Advertisement

Development and Structure of the Cardiac Conduction System

  • Parvin Dorostkar
  • Mark W. Russell

Abstract

The development and structure of the cardiac conduction system, including the known molecular and cellular factors that regulate development of the conduction system are outlined. Part II includes the structure of the cardiac conduction system and its relationship to the working myocardium, including the influence of the autonomic nervous system. The final section outlines the impact of individual congenital heart defects on the anatomy and function of the conduction system.

Keywords

Atrioventricular node Cardiac looping Conduction system Transcription factors Development of the conduction system Heart tube His-Purkinje system Signaling pathways Sinoatrial node 

References

  1. 1.
    Gittenberger-de Groot AC, Bartelings MM, Deruiter MC, Poelmann RE. Basics of cardiac development for the understanding of congenital heart malformations. Pediatr Res. 2005;57:169–76.PubMedCrossRefGoogle Scholar
  2. 2.
    Bruneau BG. Transcriptional regulation of vertebrate cardiac morphogenesis. Circ Res. 2002;90:509–19.PubMedCrossRefGoogle Scholar
  3. 3.
    Srivastava D, Olson EN. A genetic blueprint for cardiac development. Nature. 2000;407:221–6.PubMedCrossRefGoogle Scholar
  4. 4.
    Kirby ML, Waldo K. Cardiac development. New York: Oxford University Press; 2007.Google Scholar
  5. 5.
    Gourdie RG, Harris BS, Bond J, et al. His-Purkinje lineages and development. Novartis Found Symp. 2003;250:110–22; discussion 122–4, 276–9.PubMedCrossRefGoogle Scholar
  6. 6.
    Gourdie RG, Harris BS, Bond J, et al. Development of the cardiac pacemaking and conduction system. Birth Defects Res C Embryo Today. 2003;69:46–57.PubMedCrossRefGoogle Scholar
  7. 7.
    Gourdie RG, Kubalak S, Mikawa T. Conducting the embryonic heart: orchestrating development of specialized cardiac tissues. Trends Cardiovasc Med. 1999;9:18–26.PubMedCrossRefGoogle Scholar
  8. 8.
    Gourdie RG, Mima T, Thompson RP, Mikawa T. Terminal diversification of the myocyte lineage generates Purkinje fibers of the cardiac conduction system. Development. 1995;121:1423–31.PubMedGoogle Scholar
  9. 9.
    Gourdie RG, Severs NJ, Green CR, Rothery S, Germroth P, Thompson RP. The spatial distribution and relative abundance of gap-junctional connexin40 and connexin43 correlate to functional properties of components of the cardiac atrioventricular conduction system. J Cell Sci. 1993;105:985–91.PubMedGoogle Scholar
  10. 10.
    Rentschler S, Morley GE, Fishman GI. Molecular and functional maturation of the murine cardiac conduction system. Cold Spring Harb Symp Quant Biol. 2002;67:353–61.PubMedCrossRefGoogle Scholar
  11. 11.
    Rentschler S, Morley GE, Fishman GI. Patterning of the mouse conduction system. Novartis Found Symp. 2003;250:194–205; discussion 205–9, 276–9.PubMedCrossRefGoogle Scholar
  12. 12.
    Rentschler S, Harris BS, Kuznekoff L, et al. Notch signaling regulates murine atrioventricular conduction and the formation of accessory pathways. J Clin Invest. 2011;121:525–33.PubMedCentralPubMedCrossRefGoogle Scholar
  13. 13.
    Rentschler S, Vaidya DM, Tamaddon H, et al. Visualization and functional characterization of the developing murine cardiac conduction system. Development. 2001;128:1785–92.PubMedCentralPubMedGoogle Scholar
  14. 14.
    Rentschler S, Yen AH, Lu J, et al. Myocardial Notch signaling reprograms cardiomyocytes to a conduction-like phenotype. Circulation. 2012;126:1058–66.PubMedCentralPubMedCrossRefGoogle Scholar
  15. 15.
    Rentschler S, Zander J, Meyers K, et al. Neuregulin-1 promotes formation of the murine cardiac conduction system. Proc Natl Acad Sci U S A. 2002;99:10464–9.PubMedCentralPubMedCrossRefGoogle Scholar
  16. 16.
    Pennisi DJ, Rentschler S, Gourdie RG, Fishman GI, Mikawa T. Induction and patterning of the cardiac conduction system. Int J Dev Biol. 2002;46:765–75.PubMedGoogle Scholar
  17. 17.
    Wenink A. Development of the human cardiac conducting system. J Anat. 1976;121:617.PubMedCentralPubMedGoogle Scholar
  18. 18.
    Gorza L, Gundersen K, Lomo T, Schiaffino S, Westgaard RH. Slow-to-fast transformation of denervated soleus muscles by chronic high-frequency stimulation in the rat. J Physiol. 1988;402:627–49.PubMedCentralPubMedCrossRefGoogle Scholar
  19. 19.
    Gorza L, Saggin L, Sartore S, Ausoni S. An embryonic-like myosin heavy chain is transiently expressed in nodal conduction tissue of the rat heart. J Mol Cell Cardiol. 1988;20:931–41.PubMedCrossRefGoogle Scholar
  20. 20.
    Gorza L, Schiaffino S, Vitadello M. Heart conduction system: a neural crest derivative? Brain Res. 1988;457:360–6.PubMedCrossRefGoogle Scholar
  21. 21.
    Gorza L, Thornell LE, Schiaffino S. Nodal myosin distribution in the bovine heart during prenatal development: an immunohistochemical study. Circ Res. 1988;62:1182–90.PubMedCrossRefGoogle Scholar
  22. 22.
    Maier A, Gorza L, Schiaffino S, Pette D. A combined histochemical and immunohistochemical study on the dynamics of fast-to-slow fiber transformation in chronically stimulated rabbit muscle. Cell Tissue Res. 1988;254:59–68.PubMedCrossRefGoogle Scholar
  23. 23.
    Blom NA, Gittenberger-de Groot AC, DeRuiter MC, Poelmann RE, Mentink MMT, Ottenkamp J. Development of the cardiac conduction tissue in human embryos using HNK-1 antigen expression—possible relevance for understanding of abnormal atrial automaticity. Circulation. 1999;99:800–6.PubMedCrossRefGoogle Scholar
  24. 24.
    DeRuiter MC, Hahurij N, Mahtab EA, Douglas YL, Poelmann RE, Gittenberger-de Groot AC. The influence of immigrating extracardiac cells during embryonic development. Wien Klin Wochenschr. 2007;119:13–5.PubMedGoogle Scholar
  25. 25.
