Sex-dependent gene regulatory networks of the heart rhythm

Functional and Integrative Genomics

Volumn 10, Issue 1, 2010, Pages 73-86

  Iacobas, D A ^a   Iacobas, S ^a   Thomas, N ^a   Spray, D C ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Arrhythmia; Atria; Cardiac connexins; Intercalated discs; Ion channels; Ventricles

Indexed keywords

ADRENERGIC RECEPTOR; ANKYRIN; CADHERIN; GAP JUNCTION PROTEIN; ION CHANNEL; PLAKOPHILIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; FUNCTIONAL GENOMICS; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE REGULATORY NETWORK; GENETIC STABILITY; HEART ATRIUM; HEART RHYTHM; HEART VENTRICLE; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SEX DIFFERENCE; TRANSCRIPTOMICS;

ANIMALS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HEART ATRIA; HEART RATE; HEART VENTRICLES; MALE; MICE; MICE, INBRED C57BL; RNA, MESSENGER; SEX CHARACTERISTICS;

MUS;

EID: 77949423720     PISSN: 1438793X     EISSN: 14387948     Source Type: Journal    
DOI: 10.1007/s10142-009-0137-8     Document Type: Article

References (82)

1. Adams W (1936) The normal duration of the electrocardiographic ventricular complex. J Clin Invest 15:335-342
2. Albert CM, McGovern BA, Newell JB, Ruskin JN (1996) Sex differences in cardiac arrest survivors. Circulation 15:1170-1176
3. AVID (1997) The antiarrhythmics versus implantable defibrillators (AVID) investigators. A comparison of antiarrhythmic drug therapy with implantable defibrillators in patients resuscitated from near-fatal ventricular arrhythmias. N Engl J Med 337:1576-1583 Bazett H (1920) An analysis of the time-relations of electrocardiograms. Heart 7:353-370
4. Benjamin EJ, Wolf PA, D'Agostino RB, Silbershatz H, Kannel WB, Levy D (1998) Impact of atrial fibrillation on the risk of death: the Framington Heart Study. Circulation 98(10):946-952
5. Boden MJ, Kennaway DJ (2006) Circadian rhythms and reproduction. Reproduction 132(3):379-392 Review
6. Boles MK, Wilkinson BM, Maxwell A, Lai L, Mills AA, Nishijima I, Salinger AP, Moskowitz I, Hirschi KK, Liu B, Bradley A, Justice MJ (2009) A mouse chromosome 4 balancer ENU-mutagenesis screen isolates eleven lethal lines. BMC Genet 10:12
7. Buxton AE, Hafley GE, Lehmann MH, Gold M, O'Toole M, Tang A, Coromilas J, Hook B, Stamato NJ, Lee KL (1999a) Prediction of sustained ventricular tachycardia inducible by programmed stimulation in patients with coronary artery disease. Utility of clinical variables. Circulation 99(14):1843-1850
8. Buxton AE, Lee KL, Fisher JD, Josephson ME, Prystowsky EN, Hafley G (1999b) A randomized study of the prevention of sudden death in patients with coronary artery disease. Multicenter unsustained tachycardia trial investigators. N Engl J Med 341(25):1882-90 Erratum in: N Engl J Med (2000) 342 (17):1300
9. Chugh SS, Whitesel S, Turner M, Roberts CT Jr, Nagalla SR (2003) Genetic basis for chamber-specific ventricular phenotypes in the rat infarct model. Cardiovasc Res 57(2):477-485
10. Dalal D, James C, Devanagondi R, Tichnell C, Tucker A, Prakasa K, Spevak PJ, Bluemke DA, Abraham T, Russell SD, Calkins H, Judge DP (2006) Penetrance of mutations in plakophilin-2 among families with arrhythmogenic right ventricular dysplasia/ cardiomyopathy. J Am Coll Cardiol 48(7):1416-1424
11. Danik SB, Rosner G, Lader J, Gutstein DE, Fishman GI, Morley GE (2008) Electrical remodeling contributes to complex tachyarrhythmias in connexin43-deficient mouse hearts. FASEB J 22 (4):1204-1212
