubahn, Dennis B ^b   Gross, David R ^a,c  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

^c 3516 VMBS Bldg ^*  (United States)

Author keywords

Calcium; Mitochondrial function; Myocardial ultrastructure; Nitric oxide

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; CALCIUM; ESTROGEN RECEPTOR ALPHA; NITRITE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORONARY ARTERY BLOOD FLOW; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HEART VENTRICLE FIBRILLATION; KNOCKOUT MOUSE; MALE; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; TACHYCARDIA;

EID: 0034084149     PISSN: 03636135     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpheart.2000.278.5.h1640     Document Type: Article

References (56)

1. Arnal JF, Clamens S, Pechet C, Negre-Salvayre A, Allera C, Girolami JP, Salvayre R, and Bayard F. Ethinylestradiol does not enhance the expression of nitric oxide synthase in bovine endothelial cells but does increase the release of bioactive nitric oxide by inhibiting superoxide anion production. Proc Natl Acad Sci USA 93: 4108-4113, 1996.
2. Arroyo CM, Kramer JH, Dickens BF, and Welglicki WB. Identification of free radicals in myocardial ischemia/reperfusion by spin trapping with nitrone DMPO. FEBS Lett 221: 101-104, 1987.
3. Baulieu E-E and Mester J. Steroid hormone receptors. In: Endocrinology (2nd ed), edited by DeGroot LJ, Besser GM, Cahill GF Jr, Marshal JC, Nelson DH, Odell WD, Potts JT Jr, Rubenstein AH, and Steinberger E. Philadelphia, PA: Saunders, 1989, 16-39.
4. Berger F, Borchard U, Hafner D, Putz I, and Weis TM. Effects of 17 beta-estradiol on action potential and ionic currents in male rat ventricular myocytes. Naunyn Schmiedebergs Arch Pharmacol 356: 788-796, 1997.
5. Blough NV and Zafiriou OC. Reaction of superoxide with nitric oxide to form peroxonitrite in alkaline aqueous solution. Inorg Chem 24: 3502-3504, 1985.
6. Bolli R, Patel BS, Jeroudi MO, Lai EK, and McCay PB. Demonstration of free radical generation in "stunned" myocardium of intact dogs with the use of the spin trap α-phenyl N-tert-butyl nitrone. J Clin Invest 82: 476-485, 1988.
7. 2+ exchange increases susceptibility to ischemia/reperfusion injury in male, not in female, transgenic mice. Circ Res 83: 1215-1223, 1998.
8. Delyani JA, Murohara T, Nossuli TO, and Lefer AM. Protection from myocardial reperfusion injury by acute administration of 17 β-estradiol. J Mol Cell Cardiol 28: 1001-1008, 1996.
9. Engelman DT, Watanabe M, Engelman RM, Rousou JA, Flack JE III, Deaton DN, and Das DK. Constitutive nitric oxide release is impaired after ischemia and reperfusion. J Thorac Cardiovasc Surg 110: 1047-1053, 1995.
10. Garlick PB, Davies MJ, Hearse DJ, and Slater TF. Direct detection of free radicals in the reperfused rat heart using electron spin resonance spectroscopy. Circ Res 61: 757-760, 1987.
11. Gilad E, Zingarelli B, Salzman AL, and Szabo C. Protection by inhibition of poly (ADP-ribose) synthetase against oxidant injury in cardiac myoblasts in vitro. J Mol Cell Cardiol 29: 2585-2597, 1997.
12. Grohe C, Kahlert S, Lobbert K, and Vetter H. Expression of oestrogen receptor a and β in rat heart: role of local oestrogen synthesis. J Endocrinol 156: R1-R7, 1997.
13. Hajashi T, Yamada K, Esaki T, Kuzuya M, Satake S, Ishikawa T, Hidaka H, and Iguchi A. Estrogen increases endothelial nitric oxide by a receptor-mediated system. Biochem Biophys Res Commun 214: 847-855, 1995.
14. Hale SL, Birnbaum Y, and Kloner RA. β-Estradiol, but not α-estradiol, reduced myocardial necrosis in rabbits after ischemia and reperfusion. Am Heart J 132: 258-262, 1996.
15. Hilakivi-Clarke L, Raygada M, and Cho E. Serum estradiol levels and ethanol-induced aggression. Pharmacol Biochem Behav 58: 785-791, 1997.
