New insights into the developmental mechanisms of coronary vessels and epicardium

International Review of Cell and Molecular Biology

Volumn 303, Issue , 2013, Pages 263-317

  Nakajima, Yuji ^a   Imanaka Yoshida, Kyoko ^b  

^a OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b MIE UNIVERSITY   (Japan)

Author keywords

Coronary vessel development; Epicardium; Growth factors; Proepicardial organ

Indexed keywords

ANGIOPOIETIN 1; ANGIOPOIETIN RECEPTOR; BETA CATENIN; BONE MORPHOGENETIC PROTEIN; FIBROBLAST GROWTH FACTOR; NOTCH RECEPTOR; PLATELET DERIVED GROWTH FACTOR; RETINOIC ACID; SONIC HEDGEHOG PROTEIN; THYMOSIN BETA4; TRANSFORMING GROWTH FACTOR BETA; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN; WILM TUMOR SUPPRESSOR PROTEIN 1; WNT PROTEIN;

ANATOMICAL VARIATION; ANGIOGENESIS; ARTICLE; BLOOD VESSEL WALL; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; CELL PROLIFERATION; CORONARY ARTERY; CORONARY ARTERY ANOMALY; CORONARY BLOOD VESSEL; CORONARY ENDOTHELIAL CELL; CORONARY PLEXUS; CORONARY VEIN; ENDOTHELIUM CELL; EPICARDIUM; EPITHELIAL MESENCHYMAL TRANSITION; HEART; HEART DEVELOPMENT; HEART FUNCTION; HEART MUSCLE; HISTOPATHOLOGY; HUMAN; MESENCHYME; MORPHOGENESIS; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROEPICARDIAL ORGAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ZEBRA FISH;

EID: 84874236612     PISSN: 19376448     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-407697-6.00007-6     Document Type: Chapter

References (280)

1. Abramsson A., Kurup S., Busse M., Yamada S., Lindblom P., Schallmeiner E., Stenzel D., Sauvaget D., Ledin J., Ringvall M., Landegren U., Kjellen L., Bondjers G., Li J.P., Lindahl U., Spillmann D., Betsholtz C., Gerhardt H. Defective N-sulfation of heparan sulfate proteoglycans limits PDGF-BB binding and pericyte recruitment in vascular development. Genes. Dev. 2007, 21:316-331.
2. Abu-Issa R., Kirby M.L. Patterning of the heart field in the chick. Dev. Biol. 2008, 319:223-233.
3. Acloque H., Adams M.S., Fishwick K., Bronner-Fraser M., Nieto M.A. Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease. J. Clin. Invest. 2009, 119:1438-1449.
4. Adams R.H., Wilkinson G.A., Weiss C., Diella F., Gale N.W., Deutsch U., Risau W., Klein R. Roles of ephrinB ligands and EphB receptors in cardiovascular development: demarcation of arterial/venous domains, vascular morphogenesis, and sprouting angiogenesis. Genes. Dev. 1999, 13:295-306.
5. Aisagbonhi O., Rai M., Ryzhov S., Atria N., Feoktistov I., Hatzopoulos A.K. Experimental myocardial infarction triggers canonical Wnt signaling and endothelial-to-mesenchymal transition. Dis. Model. Mech. 2011, 4:469-483.
6. Ando K., Nakajima Y., Yamagishi T., Yamamoto S., Nakamura H. Development of proximal coronary arteries in quail embryonic heart: multiple capillaries penetrating the aortic sinus fuse to form main coronary trunk. Circ. Res. 2004, 94:346-352.
7. Ando K., Takahashi M., Yamagishi T., Miyagawa-Tomita S., Imanaka-Yoshida K., Yoshida T., Nakajima Y. Tenascin C may regulate the recruitment of smooth muscle cells during coronary artery development. Differentiation 2011, 81:299-306.
8. Andrae J., Gallini R., Betsholtz C. Role of platelet-derived growth factors in physiology and medicine. Genes. Dev. 2008, 22:1276-1312.
9. Armulik A., Genove G., Mae M., Nisancioglu M.H., Wallgard E., Niaudet C., He L., Norlin J., Lindblom P., Strittmatter K., Johansson B.R., Betsholtz C. Pericytes regulate the blood-brain barrier. Nature 2010, 468:557-561.
10. Armulik A., Genove G., Betsholtz C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev. Cell 2011, 21:193-215.
11. Austin A.F., Compton L.A., Love J.D., Brown C.B., Barnett J.V. Primary and immortalized mouse epicardial cells undergo differentiation in response to TGFbeta. Dev. Dyn. 2008, 237:366-376.
12. Banerjee I., Zhang J., Moore-Morris T., Lange S., Shen T., Dalton N.D., Gu Y., Peterson K.L., Evans S.M., Chen J. Thymosin beta 4 is dispensable for murine cardiac development and function. Circ. Res. 2012, 110:456-464.
13. Begemann G., Gibert Y., Meyer A., Ingham P.W., et al. Cloning of zebrafish T-box genes tbx15 and tbx18 and their expression during embryonic development. Mech. Dev. 2002, 114:137-141.
14. Benedito R., Roca C., Sorensen I., Adams S., Gossler A., Fruttiger M., Adams R.H. The Notch ligands Dll4 and jagged1 have opposing effects on angiogenesis. Cell 2009, 137:1124-1135.
15. Bjarnegard M., Enge M., Norlin J., Gustafsdottir S., Fredriksson S., Abramsson A., Takemoto M., Gustafsson E., Fassler R., Betsholtz C. Endothelium-specific ablation of PDGFB leads to pericyte loss and glomerular, cardiac and placental abnormalities. Development 2004, 131:1847-1857.
16. Bock-Marquette I., Shrivastava S., Pipes G.C., Thatcher J.E., Blystone A., Shelton J.M., Galindo C.L., Melegh B., Srivastava D., Olson E.N., DiMaio J.M. Thymosin beta4 mediated PKC activation is essential to initiate the embryonic coronary developmental program and epicardial progenitor cell activation in adult mice in vivo. J. Mol. Cell Cardiol. 2009, 46:728-738.
17. Brand T. Heart development: molecular insights into cardiac specification and early morphogenesis. Dev. Biol. 2003, 258:1-19.
18. Buckingham M., Meilhac S., Zaffran S. Building the mammalian heart from two sources of myocardial cells. Nat. Rev. Genet. 2005, 6:826-835.
19. Cai C.L., Martin J.C., Sun Y., Cui L., Wang L., Ouyang K., Yang L.BuL., Liang X., Zhang X., Stallcup W.B., Denton C.P., McCulloch A., Chen J., Evans S.M. A myocardial lineage derives from Tbx18 epicardial cells. Nature 2008, 454:104-108.
20. Capurro M.I., Xu P., Shi W., Li F., Jia A., Filmus J. Glypican-3 inhibits hedgehog signaling during development by competing with patched for hedgehog binding. Dev. Cell 2008, 14:700-711.
21. Carmeliet P., Ferreira V., Breier G., Pollefeyt S., Kieckens L., Gertsenstein M., Fahrig M., Vandenhoeck A., Harpal K., Eberhardt C., Declercq C., Pawling J., Moons L., Collen D., Risau W., Nagy A. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996, 380:435-439.
22. Chen S., Kulik M., Lechleider R.J. Smad proteins regulate transcriptional induction of the SM22alpha gene by TGF-beta. Nucleic Acids Res. 2003, 31:1302-1310.
23. Cheng Z., Sundberg-Smith L.J., Mangiante L.E., Sayers R.L., Hakim Z.S., Musunuri S., Maguire C.T., Majesky M.W., Zhou Z., Mack C.P., Taylor J.M. Focal adhesion kinase regulates smooth muscle cell recruitment to the developing vasculature. Arterioscler. Thromb. Vasc. Biol. 2011, 31:2193-2202.
24. Choi K., Kennedy M., Kazarov A., Papadimitriou J.C., Keller G. A common precursor for hematopoietic and endothelial cells. Development 1998, 125:725-732.
25. Clauss S.B., Walker D.L., Kirby M.L., Schimel D., Lo C.W. Patterning of coronary arteries in wildtype and connexin43 knockout mice. Dev. Dyn. 2006, 235:2786-2794.
26. Compton L.A., Potash D.A., Mundell N.A., Barnett J.V. Transforming growth factor-beta induces loss of epithelial character and smooth muscle cell differentiation in epicardial cells. Dev. Dyn. 2006, 235:82-93.
27. Craig E.A., Austin A.F., Vaillancourt R.R., Barnett J.V., Camenisch T.D. TGFbeta2-mediated production of hyaluronan is important for the induction of epicardial cell differentiation and invasion. Exp. Cell Res. 2010, 316:3397-3405.
