Age-related differences in cardiac ischemia-reperfusion injury: Effects of estrogen deficiency

Pflugers Archiv European Journal of Physiology

Volumn 465, Issue 5, 2013, Pages 669-685

  Korzick, Donna H ^a   Lancaster, Timothy S ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Cardioprotection; Estrogen receptors; Proteomics; Senescence

Indexed keywords

1,3,5 TRIS(4 HYDROXYPHENYL) 4 PROPYLPYRAZOLE; ADENINE NUCLEOTIDE TRANSLOCASE; ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; CALCIUM ION; CASPASE; CLORGYLINE; EARLY PREGNANCY FACTOR; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GLUTATHIONE PEROXIDASE; GLYCOGEN SYNTHASE KINASE 3BETA; HEAT SHOCK PROTEIN 70; MANGANESE SUPEROXIDE DISMUTASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; NICORANDIL; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAD; PROTEIN BAX; PROTEIN KINASE B; PROTEIN KINASE C EPSILON; PROTEOME; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UNINDEXED DRUG; VOLTAGE DEPENDENT ANION CHANNEL;

ACUTE HEART INFARCTION; AGE; AGING; CELL DEATH; DRUG EFFECT; DRUG EFFICACY; ESTROGEN DEFICIENCY; GENE EXPRESSION; HEART INFARCTION PREVENTION; HEART MITOCHONDRION; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HORMONE SUBSTITUTION; HUMAN; ISCHEMIC HEART DISEASE; MENOPAUSE; MITOCHONDRIAL RESPIRATION; NONHUMAN; OVARIECTOMY; POSTMENOPAUSE; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

AGE FACTORS; ANIMALS; ESTRADIOL; ESTROGENS; FEMALE; HUMANS; MALE; MYOCARDIAL REPERFUSION INJURY;

EID: 84878014406     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-013-1255-7     Document Type: Review

References (229)

1. Aasum E, Cooper M, Severson DL, Larsen TS (2005) Effect of BM 17.0744, a PPARa ligand, on the metabolism of perfused hearts from control and diabetic mice. Can J Physiol Pharmacol 83:183-190
2. Abete P, Calabrese C, Ferrara N, Cioppa A, Pisanelli P, Cacciatore F, Longobardi G, Napoli C, Rengo F (2000) Exercise training restores ischemic preconditioning in the aging heart. J Am Coll Cardiol 36(2):643-650
3. Abete P, Cioppa A, Calabrese C, Pascucci I, Cacciatore F, Napoli C, Carnovale V, Ferrara N, Rengo F (1999) Ischemic threshold and myocardial stunning in the aging heart. Exp Gerontol 34(7):875-884
4. Abete P, de Santis D, Condorelli M, Napoli C, Rengo F (2002) A four-year-old rabbit cannot be considered the right model for investigating cardiac senescence. J Am Coll Cardiol 39(10):1701, author reply 1701-2
5. Abete P, Ferrara N, Cacciatore F, Madrid A, Bianco S, Calabrese C, Napoli C, Scognamiglio P, Bollella O, Cioppa A, Longobardi G, Rengo F (1997) Angina-induced protection against myocardial infarction in adult and elderly patients: a loss of preconditioning mechanism in the aging heart? J Am Coll Cardiol 30(4):947-954
6. Abete P, Ferrara N, Cioppa A, Ferrara P, Bianco S, Calabrese C, Cacciatore F, Longobardi G, Rengo F (1996) Preconditioning does not prevent postischemic dysfunction in aging heart. J Am Coll Cardiol 27(7):1777-1786
7. Adler A, Messina E, Sherman B, Wang Z, Huang H, Linke A, Hintze TH (2003) NAD(P)H oxidase-generated superoxide anion accounts for reduced control of myocardial O2 consumption by NO in old Fischer 344 rats. Am J Physiol Heart Circ Physiol 285(3):H1015-H1022
8. Alexaki VI, Charalampopoulos I, Kampa M, Artemissia-Phoebe N, Hatzoglou A, Gravanis A, Elias C (2006) Activation of membrane estrogen receptors induce pro-survival kinases. J Steriod Biochem Mol Biol 98:97-110
9. 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(2):507-513
10. Arnstein PM, Buselli EF, Rankin SH (1996) Women and heart attacks: prevention, diagnosis, and care. Nurse Pract 21(5):57-58, 61-4, 67-9; quiz 70-1
11. Azhar G, Gao W, Liu L, Wei JY (1999) Ischemia-reperfusion in the adult mouse heart influence of age. Exp Gerontol 34(5):699-714
12. Azhar G, Liu L, Zhang X, Wei JY (1999) Influence of age on hypoxiz/reoxygenation-induced DNA fragmentation and bcl-2, bcl-xl, ba and fas in the rat heart and brain. Mech Ageing Dev 112:5-25
13. Baines CP, Goto M, Downey JM (1997) Oxygen radicals released during ischemic preconditioning contribute to cardioprotection in the rabbit myocardium. J Mol Cell Cardiol 29(1):207-216
14. Baines CP, Song CX, Zheng YT, Wang GW, Zhang J, Wang OL, Guo Y, Bolli R, Cardwell EM, Ping P (2003) Protein kinase Cepsilon interacts with and inhibits the permeability transition pore in cardiac mitochondria. Circ Res 92(8):873-880
15. Baines CP, Zhang J, Wang GW, Zheng YT, Xiu JX, Cardwell EM, Bolli R, Ping P (2002) Mitochondrial PKCepsilon and MAPK form signaling modules in the murine heart: enhanced mitochondrial PKCepsilon-MAPK interactions and differential MAPK activation in PKCepsilon-induced cardioprotection. Circ Res 90(4):390-397
16. Barrett-Connor E (1997) Sex differences in coronary heart disease. Why are women so superior? The 1995 Ancel Keys Lecture. Circulation 95(1):252-264
17. Barrett-Connor E, Bush TL (1991) Estrogen and coronary heart disease in women. JAMA 265(14):1861-1867
18. Bartling B, Hilgefort C, Friedrich I, Silber RE, Simm A (2003) Cardio-protective determinants are conserved in aged human myocardium after ischemic preconditioning. FEBS Lett 555(3):539-544
19. Batandier C, Leverve X, Fontaine E (2004) Opening of the mitochondrial permeability transition pore induces reactive oxygen species production at the level of the respiratory chain complex I. J Biol Chem 279(17):17197-17204
20. Bianchi P, Kunduzova O, Masini E, Cambon C, Bani D, Raimondi L, Seguelas MH, Nistri S, Colucci W, Leducq N, Parini A (2005) Oxidative stress by monoamine oxidase mediates receptor-independent cardiomyocyte apoptosis by serotonin and postischemic myocardial injury. Circulation 112(21):3297-3305
21. Boengler K, Konietzka I, Buechert A, Heinen Y, Garcia-Dorado D, Heusch G, Schulz R (2007) 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(4):H1764-H1769