    Douglas YL, Mahtab EA, Jongbloed MR, et al. Pulmonary vein, dorsal atrial wall and atrial septum abnormalities in podoplanin knockout mice with disturbed posterior heart field contribution. Pediatr Res. 2009;65:27–32.PubMedCrossRefGoogle Scholar
  26. 26.
    Jongbloed MR, Vicente-Steijn R, Douglas YL, et al. Expression of Id2 in the second heart field and cardiac defects in Id2 knock-out mice. Dev Dyn. 2011;240:2561–77.PubMedCrossRefGoogle Scholar
  27. 27.
    Mahtab EA, Gittenberger-de Groot AC, Vicente-Steijn R, et al. Disturbed myocardial connexin 43 and N-cadherin expressions in hypoplastic left heart syndrome and borderline left ventricle. J Thorac Cardiovasc Surg. 2012;144:1315–22.PubMedCrossRefGoogle Scholar
  28. 28.
    Mahtab EA, Vicente-Steijn R, Hahurij ND, et al. Podoplanin deficient mice show a RhoA-related hypoplasia of the sinus venosus myocardium including the sinoatrial node. Dev Dyn. 2009;238:183–93.PubMedCrossRefGoogle Scholar
  29. 29.
    Mahtab EA, Wijffels MC, Van Den Akker NM, et al. Cardiac malformations and myocardial abnormalities in podoplanin knockout mouse embryos: Correlation with abnormal epicardial development. Dev Dyn. 2008;237:847–57.PubMedCrossRefGoogle Scholar
  30. 30.
    van Loo PF, Mahtab EA, Wisse LJ, et al. Transcription factor Sp3 knockout mice display serious cardiac malformations. Mol Cell Biol. 2007;27:8571–82.PubMedCentralPubMedCrossRefGoogle Scholar
  31. 31.
    Vicente-Steijn R, Kolditz DP, Mahtab EA, et al. Electrical activation of sinus venosus myocardium and expression patterns of RhoA and Isl-1 in the chick embryo. J Cardiovasc Electrophysiol. 2010;21:1284–92.PubMedCrossRefGoogle Scholar
  32. 32.
    Weeke-Klimp A, Bax NA, Bellu AR, et al. Epicardium-derived cells enhance proliferation, cellular maturation and alignment of cardiomyocytes. J Mol Cell Cardiol. 2010;49:606–16.PubMedCrossRefGoogle Scholar
  33. 33.
    Breiteneder-Geleff S, Matsui K, Soleiman A, et al. Podoplanin, novel 43-kd membrane protein of glomerular epithelial cells, is down-regulated in puromycin nephrosis. Am J Pathol. 1997;151:1141–52.PubMedCentralPubMedGoogle Scholar
  34. 34.
    Schacht V, Ramirez MI, Hong Y-K, et al. T1alpha/podoplanin deficiency disrupts normal lymphatic vasculature formation and causes lymphedema. EMBO J. 2003;22:3546–56.PubMedCentralPubMedCrossRefGoogle Scholar
  35. 35.
    Wetterwald A, Hoffstetter W, Cecchini MG, et al. Characterization and cloning of the E11 antigen, a marker expressed by rat osteoblasts and osteocytes. Bone. 1996;18:125–32.PubMedCrossRefGoogle Scholar
  36. 36.
    Williams MC, Cao Y, Hinds A, Rishi AK, Wetterwald A. T1 alpha protein is developmentally regulated and expressed by alveolar type I cells, choroid plexus, and ciliary epithelia of adult rats. Am J Respir Cell Mol Biol. 1996;14:577–85.PubMedCrossRefGoogle Scholar
  37. 37.
    Astarita JL, Acton SE, Turley SJ. Podoplanin: emerging functions in development, the immune system, and cancer. Front Immunol. 2012;3:283.PubMedCentralPubMedCrossRefGoogle Scholar
  38. 38.
    Davies MJ, Anderson RH. The conduction system of the heart. London: Butterworth-Heinemann; 1983.Google Scholar
  39. 39.
    Oosthoek P, Virágh S, Mayen A, Van Kempen M, Lamers W, Moorman A. Immunohistochemical delineation of the conduction system. I: The sinoatrial node. Circ Res. 1993;73:473–81.PubMedCrossRefGoogle Scholar
  40. 40.
    Wessels A, Vermeulen J, Verbeek F, et al. Spatial distribution of “tissue‐specific” antigens in the developing human heart and skeletal muscle III. An immunohistochemical analysis of the distribution of the neural tissue antigen G1N2 in the embryonic heart; implications for the development of the atrioventricular conduction system. Anat Rec. 1992;232:97–111.PubMedCrossRefGoogle Scholar
  41. 41.
    Kamino K. Optical approaches to ontogeny of electrical activity and related functional organization during early heart development. Physiol Rev. 1991;71:53–91.PubMedGoogle Scholar
  42. 42.
    van den Hoff MJ, Kruithof BP, Moorman AF, Markwald RR, Wessels A. Formation of myocardium after the initial development of the linear heart tube. Dev Biol. 2001;240:61–76.PubMedCrossRefGoogle Scholar
  43. 43.
    de Jong F, Opthof T, Wilde AA, et al. Persisting zones of slow impulse conduction in developing chicken hearts. Circ Res. 1992;71:240–50.PubMedCrossRefGoogle Scholar
  44. 44.
    Manasek FJ, Burnside B, Stroman J. The sensitivity of developing cardiac myofibrils to cytochalasin-B (electron microscopy-polarized light-Z-bands-heartbeat). Proc Natl Acad Sci U S A. 1972;69:308–12.PubMedCentralPubMedCrossRefGoogle Scholar
  45. 45.
    Manasek FJ, Burnside MB, Waterman RE. Myocardial cell shape change as a mechanism of embryonic heart looping. Dev Biol. 1972;29:349–71.PubMedCrossRefGoogle Scholar
  46. 46.
    Manasek FJ, Monroe RG. Early cardiac morphogenesis is independent of function. Dev Biol. 1972;27:584–8.PubMedCrossRefGoogle Scholar
  47. 47.
    Fishman MC, Chien KR. Fashioning the vertebrate heart: earliest embryonic decisions. Development. 1997;124:2099–117.PubMedGoogle Scholar
  48. 48.
    Wessels A, Markman MW, Vermeulen JL, Anderson RH, Moorman AF, Lamers WH. The development of the atrioventricular junction in the human heart. Circ Res. 1996;78:110–7.PubMedCrossRefGoogle Scholar
  49. 49.
    Biel M, Schneider A, Wahl C. Cardiac HCN channels: structure, function, and modulation. Trends Cardiovasc Med. 2002;12:206–12.PubMedCrossRefGoogle Scholar
  50. 50.