28. Davis S., Aldrich T.H., Jones P.F., Acheson A., Compton D.L., Jain V., Ryan T.E., Bruno J., Radziejewski C., Maisonpierre P.C., Yancopoulos G.D. Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning. Cell 1996, 87:1161-1169.
29. De Cat B., Muyldermans S.Y., Coomans C., Degeest G., Vanderschueren B., Creemers J., Biemar F., Peers B., David G. Processing by proprotein convertases is required for glypican-3 modulation of cell survival, Wnt signaling, and gastrulation movements. J. Cell Biol. 2003, 163:625-635.
30. de la Pompa J.L., Epstein J.A. Coordinating tissue interactions: Notch signaling in cardiac development and disease. Dev. Cell 2012, 22:244-254.
31. del Monte G., Casanova J.C., Guadix J.A., MacGrogan D., Burch J.B., Perez-Pomares J.M., de la Pompa J.L. Differential Notch signaling in the epicardium is required for cardiac inflow development and coronary vessel morphogenesis. Circ. Res. 2011, 108:824-836.
32. Dettman R.W., Denetclaw W., Ordahl C.P., Bristow J. Common epicardial origin of coronary vascular smooth muscle, perivascular fibroblasts, and intermyocardial fibroblasts in the avian heart. Dev. Biol. 1998, 193:169-181.
33. Domenga V., Fardoux P., Lacombe P., Monet M., Maciazek J., Krebs L.T., Klonjkowski B., Berrou E., Mericskay M., Li Z., Tournier-Lasserve E., Gridley T., Joutel A. Notch3 is required for arterial identity and maturation of vascular smooth muscle cells. Genes Dev. 2004, 2730-2735. United States.
34. Duan J., Gherghe C., Liu D., Hamlett E., Srikantha L., Rodgers L., Regan J.N., Rojas M., Willis M., Leask A., Majesky M., Deb A. Wnt1/betacatenin injury response activates the epicardium and cardiac fibroblasts to promote cardiac repair. EMBO J. 2012, 31:429-442.
35. Duarte A., Hirashima M., Benedito R., Trindade A., Diniz P., Bekman E., Costa L., Henrique D., Rossant J. Dosage-sensitive requirement for mouse Dll4 in artery development. Genes. Dev. 2004, 18:2474-2478.
36. Dumont D.J., Yamaguchi T.P., Conlon R.A., Rossant J., Breitman M.L. tek, a novel tyrosine kinase gene located on mouse chromosome 4, is expressed in endothelial cells and their presumptive precursors. Oncogene 1992, 7:1471-1480.
37. Dumont D.J., Jussila L., Taipale J., Lymboussaki A., Mustonen T., Pajusola K., Breitman M., Alitalo K. Cardiovascular failure in mouse embryos deficient in VEGF receptor-3. Science 1998, 282:946-949.
38. Enge M., Bjarnegard M., Gerhardt H., Gustafsson E., Kalen M., Asker N., Hammes H.P., Shani M., Fassler R., Betsholtz C. Endothelium-specific platelet-derived growth factor-B ablation mimics diabetic retinopathy. EMBO J. 2002, 21:4307-4316.
39. Feng X., Krebs L.T., Gridley T. Patent ductus arteriosus in mice with smooth muscle-specific Jag1 deletion. Development 2010, 137:4191-4199.
40. Ferrara N., Carver-Moore K., Chen H., Dowd M., Lu L., O'Shea K.S., Powell-Braxton L., Hillan K.J., Moore M.W. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 1996, 380:439-442.
41. Fong G.H., Rossant J., Gertsenstein M., Breitman M.L. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 1995, 376:66-70.
42. Gaengel K., Genove G., Armulik A., Betsholtz C. Endothelial-mural cell signaling in vascular development and angiogenesis. Arterioscler. Thromb. Vasc. Biol. 2009, 29:630-638.
43. Gaur P., Bielenberg D.R., Samuel S., Bose D., Zhou Y., Gray M.J., Dallas N.A., Fan F., Xia L., Lu J., Ellis L.M. Role of class 3 semaphorins and their receptors in tumor growth and angiogenesis. Clin. Cancer Res. 2009, 15:6763-6770.
44. Gerety S.S., Wang H.U., Chen Z.F., Anderson D.J. Symmetrical mutant phenotypes of the receptor EphB4 and its specific transmembrane ligand ephrin-B2 in cardiovascular development. Mol. Cell 1999, 4:403-414.
45. Gerety S.S., Anderson D.J. Cardiovascular ephrinB2 function is essential for embryonic angiogenesis. Development 2002, 129:1397-1410.
46. Gerhardt H., Betsholtz C. Endothelial-pericyte interactions in angiogenesis. Cell Tissue Res. 2003, 314:15-23.
47. Gerhardt H., Golding M., Fruttiger M., Ruhrberg C., Lundkvist A., Abramsson A., Jeltsch M., Mitchell C., Alitalo K., Shima D., Betsholtz C. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 2003, 161:1163-1177.
48. Gittenberger-de Groot A.C., Mahtab E.A., Hahurij N.D., Wisse L.J., Deruiter M.C., Wijffels M.C., Poelmann R.E. 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.
49. Gonzalez-Rosa J.M., Martin V., Peralta M., Torres M., Mercader N. Extensive scar formation and regression during heart regeneration after cryoinjury in zebrafish. Development 2011, 138:1663-1674.
50. Goumans M.J., Valdimarsdottir G., Itoh S., Lebrin F., Larsson J., Mummery C., Karlsson S., ten Dijke P. Activin receptor-like kinase (ALK)1 is an antagonistic mediator of lateral TGFbeta/ALK5 signaling. Mol. Cell 2003, 12:817-828.
51. Goumans M.J., Valdimarsdottir G., Itoh S., Rosendahl A., Sideras P., ten Dijke P. Balancing the activation state of the endothelium via two distinct TGF-beta type I receptors. EMBO J. 2002, 21:1743-1753.
52. Gu C., Rodriguez E.R., Reimert D.V., Shu T., Fritzsch B., Richards L.J., Kolodkin A.L., Ginty D.D. Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development. Dev. Cell 2003, 5:45-57.
53. Guadix J.A., Carmona R., Munoz-Chapuli R., Perez-Pomares J.M. In vivo and in vitro analysis of the vasculogenic potential of avian proepicardial and epicardial cells. Dev. Dyn. 2006, 235:1014-1026.
54. Guadix J.A., Ruiz-Villalba A., Lettice L., Velecela V., Munoz-Chapuli R., Hastie N.D., Perez-Pomares J.M., Martinez-Estrada O.M. Wt1 controls retinoic acid signalling in embryonic epicardium through transcriptional activation of Raldh2. Development 2011, 138:1093-1097.
55. Gray R.S., Roszko I., Solnica-Krezel L. Planar cell polarity: coordinating morphogenetic cell behaviors with embryonic polarity. Dev. Cell 2011, 21:120-133.
56. Gridley T. Notch signaling in the vasculature. Curr. Top. Dev. Biol. 2010, 92:277-309.
57. Grieskamp T., Rudat C., Ludtke T.H., Norden J., Kispert A. Notch signaling regulates smooth muscle differentiation of epicardium-derived cells. Circ. Res. 2011, 108:813-823.
58. Grisaru S., Cano-Gauci D., Tee J., Filmus J., Rosenblum N.D. Glypican-3 modulates BMP- and FGF-mediated effects during renal branching morphogenesis. Dev. Biol. 2001, 231:31-46.
59. Haenig B., Kispert A. Analysis of TBX18 expression in chick embryos. Dev. Genes. Evil 2004, 214:407-411.
60. Hayashi H., Kume T. Foxc transcription factors directly regulate Dll4 and Hey2 expression by interacting with the VEGF-Notch signaling pathways in endothelial cells. PLoS One 2008, 3:e2401.
61. Hellstrom M., Kalen M., Lindahl P., Abramsson A., Betsholtz C. Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 1999, 126:3047-3055.
62. Hellstrom M., Phng L.K., Hofmann J.J., Wallgard E., Coultas L., Lindblom P., Alva J., Nilsson A.K., Karlsson L., Gaiano N., Yoon K., Rossant J., Iruela-Arispe M.L., Kalen M., Gerhardt H., Betsholtz C. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 2007, 445:776-780.
63. Hidaka M., Stanford W.L., Bernstein A. Conditional requirement for the Flk-1 receptor in the in vitro generation of early hematopoietic cells. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:7370-7375.
64. High F.A., Zhang M., Proweller A., Tu L., Parmacek M.S., Pear W.S., Epstein J.A. An essential role for Notch in neural crest during cardiovascular development and smooth muscle differentiation. J. Clin. Invest. 2007, 117:353-363.
