Sex differences in exercise-induced physiological myocardial hypertrophy are modulated by oestrogen receptor beta

Cardiovascular Research

Volumn 102, Issue 3, 2014, Pages 418-428

  Dworatzek, Elke ^a   Mahmoodzadeh, Shokoufeh ^a   Schubert, Carola ^a   Westphal, Christina ^b   Leber, Joachim ^a   Kusch, Angelika ^a,c   Kararigas, Georgios ^a   Fliegner, Daniela ^a   Moulin, Maryline ^d   Ventura Clapier, Renée ^d   Gustafsson, Jan Ake ^e   Davidson, Mercy M ^f   Dragun, Duska ^a,c   Regitz Zagrosek, Vera ^a  

^a DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d INSERM   (France)

^e University of Houston   (United States)

^f Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Exercise induced physiological MH; Hypertrophy associated; Mitochondrial adaptation; Oestrogen receptor; Sex; Signalling pathway

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GA BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; NUCLEAR RESPIRATORY FACTOR 1; PROTEIN S6; PROTEIN SERINE THREONINE KINASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE; VIRUS PROTEIN V; ESTROGEN RECEPTOR; PROTEIN KINASE B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; EXERCISE; EXPERIMENTAL TEST; FEMALE; HEART LEFT VENTRICLE MASS; HEART MUSCLE CELL; HEART VENTRICLE HYPERTROPHY; HUMAN; HUMAN CELL; MALE; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; SEX DIFFERENCE; VOLUNTARY CAGE WHEEL RUNNING; ADAPTATION; ANIMAL; C57BL MOUSE; CARDIOMEGALY; CELL CULTURE; METABOLISM; PHYSIOLOGY; SEXUAL DEVELOPMENT; SIGNAL TRANSDUCTION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CARDIOMEGALY; CELLS, CULTURED; ESTROGEN RECEPTOR BETA; FEMALE; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MITOCHONDRIA; OXIDATIVE PHOSPHORYLATION; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHYSICAL CONDITIONING, ANIMAL; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, ESTROGEN; SEX CHARACTERISTICS; SIGNAL TRANSDUCTION;

EID: 84901468382     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvu065     Document Type: Article

References (58)

