The Epicardium and Epicardially Derived Cells (EPDCs) as Cardiac Stem Cells

Anatomical Record - Part A Discoveries in Molecular, Cellular, and Evolutionary Biology

Volumn 276, Issue 1, 2004, Pages 43-57

  Wessels, Andy ^a   Perez Pomares J M ^b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF MÁLAGA   (Spain)

Author keywords

Coronary vasculogenesis; Epicardially derived cells; Epicardium; Heart; Stem cells

Indexed keywords

ANGIOGENESIS; ANIMAL CELL; CELL DIFFERENTIATION; CELL INVASION; CELL MIGRATION; CELL TRANSFORMATION; CORONARY ARTERY; EMBRYO; EMBRYO CELL; ENDOTHELIUM CELL; EPICARDIALLY DERIVED CELL; EPICARDIUM; FIBROBLAST; MESENCHYME CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SMOOTH MUSCLE FIBER; STEM CELL; VASCULAR ENDOTHELIUM;

EID: 0346690330     PISSN: 0003276X     EISSN: None     Source Type: Journal    
DOI: 10.1002/ar.a.10129     Document Type: Review

References (136)

1. Bacigalupo A, Frassoni F, Van Lint MT. 2002. Bone marrow or peripheral blood as a source of stem cells for allogeneic transplantation. Haematologica 87(Suppl 8):4-8.
2. Baird PM, Simmons PJ. 1997. Expression of the Wilms' tumor gene (WT1) in normal hemopoiesis. Exp Hematol 25:312-320.
3. Begley CG, Green AR. 1999. The SCL gene: from case report to critical hematopoietic regulator. Blood 93:2760-2770.
4. Bergmann L, Miething C, Maurer U, Brieger J, Karakas T, Weidmann E, Hoelzer D. 1997. High levels of Wilms' tumor gene (wt1) mRNA in acute myeloid leukemias are associated with a worse long-term outcome. Blood 90:1217-1225.
5. Bouchey D, Drake CJ, Wunsch AM, Little CD. 1996. Distribution of connective tissue proteins during development and neovascularization of the epicardium. Cardiovasc Res 3:104-115.
6. Brown KW, Wilmore HP, Watson JE, Mott MG, Berry PJ, Maitland NJ. 1992. Inactivation of the remaining allele of the WT1 gene in a Wilms' tumour from a WAGR patient. Oncogene 7:763-768.
7. Burch GH, Bedolli MA, McDonough SM, Rosenthal SM, Bristow J. 1995. Embryonic expression of tenascin-X suggests a role in limb muscle, and heart development. Dev Dyn 203:491-504.
8. Carmona R, Gonzalez-Iriarte M, Macias D, Perez-Pomares JM, Garcia-Garrido L, Muñoz-Chápuli R. 2000. Immunolocalization of the transcription factor Slug in the developing avian heart. Anat Embryol (Berl) 201:103-109.
9. Carmona R, González-Iriarte M, Pérez-Pomares JM, Muñoz-Chápuli R. 2001., Localization of the Wilms' tumour protein WT1 in avian embryos. Cell Tiss Res 303:173-186.
10. Chen TH, Chang TC, Kang JO, Choudhary B, Makita T, Tran CM, Burch JB, Eid H, Sucov HM. 2002. Epicardial induction of fetal cardiomyocyte proliferation via a retinoic acid-inducible trophic factor. Dev Biol 250:198-207.
11. Chen Z, Friedrich GA, Soriano P. 1994. Transcriptional enhancer factor 1 disruption by a retroviral gene trap leads to heart defects and embryonic lethality in mice. Genes Dev 8:2293-2301.
12. De Haan RL. 1965. Morphogenesis of the vertebrate heart. In: De Haan RL, Ursprung H, editors. Organogenesis. New York: Holt, Reinhardt & Winston. p 377-419.
