Sex differences in animal models for cardiovascular diseases and the role of estrogen

Handbook of Experimental Pharmacology

Volumn 214, Issue , 2012, Pages 23-48

  Mahmoodzadeh, S ^a   Fliegner, D ^a   Dworatzek, E ^a  

^a DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

Author keywords

Animal model; Estrogen; Estrogen receptor; Heart disease; Myocardial hypertrophy; Sex differences

Indexed keywords

1,3,5 TRIS(4 HYDROXYPHENYL) 4 PROPYLPYRAZOLE; DIARYLPROPIONITRILE; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; MINERALOCORTICOID;

CARDIOVASCULAR DISEASE; DISEASE MODEL; DRUG MECHANISM; EXERCISE; EXPERIMENTAL ANIMAL; HEART FAILURE; HEART INFARCTION; HEART LEFT VENTRICLE HYPERTROPHY; HEART MUSCLE INJURY; HEART PROTECTION; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE OVERLOAD; HORMONE ACTION; HUMAN; MOLECULAR MECHANICS; NONHUMAN; OVARIECTOMY; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SEX DIFFERENCE; TRANSGENIC MOUSE; ANIMAL; CARDIOMEGALY; FEMALE; MALE; PHYSIOLOGY; SEXUAL DEVELOPMENT;

ANIMALS; CARDIOMEGALY; CARDIOVASCULAR DISEASES; DISEASE MODELS, ANIMAL; ESTROGENS; FEMALE; HEART FAILURE; MALE; SEX CHARACTERISTICS;

EID: 84868314340     PISSN: 01712004     EISSN: 18650325     Source Type: Book Series    
DOI: 10.1007/978-3-642-30726-3_2     Document Type: Review

References (113)

