Home LiteratureArticle Details
PMID: 16617120 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Distinct genetic interactions between multiple Vegf receptors are required for development of different blood vessel types in zebrafish.

Covassin LD, Villefranc JA, Kacergis MC, Weinstein BM, Lawson ND

Abstract

Recent evidence indicates a specific role for vascular endothelial growth factor a (Vegfa) during artery development in both zebrafish and mouse embryos, whereas less is known about signals that govern vein formation. In zebrafish, loss of vegfa blocks segmental artery formation and reduces artery-specific gene expression, whereas veins are largely unaffected. Here, we describe a mutation in the zebrafish vegf receptor-2 homolog, kdra, which eliminates its kinase activity and leads to specific defects in artery development. We further find that Flt4, a receptor for Vegfc, cooperates with Kdr during artery morphogenesis, but not differentiation. We also identify an additional zebrafish vegfr-2 ortholog, referred to as kdrb, which can partially compensate for loss of kdra but is dispensable for vascular development in wild-type embryos. Interestingly, we find that these Vegf receptors are also required for formation of veins but in distinct genetic interactions that differ from those required for artery development. Taken together, our results indicate that formation of arteries and veins in the embryo is governed in part by different Vegf receptor combinations and suggest a genetic mechanism for generating blood vessel diversity during vertebrate development.

