Molecular analysis of patterning of conduction tissues in the developing human heart

Circulation: Arrhythmia and Electrophysiology

Volumn 4, Issue 4, 2011, Pages 532-542

  Sizarov, Aleksander ^a   Devalla, Harsha D ^c   Anderson, Robert H ^b   Passier, Robert ^c   Christoffels, Vincent M ^a   Moorman, Antoon F M ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Atrioventricular axis; Heart development; Human embryo; Sinus node

Indexed keywords

CATION CHANNEL; GAP JUNCTION PROTEIN; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED CATION CHANNEL 4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ISL1; TRANSCRIPTION FACTOR NKX2.5; TRANSCRIPTION FACTOR TBX18; TRANSCRIPTION FACTOR TBX3; UNCLASSIFIED DRUG; CONNEXIN 40; CONNEXIN 43; CYCLIC NUCLEOTIDE GATED CHANNEL; HCN4 PROTEIN, HUMAN; MUSCLE PROTEIN; T BOX TRANSCRIPTION FACTOR; TBX3 PROTEIN, HUMAN;

ARTICLE; ATRIOVENTRICULAR CONDUCTION; DEVELOPMENTAL STAGE; EMBRYO; HEART DEVELOPMENT; HEART MUSCLE; HEART MUSCLE CONDUCTION SYSTEM; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SINUS NODE; HEART; HEART ATRIOVENTRICULAR NODE; METABOLISM; PATHOLOGY; PRENATAL DEVELOPMENT;

ATRIOVENTRICULAR NODE; CONNEXIN 43; CONNEXINS; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; HEART; HEART CONDUCTION SYSTEM; HUMANS; MUSCLE PROTEINS; MYOCARDIUM; SINOATRIAL NODE; T-BOX DOMAIN PROTEINS; TRANSCRIPTION FACTORS;

EID: 80054043603     PISSN: 19413149     EISSN: 19413084     Source Type: Journal    
DOI: 10.1161/CIRCEP.111.963421     Document Type: Article

References (48)

