Skip to main content

Vascular Development in the Zebrafish

  • Chapter
  • First Online:
Endothelial Signaling in Development and Disease

Abstract

One of the earliest processes during vertebrate development is the formation of the cardiovascular system. This highly complex system of differently sized tubes permits circulation of blood while enabling the exchange of oxygen and nutrients in all perfused tissues. Recent studies in zebrafish have provided additional insight into the initial establishment of the vasculature, particularly the process of vasculogenesis. During vasculogenesis, angioblasts exhibit a complex migratory behavior before they differentiate into endothelial cells and form a primitive vascular network. In addition to migrating to specific locations, endothelial precursor cells also need to be specified to take on arterial and venous fates. In particular, the interdependence between the spatial and temporal localization of early angioblasts and their arterial-venous specification has gained some interest and is one focus of this review. Furthermore, we discuss the complex network of genetic interactions that play a role in arterial-venous specification.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

DA:

Dorsal aorta

DLAV:

Dorsal longitudinal anastomotic vessel

HLT:

Hypotrichosis-lymphedema-telangiectasia

HMG:

High-mobility group

HPF:

Hours post-fertilization

ISV:

Intersegmental vessels

LDA:

Lateral dorsal aorta

LPM:

Lateral plate mesoderm

MO:

Morpholino

NICD:

Notch intracellular domain

PCV:

Posterior cardinal vein

PHBC:

Primordial hindbrain channel

TAD:

Transactivation domain

References

  1. 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(3):295–306.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  2. Alexander J, Stainier DY. A molecular pathway leading to endoderm formation in zebrafish. Curr Biol. 1999;9(20):1147–57.

    Article  CAS  PubMed  Google Scholar 

  3. Bahary N, Goishi K, Stuckenholz C, Weber G, Leblanc J, Schafer CA, Berman SS, Klagsbrun M, Zon LI. Duplicate VegfA genes and orthologues of the KDR receptor tyrosine kinase family mediate vascular development in the zebrafish. Blood. 2007;110(10):3627–36.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  4. Bowles J, Schepers G, Koopman P. Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev Biol. 2000;227(2):239–55.

    Article  CAS  PubMed  Google Scholar 

  5. Bruckner K, Pasquale EB, Klein R. Tyrosine phosphorylation of transmembrane ligands for Eph receptors. Science. 1997;275(5306):1640–3.

    Article  CAS  PubMed  Google Scholar 

  6. Bussmann J, Lawson N, Zon L, Schulte-Merker S. Zebrafish VEGF receptors: a guideline to nomenclature. PLoS Genet. 2008;4(5):e1000064.

    Article  PubMed Central  PubMed  Google Scholar 

  7. Bussmann J, Wolfe SA, Siekmann AF. Arterial-venous network formation during brain vascularization involves hemodynamic regulation of chemokine signaling. Development. 2011;138(9):1717–26.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  8. Cermenati S, Moleri S, Cimbro S, Corti P, Del Giacco L, Amodeo R, Dejana E, Koopman P, Cotelli F, Beltrame M. Sox18 and Sox7 play redundant roles in vascular development. Blood. 2008;111(5):2657–66.

    Article  CAS  PubMed  Google Scholar 

  9. Chew LJ, Gallo V. The Yin and Yang of Sox proteins: activation and repression in development and disease. J Neurosci Res. 2009;87(15):3277–87.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. Chun CZ, Remadevi I, Schupp MO, Samant GV, Pramanik K, Wilkinson GA, Ramchandran R. Fli+ etsrp+ hemato-vascular progenitor cells proliferate at the lateral plate mesoderm during vasculogenesis in zebrafish. PLoS One. 2011;6(2):e14732.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  11. Chung MI, Ma AC, Fung TK, Leung AY. Characterization of Sry-related HMG box group F genes in zebrafish hematopoiesis. Exp Hematol. 2011;39(10):986–998.e5.