1. Angele MK, Nitsch S, Knoferl MW, Ayala A, Angele P, Schildberg FW, Jauch KW, Chaudry IH (2003) Sex-specific p38 MAP kinase activation following trauma-hemorrhage: involvement of testosterone and estradiol. Am J Physiol Endocrinol Metab 285:E189-E196
2. Antos CL, McKinsey TA, Frey N, Kutschke W, McAnally J, Shelton JM, Richardson JA, Hill JA, Olson EN (2002) Activated glycogen synthase-3 beta suppresses cardiac hypertrophy in vivo. Proc Natl Acad Sci U S A 99:907-912
3. Babiker FA, De Windt LJ, van Eickels M, Thijssen V, Bronsaer RJ, Grohe C, van Bilsen M, Doevendans PA (2004) 17beta-estradiol antagonizes cardiomyocyte hypertrophy by autocrine/ paracrine stimulation of a guanylyl cyclase A receptor-cyclic guanosine monophosphate-dependent protein kinase pathway. Circulation 109:269-276
4. Babiker FA, Lips D, Meyer R, Delvaux E, Zandberg P, Janssen B, van Eys G, Grohe C, Doevendans PA (2006) Estrogen receptor beta protects the murine heart against left ventricular hypertrophy. Arterioscler Thromb Vasc Biol 26(7):1524-1530
5. Babiker FA, Lips DJ, Delvaux E, Zandberg P, Janssen BJ, Prinzen F, van Eys G, Grohe C, Doevendans PA (2007) Oestrogen modulates cardiac ischaemic remodelling through oestrogen receptor-specific mechanisms. Acta Physiol (Oxf) 189:23-31
6. Bae S, Zhang L (2005) Gender differences in cardioprotection against ischemia/reperfusion injury in adult rat hearts: focus on Akt and protein kinase C signaling. J Pharmacol Exp Ther 315:1125-1135
7. Bell JR, Porrello ER, Huggins CE, Harrap SB, Delbridge LM (2008) The intrinsic resistance of female hearts to an ischemic insult is abrogated in primary cardiac hypertrophy. Am J Physiol Heart Circ Physiol 294:H1514-H1522
8. Bernardo BC, Weeks KL, Pretorius L, McMullen JR (2010) Molecular distinction between physiological and pathological cardiac hypertrophy: experimental findings and therapeutic strategies. Pharmacol Ther 128:191-227
9. Booth EA, Marchesi M, Kilbourne EJ, Lucchesi BR (2003) 17Beta-estradiol as a receptor-mediated cardioprotective agent. J Pharmacol Exp Ther 307:395-401
10. Booth EA, Obeid NR, Lucchesi BR (2005) Activation of estrogen receptor-alpha protects the in vivo rabbit heart from ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 289: H2039-H2047
11. Booth EA, Marchesi M, Knittel AK, Kilbourne EJ, Lucchesi BR (2007) The pathway-selective estrogen receptor ligand WAY-169916 reduces infarct size after myocardial ischemia and reperfusion by an estrogen receptor dependent mechanism. J Cardiovasc Pharmacol 49:401-407
12. Bouma W, Noma M, Kanemoto S, Matsubara M, Leshnower BG, Hinmon R, Gorman JH III, Gorman RC (2010) Sex-related resistance to myocardial ischemia-reperfusion injury is associated with high constitutive ARC expression. Am J Physiol Heart Circ Physiol 298: H1510-H1517
13. Brower GL, Gardner JD, Janicki JS (2003) Gender mediated cardiac protection from adverse ventricular remodeling is abolished by ovariectomy. Mol Cell Biochem 251:89-95
14. Brown DA, Lynch JM, Armstrong CJ, Caruso NM, Ehlers LB, Johnson MS, Moore RL (2005) Susceptibility of the heart to ischaemia-reperfusion injury and exercise-induced cardioprotection are sex-dependent in the rat. J Physiol 564:619-630
15. Camper-Kirby D, Welch S, Walker A, Shiraishi I, Setchell KD, Schaefer E, Kajstura J, Anversa P, Sussman MA (2001) Myocardial Akt activation and gender: increased nuclear activity in females versus males. Circ Res 88:1020-1027
16. Carroll JD, Carroll EP, Feldman T, Ward DM, Lang RM, McGaughey D, Karp RB (1992) Sex-associated differences in left ventricular function in aortic stenosis of the elderly. Circulation 86:1099-1107
17. Cavasin MA, Tao Z, Menon S, Yang XP (2004) Gender differences in cardiac function during early remodeling after acute myocardial infarction in mice. Life Sci 75:2181-2192