22. Boengler K, Schulz R, Heusch G (2009) Loss of cardioprotection with ageing. Cardiovasc Res 83(2):247-261. doi: 10.1093/cvr/cvp033
23. Bognar Z, Kalai T, Palfi A, Hanto K, Bognar B, Mark L, Szabo Z, Tapodi A, Radnai B, Sarszegi Z, Szanto A, Gallyas F Jr, Hideg K, Sumegi B, Varbiro G (2006) A novel SOD-mimetic permeability transition inhibitor agent protects ischemic heart by inhibiting both apoptotic and necrotic cell death. Free Radic Biol Med 41(5):835-848
24. Booth EA, Obeid NR, Lucchesi BR (2005) Activation of estrogen receptor-a protects the in vivo rabbit heart from ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 289:H2039-H2047
25. Bratic I, Trifunovic A (2010) Mitochondrial energy metabolism and ageing. Biochim Biophys Acta 1797(6-7):961-967
26. Bremnes Y, Ursin G, Bjurstam N, Rinaldi S, Kaaks R, Gram IT (2007) Endogenous sex hormones, prolactin and mammographic density in postmenopausal Norwegian women. Int J Cancer 121(11):2506-2511
27. Bryzgalova G, Gao H, Ahren B, Zierath JR, Galuska D, Steiler TL, Dahlman-Wright K, Nilsson S, Gustafsson JA, Efendic S, Khan A (2006) Evidence that oestrogen receptor-alpha plays an important role in the regulation of glucose homeostasis in mice: insulin sensitivity in the liver. Diabetologia 49:588-597
28. Budas GR, Churchill EN, Disatnik M, Sun L, Mochly-Rosen D (2010) Mitochondrial import of PKCepsilong mediated by HSP90: a role in cardioprotection from ischaemia and reperfusion injury. Cardiovasc Res 88(1):83-92
29. Budas GR, Churchill EN, Mochly-Rosen D (2007) Cardioprotective mechanisms of PKC isozyme-selective activators and inhibitors in the treatment of ischemia-reperfusion injury. Pharmacol Res 55(6):523-536
30. Burns PG, Krukenkamp IB, Caldarone CC, Kirvaitis RJ, Gaudette GR, Levitsky S (1996) Is the preconditioning response conserved in the senescent myocardium? Ann Thorac Surg 61:925-929
31. 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(10):1020-1027
32. Centurione L, Antonucci A, Miscia S, Grilli A, Rapino M, Grifone G, DiGiacomo V, DiGuiulio C, Falconi M, Cataldi A (2002) Age-related death-survival balance in myocardium: an immunohistochemical and biochemical study. Mech Ageing Dev 123:341-350
33. Chakraborty TR, Gore AC (2004) Aging-related changes in ovarian hormones, their receptors, and neuroendocrine function. Exp Biol Med 229(10):977-987
34. Chakravarti B, Oseguera M, Dalal N, Fathy P, Mallik B, Raval A, Chakravarti DN (2008) Proteomic profiling of aging in the mouse heart: altered expression of mitochondrial proteins. Arch Biochem Biophys 474(1):22-31
35. Chen L, Hahn H, Wu G, Chen CH, Liron T, Schechtman D, Cavallaro G, Banci L, Guo Y, Bolli R, Dorn GW 2nd, Mochly-Rosen D (2001) Opposing cardioprotective actions and parallel hypertrophic effects of delta PKC and epsilon PKC. Proc Natl Acad Sci U S A 98(20):11114-11119
36. Chen D, Washbrook E, Sarwar N, Bates G, Pace P, Thirunuvakkarasu V, Taylor J, Epstein RJ, Fuller-Pace FV, Egly J, Coombes RC, Ali S (2002) Phosphorylation of human estrogen receptor a at serine 118 by two distinct signal transduction pathways revealed by phosphorylation-specific antisera. Oncogene 21:4921-4931
37. Cheskis BJ, Greger JG, Nagpal S, Freedman LP (2007) Signaling by estrogens. J Cell Physiol 213:610-617
38. Chimenti C, Kajstura J, Torella D, Urbanek K, Heleniak H, Colussi C, Di Meglio F, Nadal-Ginard B, Frustaci A, Leri A, Maseri A, Anversa P (2003) Senescence and death of primitive cells and myocytes leads to premature cardiac aging and heart failure. Circ Res 93(7):604-613
39. Choksi KB, Papaconstantinou J (2008) Age-related alterations in oxidatively damaged proteins of mouse heart mitochondrial electron transport chain complexes. Free Radic Biol Med 44(10):1795-1805. doi: 10.1016/j. freeradbiomed.2008.01.032
40. Cocco T, Sgobbo P, Clemente M, Lopriore B, Grattagliano I, Di Paola M, Villani G (2005) Tissue-specific changes of mitochondrial functions in aged rats: effect of a long-term dietary treatment with N-acetylcysteine. Free Radic Biol Med 38(6):796-805. doi: 10.1016/j.freeradbiomed.2004.11.034
41. Cochran R, Gwinup G (1962) Coronary artery disease in young females. Possibility of oophorectomy as an etiologic agent. Arch Intern Med 110:162-165
42. Cohen MV, Baines CP, Downey JM (2000) Ischemic preconditioning: from adenosine receptor to KATP channel. Annu Rev Physiol 62:79-109
43. Colditz GA, Willett WC, Stampfer MJ, Rosner B, Speizer FE, Hennekens CH (1987) Menopause and the risk of coronary heart disease in women. N Engl J Med 316(18):1105-1110
44. Craig EE, Hood DA (1997) Influence of aging on protein import into cardiac mitochondria. Am J Physiol Heart Circ Physiol 272(41):H2983-H2988
45. Dai D-F, Rabinovitch PS, Ungvari Z (2012) Mitochondria and cardiovascular aging. Circ Res 110(8):1109-1124. doi: 10.1161/circresaha.111.246140
46. Davies SM, Poljak A, Duncan MW, Smythe GA, Murphy MP (2001) Measurements of protein carbonyls, ortho- and meta-tyrosine and oxidative phosphorylation complex activity in mitochondria from young and old rats. Free Radic Biol Med 31(2):181-190
47. Dawn B, Bolli R (2006) Increasing evidence that estrogen is an important modulator of bone marrow-mediated cardiac repair after acute infarction. Circulation 114(21):2203-2205
48. Deng N, Zhang J, Zong C, Wang Y, Lu H, Yang P, Wang W, Young GW, Wang Y, Korge P, Lotz C, Doran P, Liem DA, Apweiler R, Weiss JN, Duan H, Ping P (2011) Phosphoproteome analysis reveals regulatory sites in major pathways of cardiac mitochondria. Mol Cell Proteomics 10(2):M110.000117. doi: 10.1074/mcp.M110. 000117
49. Deroo B, Korach K (2006) Estrogen receptors and human disease. J Clin Invest 116:561-570
50. Di Lisa F, Canton M, Menabo R, Kaludercic N, Bernardi P (2007) Mitochondria and cardioprotection. Heart Fail Rev 12:249-260