    Xavier-Neto J, Neville CM, Shapiro MD, et al. A retinoic acid-inducible transgenic marker of sino-atrial development in the mouse heart. Development. 1999;126:2677–87.PubMedGoogle Scholar
  51. 51.
    Christoffels VM, Smits GJ, Kispert A, Moorman AF. Development of the pacemaker tissues of the heart. Circ Res. 2010;106:240–54.PubMedCrossRefGoogle Scholar
  52. 52.
    Dobrzynski H, Boyett MR, Anderson RH. New insights into pacemaker activity: promoting understanding of sick sinus syndrome. Circulation. 2007;115:1921–32.PubMedCrossRefGoogle Scholar
  53. 53.
    Mangoni ME, Nargeot J. Genesis and regulation of the heart automaticity. Physiol Rev. 2008;88:919–82.PubMedCrossRefGoogle Scholar
  54. 54.
    Koushik SV, Wang J, Rogers R, et al. Targeted inactivation of the sodium-calcium exchanger (Ncx1) results in the lack of a heartbeat and abnormal myofibrillar organization. FASEB J. 2001;15:1209–11.PubMedGoogle Scholar
  55. 55.
    Christoffels VM, Habets PE, Franco D, et al. Chamber formation and morphogenesis in the developing mammalian heart. Dev Biol. 2000;223:266–78.PubMedCrossRefGoogle Scholar
  56. 56.
    Christoffels VM, Moorman AF. Development of the cardiac conduction system: why are some regions of the heart more arrhythmogenic than others? Circ Arrhythm Electrophysiol. 2009;2:195–207.PubMedCrossRefGoogle Scholar
  57. 57.
    Fozzard HA. Cardiac sodium and calcium channels: a history of excitatory currents. Cardiovasc Res. 2002;55:1–8.PubMedCrossRefGoogle Scholar
  58. 58.
    Fozzard HA, Kyle JW. Do defects in ion channel glycosylation set the stage for lethal cardiac arrhythmias? Sci STKE. 2002;2002:pe19.PubMedGoogle Scholar
  59. 59.
    Hilber K, Sandtner W, Kudlacek O, et al. Interaction between fast and ultra-slow inactivation in the voltage-gated sodium channel. Does the inactivation gate stabilize the channel structure? J Biol Chem. 2002;277:37105–15.PubMedCrossRefGoogle Scholar
  60. 60.
    Mikawa T, Hurtado R. Development of the cardiac conduction system. Semin Cell Dev Biol. 2007;18:90–100.PubMedCrossRefGoogle Scholar
  61. 61.
    Virágh S, Challice C. The development of the conduction system in the mouse embryo heart: I. The first embryonic AV conduction pathway. Dev Biol. 1977;56:382–96.PubMedCrossRefGoogle Scholar
  62. 62.
    Alcolea S, Jarry-Guichard T, de Bakker J, et al. Replacement of connexin40 by connexin45 in the mouse: impact on cardiac electrical conduction. Circ Res. 2004;94:100–9.PubMedCrossRefGoogle Scholar
  63. 63.
    Alcolea S, Theveniau-Ruissy M, Jarry-Guichard T, et al. Downregulation of connexin 45 gene products during mouse heart development. Circ Res. 1999;84:1365–79.PubMedCrossRefGoogle Scholar
  64. 64.
    Coppen SR, Kodama I, Boyett MR, et al. Connexin45, a major connexin of the rabbit sinoatrial node, is co-expressed with connexin43 in a restricted zone at the nodal-crista terminalis border. J Histochem Cytochem. 1999;47:907–18.PubMedCrossRefGoogle Scholar
  65. 65.
    Coppen SR, Severs NJ, Gourdie RG. Connexin45 (α6) expression delineates an extended conduction system in the embryonic and mature rodent heart. Dev Genet. 1999;24:82–90.PubMedCrossRefGoogle Scholar
  66. 66.
    Nishii K, Kumai M, Shibata Y. Regulation of the epithelial-mesenchymal transformation through gap junction channels in heart development. Trends Cardiovasc Med. 2001;11:213–8.PubMedCrossRefGoogle Scholar
  67. 67.
    Shibata Y, Kumai M, Nishii K, Nakamura K. Diversity and molecular anatomy of gap junctions. Med Electron Microsc. 2001;34:153–9.PubMedCrossRefGoogle Scholar
  68. 68.
    Abramson DI, Margolin S. A Purkinje conduction network in the myocardium of the mammalian ventricles. J Anat. 1936;70:250.PubMedCentralPubMedGoogle Scholar
  69. 69.
    Hyer J, Johansen M, Prasad A, et al. Induction of Purkinje fiber differentiation by coronary arterialization. Proc Natl Acad Sci U S A. 1999;96:13214–8.PubMedCentralPubMedCrossRefGoogle Scholar
  70. 70.
    Takebayashi-Suzuki K, Yanagisawa M, Gourdie RG, Kanzawa N, Mikawa T. In vivo induction of cardiac Purkinje fiber differentiation by coexpression of preproendothelin-1 and endothelin converting enzyme-1. Development. 2000;127:3523–32.PubMedGoogle Scholar
  71. 71.
    Patel R, Kos L. Endothelin-1 and Neuregulin-1 convert embryonic cardiomyocytes into cells of the conduction system in the mouse. Dev Dyn. 2005;233:20–8.PubMedCrossRefGoogle Scholar
  72. 72.
    Gassanov N, Er F, Zagidullin N, Hoppe UC. Endothelin induces differentiation of ANP-EGFP expressing embryonic stem cells towards a pacemaker phenotype. FASEB J. 2004;18:1710–2.PubMedGoogle Scholar
  73. 73.
    Watanabe M, Chuck ET, Rothenberg F, Rosenbaum DS. Developmental transitions in cardiac conduction. Novartis Found Symp. 2003;250:68–75; discussion 76–9, 276–9.PubMedCrossRefGoogle Scholar
  74. 74.
    Watanabe M, Timm M, Fallah‐Najmabadi H. Cardiac expression of polysialylated NCAM in the chicken embryo: correlation with the ventricular conduction system. Dev Dyn. 1992;194:128–41.PubMedCrossRefGoogle Scholar
  75. 75.
    Cai C-L, Liang X, Shi Y, et al. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev Cell. 2003;5:877–89.PubMedCrossRefGoogle Scholar
  76. 76.
    Christoffels VM, Hoogaars WMH, Tessari A, Clout DEW, Moorman AFM, Campione M. T-box transcription factor Tbx2 represses differentiation and formation of the cardiac chambers. Dev Dyn. 2004;229:763–70.PubMedCrossRefGoogle Scholar
  77. 77.
    Chuck ET, Watanabe M. Differential expression of PSA‐NCAM and HNK‐1 epitopes in the developing cardiac conduction system of the chick. Dev Dyn. 1997;209:182–95.PubMedCrossRefGoogle Scholar
  78. 78.
