Estrogen regulation of protein expression and signaling pathways in the heart

Biology of Sex Differences

Volumn 5, Issue 1, 2014, Pages

  Murphy, Elizabeth ^a   Steenbergen, Charles ^b  

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

^b JHMI   (United States)

Author keywords

Cardiac; Estrogen; Ischemia reperfusion; Metabolism

Indexed keywords

EID: 84927944141     PISSN: None     EISSN: 20426410     Source Type: Journal    
DOI: 10.1186/2042-6410-5-6     Document Type: Review

References (81)

1. Ji H, Zheng W, Wu X, Liu J, Ecelbarger CM, Watkins R, Arnold AP, Sandberg K: Sex chromosome effects unmasked in angiotensin II-induced hypertension. Hypertension 2010, 55(5):1275-1282.
2. Murphy E: Estrogen signaling and cardiovascular disease. Circ Res 2011, 109(6):687-696.
3. Liu D, Deschamps A, Korach KS, Murphy E: Estrogen-enhanced gene expression of lipoprotein lipase in heart is antagonized by progesterone. Endocrinology 2008, 149(2):711-716.
4. Evangelista AM, Deschamps AM, Liu D, Raghavachari N, Murphy E: miR-222 contributes to sex-dimorphic cardiac eNOS expression via ets-1. Physiol Genomics 2013, 45(12):493-498.
5. Kim KH, Toomre D, Bender JR: Splice isoform estrogen receptors as integral transmembrane proteins. Mol Biol Cell 2011, 22(22):4415-4423.
6. Revankar CM, Cimino DF, Sklar LA, Arterburn JB, Prossnitz ER: A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 2005, 307(5715):1625-1630.
7. Deschamps AM, Murphy E: Activation of a novel estrogen receptor, GPER, is cardioprotective in male and female rats. Am J Physiol Heart Circ Physiol 2009, 297(5):H1806-H1813.
8. Hsieh YC, Yang S, Choudhry MA, Yu HP, Rue LW III, Bland KI, Chaudry IH: PGC-1 upregulation via estrogen receptors: a common mechanism of salutary effects of estrogen and flutamide on heart function after trauma-hemorrhage. Am J Physiol Heart Circ Physiol 2005, 289(6):H2665-H2672.
9. Yu W, Dahl G, Werner R: The connexin43 gene is responsive to oestrogen. Proc Biol Sci 1994, 255(1343):125-132.
10. Chung TH, Wang SM, Wu JC: 17beta-estradiol reduces the effect of metabolic inhibition on gap junction intercellular communication in rat cardiomyocytes via the estrogen receptor. J Mol Cell Cardiol 2004, 37(5):1013-1022.
11. Too CK, Giles A, Wilkinson M: Estrogen stimulates expression of adenine nucleotide translocator ANT1 messenger RNA in female rat hearts. Mol Cell Endocrinol 1999, 150(1-2):161-167.
12. Voss MR, Stallone JN, Li M, Cornelussen RN, Knuefermann P, Knowlton AA: Gender differences in the expression of heat shock proteins: the effect of estrogen. Am J Physiol Heart Circ Physiol 2003, 285(2):H687-H692.
13. Pedram A, Razandi M, Aitkenhead M, Levin ER: Estrogen inhibits cardiomyocyte hypertrophy in vitro: antagonism of calcineurin-related hypertrophy through induction of MCIP1. J Biol Chem 2005, 280(28):26339-26348.
14. Gaborit N, Andras V, Le Bouter S, Szuts V, Escande D, Nattel S, Demolombe S: Gender-related differences in ion-channel and transporter subunit expression in non-diseased human hearts. J Mol Cell Cardiol 2010, 49(4):639-646.
15. Ambrosi CM, Yamada KA, Nerbonne JM, Efimov IR: Gender differences in electrophysiological gene expression in failing and non-failing human hearts. PLoS One 2013, 8(1):e54635.
16. Otsuki M, Gao H, Dahlman-Wright K, Ohlsson C, Eguchi N, Urade Y, Gustafsson JA: Specific regulation of lipocalin-type prostaglandin D synthase in mouse heart by estrogen receptor beta. Mol Endocrinol 2003, 17(9):1844-1855.
17. Pinho FG, Frampton AE, Nunes J, Krell J, Alshaker H, Jacob J, Pellegrino L, Roca-Alonso L, de Giorgio A, Harding V, Waxman J, Stebbing J, Pchejetski D, Castellano L: Downregulation of microRNA-515-5p by the estrogen receptor modulates sphingosine kinase 1 and breast cancer cell proliferation. Cancer Res 2013, 73(19):5936-5948.
