Abstract
Blood vessels form de novo (vasculogenesis) or upon sprouting of capillaries from preexisting vessels (angiogenesis). With high-resolution imaging of zebrafish vascular development, we uncovered a third mode of blood vessel formation whereby the first embryonic artery and vein, two unconnected blood vessels, arise from a common precursor vessel. The first embryonic vein formed by selective sprouting of progenitor cells from the precursor vessel, followed by vessel segregation. These processes were regulated by the ligand EphrinB2 and its receptor EphB4, which are expressed in arterial-fated and venous-fated progenitors, respectively, and interact to orient the direction of progenitor migration. Thus, directional control of progenitor migration drives arterial-venous segregation and generation of separate parallel vessels from a single precursor vessel, a process essential for vascular development.
MeSH Terms
Animals
Animals, Genetically Modified
Aorta/cytology,embryology
Arteries/cytology,embryology
Cell Movement
Endothelial Cells/cytology,physiology
Ephrin-B2/metabolism
Morphogenesis
Phosphatidylinositol 3-Kinases/metabolism
Receptor, EphB4/metabolism
Receptors, Notch/metabolism
Signal Transduction
Stem Cells/cytology,physiology
Vascular Endothelial Growth Factor A/metabolism
Vascular Endothelial Growth Factor Receptor-2/metabolism
Vascular Endothelial Growth Factor Receptor-3/metabolism
Veins/cytology,embryology
Zebrafish
Zebrafish Proteins/metabolism
Chemicals
Ephrin-B2
Receptors, Notch
Vascular Endothelial Growth Factor A
Zebrafish Proteins
Phosphatidylinositol 3-Kinases
Receptor, EphB4
Vascular Endothelial Growth Factor Receptor-2
Vascular Endothelial Growth Factor Receptor-3
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Herbert Shane P
Department of Biochemistry and Biophysics, Programs in Developmental Biology, Genetics and Human Genetics, Cardiovascular Research Institute, University of California, San Francisco, CA 94158, USA.
Huisken Jan
Kim Tyson N
Feldman Morri E
Houseman Benjamin T
Wang Rong A
Shokat Kevan M
Stainier Didier Y R
References (26)
26 references, click to expand
-
The cytoplasmic domain of the ligand ephrinB2 is required for vascular morphogenesis but not cranial neural crest migration.
Cell. 2001 Jan 12;104(1):57-69
PMID: 11163240
-
Genetic single-cell mosaic analysis implicates ephrinB2 reverse signaling in projections from the posterior tectum to the hindbrain in zebrafish.
J Neurosci. 2007 May 16;27(20):5271-9
PMID: 17507550
-
Gridlock signalling pathway fashions the first embryonic artery.
Nature. 2001 Nov 8;414(6860):216-20
PMID: 11700560
-
Hedgehog signaling is required for adult blood stem cell formation in zebrafish embryos.
Dev Cell. 2005 Mar;8(3):389-400
PMID: 15737934
-
Angiogenesis selectively requires the p110alpha isoform of PI3K to control endothelial cell migration.
Nature. 2008 May 29;453(7195):662-6
PMID: 18449193
-
Notch signalling limits angiogenic cell behaviour in developing zebrafish arteries.
Nature. 2007 Feb 15;445(7129):781-4
PMID: 17259972
-
Sox18 and Sox7 play redundant roles in vascular development.
Blood. 2008 Mar 1;111(5):2657-66
PMID: 18094332
-
Cardiac troponin T is essential in sarcomere assembly and cardiac contractility.
Nat Genet. 2002 May;31(1):106-10
PMID: 11967535
-
Artery and vein formation: a tug of war between different forces.
EMBO Rep. 2007 Oct;8(10):920-4
PMID: 17906673
-
Endothelial signalling by the Notch ligand Delta-like 4 restricts angiogenesis.
Development. 2007 Mar;134(5):839-44
PMID: 17251261
-
Optical sectioning deep inside live embryos by selective plane illumination microscopy.
Science. 2004 Aug 13;305(5686):1007-9
PMID: 15310904
-
Ephrin-B2 controls cell motility and adhesion during blood-vessel-wall assembly.
Cell. 2006 Jan 13;124(1):161-73
PMID: 16413489
-
The endothelial-cell-derived secreted factor Egfl7 regulates vascular tube formation.
Nature. 2004 Apr 15;428(6984):754-8
PMID: 15085134
-
Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis.
Nature. 2007 Feb 15;445(7129):776-80
PMID: 17259973
-
Proliferative defect and embryonic lethality in mice homozygous for a deletion in the p110alpha subunit of phosphoinositide 3-kinase.
J Biol Chem. 1999 Apr 16;274(16):10963-8
PMID: 10196176
-
Transplantation and in vivo imaging of multilineage engraftment in zebrafish bloodless mutants.
Nat Immunol. 2003 Dec;4(12):1238-46
PMID: 14608381
-
Zebrafish Sox7 and Sox18 function together to control arterial-venous identity.
Dev Biol. 2008 May 15;317(2):405-16
PMID: 18377889
-
SHIP prevents lipopolysaccharide from triggering an antiviral response in mice.
Blood. 2009 Mar 26;113(13):2945-54
PMID: 19139077
-
phospholipase C gamma-1 is required downstream of vascular endothelial growth factor during arterial development.
Genes Dev. 2003 Jun 1;17(11):1346-51
PMID: 12782653
-
Cellular and molecular analyses of vascular tube and lumen formation in zebrafish.
Development. 2005 Dec;132(23):5199-209
PMID: 16251212
-
A pharmacological map of the PI3-K family defines a role for p110alpha in insulin signaling.
Cell. 2006 May 19;125(4):733-47
PMID: 16647110
-
Increased insulin sensitivity in mice lacking p85beta subunit of phosphoinositide 3-kinase.
Proc Natl Acad Sci U S A. 2002 Jan 8;99(1):419-24
PMID: 11752399
-
Artery and vein size is balanced by Notch and ephrin B2/EphB4 during angiogenesis.
Development. 2008 Nov;135(22):3755-64
PMID: 18952909
-
Roles of ephrinB ligands and EphB receptors in cardiovascular development: demarcation of arterial/venous domains, vascular morphogenesis, and sprouting angiogenesis.
Genes Dev. 1999 Feb 1;13(3):295-306
PMID: 9990854
-
Molecular regulation of angiogenesis and lymphangiogenesis.
Nat Rev Mol Cell Biol. 2007 Jun;8(6):464-78
PMID: 17522591
-
sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation.
Dev Cell. 2002 Jul;3(1):127-36
PMID: 12110173