13. Dettman RW, Denetclaw W, Ordahl CP, Bristow J. 1998. Common epicardial origin of coronary vascular smooth muscle, perivascular fibroblasts, and intramyocardial fibroblasts in the avian heart. Dev Biol 193:169-181.
14. Dieterlen-Lievre F, Pardanaud L, Bollerot K, Jaffredo T. 2002. Hemangioblasts and hemopoietic stem cells during ontogeny. C R Biol 325:1013-1020.
15. Drake CJ, Brandt SJ, Trusk TC, Little CD. 1997. TAL1/SCL is expressed in endothelial progenitor cells/angioblasts and defines a dorsal-to-ventral gradient of vasculogenesis. Dev Biol 192:17-30.
16. Drake CJ, Flemming PA. 2000. Vasculogenesis in the day 6.5 to 9.5 mouse embryo. Blood 95:1671-1679.
17. Dyson E, Sukov HM, Kubalak SW, Schmid-Schonhein GW, DeLano FA, Evans RM, Chien KR. 1995 Atrial-like phenotype is associated with embryonic ventricular failure in retinoid X receptor alpha -/-mice. Proc Natl Acad Sci USA 92:7386-7390.
18. Eichmann A, Corbel C, Nataf V, Vaigot P, Breant C, Le Douarin NM. 1997. Ligand-dependent development of the endothelial and hemopoietic lineages from embryonic mesodermal cells expressing vascular endothelial growth factor receptor 2. Proc Natl Acad Sci USA 94:5141-5146.
19. Eid H, Larson DM, Springhorn JP, Attawia NA, Nayak RC, Smith TW, Kelly RA. 1992. Role of epicardial mesothelial cells in the modification of phenotype and function of adult rat ventricular myocytes in primary coculture. Circ Res 71:40-50.
20. Filip DA, Radu A, Simionescu M. 1986. Interstitial cells of the heart valves possess characteristics similar to smooth muscle cells. Circ Res 59:310-320.
21. Fransen ME, Lemanski LF. 1990. Epicardial development in the axolotl, Ambystoma mexicanum. Anat Rec 226:228-236.
22. Gittenberger-de Groot AC, Vrancken Peeters MPFM, Mentink MMT, Gourdie RG, Poelmann RE. 1998. Epicardium-derived cells contribute a novel population to the myocardial wall and the atrioventricular cushions. Circ Res 82:1043-1052.
23. Gittenberger-de Groot AC, Vrancken Peeters MP, Bergwerff M, Mentink MM, Poelmann RE. 2000. Epicardial outgrowth inhibition leads to compensatory mesothelial outflow tract collar and abnormal cardiac septation and coronary formation. Circ Res 2000 87: 969-971.
24. Gittenberger-de Groot AC, Tennsdet C, Chaoui R, Lie-Venema H, Sauer U, Poelmann RE. 2001. Ventriculo coronary arterial communications (VCAC) and myocardial sinusoids in hearts with pulmonary atresia with intact ventricular septum: two different diseases. Progr Pediatric Cardiol 13:157-164.
25. Gruber PJ, Kubalak SW, Pexieder T, Sucov HM, Evans RM, Chien KR. 1996. RXR alpha deficiency confers genetic susceptibility for aortic sac, conotruncal, atrioventricular cushion, and ventricular muscle defects in mice. J Clin Invest 98:1332-1343.
26. Haber DA, Housman DE. 1992. Role of the WT1 gene in Wilms' tumour. Cancer Surv 12:105-117.
27. Hadjantonakis A, Papaioannou V. 2001. The stem cells of early embryos. Differentiation 68:159-166.
28. Hay E. 1995. An overview of epithelio-mesenchymal transformation. Acta Anat 154:8-20.
29. Hierlihy AM, Seale P, Lobe C, Rudnicki MA, Megeney LA. 2002. The post-natal heart contains a myocardial stem cell population. FEBS Lett 530:239-243.