12. Derangeon M, Spray DC, Bourmeyster N, Sarrouilhe D, Herve JC (2009) Reciprocal influence of connexins and apical junction proteins on their expressions and functions. Biochim Biophys Acta 1788(4):768-778
13. Dhein S (2006) Cardiac ischemia and uncoupling: gap junctions in ischemia and infarction. Adv Cardiol 42:198-212 Review
14. Donnelly-Roberts DL, Namovic MT, Han P, Jarvis MF (2009) Mammalian P2X7 receptor pharmacology: comparison of recombinant mouse, rat and human P2X7 receptors. Br J Pharmacol 157 (7):1203-1214
15. Dostanic I, Schultz Jel J, Lorenz JN, Lingrel JB (2004) The alpha 1 isoform of Na, K-ATPase regulates cardiac contractility and functionally interacts and co-localizes with the Na/Ca exchanger in heart. J Biol Chem 279(52):54053-54061
16. Drici MD, Knollmann BC, Wang WX, Woosley RL (1998) Cardiac actions of erythromycin: influence of female sex. JAMA 280 (20):1774-1776
17. Duffy HS, Fort AG, Spray DC (2006) Cardiac connexins: genes to nexus. Adv Cardiol 42:1-17
18. Fan C, Iacobas DA, Zhou D, Chen Q, Gavrialov O, Haddad GG (2005) Gene expression and phenotypic characterization of mouse heart after chronic constant and intermittent hypoxia. Physiol Genomics 22:292-307
19. Fischer R, PollerW, Schultheiss HP, GotthardtM (2009) CAR-diology-a virus receptor in the healthy and diseased heart. J Mol Med 87 (9):879-884
20. Fishman GI (2005) Gap junction remodeling and ventricular arrhythmias. Heart Rhythm 2(8):887-889
21. Gilbert JS, Nijland MJ (2008) Sex differences in the developmental origins of hypertension and cardiorenal disease. Am J Physiol Regul Integr Comp Physiol 295(6):R1941-R1952
22. Györke S (2009) Molecular basis of catecholaminergic polymorphic ventricular tachycardia. Heart Rhythm 6(1):123-129
23. Herren T, Gerber PA, Duru F (2009) Arrhythmogenic right ventricular cardiomyopathy/dysplasia: a not so rare "disease of the desmosome" with multiple clinical presentations. Clin Res Cardiol 98 (3):141-158
24. Hervé JC, Derangeon M, Théveniau-Ruissy M, Miquerol L, Sarrouilhe D, Gros D (2008) Connexins and junctional channels. Roles in the spreading of cardiac electrical excitation and heart development. Pathol Biol (Paris) 56(5):334-341
25. Harris AL (2008) Connexin specificity of second messenger permeation: real numbers at last. J Gen Physiol 131(4):287-292
26. Iacobas DA, Fan C, Iacobas S, Haddad GG (2008a) Integrated transcriptomic response to cardiac chronic hypoxia: translation regulators and response to stress in cell survival. Funct Integr Genomics 8(3):265-275
27. Iacobas DA, Iacobas S, Li WE, Zoidl G, Dermietzel R, Spray DC (2005a) Genes controlling multiple functional pathways are transcriptionally regulated in connexin43 null mouse heart. Physiol Genomics 20:211-223
28. Iacobas DA, Iacobas S, Spray DC (2005b) Use of cDNA arrays to explore gene expression in genetically manipulated mice and cell lines. In: Dhein S, Mohr FW, Delmar M (eds) Practical methods in cardiovascular research. Springer, New York, pp 907-915
29. Iacobas DA, Fan C, Iacobas S, Spray DC, Haddad GG (2006) Transcriptomic changes in developing kidney exposed to chronic hypoxia. Biochem Biophys Res Comm 349(1):329-338
30. Iacobas DA, Iacobas S, Spray DC (2007a) Connexin43 and the brain transcriptome of the newborn mice. Genomics 89:113-123
31. Iacobas DA, Iacobas S, Spray DC (2007b) Connexin-dependent transcellular transcriptomic networks in mouse brain. Prog Biophys Mol Biol 94(1-2):168-184
