Mechanisms of endothelial differentiation in embryonic vasculogenesis

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 25, Issue 11, 2005, Pages 2246-2254

  Ferguson III, J E ^a,b   Kelley, Rusty W ^a   Patterson, Cam ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Development; Embryogenesis; Endothelium; Vasculogenesis

Indexed keywords

ANGIOGENESIS; CANCER; CELL DIFFERENTIATION; DIABETIC RETINOPATHY; EMBRYO DEVELOPMENT; ENDOTHELIUM CELL; HUMAN; ISCHEMIA; NONHUMAN; PRIORITY JOURNAL; SHORT SURVEY; STEM CELL;

ANIMALS; BLOOD VESSELS; CELL DIFFERENTIATION; ENDOTHELIUM, VASCULAR; HUMANS; PLURIPOTENT STEM CELLS;

EID: 27644435456     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.0000183609.55154.44     Document Type: Short Survey

References (107)

1. Bailey AS, Fleming WH. Converging roads: evidence for an adult hemangioblast. Exp Hematol. 2003;31:987-993.
2. Noden DM. Embryonic origins and assembly of blood vessels. Am Rev Respir Dis. 1989;140:1097-1103.
3. Belaoussoff M, Farrington SM, Baron MH. Hematopoietic induction and respecification of A-P identity by visceral endoderm signaling in the mouse embryo. Development. 1998;125:5009-5018.
4. Dyer MA, Farrington SM, Mohn D, Munday JR, Baron MH. Indian hedgehog activates hematopoiesis and vasculogenesis and can respecify prospective neurectodermal cell fate in the mouse embryo. Development. 2001;128:1717-1730.
5. Vokes SA, Krieg PA. Endoderm is required for vascular endothelial tube formation, but not for angioblast specification. Development. 2002;129:775-785.
6. Sabin FR. Preliminary note on the differentiation of angioblasts and the method by which they produce blood-vessels, blood-plasma, and red blood-cells as seen in the living chick. Anatomical Record. 1917;13:199-204.
7. Choi K, Kennedy M, Kazarov A, Papadimitriou JC, Keller G. A common precursor for hematopoietic and endothelial cells. Development. 1998;125:725-732.
8. Nishikawa SI, 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.
9. Drake CJ, Fleming PA. Vasculogenesis in the day 6.5 to 9.5 mouse embryo. Blood. 2000;95:1671-1679.
10. Noden DM. Origins and assembly of avian embryonic blood vessels. Ann N Y Acad Sci. 1990;588:236-249.
11. Pardanaud L, Dieterlen-Lievre F. Emergence of endothelial and hemopoietic cells in the avian embryo. Anat Embryol (Berl). 1993;187:107-114.
12. de Bruijn MF, Ma X, Robin C, Ottersbach K, Sanchez MJ, Dzierzak E. Hematopoietic stem cells localize to the endothelial cell layer in the midgestation mouse aorta. Immunity. 2002;16:673-683.
13. Medvinsky A, Dzierzak E. Definitive hematopoiesis is autonomously initiated by the AGM region. Cell. 1996;86:897-906.
14. Fehling HJ, Lacaud G, Kubo A, Kennedy M, Robertson S, Keller G, Kouskoff V. Tracking mesoderm induction and its specification to the hemangioblast during embryonic stem cell differentiation. Development. 2003;130:4217-4227.
15. Huber TL, Kouskoff V, Fehling HJ, Palis J, Keller G. Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature. 2004;432:625-630.
16. Mitrani E, Gruenbaum Y, Shohat H, Ziv T. Fibroblast growth factor during mesoderm induction in the early chick embryo. Development. 1990;109:387-393.
17. Downs KM, Harmann C. Developmental potency of the murine allantois. Development. 1997;124:2769-2780.
18. Downs KM, Gifford S, Blahnik M, Gardner RL. Vascularization in the murine allantois occurs by vasculogenesis without accompanying erythropoiesis. Development. 1998;125:4507-4520.