1. Bernardo BC, Weeks KL, Pretorius L, McMullen JR. Molecular distinction between physiological and pathological cardiac hypertrophy: Experimental findings and therapeutic strategies. Pharmacol Ther 2010;128: 191-227.
2. Maillet M, van Berlo JH, Molkentin JD. Molecular basis of physiological heart growth: Fundamental concepts and new players. Nat Rev Mol Cell Biol 2012;14: 38-48.
3. DeBosch B, Treskov I, Lupu TS, Weinheimer C, Kovacs A, Courtois M, Muslin AJ. Akt1 is required for physiological cardiac growth. Circulation 2006;113: 2097-2104.
4. McMullen JR, Jennings GL. Differences between pathological and physiological cardiac hypertrophy: Novel therapeutic strategies to treat heart failure. Clin Exp Pharmacol Physiol 2007;34: 255-262.
5. Weeks KL, Gao X, Du XJ, Boey EJ, Matsumoto A, Bernardo BC, Kiriazis H, Cemerlang N, Tan JW, Tham YK, Franke TF, Qian H, Bogoyevitch MA, Woodcock EA, Febbraio MA, Gregorevic P, McMullen JR. Phosphoinositide 3-kinase p110a is a master regulator of exercise-induced cardioprotection and PI3K gene therapy rescues cardiac dysfunction. Circ Heart Fail 2012;5: 523-534.
6. 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. Protective effectsof exercise and phosphoinositide 3-kinase(p110a) signaling in dilated and hypertrophic cardiomyopathy. Proc Natl Acad Sci USA 2007;104: 612-617.
7. De Bono JP, Adlam D, Paterson DJ, Channon KM. Novel quantitative phenotypes of exercise training in mouse models. Am J Physiol Regul Integr Comp Physiol 2006;290: R926-R934.
8. Konhilas JP, Maass AH, Luckey SW, Stauffer BL, Olson EN, Leinwand LA. Sex modifies exercise and cardiac adaptation in mice. Am J Physiol Heart Circ Physiol 2004;287: H2768-H2776.
9. Foryst-Ludwig A, Kreissl MC, Sprang C, Thalke B, Bohm C, Benz V, Gurgen D, Dragun D, SchubertC, Mai K, Stawowy P, Spranger J, Regitz-Zagrosek V, Unger T, Kintscher U. Sex differences in physiological cardiac hypertrophy are associated with exercise-mediated changes in energy substrate availability. Am J Physiol Heart Circ Physiol 2011;301: H115-H122.
10. Aurigemma GP, Silver KH, McLaughlin M, Mauser J, Gaasch WH. Impact of chamber geometry and gender on left ventricular systolic function in patients .60 years of age with aortic stenosis. Am J Cardiol 1994;74: 794-798.
11. Carroll JD, Carroll EP, Feldman T, Ward DM, Lang RM, McGaughey D, Karp RB. Sexassociated differences in left ventricular function in aortic stenosis of the elderly. Circulation 1992;86: 1099-1107.
12. Isensee J, Witt H, Pregla R, Hetzer R, Regitz-Zagrosek V, Noppinger PR. Sexually dimorphic gene expression in the heart of mice and men. J Mol Med 2008;86: 61-74.
13. Murphy E. Estrogen signaling and cardiovascular disease. Circ Res 2011;109: 687-696.
14. Gurgen D, Hegner B, Kusch A, Catar R, Chaykovska L, Hoff U, Gross V, Slowinski T, da Costa GoncalvesAC, Kintscher U, Gustafsson JA, Luft FC, Dragun D. Estrogen receptorbeta signals left ventricular hypertrophy sex differences in normotensive deoxycorticosterone acetate-salt mice. Hypertension 2011;57: 648-654.
15. van Eickels M, Grohe C, Cleutjens JP, Janssen BJ, Wellens HJ, Doevendans PA. 17b-estradiol attenuates the development of pressure-overload hypertrophy. Circulation 2001;104: 1419-1423.
16. Westphal C, Schubert C, Prelle K, Penkalla A, Fliegner D, Petrov G, Regitz-Zagrosek V. Effects of estrogen, an ERa agonist and raloxifene on pressure overload induced cardiac hypertrophy. PLoS ONE 2012;7: E50802.
17. 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. Female sex and estrogen receptor-beta attenuate cardiac remodeling and apoptosis in pressure overload. Am J Physiol Regul Integr Comp Physiol 2010;298: R1597-R1606.
18. 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: 410-417.
19. 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. Regression of myocardial hypertrophy after aortic valve replacement: Faster in women? Circulation 2010;122: S23-S28.
