17-β estradiol attenuates ovariectomy-induced changes in cardiomyocyte contractile function via activation of AMP-activated protein kinase

Toxicology Letters

Volumn 232, Issue 1, 2015, Pages 253-262

  Turdi, Subat ^a   Huff, Anna F ^a   Pang, Jiaojiao ^a,b   He, Emily Y ^a   Chen, Xiyao ^a,c   Wang, Shuyi ^a   Chen, Yuguo ^b   Zhang, Yingmei ^a   Ren, Jun ^a,c  

^a UNIVERSITY OF WYOMING COLLEGE OF HEALTH SCIENCES   (United States)

^b SHANDONG UNIVERSITY   (China)

^c FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

AMPK; Cardiomyocyte; Contractile Function; Estrogen; Estrogen replacement

Indexed keywords

CALCIUM ION; ESTRADIOL; GLUCOSE TRANSPORTER 4; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PEPTIDES AND PROTEINS; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN ACC; PROTEIN AS160; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; ACETYL COENZYME A CARBOXYLASE; AMPK ALPHA2 SUBUNIT, MOUSE; PROTEIN KINASE B;

ADULT; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; ESTROGEN DEFICIENCY; FEMALE; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; MOUSE; NONHUMAN; OVARIECTOMY; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CALCIUM SIGNALING; CARDIAC MUSCLE CELL; DEFICIENCY; DRUG EFFECTS; ENZYMOLOGY; ESTROGEN THERAPY; GENETICS; HEART CONTRACTION; ISOLATED HEART; KNOCKOUT MOUSE; METABOLISM; PHOSPHORYLATION;

ACETYL-COA CARBOXYLASE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CALCIUM SIGNALING; ENZYME ACTIVATION; ESTRADIOL; ESTROGEN REPLACEMENT THERAPY; FEMALE; ISOLATED HEART PREPARATION; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; OVARIECTOMY; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT;

EID: 84911448052     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2014.11.012     Document Type: Article

References (46)