65. High F.A., Epstein J.A. The multifaceted role of Notch in cardiac development and disease. Nat. Rev. Genet. 2008, 9:49-61.
66. Hill C.R., Sanchez N.S., Love J.D., Arrieta J.A., Hong C.C., Brown C.B., Austin A.F., Barnett J.V. BMP2 signals loss of epithelial character in epicardial cells but requires the type III TGFbeta receptor to promote invasion. Cell Signal. 2012, 24:1012-1022.
67. Hirashima M. Regulation of endothelial cell differentiation and arterial specification by VEGF and Notch signaling. Anat. Sci. Int. 2009, 84:95-101.
68. Hiratsuka S., Minowa O., Kuno J., Noda T., Shibuya M. Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice. Proc. Natl. Acad. Sci. U. S. A 1998, 95:9349-9354.
69. Hirose T., Karasawa M., Sugitani Y., Fujisawa M., Akimoto K., Ohno S., Noda T. PAR3 is essential for cyst-mediated epicardial development by establishing apical cortical domains. Development 2006, 133:1389-1398.
70. Hirschi K.K., Burt J.M., Hirschi K.D., Dai C. Gap junction communication mediates transforming growth factor-beta activation and endothelial-induced mural cell differentiation. Circ. Res. 2003, 93:429-437.
71. Hiruma T., Hirakow R. Epicardial formation in embryonic chick heart: computer-aided reconstruction, scanning, and transmission electron microscopic studies. Am. J. Anat. 1989, 184:129-138.
72. Hoglund V.J., Majesky M.W. Patterning the artery wall by lateral induction of Notch signaling. Circulation 2012, 125:212-215.
73. Hoover L.L., Burton E.G., Brooks B.A., Kubalak S.W. The expanding role for retinoid signaling in heart development. ScientificWorldJournal 2008, 8:194-211.
74. Houck K.A., Leung D.W., Rowland A.M., Winer J., Ferrara N. Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms. J. Biol. Chem. 1992, 267:26031-26037.
75. Iivanainen E., Nelimarkka L., Elenius V., Heikkinen S.M., Junttila T.T., Sihombing L., Sundvall M., Maatta J.A., Laine V.J., Yla-Herttuala S., Higashiyama S., Alitalo K., Elenius K. Angiopoietin-regulated recruitment of vascular smooth muscle cells by endothelial-derived heparin binding EGF-like growth factor. FASEB J. 2003, 17:1609-1621.
76. Ishigaki T., Imanaka-Yoshida K., Shimojo N., Matsushima S., Taki W., Yoshida T. Tenascin-C enhances crosstalk signaling of integrin αvβ3/PDGFR-beta complex by SRC recruitment promoting PDGF-induced proliferation and migration in smooth muscle cells. J. Cell Physiol. 2011, 226:2617-2624.
77. Ishii Y., Langberg J.D., Hurtado R., Lee S., Mikawa T. Induction of proepicardial marker gene expression by the liver bud. Development 2007, 134:3627-3637.
78. Ishii Y., Garriock R.J., Navetta A.M., Coughlin L.E., Mikawa T. BMP signals promote proepicardial protrusion necessary for recruitment of coronary vessel and epicardial progenitors to the heart. Dev. Cell 2010, 19:307-316.
79. Jeansson M., Gawlik A., Anderson G., Li C., Kerjaschki D., Henkelman M., Quaggin S.E. Angiopoietin-1 is essential in mouse vasculature during development and in response to injury. J. Clin. Invest. 2011, 121:2278-2289.
80. Kalluri R., Weinberg R.A. The basics of epithelial-mesenchymal transition. J. Clin. Invest. 2009, 119:1420-1428.
81. Kamei M., Saunders W.B., Bayless K.J., Dye L., Davis G.E., Weinstein B.M. Endothelial tubes assemble from intracellular vacuoles in vivo. Nature 2006, 442:453-456.
82. Kanda S., Mochizuki Y., Suematsu T., Miyata Y., Nomata K., Kanetake H. Sonic hedgehog induces capillary morphogenesis by endothelial cells through phosphoinositide 3-kinase. J. Biol. Chem. 2003, 278:8244-8249.
83. Kattan J., Dettman R.W., Bristow J. Formation and remodeling of the coronary vascular bed in the embryonic avian heart. Dev. Dyn. 2004, 230:34-43.
84. Katz T.C., Singh M.K., Degenhardt K., Rivera-Feliciano J., Johnson R.L., Epstein J.A., Tabin C.J. Distinct compartments of the proepicardial organ give rise to coronary vascular endothelial cells. Dev. Cell 2012, 22:639-650.
85. Kim J., Wu Q., Zhang Y., Wiens K.M., Huang Y., Rubin N., Shimada H., Handin R.I., Chao M.Y., Tuan T.L., Starnes V.A., Lien C.L. PDGF signaling is required for epicardial function and blood vessel formation in regenerating zebrafish hearts. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:17206-17210.
86. Kirschner K.M., Wagner N., Wagner K.D., Wellmann S., Scholz H. The Wilms tumor suppressor Wt1 promotes cell adhesion through transcriptional activation of the alpha4integrin gene. J. Biol. Chem. 2006, 281:31930-31939.
87. Komiyama M., Ito K., Shimada Y. Origin and development of the epicardium in the mouse embryo. Anat. Embryol. 1987, 176:183-189.
88. Kovacic J.C., Mercader N., Torres M., Boehm M., Fuster V. Epithelial-to-mesenchymal and endothelial-to-mesenchymal transition: from cardiovascular development to disease. Circulation 2012, 125:1795-1808.
89. Krebs L.T., Shutter J.R., Tanigaki K., Honjo T., Stark K.L., Gridley T. Haploinsufficient lethality and formation of arteriovenous malformations in Notch pathway mutants. Genes. Dev. 2004, 18:2469-2473.
90. Kruger O., Plum A., Kim J.S., Winterhager E., Maxeiner S., Hallas G., Kirchhoff S., Traub O., Lamers W.H., Willecke K. Defective vascular development in connexin 45-deficient mice. Development 2000, 127:4179-4193.
91. Kruithof B.P., van Wijk B., Somi S., Kruithof-de Julio M., Perez Pomares J.M., Weesie F., Wessels A., Moorman A.F., van den Hoff M.J. BMP and FGF regulate the differentiation of multipotential pericardial mesoderm into the myocardial or epicardial lineage. Dev. Biol. 2006, 295:507-522.
92. Kuhn H.J., Liebherr G. The early development of the epicardium in Tupaia belangeri. Anat. Embryol. 1988, 177:225-234.
93. Kukk E., Lymboussaki A., Taira S., Kaipainen A., Jeltsch M., Joukov V., Alitalo K. VEGF-C receptor binding and pattern of expression with VEGFR-3 suggests a role in lymphatic vascular development. Development 1996, 122:3829-3837.
94. Kume T. Specification of arterial, venous, and lymphatic endothelial cells during embryonic development. Histol. Histopathol. 2010, 25:637-646.
95. Kwee L., Baldwin H.S., Shen H.M., Stewart C.L., Buck C., Buck C.A., Labow M.A. Defective development of the embryonic and extraembryonic circulatory systems in vascular cell adhesion molecule (VCAM-1) deficient mice. Development 1995, 121:489-503.
96. Landerholm T.E., Dong X.R., Lu J., Belaguli N.S., Schwartz R.J., Majesky M.W. A role for serum response factor in coronary smooth muscle differentiation from proepicardial cells. Development 1999, 126:2053-2062.
97. Lanner F., Sohl M., Farnebo F. Functional arterial and venous fate is determined by graded VEGF signaling and Notch status during embryonic stem cell differentiation. Arterioscler. Thromb. Vasc. Biol. 2007, 27:487-493.
98. Lawson N.D., Scheer N., Pham V.N., Kim C.H., Chitnis A.B., Campos-Ortega J.A., Weinstein B.M. Notch signaling is required for arterial-venous differentiation during embryonic vascular development. Development 2001, 128:3675-3683.
99. Lawson N.D., Vogel A.M., Weinstein B.M. Sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation. Dev. Cell 2002, 3:127-136.
100. Lavine K.J., Yu K., White A.C., Zhang X., Smith C., Partanen J., Ornitz D.M. Endocardial and epicardial derived FGF signals regulate myocardial proliferation and differentiation in vivo. Dev. Cell 2005, 8:85-95.
101. Lavine K.J., White A.C., Park C., Smith C.S., Choi K., Long F., Hui C.C., Ornitz D.M. Fibroblast growth factor signals regulate a wave of hedgehog activation that is essential for coronary vascular development. Genes. Dev. 2006, 20:1651-1666.
102. Lavine K.J., Long F., Choi K., Smith C., Ornitz D.M. Hedgehog signaling to distinct cell types differentially regulates coronary artery and vein development. Development 2008, 135:3161-3171.
