Unraveling the influence of endothelial cell density on VEGF-A signaling

Blood

Volumn 119, Issue 23, 2012, Pages 5599-5607

  Napione, Lucia ^a,b   Pavan, Simona ^a,b   Veglio, Andrea ^a,b   Picco, Andrea ^c   Boffetta, Guido ^b,d   Celani, Antonio ^e   Seano, Giorgio ^a,b   Primo, Luca ^a,b   Gamba, Andrea ^a,d,f   Bussolino, Federico ^a,b  

^a CANDIOLO CANCER INSTITUTE   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

^c Research Unit of Cell Biology and Biophysics   (Germany)

^d SEZIONE DI TORINO   (Italy)

^e INSTITUT PASTEUR   (France)

^f POLITECNICO DI TORINO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

DENSITY ENHANCED PHOSPHATASE 1; PHOSPHOLIPASE C GAMMA; PROTEIN KINASE B; PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE 1B; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL PROTEIN TYROSINE PHOSPHATASE; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ARTICLE; BINDING AFFINITY; CELL DENSITY; CONTROLLED STUDY; DEPHOSPHORYLATION; ENDOTHELIUM CELL; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; LIGAND BINDING; MATHEMATICAL MODEL; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN TARGETING; RECEPTOR BINDING; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM;

EID: 84862537741     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-11-390666     Document Type: Article

References (47)

