Cardiac cell lineages that form the heart

Cold Spring Harbor Perspectives in Medicine

Volumn 4, Issue 9, 2014, Pages

  Meilhac, Sigolène M ^a   Lescroart, Fabienne ^b   Blanpain, Cédric ^b   Buckingham, Margaret E ^a  

^a CNRS   (France)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CONGENITAL HEART MALFORMATION; EMBRYO CELL; ENDOCARDIUM; ENDOTHELIUM CELL; ENHANCER REGION; EPICARDIUM; FACIAL EXPRESSION; GENETIC ENGINEERING; HEART MUSCLE; HEART MUSCLE CELL; HEART MUSCLE CONDUCTION SYSTEM; NONHUMAN; PRIMITIVE STREAK; SMOOTH MUSCLE FIBER; STEM CELL; ANIMAL; CYTOLOGY; EMBRYOLOGY; HEART; HUMAN;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; HEART; HEART DEFECTS, CONGENITAL; HUMANS; MYOCYTES, CARDIAC;

EID: 84922335315     PISSN: None     EISSN: 21571422     Source Type: Journal    
DOI: 10.1101/cshperspect.a013888     Document Type: Article

References (103)

1. Abu-Issa R, Kirby ML. 2007. Heart field: From mesoderm to heart tube. Annu Rev Cell Dev Biol 23: 45–68.
2. Bajolle F, Zaffran S, Meilhac SM, Dandonneau M, Chang T, Kelly RG, Buckingham ME. 2008. 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 313: 25–34.
3. Bajolle F, Zaffran S, Losay J, Ou P, Buckingham M, Bonnt D. 2009. Conotruncal defects associated with anomalous pulmonary venous connections. Arch Cardiovasc Dis 102: 105–110.
4. Bondue A, Lapouge G, Paulissen C, Semeraro C, Iacovino M, Kyba M, Blanpain C. 2008. Mesp1 acts as a master regulator of multipotent cardiovascular progenitor specification. Cell Stem Cell 3: 69–84.
5. Bondue A, Tannler S, Chiapparo G, Chabab S, Ramialison M, Paulissen C, Beck B, Harvey R, Blanpain C. 2011. Defining the earliest step of cardiovascular progenitor specification during embryonic stem cell differentiation. J Cell Biol 192: 751–765.
6. Bressan M, Liu G, Mikawa T. 2013. Early mesodermal cues assign avian cardiac pacemaker fate potential in a tertiary heart field. Science 340: 744–748.
7. Brown CB, Wenning JM, Lu MM, Epstein DJ, Meyers EN, Epstein JA. 2004. Cre-mediated excision of Fgf8 in the Tbx1 expression domain reveals a critical role for Fgf8 in cardiovascular development in the mouse. Dev Biol 267: 190–202.
8. Buckingham ME, Meilhac SM. 2011. Tracing cells for tracking cell lineage and clonal behavior. DevCell 21: 394–409.
9. Buckingham M, Biben C, Lawson KA. 1997. Fate mapping of pre-cardiac cells in the developing mouse. In Genetic control of heart development (ed. Olson EN, Harvey RP, Schultz RA, Altman JS), pp. 31–33. HSFP, Strasbourg.
10. Cai CL, Liang X, Shi Y, Chu PH, Pfaff SL, Chen J, Evans S. 2003. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev Cell 5: 877–889.
11. Cai CL, Martin JC, Sun Y, Cui L, Wang L, Ouyang K, Yang L, Bu L, Liang X, Zhang X, et al. 2008. A myocardial lineage derives from Tbx18 epicardial cells. Nature 454: 104-108.
12. Chan-Thomas PS, Thompson RP, Robert B, Yacoub MH, Barton PJ. 1993. Expression of homeobox genes Msx-1 (Hox-7) and Msx-2 (Hox-8) during cardiac development in the chick. Dev Dyn 197: 203–216.
13. Christoffels VM, Habets PE, Franco D, Campione M, de Dong F, Lamers WH, Bao ZZ, Palmer S, Biben C, Harvey RP, et al. 2000. Chamberformation and morphogenesis in the developing mammalian heart. Dev Biol 223: 266–278.
14. Christoffels VM, Mommersteeg MT, Trowe MO, Prall O W, de Gier-de Vries C, Soufan AT, Bussen M, Schuster-Gossler K, Harvey RP, Moorman AF, et al. 2006. Formation of the venous pole of the heart froman Nkx2-5-negative precursor population requires Tbx18. Circ Res 98: 1555–1563.