30. Hirakow R. 1985. The vertebrate heart in phylogenetic relation to the prechordates. In: Duncker HR, Fleischer G, editors. Vertebrate morphology. Stuttgart: Fischer. p 367-369.
31. Hirakow R. 1992. Epicardial formation in staged human embryos. Acta Anat Nippon 67:616-622.
32. Hiruma T, Hirakow R. 1989. Epicardial formation in embryonic chick heart. Computer aided reconstruction, scanning and transmission electron microscopic studies. Am J Anat 184:129-138.
33. Ho E, Shimada E. 1978. Formation of the epicardium studied with the electron microscope. Dev Biol 66:579-585.
34. Hughes S. 2002. Cardiac stem cells. J Pathol 197:468-478.
35. Hungerford JE, Little CD. 1999. Developmental biology of the vascular smooth muscle cell: building a multilayered vessel wall. J Vasc Res 36:22-27.
36. Hurlé JM, Kitten GT, Sakai LY, Volpiun D, Solursch M. 1994. Elastic extracellular matrix of the embryonic chick heart: an immunohistological study using laser confocal microscopy. Dev Dyn 200:321-332.
37. Hutchins GM, Kessler-Hanna A, Moore GW. 1988. Development of the coronary arteries in the embryonic human heart. Circulation 77:1250-1257.
38. Jaber M, Koch WJ, Rockman H, Smith B, Bond RA, Sulik KK, Ross Jr J, Lefkowitz RJ, Caron MG, Giros B. 1996. Essentíal role of beta-adrenergic receptor kinase 1 in cardiac development and function. Proc Natl Acad Sci USA 93:12974-12979.
39. Jackson KA, Majka SM, Wang H, Pocius J, Hartley CJ, Majesky MW, Entman ML, Michael LH, Hirschi KK, Goodell MA. 2001. Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J Clin Invest 107:1395-1402.
40. Jaffredo T, Gautier R, Eichmann A, Dieterlen-Lievre F. 1998. Intraaortic hemopoietic cells are derived from endothelial cells during ontogeny. Development 125:4575-4583.
41. Kálmán F, Viragh S, Modis L. 1995. Cell surface glycoconjugates and the extracellular matrix of the developing mouse embryo epicardium. Anat Embryol 191:451-464.
42. Kastner P, Mark M, Ghyselinck N, Krezel W, Dupe V, Grondona JM, Chambon P. 1997. Genetic evidence that the retinoid signal is transduced by heterodimeric RXR/RAR functional units during mouse development. Development 124:313-326.
43. Kim H, Yoon CS, Kim H, Rah B. 1999. Expression of extracellular matrix components fibronectin and laminin in the human fetal heart. Cell Struct Funct 24:19-26.
44. King-Underwood L, Renshaw J, Pritchard-Jones K. 1996. Mutations in the Wilms' tumor gene WT1 in leukemias. Blood 87:2171-2179.
45. Kitsukawa T, Shimono A, Kawakami A, Kondoh H, Fujisawa H. 1995. Overexpression of a membrane protein, neuropilin, in chimeric mice causes anomalies in the cardiovascular system, nervous system and limbs. Development 121:4309-4318.
46. Kon K, Fujiwara T. 1994. Transformation of fibroblasts into endothelial cells during angiogenesis. Cell Tissue Res 278:625-628.
47. Krug EL, Rezaee M, Isokawa K, Turner DK, Litke LL, Wunsch AM, Bain JL, Riley DA, Capehart AA, Markwald RR. 1995. Transformation of cardiac endothelium into cushion mesenchyme is dependent on ES/130: temporal, spatial, and functional studies in the early chick embryo. Cell Mol Biol Res 41:263-277.
48. Kuhn HJ, Liebherr G. 1988. The early development of the epicardium in Tupaia belangeri. Anat Embryol 177:225-234.
49. Kurkiewicz T. 1909. O histogenezie miesna sercowego zwierzat kregowych-Zur Histogenese des Hersmuskels der Wilbertiere. Bull Int Acad Sci Cracovie 148-191.