51. Downey JM, Cohen MV (2006) Reducing infarct size in the setting of acute myocardial infarction. Prog Cardiovasc Dis 48(5):363-371
52. Downey JM, Davis AM, Cohen MV (2007) Signaling pathways in ischemic preconditioning. Heart Fail Rev 12(3-4):181-188
53. Driggers PH, Segars JH (2002) Estrogen action and cytoplasmic signaling pathways. Part II: the role of growth factors and phosphorylation in estrogen signaling. Trends Endocrinol Metab 13:422-427
54. Du XJ, Dart AM, Riemersma RA, Oliver MF (1991) Sex difference in presynaptic adrenergic inhibition of norepinephrine release during normoxia and ischemia in the rat heart. Circ Res 68(3):827-835
55. Du X-J, Riemersma RA, Dart AM (1995) Cardiovascular protection by oestrogen is partly mediated through modulation of autonomic nervous function. Cardiovasc Res 30(2):161-165. doi: 10.1016/s0008-6363(95)00030-5
56. Dutta D, Calvani R, Bernabei R, Leeuwenburgh C, Marzetti E (2012) Contribution of impaired mitochondrial autophagy to cardiac aging: mechanisms and therapeutic opportunities. Circ Res 110(8):1125-1138. doi: 10.1161/circresaha.111.246108
57. Eefting F, Rensing B, Wigman J, Pannekoek WJ, Liu WM, Cramer MJ, Lips DJ, Doevendans PA (2004) Role of apoptosis in reperfusion injury. Cardiovasc Res 61(3):414-426
58. Falkeborn M, Persson I, Adami HO, Bergstrom R, Eaker E, Lithell H, Mohsen R, Naessen T (1992) The risk of acute myocardial infarction after oestrogen and oestrogen-progestogen replacement. Br J Obstet Gynaecol 99(10):821-828
59. Falkeborn M, Schairer C, Naessen T, Persson I (2000) Risk of myocardial infarction after oophorectomy and hysterectomy. J Clin Epidemiol 53(8):832-837
60. Fannin SW, Lesnefsky EJ, Slabe TJ, Hassan MO, Hoppel CL (1999) Aging selectively decreases oxidative capacity in rat heart interfibrillar mitochondria. Arch Biochem Biophys 372(2):399-407. doi: 10.1006/abbi.1999.1508
61. Faus H, Haendler B (2006) Post-transloational modifications of steriod receptors. Biomed Pharmacother 60:520-528
62. Fenton R, Dickson E, Dobson J Jr (2005) Inhibition of phosphatase activity enhances preconditioning and limits cell death in the ischemic/reperfused aged rat heart. Life Sci 77:3375-3388
63. Fenton RA, Dickson EW, Meyer TE, Dobson JG Jr (2000) Aging reduces the cardioprotective effect of ischemic preconditioning in the rat heart. J Mol Cell Cardiol 32(7):1371-1375
64. Filardo EJ, Thomas P (2005) GPR30: a seven-transmembrane-spanning estrogen receptor that triggers EGF release. Trends Endocrinol Metab 16(8):362-367
65. Forster C, Kietz S, Hultenby K, Warner M, Gustafsson JA (2004) Characterization of the ERbeta-/- mouse heart. Proc Natl Acad Sci U S A 101(39):14234-14239. doi: 10.1073/pnas.0405571101
66. Fu M, Wang C, Zhang X, Pestell RG (2004) Acetylation of nuclear receptors in cellular growth and apoptosis. Biochem Pharmacol 68:1199-1208
67. 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(2):289-297
68. 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
69. Garg V, Hu K (2007) Protein kinase C isoform-dependent modulation of ATP-sensitive K + channels in mitochondrial inner membrane. Am J Physiol Heart Circ Physiol 293(1):H322-H332
70. Goto M, Liu Y, Yang XM, Ardell JL, Cohen MV, Downey JM (1995) Role of bradykinin in protection of ischemic preconditioning in rabbit hearts. Circ Res 77(3):611-621
71. Gottlieb RA (2003) Mitochondrial signaling in apoptosis: mitochondrial daggers to the breaking heart. Basic Res Cardiol 98:242-249
72. Grodstein F, Manson JE, Colditz GA, Willett WC, Speizer FE, Stampfer MJ (2000) A prospective, observational study of postmenopausal hormone therapy and primary prevention of cardiovascular disease. Ann Intern Med 133(12):933-941
73. Hale GE, Zhao X, Hughes CL, Burger HG, Robertson DM, Fraser IS (2007) Endocrine features of menstrual cycles in middle and late reproductive age and the menopausal transition classified according to the Staging of Reproductive Aging Workshop (STRAW) staging system. J Clin Endocrinol Metab 92(8):3060-3067. doi: 10.1210/jc.2007-0066
74. Halestrap AP, Clarke SJ, Javadov SA (2004) Mitochondrial permeability transition pore opening during myocardial reperfusion - a target for cardioprotection. Cardiovasc Res 61(3):372-385
75. Hall JE (2004) Neuroendocrine physiology of the early and late menopause. Endocrinol Metab Clin N Am 33:637-659
76. Hamada H, Kim MK, Iwakura A, Ii M, Thorne T, Qin G, Asai J, Tsutsumi Y, Sekiguchi H, Silver M, Wecker A, Bord E, Zhu Y, Kishore R, Losordo DW (2006) Estrogen receptors alpha and beta mediate contribution of bone marrow-derived endothelial progenitor cells to functional recovery after myocardial infarction. Circulation 114(21):2261-2270
77. Hamilton KL, Gupta S, Knowlton AA (2004) Estrogen and regulation of heat shock protein expression in female cardiomyocytes: cross-talk with NF kappa B signaling. J Mol Cell Cardiol 36(4):577-584
78. Hansford RG (1978) Lipid oxidation by heart mitochondria from young adult and senescent rats. Biochem J 170:285-295
79. Harman SM, Brinton EA, Cedars M, Lobo R, Manson JE, Merriam GR, Miller VM, Naftolin F, Santoro N (2005) KEEPS: the Kronos Early Estrogen Prevention Study. Climacteric 8(1):3-12
80. Hausenloy DJ, Tsang A, Mocanu MM, Yellon DM (2005) Ischemic preconditioning protects by activating prosurvival kinases at reperfusion. Am J Physiol Heart Circ Physiol 288(2):H971-H976
81. Hausenloy DJ, Yellon DM, Mani-Babu S, Duchen MR (2004) Preconditioning protects by inhibiting the mitochondrial permeability transition. Am J Physiol Heart Circ Physiol 287(2):H841-H849
82. Hayward CS, Kelly RP, Collins P (2000) The roles of gender, the menopause and hormone replacement on cardiovascular function. Cardiovasc Res 46(1):28-49
83. Heine PA, Taylor JA, Iwamoto GA, Lubahn DB, Cooke PS (2000) Increased adipose tissue in male and female estrogen receptor-alpha knockout mice. Proc Natl Acad Sci 97(23):12729-12734. doi: 10.1073/pnas.97.23.12729