    Article  CAS  PubMed  Google Scholar 

  12. Corada M, Orsenigo F, Morini MF, Pitulescu ME, Bhat G, Nyqvist D, Breviario F, Conti V, Briot A, Iruela-Arispe ML, et al. Sox17 is indispensable for acquisition and maintenance of arterial identity. Nat Commun. 2013;4:2609.

    Article  PubMed Central  PubMed  Google Scholar 

  13. De Val S, Chi NC, Meadows SM, Minovitsky S, Anderson JP, Harris IS, Ehlers ML, Agarwal P, Visel A, Xu SM, et al. Combinatorial regulation of endothelial gene expression by ets and forkhead transcription factors. Cell. 2008;135(6):1053–64.

    Article  PubMed Central  PubMed  Google Scholar 

  14. de Vries C, Escobedo JA, Ueno H, Houck K, Ferrara N, Williams LT. The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science. 1992;255(5047):989–91.

    Article  PubMed  Google Scholar 

  15. Downes M, Francois M, Ferguson C, Parton RG, Koopman P. Vascular defects in a mouse model of hypotrichosis-lymphedema-telangiectasia syndrome indicate a role for SOX18 in blood vessel maturation. Hum Mol Genet. 2009;18(15):2839–50.

    Article  CAS  PubMed  Google Scholar 

  16. Ekker SC, Ungar AR, Greenstein P, von Kessler DP, Porter JA, Moon RT, Beachy PA. Patterning activities of vertebrate hedgehog proteins in the developing eye and brain. Curr Biol. 1995;5(8):944–55.

    Article  CAS  PubMed  Google Scholar 

  17. Fouquet B, Weinstein BM, Serluca FC, Fishman MC. Vessel patterning in the embryo of the zebrafish: guidance by notochord. Dev Biol. 1997;183(1):37–48.

    Article  CAS  PubMed  Google Scholar 

  18. Francois M, Caprini A, Hosking B, Orsenigo F, Wilhelm D, Browne C, Paavonen K, Karnezis T, Shayan R, Downes M, et al. Sox18 induces development of the lymphatic vasculature in mice. Nature. 2008;456(7222):643–7.

    Article  CAS  PubMed  Google Scholar 

  19. Gale NW, Holland SJ, Valenzuela DM, Flenniken A, Pan L, Ryan TE, Henkemeyer M, Strebhardt K, Hirai H, Wilkinson DG, et al. Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis. Neuron. 1996;17(1):9–19.

    Article  CAS  PubMed  Google Scholar 

  20. 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(3):403–14.

    Article  CAS  PubMed  Google Scholar 

  21. Gering M., Patient, R. Hedgehog signaling is required for adult blood stem cell formation in zebrafish embryos. Dev Cell. 2005;8(3):389–400.

    Article  CAS  PubMed  Google Scholar 

  22. Gonzalez-Crussi F. Vasculogenesis in the chick embryo. An ultrastructural study. Am J Anat. 1971;130(4):441–60.

    Article  CAS  PubMed  Google Scholar 

  23. Habeck H, Odenthal J, Walderich B, Maischein H, Schulte-Merker S. Analysis of a zebrafish VEGF receptor mutant reveals specific disruption of angiogenesis. Curr Biol. 2002;12(16):1405–12.

    Article  CAS  PubMed  Google Scholar 

  24. Hagerling R, Pollmann C, Andreas M, Schmidt C, Nurmi H, Adams RH, Alitalo K, Andresen V, Schulte-Merker S, Kiefer F. A novel multistep mechanism for initial lymphangiogenesis in mouse embryos based on ultramicroscopy. EMBO J. 2013;32(5):629–44.

    Article  PubMed Central  PubMed  Google Scholar 

  25. 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(6):e2401.

    Article  PubMed Central  PubMed  Google Scholar 

  26. Herbert SP, Huisken J, Kim TN, Feldman ME, Houseman BT, Wang RA, Shokat KM, Stainier DY. Arterial-venous segregation by selective cell sprouting: an alternative mode of blood vessel formation. Science. 2009;326(5950):294–8..

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Hermkens DMA, Impel A, Urasaki A, Bussmann J, Duckers HJ, Schulte-Merker S. Sox7 controls arterial specification in conjunction with hey2 and efnb2 function. Development. 2015;142(9):1695–704.