    Davis DL, Edwards AV, Juraszek AL, Phelps A, Wessels A, Burch JB. A GATA-6 gene heart-region-specific enhancer provides a novel means to mark and probe a discrete component of the mouse cardiac conduction system. Mech Dev. 2001;108:105–19.PubMedCrossRefGoogle Scholar
  79. 79.
    Franco D, Campione M. The role of Pitx2 during cardiac development. Linking left-right signaling and congenital heart diseases. Trends Cardiovasc Med. 2003;13:157–63.PubMedCrossRefGoogle Scholar
  80. 80.
    Gaussin V, Morley GE, Cox L, et al. Alk3/Bmpr1a receptor is required for development of the atrioventricular canal into valves and annulus fibrosus. Circ Res. 2005;97:219–26.PubMedCentralPubMedCrossRefGoogle Scholar
  81. 81.
    Ji X, Chen D, Xu C, Harris SE, Mundy GR, Yoneda T. Patterns of gene expression associated with BMP-2-induced osteoblast and adipocyte differentiation of mesenchymal progenitor cell 3T3-F442A. J Bone Miner Metab. 2000;18:132–9.PubMedCrossRefGoogle Scholar
  82. 82.
    Kuo CT, Morrisey EE, Anandappa R, et al. GATA4 transcription factor is required for ventral morphogenesis and heart tube formation. Genes Dev. 1997;11:1048–60.PubMedCrossRefGoogle Scholar
  83. 83.
    Liu C, Liu W, Palie J, Lu MF, Brown NA, Martin JF. Pitx2c patterns anterior myocardium and aortic arch vessels and is required for local cell movement into atrioventricular cushions. Development. 2002;129:5081–91.PubMedCrossRefGoogle Scholar
  84. 84.
    MacNeill C, French R, Evans T, Wessels A, Burch JB. Modular regulation of cGATA-5 gene expression in the developing heart and gut. Dev Biol. 2000;217:62–76.PubMedCrossRefGoogle Scholar
  85. 85.
    Moskowitz IPG, Pizard A, Patel VV, et al. The T-Box transcription factor Tbx5 is required for the patterning and maturation of the murine cardiac conduction system. Development. 2004;131:4107–16.PubMedCrossRefGoogle Scholar
  86. 86.
    Munshi NV. Gene regulatory networks in cardiac conduction system development. Circ Res. 2012;110:1525–37.PubMedCentralPubMedCrossRefGoogle Scholar
  87. 87.
    Christoffels VM, Mommersteeg MTM, Trowe M-O, et al. Formation of the venous pole of the heart from an Nkx2-5-negative precursor population requires Tbx18. Circ Res. 2006;98:1555–63.PubMedCrossRefGoogle Scholar
  88. 88.
    Hoogaars WMH, Engel A, Brons JF, et al. Tbx3 controls the sinoatrial node gene program and imposes pacemaker function on the atria. Genes Dev. 2007;21:1098–112.PubMedCentralPubMedCrossRefGoogle Scholar
  89. 89.
    Hoogaars WMH, Tessari A, Moorman AFM, et al. The transcriptional repressor Tbx3 delineates the developing central conduction system of the heart. Cardiovasc Res. 2004;62:489–99.PubMedCrossRefGoogle Scholar
  90. 90.
    Davenport TG, Jerome-Majewska LA, Papaioannou VE. Mammary gland, limb and yolk sac defects in mice lacking Tbx3, the gene mutated in human ulnar mammary syndrome. Development. 2003;130:2263–73.PubMedCrossRefGoogle Scholar
  91. 91.
    Habets PEMH, Moorman AFM, Clout DEW, et al. Cooperative action of Tbx2 and Nkx2.5 inhibits ANF expression in the atrioventricular canal: implications for cardiac chamber formation. Genes Dev. 2002;16:1234–46.PubMedCentralPubMedCrossRefGoogle Scholar
  92. 92.
    Thomas PS, Kasahara H, Edmonson AM, et al. Elevated expression of Nkx‐2.5 in developing myocardial conduction cells. Anat Rec. 2001;263:307–13.PubMedCrossRefGoogle Scholar
  93. 93.
    Jay PY. Genetic wiring diagram of the cardiac conduction system. Circulation. 2007;116:2520–2.PubMedCrossRefGoogle Scholar
  94. 94.
    Jay PY, Harris BS, Maguire CT, et al. Nkx2-5 mutation causes anatomic hypoplasia of the cardiac conduction system. J Clin Invest. 2004;113:1130–7.PubMedCentralPubMedCrossRefGoogle Scholar
  95. 95.
    Jay PY, Maguire CT, Wakimoto H, Izumo S, Berul CI. Absence of Msx2 does not affect cardiac conduction or rescue conduction defects associated with Nkx2-5 mutation. J Cardiovasc Electrophysiol. 2005;16:82–5.PubMedCrossRefGoogle Scholar
  96. 96.
    Kasahara H, Wakimoto H, Liu M, et al. Progressive atrioventricular conduction defects and heart failure in mice expressing a mutant Csx/Nkx2.5 homeoprotein. J Clin Invest. 2001;108:189–201.PubMedCentralPubMedCrossRefGoogle Scholar
  97. 97.
    Linhares VLF, Almeida NAS, Menezes DC, et al. Transcriptional regulation of the murine Connexin40 promoter by cardiac factors Nkx2-5, GATA4 and Tbx5. Cardiovasc Res. 2004;64:402–11.PubMedCentralPubMedCrossRefGoogle Scholar
  98. 98.
    Satokata I, Ma L, Ohshima H, et al. Msx2 deficiency in mice causes pleiotropic defects in bone growth and ectodermal organ formation. Nat Genet. 2000;24:391–5.PubMedCrossRefGoogle Scholar
  99. 99.
    Ismat FA, Zhang M, Kook H, et al. Homeobox protein Hop functions in the adult cardiac conduction system. Circ Res. 2005;96:898–903.PubMedCentralPubMedCrossRefGoogle Scholar
  100. 100.
    Blaschke RJ, Hahurij ND, Kuijper S, et al. Targeted mutation reveals essential functions of the homeodomain transcription factor Shox2 in sinoatrial and pacemaking development. Circulation. 2007;115:1830–8.PubMedCrossRefGoogle Scholar
  101. 101.
    Blaschke RJ, Monaghan AP, Schiller S, et al. SHOT, a SHOX-related homeobox gene, is implicated in craniofacial, brain, heart, and limb development. Proc Natl Acad Sci U S A. 1998;95:2406–11.PubMedCentralPubMedCrossRefGoogle Scholar
  102. 102.