MeSH Terms
Animals Base Sequence Blood Vessels/embryology,metabolism DNA, Complementary/genetics Molecular Sequence Data Mutation Phenotype Phylogeny Receptors, Vascular Endothelial Growth Factor/genetics,metabolism Vascular Endothelial Growth Factor C/metabolism Vascular Endothelial Growth Factor Receptor-2/genetics,metabolism Vascular Endothelial Growth Factor Receptor-3/genetics,metabolism Zebrafish/embryology,genetics,metabolism Zebrafish Proteins/genetics,metabolism
Chemicals
DNA, Complementary Vascular Endothelial Growth Factor C Zebrafish Proteins vascular endothelial growth factor C, zebrafish Receptors, Vascular Endothelial Growth Factor Vascular Endothelial Growth Factor Receptor-2 Vascular Endothelial Growth Factor Receptor-3
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Covassin L D
Program in Gene Function and Expression, University of Massachusetts Medical School, Worcester, MA 01605, USA.
Villefranc J A
Kacergis M C
Weinstein B M
Lawson N D
References (40)
40 references, click to expand
  1. Orchestration of angiogenesis and arteriovenous contribution by angiopoietins and vascular endothelial growth factor (VEGF).
    Proc Natl Acad Sci U S A. 2002 Jun 11;99(12):8219-24 PMID: 12048246
  2. Regulation of vascular permeability by vascular endothelial growth factors.
    Vascul Pharmacol. 2002 Nov;39(4-5):225-37 PMID: 12747962
  3. Distinct requirements for zebrafish angiogenesis revealed by a VEGF-A morphant.
    Yeast. 2000 Dec;17(4):294-301 PMID: 11119306
  4. In vivo imaging of embryonic vascular development using transgenic zebrafish.
    Dev Biol. 2002 Aug 15;248(2):307-18 PMID: 12167406
  5. SU5416 is a potent and selective inhibitor of the vascular endothelial growth factor receptor (Flk-1/KDR) that inhibits tyrosine kinase catalysis, tumor vascularization, and growth of multiple tumor types.
    Cancer Res. 1999 Jan 1;59(1):99-106 PMID: 9892193
  6. Signaling transduction mechanisms mediating biological actions of the vascular endothelial growth factor family.
    Cardiovasc Res. 2001 Feb 16;49(3):568-81 PMID: 11166270
  7. Disruption of acvrl1 increases endothelial cell number in zebrafish cranial vessels.
    Development. 2002 Jun;129(12):3009-19 PMID: 12050147
  8. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele.
    Nature. 1996 Apr 4;380(6573):435-9 PMID: 8602241
  9. The biology of VEGF and its receptors.
    Nat Med. 2003 Jun;9(6):669-76 PMID: 12778165
  10. The zebrafish gene cloche acts upstream of a flk-1 homologue to regulate endothelial cell differentiation.
    Development. 1997 Jan;124(2):381-9 PMID: 9053314
  11. Zebrafish angiogenesis: a new model for drug screening.
    Angiogenesis. 1999;3(4):353-9 PMID: 14517415
  12. Utilization of distinct signaling pathways by receptors for vascular endothelial cell growth factor and other mitogens in the induction of endothelial cell proliferation.
    J Biol Chem. 2000 Feb 18;275(7):5096-103 PMID: 10671553
  13. VEGF-C signaling pathways through VEGFR-2 and VEGFR-3 in vasculoangiogenesis and hematopoiesis.
    Blood. 2000 Dec 1;96(12):3793-800 PMID: 11090062
  14. A novel vascular endothelial growth factor, VEGF-C, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases.
    EMBO J. 1996 Jan 15;15(2):290-98 PMID: 8617204
  15. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains.
    Science. 1988 Jul 1;241(4861):42-52 PMID: 3291115
  16. Missense mutations interfere with VEGFR-3 signalling in primary lymphoedema.
    Nat Genet. 2000 Jun;25(2):153-9 PMID: 10835628
  17. Vascular endothelial growth factor receptor Flt-1 negatively regulates developmental blood vessel formation by modulating endothelial cell division.
    Blood. 2002 Apr 1;99(7):2397-407 PMID: 11895772
  18. Arteriolar and venular patterning in retinas of mice selectively expressing VEGF isoforms.
    J Clin Invest. 2002 Feb;109(3):327-36 PMID: 11827992
  19. Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice.
    Proc Natl Acad Sci U S A. 1998 Aug 4;95(16):9349-54 PMID: 9689083
  20. 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
  21. Analysis of a zebrafish VEGF receptor mutant reveals specific disruption of angiogenesis.
    Curr Biol. 2002 Aug 20;12(16):1405-12 PMID: 12194822
  22. Role of PlGF in the intra- and intermolecular cross talk between the VEGF receptors Flt1 and Flk1.
    Nat Med. 2003 Jul;9(7):936-43 PMID: 12796773
  23. The cloche and spadetail genes differentially affect hematopoiesis and vasculogenesis.
    Dev Biol. 1998 May 15;197(2):248-69 PMID: 9630750
  24. Cardiovascular failure in mouse embryos deficient in VEGF receptor-3.
    Science. 1998 Oct 30;282(5390):946-9 PMID: 9794766
  25. Suppression of Notch signalling by the COUP-TFII transcription factor regulates vein identity.
    Nature. 2005 May 5;435(7038):98-104 PMID: 15875024
  26. dCAPS, a simple technique for the genetic analysis of single nucleotide polymorphisms: experimental applications in Arabidopsis thaliana genetics.
    Plant J. 1998 May;14(3):387-92 PMID: 9628033
  27. Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor.
    Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10705-9 PMID: 8248162
  28. The biology of vascular endothelial growth factor.
    Endocr Rev. 1997 Feb;18(1):4-25 PMID: 9034784
  29. Ligand-induced vascular endothelial growth factor receptor-3 (VEGFR-3) heterodimerization with VEGFR-2 in primary lymphatic endothelial cells regulates tyrosine phosphorylation sites.
    J Biol Chem. 2003 Oct 17;278(42):40973-9 PMID: 12881528
  30. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice.
    Nature. 1995 Jul 6;376(6535):62-6 PMID: 7596435
  31. Notch signaling is required for arterial-venous differentiation during embryonic vascular development.
    Development. 2001 Oct;128(19):3675-83 PMID: 11585794
  32. Angiogenic network formation in the developing vertebrate trunk.
    Development. 2003 Nov;130(21):5281-90 PMID: 12954720
  33. Sensory nerves determine the pattern of arterial differentiation and blood vessel branching in the skin.
    Cell. 2002 Jun 14;109(6):693-705 PMID: 12086669
  34. Vegfc is required for vascular development and endoderm morphogenesis in zebrafish.
    EMBO Rep. 2004 Jan;5(1):78-84 PMID: 14710191
  35. Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor.
    J Biol Chem. 1994 Oct 28;269(43):26988-95 PMID: 7929439
  36. Coordinate expression of vascular endothelial growth factor receptor-1 (flt-1) and its ligand suggests a paracrine regulation of murine vascular development.
    Dev Dyn. 1995 Nov;204(3):228-39 PMID: 8573716
  37. Modulation of VEGFR-2-mediated endothelial-cell activity by VEGF-C/VEGFR-3.
    Blood. 2003 Feb 15;101(4):1367-74 PMID: 12393458
  38. 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
  39. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium.
    Nature. 1995 Jul 6;376(6535):66-70 PMID: 7596436
  40. A single autophosphorylation site on KDR/Flk-1 is essential for VEGF-A-dependent activation of PLC-gamma and DNA synthesis in vascular endothelial cells.
    EMBO J. 2001 Jun 1;20(11):2768-78 PMID: 11387210
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2006-04-25
Epub
2006-00-14
Pages
6554-9
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1458922
Subset
IM
Grants
NCI NIH HHS · R01 CA107454 · United States
NCI NIH HHS · R01CA107454 · United States
Databases
GENBANK
AY833404, AY833405
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com