20. Mahmoodzadeh S, Dworatzek E, Fritschka S, Pham TH, Regitz-Zagrosek V. 17b-Estradiol inhibits matrix metalloproteinase-2 transcription via MAP kinase in fibroblasts. Cardiovasc Res 2010;85: 719-728.
21. Mahmoodzadeh S, Pham TH, Kuehne A, Fielitz B, Dworatzek E, Kararigas G, Petrov G, DavidsonMM, Regitz-Zagrosek V. 17b-Estradiol-induced interaction of ERawith NPPA regulates gene expression in cardiomyocytes. Cardiovasc Res 2012;96: 411-421.
22. Rimbaud S, Garnier A, Ventura-Clapier R. Mitochondrial biogenesis in cardiac pathophysiology. Pharmacol Rep 2009;61: 131-138.
23. Abel ED, Doenst T. Mitochondrial adaptations to physiological vs. pathological cardiac hypertrophy. Cardiovasc Res 2011;90: 234-242.
24. Bo H, Zhang Y, Ji LL. Redefining the role of mitochondria in exercise: A dynamic remodeling. Ann N Y Acad Sci 2010;1201: 121-128.
25. Chen JQ, Cammarata PR, Baines CP, Yager JD. Regulation of mitochondrial respiratory chain biogenesis by estrogens/estrogen receptors and physiological, pathological and pharmacological implications. Biochim Biophys Acta 2009;1793: 1540-1570.
26. Krege JH, Hodgin JB, Couse JF, Enmark E, Warner M, Mahler JF, Sar M, Korach KS, Gustafsson JA, Smithies O. Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc Natl Acad Sci USA 1998;95: 15677-15682.
27. Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, Mark M. Effect of single and compound knockouts of estrogen receptors alpha (ERa) and beta (ERb) on mouse reproductive phenotypes. Development 2000;127: 4277-4291.
28. Reynolds ES. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Biol Chem 1963;17: 208-212.
29. Davidson MM, Nesti C, Palenzuela L, Walker WF, Hernandez E, Protas L, Hirano M, Isaac ND. Novel cell lines derived from adult human ventricular cardiomyocytes. J Mol Cell Cardiol 2005;39: 133-147.
30. Ogawa S, Chan J, Gustafsson JA, Korach KS, PfaffDW. Estrogen increases locomotor activity in mice through estrogen receptor alpha: Specificity for the type of activity. Endocrinology 2003;144: 230-239.
31. Haines CD, Harvey PA, Leinwand LA. Estrogens mediate cardiac hypertrophy in a stimulus-dependent manner. Endocrinology 2012;153: 4480-4490.
32. Garey J, Goodwillie A, Frohlich J, Morgan M, Gustafsson JA, Smithies O, Korach KS, Ogawa S, PfaffDW. Genetic contributions to generalized arousal of brain and behavior. Proc Natl Acad Sci USA 2003;100: 11019-11022.
33. Wang L, Gout I, ProudCG.Cross-talk between the ERKand p70 S6 kinase (S6K) signaling pathways. MEK-dependent activation of S6K2 in cardiomyocytes. J Biol Chem 2001;276: 32670-32677.
34. Iijima Y, Laser M, Shiraishi H, Willey CD, Sundaravadivel B, Xu L, McDermott PJ, Kuppuswamy D. c-Raf/MEK/ERK pathway controls protein kinase C-mediated p70S6K activation in adult cardiac muscle cells. J Biol Chem 2002;277: 23065-23075.
35. Pende M, Um SH, Mieulet V, Sticker M, Goss VL, Mestan J, Mueller M, Fumagalli S, Kozma SC, Thomas G. S6K1(2/2)/S6K2(2/2) mice exhibit perinatal lethality and rapamycin-sensitive 5′-terminal oligopyrimidine mRNA translation and reveal a mitogen-activated protein kinase-dependent S6 kinase pathway. Mol Cell Biol 2004;24: 3112-3124.
36. Dionyssiou MG, Nowacki NB, Hashemi S, Zhao J, Kerr A, Tsushima RG, McDermott JC. Cross-talk between glycogen synthase kinase 3b (GSK3b) and p38MAPK regulates myocyte enhancer factor 2 (MEF2) activity in skeletal and cardiac muscle. J Mol Cell Cardiol 2013;54: 35-44.
37. Simpson E, Rubin G, Clyne C, Robertson K, O'Donnell L, Jones M, Davis S. The role of local estrogen biosynthesis in males and females. Trends Endocrinol Metab 2000;11: 184-188.
38. Grohe C, Kahlert S, Lobbert K, Vetter H. Expression of oestrogen receptor alpha and beta in rat heart: Role of local oestrogen synthesis. J Endocrinol 1998;156: R1-R7.
39. Bueno OF, De Windt LJ, Tymitz KM, Witt SA, Kimball TR, Klevitsky R, Hewett TE, Jones SP, Lefer DJ, Peng CF, Kitsis RN, Molkentin JD. The MEK1-ERK1/2 signaling pathway promotes compensated cardiac hypertrophy in transgenic mice. EMBO J 2000;19: 6341-6350.