15. Christoffels VM, Grieskamp T, Norden J, Mommersteeg MT, Rudat C, Kispert A. 2009. Tbx18 and the fate of epicardial progenitors. Nature 458: 8–9; discussion E9–E10.
16. Cui C, Cheuvront TJ, Lansford RD, Moreno-Rodriguez RA, Schultheiss TM, Rongish BJ. 2009. Dynamic positional fate map of the primary heart-forming region. Dev Biol 332: 212–222.
17. David R, Brenner C, Stieber J, Schwarz F, Brunner S, Vollmer M, Mentele E, Muller-Hocker J, Kitajima S, Lickert H, et al. 2008.MesP1 drives vertebrate cardiovascular differentiation through Dkk-1-mediated blockade of Wnt-signalling. Nat Cell Biol 10: 338–345.
18. Delorme B, Dahl E, Jarry-Guichard T, Briand JP, Willecke K, Gros D, Theveniau-Ruissy M. 1997. Expression pattern of connexin gene products at the early developmental stages of the mouse cardiovascular system. CircRes 81: 423–437.
19. De Val S, Chi NC, Meadows SM, Minovitsky S, Anderson JP, Harris IS, Ehlers ML, Agarwal P, Visel A, Xu SM, et al. 2008. Combinatorial regulation of endothelial gene expression by ets and forkhead transcription factors. Cell 135: 1053–1064.
20. Dodou E, Verzi MP, Anderson JP, Xu SM, Black BL. 2004. Mef2c is a direct transcriptional target of ISL1 and GATA factors in the anterior heart field during mouse embryonic development. Development 131: 3931–3942.
21. Dominguez JN, Meilhac SM, Bland YS, Buckingham ME, Brown NA. 2012. Asymmetric fate of the posterior part of the second heart field results in unexpected left/right contributions to both poles of the heart. Circ Res 111: 1323–1335.
22. Dunwoodie SL, Rodriguez TA, Beddington RS. 1998. Msg1 and Mrg1, founding members of a gene family, show distinct patterns of gene expression during mouse embryogenesis. Mech Dev 72: 27–40.
23. Ferdous A, Caprioli A, Iacovino M, Martin CM, Morris J, Richardson JA, Latif S, Hammer RE, Harvey RP, Olson EN, et al. 2009.Nkx2–5 transactivates the Ets-related protein 71 gene and specifies an endothelial/endocardial fate in the developing embryo. Proc Natl Acad Sci 106: 814–819.
24. Franco D, Meilhac SM, Christoffels VM, Kisp ert A, Buckingham M, Kelly RG. 2006. Left and right ventricular contributions to the formation of the interventricular septum in the mouse heart. Dev Biol 294: 366–375.
25. Galli D, Dominguez JN, Zaffran S, Munk A, Brown NA, Buckingham ME. 2008. Atrial myocardium derives from the posterior region of the second heart field, which acquires left-right identity as Pitx2c is expressed. Development 135: 1157–1167.
26. Galvez BG, Sampaolesi M, Barbuti A, Crespi A, Covarello D, Brunelli S, Dellavalle A, Crippa S, Balconi G, Cuccovillo I, et al. 2008. Cardiac mesoangioblasts are committed, selfrenewable progenitors, associated with small vessels of juvenilemouseventricle. CellDeath Differ 15: 1417–1428.
27. Garcia-Martinez V, Schoenwolf GC. 1993. Primitive-streak origin of the cardiovascular system in avian embryos. Dev Biol 159: 706–719.
28. Gelb B, Brueckner M, Chung W, Goldmuntz E, Kaltman J, Kaski JP, Kim R, Kline J, Mercer-Rosa L, Porter G, et al. 2013. The Congenital Heart Disease Genetic Network Study: Rationale, design, and early results. Circ Res 112: 698–706.
29. Gorza L, Schiaffino S, Vitadello M. 1988. Heart conduction system: A neural crest derivative? Brain Res 457: 360–366.
30. Gourdie RG, Wei Y, Kim D, Klatt SC, Mikawa T. 1998. Endothelin induced conversion of embryonic heart muscle cells into impulse-conducting Purkinje fibers. Proc Natl Acad Sci 95: 6815–6818.