1. Paff GH, Boucek RJ, Harrell TC. Observations on the development of the electrocardiogram. Anat Rec. 1968;160:575-582.
2. de Jong F, Opthof T, Wilde AA, Janse MJ, Charles R, Lamers WH, Moorman AF. Persisting zones of slow impulse conduction in developing chicken hearts. Circ Res. 1992;71:240-250.
3. Schram G, Pourrier M, Malnyk P, Nattel S. Differential distribution of cardiac ion channel expression as a basis for regional specialization in electrical function. Circ Res. 2002;90:939-950. (Pubitemid 34633859)
4. Christoffels VM, Smits GJ, Kispert A, Moorman AF. Development of the pacemaker tissues of the heart. Circ Res. 2010;106:240-254.
5. Walls EW. The development of the specialized conducting tissue of the human heart. J Anat. 1947;81:93-110.
6. Navaratnam V. The development of the specialized musculature of the human heart. Ceylon J Med Sci. 1965;14:68-80.
7. Anderson RH, Taylor IM. Development of atrioventricular specialized tissue in human heart. Br Heart J. 1972;34:1205-1214.
8. Wenink ACG. Development of the human cardiac conduction system. J Anat. 1976;121:617-631.
9. Anderson RH, Ho SY, Becker AE, Gosling JA. The development of the sinoatrial node. In: Bonke FIM, ed. The Sinus Node: Structure, Function and Clinical Relevance. Leiden: Martinus Nijhoff Medical Division, 1978;166-182.
10. Truex RC, Marino TA, Marino DR. Observations on the development of the human atrioventricular node and bundle. Anat Rec. 1978;192: 337-350. (Pubitemid 9049198)
11. Wessels A, Vermeulen JL, Verbeek FJ, Virágh S, Kálmán F, Lamers WH, Moorman AF. An immunohistochemical analysis of the distribution of the neural tissue antigen G1N2 in the embryonic human heart. Anat Rec. 1992;232:97-111.
12. 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;99:800-806. (Pubitemid 29083021)
13. Sizarov A, Anderson RH, Christoffels VM, Moorman AF. Threedimensional and molecular analysis of the venous pole of the developing human heart. Circulation. 2010;122:798-807.
14. Sizarov A, Ya J, de Boer BA, Christoffels VM, Lamers WH, Moorman AF. Development of the building plan of the human heart: morphogenesis, growth and differentiation. Circulation. 2011;123:1125-1135.
15. Jansen JA, van Veen TA, de Bakker JM, van Rijen HV. Cardiac connexins and impulse propagation. J Mol Cell Cardiol. 2010;48:76-82.
16. Mangoni ME, Nargeot J. Genesis and regulation of the heart automaticity. Physiol Rev. 2008;88:919-982.
17. Stieber J, Herrmann S, Feil S, Löster J, Feil R, Biel M, Hofmann F, Ludwig A. 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;100:15235-15240. (Pubitemid 37518045)
18. Gourdie RG, Harris BS, Bond J, Justus C, Hewett KW, O'Brien TX, Thompson RP, Sedmera D. Development of the cardiac pacemaking and conduction system. Birth Defects Res. 2003;69:46-57. (Pubitemid 37238415)
19. Hoogaars WM, Tessari A, Moorman AF, de Boer PA, Hagoort J, Soufan AT, Campione M, Christoffels VM. The transcriptional repressor Tbx3 delineates the developing central conduction system of the heart. Cardiovasc Res. 2004;62:489-499. (Pubitemid 38648963)
20. Christoffels VM, Burch JBE, Moorman AFM. Architectural plan for the heart: early patterning and delineation of the chambers and nodes. Trends Cardiovasc Med. 2004;14:301-307. (Pubitemid 41110608)
21. Davis LM, Rodefeld ME, Green K, Beyer EC, Saffitz JE. Gap junction protein phenotypes of the human heart and conduction system. J Cardiovasc Electrophysiol. 1995;6:813-822.
22. Jongbloed MR, Mahtab EA, Blom NA, Schalij MJ, Gittenberger-de Groot AC. Development of the cardiac conduction system. Sci World J. 2008; 8:239-269.
23. Christoffels VM, Mommersteeg MT, Trowe MO, Prall OW, de Gier-de Vries C, Soufan AT, Bussen M, Schuster-Gossler K, Harvey RP, Moorman AF, Kispert A. Formation of the venous pole of the heart from an Nkx2-5-negative precursor population requires Tbx18. Circ Res. 2006;98:1555-1563. (Pubitemid 44297079)
24. Bakker ML, Boukens BJ, Mommersteeg MT, Brons JF, Wakker V, Moorman AF, Christoffels VM. Transcription factor Tbx3 is required for the specification of the atrioventricular conduction system. Circ Res. 2008;102:1340-1349.
25. 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;129:1365-1376. (Pubitemid 46962088)
26. Kolditz DP, Wijffels MC, Blom NA, van der Laarse A, Hahurij ND, Lie-Venema H, Markwald RR, Poelmann RE, Schalij MJ, Gittenberger-de Groot AC. Epicardium-derived cells in development of annulus fibrosis and persistence of accessory pathways. Circulation. 2008;117:1508-1517. (Pubitemid 351440639)
27. Yanni J, Boyett MR, Anderson RH, Dobrzynski H. The extent of the specialized atrioventricular ring tissues. Heart Rhythm. 2009;6:672-680.