1. Olsson AK, Dimberg A, Kreuger J, Claesson-Welsh L. VEGF receptor signalling: in control of vascular function. Nat Rev Mol Cell Biol. 2006;7(5):359-371.
2. Ferrara N, Mass RD, Campa C, Kim R. Targeting VEGF-A to treat cancer and age-related macular degeneration. Annu Rev Med. 2007;58:491-504. (Pubitemid 46706529)
3. Waltenberger J, Claesson-Welsh L, Siegbahn A, Shibuya M, Heldin CH. Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor. J Biol Chem. 1994;269(43):26988-26995. (Pubitemid 24332901)
4. Seetharam L, Gotoh N, Maru Y, Neufeld G, Yamaguchi S, Shibuya M. A unique signal transduction from FLT tyrosine kinase, a receptor for vascular endothelial growth factor VEGF. Oncogene. 1995;10(1):135-147.
5. Shibuya M. Differential roles of vascular endothelial growth factor receptor-1 and receptor-2 in angiogenesis. J Biochem Mol Biol. 2006;39(5):469-478. (Pubitemid 44714526)
6. Takahashi T, Shibuya M. The 230 kDa mature form of KDR/Flk-1 (VEGF receptor-2) activates the PLC-gamma pathway and partially induces mitotic signals in NIH3T3 fibroblasts. Oncogene. 1997;14(17):2079-2089. (Pubitemid 27237011)
7. Takahashi T, Yamaguchi S, Chida K, Shibuya M. 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;20(11):2768-2778. (Pubitemid 32938560)
8. Bates DO, Heald RI, Curry FE, Williams B. Vascular endothelial growth factor increases Rana vascular permeability and compliance by different signalling pathways. J Physiol. 2001;533(1):263-272. (Pubitemid 32499377)
9. Bussolino F, Serini G, Mitola S, Bazzoni G, Dejana E. Dynamic modules and heterogeneity of function: a lesson from tyrosine kinase receptors in endothelial cells. EMBO Rep. 2001;2(9):763-767. (Pubitemid 32982741)
10. Dejana E. Endothelial cell-cell junctions: happy together. Nat Rev Mol Cell Biol. 2004;5(4):261-270. (Pubitemid 38480607)
11. Lampugnani MG, Zanetti A, Corada M, et al. Contact inhibition of VEGF-induced proliferation requires vascular endothelial cadherin, beta-catenin, and the phosphatase DEP-1/CD148. J Cell Biol. 2003;161(4):793-804. (Pubitemid 36648762)
12. Esser S, Lampugnani MG, Corada M, Dejana E, Risau W. Vascular endothelial growth factor induces VE-cadherin tyrosine phosphorylation in endothelial cells. J Cell Sci. 1998;111(13):1853-1865. (Pubitemid 28370530)
13. Gavard J, Gutkind JS. VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin. Nat Cell Biol. 2006;8(11):1223-1234. (Pubitemid 44660587)
14. Bussolino F, Di Renzo MF, Ziche M, et al. Hepatocyte growth factor is a potent angiogenic factor which stimulates endothelial cell motility and growth. J Cell Biol. 1992;119(3):629-641.
15. Lampugnani MG, Corada M, Caveda L, et al. The molecular organization of endothelial cell to cell junctions: differential association of plakoglobin, beta-catenin, and alpha-catenin with vascular endothelial cadherin (VE-cadherin). J Cell Biol. 1995;129(1):203-217.
16. Gampel A, Moss L, Jones MC, Brunton V, Norman JC, Mellor H. VEGF regulates the mobilization of VEGFR2/KDR from an intracellular endothelial storage compartment. Blood. 2006;108(8):2624-2631.
17. Le Novere N, Hucka M, Mi H, et al. The systems biology graphical notation. Nat Biotechnol. 2009;27(8):735-741.
18. Alarcòn T, Page KM. Mathematical models of the VEGF receptor and its role in cancer therapy. J R Soc Interface. 2007;4(13):283-304.
19. Ruch C, Skiniotis G, Steinmetz MO, Walz T, Ballmer-Hofer K. Structure of a VEGF-VEGF receptor complex determined by electron microscopy. Nat Struct Mol Biol. 2007;14(3):249-250. (Pubitemid 46355572)
20. Nicholson KM, Anderson NG. The protein kinase B/Akt signalling pathway in human malignancy. Cell Signal. 2002;14(5):381-395. (Pubitemid 34214843)
21. Cuevas B, Lu Y, Watt S, et al. SHP-1 regulates Lck-induced phosphatidylinositol 3-kinase phosphorylation and activity. J Biol Chem. 1999;274(39):27583-27589.
22. Maehama T, Dixon JE. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J Biol Chem. 1998;273(22):13375-13378. (Pubitemid 28268370)
23. Choi JH, Ryu SH, Suh PG. On/off-regulation of phospholipase C-gamma 1-mediated signal transduction. Adv Enzyme Regul. 2007;47:104-116. (Pubitemid 47302066)
24. Lee S, Mandic J, Van Vliet KJ. Chemomechanical mapping of ligand-receptor binding kinetics on cells. Proc Natl Acad Sci U S A. 2007;104(23):9609-9614. (Pubitemid 47175314)
25. Dougher M, Terman BI. Autophosphorylation of KDR in the kinase domain is required for maximal VEGF-stimulated kinase activity and receptor internalization. Oncogene. 1999;18(8):1619-1627. (Pubitemid 29108062)