31. Grego-Bessa J, Luna-Zurita L, delMonte G, Bolos V, Melgar P, Arandilla A, Garratt AN, Zang H, Mukouyama YS, Chen H, et al. 2007. Notch signaling is essential for ventricular chamber development. Dev Cell 12: 415–429.
32. Gupta V, Poss KD. 2012. Clonally dominant cardiomyocytes direct heart morphogenesis. Nature 484: 479–484.
33. Harel I, Nathan E, Tirosh-Finkel L, Zigdon H, Guimaraes Camboa N, Evans SM, Tzahor E. 2009. Distinct origins and genetic programs of head muscle satellite cells. Dev Cell 16: 822–832.
34. Harris IS, Black BL. 2010. Development of the endocardium. Pediatr Cardiol 31: 391–399.
35. Hoogaars WM, Tessari A, Moorman AF, de Boer PA, Hagoort J, Soufan AT, Campione M, Christoffels VM. 2004. The transcriptional repressor Tbx3 delineates the developing central conduction system of the heart. Cardiovasc Res 62: 489–499.
36. Hutson MR, Zeng XL, Kim AJ, Antoon E, Harward S, Kirby ML. 2010. Arterial pole progenitors interpret opposing FGF/BMP signals to proliferate or differentiate. Development 137: 3001–3011.
37. Kattman SJ, Huber TL, Keller GM. 2006.Multipotent flk-1þ cardiovascular progenitor cells give rise to the cardiomyocyte, endothelial, and vascular smooth muscle lineages. Dev Cell 11: 723–732.
38. Kaufman MH, Navaratnam V. 1981. Early differentiation of the heart in mouse embryos. J Anat 133: 235–246.
39. Kelly RG, Brown NA, Buckingham ME. 2001. The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev Cell 1: 435–440.
40. Kinder SJ, Tsang TE, Quinlan GA, Hadjantonakis AK, Nagy A, Tam PP. 1999. The orderly allocation of mesodermal cells to the extraembryonic structures and the anteroposterior axis during gastrulation of the mouse embryo. Development 126: 4691–4701.
41. Kitajima S, Takagi A, Inoue T, Saga Y. 2000. MesP1 and MesP2 are essential for the development of cardiac mesoderm. Development 127: 3215–3226.
42. Kitajima S, Miyagawa-Tomita S, Inoue T, Kanno J, Saga Y. 2006. Mesp1-nonexpressing cells contribute to the ventricularcardiac conduction system. Dev Dyn 235: 395–402.
43. Kochilas LK, Li J, Jin F, Buck CA, Epstein JA. 1999. p57Kip2 expression is enhanced during mid-cardiac murine development and is restricted to trabecular myocardium. Pediatr Res 45: 635–642.
44. Kraus F, Haenig B, Kispert A. 2001. Cloning and expression analysis of the mouse T-box gene Tbx18. Mech Dev 100: 83–86.
45. Kruithof BP, vanWijk B, Somi S, Kruithof-de Julio M, Perez Pomares JM, Weesie F, Wessels A, Moorman AF, van den Hoff MJ. 2006. BMPand FGF regulate the differentiation of multipotential pericardial mesoderm into themyocardial or epicardial lineage. Dev Biol 295: 507–522.
46. Lamers WH, De Jong F, De Groot IJ, Moorman AF. 1991. The development of the avian conduction system, a review. Eur J Morphol 29: 233–253.
47. Lawson KA, Pedersen RA. 1987. Cell fate, morphogenetic movement and population kinetics of embryonic endoderm at the time of germ layer formation in the mouse. Development 101: 627–652.
48. Lescroart F, Kelly RG, Le Garrec JF, Nicolas JF, Meilhac S, Buckingham M. 2010. Clonal analysis reveals common lineage relationships between head muscles and second heart field derivatives in the mouse embryo. Development 137: 3269–3279.
49. Lescroart F, Mohun T, Meilhac SM, Bennett M, Buckingham M. 2012. Lineage tree for the venous pole of the heart: Conal analysis clarifies controversial genealogy based on genetic tracing. Circ Res 111: 1313–1322.
50. Liang X, Wang G, Lin L, Lowe J, Zhang Q, Bu L, Chen Y, Chen J, Sun Y, Evans SM. 2013.HCN4dynamically marks the first heart field and conduction system precursors. Circ Res 113: 399–407.
51. Linask KK, Knudsen KA, Gui YH. 1997. N-cadherin-catenin interaction: Necessary component of cardiac cell compartmentalization during early vertebrate heart development. Dev Biol 185: 148–164.
