Vascular development in the zebrafish

Cold Spring Harbor Perspectives in Medicine

Volumn 2, Issue 5, 2012, Pages

  Gore, Aniket V ^a   Monzo, Kathryn ^a   Cha, Young R ^a   Pan, Weijun ^a   Weinstein, Brant M ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR SOX18; TRANSCRIPTION FACTOR SOX7; TUBULIN; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR;

ANATOMIC MODEL; ANATOMICAL CONCEPTS; ARTICLE; BLOOD VESSEL; BLOOD VESSEL PERMEABILITY; EMBRYO DEVELOPMENT; ENDOTHELIUM; ENDOTHELIUM CELL; GENE EXPRESSION; HEMANGIOBLAST; LYMPHANGIOGENESIS; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ZEBRA FISH; ANGIOGENESIS; ANIMAL; BRAIN; CAPILLARY PERMEABILITY; KIDNEY; LYMPHATIC SYSTEM; MICROTUBULE; PHYSIOLOGY; PRENATAL DEVELOPMENT; REVIEW; VASCULAR ENDOTHELIUM; VASCULARIZATION;

DANIO RERIO; VERTEBRATA;

ANIMALS; BLOOD VESSELS; BRAIN; CAPILLARY PERMEABILITY; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; KIDNEY; LYMPHATIC SYSTEM; MICROTUBULES; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TUBULIN; VASCULAR ENDOTHELIAL GROWTH FACTOR A; ZEBRAFISH;

EID: 84871696023     PISSN: None     EISSN: 21571422     Source Type: Journal    
DOI: 10.1101/cshperspect.a006684     Document Type: Article

References (128)

1. Alders M, Hogan BM, Gjini E, Salehi F, Al-Gazali L, Hennekam EA, HolmbergEE, Mannens MM, Mulder MF, Offerhaus GJ, et al. 2009. Mutations in CCBE1 cause generalized lymph vessel dysplasia in humans. Nat Genet 41: 1272-1274.
2. Alvarez Y, Cederlund ML, Cottell DC, Bill BR, Ekker SC, Torres-Vazquez J, Weinstein BM, Hyde DR, Vihtelic TS, Kennedy BN. 2007. Genetic determinants of hyaloid and retinal vasculature in zebrafish. BMC Dev Biol 7: 114.
3. Alvarez Y, Astudillo O, Jensen L, Reynolds AL, Waghorne N, Brazil DP, Cao Y, O'Connor JJ, Kennedy BN. 2009. Selective inhibition of retinal angiogenesis by targeting PI3 kinase. PLoS One 4: e7867.
4. Bayless KJ, Davis GE. 2002. The Cdc42 and Rac1 GTPases are required for capillary lumen formation in three-dimensional extracellular matrices. J Cell Sci 115: 1123-1136.
5. 1 integrins. Am J Pathol 156: 1673-1683.
6. Blum Y, Belting HG, Ellertsdottir E, Herwig L, Luders F, Affolter M. 2008. Complex cell rearrangements during intersegmental vessel sprouting and vessel fusion in the zebrafish embryo. Dev Biol 316: 312-322.
7. Bouvree K, Larrivee B, Lv X, Yuan L, DeLafarge B, Freitas C, Mathivet T, BreantC, Tessier-Lavigne M, Bikfalvi A, et al. 2008. Netrin-1 inhibits sprouting angiogenesis in developing avian embryos. Dev Biol 318: 172-183.
8. Bressan M, Davis P, Timmer J, Herzlinger D, Mikawa T. 2009. Notochord-derived BMP antagonists inhibit endothelial cell generation and network formation. Dev Biol 326: 101-111.
9. Buchner DA, Su F, Yamaoka JS, Kamei M, Shavit JA, Barthel LK, McGee B, AmigoJD, Kim S, Hanosh AW, et al. 2007. pak2a mutations cause cerebral hemorrhage in redhead zebrafish. Proc Natl Acad Sci 104: 13996-4001.
10. Bussmann J, Bos FL, Urasaki A, Kawakami K, Duckers HJ, Schulte-Merker S. 2010. Arteries provide essential guidance cues for lymphatic endothelial cells in the zebrafish trunk. Development 137: 2653-2657.