16. Hiramatsu T, Forbess JM, Miura T, and Mayer JE Jr. Effects of L-arginine and L-nitro-arginine methyl ester on recovery of neonatal lamb hearts after cold ischemia: evidence for an important role of endothelial production of nitric oxide. J Thorac Cardiovasc Surg 109: 81-87, 1995.
17. Itkonen P and Collan Y. Mitochondrial flocculent densities in ischemia, digestion experiments. Acta Pathol Microbiol Immunol Scand 91: 463-468, 1983.
18. 2+ in guinea pig isolated cardiac myocytes. Br J Pharmacol 106: 739-745, 1992.
19. Johnson BD, Zheng W, Korach KS, Scheuer T, Catterall WA, and Rubanyi GM. Increased expression of the cardiac L-type calcium channel in estrogen receptor-deficient mice. J Gen Physiol 110: 135-140, 1997.
20. Kauser K and Rubanyi GM. Potential cellular signaling mechanisms mediating upregulation of endothelial nitric oxide production by estrogen. J Vasc Res 34: 229-236, 1997.
21. Kim YD, Chen B, Bearegard J, Kouretas P, Thomas G, Farhat MY, Myers AK, and Lees DE. 17β-Estradiol prevents dysfunction of canine coronary endothelium and myocardium and reperfusion arrhythmias after brief ischemia/reperfusion. Circulation 94: 2901-2908, 1996.
22. Kim-Schulze S, McGowan KA, Hubchak SC, Cid MC, Martin MB, Kleinman HK, Greene GL, and Schnaper HW. Expression of an estrogen receptor by human coronary artery and umbilical vein endothelial cells. Circulation 94: 1402-1407, 1996.
23. Kloner RA, Ganote CE, Whaler D, and Jennings RB. Effect of a transient period of ischemia on myocardiac cells. II. Fine structure during the first few minutes of reflow. Am J Pathol 74: 399-442, 1974.
24. Kolodgie FD, Farb A, Litovsky SH, Narula J, Jeffers LA, Lee SJ, and Virmani R. Myocardial protection of contractile function after global ischemia by physiologic estrogen replacement in the ovariectomized rat. J Mol Cell Cardiol 29: 2403-2414, 1997.
25. Kuiper GGJM, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, and Gustafsson J-A. Comparison of the ligand binding specificity and transcript tissue distributions of estrogen receptors a and β. Endocrinology 138: 863-870, 1997.
26. Kuiper GGJM, and Gustafsson J-A. The novel estrogen receptor-β subtype: potential role in the cell- and promoter-specific actions of estrogens and anti-estrogens. FEBS Lett 410: 87-90, 1997.
27. Lefer AM and Lefer DJ. Pharmacology of the endothelium in ischemia/reperfusion and circulatory shock. Annu Rev Pharmacol Toxicol 33: 71-90, 1993.
28. Lefer DJ. Myocardial protective actions of nitric oxide donors after myocardial ischemia and reperfusion. New Horiz 3: 105-112, 1995.
29. Lie JT, Holley KE, and Titus JL. Fuchsinorrhagia - A new histochemical indication of inapparant early myocardial ischemia. Lab Med. 3: 37-40, 1972.
30. Liu Y, Peterson DA, Kimura H, and Schubert D. Mechanism of cellular 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) reduction. J Neurochem 69: 581-593, 1997.
31. Liu Y and Schukert D. Cytotoxic amyloid peptides inhibit cellular 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) reduction by enhancing MTT formazan exocytosis. J Neurochem 69: 2285-2293, 1997.
32. Losordo DW, Kearney M, Kim EA, Jekanowski J, and Isner JM. Variable expression of the estrogen receptor in normal and atherosclerotic coronary arteries of premenopausal women. Circulation 89: 1501-1510, 1994.
33. Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS, and Smithies O. 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, 1993.
34. Madesh M, Bhaskar L, and Balasubramanian KA. Enterocyte viability and mitochondrial function after graded intestinal ischemia and reperfusion in rats. Mol Cell Biochem 167: 81-87, 1997.
35. Maxwell SRJ. Women and heart disease. Basic Res Cardiol 93, Suppl 2: 79-84, 1993.
36. McCord JM. Oxygen-derived free radicals in post ischemic tissue injury. N Engl J Med 312: 159-163, 1985.
37. Node K, Kitakaze M, Kosaka H, Minamino T, Funaya H, and Hori M. Amelioration of ischemia- and reperfusion-induced myocardial injury by 17β-estradiol. Role of nitric oxide and calcium-activated potassium channels. Circulation 96: 1953-1963, 1997.