18. Di Leva G, Piovan C, Gasparini P, Ngankeu A, Taccioli C, Briskin D, Cheung DG, Bolon B, Anderlucci L, Alder H, Nuovo G, Li M, Iorio MV, Galasso M, Santhanam R, Marcucci G, Perrotti D, Powell KA, Bratasz A, Garofalo M, Nephew KP, Croce CM: Estrogen mediated-activation of miR-191/425 cluster modulates tumorigenicity of breast cancer cells depending on estrogen receptor status. PLoS Genet 2013, 9(3):e1003311.
19. Kim K, Madak-Erdogan Z, Ventrella R, Katzenellenbogen BS: A MicroRNA196a2∗and TP63 circuit regulated by estrogen receptor-alpha and ERK2 that controls breast cancer proliferation and invasiveness properties. Horm Cancer 2013, 4(2):78-91.
20. Queiros AM, Eschen C, Fliegner D, Kararigas G, Dworatzek E, Westphal C, Sanchez Ruderisch H, Regitz-Zagrosek V: Sex-and estrogen-dependent regulation of a miRNA network in the healthy and hypertrophied heart. Int J Cardiol 2013, 169(5):331-338.
21. Zhang Y, Wang R, Du W, Wang S, Yang L, Pan Z, Li X, Xiong X, He H, Shi Y, Liu X, Yu S, Bi Z, Lu Y, Shan H: Downregulation of miR-151-5p contributes to increased susceptibility to arrhythmogenesis during myocardial infarction with estrogen deprivation. PLoS One 2013, 8(9):e72985.
22. Zhao J, Imbrie GA, Baur WE, Iyer LK, Aronovitz MJ, Kershaw TB, Haselmann GM, Lu Q, Karas RH: Estrogen receptor-mediated regulation of microRNA inhibits proliferation of vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 2012, 33(2):257-265.
23. Gabel SA, Chen J, Petranka JG, Yamamura K, Walker VR, London RE, Korach KS, Steenbergen C, Murphy: Estrogen receptor beta mediates gender differences in ischemia reperfusion injury. J Mol Cell Cardiol 2003, 35(6):A16-A.
24. Nikolic I, Liu D, Bell JA, Collins J, Steenbergen C, Murphy E: Treatment with an estrogen receptor-beta-selective agonist is cardioprotective. J Mol Cell Cardiol 2007, 42(4):769-780.
25. O'Lone R, Knorr K, Jaffe IZ, Schaffer ME, Martini PG, Karas RH, Bienkowska J, Mendelsohn ME, Hansen U: Estrogen receptors alpha and beta mediate distinct pathways of vascular gene expression, including genes involved in mitochondrial electron transport and generation of reactive oxygen species. Mol Endocrinol 2007, 21(6):1281-1296.
26. Lindberg MK, Moverare S, Skrtic S, Gao H, Dahlman-Wright K, Gustafsson JA, Ohlsson C: Estrogen receptor (ER)-beta reduces ER alpha-regulated gene transcription, supporting a "ying yang" relationship between ER alpha and ER beta in mice. Mol Endocrinol 2003, 17(2):203-208.
27. Barros RP, Machado UF, Warner M, Gustafsson JA: Muscle GLUT4 regulation by estrogen receptors ERbeta and ERalpha. Proc Natl Acad Sci USA 2006, 103(5):1605-1608.
28. Tsutsumi S, Zhang X, Takata K, Takahashi K, Karas RH, Kurachi H, Mendelsohn ME: Differential regulation of the inducible nitric oxide synthase gene by estrogen receptors 1 and 2. J Endocrinol 2008, 199(2):267-273.
29. 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: Sex-specific pathways in early cardiac response to pressure overload in mice. J Mol Med (Berl) 2008, 86(9):1013-1024.
30. Kararigas G, Bito V, Tinel H, Becher E, Baczko I, Knosalla C, Albrecht-Kupper B, Sipido KR, Regitz-Zagrosek V: Transcriptome characterization of estrogen-treated human myocardium identifies myosin regulatory light chain interacting protein as a sex-specific element influencing contractile function. J Am Coll Cardiol 2012, 59(4):410-417.
31. Kararigas G, Becher E, Mahmoodzadeh S, Knosalla C, Hetzer R, Regitz-Zagrosek V: Sex-specific modification of progesterone receptor expression by 17beta-oestradiol in human cardiac tissues. Biol Sex Differ 2010, 1(1):2.
