Embryology of the heart and its impact on understanding fetal and neonatal heart disease

Seminars in Fetal and Neonatal Medicine

Volumn 18, Issue 5, 2013, Pages 237-244

  Gittenberger de Groot, Adriana C ^a   Bartelings, Margot M ^a   Poelmann, Robert E ^a   Haak, Monique C ^a   Jongbloed, Monique R M ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Cardiac development; Congenital heart malformation; Epicardium; First heart field; Neural crest cells; Nuchal translucency; Second heart field

Indexed keywords

AORTA ARCH; AORTA ARCH ANOMALY; AORTA VALVE; AORTA VALVE REGURGITATION; ARTICLE; ATRIOVENTRICULAR CANAL; ATRIOVENTRICULAR SEPTAL DEFECT; BASEMENT MEMBRANE; CONGENITAL HEART DISEASE; CORONARY ARTERY ANOMALY; CORONARY BLOOD VESSEL; DUCTUS ARTERIOSUS; ENDOCARDIAL CUSHION; ENDOCARDIUM; EPICARDIUM; FALLOT TETRALOGY; FETUS DISEASE; GREAT VESSELS TRANSPOSITION; HEART ATRIUM CONDUCTION; HEART DEVELOPMENT; HEART DISEASE; HEART LEFT VENTRICLE OUTFLOW TRACT; HEART MUSCLE; HEART RIGHT VENTRICLE DOUBLE OUTLET; HEART RIGHT VENTRICLE OUTFLOW TRACT; HEART VENTRICLE SEPTUM; HEART VENTRICLE SEPTUM DEFECT; HUMAN; MESODERM; MITRAL VALVE; NEURAL CREST CELL; NEWBORN DISEASE; NONHUMAN; NUCHAL TRANSLUCENCY MEASUREMENT; PRENATAL DIAGNOSIS; PULMONARY VALVE ATRESIA; PULMONARY VEIN; TRICUSPID VALVE;

CARDIAC DEVELOPMENT; CONGENITAL HEART MALFORMATION; EPICARDIUM; FIRST HEART FIELD; NEURAL CREST CELLS; NUCHAL TRANSLUCENCY; SECOND HEART FIELD;

ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; FETAL DEVELOPMENT; FETAL HEART; HEART DEFECTS, CONGENITAL; HEART DISEASES; HUMANS; INFANT, NEWBORN; MALE; MODELS, CARDIOVASCULAR; PREGNANCY; PRENATAL DIAGNOSIS;

EID: 84884356712     PISSN: 1744165X     EISSN: 18780946     Source Type: Journal    
DOI: 10.1016/j.siny.2013.04.008     Document Type: Article

References (53)