18. Chu SH, Goldspink P, Kowalski J, Beck J, Schwertz DW (2006) Effect of estrogen on calcium-handling proteins, beta-adrenergic receptors, and function in rat heart. Life Sci 79:1257-1267
19. Cross HR, Murphy E, Steenbergen C (2002) Ca(2+) loading and adrenergic stimulation reveal male/female differences in susceptibility to ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 283:H481-H489
20. Cross HR, Kranias EG, Murphy E, Steenbergen C (2003) 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:H683-H690
21. Cui YH, Tan Z, Fu XD, Xiang QL, Xu JW, Wang TH (2011) 17beta-estradiol attenuates pressure overload-induced myocardial hypertrophy through regulating caveolin-3 protein in ovariectomized female rats. Mol Biol Rep 38:4885-4892
22. Czubryt MP, McAnally J, Fishman GI, Olson EN (2003) Regulation of peroxisome proliferator-activated receptor gamma coactivator 1 alpha (PGC-1 alpha) and mitochondrial function by MEF2 and HDAC5. Proc Natl Acad Sci U S A 100:1711-1716
23. Dash R, Schmidt AG, Pathak A, Gerst MJ, Biniakiewicz D, Kadambi VJ, Hoit BD, Abraham WT, Kranias EG (2003) Differential regulation of p38 mitogen-activated protein kinase mediates gender-dependent catecholamine-induced hypertrophy. Cardiovasc Res 57:704-714
24. De Bono JP, Adlam D, Paterson DJ, Channon KM (2006) Novel quantitative phenotypes of exercise training in mouse models. Am J Physiol Regul Integr Comp Physiol 290:R926-R934
25. DeBosch B, Treskov I, Lupu TS, Weinheimer C, Kovacs A, Courtois M, Muslin AJ (2006) Akt1 is required for physiological cardiac growth. Circulation 113:2097-2104
26. Dent MR, Tappia PS, Dhalla NS (2010) Gender differences in apoptotic signaling in heart failure due to volume overload. Apoptosis 15:499-510
27. Dent MR, Tappia PS, Dhalla NS (2011) Gender differences in beta-adrenoceptor system in cardiac hypertrophy due to arteriovenous fistula. J Cell Physiol 226:181-186
28. Djouadi F, Weinheimer CJ, Saffitz JE, Pitchford C, Bastin J, Gonzalez FJ, Kelly DP (1998) A gender-related defect in lipid metabolism and glucose homeostasis in peroxisome proliferator-activated receptor alpha-deficient mice. J Clin Invest 102:1083-1091
29. Douglas PS, Katz SE, Weinberg EO, Chen MH, Bishop SP, Lorell BH (1998) Hypertrophic remodeling: gender differences in the early response to left ventricular pressure overload. J Am Coll Cardiol 32:1118-1125
30. Du XJ (2004) Gender modulates cardiac phenotype development in genetically modified mice. Cardiovasc Res 63:510-519
31. Dubey RK, Jackson EK, Keller PJ, Imthurn B, Rosselli M (2001) Estradiol metabolites inhibit endothelin synthesis by an estrogen receptor-independent mechanism. Hypertension 37:640-644
32. Fang L, Gao XM, Moore XL, Kiriazis H, Su Y, Ming Z, Lim YL, Dart AM, Du XJ (2007) Differences in inflammation, MMP activation and collagen damage account for gender difference in murine cardiac rupture following myocardial infarction. J Mol Cell Cardiol 43:535-544
33. Fliegner D, Schubert C, Penkalla A, Witt H, Kararigas G, Dworatzek E, Staub E, Martus P, Ruiz Noppinger P, Kintscher U, Gustafsson JA, Regitz-Zagrosek V (2010) Female sex and estrogen receptor-beta attenuate cardiac remodeling and apoptosis in pressure overload. Am J Physiol Regul Integr Comp Physiol 298:R1597-R1606
34. Foryst-Ludwig A, Kintscher U (2010) Metabolic impact of estrogen signalling through ERalpha and ERbeta. J Steroid Biochem Mol Biol 122:74-81
35. Foryst-Ludwig A, Kreissl MC, Sprang C, Thalke B, Bohm C, Benz V, Gurgen D, Dragun D, Schubert C, Mai K, Stawowy P, Spranger J, Regitz-Zagrosek V, Unger T, Kintscher U (2011) Sex differences in physiological cardiac hypertrophy are associated with exercise-mediated changes in energy substrate availability. Am J Physiol Heart Circ Physiol 301:H115-H122
36. Gabel SA, Walker VR, London RE, Steenbergen C, Korach KS, Murphy E (2005) Estrogen receptor beta mediates gender differences in ischemia/reperfusion injury. J Mol Cell Cardiol 38:289-297