52. Lindsley RC, Gill JG, Murphy TL, Langer EM, Cai M, Mashayekhi M, Wang W, Niwa N, Nerbonne JM, Kyba M, et al. 2008. Mesp1 coordinately regulates cardiovascular fate restriction and epithelial-mesenchymal transition in differentiating ESCs. Cell Stem Cell 3: 55–68.
53. Ma Q, Zhou B, Pu WT. 2008. Reassessment of Isl1 and Nkx2-5 cardiac fate maps using a Gata4-based reporter of Cre activity. Dev Biol 323: 98–104.
54. Martinez-Estrada OM, Lettice LA, Essafi A, Guadix JA, Slight J, Velecela V, Hall E, Reichmann J, Devenney PS, Hohenstein P, et al. 2010. Wt1 is required for cardiovascular progenitor cell formation through transcriptional control of Snail and E-cadherin. Nat Genet 42: 89–93.
55. Meilhac SM, Kelly RG, Rocancourt D, Eloy-Trinquet S, Nicolas JF, Buckingham ME. 2003. A retrospective clonal analysis of the myocardium reveals two phases of clonal growth in the developing mouse heart. Development 130: 3877–3889.
56. Meilhac SM, Esner M, Kelly RG, Nicolas JF, Buckingham ME. 2004. The clonal origin of myocardial cells in different regions of the embryonic mouse heart. Dev Cell 6: 685–698.
57. Merki E, Zamora M, Raya A, Kawakami Y, Wang J, Zhang X, Burch J, Kubalak SW, Kaliman P, Belmonte JC, et al. 2005. Epicardial retinoid X receptor a is required for myocardial growth and coronary artery formation. Proc Natl Acad Sci 102: 18455–18460.
58. Mikawa T, Cohen-Gould L, Fischman DA. 1992. Clonal analysis of cardiac morphogenesis in the chicken embryo using a replication-defective retrovirus: III. Polyclonal origin of adjacent ventricular myocytes. Dev Dyn 195:133–141.
59. Miquerol L, Moreno-Rascon N, Beyer S, Dupays L, Meilhac SM, Buckingham ME, Franco D, Kelly RG. 2010. Biphasic development of the mammalian ventricular conduction system. Circ Res 107: 153–161.
60. Miquerol L, Bellon A, Moreno N, Beyer S, Meilhac SM, Buckingham M, Franco D, Kelly RG. 2013. Resolving cell lineage contributions to the ventricular conduction systemwith a Cx40-GFPallele: Adual contribution of the first and second heart fields. Dev Dyn 242: 665–677.
61. Misfeldt AM, Boyle SC, Tompkins KL, Bautch VL, Labosky PA, Baldwin HS. 2009. Endocardial cells are a distinct endothelial lineage derived from Flk1þ multipotent cardiovascular progenitors. Dev Biol 333: 78–89.
62. Moens CB, Stanton BR, Parada LF, Rossant J. 1993. Defects in heart and lung development in compound heterozygotes for two different targeted mutations at the N-myc locus. Development 119: 485–499.
63. Mommersteeg MT, Dominguez JN, Wiese C, Norden J, de Gier-de Vries C, Burch JB, Kispert A, Brown NA, Moorman AF, Christoffels VM. 2010. The sinus venosus progenitors separate and diversify from the first and second heart fields early in development. Cardiovasc Res 87: 92-101.
64. Moretti A, Caron L, Nakano A, Lam JT, Bernshausen A, Chen Y, Qyang Y, Bu L, Sasaki M, Martin-Puig S, et al. 2006. Multipotent embryonic isl1þ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell 127: 1151–1165.
65. Nakagawa O, Nakagawa M, Richardson JA, Olson EN, Srivastava D. 1999.HRT1,HRT2, andHRT3:A newsubclass of bHLH transcription factors marking specific cardiac, somitic, and pharyngeal arch segments. Dev Biol 216: 72–84.
66. Nathan E, Monovich A, Tirosh-Finkel L, Harrelson Z, Rousso T, Rinon A, Harel I, Evans SM, Tzahor E. 2008. The contribution of Islet1-expressing splanchnic mesoderm cells to distinct branchiomeric muscles reveals significant heterogeneity in head muscle development. Development 135: 647–657.
67. Neuhaus H, Rosen V, Thies RS. 1999. Heart specific expression of mouse BMP-10 a novel member of the TGF-b superfamily. Mech Dev 80: 181–184.