11. Cermenati S, Moleri S, Cimbro S, Corti P, Del Giacco L, Amodeo R, Dejana E, Koopman P, Cotelli F, Beltrame M. 2008. Sox18 and Sox7 play redundant roles in vascular development. Blood 111: 2657-2666.
12. Cha YR, Weinstein BM. 2007. Visualization and experimental analysis of blood vessel formation using transgenic zebrafish. Birth Defects Res C Embryo Today 81: 286-296.
13. Chappell JC, Taylor SM, Ferrara N, Bautch VL. 2009. Local guidance of emerging vessel sprouts requires soluble Flt-1. Dev Cell 17: 377-386.
14. Chen Z, Fisher RJ, Riggs CW, Rhim JS, Lautenberger JA. 1997. Inhibition of vascular endothelial growth factor-induced endothelial cell migration by ETS1 antisense oligonucleotides. Cancer Res 57: 2013-2019.
15. Childs S, Chen JN, Garrity DM, Fishman MC. 2002. Patterning of angiogenesis in the zebrafish embryo. Development 129: 973-982.
16. Cleaver O, Krieg PA. 1998. VEGF mediates angioblast migration during development of the dorsal aorta in Xenopus. Development 125: 3905-3914.
17. Cleaver O, Seufert DW, Krieg PA. 2000. Endoderm patterning by the notochord: Development of the hypochord in Xenopus. Development 127: 869-879.
18. Connell F, Kalidas K, Ostergaard P, Brice G, Homfray T, Roberts L, Bunyan DJ, Mitton S, Mansour S, Mortimer P, et al. 2010. Linkage and sequence analysis indicate that CCBE1 is mutated in recessively inherited generalised lymphatic dysplasia. Hum Genet 127: 231-241.
19. Covassin LD, Villefranc JA, Kacergis MC, Weinstein BM, Lawson ND. 2006. Distinct genetic interactions between multiple Vegf receptors are required for development of different blood vessel types in zebrafish. Proc Natl Acad Sci 103: 6554-6559.
20. Davis GE, Camarillo CW. 1996. An α2β1 integrin-dependent pinocytic mechanism involving intracellular vacuole formation and coalescence regulates capillary lumen and tube formation in three-dimensional collagen matrix. Exp Cell Res 224: 39-51.
21. Dejana E. 2004. Endothelial cell-cell junctions: Happy together. Nat Rev Mol Cell Biol 5: 261-270.
22. Desplantez T, Marics I, Jarry-Guichard T, Veteikis R, Briand JP, Weingart R, Gros D. 2003. Characterization of zebrafish Cx43. 4 connexin and its channels. Exp Physiol 88: 681-690.
23. Detrich HW 3rd., Kieran MW, Chan FY, Barone LM, Yee K, Rundstadler JA, PrattS, Ransom D, Zon LI. 1995. Intraembryonic hematopoietic cell migration during vertebrate development. Proc Natl Acad Sci 92: 10713-10717.
24. De Val S, Chi NC, Meadows SM, Minovitsky S, Anderson JP, Harris IS, EhlersML, Agarwal P, Visel A, Xu SM, et al. 2008. Combinatorial regulation of endothelial gene expression by ets and forkhead transcription factors. Cell 135: 1053-1064.
25. Drake CJ, Fleming PA. 2000. Vasculogenesis in the day 6. 5 to 9. 5 mouse embryo. Blood 95: 1671-1679.
26. Fadool JM, Dowling JE. 2008. Zebrafish: A model system for the study of eye genetics. Prog Retin Eye Res 27: 89-110.
27. Folkman J, Haudenschild C. 1980. Angiogenesis in vitro. Nature 288: 551-556.
28. Fouquet B, Weinstein BM, Serluca FC, Fishman MC. 1997. Vessel patterning in the embryo of the zebrafish: Guidance by notochord. Dev Biol 183: 37-48.
29. Francois M, Caprini A, Hosking B, Orsenigo F, Wilhelm D, Browne C, PaavonenK, Karnezis T, Shayan R, Downes M, et al. 2008. Sox18 induces development of the lymphatic vasculature in mice. Nature 456: 643-647.
30. Gerety SS, Anderson DJ. 2002. Cardiovascular ephrinB2 function is essential for embryonic angiogenesis. Development 129: 1397-1410.
31. Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, Abramsson A, Jeltsch M, Mitchell C, Alitalo K, Shima D, et al. 2003. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 161: 1163-1177.
32. Gitler AD, Lu MM, Epstein JA. 2004. PlexinD1 and semaphorin signaling are required in endothelial cells for cardiovascular development. Dev Cell 7: 107-116.
33. Gore AV, Lampugnani MG, Dye L, Dejana E, Weinstein BM. 2008. Combinatorial interaction between CCM pathway genes precipitates hemorrhagic stroke. Dis Model Mech 1: 275-281.
34. Gu C, Yoshida Y, Livet J, Reimert DV, Mann F, Merte J, Henderson CE, JessellTM, Kolodkin AL, Ginty DD. 2005. Semaphorin 3E and plexin-D1 control vascular pattern independently of neuropilins. Science 307: 265-268.
35. Haar JL, Ackerman GA. 1971. Ultrastructural changes in mouse yolk sac associated with the initiation of vitelline circulation. Anat Rec 170: 437-455.
36. Habeck H, Odenthal J, Walderich B, Maischein H, Schulte-Merker S. 2002. Analysis of a zebrafish VEGF receptor mutant reveals specific disruption of angiogenesis. Curr Biol 12: 1405-1412.
37. Hellstrom M, Phng LK, Hofmann JJ, Wallgard E, Coultas L, Lindblom P, Alva J, Nilsson AK, Karlsson L, Gaiano N, et al. 2007. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445: 776-780.
38. Herbert SP, Huisken J, Kim TN, Feldman ME, Houseman BT, Wang RA, ShokatKM, Stainier DY. 2009. Arterial-venous segregation by selective cell sprouting: An alternative mode of blood vessel formation. Science 326: 294-298.
39. Herpers R, van de Kamp E, Duckers HJ, Schulte-Merker S. 2008. Redundant roles for sox7 and sox18 in arteriovenous specification in zebrafish. Circ Res 102: 12-15.
40. Hogan BM, Bos FL, Bussmann J, Witte M, Chi NC, Duckers HJ, Schulte-MerkerS. 2009. Ccbe1 is required for embryonic lymphangiogenesis and venous sprouting. Nat Genet 41: 396-398.
41. Hong CC, Peterson QP, Hong JY, Peterson RT. 2006. Artery/vein specification is governed by opposing phosphatidylinositol-3 kinase and MAP kinase/ERK signaling. Curr Biol 16: 1366-1372.
42. Huber TL, Kouskoff V, Fehling HJ, Palis J, Keller G. 2004. Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature 432: 625-630.
43. Isogai S, Horiguchi M, Weinstein BM. 2001. The vascular anatomy of the developing zebrafish: An atlas of embryonic and early larval development. Dev Biol 230: 278-301.
44. Isogai S, Lawson ND, Torrealday S, Horiguchi M, Weinstein BM. 2003. Angiogenic network formation in the developing vertebrate trunk. Development 130: 5281-5290.
45. Isogai S, Hitomi J, Yaniv K, Weinstein BM. 2009. Zebrafish as a new animal model to study lymphangiogenesis. Anat Sci Int 84: 102-111.
46. Jeltsch M, Tammela T, Alitalo K, Wilting J. 2003. Genesis and pathogenesis of lymphatic vessels. Cell Tissue Res 314: 69-84.
47. Jin SW, Beis D, Mitchell T, Chen JN, Stainier DY. 2005. Cellular and molecular analyses of vascular tube and lumen formation in zebrafish. Development 132: 5199-5209.
48. Kabrun N, Buhring HJ, Choi K, Ullrich A, Risau W, Keller G. 1997. Flk-1 expression defines a population of early embryonic hematopoietic precursors. Development 124: 2039-2048.
49. Kamei M, Isogai S, Weinstein BM. 2004. Imaging blood vessels in the zebrafish. Methods Cell Biol 76: 51-74.
50. Kamei M, Saunders WB, Bayless KJ, Dye L, Davis GE, Weinstein BM. 2006. Endothelial tubes assemble from intracellular vacuoles in vivo. Nature 442: 453-456.
51. Karkkainen MJ, Haiko P, Sainio K, Partanen J, Taipale J, Petrova TV, Jeltsch M, Jackson DG, Talikka M, Rauvala H, et al. 2004. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat Immunol 5: 74-80.