    Mommersteeg MTM, Brown NA, Prall OWJ, et al. Pitx2c and Nkx2-5 are required for the formation and identity of the pulmonary myocardium. Circ Res. 2007;101:902–9.PubMedCrossRefGoogle Scholar
  103. 103.
    Mommersteeg MTM, Hoogaars WMH, Prall OWJ, et al. Molecular pathway for the localized formation of the sinoatrial node. Circ Res. 2007;100:354–62.PubMedCrossRefGoogle Scholar
  104. 104.
    Kitajima S, Miyagawa-Tomita S, Inoue T, Kanno J, Saga Y. Mesp1-nonexpressing cells contribute to the ventricular cardiac conduction system. Dev Dyn. 2006;235:395–402.PubMedCrossRefGoogle Scholar
  105. 105.
    Molkentin JD. The zinc finger-containing transcription factors GATA-4, -5, and -6. Ubiquitously expressed regulators of tissue-specific gene expression. J Biol Chem. 2000;275:38949–52.PubMedCrossRefGoogle Scholar
  106. 106.
    Takebayashi-Suzuki K, Pauliks LB, Eltsefon Y, Mikawa T. Purkinje fibers of the avian heart express a myogenic transcription factor program distinct from cardiac and skeletal muscle. Dev Biol. 2001;234:390–401.PubMedCrossRefGoogle Scholar
  107. 107.
    Morrisey EE, Ip HS, Tang Z, Lu MM, Parmacek MS. GATA-5: a transcriptional activator expressed in a novel temporally and spatially-restricted pattern during embryonic development. Dev Biol. 1997;183:21–36.PubMedCrossRefGoogle Scholar
  108. 108.
    Edwards AV, Davis DL, Juraszek AL, Wessels A, Burch JBE. Transcriptional regulation in the mouse atrioventricular conduction system. Novartis Found Symp. 2003;250:177–89.PubMedCrossRefGoogle Scholar
  109. 109.
    Kupershmidt S, Yang T, Anderson ME, et al. Replacement by homologous recombination of the minK gene with lacZ reveals restriction of minK expression to the mouse cardiac conduction system. Circ Res. 1999;84:146–52.PubMedCrossRefGoogle Scholar
  110. 110.
    Drici MD, Arrighi I, Chouabe C, et al. Involvement of IsK-associated K+ channel in heart rate control of repolarization in a murine engineered model of Jervell and Lange-Nielsen syndrome. Circ Res. 1998;83:95–9102.PubMedCrossRefGoogle Scholar
  111. 111.
    Kondo RP, Anderson RH, Kupershmidt S, Roden DM, Evans SM. Development of the cardiac conduction system as delineated by minK-lacZ. J Cardiovasc Electrophysiol. 2003;14:383–91.PubMedCrossRefGoogle Scholar
  112. 112.
    Stroud DM, Darrow BJ, Kim SD, et al. Complex genomic rearrangement in CCS-LacZ transgenic mice. Genesis. 2007;45:76–82.PubMedCentralPubMedCrossRefGoogle Scholar
  113. 113.
    Hagenbuch B, Meier PJ. The superfamily of organic anion transporting polypeptides. Biochim Biophys Acta. 2003;1609:1–18.PubMedCrossRefGoogle Scholar
  114. 114.
    Gonzalez MD, Contreras LJ, Jongbloed MRM, et al. Left atrial tachycardia originating from the mitral annulus–aorta junction. Circulation. 2004;110:3187–92.PubMedCrossRefGoogle Scholar
  115. 115.
    Jongbloed MRM, Schalij MJ, Poelmann RE, et al. Embryonic conduction tissue: a spatial correlation with adult arrhythmogenic areas. J Cardiovasc Electrophysiol. 2004;15:349–55.PubMedCrossRefGoogle Scholar
  116. 116.
    Jongbloed MRM, Wijffels MCEF, Schalij MJ, et al. Development of the right ventricular inflow tract and moderator band: a possible morphological and functional explanation for Mahaim tachycardia. Circ Res. 2005;96:776–83.PubMedCrossRefGoogle Scholar
  117. 117.
    Viswanathan S, Burch JBE, Fishman GI, Moskowitz IP, Benson DW. Characterization of sinoatrial node in four conduction system marker mice. J Mol Cell Cardiol. 2007;42:946–53.PubMedCentralPubMedCrossRefGoogle Scholar
  118. 118.
    Garcia-Frigola C, Shi Y, Evans SM. Expression of the hyperpolarization-activated cyclic nucleotide-gated cation channel HCN4 during mouse heart development. Gene Expr Patterns. 2003;3:777–83.PubMedCrossRefGoogle Scholar
  119. 119.
    Stieber J, Herrmann S, Feil S, et al. The hyperpolarization-activated channel HCN4 is required for the generation of pacemaker action potentials in the embryonic heart. Proc Natl Acad Sci U S A. 2003;100:15235–40.PubMedCentralPubMedCrossRefGoogle Scholar
  120. 120.
    Kamino K, Hirota A, Fujii S. Localization of pacemaking activity in early embryonic heart monitored using voltage-sensitive dye. Nature. 1981;290:595–7.PubMedCrossRefGoogle Scholar
  121. 121.
    Van Mierop LH. Location of pacemaker in chick embryo heart at the time of initiation of heartbeat. Am J Physiol. 1967;212:407–15.PubMedGoogle Scholar
  122. 122.
    Delorme B, Dahl E, Jarry-Guichard T, et al. Expression pattern of connexin gene products at the early developmental stages of the mouse cardiovascular system. Circ Res. 1997;81:423–37.PubMedCrossRefGoogle Scholar
  123. 123.
    Delorme B, Dahl E, Jarry‐guichard T, et al. Developmental regulation of connexin 40 gene expression in mouse heart correlates with the differentiation of the conduction system. Dev Dyn. 1995;204:358–71.PubMedCrossRefGoogle Scholar
  124. 124.
    Yeager M. Structure of cardiac gap junction intercellular channels. J Struct Biol. 1998;121:231–45.PubMedCrossRefGoogle Scholar
  125. 125.
    Bevilacqua LM, Simon AM, Maguire CT, et al. A targeted disruption in connexin40 leads to distinct atrioventricular conduction defects. J Interv Card Electrophysiol. 2000;4:459–67.PubMedCrossRefGoogle Scholar
  126. 126.
    Simon AM, Goodenough DA, Paul DL. Mice lacking connexin40 have cardiac conduction abnormalities characteristic of atrioventricular block and bundle branch block. Curr Biol. 1998;8:295–8.PubMedCrossRefGoogle Scholar
  127. 127.
    Tamaddon HS, Vaidya D, Simon AM, Paul DL, Jalife J, Morley GE. High-resolution optical mapping of the right bundle branch in connexin40 knockout mice reveals slow conduction in the specialized conduction system. Circ Res. 2000;87:929–36.PubMedCrossRefGoogle Scholar
  128. 128.
