Mechanism of cardioprotection: What can we learn from females?

Pediatric Cardiology

Volumn 32, Issue 3, 2011, Pages 354-359

  Murphy, Elizabeth ^a   Lagranha, Claudia ^a   Deschamps, Anne ^a   Kohr, Mark ^a,b   Nguyen, Tiffany ^a   Wong, Renee ^a   Sun, Junhui ^a   Steenbergen, Charles ^b  

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

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Cardioprotection; Estrogen signaling; G protein coupled receptor; Nuclear estrogen receptors

Indexed keywords

ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; G PROTEIN COUPLED RECEPTOR 30; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE;

CONFERENCE PAPER; ELECTRON TRANSPORT; ESTROGEN BLOOD LEVEL; GENE EXPRESSION; GENETIC TRANSCRIPTION; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART PROTECTION; NONHUMAN; PROTEIN BINDING; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; SEX DIFFERENCE; SIGNAL TRANSDUCTION;

CARDIOTONIC AGENTS; CARDIOVASCULAR DISEASES; ESTROGENS; FEMALE; HUMANS; MYOCYTES, CARDIAC; PHOSPHATIDYLINOSITOL 3-KINASES; REACTIVE OXYGEN SPECIES; RECEPTORS, ESTROGEN; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

EID: 79953761440     PISSN: 01720643     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00246-010-9877-4     Document Type: Conference Paper

References (40)