    Article  CAS  PubMed  Google Scholar 

  28. Herpers R, van de Kamp E, Duckers HJ, Schulte-Merker S. Redundant roles for sox7 and sox18 in arteriovenous specification in zebrafish. Circ Res. 2008;102(1):12–5.

    Article  CAS  PubMed  Google Scholar 

  29. Hogan BM, Bos FL, Bussmann J, Witte M, Chi NC, Duckers HJ, Schulte-Merker S. Ccbe1 is required for embryonic lymphangiogenesis and venous sprouting. Nat Genet. 2009a;41(4):396–8.

    Article  CAS  PubMed  Google Scholar 

  30. Hogan BM, Herpers R, Witte M, Helotera H, Alitalo K, Duckers HJ, Schulte-Merker S. Vegfc/Flt4 signalling is suppressed by Dll4 in developing zebrafish intersegmental arteries. Development. 2009;136(23):4001–9.

    Article  CAS  PubMed  Google Scholar 

  31. Irrthum A, Devriendt K, Chitayat D, Matthijs G, Glade C, Steijlen PM, Fryns JP, Van Steensel MA, Vikkula M. Mutations in the transcription factor gene SOX18 underlie recessive and dominant forms of hypotrichosis-lymphedema-telangiectasia. Am J Hum Genet. 2003;72(6):1470–8.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. Isogai S, Lawson ND, Torrealday S, Horiguchi M, Weinstein BM. Angiogenic network formation in the developing vertebrate trunk. Development. 2003;130(21):5281–90.

    Article  CAS  PubMed  Google Scholar 

  33. James K, Hosking B, Gardner J, Muscat GE, Koopman P. Sox18 mutations in the ragged mouse alleles ragged-like and opossum. Genesis. 2003;36(1):1–6.

    Article  CAS  PubMed  Google Scholar 

  34. Jin SW, Beis D, Mitchell T, Chen JN, Stainier DY. Cellular and molecular analyses of vascular tube and lumen formation in zebrafish. Development. 2005;132(23):5199–209.

    Article  CAS  PubMed  Google Scholar 

  35. Kanai-Azuma M, Kanai Y, Gad JM, Tajima Y, Taya C, Kurohmaru M, Sanai Y, Yonekawa H, Yazaki K, Tam PP, et al. Depletion of definitive gut endoderm in Sox17-null mutant mice. Development. 2002;129(10):2367–79.

    CAS  PubMed  Google Scholar 

  36. Kao HY, Ordentlich P, Koyano-Nakagawa N, Tang Z, Downes M, Kintner CR, Evans RM, Kadesch T. A histone deacetylase corepressor complex regulates the Notch signal transduction pathway. Genes Dev. 1998;12(15):2269–77.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  37. Kim I, Saunders TL, Morrison SJ. Sox17 dependence distinguishes the transcriptional regulation of fetal from adult hematopoietic stem cells. Cell. 2007;130(3):470–83.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Kim SH, Schmitt CE, Woolls MJ, Holland MB, Kim JD, Jin SW. Vascular endothelial growth factor signaling regulates the segregation of artery and vein via ERK activity during vascular development. Biochem Biophys Res Commun. 2013;430(4):1212–6.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. Kohli V, Schumacher JA, Desai SP, Rehn K, Sumanas S. Arterial and venous progenitors of the major axial vessels originate at distinct locations. Dev Cell. 2013;25(2):196–206.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  40. Kok FO, Shin M, Ni CW, Gupta A, Grosse AS, van Impel A, Kirchmaier BC, Peterson-Maduro J, Kourkoulis G, Male I, et al. Reverse genetic screening reveals poor correlation between morpholino-induced and mutant phenotypes in zebrafish. Dev Cell. 2015;32(1):97–108.

    Article  CAS  PubMed  Google Scholar 

  41. Kullander K, Klein R. Mechanisms and functions of Eph and ephrin signalling. Nat Rev Mol Cell Biol. 2002;3(7):475–86.