38. Nozik-Grayck E, Piantadosi CA, Adelsberg JV, Alper SL, and Huang Y-CT. Protection of perfused lung from oxidant injury by inhibitors of anion exchange. Am J Physiol Lung Cell Mol Physiol 273: L296-L304, 1997.
39. Overpeck JG, Sylvia CH, Hohmann JR, Applestine MS, and Reilly JF. Concentrations of circulating steroids in normal prepubertal and adult male and female humans, chimpanzees, rhesus monkeys, rats, mice, and hamsters: a literature survey. J Toxicol Environ Health 4: 785-803, 1978.
40. Pabla R, Buda AJ, Flynn DM, Salzberg DB, and Lefer DJ. Intracoronary nitric oxide improves postischemic coronary blood flow and myocardial contractile function. Am J Physiol Heart Circ Physiol 269: H1113-H1121, 1995.
41. Paech K, Webb P, Kuiper GGJM, Nilsson S, Gustufsson J-A, Kushner PJ, and Scanlan TS. Differential ligand activation of estrogen receptors ERa and ERβ at AP1 sites. Science 277: 1508-1510, 1997.
42. + exchanger. Am J Physiol Heart Circ Physiol 276: H1581-H1590, 1999.
43. 2+-chelating agents. J Mol Cell Cardiol 9: 897-908, 1977.
44. Phillips GB, Yano K, and Stemmermann GN. Serum sex hormone levels and myocardial infarction in the Honolulu Heart Program. Pitfalls in perspective studies on sex hormones. J Clin Epidemiol 41: 1151-1156, 1988.
45. Register TC and Adams MR. Coronary artery and cultured aortic smooth muscle cells express mRNA for both the classical estrogen receptor and the newly described estrogen receptor-β. J Steroid Biochem Mol Biol 64: 187-191, 1998.
46. Rubanyi GM, Freay AD, Kauser K, Sukovich D, Burton G, Lubahn DB, Couse JF, Curtis SW, and Korach KS. Vascular estrogen receptors and endothelium-derived nitric oxide production in the mouse aorta. Gender differences and effect of estrogen receptor gene disruption. J Clin Invest 99: 2429-2437, 1997.
47. Sato H, Zhao Z-Q, McGee DS, Williams MW, Hammon JW, Jr, and Vinten-Johansen J. Supplemental L-arginine during cardioplegic arrest and reperfusion avoids regional postischemic injury. J Thorac Cardiovasc Surg 110: 302-314, 1995.
48. Schaper J, Heherlein F, Schlepper M, and Thiedemann K-U. Ultrastructural alterations during ischemia and reperfusion in human hearts during cardiac surgery. J Mol Cell Cardiol 9: 175-189, 1977.
49. Slater TF, Sawyer B, and Strauli U. Studies on succinatetetrazolium reductase systems. III. Points of coupling of four different tetrazolium salts. Biochem Biophys Acta 77: 383-393, 1963.
50. Stampfer MJ, Colditz GA, Willett WC, Manson JE, Rosner B, Speizer FE, and Hennekens CH. Postmenopausal estrogen therapy and cardiovascular disease. Ten-year follow-up from the nurses' health study. N Engl J Med 325: 756-762, 1991.
51. Sudhir K, Chou TM, Messina LM, Hutchison SJ, Korack KS, Chatterjee K, and Rubanyi GM. Endothelial dysfunction in a man with disruptive mutation in oestrogen-receptor gene. Lancet 349: 1146-1147, 1997.
52. Sudhir K, Chou TM, Chatterjee K, Smith EP, Williams TC, Kane JP, Malloy MJ, Korach KS, and Rubanyi GM. Premature coronary disease associated with a disruptive mutation in the estrogen receptor gene in a man. Circulation 96: 3774-3777, 1997.
53. 2+ overload in reperfused ischemic myocardium. Annu Rev Physiol 52: 543-559, 1990.
54. Tsao PS, Aoki N, Lefer DJ, Johnson G, and Lefer AM. Time course of endothelial dysfunction and myocardial injury during myocardial ischemia and reperfusion in cat. Circulation 82: 1402-1412, 1990.
55. Vinten-Johansen J and Hammon JW. Myocardial protection during cardiac surgery. In: Cardiopulmonary Bypass: Principles and Practice, edited by Gravlee, GP, Davis RF, and Urley JR. Baltimore, MD: Williams and Wilkins, 1993, p. 158-195.
56. Zweier JL, Flaherty JT, and Weisfeldt ML. Direct measurement of free radical generation following reperfusion of ischemic myocardium. Proc Natl Acad Sci USA 84: 1404-1407, 1987.