Gender-based differences in cardiac disease

Journal of Biomedical Research

Volumn 25, Issue 2, 2011, Pages 81-89

  Yang, Pei Chi ^a   Clancy, Colleen E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Brugada syndrome; Gender differences; Heart failure; Long QT

Indexed keywords

POTASSIUM CHANNEL; SEX HORMONE; TRANSCRIPTION FACTOR;

BRUGADA SYNDROME; CLINICAL FEATURE; DRUG EFFECT; GENE EXPRESSION; HEART ARRHYTHMIA; HEART DISEASE; HEART ELECTROPHYSIOLOGY; HEART FAILURE; HORMONE ACTION; HUMAN; LONG QT SYNDROME; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SEX DIFFERENCE; SIMULATION;

EID: 79955162942     PISSN: 16748301     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1674-8301(11)60010-9     Document Type: Review

References (93)

1. Andelfinger G, Tapper AR, Welch RC, Vanoye CG, George AL, DW Benson KCNJ2 mutation results in Andersen syndrome with sex-specific cardiac and skeletal muscle phenotypes. Am J Hum Genet 2002, 71(3):663-668.
2. Arya A Gender-related differences in ventricular repolarization: beyond gonadal steroids. J Cardiovasc Electrophysiol 2005, 16(5):525-527.
3. Teplitz L, Igic R, Berbaum ML, Schwertz DW Sex differences in susceptibility to epinephrine-induced arrhythmias. J Cardiovasc Pharmacol 2005, 46(4):548-555.
4. Di Diego JM, JM Cordeiro, RJ Goodrow, JM Fish, AC Zygmunt, GJ Perez, et al. Ionic and cellular basis for the predominance of the Brugada syndrome phenotype in males. Circulation 2002, 106(15):2004-2011.
5. Fish JM, Antzelevitch C Cellular and ionic basis for the sex-related difference in the manifestation of the Brugada syndrome and progressive conduction disease phenotypes. J Electrocardiol 2003, 36(Suppl):173-179.
6. Xiao L, Zhang L, Han W, Wang Z, Nattel S Sex-based transmural differences in cardiac repolarization and ionic-current properties in canine left ventricles. Am J Physiol Heart Circ Physiol 2006, 291(2):H570-H580.
7. Pham TV, Robinson RB, Danilo P, MR Rosen Effects of gonadal steroids on gender-related differences in transmural dispersion of L-type calcium current. Cardiovasc Res 2002, 53(3):752-762.
8. Hara M, Danilo P, Rosen MR Effects of gonadal steroids on ventricular repolarization and on the response to E4031. J Pharmacol Exp Ther 1998, 285(3):1068-1072.
9. Pham TV, Rosen MR Sex, hormones, and repolarization. Cardiovasc Res 2002, 53(3):740-751.
10. Gowda RM, Khan IA, Punukollu G, Vasavada BC, Sacchi TJ, Wilbur SL Female preponderance in ibutilide-induced torsade de pointes. Int J Cardiol 2004, 95(2-3):219-222.
11. Bai CX, Kurokawa J, Tamagawa M, Nakaya H, Furukawa T Nontranscriptional regulation of cardiac repolarization currents by testosterone. Circulation 2005, 112(12):1701-1710.
12. Furukawa T, Kurokawa J Regulation of cardiac ion channels via non-genomic action of sex steroid hormones: implication for the gender difference in cardiac arrhythmias. Pharmacol Ther 2007, 115(1):106-115.
13. Korte T, Fuchs M, Arkudas A, Geertz S, Meyer R, Gardiwal A, et al. Female mice lacking estrogen receptor beta display prolonged ventricular repolarization and reduced ventricular automaticity after myocardial infarction. Circulation 2005, 111(18):2282-2290.
14. Nakagawa M, Ooie T, Ou B, Ichinose M, Takahashi N, Hara M, et al. Gender differences in autonomic modulation of ventricular repolarization in humans. J Cardiovasc Electrophysiol 2005, 16(3):278-284.
15. What is heart failure? [cited 2010 Sep. 20] http://www.americanheart.org/print_presenter.jhtml?identifier=337.
16. Definition of Heart failure. June 18, 2002 [cited 2010 Sep. 20] http://www.medterms.com/script/main/art.asp?articlekey=3672.
17. Heart Disease and Stroke Statistics - 2010 Update. [cited 2010 Oct. 22] http://americanheart.org/presenter.jhtml?identifier=3000090.