    Article  CAS  PubMed  Google Scholar 

  42. Kume T, Jiang H, Topczewska JM, Hogan BL. The murine winged helix transcription factors, Foxc1 and Foxc2, are both required for cardiovascular development and somitogenesis. Genes Dev. 2001;15(18):2470–82.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  43. Lawson ND, Weinstein BM. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol. 2002;248(2):307–18.

    Article  CAS  PubMed  Google Scholar 

  44. 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(19):3675–83.

    CAS  PubMed  Google Scholar 

  45. 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(1):127–36.

    Article  CAS  PubMed  Google Scholar 

  46. Lawson ND, Mugford JW, Diamond BA, Weinstein BM. Phospholipase C gamma-1 is required downstream of vascular endothelial growth factor during arterial development. Genes Dev. 2003;17(11):1346–51.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  47. Lee P, Goishi K, Davidson AJ, Mannix R, Zon L, Klagsbrun M. Neuropilin-1 is required for vascular development and is a mediator of VEGF-dependent angiogenesis in zebrafish. Proc Natl Acad Sci U S A. 2002;99(16):10470–5.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  48. Lewis KE, Concordet JP, Ingham PW. Characterisation of a second patched gene in the zebrafish Danio rerio and the differential response of patched genes to Hedgehog signalling. Dev Biol. 1999;208(1):14–29.

    Article  CAS  PubMed  Google Scholar 

  49. Liang D, Xu X, Chin AJ, Balasubramaniyan NV, Teo MA, Lam TJ, Weinberg ES, Ge R. Cloning and characterization of vascular endothelial growth factor (VEGF) from zebrafish, Danio rerio. Biochim Biophys Acta. 1998;1397(1):14–20.

    Article  CAS  PubMed  Google Scholar 

  50. Lohela M, Bry M, Tammela T, Alitalo K. VEGFs and receptors involved in angiogenesis versus lymphangiogenesis. Curr Opin Cell Biol. 2009;21(2):154–65.

    Article  CAS  PubMed  Google Scholar 

  51. Martyn U, Schulte-Merker S. The ventralized ogon mutant phenotype is caused by a mutation in the zebrafish homologue of Sizzled, a secreted Frizzled-related protein. Dev Biol. 2003;260(1):58–67.

    Article  CAS  PubMed  Google Scholar 

  52. Nakagawa O, McFadden DG, Nakagawa M, Yanagisawa H, Hu T, Srivastava D, Olson EN. Members of the HRT family of basic helix-loop-helix proteins act as transcriptional repressors downstream of Notch signaling. Proc Natl Acad Sci U S A. 2000;97(25):13655–60.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  53. Nasevicius A, Larson J, Ekker SC. Distinct requirements for zebrafish angiogenesis revealed by a VEGF-A morphant. Yeast. 2000;17(4):294–301.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  54. Nicoli S, Tobia C, Gualandi L, De Sena G, Presta M. Calcitonin receptor-like receptor guides arterial differentiation in zebrafish. Blood. 2008;111(10):4965–72.

    Article  CAS  PubMed  Google Scholar 

  55. Pendeville H, Winandy M, Manfroid I, Nivelles O, Motte P, Pasque V, Peers B, Struman I, Martial JA, Voz ML. Zebrafish Sox7 and Sox18 function together to control arterial-venous identity. Dev Biol. 2008;317(2):405–16.

    Article  CAS  PubMed  Google Scholar 

  56. Pennisi D, Gardner J, Chambers D, Hosking B, Peters J, Muscat G, Abbott C, Koopman P. Mutations in Sox18 underlie cardiovascular and hair follicle defects in ragged mice. Nat Genet. 2000;24(4):434–7.

    Article  CAS  PubMed  Google Scholar 

  57. Peterson RT, Shaw SY, Peterson TA, Milan DJ, Zhong TP, Schreiber SL, MacRae CA, Fishman MC. Chemical suppression of a genetic mutation in a zebrafish model of aortic coarctation. Nat Biotechnol. 2004;22(5):595–9.

