Home LiteratureArticle Details
PMID: 18628209 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Neuropilin-1-VEGFR-2 complexing requires the PDZ-binding domain of neuropilin-1.

The Journal of biological chemistry ·Vol. 283 ·No. 37 ·2008-09-12 ·Pages 25110-25114

Prahst C, Héroult M, Lanahan AA, Uziel N, Kessler O, Shraga-Heled N, Simons M, Neufeld G, Augustin HG

Abstract

Vascular endothelial growth factor (VEGF) acts as a hierarchically high switch of the angiogenic cascade by interacting with its high affinity VEGF receptors and with neuropilin co-receptors. VEGF(165) binds to both Neuropilin-1 (NP-1) and VEGFR-2, and it is believed that ligand binding forms an extracellular bridge between both molecules. This leads to complex formation, thereby enhancing VEGFR-2 phosphorylation and subsequent signaling. We found that inhibition of VEGF receptor (VEGFR) phosphorylation reduced complex formation between NP-1 and VEGFR-2, suggesting a functional role of the cytoplasmic domain of VEGFR-2 for complex formation. Correspondingly, deleting the PDZ-binding domain of NP-1 decreased complex formation, indicating that extracellular VEGF(165) binding is not sufficient for VEGFR-2-NP-1 interaction. Synectin is an NP-1 PDZ-binding domain-interacting molecule. Experiments in Synectin-deficient endothelial cells revealed reduced VEGFR-2-NP-1 complex formation, suggesting a role for Synectin in VEGFR-2-NP-1 signaling. Taken together, the experiments have identified a novel mechanism of NP-1 interaction with VEGFR-2, which involves the cytoplasmic domain of NP-1.