1. Barrett-Connor E (1997) Sex differences in coronary heart disease: why are women so superior? The 1995 Ancel Keys Lecture. Circulation 95:252-264
2. Hayward CS, Kelly RP, Collins P (2000) The roles of gender, the menopause and hormone replacement on cardiovascular function. Cardiovasc Res 46:28-49 (Pubitemid 30155943)
3. 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 106:1681-1691
4. 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 (Pubitemid 41635399)
5. 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 (Pubitemid 41507355)
6. 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 (Pubitemid 26292388)
7. Wang M, Crisostomo P, Wairiuko GM, Meldrum DR (2006) Estrogen receptor-alpha mediates acute myocardial protection in females. Am J Physiol Heart Circ Physiol 290:H2204-H2209 (Pubitemid 43846046)
8. 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 (Pubitemid 46527602)
9. Lin J, Steenbergen C, Murphy E, Sun J (2009) Estrogen receptorbeta activation results in S-nitrosylation of proteins involved in cardioprotection. Circulation 120:245-254
10. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SA, Howard BV, Johnson KC, Kotchen JM, Ockene J (2002) Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA 288:321-333 (Pubitemid 34761611)
11. Toh S, Hernandez-Diaz S, Logan R, Rossouw JE, Hernan MA (2010) Coronary heart disease in postmenopausal recipients of estrogen plus progestin therapy: does the increased risk ever disappear? A randomized trial. Ann Intern Med 152:211-217
12. MendelsohnME,KarasRH(1999) The protective effects of estrogen on the cardiovascular system. N Engl J Med 340:1801-1811
13. 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
14. Filardo EJ, Thomas P (2005) GPR30: a seven-transmembranespanning estrogen receptor that triggers EGF release. Trends Endocrinol Metab 16:362-367 (Pubitemid 41338741)
15. Revankar CM, Cimino DF, Sklar LA, Arterburn JB, Prossnitz ER (2005) A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 307:1625-1630 (Pubitemid 40354745)
16. Booth EA, Marchesi M, Kilbourne EJ, Lucchesi BR (2003) 17Beta-estradiol as a receptor-mediated cardioprotective agent. J Pharmacol Exp Ther 307:395-401
17. Przyklenk K, Ovize M, Bauer B, Kloner RA (1995) Gender does not influence acute myocardial infarction in adult dogs. Am Heart J 129:1108-1113
18. Li Y, Kloner RA (1995) Is there a gender difference in infarct size and arrhythmias following experimental coronary occlusion and reperfusion? J Thromb Thrombolysis 2:221-225
19. Cross HR, Lu L, Steenbergen C, Philipson KD, Murphy E (1998) Overexpression of the cardiac Na+/Ca2+ exchanger increases susceptibility to ischemia/reperfusion injury in male, but not female, transgenic mice. Circ Res 83:1215-1223 (Pubitemid 29006036)
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 (Pubitemid 36142897)
21. 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 (Pubitemid 34790839)
22. 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 (Pubitemid 40215198)
23. Sun J, Picht E, Ginsburg KS, Bers DM, Steenbergen C, Murphy E (2006) Hypercontractile female hearts exhibit increased S-nitrosylation of the L-type Ca2+ channel alpha1 subunit and reduced ischemia/reperfusion injury. Circ Res 98:403-411
24. Tretter L, Adam-Vizi V (2005) Alpha-ketoglutarate dehydrogenase: a target and generator of oxidative stress. Philos Trans R Soc Lond B Biol Sci 360:2335-2345 (Pubitemid 46682153)
25. Starkov AA, Fiskum G, Chinopoulos C, Lorenzo BJ, Browne SE, Patel MS, Beal MF (2004) Mitochondrial alpha-ketoglutarate dehydrogenase complex generates reactive oxygen species. J Neurosci 24:7779-7788 (Pubitemid 39215681)
26. Stirone C, Duckles SP, Krause DN, Procaccio V (2005) Estrogen increases mitochondrial efficiency and reduces oxidative stress in cerebral blood vessels. Mol Pharmacol 68:959-965 (Pubitemid 41345787)
27. Borras C, Sastre J, Garcia-Sala D, Lloret A, Pallardo FV, Vina J (2003) Mitochondria from females exhibit higher antioxidant gene expression and lower oxidative damage than males. Free Radic Biol Med 34:546-552 (Pubitemid 36254828)
28. 2 production and oxidative damage. Cardiovasc Res 74:456-465
29. Razmara A, Duckles SP, Krause DN, Procaccio V (2007) Estrogen suppresses brain mitochondrial oxidative stress in female and male rats. Brain Res 1176:71-81 (Pubitemid 47553127)
30. Roy D, Cai Q, Felty Q, Narayan S (2007) Estrogen-induced generation of reactive oxygen and nitrogen species, gene damage, and estrogen-dependent cancers. J Toxicol Environ Health B Crit Rev 10:235-257 (Pubitemid 47057178)
31. Chen CH, Budas GR, Churchill EN, Disatnik MH, Hurley TD, Mochly-Rosen D (2008) Activation of aldehyde dehydrogenase-2 reduces ischemic damage to the heart. Science 321:1493-1495
32. Yan L, Ge H, Li H, Lieber SC, Natividad F, Resuello RR, Kim SJ, Akeju S, Sun A, Loo K, Peppas AP, Rossi F, Lewandowski ED, Thomas AP, Vatner SF, Vatner DE (2004) Gender-specific proteomic alterations in glycolytic and mitochondrial pathways in aging monkey hearts. J Mol Cell Cardiol 37:921-929 (Pubitemid 39446817)
33. Arieli Y, Gursahani H, Eaton MM, Hernandez LA, Schaefer S (2004) Gender modulation of Ca(2+) uptake in cardiac mitochondria. J Mol Cell Cardiol 37:507-513 (Pubitemid 38953378)
34. Sun J, Murphy E (2010) Protein S-nitrosylation and cardioprotection. Circ Res 106:285-296
35. Lima B, Forrester MT, Hess DT, Stamler JS (2010) S-nitrosylation in cardiovascular signaling. Circ Res 106:633-646
36. Nisoli E, Tonello C, Cardile A, Cozzi V, Bracale R, Tedesco L, Falcone S, Valerio A, Cantoni O, Clementi E, Moncada S, Carruba MO (2005) Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310:314-317 (Pubitemid 41457197)
37. Deschamps AM, Murphy E (2009) Activation of a novel estrogen receptor, GPER, is cardioprotective in male and female rats. Am J Physiol Heart Circ Physiol 297:H1806-H1813
38. Lindsey SH, Cohen JA, Brosnihan KB, Gallagher PE, Chappell MC (2009) Chronic treatment with the G protein-coupled receptor 30 agonist G-1 decreases blood pressure in ovariectomized mRen2.Lewis rats. Endocrinology 150:3753-3758
39. Haas E, Bhattacharya I, Brailoiu E, Damjanovic M, Brailoiu GC, Gao X, Mueller-Guerre L, Marjon NA, Gut A, Minotti R, Meyer MR, Amann K, Ammann E, Perez-Dominguez A, Genoni M, Clegg DJ, Dun NJ, Resta TC, Prossnitz ER, Barton M (2009) Regulatory role of G protein-coupled estrogen receptor for vascular function and obesity. Circ Res 104:288-291
40. Nuedling S, Karas RH, Mendelsohn ME, Katzenellenbogen JA, Katzenellenbogen BS, Meyer R, Vetter H, Grohe C (2001) Activation of estrogen receptor-beta is a prerequisite for estrogen-dependent upregulation of nitric oxide synthases in neonatal rat cardiac myocytes. FEBS Lett 502:103-108 (Pubitemid 32728269)