52. Karpanen T, Alitalo K. 2008. Molecular biology and pathology of lymphangiogenesis. Annu Rev Pathol 3: 367-397.
53. Kimmel CB, Warga RM, Schilling TF. 1990. Origin and organization of the zebrafish fate map. Development 108: 581-594.
54. Kitambi SS, McCulloch KJ, Peterson RT, Malicki JJ. 2009. Small molecule screen for compounds that affect vascular development in the zebrafish retina. Mech Dev 126: 464-477.
55. Koh W, Mahan RD, Davis GE. 2008. Cdc42-and Rac1-mediated endothelial lumen formation requires Pak2, Pak4 and Par3, and PKC-dependent signaling. J Cell Sci 121: 989-1001.
56. Koh W, Sachidanandam K, Stratman AN, Sacharidou A, Mayo AM, Murphy EA, Cheresh DA, Davis GE. 2009. Formation of endothelial lumens requires a coordinated PKCepsilon-, Src-, Pak-and Raf-kinase-dependent signaling cascade downstream of Cdc42 activation. J Cell Sci 122: 1812-1822.
57. Kuchler AM, Gjini E, Peterson-Maduro J, Cancilla B, Wolburg H, Schulte-MerkerS. 2006. Development of the zebrafish lymphatic system requires VEGFC signaling. Curr Biol 16: 1244-1248.
58. Lamont RE, Lamont EJ, Childs SJ. 2009. Antagonistic interactions among Plexins regulate the timing of intersegmental vessel formation. Dev Biol 331: 199-209.
59. Larrivee B, Freitas C, Trombe M, Lv X, Delafarge B, Yuan L, Bouvree K, Breant C, Del Toro R, Brechot N, et al. 2007. Activation of the UNC5B receptor by Netrin-1 inhibits sprouting angiogenesis. Genes Dev 21: 2433-2447.
60. Lawson ND, Weinstein BM. 2002a. Arteries and veins: Making a difference with zebrafish. Nat Rev Genet 3: 674-682.
61. Lawson ND, Weinstein BM. 2002b. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol 248: 307-318.
62. Lawson ND, Scheer N, Pham VN, Kim CH, Chitnis AB, Campos-Ortega JA, Weinstein BM. 2001. Notch signaling is required for arterial-venous differentiation during embryonic vascular development. Development 128: 3675-3683.
63. Lawson ND, Vogel AM, Weinstein BM. 2002. Sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation. Dev Cell 3: 127-136.
64. Lawson ND, Mugford JW, Diamond BA, Weinstein BM. 2003. PPPhospholipase C γ-1 is required downstream of vascular endothelial growth factor during arterial development. Genes Dev 17: 1346-1351.
65. Lee HS, Han J, Bai HJ, Kim KW. 2009. Brain angiogenesis in developmental and pathological processes: Regulation, molecular and cellular communication at the neurovascular interface. FEBS J 276: 4622-4635.
66. Lelievre E, Lionneton F, Soncin F, Vandenbunder B. 2001. The Ets family contains transcriptional activators and repressors involved in angiogenesis. Int J Biochem Cell Biol 33: 391-407.
67. Lelievre E, Mattot V, Huber P, Vandenbunder B, Soncin F. 2000. ETS1 lowers capillary endothelial cell density at confluence and induces the expression of VE-cadherin. Oncogene 19: 2438-2446.
68. le Noble F, Klein C, Tintu A, Pries A, Buschmann I. 2008. Neural guidance molecules, tip cells, and mechanical factors in vascular development. Cardiovasc Res 78: 232-241.
69. Leslie JD, Ariza-McNaughton L, Bermange AL, McAdow R, Johnson SL, Lewis J. 2007. Endothelial signalling by the Notch ligand Delta-like 4 restricts angiogenesis. Development 134: 839-844.
70. Liu J, Fraser SD, Faloon PW, Rollins EL, Vom Berg J, Starovic-Subota O, Laliberte AL, Chen JN, Serluca FC, Childs SJ. 2007. A βPix Pak2a signaling pathway regulates cerebral vascular stability in zebrafish. Proc Natl Acad Sci 104: 13990-13995.