103. le Noble F., Moyon D., Pardanaud L., Yuan L., Djonov V., Matthijsen R., Breant C., Fleury V., Eichmann A. Flow regulates arterial-venous differentiation in the chick embryo yolk sac. Development 2004, 131:361-375.
104. Lepilina A., Coon A.N., Kikuchi K., Holdway J.E., Roberts R.W., Burns C.G., Poss K.D. A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell 2006, 127:607-619.
105. Leveen P., Pekny M., Gebre-Medhin S., Swolin B., Larsson E., Betsholtz C. Mice deficient for PDGF B show renal, cardiovascular, and hematological abnormalities. Genes. Dev. 1994, 8:1875-1887.
106. Li W.E., Waldo K., Linask K.L., Chen T., Wessels A., Parmacek M.S., Kirby M.L., Lo C.W. An essential role for connexin43 gap junctions in mouse coronary artery development. Development 2002, 129:2031-2042.
107. Limana F., Zacheo A., Mocini D., Mangoni A., Borsellino G., Diamantini A., De Mori R., Battistini L., Vigna E., Santini M., Loiaconi V., Pompilio G., Germani A., Capogrossi M.C. Identification of myocardial and vascular precursor cells in human and mouse epicardium. Circ. Res. 2007, 101:1255-1265.
108. Limbourg A., Ploom M., Elligsen D., Sorensen I., Ziegelhoeffer T., Gossler A., Drexler H., Limbourg F.P. Notch ligand delta-like 1 is essential for postnatal arteriogenesis. Circ. Res. 2007, 100:363-371.
109. Lin S.C., Dolle P., Ryckebusch L., Noseda M., Zaffran S., Schneider M.D., Niederreither K. Endogenous retinoic acid regulates cardiac progenitor differentiation. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:9234-9239.
110. Lindahl P., Johansson B.R., Leveen P., Betsholtz C. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 1997, 277:242-245.
111. Lindblom P., Gerhardt H., Liebner S., Abramsson A., Enge M., Hellstrom M., Backstrom G., Fredriksson S., Landegren U., Nystrom H.C., Bergstrom G., Dejana E., Ostman A., Lindahl P., Betsholtz C. Endothelial PDGF-B retention is required for proper investment of pericytes in the microvessel wall. Genes. Dev. 2003, 17:1835-1840.
112. Liu H., Kennard S., Lilly B. NOTCH3 expression is induced in mural cells through an autoregulatory loop that requires endothelial-expressed JAGGED1. Circ. Res. 2009, 104:466-475.
113. Liu J., Stainier D.Y. Tbx5 and Bmp signaling are essential for proepicardium specification in zebrafish. Circ. Res. 2010, 106:1818-1828.
114. Liu W., Parikh A.A., Stoeltzing O., Fan F., McCarty M.F., Wey J., Hicklin D.J., Ellis L.M. Upregulation of neuropilin-1 by basic fibroblast growth factor enhances vascular smooth muscle cell migration in response to VEGF. Cytokine 2005, 32:206-212.
115. Lobov I.B., Renard R.A., Papadopoulos N., Gale N.W., Thurston G., Yancopoulos G.D., Wiegand S.J. Delta-like ligand 4 (Dll4) is induced by VEGF as a negative regulator of angiogenic sprouting. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:3219-3224.
116. Lu J., Landerholm T.E., Wei J.S., Dong X.R., Wu S.P., Liu X., Nagata K., Inagaki M., Majesky M.W. Coronary smooth muscle differentiation from proepicardial cells requires rhoA-mediated actin reorganization and p160 rho-kinase activity. Dev. Biol. 2001, 240:404-418.
117. Majesky M.W. Developmental basis of vascular smooth muscle diversity. Arterioscler. Thromb. Vasc. Biol. 2007, 27:1248-1258.
118. Majesky M.W., Dong X.R., Hoglund V., Mahoney W.M., Daum G. The adventitia: a dynamic interface containing resident progenitor cells. Arterioscler. Thromb. Vasc. Biol. 2011, 31:1530-1539.
119. Majesky M.W., Dong X.R., Regan J.N., Hoglund V.J. Vascular smooth muscle progenitor cells: building and repairing blood vessels. Circ. Res. 2011, 108:365-377.
120. Manderfield L.J., High F.A., Engleka K.A., Liu F., Li L., Rentschler S., Epstein J.A. Notch activation of Jagged1 contributes to the assembly of the arterial wall. Circulation 2012, 125:314-323.
121. Männer J., Pérez-Pomares J.M., Macias D., Muñoz-Chápuli R. The origin, formation and developmental significance of the epicardium: a review. Cells Tissues Organs 2001, 169:89-103.
122. Massague J. Integration of Smad and MAPK pathways: a link and a linker revisited. Genes. Dev. 2003, 17:2993-2997.
123. Martin P., Lewis J. Origins of the neurovascular bundle: interactions between developing nerves and blood vessels in embryonic chick skin. Int. J. Dev. Biol. 1989, 33:379-387.
124. Martinez-Estrada O.M., Lettice L.A., Essafi A., Guadix J.A., Slight J., Velecela V., Hall E., Reichmann J., Devenney P.S., Hohenstein P., Hosen N., Hill R.E., Munoz-Chapuli R., Hastie N.D. Wt1 is required for cardiovascular progenitor cell formation through transcriptional control of Snail and E-cadherin. Nat. Genet. 2010, 42:89-93.
125. Matsui H., Sakabe M., Sakata H., Yanagawa N., Ikeda K., Yamagishi T., Nakajima Y. Induction of initial heart alpha-actin, smooth muscle alpha-actin, in chick pregastrula epiblast: the role of hypoblast and fibroblast growth factor-8. Dev. Growth Differ. 2008, 50:143-157.
126. Masumura T., Yamamoto K., Shimizu N., Obi S., Ando J. Shear stress increases expression of the arterial endothelial marker ephrinB2 in murine ES cells via the VEGF-Notch signaling pathways. Arterioscler. Thromb. Vasc. Biol. 2009, 29:2125-2131.
127. Merki E., Zamora M., Raya A., Kawakami Y., Wang J., Zhang X., Burch J., Kubalak S.W., Kaliman P., Izpisua Belmonte J.C., Chien K.R., Ruiz-Lozano P. Epicardial retinoid X receptor alpha is required for myocardial growth and coronary artery formation. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:18455-18460.
128. Mikawa T., Fischman D.A. Retroviral analysis of cardiac morphogenesis: discontinuous formation of coronary vessels. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:9504-9508.
129. Mikawa T., Gourdie R.G. Pericardial mesoderm generates a population of coronary smooth muscle cells migrating into the heart along with ingrowth of the epicardial organ. Dev. Biol. 1996, 174:221-232.
130. Millauer B., Wizigmann-Voos S., Schnurch H., Martinez R., Moller N.P., Risau W., Ullrich A. High affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell 1993, 72:835-846.
131. Miquerol L., Langille B.L., Nagy A. Embryonic development is disrupted by modest increases in vascular endothelial growth factor gene expression. Development 2000, 127:3941-3946.
132. Mommersteeg M.T., Dominguez J.N., Wiese C., Norden J., de Gier-de Vries C., Burch J.B., Kispert A., Brown N.A., Moorman A.F., Christoffels V.M. The sinus venosus progenitors separate and diversify from the first and second heart fields early in development. Cardiovasc. Res. 2010, 87:92-101.
133. Morabito C.J., Dettman R.W., Kattan J., Collier J.M., Bristow J. Positive and negative regulation of epicardial-mesenchymal transformation during avian heart development. Dev. Biol. 2001, 234:204-215.
134. Mu H., Ohashi R., Lin P., Yao Q., Chen C. Cellular and molecular mechanisms of coronary vessel development. Vasc. Med. 2005, 10:37-44.
135. Mukouyama Y.S., Shin D., Britsch S., Taniguchi M., Anderson D.J. Sensory nerves determine the pattern of arterial differentiation and blood vessel branching in the skin. Cell 2002, 109:693-705.
136. Mukouyama Y.S., Gerber H.P., Ferrara N., Gu C., Anderson D.J. Peripheral nerve-derived VEGF promotes arterial differentiation via neuropilin 1-mediated positive feedback. Development 2005, 132:941-952.
137. Moyon D., Pardanaud L., Yuan L., Breant C., Eichmann A. Plasticity of endothelial cells during arterial-venous differentiation in the avian embryo. Development 2001, 128:3359-3370.
138. Nahirney P.C., Mikawa T., Fischman D.A. Evidence for an extracellular matrix bridge guiding proepicardial cell migration to the myocardium of chick embryos. Dev. Dyn. 2003, 227:511-523.