18. Theodoraki A, Bouloux PM Low sex hormones in heart failure. Heart 2010, 96(7):496-497.
19. Malkin CJ, Pugh PJ, West JN, van Beek EJ, TH Jones, KS Channer Testosterone therapy in men with moderate severity heart failure: a double-blind randomized placebo controlled trial. Eur Heart J 2006, 27(1):57-64.
20. Caminiti G, Volterrani M, Iellamo F, Marazzi G, Massaro R, Miceli M, et al. Effect of long-acting testosterone treatment on functional exercise capacity, skeletal muscle performance, insulin resistance, and baroreflex sensitivity in elderly patients with chronic heart failure a double-blind, placebo-controlled, randomized study. J Am Coll Cardiol 2009, 54(10):919-927.
21. Adams KF, Sueta CA, Gheorghiade M, CM O'Connor, TA Schwartz, GG Koch, et al. Gender differences in survival in advanced heart failure. Insights from the FIRST study. Circulation 1999, 99(14):1816-1821.
22. Ho KK, Anderson KM, Kannel WB, Grossman W, Levy D Survival after the onset of congestive heart failure in Framingham Heart Study subjects. Circulation 1993, 88(1):107-115.
23. Adams KF, Dunlap SH, Sueta CA, Clarke SW, Patterson JH, MB Blauwet, et al. Relation between gender, etiology and survival in patients with symptomatic heart failure. J Am Coll Cardiol 1996, 28(7):1781-1788.
24. Croft JB, Giles WH, Pollard RA, Keenan NL, Casper ML, Anda RF Heart failure survival among older adults in the United States: a poor prognosis for an emerging epidemic in the Medicare population. Arch Intern Med 1999, 159(5):505-510.
25. Simon T, M Mary-Krause, C Funck-Brentano, P Jaillon Sex differences in the prognosis of congestive heart failure: results from the Cardiac Insufficiency Bisoprolol Study (CIBIS II). Circulation 2001, 103(3):375-380.
26. Stromberg A, Martensson J Gender differences in patients with heart failure. Eur J Cardiovasc Nurs 2003, 2(1):7-18.
27. Wang Y, Hill JA Electrophysiological remodeling in heart failure. J Mol Cell Cardiol 2010, 48(4):619-632.
28. Tomaselli GF, Zipes DP What causes sudden death in heart failure?. Circ Res 2004, 95(8):754-763.
29. Nattel S, Maguy A, Le Bouter S, YH Yeh Arrhythmogenic ion-channel remodeling in the heart: heart failure, myocardial infarction, and atrial fibrillation. Physiol Rev 2007, 87(2):425-456.
30. Nass RD, Aiba T, Tomaselli GF, Akar FG Mechanisms of disease: ion channel remodeling in the failing ventricle. Nat Clin Pract Cardiovasc Med 2008, 5(4):196-207.
31. Heo S, Moser DK, Widener J Gender differences in the effects of physical and emotional symptoms on health-related quality of life in patients with heart failure. Eur J Cardiovasc Nurs 2007, 6(2):146-152.
32. Riedinger MS, Dracup KA, Brecht ML, Padilla G, Sarna L, Ganz PA Quality of life in patients with heart failure: do gender differences exist?. Heart Lung 2001, 30(2):105-116.
33. Frank K, Kranias EG Phospholamban and cardiac contractility. Ann Med 2000, 32(8):572-578.
34. Borlak J, Thum T Hallmarks of ion channel gene expression in end-stage heart failure. FASEB J 2003, 17(12):1592-1608.
35. Freeman K, Lerman I, Kranias EG, Bohlmeyer T, Bristow MR, Lefkowitz RJ, et al. Alterations in cardiac adrenergic signaling and calcium cycling differentially affect the progression of cardiomyopathy. J Clin Invest 2001, 107(8):967-974.
36. Gaborit N, Varro A, Le Bouter S, V Szuts, D Escande, S Nattel, et al. Gender-related differences in ion-channel and transporter subunit expression in non-diseased human hearts. J Mol Cell Cardiol 2010.
37. Yang D, Song LS, Zhu WZ, Chakir K, Wang W, Wu C, et al. Calmodulin regulation of excitation-contraction coupling in cardiac myocytes. Circ Res 2003, 92(6):659-667.
