Gender-based differences in mechanisms of protection in myocardial ischemia-reperfusion injury

Cardiovascular Research

Volumn 75, Issue 3, 2007, Pages 478-486

  Murphy, Elizabeth ^a   Steenbergen, Charles ^b  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b DEPARTMENT OF PATHOLOGY   (United States)

Author keywords

Calcium; Estrogen; Ischemia; Receptors; Signal transduction

Indexed keywords

CALCIUM CHANNEL L TYPE; ESTROGEN; ESTROGEN RECEPTOR; HEAT SHOCK PROTEIN; NITRIC OXIDE SYNTHASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHOSPHATIDYLINOSITOL 3 KINASE; PROSTAGLANDIN D2;

CALCIUM CELL LEVEL; ENZYME ACTIVATION; ENZYME METABOLISM; FEMALE; GENE EXPRESSION; HEART CONTRACTION; HEART HYPERTROPHY; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HUMAN; MALE; NITROSYLATION; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; SEX DIFFERENCE; SIGNAL TRANSDUCTION;

ANIMALS; CARDIOMEGALY; ESTROGENS; FEMALE; HUMANS; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MALE; MYOCARDIAL CONTRACTION; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; RECEPTORS, ESTROGEN; SEX CHARACTERISTICS;

EID: 34447517169     PISSN: 00086363     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cardiores.2007.03.025     Document Type: Review

References (86)