139. Nakajima Y., Yamagishi T., Ando K., Nakamura H. Significance of bone morphogenetic protein-4 function in the initial myofibrillogenesis of chick cardiogenesis. Dev. Biol. 2002, 245:291-303.
140. Nakajima Y., Sakabe M., Matsui H., Sakata H., Yanagawa N., Yamagishi T. Significance of bone morphogenetic protein-4 function in the initial myofibrillogenesis of chick cardiogenesis. Anat. Sci. Int. 2009, 84:67-76.
141. Nakajima Y. Second lineage of heart forming region provides new understanding of conotruncal heart defects. Cong. Anom. 2010, 50:8-14.
142. Nesbitt T., Lemley A., Davis J., Yost M.J., Goodwin R.L., Potts J.D. Epicardial development in the rat: a new perspective. Microsc. Microanal. 2006, 12:390-398.
143. Ng A., Wong M., Viviano B., Erlich J.M., Alba G., Pflederer C., Jay P.Y., Saunders S. Loss of glypican-3 function causes growth factor-dependent defects in cardiac and coronary vascular development. Dev. Biol. 2009, 335:208-215.
144. Niederreither K., Subbarayan V., Dolle P., Chambon P. Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat. Genet. 1999, 21:444-448.
145. Nicoli S., Knyphausen C.P., Zhu L.J., Lakshmanan A., Lawson N.D. miR-221 is required for endothelial tip cell behaviors during vascular development. Dev. Cell 2012, 22:418-429.
146. Nishikawa S.I., Nishikawa S., Hirashima M., Matsuyoshi N., Kodama H. Progressive lineage analysis by cell sorting and culture identifies FLK1+VE-cadherin+ cells at a diverging point of endothelial and hemopoietic lineages. Development 1998, 125:1747-1757.
147. Ohno S. Intercellular junctions and cellular polarity: the PAR-aPKC complex, a conserved core cassette playing fundamental roles in cell polarity. Curr. Opin. Cell Biol. 2001, 13:641-648.
148. Olivey H.E., Svensson E.C. Epicardial-myocardial signaling directing coronary vasculogenesis. Circ. Res. 2010, 106:818-832.
149. Orr-Urtreger A., Bedford M.T., Do M.S., Eisenbach L., Lonai P. Developmental expression of the alpha receptor for platelet-derived growth factor, which is deleted in the embryonic lethal Patch mutation. Development 1992, 115:289-303.
150. Ota T., Fujii M., Sugizaki T., Ishii M., Miyazawa K., Aburatani H., Miyazono K. Targets of transcriptional regulation by two distinct type I receptors for transforming growth factor-beta in human umbilical vein endothelial cells. J. Cell Physiol. 2002, 193:299-318.
151. Pae S.H., Dokic D., Dettman R.W. Communication between integrin receptors facilitates epicardial cell adhesion and matrix organization. Dev. Dyn. 2008, 237:962-978.
152. Paine-Saunders S., Viviano B.L., Zupicich J., Skarnes W.C., Saunders S. Glypican-3 controls cellular responses to Bmp4 in limb patterning and skeletal development. Dev. Biol. 2000, 225:179-187.
153. Parker M.W., Xu P., Li X., Vander Kooi C.W. Structural basis for selective vascular endothelial growth factor-a (VEGF-A) binding to neuropilin-1. J. Biol. Chem. 2012, 287:11082-11089.
154. Patan S. TIE1 and TIE2 receptor tyrosine kinases inversely regulate embryonic angiogenesis by the mechanism of intussusceptive microvascular growth. Microvasc. Res. 1998, 56:1-21.
155. Patel-Hett S., D'Amore P.A. Signal transduction in vasculogenesis and developmental angiogenesis. Int. J. Dev. Biol. 2011, 55:353-363.
156. Pennisi D.J., Mikawa T. Normal patterning of the coronary capillary plexus is dependent on the correct transmural gradient of FGF expression in the myocardium. Dev. Biol. 2005, 279:378-390.
157. Pera E.M., Ikeda A., Eivers E., De Robertis E.M. Integration of IGF, FGF, and anti-BMP signals via Smad1 phosphorylation in neural induction. Genes. Dev. 2003, 17:3023-3028.
158. Perez-Pomares J.M., Macias D., Garcia-Garrido L., Munoz-Chapuli R. Contribution of the primitive epicardium to the subepicardial mesenchyme in hamster and chick embryos. Dev. Dyn. 1997, 210:96-105.
159. Perez-Pomares J.M., Macias D., Garcia-Garrido L., Munoz-Chapuli R. The origin of the subepicardial mesenchyme in the avian embryo: an immunohistochemical and quail-chick chimera study. Dev. Biol. 1998, 200:57-68.
160. Perez-Pomares J.M., Carmona R., Gonzalez-Iriarte M., Atencia G., Wessels A., Munoz-Chapuli R. Origin of coronary endothelial cells from epicardial mesothelium in avian embryos. Int. J. Dev. Biol. 2002, 46:1005-1013.
161. Perez-Pomares J.M., de la Pompa J.L. Signaling during epicardium and coronary vessel development. Circ. Res. 2011, 109:1429-1442.
162. Poelmann R.E., Gittenberger-de Groot A.C., Mentink M.M., Bokenkamp R., Hogers B. Development of the cardiac coronary vascular endothelium, studied with antiendothelial antibodies, in chicken-quail chimeras. Circ. Res. 1993, 73:559-568.
163. Pola R., Ling L.E., Silver M., Corbley M.J., Kearney M., Blake Pepinsky R., Shapiro R., Taylor F.R., Baker D.P., Asahara T., Isner J.M. The morphogen Sonic hedgehog is an indirect angiogenic agent upregulating two families of angiogenic growth factors. Nat. Med. 2001, 7:706-711.
164. Poole T.J., Coffin J.D. Vasculogenesis and angiogenesis: two distinct morphogenetic mechanisms establish embryonic vascular pattern. J. Exp. Zool. 1989, 251:224-231.
165. Purhonen S., Palm J., Rossi D., Kaskenpaa N., Rajantie I., Yla-Herttuala S., Alitalo K., Weissman I.L., Salven P. Bone marrow-derived circulating endothelial precursors do not contribute to vascular endothelium and are not needed for tumor growth. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:6620-6625.
166. Ratajska A., Ciszek B., Sowinska A. Embryonic development of coronary vasculature in rats: corrosion casting studies. Anat. Rec. A. Discov. Mol. Cell Evol. Biol. 2003, 270:109-116.
167. Ratajska A., Czarnowska E., Ciszek B. Embryonic development of the proepicardium and coronary vessels. Int. J. Dev. Biol. 2008, 52:229-236.
168. Ratajska A., Czarnowska E., Kolodzinska A., Kluzek W., Lesniak W. Vasculogenesis of the embryonic heart: origin of blood island-like structures. Anat. Rec. A. Discov. Mol. Cell Evol. Biol. 2006, 288:223-232.
169. Red-Horse K., Crawford Y., Shojaei F., Ferrara N. Endothelium-microenvironment interactions in the developing embryo and in the adult. Dev. Cell 2007, 12:181-194.
170. Red-Horse K., Ueno H., Weissman I.L., Krasnow M.A. Coronary arteries form by developmental reprogramming of venous cells. Nature 2010, 464:549-553.
171. Riley P.R., Smart N. Vascularizing the heart. Cardiovasc. Res. 2011, 91:260-268.
172. Risau W., Sariola H., Zerwes H.G., Sasse J., Ekblom P., Kemler R., Doetschman T. Vasculogenesis and angiogenesis in embryonic-stem-cell-derived embryoid bodies. Development 1988, 102:471-478.
173. Russell J.L., Goetsch S.C., Gaiano N.R., Hill J.A., Olson E.N., Schneider J.W. A dynamic Notch injury response activates epicardium and contributes to fibrosis repair. Circ. Res. 2011, 108:51-59.
174. Saharinen P., Eklund L., Miettinen J., Wirkkala R., Anisimov A., Winderlich M., Nottebaum A., Vestweber D., Deutsch U., Koh G.Y., Olsen B.R., Alitalo K. Angiopoietins assemble distinct Tie2 signalling complexes in endothelial cell-cell and cell-matrix contacts. Nat. Cell Biol. 2008, 10:527-537.
175. Sanchez N.S., Hill C.R., Love J.D., Soslow J.H., Craig E., Austin A.F., Brown C.B., Czirok A., Camenisch T.D., Barnett J.V. The cytoplasmic domain of TGFbetaR3 through its interaction with the scaffolding protein, GIPC, directs epicardial cell behavior. Dev. Biol. 2011, 358:331-343.