71. Lobov IB, Rao S, Carroll TJ, Vallance JE, Ito M, Ondr JK, Kurup S, Glass DA, PatelMS, Shu W, et al. 2005. WNT7b mediates macrophage-induced programmed cell death in patterning of the vasculature. Nature 437: 417-421.
72. Lu X, Le Noble F, Yuan L, Jiang Q, De Lafarge B, Sugiyama D, Breant C, Claes F, De Smet F, Thomas JL, et al. 2004. The netrin receptor UNC5B mediates guidance events controlling morphogenesis of the vascular system. Nature 432: 179-186.
73. Lubarsky B, Krasnow MA. 2003. Tube morphogenesis: Making and shaping biological tubes. Cell 112: 19-28.
74. Makinen T, Jussila L, Veikkola T, Karpanen T, Kettunen MI, Pulkkanen KJ, Kauppinen R, Jackson DG, Kubo H, Nishikawa S, et al. 2001. Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor-3. Nat Med 7: 199-205.
75. McKinney MC, Weinstein BM. 2008. Using the zebrafish to study vessel formation. Methods Enzymol 444: 65-97.
76. Meadows SM, Salanga MC, Krieg PA. 2009. Krüppel-like factor 2 cooperates with the ETS family protein ERG to activate Flk1 expression during vascular development. Development 136: 1115-1125.
77. Melani M, Weinstein BM. 2010. Common factors regulating patterning of the nervous and vascular systems. Annu Rev Cell Dev Biol 10: 639-665.
78. Montero-Balaguer M, Swirsding K, Orsenigo F, Cotelli F, Mione M, Dejana E. 2009. Stable vascular connections and remodeling require full expression of VE-cadherin in zebrafish embryos. PLoS One 4: e5772.
79. Moore MA, Owen JJ. 1965. Chromosome marker studies on the development of the haemopoietic system in the chick embryo. Nature 208: 956 passim.
80. Moyon D, Pardanaud L, Yuan L, Breant C, Eichmann A. 2001. Plasticity of endothelial cells during arterial-venous differentiation in the avian embryo. Development 128: 3359-3370.
81. Mukouyama YS, Shin D, Britsch S, Taniguchi M, Anderson DJ. 2002. Sensory nerves determine the pattern of arterial differentiation and blood vessel branching in the skin. Cell 109: 693-705.
82. Murray PDF. 1932. The development in vitro of the blood of the early chick embryo. Proc Roy Soc London B 111: 497-521.
83. Nakano T, Abe M, Tanaka K, Shineha R, Satomi S, Sato Y. 2000. Angiogenesis inhibition by transdominant mutant Ets-1. J Cell Physiol 184: 255-262.
84. Navankasattusas S, Whitehead KJ, Suli A, Sorensen LK, Lim AH, Zhao J, ParkKW, Wythe JD, Thomas KR, Chien CB, et al. 2008. The netrin receptor UNC5B promotes angiogenesis in specific vascular beds. Development 135: 659-667.
85. Ny A, Koch M, Schneider M, Neven E, Tong RT, Maity S, Fischer C, Plaisance S, Lambrechts D, Heligon C, et al. 2005. A genetic Xenopus laevis tadpole model to study lymphangiogenesis. Nat Med 11: 998-1004.
86. Oliver G. 2004. Lymphatic vasculature development. Nat Rev Immunol 4: 35-45.
87. Othman-Hassan K, Patel K, Papoutsi M, Rodriguez-Niedenfuhr M, Christ B, Wilting J. 2001. Arterial identity of endothelial cells is controlled by local cues. Dev Biol 237: 398-409.
88. Paik EJ, Zon LI. 2010. Hematopoietic development in the zebrafish. Int J Dev Biol 54: 1127-1137.
89. Parker LH, Schmidt M, Jin SW, Gray AM, Beis D, Pham T, Frantz G, Palmieri S, Hillan K, Stainier DY, et al. 2004. The endothelial-cell-derived secreted factor Egfl7 regulates vascular tube formation. Nature 428: 754-758.
90. Pendeville H, Winandy M, Manfroid I, Nivelles O, Motte P, Pasque V, Peers B, Struman I, Martial JA, Voz ML. 2008. Zebrafish Sox7 and Sox18 function together to control arterial-venous identity. Dev Biol 317: 405-416.