1. Barrett-Connor E. Sex differences in coronary heart disease. Why are women so superior? The 1995 Ancel Keys Lecture. Circulation 95 (1997) 252-264
2. Crabbe D.L., Dipla K., Ambati S., Zafeiridis A., Gaughan J.P., Houser S.R., et al. Gender differences in post-infarction hypertrophy in end-stage failing hearts. J Am Coll Cardiol 41 (2003) 300-306
3. Hayward C.S., Kelly R.P., and Collins P. The roles of gender, the menopause and hormone replacement on cardiovascular function. Cardiovasc Res 46 (2000) 28-49
4. Rossouw J.E., Anderson G.L., Prentice R.L., LaCroix A.Z., Kooperberg C., Stefanick M.L., et al. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women's Health Initiative randomized controlled trial. JAMA 288 (2002) 321-333
5. Jacobs A.K. Coronary revascularization in women in 2003: sex revisited. Circulation 107 (2003) 375-377
6. Jacobs A.K., Johnston J.M., Haviland A., Brooks M.M., Kelsey S.F., Holmes Jr. D.R., et al. Improved outcomes for women undergoing contemporary percutaneous coronary intervention: a report from the National Heart, Lung, and Blood Institute Dynamic registry. J Am Coll Cardiol 39 (2002) 1608-1614
7. Berger J.S., Sanborn T.A., Sherman W., and Brown D.L. Influence of sex on in-hospital outcomes and long-term survival after contemporary percutaneous coronary intervention. Am Heart J 151 (2006) 1026-1031
8. Mehilli J., Kastrati A., Dirschinger J., Bollwein H., Neumann F.J., and Schomig A. Differences in prognostic factors and outcomes between women and men undergoing coronary artery stenting. JAMA 284 (2000) 1799-1805
9. Mehilli J., Ndrepepa G., Kastrati A., Nekolla S.G., Markwardt C., Bollwein H., et al. Gender and myocardial salvage after reperfusion treatment in acute myocardial infarction. J Am Coll Cardiol 45 (2005) 828-831
10. Kelsey S.F., James M., Holubkov A.L., Holubkov R., Cowley M.J., and Detre K.M. Results of percutaneous transluminal coronary angioplasty in women. 1985-1986 National Heart, Lung, and Blood Institute's Coronary Angioplasty Registry. Circulation 87 (1993) 720-727
11. Peter I., Shearman A.M., Vasan R.S., Zucker D.R., Schmid C.H., Demissie S., et al. Association of estrogen receptor beta gene polymorphisms with left ventricular mass and wall thickness in women. Am J Hypertens 18 (2005) 1388-1395
12. Fox C.S., Yang Q., Cupples L.A., Guo C.Y., Atwood L.D., Murabito J.M., et al. Sex-specific association between estrogen receptor-alpha gene variation and measures of adiposity: the Framingham Heart Study. J Clin Endocrinol Metab 90 (2005) 6257-6262
13. Shearman A.M., Cooper J.A., Kotwinski P.J., Miller G.J., Humphries S.E., Ardlie K.G., et al. Estrogen receptor alpha gene variation is associated with risk of myocardial infarction in more than seven thousand men from five cohorts. Circ Res 98 (2006) 590-592
14. Newton-Cheh C., and O'Donnell C.J. Sex differences and genetic associations with myocardial infarction. JAMA 291 (2004) 3008-3010
15. Schuit S.C., de Jong F.H., Stolk L., Koek W.N., van Meurs J.B., Schoofs M.W., et al. Estrogen receptor alpha gene polymorphisms are associated with estradiol levels in postmenopausal women. Eur J Endocrinol 153 (2005) 327-334
16. Bae S., and Zhang L. Gender differences in cardioprotection against ischemia/reperfusion injury in adult rat hearts: focus on Akt and protein kinase C signaling. J Pharmacol Exp Ther 315 (2005) 1125-1135
17. Wang M., Crisostomo P., Wairiuko G.M., and Meldrum D.R. Estrogen receptor-alpha mediates acute myocardial protection in females. Am J Physiol Heart Circ Physiol 290 (2006) H2204-H2209
18. Przyklenk K., Ovize M., Bauer B., and Kloner R.A. Gender does not influence acute myocardial infarction in adult dogs. Am Heart J 129 (1995) 1108-1113
19. Li Y., and Kloner R.A. Is there a gender difference in infarct size and arrhythmias following experimental coronary occlusion and reperfusion?. J Thromb Thrombolysis 2 (1995) 221-225
20. Cross H.R., Lu L., Steenbergen C., Philipson K.D., and Murphy E. Overexpression of the cardiac Na+/Ca2+ exchanger increases susceptibility to ischemia/reperfusion injury in male, but not female, transgenic mice. Circ Res 83 (1998) 1215-1223
21. Gabel S.A., Walker V.R., London R.E., Steenbergen C., Korach K.S., and Murphy E. Estrogen receptor beta mediates gender differences in ischemia/reperfusion injury. J Mol Cell Cardiol 38 (2005) 289-297
22. Cross H.R., Kranias E.G., Murphy E., and Steenbergen C. Ablation of PLB exacerbates ischemic injury to a lesser extent in female than male mice: protective role of NO. Am J Physiol Heart Circ Physiol 284 (2003) H683-H690