    Article  CAS  PubMed  Google Scholar 

  58. Pham VN, Lawson ND, Mugford JW, Dye L, Castranova D, Lo B, Weinstein BM. Combinatorial function of ETS transcription factors in the developing vasculature. Dev Biol. 2007;303(2):772–83.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  59. Phng LK, Gerhardt H. Angiogenesis: a team effort coordinated by notch. Dev Cell. 2009;16(2):196–208.

    Article  CAS  PubMed  Google Scholar 

  60. Poole TJ, Coffin JD. Vasculogenesis and angiogenesis: two distinct morphogenetic mechanisms establish embryonic vascular pattern. J Exp Zool. 1989;251(2):224–31.

    Article  CAS  PubMed  Google Scholar 

  61. Risau W, Flamme I. Vasculogenesis. Annu Rev Cell Dev Biol. 1995;11:73–91.

    Article  CAS  PubMed  Google Scholar 

  62. Rowlinson JM, Gering M. Hey2 acts upstream of Notch in hematopoietic stem cell specification in zebrafish embryos. Blood. 2010;116(12):2046–56.

    Article  CAS  PubMed  Google Scholar 

  63. 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. 1917. J Hematother Stem Cell Res. 2002;11(1):5–7.

    Article  PubMed  Google Scholar 

  64. Sacilotto N, Monteiro R, Fritzsche M, Becker PW, Sanchez-Del-Campo L, Liu K, Pinheiro P, Ratnayaka I, Davies B, Goding CR, et al. Analysis of Dll4 regulation reveals a combinatorial role for Sox and Notch in arterial development. Proc Natl Acad Sci U S A. 2013;110(29):11893–8.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  65. Schuermann A, Helker CS, Herzog W. Angiogenesis in zebrafish. Semin Cell Dev Biol. 2014;31C:106–14.

    Article  Google Scholar 

  66. Schulte-Merker S, Stainier DY. Out with the old, in with the new: reassessing morpholino knockdowns in light of genome editing technology. Development. 2014;141(16):3103–4.

    Article  CAS  PubMed  Google Scholar 

  67. 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(2):458–70.

    Article  CAS  PubMed  Google Scholar 

  68. Shibuya M. Vascular endothelial growth factor and its receptor system: physiological functions in angiogenesis and pathological roles in various diseases. J Biochem. 2013;153(1):13–9.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  69. Shoji W, Isogai S, Sato-Maeda M, Obinata M, Kuwada JY. Semaphorin3a1 regulates angioblast migration and vascular development in zebrafish embryos. Development. 2003;130(14):3227–36.

    Article  CAS  PubMed  Google Scholar 

  70. Siekmann AF, Standley C, Fogarty KE, Wolfe SA, Lawson ND. Chemokine signaling guides regional patterning of the first embryonic artery. Genes Dev. 2009;23(19):2272–7.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  71. Srinivasan RS, Geng X, Yang Y, Wang Y, Mukatira S, Studer M, Porto MP, Lagutin O, Oliver G. The nuclear hormone receptor Coup-TFII is required for the initiation and early maintenance of Prox1 expression in lymphatic endothelial cells. Genes Dev. 2010;24(7):696–707.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  72. 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(10):3141–50.

    CAS  PubMed  Google Scholar 

  73. Stainier DY, Fouquet B, Chen JN, Warren KS, Weinstein BM, Meiler SE, Mohideen MA, Neuhauss SC, Solnica-Krezel L, Schier AF, et al. Mutations affecting the formation and function of the cardiovascular system in the zebrafish embryo. Development. 1996;123:285–92.

    CAS  PubMed  Google Scholar 

  74. Sumanas S, Lin S. Ets1-related protein is a key regulator of vasculogenesis in zebrafish. PLoS Biol. 2006;4(1):e10.

    Article  PubMed Central  PubMed  Google Scholar 

  75. Terman BI, Carrion ME, Kovacs E, Rasmussen BA, Eddy RL, Shows TB. Identification of a new endothelial cell growth factor receptor tyrosine kinase. Oncogene. 1991;6(9):1677–83.