1. Kelly R.G. Molecular inroads into the anterior heart field. Trends Cardiovasc Med 2005, 15:51-56.
2. Brandon E.P., Idzerda R.L., McKnight G.S. Targeting the mouse genome: a compendium of knockouts (part I). Curr Biol 1995, 5:625-634.
3. Noden D.M. Origins and patterning of avian outflow tract endocardial tissues and cushion mesenchyme. Anat Rec 1990, 226:72A-73A.
4. Poelmann R.E., Gittenberger-de Groot A.C., Groenendijk B.C.W., et al. Shear stress in the developing cardiovascular system. Cardiovascular development and congenital malformations: molecular and genetic mechanisms 2005, 169-173. Blackwell Futura, Massachusetts. M. Artman, D.W. Benson, D. Srivastava, M. Nakazawa (Eds.).
5. 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, 5:877-889.
6. Lindsay E.A., Vitelli F., Su H., et al. Tbx1 haploinsufficiency in the DiGeorge syndrome region causes aortic arch defects in mice. Nature 2001, 410:97-101.
7. van den Hoff M.J., Moorman A.F., Ruijter J.M., et al. Myocardialization of the cardiac outflow tract. Dev Biol 1999, 212:477-490.
8. Waldo K.L., Hutson M.R., Stadt H.A., Zdanowicz M., Zdanowicz J., Kirby M.L. Cardiac neural crest is necessary for normal addition of the myocardium to the arterial pole from the secondary heart field. Dev Biol 2005, 281:66-77.
9. Gittenberger-de Groot A.C., Bartelings M.M., DeRuiter M.C., Poelmann R.E. Basics of cardiac development for the understanding of congenital heart malformations. Pediatr Res 2005, 57:169-176.
10. Scherptong R.W., Jongbloed M.R., Wisse L.J., et al. Morphogenesis of outflow tract rotation during cardiac development: the pulmonary push concept. Dev Dyn 2012, 241:1413-1422.
11. Bajolle F., Zaffran S., Meilhac S.M., et al. Myocardium at the base of the aorta and pulmonary trunk is prefigured in the outflow tract of the heart and in subdomains of the second heart field. Dev Biol 2008, 313:25-34.
12. Poelmann R.E., Mikawa T., Gittenberger-de Groot A.C. Neural crest cells in outflow tract septation of the embryonic chicken heart: differentiation and apoptosis. Dev Dyn 1998, 212:373-384.
13. Wenink A.C.G. Embryology of the ventricular septum. Separate origin of its components. Virchows Arch 1981, 390:71-79.
14. Lamers W.H., Wessels A., Verbeek F.J., et al. New findings concerning ventricular septation in the human heart. Implications for maldevelopment. Circulation 1992, 86:1194-1205.
15. Bartelings M.M., Gittenberger-de Groot A.C. The outflow tract of the heart - embryologic and morphologic correlations. Int J Cardiol 1989, 22:289-300.
16. Bartelings M.M., Gittenberger-de Groot A.C. Morphogenetic considerations on congenital malformations of the outflow tract. Part 2: complete transposition of the great arteries and double outlet right ventricle. Int J Cardiol 1991, 33:5-26.
17. Bartelings M.M., Gittenberger-de Groot A.C. Morphogenetic considerations on congenital malformations of the outflow tract. Part 1: common arterial trunk and tetralogy of Fallot. Int J Cardiol 1991, 32:213-230.
18. Gittenberger-de Groot A.C., Bartelings M.M., Bogers A.J.J.C., Boot M.J., Poelmann R.E. The embryology of the common arterial trunk. Prog Pediatr Cardiol 2002, 15:1-8.
19. Jacobs M.L., Anderson R.H. Rationalising the nomenclature of common arterial trunk. Cardiol Young 2012, 22:639-646.
20. Garg V., Muth A.N., Ransom J.F., et al. Mutations in NOTCH1 cause aortic valve disease. Nature 2005, 437:270-274.
21. Matthias Bechtel J.F., Noack F., Sayk F., Erasmi A.W., Bartels C., Sievers H.H. Histopathological grading of ascending aortic aneurysm: comparison of patients with bicuspid versus tricuspid aortic valve. JHeart Valve Dis 2003, 12:54-59.
22. Gittenberger-De Groot A.C., Jongbloed M.R.M., Poelmann R.E. Normal and abnormal cardiac development. Pediatric cardiovascular medicine 2012, 1-22. Blackwell, Oxford. 2nd ed. J.H. Moller, J.I. Hoffman (Eds.).
23. Moene R.J., Oppenheimer-Dekker A., Moulaert A.J. The concurrence of dimensional aortic arch anomalies and abnormal left ventricular muscle bundles. Pediatr Cardiol 1982, 2:107-114.
24. Gittenberger-de Groot A.C., Mahtab E.A.F., Hahurij N.D., et al. Nkx2.5 negative myocardium of the posterior heart field and its correlation with podoplanin expression in cells from the developing cardiac pacemaking and conduction system. Anat Rec 2007, 290:115-122.
25. Christoffels V.M., Mommersteeg M.T., 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, 98:1555-1563.
26. Douglas Y.L., Jongbloed M.R., DeRuiter M.C., Gittenberger-de Groot A.C. Normal and abnormal development of pulmonary veins: state of the art and correlation with clinical entities. Int J Cardiol 2011, 147:13-24.
27. Lescroart F., Mohun T., Meilhac S.M., Bennett M., Buckingham M. Lineage tree for the venous pole of the heart: clonal analysis clarifies controversial genealogy based on genetic tracing. Circ Res 2012, 111:1313-1322.
28. Blom N.A., Gittenberger-de Groot A.C., DeRuiter M.C., Poelmann R.E., Mentink M.M., 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.