40. Wang M, Wang Y, Weil B, Abarbanell A, Herrmann J, Tan J, Kelly M, Meldrum DR. 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 2009;296: R972-R978.
41. Vasconsuelo A, Milanesi L, Boland R. 17b-estradiol abrogates apoptosis in murine skeletal muscle cells through estrogen receptors: Role of the phosphatidylinositol 3-kinase/AKT pathway. J Endocrinol 2008;196: 385-397.
42. Urata Y, Ihara Y, Murata H, Goto S, Koji T, Yodoi J, Inoue S, Kondo T. 17b-estradiol protects against oxidative stress-induced cell death through the glutathione/glutaredoxindependent redox regulation of AKT in myocardiac H9c2 cells. J Biol Chem 2006;281: 13092-13102.
43. Aquila S, Sisci D, Gentile M, Middea E, Catalano S, Carpino A, Rago V, Ando S. Estrogen receptor (ER)aand ERbare both expressed in human ejaculated spermatozoa: Evidence of their direct interaction with phosphatidylinositol-3-OH kinase/AKT pathway. J Clin Endocrinol Metab 2004;89: 1443-1451.
44. Acconcia F, Totta P, Ogawa S, Cardillo I, Inoue S, Leone S, Trentalance A, Muramatsu M, Marino M. Survival versus apoptotic 17b-estradiol effect: Role of ERa and ERb activated non-genomic signaling. J Cell Physiol 2005;203: 193-201.
45. Ventura-Clapier R, Garnier A, Veksler V. Transcriptional control of mitochondrial biogenesis: The central role of PGC-1a. Cardiovasc Res 2008;79: 208-217.
46. Cam H, Balciunaite E, Blais A, Spektor A, Scarpulla RC, Young R, Kluger Y, Dynlacht BD. A common set of gene regulatory networks links metabolism and growth inhibition. Mol Cell 2004;16: 399-411.
47. Stirone C, Duckles SP, Krause DN, Procaccio V. Estrogen increases mitochondrial efficiency and reduces oxidative stress in cerebral blood vessels. Mol Pharmacol 2005;68: 959-965.
48. Mattingly KA, IvanovaMM, Riggs KA, Wickramasinghe NS, Barch MJ, Klinge CM.Estradiol stimulates transcription of nuclear respiratory factor-1 and increases mitochondrial biogenesis. Mol Endocrinol 2008;22: 609-622.
49. Hsieh YC, Yang S, Choudhry MA, Yu HP, Rue LWIII, Bland KI, Chaudry IH. PGC-1 upregulation via estrogen receptors: Acommonmechanism of salutary effectsof estrogen and flutamide on heart function after trauma-hemorrhage.AmJ Physiol Heart Circ Physiol 2005; 289: H2665-H2672.
50. Yu HP, Hsieh YC, Suzuki T, Shimizu T, ChoudhryMA, Schwacha MG, Chaudry IH. Salutary effects of estrogen receptor-beta agonist on lung injury after trauma-hemorrhage. Am J Physiol Lung Cell Mol Physiol 2006;290: L1004-L1009.
51. Liesa M, Shirihai OS. Mitochondrial dynamics in the regulation of nutrient utilization and energy expenditure. Cell Metab 2013;17: 491-506.
52. Chen H, Detmer SA, Ewald AJ, Griffin EE, Fraser SE, Chan DC. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J Biol Chem 2003;160: 189-200.
53. Sugioka R, Shimizu S, Tsujimoto Y. Fzo1, a protein involved in mitochondrial fusion, inhibits apoptosis. J Biol Chem 2004;279: 52726-52734.
54. Piquereau J, Caffin F, Novotova M, Lemaire C, Veksler V, Garnier A, Ventura-Clapier R, Joubert F. Mitochondrial dynamics in the adult cardiomyocytes: Which roles for a highly specialized cell? Front Physiol 2013;4: 102.
55. Kararigas G, Fliegner D, Gustafsson JA, Regitz-Zagrosek V. Role of the estrogen/estrogen-receptor-beta axis in the genomic response to pressure overload-induced hypertrophy. Physiol Genomics 2011;43: 438-446.
56. 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: 331-338.
57. Ranki HJ, Budas GR, Crawford RM, Davies AM, Jovanovic A. 17b-estradiol regulates expression of K(ATP) channels in heart-derived H9c2 cells. J Am Coll Cardiol 2002;40: 367-374.
58. Chicco AJ, Johnson MS, Armstrong CJ, Lynch JM, Gardner RT, Fasen GS, Gillenwater CP, Moore RL. Sex-specific and exercise-acquired cardioprotection is abolished by sarcolemmal KATP channel blockade in the rat heart. Am J Physiol Heart Circ Physiol 2007; 292: H2432-H2437.