    CAS  PubMed  Google Scholar 

  76. Thompson MA, Ransom DG, Pratt SJ, MacLennan H, Kieran MW, Detrich HW 3rd, Vail B, Huber TL, Paw B, Brownlie AJ, et al. The cloche and spadetail genes differentially affect hematopoiesis and vasculogenesis. Dev Biol. 1998;197(2):248–69.

    Article  CAS  PubMed  Google Scholar 

  77. van Impel A, Schulte-Merker S. A fisheye view on lymphangiogenesis. Adv Anat Embryol Cell Biol. 2014;214:153–65.

    Article  PubMed  Google Scholar 

  78. van Impel A, Zhao Z, Hermkens DM, Roukens MG, Fischer JC, Peterson-Maduro J, Duckers H, Ober EA, Ingham PW, Schulte-Merker S. Divergence of zebrafish and mouse lymphatic cell fate specification pathways. Development. 2014;141(6):1228–38.

    Article  PubMed Central  PubMed  Google Scholar 

  79. Villa N, Walker L, Lindsell CE, Gasson J, Iruela-Arispe ML, Weinmaster G. Vascular expression of Notch pathway receptors and ligands is restricted to arterial vessels. Mech Dev. 2001;108(1–2):161–4.

    Article  CAS  PubMed  Google Scholar 

  80. Vogeli KM, Jin SW, Martin GR, Stainier DY. A common progenitor for haematopoietic and endothelial lineages in the zebrafish gastrula. Nature. 2006;443(7109):337–9.

    Article  CAS  PubMed  Google Scholar 

  81. 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(5):741–53.

    Article  CAS  PubMed  Google Scholar 

  82. Wat MJ, Beck TF, Hernandez-Garcia A, Yu Z, Veenma D, Garcia M, Holder AM, Wat JJ, Chen Y, Mohila CA, et al. Mouse model reveals the role of SOX7 in the development of congenital diaphragmatic hernia associated with recurrent deletions of 8p23.1. Hum Mol Genet. 2012;21(18):4115–25.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  83. Weinstein BM, Stemple DL, Driever W, Fishman MC. Gridlock, a localized heritable vascular patterning defect in the zebrafish. Nat Med. 1995;1(11):1143–7.

    Article  CAS  PubMed  Google Scholar 

  84. Wilkinson RN, van Eeden FJ. The zebrafish as a model of vascular development and disease. Prog Mol Biol Transl Sci. 2014;124:93–122.

    Article  CAS  PubMed  Google Scholar 

  85. Wilkinson RN, Koudijs MJ, Patient RK, Ingham PW, Schulte-Merker S, van Eeden FJ. Hedgehog signaling via a calcitonin receptor-like receptor can induce arterial differentiation independently of VEGF signaling in zebrafish. Blood. 2012;120(2):477–88.

    Article  CAS  PubMed  Google Scholar 

  86. Xiong JW, Yu Q, Zhang J, Mably JD. An acyltransferase controls the generation of hematopoietic and endothelial lineages in zebrafish. Circ Res. 2008;102(9):1057–64.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  87. Zhong TP, Rosenberg M, Mohideen MA, Weinstein B, Fishman MC. Gridlock, an HLH gene required for assembly of the aorta in zebrafish. Science. 2000;287(5459):1820–4.

    Article  CAS  PubMed  Google Scholar 

  88. Zhong TP, Childs S, Leu JP, Fishman MC. Gridlock signalling pathway fashions the first embryonic artery. Nature. 2001;414(6860):216–20.

    Article  CAS  PubMed  Google Scholar 

  89. Zon LI. Developmental biology of hematopoiesis. Blood. 1995;86(8):2876–91.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stefan Schulte-Merker PhD .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Science+Business Media New York

About this chapter

Cite this chapter

Hermkens, D., Duckers, H., Schulte-Merker, S. (2015). Vascular Development in the Zebrafish. In: Schmidt, M., Liebner, S. (eds) Endothelial Signaling in Development and Disease. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-2907-8_2

Download citation

Publish with us

Policies and ethics