84. Hofer T, Servais S, Seo AY, Marzetti E, Hiona A, Upadhyay SJ, Wohlgemuth SE, Leeuwenburgh C (2009) Bioenergetics and permeability transition pore opening in heart subsarcolemmal and interfibrillar mitochondria: effects of aging and lifelong calorie restriction. Mech Ageing Dev 130(5):297-307. doi: 10.1016/j.mad.2009.01.004
85. Hsieh Y-C, Choudhry MA, Yu H-P, Shimizu T, Yang S, Suzuki T, Chen J, Bland KI, Chaudry IH (2006) Inhibition of cardiac PGC-1{alpha} expression abolishes ER{beta} agonist-mediated cardioprotection following trauma-hemorrhage. FASEB J 20:1109-1117
86. Hulley S, Grady D, Bush T, Furberg C, Herrington D, Riggs B, Vittinghoff E (1998) 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 280(7):605-613
87. Hunter JC, Kostyak JC, Novotny JL, Simpson AM, Korzick DH (2007) Estrogen deficiency decreases ischemic tolerance in aged rat myocardium: roles of PKC{delta}, PKC{epsilon}, Akt, and GSK3{beta}. Am J Physiol Regul Integr Comp Physiol 292(2):R800-R809. doi: 10.1152/ajpregu.00374.2006
88. Hunter JC, Kostyak JC, Novotny JL, Simpson AM, Korzick DH (2007) Estrogen deficiency decreases ischemic tolerance in the aged rat heart: roles of PKCdelta, PKCepsilon, Akt, and GSK3beta. Am J Physiol Regul Integr Comp Physiol 292(2):R800-R809
89. Hunter JC, Machikas AM, Korzick DH (2012) Age-dependent reductions in mitochondrial respiration are exacerbated by calcium in the female rat heart. Gender Med 9(3):197-206. doi: 10.1016/j.genm.2012.04.001
90. Inagaki K, Churchill E, Mochly-Rosen D (2006) Epsilon protein kinase C as a potential therapeutic target for the ischemic heart. Cardiovasc Res 70(2):222-230
91. Inagaki K, Hahn H, Dorn GW 2nd, Mochly-Rosen D (2003) Additive protection of the ischemic heart ex vivo by combined treatment with d-protein kinase c inhibitor and e-protein kinase c activator. Circulation 108:869-875
92. Isoyama S, Nitta-Komatsubara Y (2002) Acute and chronic adaptation to hemodynamic overload and ischemia in the aged heart. Heart Fail Rev 7(1):63-69
93. Jankowski M, Rachelska G, Donghao W, McCann SM, Gutkowska J (2001) Estrogen receptors activate atrial natriuretic peptide in the rat heart. Proc Natl Acad Sci U S A 98(20):11765-11770
94. Javadov SA, Clarke S, Das M, Griffiths EJ, Lim KH, Halestrap AP (2003) Ischaemic preconditioning inhibits opening of mitochondrial permeability transition pores in the reperfused rat heart. J Physiol 549(Pt 2):513-524
95. Jin ZQ, Zhou HZ, Cecchini G, Gray MO, Karliner JS (2005) MnSOD in mouse heart: acute responses to ischemic preconditioning and ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 288(6):H2986-H2994
96. Judge S, Jang YM, Smith A, Hagen T, Leeuwenburgh C (2005) Age-associated increases in oxidative stress and antioxidant enzyme activities in cardiac interfibrillar mitochondria: implications for the mitochondrial theory of aging. FASEB J 19(3):419-421
97. Juhaszova M, Rabuel C, Zorov DB, Lakatta EG, Sollott SJ (2005) Protection in the aged heart: preventing the heart-break of old age? Cardiovasc Res 66(2):233-244
98. Juhaszova M, Rabuel C, Zorov DB, Lakatta EG, Sollott SJ (2005) Protection in the aged heart: preventing the heart-break of old age? Cardiovasc Res 66:233-244
99. Juhaszova M, Zorov DB, Kim SH, Pepe S, Fu Q, Fishbein KW, Ziman BD, Wang S, Ytrehus K, Antos CL, Olson EN, Sollott SJ (2004) Glycogen synthase kinase-3beta mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore. J Clin Invest 113(11):1535-1549
100. Kabir AM, Clark JE, Tanno M, Cao X, Hothersall JS, Dashnyam S, Gorog DA, Bellahcene M, Shattock MJ, Marber MS (2006) Cardioprotection initiated by reactive oxygen species is dependent on activation of PKCepsilon. Am J Physiol Heart Circ Physiol 291(4):H1893-H1899
101. Kajstura J, Cheng W, Sarangarajan R, Li P, Li B, Nitahara JA, Chapnick S, Reiss K, Olivetti G, Anversa P (1996) Necrotic and apoptotic myoctye cell death in the aging heart of Fischer 344 rats. Am J Physiol 271:H1215-H1228
102. Kaludercic N, Carpi A, Menabà R, Di Lisa F, Paolocci N (2011) Monoamine oxidases (MAO) in the pathogenesis of heart failure and ischemia/reperfusion injury. Biochim Biophys Acta (BBA) - Mol Cell Res 1813(7):1323-1332
103. Kam KW, Qi JS, Chen M, Wong TM (2004) Estrogen reduces cardiac injury and expression of beta1-adrenoceptor upon ischemic insult in the rat heart. J Pharmacol Exp Ther 309(1):8-15
104. Kannel WB, Hjortland MC, McNamara PM, Gordon T (1976) Menopause and risk of cardiovascular disease: the Framingham study. Ann Intern Med 85(4):447-452
105. Kanno T, Sato EE, Muranaka S, Fujita H, Fujiwara T, Utsumi T, Inoue M, Utsumi K (2004) Oxidative stress underlies the mechanism for Ca(2+)-induced permeability transition of mitochondria. Free Radic Res 38(1):27-35
106. Keller ET, Zhang J, Yao Z, Qi Y (2001) The impact of chronic estrogen deprivation on immunologic parameters in the ovariectomized rhesus monkey (Macaca mulatta) model of menopause. J Reprod Immunol 50(1):41
107. Kimura M, Irahara M, Yasui T, Saito S, Tezuka M, Yamano S, Kamada M, Aono T (2002) The obesity in bilateral ovariectomized rats is related to a decrease in the expression of leptin receptors in the brain. Biochem Biophys Res Commun 290(4):1349-1353
108. Kinnally KW, Peixoto PM, Ryu SY, Dejean LM (2010) Is mPTP the gatekeeper for necrosis, apoptosis, or both? Biochim Biophys Acta 1813:616-622
109. Korichneva I, Hoyos B, Chua R, Levi E, Hammerling U (2002) Zinc release from protein kinase C as the common event during activation by lipid second messenger or reactive oxygen. J Biol Chem 277(46):44327-44331
110. Korzick DH, Kostyak JC, Hunter JC, Saupe KW (2007) Local delivery of PKC{varepsilon}-activating peptide mimics ischemic preconditioning in aged hearts through GSK-3beta but not F1-ATPase inactivation. Am J Physiol Heart Circ Physiol 293(4):H2056-H2063. doi: 10.1152/ajpheart.00403.2007