50. Kwee L, Baldwin HS, Shen HM, Stewart CL, Buck C, Buck CA, Labow MA. 1995. Defective development of the embryonic and extraembryonic circulatory systems in vascular cell adhesion molecule (VCAM-1) deficient mice. Development 121:489-503.
51. Laflamme MA, Myerson D, Saffitz JE, Murry CE. 2002. Evidence for cardiomyocyte repopulation by extracardiac progenitors in transplanted human hearts. Circ Res 90:634-640.
52. Landerholm TE, Dong XR, Lu J, Belaguli NS, Schwartz RJ, Majesky MW. 1999. A role for serum response factor in coronary smooth muscle differentiation from proepicardial cells. Development 126: 2053-2062.
53. Langford JK, Hay DA, Bolender DL. 1990. Fine structural features of coronary vasculogenesis in collagen lattices. In: Bockman DE, Kirby ML, editors. Embryonic origins of defective heart development. Ann NY Acad Sci 588:404-408.
54. Li WE, Waldo K, Linask KL, Chen T, Wessels A, Parmacek MS, Kirby ML, Lo CW. 2002. An essential role for connexin43 gap junctions in mouse coronary artery development. Development 129:2031-2042.
55. Lie-Venema H, Gittenberger-de Groot AC, van Empel LJ, Boot MJ, Kerkdijk H, de Kant E, DeRuiter MC. 2003. Ets-1 and Ets-2 transcription factors are essential for normal coronary and myocardial development in chicken embryos. Circ Res 92:749-756.
56. Little M, Holmes G, Walsh P. 1999. WT1: what has the last decade told us? Bioessays 21:191-202.
57. Lu J, Landerholm TE, Wei JS, Dong XR, Wu SP, Liu X, Nagata K, Inagaki M, Majesky MW. 2001. Coronary smooth muscle differentiation from proepicardial cells requires rhoA-mediated actin reorganization and p160 rho-kinase activity. Dev Biol 240:404-418.
58. Macias D, Pérez-Pomares JM, García-Garrido L, Carmona R, Muñoz-Chápuli R. 1998. Immunoreactivity of the ets-1 transcription factor correlates with areas of epithelial-mesenchymal transition in the developing avian heart. Anat Embryol 198:307-315.
59. Manasek FJ. 1968. Embryonic development of the heart I. A light and electron microscopic study of myocardial development in the early chick embryo. J Morphol 125:329-366.
60. Manasek FJ. 1969. Embryonic development of the heart II. Development of the epicardium. J Embryol Exp Morphol 22:333-348.
61. Männer J. 1992. The development of pericardial villi in the chick embryo. Anat Embryol 186:379-385.
62. Männer J. 1993. Experimental study on the formation of the epicardium in chick embryos. Anat Embryol 187:281-289.
63. Männer J. 1999. Does the subepicardial mesenchyme contribute myocardioblasts to the chick embryo heart? A quail-chick chimera study tracing the fate of the epicardial primordium. Anat Rec 255:212-226.
64. Männer J, Pérez-Pomares JM, Macías D, Muñoz-Chápuli R. 2001. The origin, formation, and developmental significance of the epicardium: a review. Cell Tissues Organs 169:89-103.
65. Markwald RR, Fitzharris TP, Smith WN. 1975. Structural analysis of endocardial cytodifferentiation. Dev Biol 42:160-180.
66. Markwald RR, Fitzharris TP, Manasek FJ. 1977. Structural development of endocardial cushions. Am J Anat 148:85-119.
67. Markwald RR, Eisenberg C, Esisenberg L, Trusk T, Sugi Y. 1996. Epithelial-mesenchymal transformations in early avian development. Acta Anat 156:173-186.
68. Mikawa T, Fischman, DA. 1992. Retroviral analysis of cardiac morphogenesis: discontinuous formation of coronary vessels. Proc Natl Acad Sci USA 89:9504-9508.