1. Beauloye C., Bertrand L., Horman S., Hue L. AMPK activation, a preventive therapeutic target in the transition from cardiac injury to heart failure. Cardiovasc. Res. 2011, 90:224-233.
2. Beer S., Reincke M., Kral M., Callies F., Stromer H., Dienesch C., Steinhauer S., Ertl G., Allolio B., Neubauer S. High-dose 17beta-estradiol treatment prevents development of heart failure post-myocardial infarction in the rat. Basic Res. Cardiol. 2007, 102:9-18.
3. Bendale D.S., Karpe P.A., Chhabra R., Shete S.P., Shah H., Tikoo K. 17-beta estradiol prevents cardiovascular dysfunction in post-menopausal metabolic syndrome by involving SIRT1/AMPK/H3 acetylation. Br. J. Pharmacol. 2013, 170:779-795.
4. D'Eon T.M., Rogers N.H., Stancheva Z.S., Greenberg A.S. Estradiol and the estradiol metabolite, 2-hydroxyestradiol, activate AMP-activated protein kinase in C2C12 myotubes. Obesity 2008, 16:1284-1288.
5. D'Eon T.M., Souza S.C., Aronovitz M., Obin M.S., Fried S.K., Greenberg A.S. Estrogen regulation of adiposity and fuel partitioning. Evidence of genomic and non-genomic regulation of lipogenic and oxidative pathways. J. Biol. Chem. 2005, 280:35983-35991.
6. Doser T.A., Turdi S., Thomas D.P., Epstein P.N., Li S.Y., Ren J. Transgenic overexpression of aldehyde dehydrogenase-2 rescues chronic alcohol intake-induced myocardial hypertrophy and contractile dysfunction. Circulation 2009, 119:1941-1949.
7. 2+ response between estrogen and phytoestrogen alpha-zearalanol in ventricular myocytes. Endocrine 2004, 24:33-38.
8. Duan J., Esberg L.B., Ye G., Borgerding A.J., Ren B.H., Aberle N.S., Epstein P.N., Ren J. Influence of gender on ethanol-induced ventricular myocyte contractile depression in transgenic mice with cardiac overexpression of alcohol dehydrogenase. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2003, 134:607-614.
9. Funai K., Cartee G.D. Inhibition of contraction-stimulated AMP-activated protein kinase inhibits contraction-stimulated increases in PAS-TBC1D1 and glucose transport without altering PAS-AS160 in rat skeletal muscle. Diabetes 2009, 58:1096-1104.
10. Gnatuk C.L. The controversy over estrogen replacement therapy: an update on clinical trials. Curr. Women's Health Rep. 2002, 2:89-94.
11. Gorres B.K., Bomhoff G.L., Morris J.K., Geiger P.C. In vivo stimulation of oestrogen receptor alpha increases insulin-stimulated skeletal muscle glucose uptake. J. Physiol. 2011, 589:2041-2054.
12. Hardie D.G. AMPK: a key regulator of energy balance in the single cell and the whole organism. Int. J. Obes. 2008, 32(Suppl. 4):S7-12.
13. Hardie D.G., Carling D., Carlson M. The AMP-activated/SNF1 protein kinase subfamily: metabolic sensors of the eukaryotic cell?. Ann. Rev. Biochem. 1998, 67:821-855.
14. Heidenreich P.A., Trogdon J.G., Khavjou O.A., Butler J., Dracup K., Ezekowitz M.D., Finkelstein E.A., Hong Y., Johnston S.C., Khera A., Lloyd-Jones D.M., Nelson S.A., Nichol G., Orenstein D., Wilson P.W., Woo J., American Heart Association Advocacy Coordinating Committee, Stroke Council, Council on Cardiovascular Radiology and Intervention, Council on Clinical Cardiology, Council on Epidemiology and Prevention, Council on Arteriosclerosis, Thrombosis and Vascular Biology, Council on Cardiopulmonary, Critical Care, Perioperative and Resuscitation, Council on Cardiovascular Nursing, Council on the Kidney in Cardiovascular Disease, Council on Cardiovascular Surgery and Anesthesia, Interdisciplinary Council on Quality of Care and Outcomes Research Forecasting the future of cardiovascular disease in the United States: a policy statement from the American heart association. Circulation 2011, 123:933-944.
15. Hintz K.K., Wold L.E., Colligan P.B., Scott G.I., Lee K.J., Sowers J.R., Ren J. Influence of ovariectomy on ventricular myocyte contraction in simulated diabetes. J. Biomed. Sci. 2001, 8:307-313.
16. Hu X., Xu X., Lu Z., Zhang P., Fassett J., Zhang Y., Xin Y., Hall J.L., Viollet B., Bache R.J., Huang Y., Chen Y. AMP activated protein kinase-alpha2 regulates expression of estrogen-related receptor-alpha, a metabolic transcription factor related to heart failure development. Hypertension 2011, 58:696-703.
17. Kam K.W., Kravtsov G.M., Liu J., Wong T.M. Increased PKA activity and its influence on isoprenaline-stimulated L-type Ca2+ channels in the heart from ovariectomized rats. Br. J. Pharmacol. 2005, 144:972-981.
18. Kim J.K., Pedram A., Razandi M., Levin E.R. Estrogen prevents cardiomyocyte apoptosis through inhibition of reactive oxygen species and differential regulation of p38 kinase isoforms. J. Biol. Chem. 2006, 281:6760-6767.
19. Kim M., Tian R. Targeting AMPK for cardiac protection: opportunities and challenges. J. Mol. Cell. Cardiol. 2011, 51:548-553.