91. Pham VN, Lawson ND, Mugford JW, Dye L, Castranova D, Lo B, Weinstein BM. 2007. Combinatorial function of ETS transcription factors in the developing vasculature. Dev Biol 303: 772-783.
92. Pola R, Ling LE, Silver M, Corbley MJ, Kearney M, Blake Pepinsky R, Shapiro R, Taylor FR, Baker DP, Asahara T, et al. 2001. The morphogen Sonic hedgehog is an indirect angiogenic agent upregulating two families of angiogenic growth factors. Nat Med 7: 706-711.
93. Raz E, Mahabaleshwar H. 2009. Chemokine signaling in embryonic cell migration: A fisheye view. Development 136: 1223-1229.
94. Rodriguez F, Vacaru A, Overvoorde J, den Hertog J. 2008. The receptor protein-tyrosine phosphatase, Dep1, acts in arterial/venous cell fate decisions in zebrafish development. Dev Biol 324: 122-130.
95. Roman BL, Pham VN, Lawson ND, Kulik M, Childs S, Lekven AC, Garrity DM, Moon RT, Fishman MC, Lechleider RJ, et al. 2002. Disruption of acvrl1 increases endothelial cell number in zebrafish cranial vessels. Development 129: 3009-3019.
96. Sabin FR. 1920. Studies on the origin of blood-vessels and of red blood-corpuscles as seen in the living blastoderm of chicks during the second day of incubation. Contrib Embryol 9: 213-262.
97. Salanga MC, Meadows SM, Myers CT, Krieg PA. 2010. ETS family protein ETV2 is required for initiation of the endothelial lineage but not the hematopoietic lineage in the Xenopus embryo. Dev Dyn 239: 1178-1187.
98. Santoro MM, Samuel T, Mitchell T, Reed JC, Stainier DY. 2007. Birc2 (cIap1) regulates endothelial cell integrity and blood vessel homeostasis. Nat Genet 39: 1397-1402.
99. Siekmann AF, Lawson ND. 2007. Notch signalling limits angiogenic cell behaviour in developing zebrafish arteries. Nature 445: 781-784.
100. Siekmann AF, Standley C, Fogarty KE, Wolfe SA, Lawson ND. 2009. Chemokine signaling guides regional patterning of the first embryonic artery. Genes Dev 23: 2272-2277.
101. Srinivasan RS, Dillard ME, Lagutin OV, Lin FJ, Tsai S, Tsai MJ, Samokhvalov IM, Oliver G. 2007. Lineage tracing demonstrates the venous origin of the mammalian lymphatic vasculature. Genes Dev 21: 2422-2432.
102. Stainier DY, Weinstein BM, Detrich HW 3rd., Zon LI, Fishman MC. 1995. Cloche, an early acting zebrafish gene, is required by both the endothelial and hematopoietic lineages. Development 121: 3141-3150.
103. Strilic B, Kucera T, Eglinger J, Hughes MR, McNagny KM, Tsukita S, Dejana E, Ferrara N, Lammert E. 2009. The molecular basis of vascular lumen formation in the developing mouse aorta. Dev Cell 17: 505-515.
104. Suchting S, Freitas C, le Noble F, Benedito R, Breant C, Duarte A, Eichmann A. 2007. The Notch ligand Delta-like 4 negatively regulates endothelial tip cell formation and vessel branching. Proc Natl Acad Sci 104: 3225-3230.
105. Sumanas S, Gomez G, Zhao Y, Park C, Choi K, Lin S. 2008. Interplay among Etsrp/ER71, Scl, and Alk8 signaling controls endothelial and myeloid cell formation. Blood 111: 4500-4510.
106. Sumanas S, Lin S. 2006. Ets1-related protein is a key regulator of vasculogenesis in zebrafish. PLoS Biol 4: e10.
107. Sumoy L, Keasey JB, Dittman TD, Kimelman D. 1997. A role for notochord in axial vascular development revealed by analysis of phenotype and the expression of VEGR-2 in zebrafish flh and ntl mutant embryos. Mech Dev 63: 15-27.
108. Swift MR, Weinstein BM. 2009. Arterial-venous specification during development. Circ Res 104: 576-588.
109. Tammela T, Alitalo K. 2010. Lymphangiogenesis: Molecular mechanisms and future promise. Cell 140: 460-476.
110. Tammela T, Enholm B, Alitalo K, Paavonen K. 2005. The biology of vascular endothelial growth factors. Cardiovasc Res 65: 550-563.