176. Sanchez N.S., Barnett J.V. TGFbeta and BMP-2 regulate epicardial cell invasion via TGFbetaR3 activation of the Par6/Smurf1/RhoA pathway. Cell. Signal. 2012, 24:539-548.
177. Sanchez-Soria P., Camenisch T.D. ErbB signaling in cardiac development and disease. Semin. Cell Dev. Biol. 2010, 21:929-935.
178. Sato T.N., Tozawa Y., Deutsch U., Wolburg-Buchholz K., Fujiwara Y., Gendron-Maguire M., Gridley T., Wolburg H., Risau W., Qin Y. Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature 1995, 376:70-74.
179. Sato Y., Rifkin D.B. Inhibition of endothelial cell movement by pericytes and smooth muscle cells: activation of a latent transforming growth factor-beta 1-like molecule by plasmin during co-culture. J. Cell Biol. 1989, 109:309-315.
180. Scheppke L., Murphy E.A., Zarpellon A., Hofmann J.J., Merkulova A., Shields D.J., Weis S.M., Byzova T.V., Ruggeri Z.M., Iruela-Arispe M.L., Cheresh D.A. Notch promotes vascular maturation by inducing integrin-mediated smooth muscle cell adhesion to the endothelial basement membrane. Blood 2012, 119:2149-2158.
181. Schlueter J., Manner J., Brand T. BMP is an important regulator of proepicardial identity in the chick embryo. Dev. Biol. 2006, 295:546-558.
182. Schlueter J., Brand T. A right-sided pathway involving FGF8/Snai1 controls asymmetric development of the proepicardium in the chick embryo. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:7485-7490.
183. Schroeder J.A., Jackson L.F., Lee D.C., Camenisch T.D. Form and function of developing heart valves: coordination by extracellular matrix and growth factor signaling. J. Mol. Med. (Berl) 2003, 81:392-403.
184. Schuh A.C., Faloon P., Hu Q.L., Bhimani M., Choi K. In vitro hematopoietic and endothelial potential of flk-1(-/-) embryonic stem cells and embryos. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:2159-2164.
185. Schulte I., Schlueter J., Abu-Issa R., Brand T., Männer J. Morphological and molecular left-right asymmetries in the development of the proepicardium: a comparative analysis on mouse and chick embryos. Dev. Dyn. 2007, 236:684-695.
186. Schultheiss T.M., Burch J.B., Lassar A.B. A role for bone morphogenetic proteins in the induction of cardiac myogenesis. Genes Dev. 1997, 11:451-462.
187. Seki T., Hong K.H., Oh S.P. Nonoverlapping expression patterns of ALK1 and ALK5 reveal distinct roles of each receptor in vascular development. Lab. Invest. 2006, 86:116-129.
188. Seki T., Yun J., Oh S.P. Arterial endothelium-specific activin receptor-like kinase 1 expression suggests its role in arterialization and vascular remodeling. Circ. Res. 2003, 93:682-689.
189. Sengbusch J.K., He W., Pinco K.A., Yang J.T. Dual functions of α4β1 integrin in epicardial development: initial migration and long-term attachment. J. Cell Biol. 2002, 157:873-882.
190. Seo S., Fujita H., Nakano A., Kang M., Duarte A., Kume T. The forkhead transcription factors, Foxc1 and Foxc2, are required for arterial specification and lymphatic sprouting during vascular development. Dev. Biol. 2006, 294:458-470.
191. Serluca F.C. Development of the proepicardial organ in the zebrafish. Dev. Biol. 2008, 315:18-27.
192. Shalaby F., Rossant J., Yamaguchi T.P., Gertsenstein M., Wu X.F., Breitman M.L., Schuh A.C. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 1995, 376:62-66.
193. Shalaby F., Ho J., Stanford W.L., Fischer K.D., Schuh A.C., Schwartz L., Bernstein A., Rossant J. A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell 1997, 89:981-990.
194. Shinbrot E., Peters K.G., Williams L.T. Expression of the platelet-derived growth factor beta receptor during organogenesis and tissue differentiation in the mouse embryo. Dev. Dyn. 1994, 199:169-175.
195. Smart N., Risebro C.A., Melville A.A., Moses K., Schwartz R.J., Chien K.R., Riley P.R. Thymosin beta4 induces adult epicardial progenitor mobilization and neovascularization. Nature 2007, 445:177-182.
196. Smart N., Dube K.N., Riley P.R. Coronary vessel development and insight towards neovascular therapy. Int. J. Exp. Pathol. 2009, 90:262-283.
197. Smart N., Risebro C.A., Clark J.E., Ehler E., Miquerol L., Rossdeutsch A., Marber M.S., Riley P.R. Thymosin beta4 facilitates epicardial neovascularization of the injured adult heart. Ann. N. Y. Acad. Sci. 2010, 1194:97-104.
198. Smart N., Bollini S., Dube K.N., Vieira J.M., Zhou B., Davidson S., Yellon D., Riegler J., Price A.N., Lythgoe M.F., Pu W.T., Riley P.R. De novo cardiomyocytes from within the activated adult heart after injury. Nature 2011, 474:640-644.
199. Smith C.L., Baek S.T., Sung C.Y., Tallquist M.D. Epicardial-derived cell epithelial-to-mesenchymal transition and fate specification require PDGF receptor signaling. Circ. Res. 2011, 108:e15-26.
200. Snarr B.S., Kern C.B., Wessels A. Origin and fate of cardiac mesenchyme. Dev. Dyn. 2008, 237:2804-2819.
201. Song N., Huang Y., Shi H., Yuan S., Ding Y., Song X., Fu Y., Luo Y. Overexpression of platelet-derived growth factor-BB increases tumor pericyte content via stromal-derived factor-1alpha/CXCR4 axis. Cancer Res. 2009, 69:6057-6064.
202. Somi S., Buffing A.A., Moorman A.F., Van Den Hoff M.J. Dynamic patterns of expression of BMP isoforms 2, 4, 5, 6, and 7 during chicken heart development. Anat. Rec. A Discov. Mol. Cell Evol. Biol. 2004, 279:636-651.
203. Soker S., Takashima S., Miao H.Q., Neufeld G., Klagsbrun M. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 1998, 92:735-745.
204. Sommer R.J., Hijazi Z.M., Rhodes J.F. Pathophysiology of congenital heart disease in the adult: part I: shunt lesions. Circulation 2008, 117:1090-1099.
205. Sorensen I., Adams R.H., Gossler A. DLL1-mediated Notch activation regulates endothelial identity in mouse fetal arteries. Blood 2009, 113:5680-5688.
206. Soriano P. Abnormal kidney development and hematological disorders in PDGF beta-receptor mutant mice. Genes. Dev. 1994, 8:1888-1896.
207. Sridurongrit S., Larsson J., Schwartz R., Ruiz-Lozano P., Kaartinen V. Signaling via the TGF-beta type I receptor Alk5 in heart development. Dev. Biol. 2008, 322:208-218.
208. Stalmans I., Ng Y.S., Rohan R., Fruttiger M., Bouche A., Yuce A., Fujisawa H., Hermans B., Shani M., Jansen S., Hicklin D., Anderson D.J., Gardiner T., Hammes H.P., Moons L., Dewerchin M., Collen D., Carmeliet P., D'Amore P.A. Arteriolar and venular patterning in retinas of mice selectively expressing VEGF isoforms. J. Clin. Invest. 2002, 109:327-336.
209. Stalmans I., Lambrechts D., De Smet F., Jansen S., Wang J., Maity S., Kneer P., von der Ohe M., Swillen A., Maes C., Gewillig M., Molin D.G., Hellings P., Boetel T., Haardt M., Compernolle V., Dewerchin M., Plaisance S., Vlietinck R., Emanuel B., Gittenberger-de Groot A.C., Scambler P., Morrow B., Driscol D.A., Moons L., Esguerra C.V., Carmeliet G., Behn-Krappa A., Devriendt K., Collen D., Conway S.J., Carmeliet P. VEGF: a modifier of the del22q11 (DiGeorge) syndrome?. Nat. Med. 2003, 9:173-182.
210. Stratman A.N., Schwindt A.E., Malotte K.M., Davis G.E. Endothelial-derived PDGF-BB and HB-EGF coordinately regulate pericyte recruitment during vasculogenic tube assembly and stabilization. Blood 2010, 116:4720-4730.
211. Stratman A.N., Davis M.J., Davis G.E. VEGF and FGF prime vascular tube morphogenesis and sprouting directed by hematopoietic stem cell cytokines. Blood 2011, 117:3709-3719.
212. Strilic B., Kucera T., Eglinger J., Hughes M.R., McNagny K.M., Tsukita S., Dejana E., Ferrara N., Lammert E. The molecular basis of vascular lumen formation in the developing mouse aorta. Dev. Cell 2009, 17:505-515.