    Fromaget C, el Aoumari A, Dupont E, Briand JP, Gros D. Changes in the expression of connexin 43, a cardiac gap junctional protein, during mouse heart development. J Mol Cell Cardiol. 1990;22:1245–58.PubMedCrossRefGoogle Scholar
  129. 129.
    Reaume AG, de Sousa PA, Kulkarni S, et al. Cardiac malformation in neonatal mice lacking connexin43. Science. 1995;267:1831–4.PubMedCrossRefGoogle Scholar
  130. 130.
    Nishii K, Kumai M, Egashira K, et al. Mice lacking connexin45 conditionally in cardiac myocytes display embryonic lethality similar to that of germline knockout mice without endocardial cushion defect. Cell Commun Adhes. 2003;10:365–9.PubMedCrossRefGoogle Scholar
  131. 131.
    Kreuzberg MM, Schrickel JW, Ghanem A, et al. Connexin30.2 containing gap junction channels decelerate impulse propagation through the atrioventricular node. Proc Natl Acad Sci U S A. 2006;103:5959–64.PubMedCentralPubMedCrossRefGoogle Scholar
  132. 132.
    Kreuzberg MM, Sohl G, Kim J-S, Verselis VK, Willecke K, Bukauskas FF. Functional properties of mouse connexin30.2 expressed in the conduction system of the heart. Circ Res. 2005;96:1169–77.PubMedCentralPubMedCrossRefGoogle Scholar
  133. 133.
    Kreuzberg MM, Willecke K, Bukauskas FF. Connexin-mediated cardiac impulse propagation: connexin 30.2 slows atrioventricular conduction in mouse heart. Trends Cardiovasc Med. 2006;16:266–72.PubMedCentralPubMedCrossRefGoogle Scholar
  134. 134.
    Anderson RH, Becker AE, Tranum-Jensen J, Janse MJ. Anatomico-electrophysiological correlations in the conduction system—a review. Br Heart J. 1981;45:67–82.PubMedCentralPubMedCrossRefGoogle Scholar
  135. 135.
    Kolditz DP, Wijffels MCEF, Blom NA, et al. Persistence of functional atrioventricular accessory pathways in postseptated embryonic avian hearts: implications for morphogenesis and functional maturation of the cardiac conduction system. Circulation. 2007;115:17–26.PubMedCrossRefGoogle Scholar
  136. 136.
    Gollob MH, Green MS, Tang AS, et al. Identification of a gene responsible for familial Wolff-Parkinson-White syndrome. N Engl J Med. 2001;344:1823–31.PubMedCrossRefGoogle Scholar
  137. 137.
    Gollob MH, Green MS, Tang AS, Roberts R. PRKAG2 cardiac syndrome: familial ventricular preexcitation, conduction system disease, and cardiac hypertrophy. Curr Opin Cardiol. 2002;17:229–34.PubMedCrossRefGoogle Scholar
  138. 138.
    Sidhu JS, Rajawat YS, Rami TG, et al. Transgenic mouse model of ventricular preexcitation and atrioventricular reentrant tachycardia induced by an AMP-activated protein kinase loss-of-function mutation responsible for Wolff-Parkinson-White syndrome. Circulation. 2005;111:21–9.PubMedCentralPubMedCrossRefGoogle Scholar
  139. 139.
    Patel VV, Arad M, Moskowitz IPG, et al. Electrophysiologic characterization and postnatal development of ventricular pre-excitation in a mouse model of cardiac hypertrophy and Wolff-Parkinson-White syndrome. J Am Coll Cardiol. 2003;42:942–51.PubMedCrossRefGoogle Scholar
  140. 140.
    Arad M, Moskowitz IP, Patel VV, et al. Transgenic mice overexpressing mutant PRKAG2 define the cause of Wolff-Parkinson-White syndrome in glycogen storage cardiomyopathy. Circulation. 2003;107:2850–6.PubMedCrossRefGoogle Scholar
  141. 141.
    Arad M, Seidman CE, Seidman JG. AMP-activated protein kinase in the heart: role during health and disease. Circ Res. 2007;100:474–88.PubMedCrossRefGoogle Scholar
  142. 142.
    Kistler PM, Sanders P, Hussin A, et al. Focal atrial tachycardia arising from the mitral annulus: electrocardiographic and electrophysiologic characterization. J Am Coll Cardiol. 2003;41:2212–9.PubMedCrossRefGoogle Scholar
  143. 143.
    Morton JB, Sanders P, Das A, Vohra JK, Sparks PB, Kalman JM. Focal atrial tachycardia arising from the tricuspid annulus: electrophysiologic and electrocardiographic characteristics. J Cardiovasc Electrophysiol. 2001;12:653–9.PubMedCrossRefGoogle Scholar
  144. 144.
    McGuire MA, de Bakker JM, Vermeulen JT, et al. Atrioventricular junctional tissue. Discrepancy between histological and electrophysiological characteristics. Circulation. 1996;94:571–7.PubMedCrossRefGoogle Scholar
  145. 145.
    Lev M. The normal anatomy of the conduction system in man and its pathlogy in atriventricular block. Ann N Y Acad Sci. 1964;111:817–29.PubMedCrossRefGoogle Scholar
  146. 146.
    Moorman AF, Christoffels VM, Anderson RH. Anatomic substrates for cardiac conduction. Heart Rhythm. 2005;2:875–86.PubMedCrossRefGoogle Scholar
  147. 147.
    Anderson RH, Yanni J, Boyett MR, Chandler NJ, Dobrzynski H. The anatomy of the cardiac conduction system. Clin Anat. 2009;22:99–113.PubMedCrossRefGoogle Scholar
  148. 148.
    Anderson RH, Ho SY. Anatomy of the atrioventricular junctions with regard to ventricular preexcitation. Pacing Clin Electrophysiol. 1997;20:2072–6.PubMedCrossRefGoogle Scholar
  149. 149.
    Anderson RH, Ho SY. The architecture of the sinus node, the atrioventricular conduction axis, and the internodal atrial myocardium. J Cardiovasc Electrophysiol. 1998;9:1233–48.PubMedCrossRefGoogle Scholar
  150. 150.
    Gulino SP. Examination of the cardiac conduction system: forensic application in cases of sudden cardiac death. Am J Forensic Med Pathol. 2003;24:227–38.PubMedCrossRefGoogle Scholar
  151. 151.
    Keith A, Flack M. The form and nature of the muscular connections between the primary divisions of the vertebrate heart. J Anat Physiol. 1907;41:172–89.PubMedCentralPubMedGoogle Scholar
  152. 152.