23. Cross H.R., Steenbergen C., Lefkowitz R.J., Koch W.J., and Murphy E. Overexpression of the cardiac beta(2)-adrenergic receptor and expression of a beta-adrenergic receptor kinase-1 (betaARK1) inhibitor both increase myocardial contractility but have differential effects on susceptibility to ischemic injury. Circ Res 85 (1999) 1077-1084
24. Cross H.R., Murphy E., and Steenbergen C. Ca(2+) loading and adrenergic stimulation reveal male/female differences in susceptibility to ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 283 (2002) H481-H489
25. Kam K.W., Qi J.S., Chen M., and Wong T.M. Estrogen reduces cardiac injury and expression of beta1-adrenoceptor upon ischemic insult in the rat heart. J Pharmacol Exp Ther 309 (2004) 8-15
26. Chen J., Petranka J., Yamamura K., London R.E., Steenbergen C., and Murphy E. Gender differences in sarcoplasmic reticulum calcium loading after isoproterenol. Am J Physiol Heart Circ Physiol 285 (2003) H2657-H2662
27. Simoncini T., Hafezi-Moghadam A., Brazil D.P., Ley K., Chin W.W., and Liao J.K. Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature 407 (2000) 538-541
28. Sugishita K., Su Z., Li F., Philipson K.D., and Barry W.H. Gender influences [Ca(2+)](i) during metabolic inhibition in myocytes overexpressing the Na(+)-Ca(2+) exchanger. Circulation 104 (2001) 2101-2106
29. Curl C.L., Wendt I.R., and Kotsanas G. Effects of gender on intracellular [Ca] in rat cardiac myocytes. Pflugers Arch 441 (2001) 709-716
30. Steenbergen C., Murphy E., Levy L., and London R.E. Elevation in cytosolic free calcium concentration early in myocardial ischemia in perfused rat heart. Circ Res 60 (1987) 700-707
31. Murphy E., Perlman M., London R.E., and Steenbergen C. Amiloride delays the ischemia-induced rise in cytosolic free calcium. Circ Res 68 (1991) 1250-1258
32. Baines C.P., Kaiser R.A., Purcell N.H., Blair N.S., Osinska H., Hambleton M.A., et al. Loss of cyclophilin d reveals a critical role for mitochondrial permeability transition in cell death. Nature 434 (2005) 658-662
33. Piper H.M., Meuter K., and Schafer C. Cellular mechanisms of ischemia-reperfusion injury. Ann Thorac Surg 75 (2003) S644-S648
34. Nuedling S., Karas R.H., Mendelsohn M.E., Katzenellenbogen J.A., Katzenellenbogen B.S., Meyer R., et al. Activation of estrogen receptor beta is a prerequisite for estrogen-dependent upregulation of nitric oxide synthases in neonatal rat cardiac myocytes. FEBS Lett 502 (2001) 103-108
35. Sun J., Picht E., Ginsburg K.S., Bers D.M., Steenbergen C., and Murphy E. Hypercontractile female hearts exhibit increased S-nitrosylation of the L-type Ca2+ channel alpha1 subunit and reduced ischemia/reperfusion injury. Circ Res 98 (2006) 403-411
36. Cross H.R., Murphy E., Koch W.J., and Steenbergen C. Male and female mice overexpressing the beta(2)-adrenergic receptor exhibit differences in ischemia/reperfusion injury: role of nitric oxide. Cardiovasc Res 53 (2002) 662-671
37. Booth E.A., Obeid N.R., and Lucchesi B.R. Activation of estrogen receptor-alpha protects the in vivo rabbit heart from ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 289 (2005) H2039-H2047
38. Das B., and Sarkar C. Similarities between ischemic preconditioning and 17beta-estradiol mediated cardiomyocyte KATP channel activation leading to cardioprotective and antiarrhythmic effects during ischemia/reperfusion in the intact rabbit heart. J Cardiovasc Pharmacol 47 (2006) 277-286
39. Booth E.A., Marchesi M., Kilbourne E.J., and Lucchesi B.R. 17Beta-estradiol as a receptor-mediated cardioprotective agent. J Pharmacol Exp Ther 307 (2003) 395-401
40. Sbarouni E., Iliodromitis E.K., Bofilis E., Kyriakides Z.S., and Kremastinos D.T. Short-term estrogen reduces myocardial infarct size in oophorectomized female rabbits in a dose-dependent manner. Cardiovasc Drugs Ther 12 (1998) 457-462
41. Lee T.M., Lin M.S., Chou T.F., Tsai C.H., and Chang N.C. Adjunctive 17beta-estradiol administration reduces infarct size by altered expression of canine myocardial connexin43 protein. Cardiovasc Res 63 (2004) 109-117
42. Kanno S., Kovacs A., Yamada K.A., and Saffitz J.E. Connexin43 as a determinant of myocardial infarct size following coronary occlusion in mice. J Am Coll Cardiol 41 (2003) 681-686
43. Li X., Heinzel F.R., Boengler K., Schulz R., and Heusch G. Role of connexin 43 in ischemic preconditioning does not involve intercellular communication through gap junctions. J Mol Cell Cardiol 36 (2004) 161-163
44. Boengler K., Dodoni G., Rodriguez-Sinovas A., Cabestrero A., Ruiz-Meana M., Gres P., et al. Connexin 43 in cardiomyocyte mitochondria and its increase by ischemic preconditioning. Cardiovasc Res 67 (2005) 234-244