213. Suchting S., Freitas C., le Noble F., Benedito R., Breant C., Duarte A., Eichmann A. The Notch ligand Delta-like 4 negatively regulates endothelial tip cell formation and vessel branching. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:3225-3230.
214. Sulpice E., Plouet J., Berge M., Allanic D., Tobelem G., Merkulova-Rainon T. Neuropilin-1 and neuropilin-2 act as coreceptors, potentiating proangiogenic activity. Blood 2008, 111:2036-2045.
215. Sundberg C., Kowanetz M., Brown L.F., Detmar M., Dvorak H.F. Stable expression of angiopoietin-1 and other markers by cultured pericytes: phenotypic similarities to a subpopulation of cells in maturing vessels during later stages of angiogenesis in vivo. Lab. Invest. 2002, 82:387-401.
216. Suri C., Jones P.F., Patan S., Bartunkova S., Maisonpierre P.C., Davis S., Sato T.N., Yancopoulos G.D. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 1996, 87:1171-1180.
217. Svensson E.C. Deciphering the signals specifying the proepicardium. Circ. Res. 2010, 106:1789-1790.
218. Swift M.R., Weinstein B.M. Arterial-venous specification during development. Circ. Res. 2009, 104:576-588.
219. Tachibana K., Jones N., Dumont D.J., Puri M.C., Bernstein A. Selective role of a distinct tyrosine residue on Tie2 in heart development and early hematopoiesis. Mol. Cell Biol. 2005, 25:4693-4702.
220. Takakura N., Yoshida H., Ogura Y., Kataoka H., Nishikawa S., Nishikawa S. PDGFR alpha expression during mouse embryogenesis: immunolocalization analyzed by whole-mount immunohistostaining using the monoclonal anti-mouse PDGFR alpha antibody APA5. J. Histochem. Cytochem. 1997, 45:883-893.
221. Takakura N. Role of intimate interactions between endothelial cells and the surrounding accessory cells in the maturation of blood vessels. J. Thromb. Haemost. 2011, 9(Suppl. 1):144-150.
222. Takashima S., Kitakaze M., Asakura M., Asanuma H., Sanada S., Tashiro F., Niwa H., Miyazaki Ji J., Hirota S., Kitamura Y., Kitsukawa T., Fujisawa H., Klagsbrun M., Hori M. Targeting of both mouse neuropilin-1 and neuropilin-2 genes severely impairs developmental yolk sac and embryonic angiogenesis. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:3657-3662.
223. Tammela T., Zarkada G., Wallgard E., Murtomaki A., Suchting S., Wirzenius M., Waltari M., Hellstrom M., Schomber T., Peltonen R., Freitas C., Duarte A., Isoniemi H., Laakkonen P., Christofori G., Yla-Herttuala S., Shibuya M., Pytowski B., Eichmann A., Betsholtz C., Alitalo K. Blocking VEGFR-3 suppresses angiogenic sprouting and vascular network formation. Nature 2008, 454:656-660.
224. Tammela T., Alitalo K. Lymphangiogenesis: molecular mechanisms and future promise. Cell 2010, 140:460-476.
225. Tammela T., Zarkada G., Nurmi H., Jakobsson L., Heinolainen K., Tvorogov D., Zheng W., Franco C.A., Murtomaki A., Aranda E., Miura N., Yla-Herttuala S., Fruttiger M., Makinen T., Eichmann A., Pollard J.W., Gerhardt H., Alitalo K. VEGFR-3 controls tip to stalk conversion at vessel fusion sites by reinforcing Notch signalling. Nat. Cell Biol. 2011, 13:1202-1213.
226. Theveniau-Ruissy M., Dandonneau M., Mesbah K., Ghez O., Mattei M.G., Miquerol L., Kelly R.G. The del22q11.2 candidate gene Tbx1 controls regional outflow tract identity and coronary artery patterning. Circ. Res. 2008, 103:142-148.
227. Thurston G., Wang Q., Baffert F., Rudge J., Papadopoulos N., Jean-Guillaume D., Wiegand S., Yancopoulos G.D., McDonald D.M. Angiopoietin 1 causes vessel enlargement, without angiogenic sprouting, during a critical developmental period. Development 2005, 132:3317-3326.
228. Tian Y., Morrisey E.E. Importance of myocyte-nonmyocyte interactions in cardiac development and disease. Circ. Res. 2012, 110:1023-1034.
229. Tomanek R.J., Holifield J.S., Reiter R.S., Sandra A., Lin J.J. Role of VEGF family members and receptors in coronary vessel formation. Dev. Dyn. 2002, 225:233-240.
230. Tomanek R.J. Formation of the coronary vasculature during development. Angiogenesis 2005, 8:273-284.
231. Tomanek R.J., Ishii Y., Holifield J.S., Sjogren C.L., Hansen H.K., Mikawa T. VEGF family members regulate myocardial tubulogenesis and coronary artery formation in the embryo. Circ. Res. 2006, 98:947-953.
232. Torlopp A., Schlueter J., Brand T. Role of fibroblast growth factor signaling during proepicardium formation in the chick embryo. Dev. Dyn. 2010, 239:2393-2403.
233. Uemura A., Ogawa M., Hirashima M., Fujiwara T., Koyama S., Takagi H., Honda Y., Wiegand S.J., Yancopoulos G.D., Nishikawa S. Recombinant angiopoietin-1 restores higher-order architecture of growing blood vessels in mice in the absence of mural cells. J. Clin. Invest. 2002, 110:1619-1628.
234. Van Den Akker N.M., Lie-Venema H., Maas S., Eralp I., DeRuiter M.C., Poelmann R.E., Gittenberger-De Groot A.C. Platelet-derived growth factors in the developing avian heart and maturating coronary vasculature. Dev. Dyn. 2005, 233:1579-1588.
235. van den Akker N.M., Molin D.G., Peters P.P., Maas S., Wisse L.J., van Brempt R., van Munsteren C.J., Bartelings M.M., Poelmann R.E., Carmeliet P., Gittenberger-de Groot A.C. Tetralogy of fallot and alterations in vascular endothelial growth factor-A signaling and Notch signaling in mouse embryos solely expressing the VEGF120 isoform. Circ. Res. 2007, 100:842-849.
236. van den Akker N.M., Caolo V., Wisse L.J., Peters P.P., Poelmann R.E., Carmeliet P., Molin D.G., Gittenberger-de Groot A.C. Developmental coronary maturation is disturbed by aberrant cardiac vascular endothelial growth factor expression and Notch signalling. Cardiovasc. Res. 2008, 78:366-375.
237. van den Akker N.M., Winkel L.C., Nisancioglu M.H., Maas S., Wisse L.J., Armulik A., Poelmann R.E., Lie-Venema H., Betsholtz C., Gittenberger-de Groot A.C. PDGF-B signaling is important for murine cardiac development: its role in developing atrioventricular valves, coronaries, and cardiac innervation. Dev. Dyn. 2008, 237:494-503.
238. Van den Eijnde S.M., Wenink A.C., Vermeij-Keers C. Origin of subepicardial cells in rat embryos. Anat. Rec. 1995, 242:96-102.
239. van Tuyn J., Atsma D.E., Winter E.M., van der Velde-van Dijke I., Pijnappels D.A., Bax N.A.M., Knaän-Shanzer S., Gittenberger-de Groot A.C., Poelmann R.E., van der Laarse A., van der Wall E.E., Schalij M.J., de Vries A.A.F. Epicardial cells of human adults can undergo an epithelial-to-mesenchymal transition and obtain characteristics of smooth muscle cells in vitro. Stem Cells 2007, 25:271-278.
240. van Wijk B., van den Berg G., Abu-Issa R., Barnett P., van der Velden S., Schmidt M., Ruijter J.M., Kirby M.L., Moorman A.F., van den Hoff M.J. Epicardium and myocardium separate from a common precursor pool by crosstalk between bone morphogenetic protein- and fibroblast growth factor-signaling pathways. Cir. Res. 2009, 105:431-441.
241. Vega-Hernandez M., Kovacs A., De Langhe S., Ornitz D.M. FGF10/FGFR2b signaling is essential for cardiac fibroblast development and growth of the myocardium. Development 2011, 138:3331-3340.
242. Villa N., Walker L., Lindsell C.E., Gasson J., Iruela-Arispe M.L., Weinmaster G. Vascular expression of Notch pathway receptors and ligands is restricted to arterial vessels. Mech. Dev. 2001, 108:161-164.
243. Viragh S., Challice C.E. The origin of the epicardium and the embryonic myocardial circulation in the mouse. Anat. Rec. 1981, 201:157-168.
244. Vogeli K.M., Jin S.W., Martin G.R., Stainier D.Y. A common progenitor for haematopoietic and endothelial lineages in the zebrafish gastrula. Nature 2006, 443:337-339.