37. Garcia-Segura LM, Sanz A, Mendez P (2006) Cross-talk between IGF-I and estradiol in the brain: focus on neuroprotection. Neuroendocrinology 84:275-279
38. Gardner JD, Brower GL, Janicki JS (2002) Gender differences in cardiac remodeling secondary to chronic volume overload. J Card Fail 8:101-107
39. Grohe C, Kahlert S, Lobbert K, Stimpel M, Karas RH, Vetter H, Neyses L (1997) Cardiac myocytes and fibroblasts contain functional estrogen receptors. FEBS Lett 416:107-112
40. Groten T, Pierce AA, Huen AC, Schnaper HW (2005) 17 beta-estradiol transiently disrupts adherens junctions in endothelial cells. FASEB J 19:1368-1370
41. Gurgen D, Hegner B, Kusch A, Catar R, Chaykovska L, Hoff U, Gross V, Slowinski T, da Costa Goncalves AC, Kintscher U, Gustafsson JA, Luft FC, Dragun D (2011) Estrogen receptor-beta signals left ventricular hypertrophy sex differences in normotensive deoxycorticosterone acetate-salt mice. Hypertension 57:648-654
42. Hale SL, Birnbaum Y, Kloner RA (1996) beta-Estradiol, but not alpha-estradiol, reduced myocardial necrosis in rabbits after ischemia and reperfusion. Am Heart J 132:258-262
43. Haq S, Choukroun G, Kang ZB, Ranu H, Matsui T, Rosenzweig A, Molkentin JD, Alessandrini A, Woodgett J, Hajjar R, Michael A, Force T (2000) Glycogen synthase kinase-3beta is a negative regulator of cardiomyocyte hypertrophy. J Cell Biol 151:117-130
44. Hill JA, Olson EN (2008) Cardiac plasticity. N Engl J Med 358:1370-1380
45. Hsieh YC, Choudhry MA, Yu HP, Shimizu T, Yang S, Suzuki T, Chen J, Bland KI, Chaudry IH (2006) Inhibition of cardiac PGC-1alpha expression abolishes ERbeta agonist-mediated cardioprotection following trauma-hemorrhage. FASEB J 20:1109-1117
46. Jain M, Liao R, Podesser BK, Ngoy S, Apstein CS, Eberli FR (2002) Influence of gender on the response to hemodynamic overload after myocardial infarction. Am J Physiol Heart Circ Physiol 283:H2544-H2550
47. Janczewski AM, Kadokami T, Lemster B, Frye CS, McTiernan CF, Feldman AM (2003) Morphological and functional changes in cardiac myocytes isolated from mice overexpressing TNF-alpha. Am J Physiol Heart Circ Physiol 284:H960-H969
48. 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 197:493-501
49. 2+ in guinea-pig isolated cardiac myocytes. Br J Pharmacol 106:739-745
50. Johnson BD, Zheng W, Korach KS, Scheuer T, Catterall WA, Rubanyi GM (1997) Increased expression of the cardiac L-type calcium channel in estrogen receptor-deficient mice. J Gen Physiol 110:135-140
51. Johnson MS, Moore RL, Brown DA (2006) Sex differences in myocardial infarct size are abolished by sarcolemmal KATP channel blockade in rat. Am J Physiol Heart Circ Physiol 290:H2644-H2647
52. 2+ loading. J Am Coll Cardiol 36:948-952
53. Kadokami T, McTiernan CF, Kubota T, Frye CS, Feldman AM (2000) Sex-related survival differences in murine cardiomyopathy are associated with differences in TNF-receptor expression. J Clin Invest 106:589-597
54. Karatas A, Hegner B, de Windt LJ, Luft FC, Schubert C, Gross V, Akashi YJ, Gurgen D, Kintscher U, da Costa Goncalves AC, Regitz-Zagrosek V, Dragun D (2008) Deoxycorticosterone acetate-salt mice exhibit blood pressure-independent sexual dimorphism. Hypertension 51:1177-1183
55. Kim J, Wende AR, Sena S, Theobald HA, Soto J, Sloan C, Wayment BE, Litwin SE, Holzenberger M, LeRoith D, Abel ED (2008) Insulin-like growth factor I receptor signaling is required for exercise-induced cardiac hypertrophy. Mol Endocrinol 22:2531-2543
56. Kolodgie FD, Farb A, Litovsky SH, Narula J, Jeffers LA, Lee SJ, Virmani R (1997) Myocardial protection of contractile function after global ischemia by physiologic estrogen replacement in the ovariectomized rat. J Mol Cell Cardiol 29:2403-2414
57. Konhilas JP, Maass AH, Luckey SW, Stauffer BL, Olson EN, Leinwand LA (2004) Sex modifies exercise and cardiac adaptation in mice. Am J Physiol Heart Circ Physiol 287:H2768-H2776