38. Lindemann JP, Watanabe AM Phosphorylation of phospholamban in intact myocardium. Role of Ca2+-calmodulin-dependent mechanisms. J Biol Chem 1985, 260(7):4516-4525.
39. Redfield MM, Jacobsen SJ, Burnett JC, Mahoney DW, Bailey KR, Rodeheffer RJ Burden of systolic and diastolic ventricular dysfunction in the community: appreciating the scope of the heart failure epidemic. JAMA 2003, 289(2):194-202.
40. Vasan RS, Larson MG, Benjamin EJ, Evans JC, Reiss CK, Levy D Congestive heart failure in subjects with normal versus reduced left ventricular ejection fraction: prevalence and mortality in a population-based cohort. J Am Coll Cardiol 1999, 33(7):1948-1955.
41. Masoudi FA, Havranek EP, Smith G, Fish RH, Steiner JF, Ordin DL, et al. Gender, age, and heart failure with preserved left ventricular systolic function. J Am Coll Cardiol 2003, 41(2):217-223.
42. Schwinger RH, Wang J, Frank K, J Muller-Ehmsen, K Brixius, AA McDonough, et al. Reduced sodium pump alpha1, alpha3, and beta1-isoform protein levels and Na+, K+-ATPase activity but unchanged Na+-Ca2+ exchanger protein levels in human heart failure. Circulation 1999, 99(16):2105-2112.
43. Wu X, Chang B, Blair NS, Sargent M, York AJ, Robbins J, et al. Plasma membrane Ca2+-ATPase isoform 4 antagonizes cardiac hypertrophy in association with calcineurin inhibition in rodents. J Clin Invest 2009, 119(4):976-985.
44. Vermeulen JT Mechanisms of arrhythmias in heart failure. J Cardiovasc Electrophysiol 1998, 9(2):208-221.
45. Pogwizd SM, Bers DM Cellular basis of triggered arrhythmias in heart failure. Trends Cardiovasc Med 2004, 14(2):61-66.
46. Wei SK, JM McCurley, SU Hanlon, MC Haigney Gender differences in Na/Ca exchanger current and beta-adrenergic responsiveness in heart failure in pig myocytes. Ann N Y Acad Sci 2007, 1099:183-189.
47. Sugishita K, Su Z, Li F, Philipson KD, Barry WH Gender influences [Ca(2+)](i) during metabolic inhibition in myocytes overexpressing the Na(+)-Ca(2+) exchanger. Circulation 2001, 104(17):2101-2106.
48. Cross HR, Lu L, Steenbergen C, Philipson KD, Murphy E Overexpression of the cardiac Na+/Ca2+ exchanger increases susceptibility to ischemia/reperfusion injury in male, but not female, transgenic mice. Circ Res 1998, 83(12):1215-1223.
49. Jovanovic S, Jovanovic A, Shen WK, Terzic A Low concentrations of 17beta-estradiol protect single cardiac cells against metabolic stress-induced Ca2+ loading. J Am Coll Cardiol 2000, 36(3):948-952.
50. Fraser H, Davidge ST, Clanachan AS Enhancement of post-ischemic myocardial function by chronic 17 beta -estradiol treatment: role of alterations in glucose metabolism. J Mol Cell Cardiol 1999, 31(8):1539-1549.
51. Keller JN, Germeyer A, Begley JG, Mattson MP 17Beta-estradiol attenuates oxidative impairment of synaptic Na+/K+-ATPase activity, glucose transport, and glutamate transport induced by amyloid beta-peptide and iron. J Neurosci Res 1997, 50(4):522-530.
52. Sarkozy A, Brugada P Sudden cardiac death and inherited arrhythmia syndromes. J Cardiovasc Electrophysiol 2005, 16(Suppl 1):S8-20.
53. Wilde AA, Antzelevitch C, Borggrefe M, Brugada J, Brugada R, Brugada P, et al. Proposed diagnostic criteria for the Brugada syndrome: consensus report. Circulation 2002, 106(19):2514-2519.
54. Clancy CE, Rudy Y Na(+) channel mutation that causes both Brugada and long-QT syndrome phenotypes: a simulation study of mechanism. Circulation 2002, 105(10):1208-1213.
55. Grant AO, Carboni MP, Neplioueva V, Starmer CF, Memmi M, Napolitano C, et al. Long QT syndrome, Brugada syndrome, and conduction system disease are linked to a single sodium channel mutation. J Clin Invest 2002, 110(8):1201-1209.