245. Vokes S.A., Yatskievych T.A., Heimark R.L., McMahon J., McMahon A.P., Antin P.B., Krieg P.A. Hedgehog signaling is essential for endothelial tube formation during vasculogenesis. Development 2004, 131:4371-4380.
246. von Gise A., Zhou B., Honor L.B., Ma Q., Petryk A., Pu W.T. WT1 regulates epicardial epithelial to mesenchymal transition through beta-catenin and retinoic acid signaling pathways. Dev. Biol. 2011, 356:421-431.
247. von Gise A., Pu W.T. Endocardial and epicardial epithelial to mesenchymal transitions in heart development and disease. Circ. Res. 2012, 110:1628-1645.
248. Vrancken Peeters M.P., Mentink M.M., Poelmann R.E., Gittenberger-de Groot A.C. Cytokeratins as a marker for epicardial formation in the quail embryo. Anat. Embryol. 1995, 191:503-508.
249. Vrancken Peeters M.P., Gittenberger-de Groot A.C., Mentink M.M., Hungerford J.E., Little C.D., Poelmann R.E. Differences in development of coronary arteries and veins. Cardiovasc. Res. 1997, 36:101-110.
250. Vrancken Peeters M.P., Gittenberger-de Groot A.C., Mentink M.M., Hungerford J.E., Little C.D., Poelmann R.E. The development of the coronary vessels and their differentiation into arteries and veins in the embryonic quail heart. Dev. Dyn. 1997, 208:338-348.
251. Wakui S., Yokoo K., Muto T., Suzuki Y., Takahashi H., Furusato M., Hano H., Endou H., Kanai Y. Localization of Ang-1, -2, Tie-2, and VEGF expression at endothelial-pericyte interdigitation in rat angiogenesis. Lab. Invest. 2006, 86:1172-1184.
252. Waldo K.L., Kumiski D.H., Kirby M.L. Association of the cardiac neural crest with development of the coronary arteries in the chick embryo. Anat. Rec. 1994, 239:315-331.
253. Waldo K.L., Lo C.W., Kirby M.L. Connexin 43 expression reflects neural crest patterns during cardiovascular development. Dev. Biol. 1999, 208:307-323.
254. Waldo K.L., Hutson M.R., Ward C.C., Zdanowicz M., Stadt H.A., Kumiski D., Abu-Issa R., Kirby M.L. Secondary heart field contributes myocardium and smooth muscle to the arterial pole of the developing heart. Dev. Biol. 2005, 281:78-90.
255. Wang H.U., Chen Z.F., Anderson D.J. Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 1998, 93:741-753.
256. Ward C., Stadt H., Hutson M., Kirby M.L. Ablation of the secondary heart field leads to tetralogy of Fallot and pulmonary atresia. Dev. Biol. 2005, 284:72-83.
257. Ward N.L., Van Slyke P., Dumont D.J. Functional inhibition of secreted angiopoietin: a novel role for angiopoietin 1 in coronary vessel patterning. Biochem. Biophys. Res. Commun. 2004, 323:937-946.
258. Watt A.J., Battle M.A., Li J., Duncan S.A. GATA4 is essential for formation of the proepicardium and regulates cardiogenesis. Proc. Natl. Acad. Sci. U S A. 2004, 101:12573-12578.
259. Wengerhoff S.M., Weiss A.R., Dwyer K.L., Dettman R.W. A migratory role for EphrinB ligands in avian epicardial mesothelial cells. Dev. Dyn. 2010, 239:598-609.
260. Winter E.M., Grauss R.W., Hogers B., van Tuyn J., van der Geest R., Lie-Venema H., Steijn R.V., Maas S., DeRuiter M.C., deVries A.A., Steendijk P., Doevendans P.A., van der Laarse A., Poelmann R.E., Schalij M.J., Atsma D.E., Gittenberger-de Groot A.C. Preservation of left ventricular function and attenuation of remodeling after transplantation of human epicardium-derived cells into the infarcted mouse heart. Circulation 2007, 116:917-927.
261. Winter E.M., van Oorschot A.A., Hogers B., van der Graaf L.M., Doevendans P.A., Poelmann R.E., Atsma D.E., Gittenberger-de Groot A.C., Goumans M.J. A new direction for cardiac regeneration therapy: application of synergistically acting epicardium-derived cells and cardiomyocyte progenitor cells. Circ. Heart Fail. 2009, 2:643-653.
262. Wu M., Smith C.L., Hall J.A., Lee I., Luby-Phelps K., Tallquist M.D. Epicardial spindle orientation controls cell entry into the myocardium. Dev. Cell 2010, 19:114-125.
263. Xu J., Lamouille S., Derynck R. TGF-beta-induced epithelial to mesenchymal transition. Cell. Res. 2009, 19:156-172.
264. Yamagishi T., Nakajima Y., Miyazono K., Nakamura H. Bone morphogenetic protein-2 acts synergistically with transforming growth factor-beta3 during endothelial-mesenchymal transformation in the developing chick heart. J. Cell Physiol. 1999, 180:35-45.
265. Yamagishi T., Nakajima Y., Nishimatsu S., Nohno T., Ando K., Nakamura H. Expression of bone morphogenetic protein-5 gene during chick heart development: possible roles in valvuloseptal endocardial cushion formation. Anat. Rec. 2001, 264:313-316.
266. Yamashita J., Itoh H., Hirashima M., Ogawa M., Nishikawa S., Yurugi T., Naito M., Nakao K. Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature 2000, 408:92-96.
267. Yamamizu K., Kawasaki K., Katayama S., Watabe T., Yamashita J.K. Enhancement of vascular progenitor potential by protein kinase A through dual induction of Flk-1 and neuropilin-1. Blood 2009, 114:3707-3716.
268. Yamamizu K., Matsunaga T., Uosaki H., Fukushima H., Katayama S., Hiraoka-Kanie M., Mitani K., Yamashita J.K. Convergence of Notch and beta-catenin signaling induces arterial fate in vascular progenitors. J. Cell Biol. 2010, 189:325-338.
269. Yamamizu K., Yamashita J.K. Roles of cyclic adenosine monophosphate signaling in endothelial cell differentiation and arterial-venous specification during vascular development. Circ. J. 2011, 75:253-260.
270. Yamanaka O., Hobbs R.E. Coronary artery anomalies in 126,595 patients undergoing coronary arteriography. Cathet. Cardiovasc. Diagn. 1990, 21:28-40.
271. Yang K., Doughman Y.Q., Karunamuni G., Gu S., Yang Y.C., Bader D.M., Watanabe M. Expression of active Notch1 in avian coronary development. Dev. Dyn. 2009, 238:162-170.
272. Yang J., Weinberg R.A. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 2008, 14:818-829.
273. Yang J.T., Rayburn H., Hynes R.O. Cell adhesion events mediated by alpha 4 integrins are essential in placental and cardiac development. Development 1995, 121:549-560.
274. Yoshida T., Owens G.K. Molecular determinants of vascular smooth muscle cell diversity. Circ. Res. 2005, 96:280-291.
275. Zamora M., Manner J., Ruiz-Lozano P. Epicardium-derived progenitor cells require beta-catenin for coronary artery formation. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:18109-18114.
276. Zeisberg M., Neilson E.G. Biomarkers for epithelial-mesenchymal transitions. J. Clin. Invest. 2009, 119:1429-1437.
277. Zhong T.P., Rosenberg M., Mohideen M.A., Weinstein B., Fishman M.C. Gridlock, an HLH gene required for assembly of the aorta in zebrafish. Science 2000, 287:1820-1824.
278. Zhou B., von Gise A., Ma Q., Rivera-Feliciano J., Puj W.T. Nkx2-5- and Isl1-expressing cardiac progenitors contribute to proepicardium. Biochem. Biophys. Res. Commun. 2008, 375:450-453.
279. Zhou B., Honor L.B., He H., Ma Q., Oh J.H., Butterfield C., Lin R.Z., Melero-Martin J.M., Dolmatova E., Duffy H.S., Gise A., Zhou P., Hu Y.W., Wang G., Zhang B., Wang L., Hall J.L., Moses M.A., McGowan F.X., Pu W.T. Adult mouse epicardium modulates myocardial injury by secreting paracrine factors. J. Clin. Invest. 2011, 121:1894-1904.
280. Zhou B., Honor L.B., Ma Q., Oh J.H., Lin R.Z., Melero-Martin J.M., von Gise A., Zhou P., Hu T., He L., Wu K.H., Zhang H., Zhang Y., Pu W.T. Thymosin beta 4 treatment after myocardial infarction does not reprogram epicardial cells into cardiomyocytes. J. Mol. Cell Cardiol. 2012, 52:43-47.