69. Mikawa T, Gourdie, RG. 1996. Pericardial mesoderm generates a population of coronary smooth muscle cells migrating into the heart along with ingrowth of the epicardial organ. Dev Biol 174:221-232.
70. Minasi MG, Riminucci M, De Angelis L, Borello U, Berarducci B, Innocenzi A, Caprioli A, Sirabella D, Baiocchi M, De Maria R, Boratto R, Jaffredo T, Broccoli V, Bianco P, Cossu G. 2002. The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development 129:2773-2783.
71. Mjaatvedt CH, Yamamura H, Wessels A, Ramsdell A, Turner D, Markwald RR. 1999. Mechanisms of segmentation, septation, and remodelling of the tubular heart: endocardial cushion fate and cardiac looping. In: Harvey RP, Rosenthal N, editors. Heart development. San Diego: Academic Press. p 159-177.
72. 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.
73. Mollier S. 1906. Die erste Anlage des Herzens bei den Wirbeltieren. In: Hertwig O, editor. Handbuch der vergleichnden und experimentellen Entwincklungslehre der Wilbertiere. Jena: Gustav Fischer. Vol. 1 (Sect 1), p 1026-1051.
74. Moore AW, McInnes L, Kreidberg J, Hastie ND, Schedl A. 1999. YAC complementation shows a requirement for Wt1 in the development of epicardium, adrenal gland and throughout nephrogenesis. Development 126:1845-1857.
75. Morabito CJ, Dettman RW, Kattan J, Collier JM, Bristow J. 2001. Positive and negative regulation of epicardial-mesenchymal transition during avian heart development. Dev Biol 234:204-215.
76. Morita T, Shinozawa T, Nakamura M, Awaya A, Sato N, Ishiwata I, Kami K. 1998. Expression of a 68kDa-glycoprotein (GP68) and laminin in the mesodermal tissue of the developing mouse embryo. Okajimas Folia Anat Jpn 75:185-195.
77. Morris EWT. 1976. Observations on the source of embryonic myocardioblasts. J Anat 121:47-64.
78. Moss JB, Xavier-Neto J, Shapiro MD, Nayeem SM, McCaffery P, Dräger U, Rosenthal N. 1998. Dynamic patterns of retinoic acid synthesis and response in the developing mammalian heart. Dev Biol 199:55-71.
79. Muñoz-Chápuli R, Macías D, Ramos C, Gallego A, de Andrés AV. 1996. Development of the subepicardial mesenchyme and the early cardiac vessels in the dogfish (Scyliorhinus canicula). J Exp Zool 275:95-111.
80. Muñoz-Chápuli R, Macias D, Ramos C, Fernández B, Sans-Coma V. 1997. Development of the epicardium in the dogfish (Scyliorhinus canicula). Acta Zool (Stockholm) 78:39-46.
81. Nahirney PC, Mikawa T, Fischman DA. 2003. Evidence for an extracellular matrix bridge guiding proepicardial cell migration to the myocardium of chick embryos. Dev Dyn 227:511-523.
82. Nakajima Y, Yamagishi T, Nakamura H, Markwald RR, Krug EL. 1998. An autocrine function for transforming growth factor (TGF)-beta3 in the transformation of atrioventricular canal endocardium into mesenchyme during chick heart development. Dev Biol 194: 99-113.
83. Nakajima Y, Yamagishi T, Hokari S, Nakamura H. 2000. Mechanisms involved in valvuloseptal endocardial cushion formation in early cardiogenesis: roles of transforming growth factor (TGF)-beta and bone morphogenetic protein (BMP). Anat Rec 258:119-127.
84. Niederreither K, Vermot J, Fraulob V, Chambon P, Dolle P. 2002. Retinaldehyde dehydrogenase 2 (RALDH2)-independent patterns of retinoic acid synthesis in the mouse embryo. Proc Natl Acad Sci USA 99:16111-16116.