56. Benson DW, Wang DW, Dyment M, Knilans TK, Fish FA, Strieper MJ, et al. Congenital sick sinus syndrome caused by recessive mutations in the cardiac sodium channel gene (SCN5A). J Clin Invest 2003, 112(7):1019-1028.
57. Bennett PB, Yazawa K, Makita N, George AL Molecular mechanism for an inherited cardiac arrhythmia. Nature 1995, 376(6542):683-685.
58. Tan HL, MT Bink-Boelkens, CR Bezzina, PC Viswanathan, GC Beaufort-Krol, van Tintelen PJ, et al. A sodium-channel mutation causes isolated cardiac conduction disease. Nature 2001, 409(6823):1043-1047.
59. Veldkamp MW, Viswanathan PC, Bezzina C, Baartscheer A, Wilde AA, Balser JR Two distinct congenital arrhythmias evoked by a multidysfunctional Na(+) channel. Circ Res 2000, 86(9):E91-E97.
60. Chen Q, Kirsch GE, Zhang D, Brugada R, Brugada J, Brugada P, et al. Genetic basis and molecular mechanism for idiopathic ventricular fibrillation. Nature 1998, 392(6673):293-296.
61. Yan GX, Antzelevitch C Cellular basis for the Brugada syndrome and other mechanisms of arrhythmogenesis associated with ST-segment elevation. Circulation 1999, 100(15):1660-1666.
62. Antzelevitch C, Brugada P, Brugada J, Brugada R, Shimizu W, Gussak I, et al. Brugada syndrome: a decade of progress. Circ Res 2002, 91(12):1114-1118.
63. Antzelevitch C, Brugada P, Brugada J, Brugada R, Towbin JA, Nademanee K Brugada syndrome: 1992-2002: a historical perspective. J Am Coll Cardiol 2003, 41(10):1665-1671.
64. Meregalli PG, Wilde AA, Tan HL Pathophysiological mechanisms of Brugada syndrome: depolarization disorder, repolarization disorder, or more?. Cardiovasc Res 2005, 67(3):367-378.
65. Wilde AA, Postema PG, Di Diego JM, S Viskin, H Morita, JM Fish, et al. The pathophysiological mechanism underlying Brugada syndrome: depolarization versus repolarization. J Mol Cell Cardiol 2010, 49(4):543-553.
66. N Abi-Gerges, K Philp, C Pollard, I Wakefield, TG Hammond, JP Valentin Sex differences in ventricular repolarization: from cardiac electrophysiology to Torsades de Pointes. Fundam Clin Pharmacol 2004, 18(2):139-151.
67. James AF, Choisy SC, Hancox JC Recent advances in understanding sex differences in cardiac repolarization. Prog Biophys Mol Biol 2007, 94(3):265-319.
68. Rautaharju PM, Zhou SH, Wong S, Calhoun HP, Berenson GS, Prineas R, et al. Sex differences in the evolution of the electrocardiographic QT interval with age. Can J Cardiol 1992, 8(7):690-695.
69. M Stramba-Badiale, D Spagnolo, G Bosi, PJ Schwartz Are gender differences in QTc present at birth? MISNES Investigators. Multicenter Italian Study on Neonatal Electrocardiography and Sudden Infant Death Syndrome. Am J Cardiol 1995, 75(17):1277-1278.
70. Locati EH, Zareba W, Moss AJ, Schwartz PJ, Vincent GM, Lehmann MH, et al. Age- and sex-related differences in clinical manifestations in patients with congenital long-QT syndrome: findings from the International LQTS Registry. Circulation 1998, 97(22):2237-2244.
71. Drici MD, Knollmann BC, Wang WX, Woosley RL Cardiac actions of erythromycin: influence of female sex. JAMA 1998, 280(20):1774-1776.
72. Makkar RR, Fromm BS, Steinman RT, Meissner MD, Lehmann MH Female gender as a risk factor for torsades de pointes associated with cardiovascular drugs. JAMA 1993, 270(21):2590-2597.
73. Lehmann MH, Hardy S, Archibald D, B Quart, DJ MacNeil Sex difference in risk of torsade de pointes with d,l-sotalol. Circulation 1996, 94(10):2535-2541.
74. Pham TV, Sosunov EA, Gainullin RZ, Danilo P, Rosen MR Impact of sex and gonadal steroids on prolongation of ventricular repolarization and arrhythmias induced by I(K)-blocking drugs. Circulation 2001, 103(17):2207-2212.
75. Ruan YF, Liu N, Zhou Q, Li Y, Wang L Experimental study on the mechanism of sex difference in the risk of torsade de pointes. Chin Med J (Engl) 2004, 117(4):538-541.