28. Snarr BS, Wirrig EE, Phelps AL, Trusk TC, Wessels A. A spatiotemporal evaluation of the contribution of the dorsal mesenchymal protrusion to cardiac development. Dev Dyn. 2007;236:1287-1294. (Pubitemid 46750260)
29. Aanhaanen WT, Mommersteeg MT, Norden J, Wakker V, de Gier-de Vries C, Anderson RH, Kispert A, Moorman AF, Christoffels VM. Developmental origin, growth, and three-dimensional architecture of the atrioventricular conduction axis of the mouse heart. Circ Res. 2010;107: 728-736.
30. Thomas PS, Kasahara H, Edmonson AM, Izumo S, Yacoub MH, Barton PJR, Gourdie RG. Elevated expression of Nkx-2.5 in developing myocardial conduction cells. Anat Rec. 2001;263:307-313.
31. Issa ZF, Miller JM, Zipes DP, eds. Clinical Arrhythmology and Electrophysiology: Companion to Braunwald's Heart Disease. Philadelphia: Saunders; 2009.
32. Boukens BJ, Christoffels VM, Coronel R, Moorman AF. Developmental basis for electrophysiological heterogeneity in the ventricular and outflow tract myocardium as a substrate for life-threatening ventricular arrhythmias. Circ Res. 2009;104:19-31.
33. Mommersteeg MTM, Hoogaars WMH, Prall OWJ, de Gier-de Vries C, Wiese C, Clout DEW, Papaioannou VE, Brown NA, Harvey RP, Moorman AFM, Christoffels VM. Molecular pathway for the localized formation of the sinoatrial node. Circ Res. 2007;100:354-362.
34. Chandler NJ, Greener ID, Tellez JO, Inada S, Musa H, Molenaar P, DiFrancesco D, Baruscotti M, Longhi R, Anderson RH, Billeter R, Sharma V, Sigg DC, Boyett MR, Dobrzynski H. Molecular architecture of the human sinus node: insights into the function of the cardiac pacemaker. Circulation. 2009;119:1562-1575.
35. Gaborit N, le Bouter S, Szuts V, Varro A, Escande D, Nattel S, Demolombe S. Regional and tissue specific transcript signatures of ion channel genes in the non-diseased human heart. J Physiol. 2007;582: 675-693. (Pubitemid 47040552)
36. Hoogaars WMH, Engel A, Brons JF, Verkerk AO, de Lange FJ, Wong LY, Bakker ML, Clout DE, Wakker V, Barnett P, Ravesloot JH, Moorman AF, Verheijck EE, Christoffels VM. Tbx3 controls the sinoatrial node gene program and imposes pacemaker function on the atria. Genes Dev. 2007;21:1098-1112. (Pubitemid 46686478)
37. Ma Q, Zhou B, Pu WT. Reassessment of Isl1 and Nkx2-5 cardiac fate maps using a Gata4-based reporter of Cre activity. Dev Biol. 2008;323: 98-104.
38. Sun Y, Liang X, Najafi N, Cass M, Lin L, Cai CL, Chen J, Evans SM. Islet1 is expressed in distinct cardiovascular lineages, including pacemaker and coronary vascular cells. Dev Biol. 2007;304:286-296. (Pubitemid 46399697)
39. Sedmera D, Wessels A, Trusk TC, Thompson RP, Hewett KW, Gourdie RG. Changes in activation sequence of embryonic chick atria correlate with developing myocardial architecture. Am J Physiol. 2006;291: H1646-H1652. (Pubitemid 44497668)
40. Op't Hof T. The mammalian sinoatrial node. Cardiovasc Drugs Ther. 1988;1:572-597.
41. Moorman AF, Christoffels VM. Cardiac chamber formation: development, genes, and evolution. Physiol Rev. 2003;83:1223-1267. (Pubitemid 37222272)
42. Ho SY, Seo JW, Brown NA, Cook AC, Fagg NL, Anderson RH. Morphology of the sinus node in human and mouse hearts with isomerism of the atrial appendages. Br Heart J. 1995;74:437-442.
43. Kurosawa H, Becker AE. Atrioventricular Conduction in Congenital Heart Disease: Surgical Anatomy. Berlin: Springer-Verlag Berlin; 1987.
44. Janse MK, Anderson RH, van Capelle FJ, Durrer D. A combined electrophysiological and anatomical study of the human fetal heart. Am Heart J. 1976;91:556-562.
45. Aanhaanen WT, Boukens BJ, Sizarov A, Wakker V, de Gier-de Vries C, van Ginneken AC, Moorman AF, Coronel R, Christoffels VM. Defective Tbx2-dependent patterning of the atrioventricular canal myocardium causes accessory pathway formation in mice. J Clin Invest. 2011;121: 534-544.
46. Gaussin V, Morley GE, Cox L, Zwijsen A, Vance KM, Emile L, Tian Y, Liu J, Hong C, Myers D, Conway SJ, Depre C, Mishina Y, Behringer RR, Hanks MC, Schneider MD, Huylebroeck D, Fishman GI, Burch JB, Vatner SF. Bmpr1a receptor is required for development of the atrioventricular canal into valves and annulus fibrosus. Circ Res. 2005;97: 219-226. (Pubitemid 41105447)
47. Peters NS, Rowland E, Bennett JG, Green CR, Anderson RH, Severs NJ. The Wolff-Parkinson-White syndrome: the cellular substrate for conduction in the accessory atrioventricular pathway. Eur Heart J. 1994;15: 981-987. (Pubitemid 24223960)
48. Hahurij ND, Gittenberger-De Groot AC, Kolditz DP, Bökenkamp R, Schalij MJ, Poelmann RE, Blom NA. Accessory atrioventricular myocardial connections in the developing human heart. Circulation. 2008;117:2850-2858.