19. Caprioli A, Minko K, Drevon C, Eichmann A, Dieterlen-Lievre F, Jaffredo T. Hemangioblast commitment in the avian allantois: cellular and molecular aspects. Dev Biol. 2001;238:64-78.
20. Caprioli A, Jaffredo T, Gautier R, Dubourg C, Dieterlen-Lievre F. Blood-borne seeding by hematopoietic and endothelial precursors from the allantois. Proc Natl Acad Sci U S A. 1998;95:1641-1646.
21. Downs KM, Hellman ER, McHugh J, Barrickman K, Inmah KE. Investigation into a role for the primitive streak in development of the murine allantois. Development. 2004;131:37-55.
22. Dzierzak E. Ontogenic emergence of definitive hematopoietic stem cells. Curr Opin Hematol. 2003;10:229-234.
23. Majesky MW. Development of coronary vessels. Curr Top Dev Biol. 2004;62:225-259.
24. Perez-Pomares JM, 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.
25. Wada AM, Willet SG, Bader D. Coronary vessel development: a unique form of vasculogenesis. Arterioscler Thromb Vasc Biol. 2003;23:2138-2145.
26. Tevosian SG, Deconinck AE, Tanaka M, Schinke M, Litovsky SH, Izumo S, Fujiwara Y, Orkin SH. FOG-2, a cofactor for GATA transcription factors, is essential for heart morphogenesis and development of coronary vessels from epicardium. Cell. 2000;101:729-739.
27. Flamme I, Risau W. Induction of vasculogenesis and hematopoiesis in vitro. Development. 1992;116:435-439.
28. Yang X, Li C, Xu X, Deng C. The tumor suppressor SMAD4/DPC4 is essential for epiblast proliferation and mesoderm induction in mice. Proc Natl Acad Sci U S A. 1998;95:3667-3672.
29. Winnier G, Blessing M, Labosky PA, Hogan BL. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 1995;9:2105-2116.
30. Sirard C, de la Pompa JL, Elia A, Itie A, Mirtsos C, Cheung A, Hahn S, Wakeham A, Schwartz L, Kern SE, Rossant J, Mak TW. The tumor suppressor gene Smad4/Dpc4 is required for gastrulation and later for anterior development of the mouse embryo. Genes Dev. 1998;12:107-119.
31. Chang H, Huylebroeck D, Verschueren K, Guo Q, Matzuk MM, Zwijsen A. Smad5 knockout mice die at mid-gestation due to multiple embryonic and extraembryonic defects. Development. 1999;126:1631-1642.
32. Moser M, Binder O, Wu Y, Aitsebaomo J, Ren R, Bode C, Bautch VL, Conlon FL, Patterson C. BMPER, a novel endothelial cell precursor-derived protein, antagonizes bone morphogenetic protein signaling and endothelial cell differentiation. Mol Cell Biol. 2003;23:5664-5679.
33. Yamaguchi TP, Takada S, Yoshikawa Y, Wu N, McMahon AP. T (Brachyury) is a direct target of Wnt3a during paraxial mesoderm specification. Genes Dev. 1999;13:3185-3190.
34. Liu P, Wakamiya M, Shea MJ, Albrecht U, Behringer RR, Bradley A. Requirement for Wnt3 in vertebrate axis formation. Nat Genet. 1999;22:361-365.
35. Monkley SJ, Delaney SJ, Pennisi DJ, Christiansen JH, Wainwright BJ. Targeted disruption of the Wnt2 gene results in placentation defects. Development. 1996;122:3343-3353.
36. Wang J, Wynshaw-Boris A. The canonical Wm pathway in early mammalian embryogenesis and stem cell maintenance/differentiation. Curr Opin Genet Dev. 2004;14:533-539.
37. 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.
38. Motoike T, Markham DW, Rossant J, Sato TN. Evidence for novel fate of Flk1+ progenitor: contribution to muscle lineage. Genesis. 2003;35:153-159.