68. Noden DM, Francis-West P. 2006. The differentiation and morphogenesis of craniofacial muscles. Dev Dyn 235: 1194–1218.
69. Peng T, Tian Y, Boogerd CJ, Lu MM, Kadzik RS, Stewart KM, Evans SM, Morrisey EE. 2013. Coordination of heart and lung co-development by a multipotent cardiopulmonary progenitor. Nature 500: 589–592.
70. Peshkovsky C, Totong R, Yelon D. 2011. Dependence of cardiac trabeculation on neuregulin signaling and blood flow in zebrafish. Dev Dyn 240: 446–456.
71. Qian L, Huang Y, Spencer CI, Foley A, Vedantham V, Liu L, Conway SJ, Fu JD, Srivastava D. 2012. In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature 485: 593–598.
72. Rasmussen TL, Kweon J, Diekmann MA, Belema-Bedada F, Song Q, Bowlin K, Shi X, Ferdous A, Li T, Kyba M, et al. 2011. ER71 directs mesodermal fate decisions during embryogenesis. Development 138: 4801–4812.
73. Red-Horse K, Ueno H, Weissman IL, Krasnow MA. 2010. Coronary arteries form by developmental reprogramming of venous cells. Nature 464: 549–553.
74. Rosenquist GC. 1970. Location and movements of cardiogenic cells in the chick embryo: The heart-forming portion of the primitive streak. Dev Biol 22: 461–475.
75. Saga Y, Miyagawa-Tomita S, Takagi A, Kitajima S, Miyazaki J, Inoue T. 1999. MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube. Development 126: 3437–3447.
76. Saga Y, Kitajima S, Miyagawa-Tomita S. 2000.Mesp1 expression is the earliest sign of cardiovascular development. Trends Cardiovasc Med 10: 345–352.
77. Schulte I, Schlueter J, Abu-Issa R, Brand T, Manner J. 2007. Morphological and molecular left-right asymmetries in the development of the proepicardium: A comparative analysis on mouse and chick embryos. Dev Dyn 236: 684–695.
78. Sedmera D, Reckova M, DeAlmeida A, Coppen SR, Kubalak SW, Gourdie RG, Thompson RP. 2003. Spatiotemporal pattern of commitment to slowed proliferation in the embryonic mouse heart indicates progressive differentiation of the cardiac conduction system. Anat Rec A Discov Mol Cell Evol Biol 274: 773–777.
79. Spater D, Abramczuk MK, Buac K, Zangi L, Stachel MW, Clarke J, Sahara M, Ludwig A, Chien KR. 2013. AHCN4þ cardiomyogenic progenitor derived from the first heart field and human pluripotent stem cells. Nat Cell Biol 15: 1098–1106.
80. Stanley EG, Biben C, Elefanty A, Barnett L, Koentgen F, Robb L, Harvey RP. 2002. Efficient Cre-mediated deletion in cardiac progenitor cells conferred by a 30UTR-ires-Cre allele of the homeobox gene Nkx2-5. Int J Dev Biol 46: 431–439.
81. Staudt DW, Liu J, Thorn KS, Stuurman N, Liebling M, Stainier DY. 2014. High-resolution imaging of cardiomyocyte behavior reveals two distinct steps in ventricular trabeculation. Development 141: 585–593.
82. Stennard FA, Costa MW, Elliott DA, Rankin S, Haast SJ, Lai D, McDonald LP, Niederreither K, Dolle P, Bruneau BG, et al. 2003. Cardiac T-box factor Tbx20 directly interacts with Nkx2-5, GATA4, and GATA5 in regulation of gene expression in the developing heart. Dev Biol 262: 206–224.
83. Sucov HM, Gu Y, Thomas S, Li P, Pashmforoush M. 2009. Epicardial control of myocardial proliferation and morphogenesis. Pediatr Cardiol 30: 617–625.
84. Sun Y, Liang X, Najafi N, Cass M, Lin L, Cai CL, Chen J, Evans SM. 2007. Islet 1 is expressed in distinct cardiovascular lineages, including pacemaker and coronary vascular cells. Dev Biol 304: 286–296.
85. Tam PP, Parameswaran M, Kinder SJ, Weinberger RP. 1997. The allocation of epiblast cells to the embryonic heart and other mesodermal lineages: The role of ingression and tissue movement during gastrulation. Development 124: 1631–1642.