111. Kostyak JC, Hunter JC, Korzick DH (2006) Acute PKCd inhibition limits ischemia-reperfusion injury in the aged rat heart: role of GSK-3β. Cardiovasc Res 70:325-334
112. Kuiper GG, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, Gustafsson JA (1997) Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 138(3):863-870
113. Kumaran S, Subathra M, Balu M, Panneerselvam C (2004) Age-associated decreased activities of mitochondrial electron transport chain complexes in heart and skeletal muscle: role of L-carnitine. Chem Biol Interact 148(1-2):11-18. doi: 10.1016/j.cbi.2003.10.010
114. Kwong LK, Sohal RS (2000) Age-related changes in activities of mitochondrial electron transport complexes in various tissues of the mouse. Arch Biochem Biophys 373(1):16-22. doi: 10.1006/abbi.1999.1495
115. Lakatta EG, Sollott SJ (2002) The «heartbreak» of older age. Mol Interv 2(7):431-446. doi: 10.1124/mi.2.7.431
116. Lakatta EG, Sollott SJ (2002) Perspectives on mammalian cardiovascular aging: humans to molecules. Comp Biochem Physiol A Mol Integr Physiol 132(4):699-721
117. Lancaster TS, Jefferson SJ, Hunter JC, Lopez V, Van Eyk JE, Lakatta EG, Korzick DH (2012) Quantitative proteomic analysis reveals novel mitochondrial targets of estrogen deficiency in the aged female rat heart. Physiol Genomics 44(20):957-969. doi: 10.1152/physiolgenomics.00184.2011
118. Lancaster TS, Jefferson SJ, Korzick DH (2011) Local delivery of a PKCe-activating peptide limits ischemia reperfusion injury in the aged female rat heart. Am J Physiol Regul Integr Comp Physiol 301(5):R1242-R1249. doi: 10.1152/ajpregu.00851.2010
119. Lee TM, Su SF, Chou TF, Lee YT, Tsai CH (2002) Loss of preconditioning by attenuated activation of myocardial ATP-sensitive potassium channels in elderly patients undergoing coronary angioplasty. Circulation 105(3):334-340
120. Lesnefsky EJ, Hoppel CL (2003) Ischemia-reperfusion injury in the aged heart: role of mitochondria. Arch Biochem Biophys 420(2):287-297
121. Lim KH, Javadov SA, Das M, Clarke SJ, Suleiman MS, Halestrap AP (2002) The effects of ischaemic preconditioning, diazoxide and 5-hydroxydecanoate on rat heart mitochondrial volume and respiration. J Physiol 545(Pt 3):961-974
122. Liu L, Azhar G, Gao W, Zhang X, Wei JY (1998) Bcl-2 and Bax expression in adult rat hearts after coronary occlusion: age-associated differences. Am J Physiol 275:R315-R322
123. Liu GS, Thornton J, Van Winkle DM, Stanley AW, Olsson RA, Downey JM (1991) Protection against infarction afforded by preconditioning is mediated by A1 adenosine receptors in rabbit heart. Circulation 84(1):350-356
124. Liu P, Xu B, Cavalieri TA, Hock CE (2002) Age-related difference in myocardial function and inflammation in a rat model of myocardial ischemia-reperfusion. Cardiovasc Res 56(3):443-453
125. Longobardi G, Abete P, Ferrara N, Papa A, Rosiello R, Furgi G, Calabrese C, Cacciatore F, Rengo F (2000) Warm-up phenomenon in adult and elderly patients with coronary artery disease: further evidence of the loss of «ischemic preconditioning» in the aging heart. J Gerontol A Biol Sci Med Sci 55(3):M124-M129
126. Lu R, Hu CP, Deng HW, Li YJ (2001) Calcitonin gene-related peptide-mediated ischemic preconditioning in the rat heart: influence of age. Regul Pept 99(2-3):183-189
127. Manson JE, Hsia J, Johnson KC, Rossouw JE, Assaf AR, Lasser NL, Trevisan M, Black HR, Heckbert SR, Detrano R, Strickland OL, Wong ND, Crouse JR, Stein E, Cushman M (2003) Estrogen plus progestin and the risk of coronary heart disease. N Engl J Med 349(6):523-534
128. Mariani J, Ou R, Bailey M, Rowland M, Nagley P, Rosenfeldt F, Pepe S (2000) Tolerance to ischemia and hypoxia is reduced in aged human myocardium. J Thorac Cardiovasc Surg 120(4):660-667
129. McDonald TG, Van Eyk JE (2003) Mitochondrial proteiomics: undercover in the lipid bilayer. Basic Res Cardiol 98:219-227
130. Meldrum DR (2006) Estrogen increases protective proteins following trauma and hemorrhage. Am J Physiol Regul Integr Comp Physiol 290(3):R809-R811
131. Mendez P, Garcia-Segura LM (2006) Phosphatidylinositol 3-kinase and glycogen synthase kinase 3 regulate estrogen receptor-mediated transcription in neuronal cells. Endocrinology 147:3027-3039
132. Miki T, Cohen MV, Downey JM (1998) Opioid receptor contributes to ischemic preconditioning through protein kinase C activation in rabbits. Mol Cell Biochem 186(1-2):3-12
133. Miller VM, Clarkson TB, Harman SM, Brinton EA, Cedars M, Lobo R, Manson JE, Merriam GR, Naftolin F, Santoro N (2005) Women, hormones, and clinical trials: a beginning, not an end. J Appl Physiol 99(2):381-383
134. Minners J, McLeod CJ, Sack MN (2003) Mitochondrial plasticity in classical ischemic preconditioning - moving beyond the mitochondrial KATP channel. Cardiovasc Res 59(1):1-6
135. Morkuniene R, Arandarcikaite O, Ivanoviene L, Borutaite V (2010) Estradiol-induced protection against ischemia-induced heart mitochondrial damage and caspase activation is mediated by protein kinase G. Biochim Biophys Acta 1797(6-7):1012-1017. doi: 10.1016/j.bbabio.2010.03.027
136. Morrison JH, Brinton RD, Schmidt PJ, Gore AC (2006) Estrogen, menopause, and the aging brain: how basic neuroscience can inform hormone therapy in women. J Neurosci 26(41):10332-10348. doi: 10.1523/jneurosci.3369-06.2006
137. Murphy E (2011) Estrogen signaling and cardiovascular disease. Circ Res 109(6):687-696. doi: 10.1161/circresaha.110.236687
138. Murphy E, Steenbergen C (2007) Gender-based differences in mechanisms of protection in myocardial ischemia-reperfusion injury. Cardiovasc Res 75(3):478-486
139. Murphy E, Steenbergen C (2007) Preconditioning: the mitochondrial connection. Annu Rev Physiol 69:51-67
140. Murry CE, Jennings RB, Reimer KA (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74(5):1124-1136