39. He Z, Tessier-Lavigne M. Neuropilin is a receptor for the axonal chemorepellent Semaphorin Spaceiiiqq. Cell. 1997;90:739-751.
40. 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.
41. Carmeliet P, Lampugnani MG, Moons L, Breviario F, Compernolle V, Bono F, Balconi G, Spagnuolo R, Oostuyse B, Dewerchin M, Zanetti A, Angellilo A, Mattot V, Nuyens D, Lutgens E, Clotman F, de Ruiter MC, Gittenberger-de Groot A, Poelmann R, Lupu F, Herbert JM, Collen D, Dejana E. Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell. 1999;98:147-157.
42. Goodwin AM, D'Amore PA. Wnt signaling in the vasculature. Angiogenesis. 2002;5:1-9.
43. Matsumoto T, Claesson-Welsh L VEGF receptor signal transduction. Sci STKE. 2001;2001:RE21.
44. Ryan HE, Lo J, Johnson RS. HIF-1 alpha is required for solid tumor formation and embryonic vascularization. Embo J. 1998;17:3005-3015.
45. Pages G, Pouyssegur J. Transcriptional regulation of the vascular endothelial growth factor gene-a concert of activating factors. Cardiovasc Res. 2005;65:564-573.
46. Wu Y, Moser M, Bautch VL, Patterson C. HoxB5 is an upstream transcriptional switch for differentiation of the vascular endothelium from precursor cells. Mol Cell Biol. 2003;23:5680-5691.
47. De Val S, Anderson JP, Heidt AB, Khiem D, Xu SM, Black BL. Mef2c is activated directly by Ets transcription factors through an evolutionarily conserved endothelial cell-specific enhancer. Dev Biol. 2004;275:424-434.
48. Liao W, Bisgrove BW, Sawyer H, Hug B, Bell B, Peters K, Grunwald DJ, Stainier DY. The zebrafish gene cloche acts upstream of a flk-1 homologue to regulate endothelial cell differentiation. Development. 1997;124:381-389.
49. Liao EC, Paw BH, Oates AC, Pratt SJ, Postlethwait JH, Zon LI. SCL/Tal-1 transcription factor acts downstream of cloche to specify hematopoietic and vascular progenitors in zebrafish. Genes Dev. 1998;12:621-626.
50. Shalaby F, Ho J, Stanford WL, Fischer KD, Schuh AC, Schwartz L, Bernstein A, Rossant J. A requirement for Flk 1 in primitive and definitive hematopoiesis and vasculogenesis. Cell. 1997;89:981-990.
51. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML, Schuh AC. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature. 1995;376:62-66.
52. Robertson SM, Kennedy M, Shannon JM, Keller G. A transitional stage in the commitment of mesoderm to hematopoiesis requiring the transcription factor SCL/tal-1. Development. 2000;127:2447-2459.
53. Robb L, Lyons I, Li R, Hartley L, Kontgen F, Harvey RP, Metcalf D, Begley CG. Absence of yolk sac hematopoiesis from mice with a targeted disruption of the scl gene. Proc Natl Acad Sci U S A. 1995;92:7075-7079.
54. Gory-Faure S, Prandini MH, Pointu H, Roullot V, Pignot-Paintrand I, Vernet M, Huber P. Role of vascular endothelial-cadherin in vascular morphogenesis. Development. 1999;126:2093-2102.
55. Sato TN, 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.
56. Kearney JB, Kappas NC, Ellerstrom C, DiPaola FW, Bautch VL. The VEGF receptor flt-1 (VEGFR-1) is a positive modulator of vascular sprout formation and branching morphogenesis. Blood. 2004;103:4527-4535.
57. Suri C, Jones PF, Patan S, Bartunkova S, Maisonpierre PC, Davis S, Sato TN, Yancopoulos GD. Requisite role of angiopoietin-1, a ligand for the T1E2 receptor, during embryonic angiogenesis. Cell. 1996;87:1171-1180.