32. Jakacka M, Ito M, Weiss J, Chien PY, Gehm BD, Jameson JL: Estrogen receptor binding to DNA is not required for its activity through the nonclassical AP1 pathway. J Biol Chem 2001, 276(17):13615-13621.
33. von Harsdorf R, Edwards JG, Shen YT, Kudej RK, Dietz R, Leinwand LA, Nadal-Ginard B, Vatner SF: Identification of a cis-acting regulatory element conferring inducibility of the atrial natriuretic factor gene in acute pressure overload. J Clin Invest 1997, 100(5):1294-1304.
34. Chen Q, Williams R, Healy CL, Wright CD, Wu SC, O'Connell TD: An association between gene expression and better survival in female mice following myocardial infarction. J Mol Cell Cardiol 2010, 49(5):801-811.
35. Banke NH, Yan L, Pound KM, Dhar S, Reinhardt H, De Lorenzo MS, Vatner SF, Lewandowski ED: Sexual dimorphism in cardiac triacylglyceride dynamics in mice on long term caloric restriction. J Mol Cell Cardiol 2012, 52(3):733-740.
36. Simoncini T, Hafezi-Moghadam A, Brazil DP, Ley K, Chin WW, Liao JK: Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature 2000, 407(6803):538-541.
37. Lagranha CJ, Deschamps A, Aponte A, Steenbergen C, Murphy E: Sex differences in the phosphorylation of mitochondrial proteins result in reduced production of reactive oxygen species and cardioprotection in females. Circ Res 2010, 106(11):1681-1691.
38. McKee LA, Chen H, Regan JA, Behunin SM, Walker JW, Walker JS, Konhilas JP: Sexually dimorphic myofilament function and cardiac troponin I phosphospecies distribution in hypertrophic cardiomyopathy mice. Arch Biochem Biophys 2013, 535(1):39-48.
39. 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: Gender-specific proteomic alterations in glycolytic and mitochondrial pathways in aging monkey hearts. J Mol Cell Cardiol 2004, 37(5):921-929.
40. Sun J, Picht E, Ginsburg KS, Bers DM, Steenbergen C, Murphy E: Hypercontractile female hearts exhibit increased S-nitrosylation of the L-type Ca2+ channel alpha1 subunit and reduced ischemia/reperfusion injury. Circ Res 2006, 98(3):403-411.
41. Lin J, Steenbergen C, Murphy E, Sun J: Estrogen receptor-beta activation results in S-nitrosylation of proteins involved in cardioprotection. Circulation 2009, 120(3):245-254.
42. Parks RJ, Howlett SE: Sex differences in mechanisms of cardiac excitation-contraction coupling. Pflugers Arch 2013, 465(5):747-763.
43. Yang PC, Clancy CE: Effects of sex hormones on cardiac repolarization. J Cardiovasc Pharmacol 2010, 56(2):123-129.
44. Yang PC, Clancy CE: Gender-based differences in cardiac diseases. J Biomed Res 2011, 25(2):81-89.
45. Drici MD, Burklow TR, Haridasse V, Glazer RI, Woosley RL: Sex hormones prolong the QT interval and downregulate potassium channel expression in the rabbit heart. Circulation 1996, 94(6):1471-1474.
46. Saito T, Ciobotaru A, Bopassa JC, Toro L, Stefani E, Eghbali M: Estrogen contributes to gender differences in mouse ventricular repolarization. Circ Res 2009, 105(4):343-352.
47. Lowe JS, Stroud DM, Yang T, Hall L, Atack TC, Roden DM: Increased late sodium current contributes to long QT-related arrhythmia susceptibility in female mice. Cardiovasc Res 2012, 95(3):300-307.
48. Sims C, Reisenweber S, Viswanathan PC, Choi BR, Walker WH, Salama G: Sex, age, and regional differences in L-type calcium current are important determinants of arrhythmia phenotype in rabbit hearts with drug-induced long QT type 2. Circ Res 2008, 102(9):e86-e100.
49. Iacobas DA, Iacobas S, Thomas N, Spray DC: Sex-dependent gene regulatory networks of the heart rhythm. Funct Integr Genomics 2010, 10(1):73-86.