    Titus JL. Normal anatomy of the human cardiac conduction system. Anesth Analg. 1973;52:508–14.CrossRefGoogle Scholar
  153. 153.
    Titus JL, Daugherty GW, Edwards JE. Anatomy of the atrioventricular conduction system in ventricular septal defect. Circulation. 1963;28:72–81.PubMedCrossRefGoogle Scholar
  154. 154.
    Truex RC. Comparative anatomy and functional considerations of the cardiac conduction system. In: The specialized tissues of the heart. Amsterdam: Elsevier; 1961. p. 22–43.Google Scholar
  155. 155.
    James TN. Anatomy of the human sinus node. Anat Rec. 1961;141:109–39.PubMedCrossRefGoogle Scholar
  156. 156.
    Anderson KR, Ho SY, Anderson RH. Location and vascular supply of sinus node in human heart. Br Heart J. 1979;41:28–32.PubMedCentralPubMedCrossRefGoogle Scholar
  157. 157.
    Saremi F, Krishnan S. Cardiac conduction system: anatomic landmarks relevant to interventional electrophysiologic techniques demonstrated with 64-detector CT. Radiographics. 2007;27:1539–65; discussion 1566–7.PubMedCrossRefGoogle Scholar
  158. 158.
    Hoogaars WM, Barnett P, Moorman AF, Christoffels VM. T-box factors determine cardiac design. Cell Mol Life Sci. 2007;64:646–60.PubMedCentralPubMedCrossRefGoogle Scholar
  159. 159.
    Moorman AF, Soufan AT, Hagoort J, de Boer PA, Christoffels VM. Development of the building plan of the heart. Ann N Y Acad Sci. 2004;1015:171–81.PubMedCrossRefGoogle Scholar
  160. 160.
    Soufan AT, van den Hoff MJ, Ruijter JM, et al. Reconstruction of the patterns of gene expression in the developing mouse heart reveals an architectural arrangement that facilitates the understanding of atrial malformations and arrhythmias. Circ Res. 2004;95:1207–15.PubMedCrossRefGoogle Scholar
  161. 161.
    Corradi D, Maestri R, Macchi E, Callegari S. The atria: from morphology to function. J Cardiovasc Electrophysiol. 2011;22:223–35.PubMedGoogle Scholar
  162. 162.
    Ho SY, Anderson RH, Sanchez-Quintana D. Atrial structure and fibres: morphologic bases of atrial conduction. Cardiovasc Res. 2002;54:325–36.PubMedCrossRefGoogle Scholar
  163. 163.
    Goldberg CS, Caplan MJ, Heidelberger KP, Dick M. The dimensions of the triangle of Koch in children. Am J Cardiol. 1999;83:117–20, A9.Google Scholar
  164. 164.
    Becker DL, Cook JE, Davies CS, Evans WH, Gourdie RG. Expression of major gap junction connexin types in the working myocardium of eight chordates. Cell Biol Int. 1998;22:527–43.PubMedCrossRefGoogle Scholar
  165. 165.
    Inoue S, Becker AE. Posterior extensions of the human compact atrioventricular node: a neglected anatomic feature of potential clinical significance. Circulation. 1998;97:188–93.PubMedCrossRefGoogle Scholar
  166. 166.
    Medkour D, Becker AE, Khalife K, Billette J. Anatomic and functional characteristics of a slow posterior AV nodal pathway: role in dual-pathway physiology and reentry. Circulation. 1998;98:164–74.PubMedCrossRefGoogle Scholar
  167. 167.
    Massing GK, James TN. Anatomical configuration of the His bundle and bundle branches in the human heart. Circulation. 1976;53:609–21.PubMedCrossRefGoogle Scholar
  168. 168.
    Gittenberger-de Groot AC, Blom NM, Aoyama N, Sucov H, Wenink AC, Poelmann RE. The role of neural crest and epicardium-derived cells in conduction system formation. Novartis Found Symp. 2003;250:125–34; discussion 134–41, 276–9.PubMedCrossRefGoogle Scholar
  169. 169.
    Crick S, Sheppard M, Anderson R, Polak J, Wharton J. A quantitative study of nerve distribution in the conduction system of the guinea pig heart. J Anat. 1996;188:403.PubMedCentralPubMedGoogle Scholar
  170. 170.
    Crick SJ, Sheppard MN, Ho SY, Anderson RH. Localisation and quantitation of autonomic innervation in the porcine heart I: conduction system. J Anat. 1999;195:341–57.PubMedCentralPubMedCrossRefGoogle Scholar
  171. 171.
    Tomita Y, Matsumura K, Wakamatsu Y, et al. Cardiac neural crest cells contribute to the dormant multipotent stem cell in the mammalian heart. J Cell Biol. 2005;170:1135–46.PubMedCentralPubMedCrossRefGoogle Scholar
  172. 172.
    Chow LT, Chow SS, Anderson RH, Gosling JA. Autonomic innervation of the human cardiac conduction system: changes from infancy to senility—an immunohistochemical and histochemical analysis. Anat Rec. 2001;264(2):169–82.PubMedCrossRefGoogle Scholar
  173. 173.
    Anderson RH, Brown NA, Mohun TJ, Moorman AF. Insights from cardiac development relevant to congenital defects and adult clinical anatomy. J Cardiovasc Transl Res. 2013;6:107–17.PubMedCrossRefGoogle Scholar
  174. 174.
    Feldt RE, Puga WD, Seward FJ, Adams FE. Atrial septal defects and atrioventricular canal. In: Adams FE, editor. Heart disease in infants, children and adolescents. Baltimore: Williams & Wilkins; 1983.Google Scholar
  175. 175.
    Adachi I, Uemura H, McCarthy KP, Ho SY. Surgical anatomy of atrioventricular septal defect. Asian Cardiovasc Thorac Ann. 2008;16:497–502.PubMedCrossRefGoogle Scholar
  176. 176.
    Kirchhoff S, Nelles E, Hagendorff A, Kruger O, Traub O, Willecke K. Reduced cardiac conduction velocity and predisposition to arrhythmias in connexin40-deficient mice. Curr Biol. 1998;8:299–302.PubMedCrossRefGoogle Scholar
  177. 177.
    Moskowitz IP, Kim JB, Moore ML, Wolf CM, Peterson MA, Shendure J, Nobrega MA, Yokota Y, Berul C, Izumo S, Seidman JG, Seidman CE. A molecular pathway including Id2, Tbx5, and Nkx2-5 required for cardiac conduction system development. Cell. 2007;129(7):1365–76.PubMedCrossRefGoogle Scholar
  178. 178.