58. Peppel K, Zhang L, Orman ES, Hagen PO, Amalfitano A, Brian L, Freedman NJ. Activation of vascular smooth muscle cells by TNF and PDGF: overlapping and complementary signal transduction mechanisms. Cardiovasc Res. 2005;65:674-682.
59. Kuhnert F, Campagnolo L, Xiong JW, Lemons D, Fitch MJ, Zou Z, Kiosses WB, Gardner H, Stuhlmann H. Dosage-dependent requirement for mouse Vezf1 in vascular system development. Dev Biol. 2005;283:140-156.
60. Kappel A, Schlaeger TM, Flamme I, Orkin SH, Risau W, Breier G. Role of SCL/Tal-1, GATA, and ets transcription factor binding sites for the regulation of flk-1 expression during murine vascular development. Blood. 2000;96:3078-3085.
61. Suzuki T, Aizawa K, Matsumura T, Nagai R. Vascular implications of the Kruppel-like family of transcription factors. Arterioscler Thromb Vasc Biol. 2005;25:1135-1141.
62. Oikawa M, Abe M, Kurosawa H, Hida W, Shirato K, Sato Y. Hypoxia induces transcription factor ETS-1 via the activity of hypoxia-inducible factor-1. Biochem Biophys Res Commun. 2001;289:39-43.
63. Sato Y. Role of ETS family transcription factors in vascular development and angiogenesis. Cell Struct Funct. 2001;26:19-24.
64. Myers C, Charboneau A, Boudreau N. Homeobox B3 promotes capillary morphogenesis and angiogenesis. J Cell Biol. 2000;148:343-351.
65. Parker LH, Schmidt M, Jin SW, Gray AM, Beis D, Pham T, Frantz G, Palmieri S, Hillan K, Stainier DY, De Sauvage FJ, Ye W. The endothelial-cell-derived secreted factor Egf17 regulates vascular tube formation. Nature. 2004;428:754-758.
66. van der Zwaag B, Hellemons AJ, Leenders WP, Burbach JP, Brunner HG, Padberg GW, Van Bokhoven H. PLEXIN-D1, a novel plexin family member, is expressed in vascular endothelium and the central nervous system during mouse embryogenesis. Dev Dyn. 2002;225:336-343.
67. Herzog Y, Guttmann-Raviv N, Neufeld G. Segregation of arterial and venous markers in subpopulations of blood islands before vessel formation. Dev Dyn. 2005;232:1047-1055.
68. Lawson ND, Vogel AM, Weinstein BM. sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation. Dev Cell. 2002;3:127-136.
69. Lawson ND, Scheer N, Pham VN, Kim CH, Chitnis AB, Campos-Ortega JA, Weinstein BM. Notch signaling is required for arterial-venous differentiation during embryonic vascular development. Development. 2001;128:3675-3683.
70. Oike Y, Ito Y, Hamada K, Zhang XQ, Miyata K, Arai F, Inada T, Araki K, Nakagata N, Takeya M, Kisanuki YY, Yanagisawa M, Gale NW, Suda T. Regulation of vasculogenesis and angiogenesis by EphB/ephrin-B2 signaling between endothelial cells and surrounding mesenchymal cells. Blood. 2002;100:1326-1333.
71. Wang HU, Chen ZF, Anderson DJ. Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell. 1998;93:741-753.
72. Wigle JT, Oliver G. Prox1 function is required for the development of the murine lymphatic system. Cell. 1999;98:769-778.
73. 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.
74. Gale NW, Thurston G, Hackett SF, Renard R, Wang Q, McClain J, Martin C, Witte C, Witte MH, Jackson D, Suri C, Campochiaro PA, Wiegand SJ, Yancopoulos GD. Angiopoietin-2 is required for postnatal angiogenesis and lymphatic patterning, and only the latter role is rescued by Angiopoietin-1. Dev Cell. 2002;3:411-423.