58. Lee TM, Su SF, Tsai CC, Lee YT, Tsai CH (2000) Cardioprotective effects of 17 beta-estradiol produced by activation of mitochondrial ATP-sensitive K(+)Channels in canine hearts. J Mol Cell Cardiol 32:1147-1158
59. Lee TM, Lin MS, Chou TF, Tsai CH, Chang NC (2004) Adjunctive 17beta-estradiol administration reduces infarct size by altered expression of canine myocardial connexin43 protein. Cardiovasc Res 63:109-117
60. Leinwand LA (2003) Sex is a potent modifier of the cardiovascular system. J Clin Invest 112:302-307
61. Lin J, Steenbergen C, Murphy E, Sun J (2009) Estrogen receptor-beta activation results in S-nitrosylation of proteins involved in cardioprotection. Circulation 120:245-254
62. Liu ML, Xu X, Rang WQ, Li YJ, Song HP (2004) Influence of ovariectomy and 17beta-estradiol treatment on insulin sensitivity, lipid metabolism and post-ischemic cardiac function. Int J Cardiol 97:485-493
63. Luczak ED, Leinwand LA (2009) Sex-based cardiac physiology. Annu Rev Physiol 71:1-18
64. Luo J, McMullen JR, Sobkiw CL, Zhang L, Dorfman AL, Sherwood MC, Logsdon MN, Horner JW, DePinho RA, Izumo S, Cantley LC (2005) Class IA phosphoinositide 3-kinase regulates heart size and physiological cardiac hypertrophy. Mol Cell Biol 25:9491-9502
65. Mahmoodzadeh S, Dworatzek E, Fritschka S, Pham TH, Regitz-Zagrosek V (2010) 17beta-Estradiol inhibits matrix metalloproteinase-2 transcription via MAP kinase in fibroblasts. Cardiovasc Res 85:719-728
66. McMullen JR, Shioi T, Huang WY, Zhang L, Tarnavski O, Bisping E, Schinke M, Kong S, Sherwood MC, Brown J, Riggi L, Kang PM, Izumo S (2004) The insulin-like growth factor 1 receptor induces physiological heart growth via the phosphoinositide 3-kinase(p110alpha) pathway. J Biol Chem 279:4782-4793
67. McMullen JR, Amirahmadi F, Woodcock EA, Schinke-Braun M, Bouwman RD, Hewitt KA, Mollica JP, Zhang L, Zhang Y, Shioi T, Buerger A, Izumo S, Jay PY, Jennings GL (2007) Protective effects of exercise and phosphoinositide 3-kinase(p110alpha) signaling in dilated and hypertrophic cardiomyopathy. Proc Natl Acad Sci U S A 104:612-617
68. Mehilli J, Ndrepepa G, Kastrati A, Nekolla SG, Markwardt C, Bollwein H, Pache J, Martinoff S, Dirschinger J, Schwaiger M, Schomig A (2005) Gender and myocardial salvage after reperfusion treatment in acute myocardial infarction. J Am Coll Cardiol 45:828-831
69. Mende S, Bleichner F, Stoeter P, Meuret G (1983) Successful treatment of brain metastases in breast cancer with blood-brain barrier-impervious cytostatics and hormones. Onkologie 6:58-61
70. Mendelsohn ME (2002) Genomic and nongenomic effects of estrogen in the vasculature. Am J Cardiol 90:3F-6F
71. Mendelsohn ME, Karas RH (2005) Molecular and cellular basis of cardiovascular gender differences. Science 308:1583-1587
72. Mendez P, Azcoitia I, Garcia-Segura LM (2003) Estrogen receptor alpha forms estrogen-dependent multimolecular complexes with insulin-like growth factor receptor and phosphatidylinositol 3-kinase in the adult rat brain. Brain Res Mol Brain Res 112:170-176
73. Mendez P, Wandosell F, Garcia-Segura LM (2006) Cross-talk between estrogen receptors and insulin-like growth factor-I receptor in the brain: cellular and molecular mechanisms. Front Neuroendocrinol 27:391-403
74. Mole PA (1978) Increased contractile potential of papillary muscles from exercise-trained rat hearts. Am J Physiol 234:H421-H425
75. Murphy E, Steenbergen C (2007) Gender-based differences in mechanisms of protection in myocardial ischemia-reperfusion injury. Cardiovasc Res 75:478-486
76. Nikolic I, Liu D, Bell JA, Collins J, Steenbergen C, Murphy E (2007) Treatment with an estrogen receptor-beta-selective agonist is cardioprotective. J Mol Cell Cardiol 42:769-780
77. Node K, Kitakaze M, Kosaka H, Minamino T, Funaya H, Hori M (1997) Amelioration of ischemia- and reperfusion-induced myocardial injury by 17beta-estradiol: role of nitric oxide and calcium-activated potassium channels. Circulation 96:1953-1963