76. Spear JF, Moore EN Gender and seasonally related differences in myocardial recovery and susceptibility to sotalol-induced arrhythmias in isolated rabbit hearts. J Cardiovasc Electrophysiol 2000, 11(8):880-887.
77. Liu XK, Wang W, Ebert SN, Franz MR, Katchman A, Woosley RL Female gender is a risk factor for torsades de pointes in an in vitro animal model. J Cardiovasc Pharmacol 1999, 34(2):287-294.
78. Pham TV, Sosunov EA, Anyukhovsky EP, Danilo P, Rosen MR Testosterone diminishes the proarrhythmic effects of dofetilide in normal female rabbits. Circulation 2002, 106(16):2132-2136.
79. Liu XK, Katchman A, Drici MD, Ebert SN, Ducic I, Morad M, et al. Gender difference in the cycle length-dependent QT and potassium currents in rabbits. J Pharmacol Exp Ther 1998, 285(2):672-679.
80. James AF, Arberry LA, Hancox JC Gender-related differences in ventricular myocyte repolarization in the guinea pig. Basic Res Cardiol 2004, 99(3):183-192.
81. Kurokawa J, Tamagawa M, Harada N, Honda SI, Bai CX, Nakaya H, et al. Acute effects of estrogen on the guinea pig and human IKr channels and drug-induced prolongation of cardiac repolarization. J Physiol 2008.
82. Nakamura H, Kurokawa J, Bai CX, Asada K, Xu J, Oren RV, et al. Progesterone regulates cardiac repolarization through a nongenomic pathway: an in vitro patch-clamp and computational modeling study. Circulation 2007, 116(25):2913-2922.
83. Wu ZY, Chen K, Haendler B, TV McDonald, JS Bian Stimulation of N-terminal truncated isoform of androgen receptor stabilizes human ether-a-go-go-related gene-encoded potassium channel protein via activation of extracellular signal regulated kinase 1/2. Endocrinology 2008, 149(10):5061-5069.
84. Liu XK, Katchman A, Whitfield BH, Wan G, Janowski EM, Woosley RL, et al. In vivo androgen treatment shortens the QT interval and increases the densities of inward and delayed rectifier potassium currents in orchiectomized male rabbits. Cardiovasc Res 2003, 57(1):28-36.
85. Nakagawa M, Ooie T, Takahashi N, Taniguchi Y, Anan F, Yonemochi H, et al. Influence of menstrual cycle on QT interval dynamics. Pacing Clin Electrophysiol 2006, 29(6):607-613.
86. Burke JH, Ehlert FA, Kruse JT, Parker MA, Goldberger JJ, Kadish AH Gender-specific differences in the QT interval and the effect of autonomic tone and menstrual cycle in healthy adults. Am J Cardiol 1997, 79(2):178-181.
87. Rodriguez I, Kilborn MJ, Liu XK, Pezzullo JC, Woosley RL Drug-induced QT prolongation in women during the menstrual cycle. JAMA 2001, 285(10):1322-1326.
88. Benton RE, Sale M, Flockhart DA, Woosley RL Greater quinidine-induced QTc interval prolongation in women. Clin Pharmacol Ther 2000, 67(4):413-418.
89. Ebert SN, Liu XK, Woosley RL Female gender as a risk factor for drug-induced cardiac arrhythmias: evaluation of clinical and experimental evidence. J Womens Health 1998, 7(5):547-557.
90. H El-Eraky, SH Thomas Effects of sex on the pharmacokinetic and pharmacodynamic properties of quinidine. Br J Clin Pharmacol 2003, 56(2):198-204.
91. N el-Sherif, RH Zeiler, W Craelius, WB Gough, R Henkin QTU prolongation and polymorphic ventricular tachyarrhythmias due to bradycardia-dependent early afterdepolarizations. Afterdepolarizations and ventricular arrhythmias. Circ Res 1988, 63(2):286-305.
92. Roden DM Early after-depolarizations and torsade de pointes: implications for the control of cardiac arrhythmias by prolonging repolarization. Eur Heart J 1993, 14(Suppl H):56-61.
93. Yang PC, Kurokawa J, Furukawa T, Clancy CE Acute effects of sex steroid hormones on susceptibility to cardiac arrhythmias: a simulation study. PLoS Comput Biol 2010, 6(1):e1000658.