75. Manner J. Does the subepicardial mesenchyme contribute myocardio-blasts to the myocardium of the chick embryo heart? A quail-chick chimera study tracing the fate of the epicardial primordium. Anat Rec. 1999;255:212-226.
76. Stainier DY, Fouquet B, Chen JN, Warren KS, Weinstein BM, Meiler SE, Mohideen MA, Neuhauss SC, Solnica-Krezel L, Schier AF, Zwartkruis F, Stemple DL, Malicki J, Driever W, Fishman MC. Mutations affecting the formation and function of the cardiovascular system in the zebrafish embryo. Development. 1996;123:285-292.
77. Stainier DY, Weinstein BM, Detrich HW, 3rd, Zon LI, Fishman MC. Cloche, an early acting zebrafish gene, is required by both the endothelial and hematopoietic lineages. Development. 1995;121:3141-3150.
78. Mao X, Fujiwara Y, Chapdelaine A, Yang H, Orkin SH. Activation of EGFP expression by Cre-mediated excision in a new ROSA26 reporter mouse strain. Blood. 2001;97:324-326.
79. Mao X, Fujiwara Y, Orkin SH. Improved reporter strain for monitoring Cre recombinase-mediated DNA excisions in mice. Proc Natl Acad Sci U S A. 1999;96:5037-5042.
80. Argraves KM, Wilkerson BA, Argraves WS, Fleming PA, Obeid LM, Drake CJ. Sphingosine-1-phosphate signaling promotes critical migratory events in vasculogenesis. J Biol Chem. 2004;279:50580-50590.
81. Kearney JB, Ambler CA, Monaco KA, Johnson N, Rapoport RG, Bautch VL. Vascular endothelial growth factor receptor Flt-1 negatively regulates developmental blood vessel formation by modulating endothelial cell division. Blood. 2002;99:2397-2407.
82. Schuh AC, Faloon P, Hu QL, 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.
83. Bautch VL, Redick SD, Scalia A, Harmaty M, Carmeliet P, Rapoport R. Characterization of the vasculogenic block in the absence of vascular endothelial growth factor-A. Blood. 2000;95:1979-1987.
84. Stanford WL, Caruana G, Vallis KA, Inamdar M, Hidaka M, Bautch VL, Bernstein A. Expression trapping: identification of novel genes expressed in hematopoietic and endothelial lineages by gene trapping in ES cells. Blood. 1998;92:4622-4631.
85. Ishikawa T, Tamai Y, Zorn AM, Yoshida H, Seldin MF, Nishikawa S, Taketo MM. Mouse Wnt receptor gene Fzd5 is essential for yolk sac and placental angiogenesis. Development. 2001;128:25-33.
86. Cattelino A, Liebner S, Gallini R, Zanetti A, Balconi G, Corsi A, Bianco P, Wolburg H, Moore R, Oreda B, Kemler R, Dejana E. The conditional inactivation of the beta-catenin gene in endothelial cells causes a defective vascular pattern and increased vascular fragility. J Cell Biol. 2003;162:1111-1122.
87. Liebner S, Cattelino A, Gallini R, Rudini N, Iurlaro M, Piccolo S, Dejana E. Beta-catenin is required for endothelial-mesenchymal transformation during heart cushion development in the mouse. J Cell Biol. 2004;166:359-367.
88. Byrd N, Becker S, Maye P, Narasimhaiah R, St-Jacques B, Zhang X, McMahon J, McMahon A, Grabel L. Hedgehog is required for murine yolk sac angiogenesis. Development. 2002;129:361-372.
89. Pepicelli CV, Lewis PM, McMahon AP. Sonic hedgehog regulates branching morphogenesis in the mammalian lung. Curr Biol. 1998;8:1083-1086.