32. Iacobas DA, Iacobas S, Urban-Maldonado M, Scemes E, Spray DC (2008b) Similar transcriptomic alterations in Cx43 knock-down and knock-out astrocytes. Cell Commun Adhes 15(1):195-206
33. Isensee J, Witt H, Pregla R, Hetzer R, Regitz-Zagrosek V, Noppinger PR (2008) Sexually dimorphic gene expression in the heart of mice and men. J Mol Med 86(1):61-74 Review
34. Joshi-Mukherjee R, Coombs W, Musa H, Oxford E, Taffet S, Delmar M (2008) Characterization of the molecular phenotype of two arrhythmogenic right ventricular cardiomyopathy (ARVC)-related
35. plakophilin-2 (PKP2) mutations. Heart Rhythm 5(12):1715-1723
36. Kamiński KA, Oledzka E, Białobrzewska K, Kozuch M, Musiał WJ, Winnicka MM (2007) The effects of moderate physical exercise on cardiac hypertrophy in interleukin 6 deficient mice. Adv Med Sci 52:164-168
37. Kanagaratnam P, Cherian A, Stanbridge RD, Glenville B, Severs NJ, Peters NS (2004) Relationship between connexins and atrial activation during human atrial fibrillation. J Cardiovasc Electrophysiol 15(2):206-216
38. Kannel WB, Wilson PWF, D'Agostino RB (1998) Sudden coronary death in women. Am Heart J 136:205-212
39. Kardami E, Dang X, Iacobas DA, Nickel BE, Jeyaraman M, Srisakuldee W, Makazan J, Tanguy S, Spray DC (2007) The role of connexins in controlling cell growth and gene expression. Prog Biophys Mol Biol 94(1-2):245-264
40. Killeen MJ, Thomas G, Sabir IN, Grace AA, Huang CL (2008) Mouse models of human arrhythmia syndromes. Acta Physiol (Oxf) 192 (4):455-469
41. Kreuzberg MM, Söhl G, Kim JS, Verselis VK, Willecke K, Bukauskas FF (2005) Functional properties of mouse connexin30.2 expressed in the conduction system of the heart. Circ Res 96 (11):1169-1177
42. Lee RS, Lam CW, Lai CK, Yuen YP, Chan KY, Shek CC, Chan AY, Chow CB (2007) Carnitine-acylcarnitine translocase deficiency in three neonates presenting with rapid deterioration and cardiac arrest. Hong Kong Med J 13(1):66-68
43. Lehman MH, Hardy S, Archibald D, MacNeil DJ (1999) JTc prolongation with d, I-sotalol in women versus men. Am J Cardiol 83:354-359
44. Li J, Patel VV, Radice GL (2006) Dysregulation of cell adhesion proteins and cardiac arrhythmogenesis. Clin Med Res 4:42-52
45. Lim BK, Xiong D, Dorner A, Youn TJ, Yung A, Liu TI, Gu Y, Dalton ND, Wright AT, Evans SM, Chen J, Peterson KL, McCulloch AD, Yajima T, Knowlton KU (2008) Coxsackievirus and adenovirus receptor (CAR) mediates atrioventricular-node function and connexin 45 localization in the murine heart. J Clin Invest 118:2758-2770
46. Lisewski U, Shi Y, Wrackmeyer U, Fischer R, Chen C, Schirdewan A, Jüttner R, Rathjen F, Poller W, Radke MH, Gotthardt M (2008) The tight junction protein CAR regulates cardiac conduction and cell-cell communication. J Exp Med 205(10):2369-2379
47. Lo CW, Cohen MF, Huang GY, Lazatin BO, Patel N, Sullivan R, Pauken C, Park SM (1997) Cx43 gap junction gene expression and gap junctional communication in mouse neural crest cells. Dev Genet 20:119-132
48. Lujan HL, Dicarlo SE (2008) Sex differences to myocardial ischemia and beta-adrenergic receptor blockade in conscious rats. Am J Physiol Heart Circ Physiol 294(4):H1523-H1529
49. Manias JL, Plante I, Gong XQ, Shao Q, Churko J, Bai D, Laird DW (2008) Fate of connexin43 in cardiac tissue harbouring a diseaselinked connexin43 mutant. Cardiovasc Res 80(3):385-395
50. Maron BJ, Roberts WC, Arad M, Haas TS, Spirito P, Wright GB, Almquist AK, Baffa JM, Saul JP, Ho CY, Seidman J, Seidman CE (2009) Clinical outcome and phenotypic expression in LAMP2 cardiomyopathy. JAMA 301(12):1253-1259