141. Nadal-Ginard B, Kajstura J, Anversa P, Leri A (2003) A matter of life and death: cardiac myocyte apoptosis and regeneration. J Clin Invest 111(10):1457-1459
142. Nelson HD, Walker M, Zakher B, Mitchell J (2012) Menopausal hormone therapy for the primary prevention of chronic conditions: a systematic review to update the U.S. Preventive Services Task Force Recommendations. Ann Intern Med 157(2):104-113
143. 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(4):769-780. doi: 10.1016/j.yjmcc.2007.01.014
144. Nitta Y, Abe K, Aoki M, Ohno I, Isoyama S (1994) Diminished heat shock protein 70 mRNA induction in aged rat hearts after ischemia. Am J Physiol 267(5 Pt 2):H1795-H1803
145. Novotny JL, Simpson AM, Tomicek NA, Lancaster TL, Korzick DH (2009) Rapid estrogen receptor-α activation improves ischemic tolerance in aged female rats through a novel PKCe-dependent mechanism. Endocrinology 150:889-896
146. 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(3):103-108
147. Ogbi M, Johnson JA (2006) Protein kinase Cepsilon interacts with cytochrome c oxidase subunit IV and enhances cytochrome c oxidase activity in neonatal cardiac myocyte preconditioning. Biochem J 393(Pt 1):191-199
148. O'Rourke B (2004) Evidence for mitochondrial K + channels and their role in cardioprotection. Circ Res 94(4):420-432
149. Oudot A, Martin C, Busseuil D, Vergely C, Demaison L, Rochette L (2006) NADPH oxidases are in part responsible for increased cardiovascular superoxide production during aging. Free Radic Biol Med 40(12):2214-2222
150. Pedram A, Razandi M, Levin ER (2006) Nature of functional estrogen receptors at the plasma membrane. Mol Endocrinol 20(9):1996-2009
151. Pelzer T, Loza PA, Hu K, Bayer B, Dienesch C, Calvillo L, Couse JF, Korach KS, Neyses L, Ertl G (2005) Increased mortality and aggravation of heart failure in estrogen receptor-beta knockout mice after myocardial infarction. Circulation 111(12):1492-1498. doi: 10.1161/01.CIR.0000159262.18512.46
152. Pepe S (2001) Dysfunctional ischemic preconditioning mechanisms in aging. Cardiovasc Res 49(1):11-14
153. 2+ activation of PDH. Am J Physiol 276:H149-H158
154. Peter I, Shearman AM, Vasan RS, Zucker DR, Schmid CH, Demissie S, Cupples A, Kuvin JT, Karas R, Mendelsohn M, Housman DE, Benjamin EJ (2005) Association of estrogen receptor b gene polymorphisms with left ventricular mass and wall thickness in women. Am J Hypertens 18:1388-1395
155. Petrosillo G, Matera M, Moro N, Ruggiero FM, Paradies G (2009) Mitochondrial complex I dysfunction in rat heart with aging: critical role of reactive oxygen species and cardiolipin. Free Radic Biol Med 46(1):88-94. doi: 10.1016/j.freeradbiomed.2008.09.031
156. Phaneuf S, Leeuwenburgh C (2002) Cytochrome c release from mitochondria in the aging heart: a possible mechanism for apoptosis with age. Am J Physiol Regul Integr Comp Physiol 282(2):R423-R430
157. Phillips GB (2005) Is atherosclerotic cardiovascular disease an endocrinological disorder? The estrogen-androgen paradox. J Clin Endocrinol Metab 90:2708-2711
158. Ping P, Takano H, Zhang J, Tang XL, Qiu Y, Li RC, Banerjee S, Dawn B, Balafonova Z, Bolli R (1999) Isoform-selective activation of protein kinase C by nitric oxide in the heart of conscious rabbits: a signaling mechanism for both nitric oxide-induced and ischemia-induced preconditioning. Circ Res 84(5):587-604
159. Preston CC, Oberlin AS, Holmuhamedov EL, Gupta A, Sagar S, Syed RH, Siddiqui SA, Raghavakaimal S, Terzic A, Jahangir A (2008) Aging-induced alterations in gene transcripts and functional activity of mitochondrial oxidative phosphorylation complexes in the heart. Mech Ageing Dev 129(6):304-312
160. Preston CC, Oberlin AS, Holmuhamedov EL, Gupta A, Sagar S, Syed RH, Siddiqui SA, Raghavakaimal S, Terzic A, Jahangir A (2008) Aging-induced alterations in gene transcripts and functional activity of mitochondrial oxidative phosphorylation complexes in the heart. Mech Ageing Dev 129(6):304-312. doi: 10.1016/j.mad.2008.02.010
161. Qiu Y, Ping P, Tang XL (1998) Direct evidence that protein kinase C plays an essential role in the development of late preconditioning against myocardial stunning in conscious rabbits and that e is the isoform involved. J Clin Investig 101:2182-2198
162. Robertson T, Kennard ED, Mehta S, Popma JJ, Carrozza JP Jr, King SB 3rd, Holmes DR, Cowley MJ, Hornung CA, Kent KM, Roubin GS, Litvack F, Moses JW, Safian R, Desvigne-Nickens P, Detre KM (1997) Influence of gender on in-hospital clinical and angiographic outcomes and on one-year follow-up in the New Approaches to Coronary Intervention (NACI) registry. Am J Cardiol 80(10A):26K-39K
163. Roger VL, Go AS, Lloyd-Jones DM, Adams RJ, Berry JD, Brown TM, Carnethon MR, Dai S, de Simone G, Ford ES, Fox CS, Fullerton HJ, Gillespie C, Greenlund KJ, Hailpern SM, Heit JA, Ho PM, Howard VJ, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Makuc DM, Marcus GM, Marelli A, Matchar DB, McDermott MM, Meigs JB, Moy CS, Mozaffarian D, Mussolino ME, Nichol G, Paynter NP, Rosamond WD, Sorlie PD, Stafford RS, Turan TN, Turner MB, Wong ND, Wylie-Rosett J (2011) Heart disease and stroke statistics - 2011 update: a report from the American Heart Association. Circulation 123(4):e18-e209. doi: 10.1161/CIR.0b013e3182009701
164. Rosenberg L, Hennekens CH, Rosner B, Belanger C, Rothman KJ, Speizer FE (1981) Early menopause and the risk of myocardial infarction. Am J Obstet Gynecol 139(1):47-51
165. 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(3):321-333
166. Rossouw JE, Prentice RL, Manson JE, Wu L, Barad D, Barnabei VM, Ko M, LaCroix AZ, Margolis KL, Stefanick ML (2007) Postmenopausal hormone therapy and risk of cardiovascular disease by age and years since menopause. JAMA 297(13):1465-1477
167. Saeedi R, Wambolt RB, Parsons H, Antler C, Leong HS, Keller A, Dunaway GA, Popov KM, Allard MF (2006) Gender and post-ischemic recovery of hypertrophied rat hearts. BMC Cardiovasc Disord 6:8