85. Orlic D, Kajstura J, Chimenti S, Limana F, Jakoniuk I, Quaini F, Nadal-Ginard B, Bodine DM, Leri A, Anversa P. 2001. Bone marrow cells regenerate infarcted myocardium. Proc Natl Acad Sci USA 98:10344-10349.
86. Patten BM. 1968. The development of the heart. In: Gould SE, editor. Pathology of the heart and blood vessels. Springfield, IL: Thomas. p 20-90.
87. Peng I, Dennis JE, Rodríguez-Boulan E, Fischman D. 1990. Polarized release of enveloped viruses in the embryonic chicken heart: demonstration of epithelial polarity in the presumptive myocardium. Dev Biol 141:164-172.
88. Pérez-Pomares JM, Macías D, García-Garrido L, Muñoz-Chápuli R. 1997. Contribution of the primitive epicardium to the subepicardial mesenchyme in hamster and chick embryos. Dev Dyn 210:96-105.
89. Pérez-Pomares JM, Macías D, García-Garrido L, Muñoz-Chápuli R. 1998a. The origin of the subepicardial mesenchyme in the avian embryo: an immunohistochemical and quail-chimera study. Dev Biol 200:57-68.
90. Pérez-Pomares JM, Macias D, García-Garrido L, Muñoz-Chápuli R. 1998b. Immunolocalization of the vascular endothelial growth factor receptor-2 in the subepicardial mesenchyme of hamster embryos: identification of the coronary vessel precursors. Histochem J 30:627-634.
91. Pérez-Pomares JM, Muñoz-Chápuli JM. 2002. Epithelial-mesenchymal transitions: a mesodermal cell strategy for evolutive innovation in metazoans. Anat Rec 268:343-351.
92. Pérez-Pomares JM, Carmona R, González-Iriarte M, Atencia G, Wessels A, Muñoz-Chápuli R. 2002a. Origin of coronary endothelial cells from epicardial mesothelium in avian embryos. Int J Dev Biol 46:1005-1013.
93. Pérez-Pomares JM, Phelps A, Sedmerova M, Carmona R, González-Iriarte M, Muñoz-Chápuli R, Wessels A. 2002b. Experimental studies on the spatiotemporal expression of WT1 and RALDH2 in the embryonic avian heart: a model for the regulation of myocardial and valvuloseptal development by epicardially-derived cells (EPDCs). Dev Biol 247:307-326.
94. Potten CS, Loeffler M. 1990. Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons from and for the crypt. Development 110:1001-1020.
95. Potten CS. 1998. Stem cells in gastrointestinal epithelium: numbers, characteristics and death. Phil Trans Soc Lond B 353:821-830.
96. Poulsom R, Alison MR, Forbes SJ, Wright NA. 2002. Adult stem cell plasticity. J Pathol 197:441-456.
97. Quaini F, Urbanek K, Beltrami AP, Finato N, Beltrami CA, Nadal-Ginard B, Kajstura J, Leri A, Anversa P. 2002. Chimerism of the transplanted heart. N Engl J Med 346:5-15.
98. Rappolee DA, Iyer A, Patel Y. 1996. Hepatocyte growth factor and its receptor are expressed in cardiac myocytes during early cardiogenesis. Circ Res 78:1028-1036.
99. Rezaee M, Isokawa K, Halligan N, Markwald RR, Krug EL. 1993. Identification of an extracellular 130-kDa protein involved in early cardiac morphogenesis. J Biol Chem 268:14404-14411.
100. Risau W, Flamme I. 1995. Vasculogenesis. Annu Rev Cell Dev Biol 11:73-91.
101. Robb L, Lyons I, Li R, Hartley L, Köntgen F, Harvey RP, Metcalf D, Begley CG. 1995. Absence of yolk sac hematopoiesis from mice with a targeted disruption of the SCL gene. Proc Natl Acad Sci USA 92:7075-7079.
102. Romano LA, Runyan RB. 1999. Slug is a mediator of epithelial-mesenchymal cell transformation in the developing chicken heart. Dev Biol 212:243-254.