51. McCurley AT, Callard GV (2008) Characterization of housekeeping genes in zebrafish: male-female differences and effects of tissue type, developmental stage and chemical treatment. BMC Mol Biol 9:102
52. Merri M, Benhorin J, Alberti M, Locati E, Moss AJ (1989) Electrocardiographic quantitation of ventricular repolarization. Circulation 80:1301-1308
53. Mohler PJ, Wehrens XH (2007) Mechanisms of human arrhythmia syndromes: abnormal cardiac macromolecular interactions. Physiology (Bethesda) 22:342-350 Review
54. Mounkes LC, Kozlov SV, Rottman JN, Stewart CL (2005) Expression of an LMNA-N195K variant of A-type lamins results in cardiac conduction defects and death in mice. Hum Mol Genet 14 (15):2167-2180
55. Nao T, Ohkusa T, Hisamatsu Y, Inoue N, Matsumoto T, Yamada J, Shimizu A, Yoshiga Y, Yamagata T, Kobayashi S, Yano M, Hamano K, Matsuzaki M (2003) Comparison of expression of connexin in right atrial myocardium in patients with chronic atrial fibrillation versus those in sinus rhythm. Am J Cardiol 15:678-83
56. Nattel S, Maguy A, Le Bouter S, Yeh YH (2007) Arrhythmogenic ionchannel remodeling in the heart: heart failure, myocardial infarction, and atrial fibrillation. Physiol Rev 87(2):425-456
57. Nonen S, Okamoto H, Fujio Y, Takemoto Y, Yoshiyama M, Hamaguchi T, Matsui Y, Yoshikawa J, Kitabatake A, Azuma J (2008) Polymorphisms of norepinephrine transporter and adrenergic receptor alpha1D are associated with the response to betablockers in dilated cardiomyopathy. Pharmacogenomics J 8 (1):78-84
58. O'Connell TD, Swigart PM, Rodrigo MC, Ishizaka S, Joho S, Turnbull L, Tecott LH, Baker AJ, Foster E, Grossman W, Simpson PC et al (2006) Alpha1-adrenergic receptors prevent a maladaptive cardiac response to pressure overload. J Clin Invest 116(4):1005-1015
59. Perriard J-C, Hirschy A, Ehler E (2003) Dilated cardiomyopathy: a disease of the intercalated disc? Trends Cardiovascu Med 13:30-38
60. Perrino C, Rockman HA (2007) Reversal of cardiac remodeling by modulation of adrenergic receptors: a new frontier in heart failure. Curr Opin Cardiol 22(5):443-449
61. Peters RW, Gold MR (2004) The influence of gender on arrhythmia. Cardiol Rev 12:97-105
62. Pham TV, Rosen MR (2002) Sex, hormones and repolarization. Cardiovasc Res 53:740-751
63. Pilote L, Dasgupta K, Guru V, Humphries KH, McGrath J, Norris C, Rabi D, Tremblay J, Alamian A, Barnett T, Cox J, Ghali WA, Grace S, Hamet P, Ho T, Kirkland S, Lambert M, Libersan D, O'Loughlin J, Paradis G, Petrovich M, Tagalakis V (2007) A comprehensive view of sex-specific issues related to cardiovascular disease. CMAJ 176(6):S1-S44 Review. Erratum in 24; 176 (9):1310
64. Polontchouk L, Haefliger JA, Ebelt B, Schaefer T, Stuhlmann D, Mehlhorn U, Kuhn-Regnier F, De Vivie ER, Dhein S (2001) Effects of chronic atrial fibrillation on gap junction distribution in human and rat atria. J Am Coll Cardiol 38(3):883-891
65. Rautaharju PM, Zhou SH, Calhoun WS, HP BGS, Prineas R, Davignon A (1992) Sex differences in the evolution of the electrocardiographic QT interval with age. Can J Cardiol 8 (7):690-695
66. Reaume AG, de Sousa PA, Kulkarni S, Langille BL, Zhu D, Davies TC, Juneja SC, Kidder GM, Rossant J (1995) Cardiac malformation in neonatal mice lacking connexin43. Science 267:1831-1834
67. Reinoehl J, Frankovich D, Machado C, Kawasaki R, Baga JJ, Pires LA, Steinman RT, Fromm BS, Lehmann MH (1996) Probucolassociated tachyarrhythmic events and QT prolongation: importance of gender. Am Heart J 131(6):1184-1191