26. Dayanir V, Meyer RD, Lashkari K, Rahimi N. Identification of tyrosine residues in vascular endothelial growth factor receptor-2/FLK-1 involved in activation of phosphatidylinositol 3-kinase and cell proliferation. J Biol Chem. 2001;276(21):17686-17692.
27. Serini G, Ambrosi D, Giraudo E, Gamba A, Preziosi L, Bussolino F. Modeling the early stages of vascular network assembly. EMBO J. 2003;22(8):1771-1779. (Pubitemid 36460134)
28. Lee S, Chen TT, Barber CL, et al. Autocrine VEGF signaling is required for vascular homeostasis. Cell. 2007;130(4):691-703. (Pubitemid 47268059)
29. Li S, Peck-Radosavljevic M, Koller E, et al. Characterization of (123)I-vascular endothelial growth factor-binding sites expressed on human tumour cells: possible implication for tumour scintigraphy. Int J Cancer. 2001;91(6):789-796. (Pubitemid 32178646)
30. Huang X, Gottstein C, Brekken RA, Thorpe PE. Expression of soluble VEGF receptor 2 and characterization of its binding by surface plasmon resonance. Biochem Biophys Res Commun. 1998;252(3):643-648. (Pubitemid 28556830)
31. Kim HK, Kim JW, Zilberstein A, et al. PDGF stimulation of inositol phospholipid hydrolysis requires PLC-gamma 1 phosphorylation on tyrosine residues 783 and 1254. Cell. 1991;65(3):435-441. (Pubitemid 121002053)
32. Heinrich R, Neel BG, Rapoport TA. Mathematical models of protein kinase signal transduction. Mol Cell. 2002;9(5):957-970. (Pubitemid 34626667)
33. Goldbeter A, Koshland DE Jr. An amplified sensitivity arising from covalent modification in biological systems. Proc Natl Acad Sci U S A. 1981;78(11):6840-6844. (Pubitemid 12216857)
34. Ciliberto A, Capuani F, Tyson JJ. Modeling networks of coupled enzymatic reactions using the total quasi-steady state approximation. PLoS Comput Biol. 2007;3(3):e45.
35. Mitola S, Brenchio B, Piccinini M, et al. Type I collagen limits VEGFR-2 signaling by a SHP2 protein-tyrosine phosphatase-dependent mechanism 1. Circ Res. 2006;98(1):45-54. (Pubitemid 43970202)
36. Nakamura Y, Patrushev N, Inomata H, et al. Role of protein tyrosine phosphatase 1B in vascular endothelial growth factor signaling and cell-cell adhesions in endothelial cells. Circ Res. 2008;102(10):1182-1191.
37. Chabot C, Spring K, Gratton JP, Elchebly M, Royal I. New role for the protein tyrosine phosphatase DEP-1 in Akt activation and endothelial cell survival. Mol Cell Biol. 2009;29(1):241-253.
38. Mellberg S, Dimberg A, Bahram F, et al. Transcriptional profiling reveals a critical role for tyrosine phosphatase VE-PTP in regulation of VEGFR2 activity and endothelial cell morphogenesis. FASEB J. 2009;23(5):1490-1502.
39. Papapetropoulos A, Fulton D, Lin MI, et al. Vanadate is a potent activator of endothelial nitric-oxide synthase: evidence for the role of the serine/threonine kinase Akt and the 90-kDa heat shock protein. Mol Pharmacol. 2004;65(2):407-415. (Pubitemid 38134269)
40. Li YM, Mackintosh C, Casida JE. Protein phosphatase 2A and its [3H]cantharidin/[3H]endothall thioanhydride binding site: inhibitor specificity of cantharidin and ATP analogues. Biochem Pharmacol. 1993;46(8):1435-1443. (Pubitemid 23319314)
41. Scott A, Mellor H. VEGF receptor trafficking in angiogenesis. Biochem Soc Trans. 2009;37(6):1184-1188.
42. Zhang Z, Neiva KG, Lingen MW, Ellis LM, Nor JE. VEGF-dependent tumor angiogenesis requires inverse and reciprocal regulation of VEGFR1 and VEGFR2. Cell Death Differ. 2010;17(3):499-512.
43. Ferrara N. Vascular endothelial growth factor: molecular and biological aspects. Curr Top Microbiol Immunol. 1999;237:1-30. (Pubitemid 28554856)
44. Plate KH, Breier G, Weich HA, Mennel HD, Risau W. Vascular endothelial growth factor and glioma angiogenesis: coordinate induction of VEGF receptors, distribution of VEGF protein and possible in vivo regulatory mechanisms. Int J Cancer. 1994;59(4):520-529. (Pubitemid 24357278)
45. Ewan LC, Jopling HM, Jia H, et al. Intrinsic tyrosine kinase activity is required for vascular endothelial growth factor receptor 2 ubiquitination, sorting and degradation in endothelial cells. Traffic. 2006;7(9):1270-1282. (Pubitemid 44204001)
46. Qian X, Karpova T, Sheppard AM, McNally J, Lowy DR. E-cadherin-mediated adhesion inhibits ligand-dependent activation of diverse receptor tyrosine kinases. EMBO J. 2004;23(8):1739-1748. (Pubitemid 38649637)
47. Lanahan AA, Hermans K, Claes F, et al. VEGF receptor 2 endocytic trafficking regulates arterial morphogenesis. Dev Cell. 2010;18(5):713-724.