20. Kramer H.F., Witczak C.A., Fujii N., Jessen N., Taylor E.B., Arnolds D.E., Sakamoto K., Hirshman M.F., Goodyear L.J. Distinct signals regulate AS160 phosphorylation in response to insulin, AICAR, and contraction in mouse skeletal muscle. Diabetes 2006, 55:2067-2076.
21. Lee Y., Kim E.K. AMP-activated protein kinase as a key molecular link between metabolism and clockwork. Exp. Mol. Med. 2013, 45:e33.
22. Liu H., Pedram A., Kim J.K. Oestrogen prevents cardiomyocyte apoptosis by suppressing p38alpha-mediated activation of p53 and by down-regulating p53 inhibition on p38beta. Cardiovasc. Res. 2011, 89:119-128.
23. Manolagas S.C., O'Brien C.A., Almeida M. The role of estrogen and androgen receptors in bone health and disease. Nat. Rev. Endocrinol. 2013, 9:699-712.
24. Mauvais-Jarvis F., Clegg D.J., Hevener A.L. The role of estrogens in control of energy balance and glucose homeostasis. Endocr. Rev. 2013, 34:309-338.
25. McInnes K.J., Corbould A., Simpson E.R., Jones M.E. Regulation of adenosine 5', monophosphate-activated protein kinase and lipogenesis by androgens contributes to visceral obesity in an estrogen-deficient state. Endocrinology 2006, 147:5907-5913.
26. Modena M.G., Muia N., Aveta P., Molinari R., Rossi R. Effects of transdermal 17beta-estradiol on left ventricular anatomy and performance in hypertensive women. Hypertension 1999, 34:1041-1046.
27. Moolman J.A. Unravelling the cardioprotective mechanism of action of estrogens. Cardiovasc. Res. 2006, 69:777-780.
28. Murphy E. Estrogen signaling and cardiovascular disease. Circ. Res. 2011, 109:687-696.
29. Oosthuyse T., Bosch A.N. Oestrogen's regulation of fat metabolism during exercise and gender specific effects. Curr. Opin. Pharmacol. 2012, 12:363-371.
30. Ren J. Cardiac health and diabetes mellitus in women: problems and prospects. Min. Cardioangiol. 2006, 54:289-309.
31. Ren J., Hintz K.K., Roughead Z.K., Duan J., Colligan P.B., Ren B.H., Lee K.J., Zeng H. Impact of estrogen replacement on ventricular myocyte contractile function and protein kinase B/Akt activation. Am. J. Physiol. Heart Circ. Physiol. 2003, 284:H1800-1807.
32. Ren J., Kelley R.O. Cardiac health in women with metabolic syndrome: clinical aspects and pathophysiology. Obesity (Silver Spring) 2009, 17:1114-1123.
33. Rossouw J.E. Postmenopausal hormone therapy and risk of cardiovascular disease by age and years since menopause. JAMA 2007, 297:1465-1477.
34. Sakamoto K., Holman G.D. Emerging role for AS160/TBC1D4 and TBC1D1 in the regulation of GLUT4 traffic. Am. J. Physiol. Endocrinol. Metab. 2008, 295:E29-37.
35. Schulz E., Anter E., Zou M.H., Keaney J.F. Estradiol-mediated endothelial nitric oxide synthase association with heat shock protein 90 requires adenosine monophosphate-dependent protein kinase. Circulation 2005, 111:3473-3480.
36. Shirwany N.A., Zou M.H. AMPK in cardiovascular health and disease. Acta Pharmacol. Sin. 2010, 31:1075-1084.
37. Stapleton D., Mitchelhill K.I., Gao G., Widmer J., Michell B.J., Teh T., House C.M., Fernandez C.S., Cox T., Witters L.A., Kemp B.E. Mammalian AMP-activated protein kinase subfamily. J. Biol. Chem. 1996, 271:611-614.
38. Stevenson J.C. Hormone replacement therapy and cardiovascular disease revisited. Menopause Int. 2009, 15:55-57.
39. Stewart J.A., Cashatt D.O., Borck A.C., Brown J.E., Carver W.E. 17beta-estradiol modulation of angiotensin II-stimulated response in cardiac fibroblasts. J. Mol. Cell. Cardiol. 2006, 41:97-107.
40. Thompson L.P., Pinkas G., Weiner C.P. Chronic 17beta-estradiol replacement increases nitric oxide-mediated vasodilation of guinea pig coronary microcirculation. Circulation 2000, 102:445-451.
41. Turdi S., Fan X., Li J., Zhao J., Huff A.F., Du M., Ren J. AMP-activated protein kinase deficiency exacerbates aging-induced myocardial contractile dysfunction. Aging Cell 2010, 9:592-606.
42. Turdi S., Kandadi M.R., Zhao J., Huff A.F., Du M., Ren J. Deficiency in AMP-activated protein kinase exaggerates high fat diet-induced cardiac hypertrophy and contractile dysfunction. J. Mol. Cell. Cardiol. 2011, 50:712-722.
43. Valdiviezo C., Lawson S., Ouyang P. An update on menopausal hormone replacement therapy in women and cardiovascular disease. Curr. Opin. Endocrinol. Diab. Obes. 2013, 20:148-155.
44. van Eickels M., Grohe C., Cleutjens J.P., Janssen B.J., Wellens H.J., Doevendans P.A. 17beta-estradiol attenuates the development of pressure-overload hypertrophy. Circulation 2001, 104:1419-1423.
45. Wattanapermpool J., Reiser P.J. Differential effects of ovariectomy on calcium activation of cardiac and soleus myofilaments. Am. J. Physiol. 1999, 277:H467-473.
46. Xiao B., Sanders M.J., Underwood E., Heath R., Mayer F.V., Carmena D., Jing C., Walker P.A., Eccleston J.F., Haire L.F., Saiu P., Howell S.A., Aasland R., Martin S.R., Carling D., Gamblin S.J. Structure of mammalian AMPK and its regulation by ADP. Nature 2011, 472:230-233.