68. Rodriguez LM, de Chillou C, Schläpfer J, Metzger J, Baiyan X, van den Dool A, Smeets JL, Wellens HJ (1992) Age at onset and gender of patients with different types of supraventricular tachycardias. Am J Cardiol 70(13):1213-1215
69. Saffitz JE, Hames KY, Kanno S (2007) Remodeling of gap junctions in ischemic and nonischemic forms of heart disease. J Membr Biol 218(1-3):65-71
70. Schulz R, Boengler K, Totzeck A, Luo Y, Garcia-Dorado D, Heusch G (2007) Connexin 43 in ischemic pre- and postconditioning. Heart Fail Rev 12(3-4):261-266
71. Silander K, Alanne M, Kristiansson K, Saarela O, Ripatti S, Auro K, Karvanen J, Kulathinal S, Niemelä M, Ellonen P, Vartiainen E, Jousilahti P, Saarela J, Kuulasmaa K, Evans A, Perola M, Salomaa V, Peltonen L (2008) Gender differences in genetic risk profiles for cardiovascular disease. PLoS ONE 3(10):e3615
72. Sousa S, Cabanes D, El-Amraoui A, Petit C, Lecuit M, Cossart P (2004) Unconventional myosin VIIa and vezatin, two proteins crucial for Listeria entry into epithelial cells. J Cell Sci 117 (Pt 10):2121-2130
73. Spray DC, Iacobas DA (2007) Organizational principles of the connexin-related brain transcriptome. J Membr Biol 218(1-3):39-47
74. Spray DC, Suadicani S, Srinivas M, Gutstein DE, Fishman GI (2001) Gap junctions in the cardiovascular system. Handbook of physiology: section 2: the cardiovascular system, vol 1: the heart: gap junctions in the cardiovascular system. Oxford University Press, New York, pp 169-212
75. Syrris P, Ward D, Asimaki A, Sen-Chowdhry S, Ebrahim HY, Evans A, Hitomi N, Norman M, Pantazis A, Shaw AL (2006) Clinical expression of plakophilin-2 mutations in familial arrhythmogenic right ventricular cardiomyopathy. Circulation 113:356-364
76. Teng GQ, Zhao X, Lees-Miller JP, Quinn FR, Li P, Rancourt DE, London B, Cross JC, Duff HJ (2008) Homozygous missense N629D hERG (KCNH2) potassium channel mutation causes developmental defects in the right ventricle and its outflow tract and embryonic lethality. Circ Res 103(12):1483-1491
77. Tribulová N, Dupont E, Soukup T, Okruhlicová L, Severs NJ (2005) Sex differences in connexin-43 expression in left ventricles of aging rats. Physiol Res 54(6):705-708
78. van Tintelen JP, Entius MM, Bhuiyan ZA, Jongbloed R, Wiesfeld AC, Wilde AA, van der Smagt J, Boven LG, Mannens MM, van Langen IM, Hofstra RM, Otterspoor LC, Doevendans PA, Rodriguez LM, van Gelder IC, Hauer RN (2006) Plakophilin-2 mutations are the major determinant of familial arrhythmogenic right ventricular dysplasia/cardiomyopathy. Circulation 113 (13):1650-1658
79. van Tintelen JP, Hofstra RM, Wiesfeld AC, van den Berg MP, Hauer RN, Jongbloed JD (2007) Molecular geneticsof arrhythmogenic right ventricular cardiomyopathy: emerging horizon? Curr Opin Cardiol 22(3):185-192
80. Wilhelm M, Kirste W, Kuly S, Amann K, Neuhuber W, Weyand M, Daniel WG, Garlichs C (2006) Atrial distribution of connexin 40 and 43 in patients with intermittent, persistent, and postoperative atrial fibrillation. Heart Lung Circ 15:30-37
81. Wit AL, Janse MJ (2001) Reperfusion arrhythmias and sudden cardiac death: a century of progress toward an understanding of the mechanisms. Circ Res 89:741-743
82. 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, Grohé C, Regitz-Zagrosek V (2008) Sex-specific pathways in early cardiac response to pressure overload in mice. J Mol Med 86(9):1013-1024