78. Nordmeyer J, Eder S, Mahmoodzadeh S, Martus P, Fielitz J, Bass J, Bethke N, Zurbrugg HR, Pregla R, Hetzer R, Regitz-Zagrosek V (2004) Upregulation of myocardial estrogen receptors in human aortic stenosis. Circulation 110:3270-3275
79. Novotny JL, Simpson AM, Tomicek NJ, Lancaster TS, Korzick DH (2009) Rapid estrogen receptor-alpha activation improves ischemic tolerance in aged female rats through a novel protein kinase C epsilon-dependent mechanism. Endocrinology 150:889-896
80. Nuedling S, Kahlert S, Loebbert K, Doevendans PA, Meyer R, Vetter H, Grohe C (1999) 17 Beta-estradiol stimulates expression of endothelial and inducible NO synthase in rat myocardium in-vitro and in-vivo. Cardiovasc Res 43:666-674
81. Oertelt-Prigione S, Regitz-Zagrosek V (2012) Sex and gender aspects in clinical medicine. Springer Science + Business Media, Springer London, Medicine and Public Health, Internal Medicine edn (Berlin: Sabine Oertelt-Prigione, Vera Regitz-Zagrosek)
82. Patten RD, Pourati I, Aronovitz MJ, Baur J, Celestin F, Chen X, Michael A, Haq S, Nuedling S, Grohe C, Force T, Mendelsohn ME, Karas RH (2004) 17beta-estradiol reduces cardiomyocyte apoptosis in vivo and in vitro via activation of phospho-inositide-3 kinase/Akt signaling. Circ Res 95:692-699
83. Patten RD, Pourati I, Aronovitz MJ, Alsheikh-Ali A, Eder S, Force T, Mendelsohn ME, Karas RH (2008) 17 Beta-estradiol differentially affects left ventricular and cardiomyocyte hypertrophy following myocardial infarction and pressure overload. J Card Fail 14:245-253
84. Pedram A, Razandi M, Lubahn D, Liu J, Vannan M, Levin ER (2008) Estrogen inhibits cardiac hypertrophy: role of estrogen receptor-beta to inhibit calcineurin. Endocrinology 149:3361-3369
85. Pelzer T, Jazbutyte V, Hu K, Segerer S, Nahrendorf M, Nordbeck P, Bonz AW, Muck J, Fritzemeier KH, Hegele-Hartung C, Ertl G, Neyses L (2005a) The estrogen receptor-alpha agonist 16alpha-LE2 inhibits cardiac hypertrophy and improves hemodynamic function in estrogen-deficient spontaneously hypertensive rats. Cardiovasc Res 67:604-612
86. Pelzer T, Loza PA, Hu K, Bayer B, Dienesch C, Calvillo L, Couse JF, Korach KS, Neyses L, Ertl G (2005b) Increased mortality and aggravation of heart failure in estrogen receptor-beta knockout mice after myocardial infarction. Circulation 111:1492-1498
87. Petrov G, Regitz-Zagrosek V, Lehmkuhl E, Krabatsch T, Dunkel A, Dandel M, Dworatzek E, Mahmoodzadeh S, Schubert C, Becher E, Hampl H, Hetzer R (2010) Regression of myocardial hypertrophy after aortic valve replacement: faster in women? Circulation 122:S23-S28
88. Pfeffer JM, Pfeffer MA, Fletcher P, Fishbein MC, Braunwald E (1982) Favorable effects of therapy on cardiac performance in spontaneously hypertensive rats. Am J Physiol 242: H776-H784
89. Ranki HJ, Budas GR, Crawford RM, Jovanovic A (2001) Gender-specific difference in cardiac ATP-sensitive K(+) channels. J Am Coll Cardiol 38:906-915
90. Ranki HJ, Budas GR, Crawford RM, Davies AM, Jovanovic A (2002) 17Beta-estradiol regulates expression of K(ATP) channels in heart-derived H9c2 cells. J Am Coll Cardiol 40:367-374
91. Schaible TF, Scheuer J (1979) Effects of physical training by running or swimming on ventricular performance of rat hearts. J Appl Physiol 46:854-860
92. Schaible TF, Scheuer J (1981) Cardiac function in hypertrophied hearts from chronically exercised female rats. J Appl Physiol 50:1140-1145
93. Schaible TF, Penpargkul S, Scheuer J (1981) Cardiac responses to exercise training in male and female rats. J Appl Physiol 50:112-117
94. Simoncini T, Hafezi-Moghadam A, Brazil DP, Ley K, Chin WW, Liao JK (2000) Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature 407:538-541
95. Simoncini T, Mannella P, Genazzani AR (2006) Rapid estrogen actions in the cardiovascular system. Ann N Y Acad Sci 1089:424-430