    Briggs LE, Takeda M, Cuadra AE, Wakimoto H, Marks MH, Walker AJ, Seki T, Oh SP, Lu JT, Sumners C, Raizada MK, Horikoshi N, Weinberg EO, Yasui K, Ikeda Y, Chien KR, Kasahara H. Perinatal loss of Nkx2-5 results in rapid conduction and contraction defects. Circ Res. 2008;103(6):580–90.PubMedCentralPubMedCrossRefGoogle Scholar
  179. 179.
    Takeda M, Briggs LE, Wakimoto H, Marks MH, Warren SA, Lu JT, Weinberg EO, Robertson KD, Chien KR, Kasahara H. Slow progressive conduction and contraction defects in loss of Nkx2-5 mice after cardiomyocyte terminal differentiation. Lab Invest. 2009;89(9):983–93.PubMedCentralPubMedCrossRefGoogle Scholar
  180. 180.
    Allwork SP, Bentall HH, Becker AE, et al. Congenitally corrected transposition of the great arteries: morphologic study of 32 cases. Am J Cardiol. 1976;38:910–23.PubMedCrossRefGoogle Scholar
  181. 181.
    Anderson RH, Danielson GK, Maloney JD, Becker AE. Atrioventricular bundle in corrected transposition. Ann Thorac Surg. 1978;26:95–7.PubMedCrossRefGoogle Scholar
  182. 182.
    Anderson RH, Arnold R, Wilkinson JL. The conducting system in congenitally corrected transposition. Lancet. 1973;1:1286–8.PubMedCrossRefGoogle Scholar
  183. 183.
    Anderson RH, Becker AE, Arnold R, Wilkinson JL. The conducting tissues in congenitally corrected transposition. Circulation. 1974;50:911–23.PubMedCrossRefGoogle Scholar
  184. 184.
    Hausen WJ. AV-conduction disorders in corrected transposition of the great vessels. Z Kreislaufforsch. 1968;57:334–44.PubMedGoogle Scholar
  185. 185.
    Attie F, Iturralde P, Zabal C, et al. Congenitally corrected transposition with atrioventricular septal defect. Cardiol Young. 1998;8:472–8.PubMedCrossRefGoogle Scholar
  186. 186.
    Daliento L, Corrado D, Buja G, John N, Nava A, Thiene G. Rhythm and conduction disturbances in isolated, congenitally corrected transposition of the great arteries. Am J Cardiol. 1986;58:314–8.PubMedCrossRefGoogle Scholar
  187. 187.
    Wilkinson JL, Anderson RH. Anatomy of discordant atrioventricular connections. World J Pediatr Congenit Heart Surg. 2011;2:43–53.PubMedCrossRefGoogle Scholar
  188. 188.
    Dick M, Norwood WI, Chipman C, Castaneda AR. Intraoperative recording of specialized atrioventricular conduction tissue electrograms in 47 patients. Circulation. 1979;59:150–60.PubMedCrossRefGoogle Scholar
  189. 189.
    Liao Z, Chang Y, Ma J, et al. Atrioventricular node reentrant tachycardia in patients with congenitally corrected transposition of the great arteries and results of radiofrequency catheter ablation. Circ Arrhythm Electrophysiol. 2012;5:1143–8.PubMedCrossRefGoogle Scholar
  190. 190.
    Epstein MR, Saul JP, Weindling SN, Triedman JK, Walsh EP. Atrioventricular reciprocating tachycardia involving twin atrioventricular nodes in patients with complex congenital heart disease. J Cardiovasc Electrophysiol. 2001;12:671–9.PubMedCrossRefGoogle Scholar
  191. 191.
    Miyazaki A, Sakaguchi H, Uchiyama T, Kurita T, Ohuchi H, Yamada O. Accessory pathway reciprocating tachycardia involving twin AV nodes in a patient with atrioventricular discordance and mitral atresia. Pacing Clin Electrophysiol. 2010;33:637–40.PubMedCrossRefGoogle Scholar
  192. 192.
    Takahashi K, Kurosawa H, Nakanishi T. Twin atrioventricular nodes connecting to sling of conduction tissue in congenitally corrected transposition associated with straddling tricuspid valve. World J Pediatr Congen Heart Surg. 2011;2:312–5.CrossRefGoogle Scholar
  193. 193.
    Amikam S, Lemer J, Kishon Y, Riss E, Neufeld HN. Complete heart block in an adult with corrected transposition of the great arteries treated with permanent pacemaker. Thorax. 1979;34:547–9.PubMedCentralPubMedCrossRefGoogle Scholar
  194. 194.
    Anderson RH. The conduction tissues in congenitally corrected transposition. Ann Thorac Surg. 2004;77:1881–2.PubMedCrossRefGoogle Scholar
  195. 195.
    Okamoto Y, Yamada K, Nozaki A, Watanabe Y. Disturbance of conduction system in corrected transposition of the great vessels. Nihon Geka Hokan. 1980;49:680–8.PubMedGoogle Scholar
  196. 196.
    Thiene G, Nava A, Rossi L. The conduction system in corrected transposition with situs inversus. Eur J Cardiol. 1977;6:57–70.PubMedGoogle Scholar
  197. 197.
    Miyazaki A, Kagisaki K, Kurita T, Yamada O. Corrected transposition of the great arteries involving situs inversus {I, D, D} and mild pulmonary stenosis: conduction system identified during preoperative investigations for a double-switch operation. Pediatr Cardiol. 2009;30:516–9.PubMedCrossRefGoogle Scholar
  198. 198.
    Bae EJ, Noh CI, Choi JY, et al. Twin AV node and induced supraventricular tachycardia in Fontan palliation patients. Pacing Clin Electrophysiol. 2005;28:126–34.PubMedCrossRefGoogle Scholar
  199. 199.
    Solomon MH, Winn KJ, White RD, et al. Kartagener’s syndrome with corrected transposition. Conducting system studies and coronary arterial occlusion complicating valvular replacement. Chest. 1976;69:677–80.PubMedCrossRefGoogle Scholar
  200. 200.
    Cheung YF, Cheng VY, Yung TC, Chau AK. Cardiac rhythm and symptomatic arrhythmia in right atrial isomerism. Am Heart J. 2002;144:159–64.PubMedCrossRefGoogle Scholar
  201. 201.
    Stroud DM, Gaussin V, Burch JB, et al. Abnormal conduction and morphology in the atrioventricular node of mice with atrioventricular canal targeted deletion of Alk3/Bmpr1a receptor. Circulation. 2007;116:2535–43.PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, New York 2015

Authors and Affiliations

  1. 1.Pediatric Cardiology, Department of PediatricsUniversity of MinnesotaSaint PaulUSA
  2. 2.Pediatric Cardiology, The University of Michigan Congenital Heart Center, Department of Pediatrics and Communicable DiseasesUniversity of MichiganAnn ArborUSA

Personalised recommendations