45. Boengler K., Konietzka I., Buechert A., Heinen Y., Garcia-Dorado D., Heusch G., et al. Loss of ischemic preconditioning's cardioprotection in aged mouse hearts is associated with reduced gap junctional and mitochondrial levels of connexin 43. Am J Physiol Heart Circ Physiol 292 (2007) H1764-H1769 [Electronic publication ahead of print]
46. Sullivan Jr. T.R., Karas R.H., Aronovitz M., Faller G.T., Ziar J.P., Smith J.J., et al. Estrogen inhibits the response-to-injury in a mouse carotid artery model. J Clin Invest 96 (1995) 2482-2488
47. Bologa C.G., Revankar C.M., Young S.M., Edwards B.S., Arterburn J.B., Kiselyov A.S., et al. Virtual and biomolecular screening converge on a selective agonist for GPR30. Nat Chem Biol 2 (2006) 207-212
48. Kuiper G.G., Lemmen J.G., Carlsson B., Corton J.C., Safe S.H., van der Saag P.T., et al. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139 (1998) 4252-4263
49. Filardo E.J. Epidermal growth factor receptor (EGFR) transactivation by estrogen via the G-protein-coupled receptor, GPR30: a novel signaling pathway with potential significance for breast cancer. J Steroid Biochem Mol Biol 80 (2002) 231-238
50. Pedram A., Razandi M., and Levin E.R. Nature of functional estrogen receptors at the plasma membrane. Mol Endocrinol 20 (2006) 1996-2009
51. Warner M., and Gustafsson J.A. Nongenomic effects of estrogen: why all the uncertainty?. Steroids 71 (2006) 91-95
52. Revankar C.M., Cimino D.F., Sklar L.A., Arterburn J.B., and Prossnitz E.R. A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 307 (2005) 1625-1630
53. Filardo E.J., and Thomas P. GPR30: a seven-transmembrane-spanning estrogen receptor that triggers EGF release. Trends Endocrinol Metab 16 (2005) 362-367
54. Medunjanin S., Hermani A., De Servi B., Grisouard J., Rincke G., and Mayer D. Glycogen synthase kinase-3 interacts with and phosphorylates estrogen receptor alpha and is involved in the regulation of receptor activity. J Biol Chem 280 (2005) 33006-33014
55. Garban H.J., Marquez-Garban D.C., Pietras R.J., and Ignarro L.J. Rapid nitric oxide-mediated S-nitrosylation of estrogen receptor: regulation of estrogen-dependent gene transcription. Proc Natl Acad Sci U S A 102 (2005) 2632-2636
56. Chen Y.X., Du J.T., Zhou L.X., Liu X.H., Zhao Y.F., Nakanishi H., et al. Alternative O-GlcNAcylation/O-phosphorylation of Ser16 induce different conformational disturbances to the N terminus of murine estrogen receptor beta. Chem Biol 13 (2006) 937-944
57. Yang S.H., Liu R., Perez E.J., Wen Y., Stevens Jr. S.M., Valencia T., et al. Mitochondrial localization of estrogen receptor beta. Proc Natl Acad Sci U S A 101 (2004) 4130-4135
58. Schwend T., and Gustafsson J.A. False positives in MALDI-TOF detection of ERbeta in mitochondria. Biochem Biophys Res Commun 343 (2006) 707-711
59. Pedram A., Razandi M., Wallace D.C., and Levin E.R. Functional estrogen receptors in the mitochondria of breast cancer cells. Mol Biol Cell 17 (2006) 2125-2137
60. Parkash J., Felty Q., and Roy D. Estrogen exerts a spatial and temporal influence on reactive oxygen species generation that precedes calcium uptake in high-capacity mitochondria: implications for rapid nongenomic signaling of cell growth. Biochemistry 45 (2006) 2872-2881
61. Lobaton C.D., Vay L., Hernandez-Sanmiguel E., Santodomingo J., Moreno A., Montero M., et al. Modulation of mitochondrial Ca(2+) uptake by estrogen receptor agonists and antagonists. Br J Pharmacol 145 (2005) 862-871
62. Pelzer T., Loza P.A., Hu K., Bayer B., Dienesch C., Calvillo L., et al. Increased mortality and aggravation of heart failure in estrogen receptor-beta knockout mice after myocardial infarction. Circulation 111 (2005) 1492-1498
63. Zhai P., Eurell T.E., Cooke P.S., Lubahn D.B., and Gross D.R. Myocardial ischemia-reperfusion injury in estrogen receptor-alpha knockout and wild-type mice. Am J Physiol Heart Circ Physiol 278 (2000) H1640-H1647
64. Skavdahl M., Steenbergen C., Clark J., Myers P., Demianenko T., Mao L., et al. Estrogen receptor-beta mediates male-female differences in the development of pressure overload hypertrophy. Am J Physiol Heart Circ Physiol 288 (2005) H469-H476
65. Babiker F.A., Lips D., Meyer R., Delvaux E., Zandberg P., Janssen B., et al. Estrogen receptor beta protects the murine heart against left ventricular hypertrophy. Arterioscler Thromb Vasc Biol 26 (2006) 1524-1530