96. Skavdahl M, Steenbergen C, Clark J, Myers P, Demianenko T, Mao L, Rockman HA, Korach KS, Murphy E (2005) Estrogen receptor-beta mediates male-female differences in the development of pressure overload hypertrophy. Am J Physiol Heart Circ Physiol 288:H469-H476
97. 2+ channel alpha1 subunit and reduced ischemia/reperfusion injury. Circ Res 98:403-411
98. van Eickels M, Grohe C, Cleutjens JP, Janssen BJ, Wellens HJ, Doevendans PA (2001) 17beta-estradiol attenuates the development of pressure-overload hypertrophy. Circulation 104:1419-1423
99. Varea O, Arevalo MA, Garrido JJ, Garcia-Segura LM, Wandosell F, Mendez P (2010) Interaction of estrogen receptors with insulin-like growth factor-I and Wnt signaling in the nervous system. Steroids 75:565-569
100. Vornehm ND, Wang M, Abarbanell A, Herrmann J, Weil B, Tan J, Wang Y, Kelly M, Meldrum DR (2009) Acute postischemic treatment with estrogen receptor-alpha agonist or estrogen receptor-beta agonist improves myocardial recovery. Surgery 146:145-154
101. Wang M, Baker L, Tsai BM, Meldrum KK, Meldrum DR (2005) Sex differences in the myocardial inflammatory response to ischemia-reperfusion injury. Am J Physiol Endocrinol Metab 288: E321-E326
102. Wang C, Chiari PC, Weihrauch D, Krolikowski JG, Warltier DC, Kersten JR, Pratt PF Jr, Pagel PS (2006a) Gender-specificity of delayed preconditioning by isoflurane in rabbits: potential role of endothelial nitric oxide synthase. Anesth Analg 103:274-280, table of contents
103. Wang M, Crisostomo P, Wairiuko GM, Meldrum DR (2006b) Estrogen receptor-alpha mediates acute myocardial protection in females. Am J Physiol Heart Circ Physiol 290:H2204-H2209
104. Wang M, Tsai BM, Reiger KM, Brown JW, Meldrum DR (2006c) 17-beta-Estradiol decreases p38 MAPK-mediated myocardial inflammation and dysfunction following acute ischemia. J Mol Cell Cardiol 40:205-212
105. Wang M, Wang Y, Weil B, Abarbanell A, Herrmann J, Tan J, Kelly M, Meldrum DR (2009) Estrogen receptor beta mediates increased activation of PI3K/Akt signaling and improved myocardial function in female hearts following acute ischemia. Am J Physiol Regul Integr Comp Physiol 296:R972-R978
106. Weinberg EO, Thienelt CD, Katz SE, Bartunek J, Tajima M, Rohrbach S, Douglas PS, Lorell BH (1999) Gender differences in molecular remodeling in pressure overload hypertrophy. J Am Coll Cardiol 34:264-273
107. Weinberg EO, Mirotsou M, Gannon J, Dzau VJ, Lee RT, Pratt RE (2003) Sex dependence and temporal dependence of the left ventricular genomic response to pressure overload. Physiol Genomics 12:113-127
108. Witt H, Schubert C, Jaekel J, Fliegner D, Penkalla A, Tiemann K, Stypmann J, Roepcke S, Brokat S, Mahmoodzadeh S, Brozova E, Davidson MM, Ruiz Noppinger P, Grohe C, Regitz-Zagrosek V (2008) Sex-specific pathways in early cardiac response to pressure overload in mice. J Mol Med (Berl) 86:1013-1024
109. Xin HB, Senbonmatsu T, Cheng DS, Wang YX, Copello JA, Ji GJ, Collier ML, Deng KY, Jeyakumar LH, Magnuson MA, Inagami T, Kotlikoff MI, Fleischer S (2002) Oestrogen protects FKBP12.6 null mice from cardiac hypertrophy. Nature 416:334-338
110. Xu Y, Arenas IA, Armstrong SJ, Davidge ST (2003) Estrogen modulation of left ventricular remodeling in the aged heart. Cardiovasc Res 57:388-394
111. Xu Y, Arenas IA, Armstrong SJ, Plahta WC, Xu H, Davidge ST (2006) Estrogen improves cardiac recovery after ischemia/reperfusion by decreasing tumor necrosis factor-alpha. Cardiovasc Res 69:836-844
112. Yu HP, Shimizu T, Choudhry MA, Hsieh YC, Suzuki T, Bland KI, Chaudry IH (2006) 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 40:185-194
113. Zhai P, Eurell TE, Cooke PS, Lubahn DB, Gross DR (2000) Myocardial ischemia-reperfusion injury in estrogen receptor-alpha knockout and wild-type mice. Am J Physiol Heart Circ Physiol 278:H1640-H1647