50. Imahashi K, London RE, Steenbergen C, Murphy E: Male/female differences in intracellular Na + regulation during ischemia/reperfusion in mouse heart. J Mol Cell Cardiol 2004, 37(3):747-753.
51. Curl CL, Wendt IR, Kotsanas G: Effects of gender on intracellular. Pflugers Arch 2001, 441(5):709-716.
52. Chen J, Petranka J, Yamamura K, London RE, Steenbergen C, Murphy E: Gender differences in sarcoplasmic reticulum calcium loading after isoproterenol. Am J Physiol Heart Circ Physiol 2003, 285(6):H2657-H2662.
53. Patrizio M, Musumeci M, Piccone A, Raggi C, Mattei E, Marano G: Hormonal regulation of beta-myosin heavy chain expression in the mouse left ventricle. J Endocrinol 2013, 216(3):287-296.
54. Gorres BK, Bomhoff GL, Morris JK, Geiger PC: In vivo stimulation of oestrogen receptor alpha increases insulin-stimulated skeletal muscle glucose uptake. J Physiol 2011, 589(Pt 8):2041-2054.
55. Arias-Loza PA, Kreissl MC, Kneitz S, Kaiser FR, Israel I, Hu K, Frantz S, Bayer B, Fritzemeier KH, Korach KS, Pelzer T: The estrogen receptor-alpha is required and sufficient to maintain physiological glucose uptake in the mouse heart. Hypertension 2012, 60(4):1070-1077.
56. Geer EB, Shen W, Strohmayer E, Post KD, Freda PU: Body composition and cardiovascular risk markers after remission of Cushing's disease: a prospective study using whole-body MRI. J Clin Endocrinol Metab 2012, 97(5):1702-1711.
57. Margolis KL, Bonds DE, Rodabough RJ, Tinker L, Phillips LS, Allen C, Bassford T, Burke G, Torrens J, Howard BV, Investigat WsHI: Effect of oestrogen plus progestin on the incidence of diabetes in postmenopausal women: results from the Women's Health Initiative Hormone Trial. Diabetologia 2004, 47(7):1175-1187.
58. Shi HF, Seeley RJ, Clegg DJ: Sexual differences in the control of energy homeostasis. Front Neuroendocrinol 2009, 30(3):396-404.
59. Banke NH, Pound KM, DeLorenzo MS, Yan L, Reinhardt HA, Vatner DE, Vatner SF, Lewandowski ED: Gender distinguishes myocardial triacylglyceride dynamics in response to long term caloric restriction in mice. Circulation 2009, 120(18):S893-S.
60. Lyons MR, Peterson LR, McGill JB, Herrero P, Coggan AR, Saeed IM, Recklein C, Schechtman KB, Gropler RJ: Impact of sex on the heart's metabolic and functional responses to diabetic therapies. Am J Physiol Heart Circ Physiol 2013, 305(11):H1584-H1591.
61. Yang XP, Reckelhoff JF: Estrogen, hormonal replacement therapy and cardiovascular disease. Curr Opin Nephrol Hypertens 2011, 20(2):133-138.
62. Harman SM, Vittinghoff E, Brinton EA, Budoff MJ, Cedars MI, Lobo RA, Merriam GR, Miller VM, Naftolin F, Pal L, Santoro N, Taylor HS, Black DM: Timing and duration of menopausal hormone treatment may affect cardiovascular outcomes. Am J Med 2011, 124(3):199-205.
63. Manson JE, Chlebowski RT, Stefanick ML, Aragaki AK, Rossouw JE, Prentice RL, Anderson G, Howard BV, Thomson CA, LaCroix AZ, Wactawski-Wende J, Jackson RD, Limacher M, Margolis KL, Wassertheil-Smoller S, Beresford SA, Cauley JA, Eaton CB, Gass M, Hsia J, Johnson KC, Kooperberg C, Kuller LH, Lewis CE, Liu S, Martin LW, Ockene JK, O'Sullivan MJ, Powell LH, Simon MS, et al: Menopausal hormone therapy and health outcomes during the intervention and extended poststopping phases of the Women's Health Initiative randomized trials. JAMA 2013, 310(13):1353-1368.
64. Prentice RL, Manson JE, Langer RD, Anderson GL, Pettinger M, Jackson RD, Johnson KC, Kuller LH, Lane DS, Wactawski-Wende J, Brzyski R, Allison M, Ockene J, Sarto G, Rossouw JE: Benefits and risks of postmenopausal hormone therapy when it is initiated soon after menopause. Am J Epidemiol 2009, 170(1):12-23.
65. Barrett-Connor E: Hormones and heart disease in women: the timing hypothesis. Am J Epidemiol 2007, 166(5):506-510.