66. Yu H.P., Shimizu T., Choudhry M.A., Hsieh Y.C., Suzuki T., Bland K.I., et al. Mechanism of cardioprotection following trauma-hemorrhagic shock by a selective estrogen receptor-beta agonist: up-regulation of cardiac heat shock factor-1 and heat shock proteins. J Mol Cell Cardiol 40 (2006) 185-194
67. Hsieh Y.C., Choudhry M.A., Yu H.P., Shimizu T., Yang S., Suzuki T., et al. Inhibition of cardiac PGC-1alpha expression abolishes ERbeta agonist-mediated cardioprotection following trauma-hemorrhage. FASEB J 20 (2006) 1109-1117
68. van Eickels M., Grohe C., Cleutjens J.P., Janssen B.J., Wellens H.J., and Doevendans P.A. 17beta-estradiol attenuates the development of pressure-overload hypertrophy. Circulation 104 (2001) 1419-1423
69. Olsson M.C., Palmer B.M., Leinwand L.A., and Moore R.L. Gender and aging in a transgenic mouse model of hypertrophic cardiomyopathy. Am J Physiol Heart Circ Physiol 280 (2001) H1136-H1144
70. Kadokami T., McTiernan C.F., Kubota T., Frye C.S., and Feldman A.M. Sex-related survival differences in murine cardiomyopathy are associated with differences in TNF-receptor expression. J Clin Invest 106 (2000) 589-597
71. Dash R., Schmidt A.G., Pathak A., Gerst M.J., Biniakiewicz D., Kadambi V.J., et al. Differential regulation of p38 mitogen-activated protein kinase mediates gender-dependent catecholamine-induced hypertrophy. Cardiovasc Res 57 (2003) 704-714
72. Jazbutyte V., Hu K., Kruchten P., Bey E., Maier S.K., Fritzemeier K.H., et al. Aging reduces the efficacy of estrogen substitution to attenuate cardiac hypertrophy in female spontaneously hypertensive rats. Hypertension 48 (2006) 579-586
73. Otsuki M., Gao H., Dahlman-Wright K., Ohlsson C., Eguchi N., Urade Y., et al. Specific regulation of lipocalin-type prostaglandin d synthase in mouse heart by estrogen receptor beta. Mol Endocrinol 17 (2003) 1844-1855
74. Too C.K., Giles A., and Wilkinson M. Estrogen stimulates expression of adenine nucleotide translocator ANT1 messenger RNA in female rat hearts. Mol Cell Endocrinol 150 (1999) 161-167
75. Stirone C., Duckles S.P., Krause D.N., and Procaccio V. Estrogen increases mitochondrial efficiency and reduces oxidative stress in cerebral blood vessels. Mol Pharmacol 68 (2005) 959-965
76. Justo R., Boada J., Frontera M., Oliver J., Bermudez J., and Gianotti M. Gender dimorphism in rat liver mitochondrial oxidative metabolism and biogenesis. Am J Physiol Cell Physiol 289 (2005) C372-C378
77. Chen J.Q., Yager J.D., and Russo J. Regulation of mitochondrial respiratory chain structure and function by estrogens/estrogen receptors and potential physiological/pathophysiological implications. Biochim Biophys Acta 1746 (2005) 1-17
78. Kim Y.D., Chen B., Beauregard J., Kouretas P., Thomas G., Farhat M.Y., et al. 17 beta-Estradiol prevents dysfunction of canine coronary endothelium and myocardium and reperfusion arrhythmias after brief ischemia/reperfusion. Circulation 94 (1996) 2901-2908
79. Dantas A.P., Tostes R.C., Fortes Z.B., Costa S.G., Nigro D., and Carvalho M.H. In vivo evidence for antioxidant potential of estrogen in microvessels of female spontaneously hypertensive rats. Hypertension 39 (2002) 405-411
80. Nikolic I., Liu D., Bell J., Collins J., Steenbergen C., and Murphy E. Treatment with an estrogen receptor-beta-selective agonist is cardioprotective. J Mol Cell Cardiol 42 (2007) 769-780
81. Jovanovic S., Jovanovic A., Shen W.K., and Terzic A. Low concentrations of 17beta-estradiol protect single cardiac cells against metabolic stress-induced Ca2+ loading. J Am Coll Cardiol 36 (2000) 948-952
82. Lindberg M.K., Moverare S., Skrtic S., Gao H., Dahlman-Wright K., Gustafsson J.A., et al. Estrogen receptor (ER)-beta reduces ERalpha-regulated gene transcription, supporting a "ying yang" relationship between ERalpha and ERbeta in mice. Mol Endocrinol 17 (2003) 203-208
83. Abdallah Y., Gkatzoflia A., Gligorievski D., Kasseckert S., Euler G., Schluter K.D., et al. Insulin protects cardiomyocytes against reoxygenation-induced hypercontracture by a survival pathway targeting SR Ca2+ storage. Cardiovasc Res 70 (2006) 346-353
84. Costa A.D., Garlid K.D., West I.C., Lincoln T.M., Downey J.M., Cohen M.V., et al. Protein kinase G transmits the cardioprotective signal from cytosol to mitochondria. Circ Res 97 (2005) 329-336
85. Burwell L.S., Nadtochiy S.M., Tompkins A.J., Young S., and Brookes P.S. Direct evidence for S-nitrosylation of mitochondrial complex I. Biochem J 394 (2006) 627-634
86. Shiva S., Huang Z., Grubina R., Sun J., Ringwood L.A., and Macarthur P.H. Deoxymyoglobin is a nitrite reductase that generates nitric oxide and regulates mitochondrial respiration. Circ Res 100 (2007) 654-661