168. Sakamoto J, Miura T, Goto M, Iimura O (1995) Limitation of myocardial infarct size by adenosine A1 receptor activation is abolished by protein kinase C inhibitors in the rabbit. Cardiovasc Res 29(5):682-688
169. Samali A, Cai J, Zhivotovsky B, Jones DP, Orrenius S (1999) Presence of a pre-apoptotic complex of pro-caspase-3, Hsp60 and Hsp10 in the mitochondrial fraction of jurkat cells. EMBO J 18(8):2040-2048
170. Sanz A, Hiona A, Kujoth GC, Seo AY, Hofer T, Kouwenhoven E, Kalani R, Prolla TA, Barja G, Leeuwenburgh C (2007) Evaluation of sex differences on mitochondrial bioenergetics and apoptosis in mice. Exp Gerontol 42(3):173-182
171. Saunders PT, Maguire SM, Gaughan J, Millar MR (1997) Expression of oestrogen receptor beta (ER beta) in multiple rat tissues visualised by immunohistochemistry. J Endocrinol 154(3):R13-R16
172. Savonenko AV, Markowska AL (2003) The cognitive effects of ovariectomy and estrogen replacement are modulated by aging. Neuroscience 119(3):821-830
173. Schulman D, Latchman DS, Yellon DM (2001) Effect of aging on the ability of preconditioning to protect rat hearts from ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 281(4):H1630-H1636
174. Schultz JE, Rose E, Yao Z, Gross GJ (1995) Evidence for involvement of opioid receptors in ischemic preconditioning in rat hearts. Am J Physiol 268(5 Pt 2):H2157-H2161
175. Schwanke U, Konietzka I, Duschin A, Li X, Schulz R, Heusch G (2002) No ischemic preconditioning in heterozygous connexin43-deficient mice. Am J Physiol Heart Circ Physiol 283(4):H1740-H1742
176. Schwend T, Gustafsson JA (2006) False positives in MALDI-TOF detection of ERbeta in mitochondria. Biochem Biophys Res Commun 343(3):707-711. doi: 10.1016/j.bbrc.2006.02.164
177. Shih CD (2009) 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 16:60. doi: 10.1186/1423-0127-16-60
178. Sniecinski R, Liu H (2004) Reduced efficacy of volatile anesthetic preconditioning with advanced age in isolated rat myocardium. Anesthesiology 100(3):589-597
179. Sone K, Yamamoto-Sawamura T, Kuwahara S, Nishijima K, Ohno T, Aoyama H, Tanaka S (2007) Changes of estrous cycles with aging in female F344/n rats. Exp Anim 56(2):139-148
180. Song X, Li G, Vaage J, Valen G (2003) Effects of sex, gonadectomy, and oestrogen substitution on ischaemic preconditioning and ischaemia-reperfusion injury in mice. Acta Physiol Scand 177(4):459-466
181. Stampfer MJ, Colditz GA, Willett WC, Manson JE, Rosner B, Speizer FE, Hennekens CH (1991) Postmenopausal estrogen therapy and cardiovascular disease. Ten-year follow-up from the Nurses' Health Study. N Engl J Med 325(11):756-762
182. Sullivan TR Jr, Karas RH, Aronovitz M, Faller GT, Ziar JP, Smith JJ, O'Donnell TF Jr, Mendelsohn ME (1995) Estrogen inhibits the response-to-injury in a mouse carotid artery model. J Clin Invest 96(5):2482-2488
183. 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(3):403-411
184. Tani M, Honma Y, Hasegawa H, Tamaki K (2001) Direct activation of mitochondrial K(ATP) channels mimics preconditioning but protein kinase C activation is less effective in middle-aged rat hearts. Cardiovasc Res 49(1):56-68
185. Tani M, Suganuma Y, Hasegawa H, Shinmura K, Ebihara Y, Hayashi Y, Guo X, Takayama M (1997) Decrease in ischemic tolerance with aging in isolated perfused Fischer 344 rat hearts: relation to increases in intracellular Na + after ischemia. J Mol Cell Cardiol 29(11):3081-3089
186. Tani M, Suganuma Y, Hasegawa H, Shinmura K, Hayashi Y, Guo X, Nakamura Y (1997) Changes in ischemic tolerance and effects of ischemic preconditioning in middle-aged rat hearts. Circulation 95(11):2559-2566
187. Tarze A, Deniaud A, Le Bras M, Maillier E, Molle D, Larochette N, Zamzami N, Jan G, Kroemer G, Brenner C (2007) GAPDH, a novel regulator of the pro-apoptotic mitochondrial membrane permeabilization. Oncogene 26(18):2606-2620
188. Tatarkova Z, Kuka S, Racay P, Lehotsky J, Dobrota D, Mistuna D, Kaplan P (2011) Effects of aging on activities of mitochondrial electron transport chain complexes and oxidative damage in rat heart. Physiol Res 60(2):281-289
189. Tiravanti E, Samouilov A, Zweier JL (2004) Nitrosyl-heme complexes are formed in the ischemic heart: evidence of nitrite-derived nitric oxide formation, storage, and signaling in post-ischemic tissues. J Biol Chem 279(12):11065-11073
190. Tomicek NJ, Miller-Lee JL, Hunter JC, Korzick DH (2013) Estrogen receptor beta does not influence ischemic tolerance in the aged female rat heart. Cardiovasc Ther 31(1):32-37. doi: 10.1111/j.1755-5922.2011.00288.x
191. Tong H, Imahashi K, Steenbergen C, Murphy E (2002) Phosphorylation of glycogen synthase kinase-3beta during preconditioning through a phosphatidylinositol-3-kinase-dependent pathway is cardioprotective. Circ Res 90(4):377-379
192. Toninello A, Salvi M, Pietrangeli P, Mondovi B (2004) Biogenic amines and apoptosis: minireview article. Amino Acids 26:339-343
193. Too CK, Giles A, Wilkinson M (1999) Estrogen stimulates expression of adenine nucleotide translocator ANT1 messenger RNA in female rat hearts. Mol Cell Endocrinol 150(1-2):161-167
194. Treloar AE (1981) Menstrual cyclicity and the pre-menopause. Maturitas 3(3-4):249-264
195. Turrens JF, Boveris A (1980) Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochem J 191(2):421-427
196. Urata Y, Ihara Y, Murata H, Goto S, Koji T, Yodoi J, Inoue S, Kondo T (2006) 17B-estradiol protects against oxidative stress-induced cell death through the glutathione/glutaredoxin-dependent redox regulation of Akt in myocardiac H9c2 cells. J Biol Chem 281:13092-13102
197. van der Loo B, Bachschmid M, Labugger R, Schildknecht S, Kilo J, Hahn R, Palacios-Callender M, Luscher TF (2005) Expression and activity patterns of nitric oxide synthases and antioxidant enzymes reveal a substantial heterogeneity between cardiac and vascular aging in the rat. Biogerontology 6(5):325-334