66. Toh S, Hernandez-Diaz S, Logan R, Rossouw JE, Hernan MA: Coronary heart disease in postmenopausal recipients of estrogen plus progestin therapy: does the increased risk ever disappear? A randomized trial. Ann Intern Med 2010, 152(4):211-217.
67. Bae S, 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 2005, 315(3):1125-1135.
68. Przyklenk K, Ovize M, Bauer B, Kloner RA: Gender does not influence acute myocardial infarction in adult dogs. Am Heart J 1995, 129(6):1108-1113.
69. Cross HR, Murphy E, Steenbergen C: Ca(2+) loading and adrenergic stimulation reveal male/female differences in susceptibility to ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 2002, 283(2):H481-H489.
70. Wang M, Crisostomo P, Wairiuko GM, Meldrum DR: Estrogen receptor-alpha mediates acute myocardial protection in females. Am J Physiol Heart Circ Physiol 2006, 290(6):H2204-H2209.
71. Zhai P, Eurell TE, Cooke PS, Lubahn DB, Gross DR: Myocardial ischemia-reperfusion injury in estrogen receptor-alpha knockout and wild-type mice. Am J Physiol Heart Circ Physiol 2000, 278(5):H1640-H1647.
72. Booth EA, Marchesi M, Kilbourne EJ, Lucchesi BR: 17Beta-estradiol as a receptor-mediated cardioprotective agent. J Pharmacol Exp Ther 2003, 307(1):395-401.
73. Hsieh YC, Choudhry MA, Yu HP, Shimizu T, Yang S, Suzuki T, Chen J, Bland KI, Chaudry IH: Inhibition of cardiac PGC-1alpha expression abolishes ERbeta agonist-mediated cardioprotection following trauma-hemorrhage. FASEB J 2006, 20(8):1109-1117.
74. Pare G, Krust A, Karas RH, Dupont S, Aronovitz M, Chambon P, Mendelsohn ME: Estrogen receptor-alpha mediates the protective effects of estrogen against vascular injury. Circ Res 2002, 90(10):1087-1092.
75. Zhu Y, Bian Z, Lu P, Karas RH, Bao L, Cox D, Hodgin J, Shaul PW, Thoren P, Smithies O, Gustafsson JA, Mendelsohn ME: Abnormal vascular function and hypertension in mice deficient in estrogen receptor beta. Science 2002, 295(5554):505-508.
76. Bopassa JC, Eghbali M, Toro L, Stefani E: A novel estrogen receptor GPER inhibits mitochondria permeability transition pore opening and protects the heart against ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 2010, 298(1):H16-H23.
77. Chambliss KL, Wu Q, Oltmann S, Konaniah ES, Umetani M, Korach KS, Thomas GD, Mineo C, Yuhanna IS, Kim SH, Madak-Erdogan Z, Maggi A, Dineen SP, Roland CL, Hui DY, Brekken RA, Katzenellenbogen JA, Katzenellenbogen BS, Shaul PW: Non-nuclear estrogen receptor alpha signaling promotes cardiovascular protection but not uterine or breast cancer growth in mice. J Clin Invest 2010, 120(7):2319-2330.
78. Skavdahl M, Steenbergen C, Clark J, Myers P, Demianenko T, Mao L, Rockman HA, Korach KS, Murphy E: Estrogen receptor-beta mediates male-female differences in the development of pressure overload hypertrophy. Am J Physiol Heart Circ Physiol 2005, 288(2):H469-H476.
79. van Eickels M, Grohe C, Cleutjens JP, Janssen BJ, Wellens HJ, Doevendans PA: 17beta-estradiol attenuates the development of pressure-overload hypertrophy. Circulation 2001, 104(12):1419-1423.
80. Martensson UE, Salehi SA, Windahl S, Gomez MF, Sward K, Daszkiewicz-Nilsson J, Wendt A, Andersson N, Hellstrand P, Grande PO, Owman C, Rosen CJ, Adamo ML, Lundquist I, Rorsman P, Nilsson BO, Ohlsson C, Olde B, Leeb-Lundberg LM: Deletion of the G protein-coupled receptor 30 impairs glucose tolerance, reduces bone growth, increases blood pressure, and eliminates estradiol-stimulated insulin release in female mice. Endocrinology 2009, 150(2):687-698.
81. Kang S, Liu Y, Sun D, Zhou C, Liu A, Xu C, Hao Y, Li D, Yan C, Sun H: Chronic activation of the G protein-coupled receptor 30 with agonist G-1 attenuates heart failure. PLoS One 2012, 7(10):e48185.