90. Chen JN, Haffter P, Odenthal J, Vogelsang E, Brand M, van Eeden FJ, Furutani-Seiki M, Granato M, Hammerschmidt M, Heisenberg CP, Jiang YJ, Kane DA, Kelsh RN, Mullins MC, Nusslein-Volhard C. Mutations affecting the cardiovascular system and other internal organs in zebrafish. Development. 1996;123:293-302.
91. Zhang H, Bradley A. Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development. 1996;122:2977-2986.
92. Chang H, Matzuk MM. Smad5 is required for mouse primordial germ cell development. Mech Dev. 2001;104:61-67.
93. Chang H, Zwijsen A, Vogel H, Huylebroeck D, Matzuk MM. Smad5 is essential for left-right asymmetry in mice. Dev Biol. 2000;219:71-78.
94. Abe K, Yamamura K, Suzuki M. Molecular and embryological characterization of a new transgene-induced null allele of mouse Brachyury locus. Mamm Genome. 2000;11:238-240.
95. Davenport TG, Jerome-Majewska LA, Papaioannou VE. Mammary gland, limb and yolk sac defects in mice lacking Tbx3, the gene mutated in human ulnar mammary syndrome. Development. 2003;130:2263-2273.
96. Yamaguchi TP, Harpal K, Henkemeyer M, Rossant J. fgfr-1 is required for embryonic growth and mesodermal patterning during mouse gastrulation. Genes Dev. 1994;8:3032-3044.
97. Deng CX, Wynshaw-Boris A, Shen MM, Daugherty C, Ornitz DM, Leder P. Murine FGFR-1 is required for early postimplantation growth and axial organization. Genes Dev. 1994;8:3045-3057.
98. Zhou M, Sutliff RL, Paul RJ, Lorenz JN, Hoying JB, Haudenschild CC, Yin M, Coffin JD, Kong L, Kranias EG, Luo W, Boivin GP, Duffy JJ, Pawlowski SA, Doetschman T. Fibroblast growth factor 2 control of vascular tone. Nat Med. 1998;4:201-207.
99. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, Powell-Braxton L, Hillan KJ, Moore MW. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature. 1996;380:439-442.
100. Kawasaki T, Kitsukawa T, Bekku Y, Matsuda Y, Sanbo M, Yagi T, Fujisawa H. A requirement for neuropilin-1 in embryonic vessel formation. Development. 1999;126:4895-4902.
101. Yuan L, Moyon D, Pardanaud L, Bream C, Karkkainen MJ, Alitalo K, Eichmann A. Abnormal lymphatic vessel development in neuropilin 2 mutant mice. Development. 2002;129:4797-4806.
102. Dumont DJ, Gradwohl G, Fong GH, Pun MC, Gertsenstein M, Auerbach A, Breitman ML. Dominant-negative and targeted null mutations in the endothelial receptor tyrosine kinase, tek, reveal a critical role in vasculogenesis of the embryo. Genes Dev. 1994;8:1897-1909.
103. Bi W, Drake CJ, Schwarz JJ. The transcription factor MEF2C-null mouse exhibits complex vascular malformations and reduced cardiac expression of angiopoietin 1 and VEGF. Dev Biol. 1999;211:255-267.
104. Lin Q, Lu J, Yanagisawa H, Webb R, Lyons GE, Richardson JA, Olson EN. Requirement of the MADS-box transcription factor MEF2C for vascular development. Development. 1998;125:4565-4574.
105. Adams RH, Wilkinson GA, Weiss C, Diella F, Gale NW, 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.
106. Gerety SS, Wang HU, Chen ZF, Anderson DJ. Symmetrical mutant phenotypes of the receptor EphB4 and its specific transmembrane ligand ephrin-B2 in cardiovascular development. Mol Cell. 1999;4:403-414.
107. Karkkainen MJ, Haiko P, Sainio K, Partanen J, Taipale J, Petrova TV, Jeltsch M, Jackson DG, Talikka M, Rauvala H, Betsholtz C, Alitalo K. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat Immunol. 2004;5:74-80.