86. Theveniau-Ruissy M, Dandonneau M, Mesbah K, Ghez O, Mattei MG, Miquerol L, Kelly RG. 2008. The del22q11.2 candidate gene Tbx1 controls regional outflow tract identity and coronary artery patterning. Circ Res 103: 142–148.
87. Tirosh-Finkel L, Elhanany H, Rinon A, Tzahor E. 2006. Mesoderm progenitor cells of common origin contribute to the head musculature and the cardiac outflow tract. Development 133: 1943–1953.
88. Tzouanacou E, Wegener A, Wymeersch FJ, WilsonV, Nicolas JF. 2009. Redefining the progression of lineage segregations during mammalian embryogenesis by clonal analysis. Dev Cell 17: 365–376.
89. Van Praagh R. 2009. The first Stella van Praagh memorial lecture: The history and anatomy of tetralogy of Fallot. Semin Thorac Cardiovasc Surg Pediatr Card Surg Annu 2009: 19–38.
90. van Wijk B, van den Berg G, Abu-Issa R, Barnett P, van der Velden S, Schmidt M, Ruijter JM, Kirby ML, Moorman AF, van den Hoff MJ. 2009. Epicardium andmyocardium separate from a common precursor pool by crosstalk between bone morphogenetic protein and fibroblast growth factor-signaling pathways. Circ Res 105: 431–441.
91. Verzi MP, McCulley DJ, De Val S, Dodou E, Black BL. 2005. The right ventricle, outflow tract, and ventricular septum comprise a restricted expression domain within the secondary/anterior heart field. Dev Biol 287: 134–145.
92. Viragh S, Challice CE. 1981. The origin of the epicardium and the embryonic myocardial circulation in the mouse. Anat Rec 201: 157–168.
93. Waldo KL, Hutson MR, Ward CC, Zdanowicz M, Stadt HA, Kumiski D, Abu-Issa R, Kirby ML. 2005. Secondary heart field contributes myocardium and smooth muscle to the arterial pole of the developing heart. Dev Biol 281: 78–90.
94. Ward C, Stadt H, Hutson M, Kirby ML. 2005. Ablation of the secondary heart field leads to tetralogy of Fallot and pulmonary atresia. Dev Biol 284: 72–83.
95. Watanabe Y, Miyagawa-Tomita S, Vincent SD, Kelly RG, Moon AM, Buckingham ME. 2010. Role of mesodermal FGF8 and FGF10 overlaps in the development of the arterial pole of the heart and pharyngeal arch arteries. Circ Res 106: 495–503.
96. Wei Y, Mikawa T. 2000. Fate diversity of primitive streak cells during heart field formation in ovo. Dev Dyn 219: 505–513.
97. Winter EM, Gittenberger-de Groot AC. 2007. Epicardiumderived cells in cardiogenesis and cardiac regeneration. Cell Mol Life Sci 64: 692–703.
98. Wu B, Zhang Z, Lui W, Chen X, Wang Y, Chamberlain AA, Moreno-Rodriguez RA, Markwald RR, O’Rourke BP, Sharp DJ, et al. 2012. Endocardial cells form the coronary arteries by angiogenesis through myocardial-endocardial VEGF signaling. Cell 151: 1083–1096.
99. Xu H, Morishima M, Wylie JN, Schwartz RJ, Bruneau BG, Lindsay EA, Baldini A. 2004. Tbx1 has a dual role in the morphogenesis of the cardiac outflow tract. Development 131: 3217–3227.
100. Zaffran S, Kelly RG, Meilhac SM, Buckingham ME, Brown NA. 2004. Right ventricular myocardium derives from the anterior heart field. Circ Res 95: 261–268.
101. Zhang Z, Cerrato F, Xu H, Vitelli F, Morishima M, Vincentz J, Furuta Y, Ma L, Martin JF, Baldini A, et al. 2005. Tbx1 xpression in pharyngeal epithelia is necessary for pharyngeal arch artery development. Development 132: 5307–5315.
102. Zhou B, Ma Q, Rajagopal S, Wu SM, Domian I, Rivera-Feliciano J, Jiang D, von Gise A, Ikeda S, Chien KR, et al. 2008a. Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454: 109–113.
103. Zhou B, von Gise A, Ma Q, Rivera-Feliciano J, Pu WT. 2008b. Nkx2-5 and Isl1-expressing cardiac progenitors contribute to proepicardium. Biochem Biophys Res Commun 375: 450–453.