103. Romano LA, Runyan RB. 2000. Slug is an essential target of TGFbeta2 signaling in the developing chicken heart. Dev Biol 223:91-102.
104. Scharnhorst V, Kranenburg O, van der Eb AJ, Jochemsen AG. 1997. Differential regulation of the Wilms' tumor gene, WT1, during differentiation of embryonal carcinoma and embryonic stem cells. Cell Growth Differ 8:133-143.
105. Song W, Majka SM, McGuire PG. 1999. Hepatocyte growth factor expression in the developing myocardium: evidence for a role in the regulation of the mesenchymal cell phenotype and urokinase expression. Dev Dyn 214:92-100.
106. Streeter GL. 1945. Developmental horizons in human embryos: description of age group XIII, embryos about 4 or 5 millimiters long, and age group XIV, period of indentation of lens vesicle. Contrib Embryol 31:29-64.
107. Stuckmann I, Evans S, Lassar AB. 2003. Erythropoietin and retinoic acid, secreted from the epicardium, are required for cardiac myocyte proliferation. Dev Biol 255:334-349.
108. Tevosian SG, Deconinck AE, Tanaka M, Schinke M, Litovsky SH, Izumo S, Fujiwara Y, Orkin SH. 2000. FOG-2, a cofactor for GATA transcription factors, is essential for heart morphogenesis and development of the coronary vessels from epicardium. Cell 101:729-739.
109. Tidball JG. 1992. Distribution of collagens and fibronectin in the subepicardium during avian cardiac development. Anat Embryol 185:155-162.
110. Tomanek RJ, Lotun K, Clark EB, Suvarna PR, Hu N. 1998. VEGF and bFGF stimulate myocardial vascularization in embryonic chick. Am J Physiol 274(Pt 2):H1620-H1626.
111. Tomanek RJ, Ratajska A, Kitten GT, Yue X, Sandra A. 1999. Vascular endothelial growth factor expression coincides with coronary vasculogenesis and angiogenesis. Dev Dyn 215:54-61.
112. Tomanek RJ, Sandra A, Zheng W, Brock T, Bjercke RJ, Holifield JS. 2001. Vascular endothelial growth factor and basic fibroblast growth factor differentially modulate early postnatal coronary angiogenesis. Circ Res 88:1135-1141.
113. Tomanek RJ, Holifield JS, Reiter RS, Sandra A, Lin JJ. 2002. Role of VEGF family members and receptors in coronary vessel formation. Dev Dyn 225:233-240.
114. Tsuda T, Majumder K, Linask KK. 1998. Differential expression of flectin in the extracellular matrix and left-right asymmetry in mouse embryonic heart during looping stages. Dev Genet 23:203-214.
115. Tsuda T, Wang H, Timpl R, Chu ML. 2001. Fibulin-2 expression marks transformed mesenchymal cells in developing cardiac valves, aortic arch vessels, and coronary vessels. Dev Dyn 222:89-100.
116. Van den Eijnde SM, Wenink ACG, Vermeij-Keers C. 1995. Origin of subepicardial cells in rat embryos. Anat Rec 242:96-102.
117. Van den Hoff MJ, Moorman AF, Ruijter JM, Lamers WH, Bennington RW, Markwald RR, Wessels A. 1999. Myocardialization of the cardiac outflow tract. Dev Biol 212:477-490.
118. Viragh S, Challice CE. 1981. The origin of the epicardium and the embryonic myocardial circulation in the mouse. Anat Rec 201:157-168.
119. Viragh S, Kalman F, Gittenberger-de Groot AC, Poelmann RE, Moorman AFM. 1990. Angiogenesis and hematopoieis in the epicardium of the vertebrate embryo heart. In: Bockman DE, Kirby ML, editors. Embryonic origins of defective heart development. Ann NY Acad Sci 588:455-458.