29. Jongbloed M.R., Vicente S.R., Hahurij N.D., et al. Normal and abnormal development of the cardiac conduction system; implications for conduction and rhythm disorders in the child and adult. Differentiation 2012, 84:131-148.
30. Blom N.A., Ottenkamp J., Wenink A.G., Gittenberger-de Groot A.C. Deficiency of the vestibular spine in atrioventricular septal defects in human fetuses with down syndrome. Am J Cardiol 2003, 91:180-184.
31. Snarr B.S., Wirrig E.E., Phelps A.L., Trusk T.C., Wessels A. Aspatiotemporal evaluation of the contribution of the dorsal mesenchymal protrusion to cardiac development. Dev Dyn 2007, 236:1287-1294.
32. Moskowitz I.P., Kim J.B., Moore M.L., et al. Amolecular pathway including Id2, Tbx5, and Nkx2-5 required for cardiac conduction system development. Cell 2007, 129:1365-1376.
33. Viragh S., Challice C.E. The origin of the epicardium and the embryonic myocardial circulation in the mouse. Anat Rec 1981, 201:157-168.
34. Poelmann R.E., Gittenberger-de Groot A.C., Mentink M.M.T., Bökenkamp R., Hogers B. Development of the cardiac coronary vascular endothelium, studied with antiendothelial antibodies, in chicken-quail chimeras. Circ Res 1993, 73:559-568.
35. Gittenberger-de Groot A.C., Vrancken Peeters M.-P.F.M., Mentink M.M.T., Gourdie R.G., Poelmann R.E. Epicardium-derived cells contribute a novel population to the myocardial wall and the atrioventricular cushions. Circ Res 1998, 82:1043-1052.
36. Lie-Venema H., van den Akker N.M.S., Bax N.A.M., et al. Origin, fate, and function of epicardium-derived cells (EPDCs) in normal and abnormal cardiac development. ScientificWorldJournal 2007, 7:1777-1798.
37. Gittenberger-de Groot A.C., Winter E.M., Bartelings M.M., Goumans M.J., DeRuiter M.C., Poelmann R.E. The arterial and cardiac epicardium in development, disease and repair. Differentiation 2012, 84:41-53.
38. van W.B., van den Hoff M. Epicardium and myocardium originate from a common cardiogenic precursor pool. Trends Cardiovasc Med 2010, 20:1-7.
39. Perez-Pomares J.M., Phelps A., Sedmerova M., Wessels A. Epicardial-like cells on the distal arterial end of the cardiac outflow tract do not derive from the proepicardium but are derivatives of the cephalic pericardium. Dev Dyn 2003, 227:56-68.
40. Gittenberger-de Groot A.C., Tennstedt C., Chaoui R., Lie-Venema H., Sauer U., Poelmann R.E. Ventriculo coronary arterial communications (VCAC) and myocardial sinusoids in hearts with pulmonary atresia with intact ventricular septum: two different diseases. Prog Pediatr Cardiol 2001, 13:157-164.
41. Bogers A.J.J.C., Gittenberger-de Groot A.C., Poelmann R.E., Péault B.M., Huysmans H.A. Development of the origin of the coronary arteries, a matter of ingrowth or outgrowth?. Anat Embryol 1989, 180:437-441.
42. Eralp I., Lie-Venema H., DeRuiter M.C., et al. Coronary artery and orifice development is associated with proper timing of epicardial outgrowth and correlated Fas ligand associated apoptosis patterns. Circ Res 2005, 96:526-534.
43. Lie-Venema H., Gittenberger-de Groot A.C., van Empel L.J.P., et al. Ets-1 and Ets-2 transcription factors are essential for normal coronary and myocardial development in chicken embryos. Circ Res 2003, 92:749-756.
44. Lie-Venema H., Eralp I., Markwald R.R., et al. Periostin expression by epicardium-derived cells (EPDCs) is involved in the development of the atrioventricular valves and fibrous heart skeleton. Differentiation 2008, 76:809-819.
45. Van Hare G.F. Radiofrequency ablation of accessory pathways associated with congenital heart disease. Pacing Clin Electrophysiol 1997, 20:2077-2081.
46. Gittenberger-de Groot A.C., Winter E.M., Poelmann R.E. Epicardium-derived cells (EPDCs) in development, cardiac disease and repair of ischemia. JCell Mol Med 2010, 14:1056-1060.
47. Limana F., Capogrossi M.C., Germani A. The epicardium in cardiac repair: from the stem cell view. Pharmacol Ther 2011, 129:82-96.
48. Zhou B., Pu W.T. Epicardial epithelial-to-mesenchymal transition in injured heart. JCell Mol Med 2011, 15:2781-2783.
49. Haak M.C., Bartelings M.M., Gittenberger-de Groot A.C., Van Vugt J.M. Cardiac malformations in first-trimester fetuses with increased nuchal translucency: ultrasound diagnosis and postmortem morphology. Ultrasound Obstet Gynecol 2002, 20:14-21.
50. Simpson J.M., Sharland G.K. Nuchal translucency and congenital heart defects: heart failure or not?. Ultrasound Obstet Gynecol 2000, 16:30-36.
51. Hyett J.A., Perdu M., Sharland G.K., Snijders R.S., Nicolaides K.H. Increased nuchal translucency at 10-14 weeks of gestation as a marker for major cardiac defects. Ultrasound Obstet Gynecol 1997, 10:242-246.
52. Bekker M.N., Van Den Akker N.M., Bartelings M.M., et al. Nuchal edema and venous-lymphatic phenotype disturbance in human fetuses and mouse embryos with aneuploidy. JSoc Gynecol Investig 2006, 13:209-216.
53. Steegers-Theunissen R.P., Steegers E.A. Nutrient-gene interactions in early pregnancy: a vascular hypothesis. Eur J Obstet Gynecol Reprod Biol 2003, 106:115-117.