111. Tammela T, Zarkada G, Wallgard E, Murtomaki A, Suchting S, Wirzenius M, Waltari M, Hellstrom M, Schomber T, Peltonen R, et al. 2008. Blocking VEGFR-3 suppresses angiogenic sprouting and vascular network formation. Nature 454: 656-660.
112. Thompson MA, Ransom DG, Pratt SJ, MacLennan H, Kieran MW, Detrich HW3rd., Vail B, Huber TL, Paw B, Brownlie AJ, et al. 1998. The cloche and spadetail genes differentially affect hematopoiesis and vasculogenesis. Dev Biol 197: 248-269.
113. Torres-Vazquez J, Gitler AD, Fraser SD, Berk JD, Van NP, Fishman MC, ChildsS, Epstein JA, Weinstein BM. 2004. Semaphorin-plexin signaling guides patterning of the developing vasculature. Dev Cell 7: 117-123.
114. Visconti RP, Richardson CD, Sato TN. 2002. Orchestration of angiogenesis and arteriovenous contribution by angiopoietins and vascular endothelial growth factor (VEGF). Proc Natl Acad Sci 99: 8219-8224.
115. Vogeli KM, Jin SW, Martin GR, Stainier DY. 2006. A common progenitor for haematopoietic and endothelial lineages in the zebrafish gastrula. Nature 443: 337-339.
116. Vokes SA, Krieg PA. 2002. Endoderm is required for vascular endothelial tube formation, but not for angioblast specification. Development 129: 775-785.
117. Vokes SA, Yatskievych TA, Heimark RL, McMahon J, McMahon AP, Antin PB, Krieg PA. 2004. Hedgehog signaling is essential for endothelial tube formation during vasculogenesis. Development 131: 4371-4380.
118. Wakiya K, Begue A, Stehelin D, Shibuya M. 1996. A cAMP response element and an Ets motif are involved in the transcriptional regulation of flt-1 tyrosine kinase (vascular endothelial growth factor receptor 1) gene. J Biol Chem 271: 30823-30828.
119. Wang Y, Nakayama M, Pitulescu ME, Schmidt TS, Bochenek ML, Sakakibara A, Adams S, Davy A, Deutsch U, Luthi U, et al. 1998. Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature 465: 483-486.
120. Wang Y, Kaiser MS, Larson JD, Nasevicius A, Clark KJ, Wadman SA, Roberg-Perez SE, Ekker SC, Hackett PB, McGrail M, et al. 2010. Moesin1 and Ve-cadherin are required in endothelial cells during in vivo tubulogenesis. Development 137: 3119-3128.
121. Weinstein B. 2002. Vascular cell biology in vivo: a new piscine paradigm?. Trends Cell Biol 12: 439-445.
122. Weinstein BM, Stemple DL, Driever W, Fishman MC. 1995. Gridlock, a localized heritable vascular patterning defect in the zebrafish. Nat Med 1: 1143-1147.
123. Wigle JT, Oliver G. 1999. Prox1 function is required for the development of the murine lymphatic system. Cell 98: 769-778.
124. Wilting J, Papoutsi M, Schneider M, Christ B. 2000. The lymphatic endothelium of the avian wing is of somitic origin. Dev Dyn 217: 271-278.
125. Wilting J, Aref Y, Huang R, Tomarev SI, Schweigerer L, Christ B, Valasek P, Papoutsi M. 2006. Dual origin of avian lymphatics. Dev Biol 292: 165-173.
126. Yang Y, Zou L, Wang Y, Xu KS, Zhang JX, Zhang JH. 2007. Axon guidance cue Netrin-1 has dual function in angiogenesis. Cancer Biol Ther 6: 743-748.
127. Yaniv K, Isogai S, Castranova D, Dye L, Hitomi J, Weinstein BM. 2006. Live imaging of lymphatic development in the zebrafish. Nat Med 12: 711-716.
128. You LR, Lin FJ, Lee CT, DeMayo FJ, Tsai MJ, Tsai SY. 2005. Suppression of Notch signalling by the COUP-TFII transcription factor regulates vein identity. Nature 435: 98-104.