198. Villablanca A, Lubahn D, Shelby L, Lloyd K, Barthold S (2004) Susceptibility to early atherosclerosis in male mice is mediated by estrogen receptor a. Arterioscler Thromb Vasc Biol 24:1055-1061
199. Wall TM, Sheehy R, Hartman JC (1994) Role of bradykinin in myocardial preconditioning. J Pharmacol Exp Ther 270(2):681-689
200. Wang M, Crisostomo PR, Markel T, Wang Y, Lillemoe KD, Meldrum DR (2008) Estrogen receptor beta mediates acute myocardial protection following ischemia. Surgery 144(2):233-238. doi: 10.1016/j.surg.2008.03.009
201. 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
202. Wang M, Tsai BM, Reiger KM, Brown JW, Meldrum DR (2006) 17-b-Estradiol decreases p38 MAPK-mediated myocardial inflammation and dysfunction following acute ischemia. J Mol Cell Cardiol 40:205-212
203. 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(4):R972-R978. doi: 10.1152/ajpregu.00045.2009
204. Wang P, Zweier JL (1996) Measurment of nitric oxide and peroxynitrite generation in the postischemic heart. J Biol Chem 271(46):29223-29230
205. Weiss G, Skurnick JH, Goldsmith LT, Santoro NF, Park SJ (2004) Menopause and hypothalamic-pituitary sensitivity to estrogen. JAMA 292(24):2991-2996. doi: 10.1001/jama.292.24.2991
206. Wenger NK, Shaw LJ, Vaccarino V (2008) Coronary heart disease in women: update 2008. Clin Pharmacol Ther 83(1):37-51
207. Willems L, Zatta A, Holmgren K, Ashton KJ, Headrick JP (2005) Age-related changes in ischemic tolerance in male and female mouse hearts. J Mol Cell Cardiol 38(2):245-256
208. Wood CE, Sitruk-Ware RL, Tsong YY, Register TC, Lees CJ, Cline JM (2007) Effects of estradiol with oral or intravaginal progesterone on risk markers for breast cancer in a postmenopausal monkey model. Menopause 14(4):639-647
209. Wu JM, Zelinski MB, Ingram DK, Ottinger MA (2005) Ovarian aging and menopause: current theories, hypotheses, and research models. Exp Biol Med (Maywood) 230(11):818-828
210. Wuest JH Jr, Dry TJ, Edwards JE (1953) The degree of coronary atherosclerosis in bilaterally oophorectomized women. Circulation 7(6):801-809
211. Xia Y, Khatchikian G, Zweier JL (1996) Adenosine deaminase inhibition prevents free radical-mediated injury in the postischemic heart. J Biol Chem 271(17):10096-10102
212. Xu Y, Arenas IA, Armstrong SJ, Davidge ST (2003) Estrogen modulation of left ventricular remodeling in the aged heart. Cardiovasc Res 57(2):388-394
213. Xu Y, Armstrong SJ, Arenas IA, Pehowich DJ, Davidge ST (2004) Cardioprotection by chronic estrogen or superoxide dismutase mimetic treatment in the aged female rat. Am J Physiol Heart Circ Physiol 287(1):H165-H171
214. Yamashita N, Hoshida S, Taniguchi N, Kuzuya T, Hori M (1998) A «second window of protection» occurs 24 h after ischemic preconditioning in the rat heart. J Mol Cell Cardiol 30(6):1181-1189
215. Yang SH, Liu R, Perez EJ, Wen Y, Stevens SM Jr, Valencia T, Brun-Zinkernagel AM, Prokai L, Will Y, Dykens J, Koulen P, Simpkins JW (2004) Mitochondrial localization of estrogen receptor beta. Proc Natl Acad Sci U S A 101(12):4130-4135. doi: 10.1073/pnas.0306948101
216. Yasmin W, Strynadka KD, Schulz R (1997) Generation of peroxynitrite contributes to ischemia-reperfusion injury in isolated rat hearts. Cardiovasc Res 33(2):422-432
217. Yin W, Gore AC (2006) Neuroendocrine control of reproductive aging: roles of GnRH neurons. Reproduction 131(3):403-414. doi: 10.1530/rep.1.00617
218. Yu W, Dahl G, Werner R (1994) The connexin43 gene is responsive to oestrogen. Proc Biol Sci 255(1343):125-132
219. Zhai P, Eurell TE, Cotthaus R, Jeffery EH, Bahr JM, Gross DR (2000) Effect of estrogen on global myocardial ischemia-reperfusion injury in female rats. Am J Physiol Heart Circ Physiol 279:H2766-H2775
220. Zhai P, Eurell TE, Cotthaus RP, Jeffery EH, Bahr JM, Gross DR (2001) Effects of dietary phytoestrogen on global myocardial ischemia-reperfusion injury in isolated female rat hearts. Am J Physiol Heart Circ Physiol 281(3):H1223-H1232
221. Zhang Y, Chong E, Herman B (2002) Age-associated increases in the activity of multiple caspases in Fisher 344 rat organs. Exp Gerontol 37(6):777-789
222. Zhang J, Liem DA, Mueller M, Wang Y, Zong C, Deng N, Vondriska TM, Korge P, Drews O, MacLellan WR, Honda H, Weiss JN, Apweiler R, Ping P (2008) Altered proteome biology of cardiac mitochondria under stress conditions. J Proteome Res 7(6):2204-2214. doi: 10.1021/pr070371f
223. Zhang D, Trudeau VL (2006) Integration of membrane and nuclear estrogen receptor signaling. Comp Biochem Physiol A Mol Integr Physiol 144:306-315
224. Zhao ZQ, Corvera JS, Halkos ME, Kerendi F, Wang NP, Guyton RA, Vinten-Johansen J (2003) Inhibition of myocardial injury by ischemic postconditioning during reperfusion: comparison with ischemic preconditioning. Am J Physiol Heart Circ Physiol 285(2):H579-H588
225. Zhao X, Eghbali-Webb M (2002) Gender-related differences in basal and hypoxia-induced activation of signal transduction pathways controlling cell cycle progression and apoptosis, in cardiac fibroblasts. Endocrine 18(2):137-145
226. Zhao L, O'Neill K, Brinton RD (2006) Estrogenic agonist activity of ICI 182,780 (Faslodex) in hippocampal neurons: implications for basic science understanding of estrogen signaling and development of estrogen modulators with a dual therapeutic profile. J Pharmacol Exp Ther 319(3):1124-1132
227. Zhao ZQ, Vinten-Johansen J (2002) Myocardial apoptosis and ischemic preconditioning. Cardiovasc Res 55(3):438-455
228. Zorov DB, Juhaszova M, Yaniv Y, Nuss HB, Wang S, Sollott SJ (2009) Regulation and pharmacology of the mitochondrial permeability transition pore. Cardiovasc Res 83(2):213-225
229. Zweier JL, Talukder MA (2006) The role of oxidants and free radicals in reperfusion injury. Cardiovasc Res 70(2):181-190