MeSH Terms
Adaptor Proteins, Signal Transducing/chemistry Animals Carrier Proteins/chemistry Cytoplasm/metabolism Humans Mice Models, Biological Neuropeptides/chemistry Neuropilin-1/metabolism Phosphorylation Protein Binding Protein Structure, Tertiary Signal Transduction Swine Vascular Endothelial Growth Factor A/metabolism Vascular Endothelial Growth Factor Receptor-2/metabolism
Chemicals
Adaptor Proteins, Signal Transducing Carrier Proteins GIPC1 protein, human Gipc1 protein, mouse Neuropeptides Vascular Endothelial Growth Factor A Neuropilin-1 Vascular Endothelial Growth Factor Receptor-2
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Prahst Claudia
Joint Research Division Vascular Biology of the Medical Faculty Mannheim (CBTM), University of Heidelberg, and the German Cancer Research Center (DKFZ), D-69120 Heidelberg, Germany.
Héroult Mélanie
Joint Research Division Vascular Biology of the Medical Faculty Mannheim (CBTM), University of Heidelberg, and the German Cancer Research Center (DKFZ), D-69120 Heidelberg, Germany.
Lanahan Anthony A
Angiogenesis Research Center and Section of Cardiology, Department of Medicine, Dartmouth Medical School, Lebanon, New Hampshire 03756.
Uziel Noa
Cancer and Vascular Biology Research Center, Rappaport Research Institute in the Medical Sciences, The Bruce Rappaport Faculty of Medicine, Technion, Israel Institute of Technology, Haifa 31096, Israel.
Kessler Ofra
Cancer and Vascular Biology Research Center, Rappaport Research Institute in the Medical Sciences, The Bruce Rappaport Faculty of Medicine, Technion, Israel Institute of Technology, Haifa 31096, Israel.
Shraga-Heled Niva
Cancer and Vascular Biology Research Center, Rappaport Research Institute in the Medical Sciences, The Bruce Rappaport Faculty of Medicine, Technion, Israel Institute of Technology, Haifa 31096, Israel.
Simons Michael
Angiogenesis Research Center and Section of Cardiology, Department of Medicine, Dartmouth Medical School, Lebanon, New Hampshire 03756.
Neufeld Gera
Cancer and Vascular Biology Research Center, Rappaport Research Institute in the Medical Sciences, The Bruce Rappaport Faculty of Medicine, Technion, Israel Institute of Technology, Haifa 31096, Israel.
Augustin Hellmut G
Joint Research Division Vascular Biology of the Medical Faculty Mannheim (CBTM), University of Heidelberg, and the German Cancer Research Center (DKFZ), D-69120 Heidelberg, Germany. Electronic address: augustin@angiogenese.de.
References (28)
28 references, click to expand
  1. Cloning and characterization of neuropilin-1-interacting protein: a PSD-95/Dlg/ZO-1 domain-containing protein that interacts with the cytoplasmic domain of neuropilin-1.
    J Neurosci. 1999 Aug 1;19(15):6519-27 PMID: 10414980
  2. The PDZ domain of TIP-2/GIPC interacts with the C-terminus of the integrin alpha5 and alpha6 subunits.
    Matrix Biol. 2002 Mar;21(2):207-14 PMID: 11852236
  3. Neuropilin-1 and neuropilin-2 enhance VEGF121 stimulated signal transduction by the VEGFR-2 receptor.
    FASEB J. 2007 Mar;21(3):915-26 PMID: 17185751
  4. Intrinsic tyrosine kinase activity is required for vascular endothelial growth factor receptor 2 ubiquitination, sorting and degradation in endothelial cells.
    Traffic. 2006 Sep;7(9):1270-82 PMID: 17004325
  5. C terminus of RGS-GAIP-interacting protein conveys neuropilin-1-mediated signaling during angiogenesis.
    FASEB J. 2006 Jul;20(9):1513-5 PMID: 16754745
  6. Angiopoietin-2 sensitizes endothelial cells to TNF-alpha and has a crucial role in the induction of inflammation.
    Nat Med. 2006 Feb;12(2):235-9 PMID: 16462802
  7. Developmentally regulated expression of a cell surface protein, neuropilin, in the mouse nervous system.
    J Neurobiol. 1996 Jan;29(1):1-17 PMID: 8748368
  8. Selective regulation of arterial branching morphogenesis by synectin.
    Dev Cell. 2006 Jun;10(6):783-95 PMID: 16740480
  9. Expression of a cell adhesion molecule, neuropilin, in the developing chick nervous system.
    Dev Biol. 1995 Jul;170(1):207-22 PMID: 7601310
  10. Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice.
    Neuron. 1997 Nov;19(5):995-1005 PMID: 9390514
  11. Neuropilin-1 regulates vascular endothelial growth factor-mediated endothelial permeability.
    Circ Res. 2005 Jun 24;96(12):1257-65 PMID: 15920019
  12. Receptors for collapsin/semaphorins.
    Curr Opin Neurobiol. 1998 Oct;8(5):587-92 PMID: 9811625
  13. Autophosphorylation of KDR in the kinase domain is required for maximal VEGF-stimulated kinase activity and receptor internalization.
    Oncogene. 1999 Feb 25;18(8):1619-27 PMID: 10102632
  14. Mechanisms of angiogenesis.
    Nature. 1997 Apr 17;386(6626):671-4 PMID: 9109485
  15. The c-Cbl/CD2AP complex regulates VEGF-induced endocytosis and degradation of Flt-1 (VEGFR-1).
    FASEB J. 2004 May;18(7):929-31 PMID: 15001553
  16. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor.
    Cell. 1998 Mar 20;92(6):735-45 PMID: 9529250
  17. PTK787/ZK 222584, a novel and potent inhibitor of vascular endothelial growth factor receptor tyrosine kinases, impairs vascular endothelial growth factor-induced responses and tumor growth after oral administration.
    Cancer Res. 2000 Apr 15;60(8):2178-89 PMID: 10786682
  18. Plasticity of endothelial cells during arterial-venous differentiation in the avian embryo.
    Development. 2001 Sep;128(17):3359-70 PMID: 11546752
  19. Differential expression of neuropilin-1 and neuropilin-2 in arteries and veins.
    Mech Dev. 2001 Nov;109(1):115-9 PMID: 11677062
  20. Neuropilin-1 modulates p53/caspases axis to promote endothelial cell survival.
    PLoS One. 2007 Nov 14;2(11):e1161 PMID: 18000534
  21. Neuropilin-1 binds to VEGF121 and regulates endothelial cell migration and sprouting.
    J Biol Chem. 2007 Aug 17;282(33):24049-56 PMID: 17575273
  22. GIPC and GAIP form a complex with TrkA: a putative link between G protein and receptor tyrosine kinase pathways.
    Mol Biol Cell. 2001 Mar;12(3):615-27 PMID: 11251075
  23. Overexpression of a membrane protein, neuropilin, in chimeric mice causes anomalies in the cardiovascular system, nervous system and limbs.
    Development. 1995 Dec;121(12):4309-18 PMID: 8575331
  24. A requirement for neuropilin-1 in embryonic vessel formation.
    Development. 1999 Nov;126(21):4895-902 PMID: 10518505
  25. Expression and regulatory role of GAIP-interacting protein GIPC in pancreatic adenocarcinoma.
    Cancer Res. 2006 Nov 1;66(21):10264-8 PMID: 17079444
  26. GIPC, a PDZ domain containing protein, interacts specifically with the C terminus of RGS-GAIP.
    Proc Natl Acad Sci U S A. 1998 Oct 13;95(21):12340-5 PMID: 9770488
  27. VEGF165 mediates formation of complexes containing VEGFR-2 and neuropilin-1 that enhance VEGF165-receptor binding.
    J Cell Biochem. 2002;85(2):357-68 PMID: 11948691
  28. Synectin in the nervous system: expression pattern and potential as a binding partner of neurotrophin receptors.
    FEBS Lett. 2004 Aug 13;572(1-3):123-8 PMID: 15304335
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
0021-9258
Published
2008-09-12
Epub
2008-00-15
Pages
25110-25114
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC2533068
Subset
IM
Grants
NHLBI NIH HHS · HL 084619 · United States
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