120. Viragh S, Gittenberger-de Groot AC, Poelmann RE, Kalman F. 1993. Early development of quail heart epicardium and associated vascular and glandular structures. Anat Embryol 188:391-393.
121. Vokes SA, Krieg PA. 2002. Endoderm is required for vascular endothelial tube formation, but not for angioblast specification. Development 129:775-785.
122. Vrancken Peeters MP, Gittenberger-de Groot AC, Mentink MM, Hungerford JE, Little CD, Poelmann RE. 1997. The development of the coronary vessels and their differentiation into arteries and veins in the embryonic quail heart. Dev Dyn 208:338-348.
123. Vrancken Peeters MPFM, Mentink MMT, Poelmann RE, Gittenberger-de Groot AC. 1995. Cytokeratins as a marker for epicardial formation in the quail embryo. Anat Embryol 191:503-508.
124. Vrancken Peeters MPFM, Gittenberger-de Groot AC, Mentink MMT, Poelmann RE. 1999. Smooth muscle cells and fibroblasts of the coronary arteries derive from epithelial-mesenchymal transformation of the epicardium. Anat Embryol 199:367-378.
125. Wada AM, Smith TK, Osler ME, Reese DE, Bader DM. 2003. Epicardial/mesothelial cell line retains vasculogenic potential of embryonic epicardium. Circ Res 92:525-531.
126. Wagner KD, Wagner N, Bondke A, Nafz B, Flemming B, Theres H, Scholz H. 2002. The Wilms' tumor suppressor Wt1 is expressed in the coronary vasculature after myocardial infarction. FASEB J 16:1117-1119.
127. Wagner KJ, Patek CE, Miles C, Christie S, Brookes AJ, Hooper ML. 2001. Truncation of WT1 results in downregulation of cyclin G1 and IGFBP-4 expression. Biochem Biophys Res Commun 287:977-982.
128. Wessels A, Markman MW, Vermeulen JL, Anderson RH, Moorman AF, Lamers WH. 1996. The development of the atrioventricular junction in the human heart. Circ Res 78:110-117.
129. Wessels A, Markwald RR. 2000. Cardiac morphogenesis and dysmorphogenesis. I. Normal development. Methods Mol Biol 136:239-259.
130. Wu H, Lee SH, Gao J, Liu X, Iruela-Arispe ML. 1999. Inactivation of erythropoietin leads to defects in cardiac morphogenesis. Development 126:3597-3605.
131. Xavier-Neto J, Shapiro MD, Houghton L, Rosenthal N. 2000. Sequential programs of retinoic acid synthesis in the myocardial and epicardial layers of the developing avian heart. Dev Biol 219:129-141.
132. Yamagishi T, Nakajima Y, Nakamura H. 1999. Expression of TGF-beta3 RNA during chick embryogenesis: a possible important role in cardiovascular development. Cell Tissue Res 298:85-93.
133. Yamashita J, Itoh H, Hirashima M, Ogawa M, Nishikawa S, Yurugi T, Naito M, Nakao K, Nishikawa SI. 2000. Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature 408:92-96.
134. Yang JT, Rayburn H, Hynes RO. 1995. Cell adhesion events mediated by alpha 4 integrins are essential in placental and cardiac development. Development 121:549-560.
135. Yoshida K, Taga T, Saito M, Suematsu S, Kumanogoh A, Tanaka T, Fujiwara H, Hirata M, Yamagami T, Nakahata T, Hirabayashi T, Yoneda Y, Tanaka K, Wang WZ, Mori C, Shiota K, Yoshida N, Kishimoto T. 1996. Targeted disruption of gp130, a common signal transducer for the interleukin 6 family of cytokines, leads to myocardial and hematological disorders. Proc Natl Acad Sci USA 93:407-411.
136. Zheng W, Seftor EA, Meininger CJ, Hendrix MJ, Tomanek RJ.2001. Mechanisms of coronary angiogenesis in response to stretch: role of VEGF and TGF-beta. Am J Physiol Heart Circ Physiol 280:H909-H917.