VEGF receptor signal transduction – A brief update

Vascular Pharmacology

Volumn 86, Issue , 2016, Pages 14-17

  Claesson Welsh, Lena ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

VASCULOTROPIN RECEPTOR; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3; VASCULOTROPIN A;

HUMAN; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; ENDOTHELIUM CELL; MACROPHAGE; METABOLISM; MONOCYTE; NEOPLASM; PATHOLOGY;

ANIMALS; ENDOTHELIAL CELLS; HUMANS; MACROPHAGES; MONOCYTES; NEOPLASMS; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84993953306     PISSN: 15371891     EISSN: 18793649     Source Type: Journal    
DOI: 10.1016/j.vph.2016.05.011     Document Type: Review

References (59)

1. [1] Dvorak, H.F., Discovery of vascular permeability factor (VPF). Exp. Cell Res. 312:5 (2006), 522–526.
2. [2] Roskoski, R. Jr., VEGF receptor protein-tyrosine kinases: structure and regulation. Biochem. Biophys. Res. Commun. 375:3 (2008), 287–291.
3. [3] Koch, S., Tugues, S., Li, X., Gualandi, L., Claesson-Welsh, L., Signal transduction by vascular endothelial growth factor receptors. Biochem. J. 437:2 (2011), 169–183.
4. [4] Pajusola, K., Aprelikova, O., Pelicci, G., Weich, H., Claesson-Welsh, L., Alitalo, K., Signalling properties of FLT4, a proteolytically processed receptor tyrosine kinase related to two VEGF receptors. Oncogene 9:12 (1994), 3545–3555.
5. [5] Yang, Y., Xie, P., Opatowsky, Y., Schlessinger, J., Direct contacts between extracellular membrane-proximal domains are required for VEGF receptor activation and cell signaling. Proc. Natl. Acad. Sci. U. S. A. 107:5 (2010), 1906–1911.
6. [6] Ruch, C., Skiniotis, G., Steinmetz, M.O., Walz, T., Ballmer-Hofer, K., Structure of a VEGF-VEGF receptor complex determined by electron microscopy. Nat. Struct. Mol. Biol. 14:3 (2007), 249–250.
7. [7] Roskoski, R. Jr., Src kinase regulation by phosphorylation and dephosphorylation. Biochem. Biophys. Res. Commun. 331:1 (2005), 1–14.
8. [8] Kendall, R.L., Thomas, K.A., Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc. Natl. Acad. Sci. U. S. A. 90:22 (1993), 10705–10709.
9. [9] Maynard, S.E., Min, J.Y., Merchan, J., Lim, K.H., Li, J., Mondal, S., et al. Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J. Clin. Invest. 111:5 (2003), 649–658.
10. [10] Clark, D.E., Smith, S.K., He, Y., Day, K.A., Licence, D.R., Corps, A.N., et al. A vascular endothelial growth factor antagonist is produced by the human placenta and released into the maternal circulation. Biol. Reprod. 59:6 (1998), 1540–1548.
11. [11] Fong, G.H., Rossant, J., Gertsenstein, M., Breitman, M.L., Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376:6535 (1995), 66–70.
12. [12] Gerber, H.P., Hillan, K.J., Ryan, A.M., Kowalski, J., Keller, G.A., Rangell, L., et al. VEGF is required for growth and survival in neonatal mice. Development 126:6 (1999), 1149–1159.
13. [13] Carmeliet, P., Ferreira, V., Breier, G., Pollefeyt, S., Kieckens, L., Gertsenstein, M., et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380:6573 (1996), 435–439.
14. [14] Baluk, P., Hashizume, H., McDonald, D.M., Cellular abnormalities of blood vessels as targets in cancer. Curr. Opin. Genet. Dev. 15:1 (2005), 102–111.
15. [15] Gille, H., Kowalski, J., Yu, L., Chen, H., Pisabarro, M.T., Davis-Smyth, T., et al. A repressor sequence in the juxtamembrane domain of Flt-1 (VEGFR-1) constitutively inhibits vascular endothelial growth factor-dependent phosphatidylinositol 3′-kinase activation and endothelial cell migration. EMBO J. 19:15 (2000), 4064–4073.
16. [16] Ito, N., Wernstedt, C., Engstrom, U., Claesson-Welsh, L., Identification of vascular endothelial growth factor receptor-1 tyrosine phosphorylation sites and binding of SH2 domain-containing molecules. J. Biol. Chem. 273:36 (1998), 23410–23418.
17. [17] Dixelius, J., Makinen, T., Wirzenius, M., Karkkainen, M.J., Wernstedt, C., Alitalo, K., et al. 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. 278:42 (2003), 40973–40979.
18. [18] Barleon, B., Sozzani, S., Zhou, D., Weich, H.A., Mantovani, A., Marme, D., Migration of human monocytes in response to vascular endothelial growth factor (VEGF) is mediated via the VEGF receptor flt-1. Blood 87:8 (1996), 3336–3343.
19. [19] Hiratsuka, S., Minowa, O., Kuno, J., Noda, T., Shibuya, M., Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice. Proc. Natl. Acad. Sci. U. S. A. 95:16 (1998), 9349–9354.
20. [20] Shibuya, M., Vascular endothelial growth factor receptor-1 (VEGFR-1/Flt-1): a dual regulator for angiogenesis. Angiogenesis 9:4 (2006), 225–230 (discussion 31).
21. [21] Hiratsuka, S., Maru, Y., Okada, A., Seiki, M., Noda, T., Shibuya, M., Involvement of Flt-1 tyrosine kinase (vascular endothelial growth factor receptor-1) in pathological angiogenesis. Cancer Res. 61:3 (2001), 1207–1213.
22. [22] Fischer, C., Jonckx, B., Mazzone, M., Zacchigna, S., Loges, S., Pattarini, L., et al. Anti-PlGF inhibits growth of VEGF(R)-inhibitor-resistant tumors without affecting healthy vessels. Cell 131:3 (2007), 463–475.
23. [23] Carmeliet, P., Moons, L., Luttun, A., Vincenti, V., Compernolle, V., De Mol, M., et al. Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat. Med. 7:5 (2001), 575–583.
24. [24] Bellomo, D., Headrick, J.P., Silins, G.U., Paterson, C.A., Thomas, P.S., Gartside, M., et al. Mice lacking the vascular endothelial growth factor-B gene (Vegfb) have smaller hearts, dysfunctional coronary vasculature, and impaired recovery from cardiac ischemia. Circ. Res. 86:2 (2000), E29–E35.
25. [25] Aase, K., von Euler, G., Li, X., Ponten, A., Thoren, P., Cao, R., et al. Vascular endothelial growth factor-B-deficient mice display an atrial conduction defect. Circulation 104:3 (2001), 358–364.
26. [26] Hagberg, C.E., Falkevall, A., Wang, X., Larsson, E., Huusko, J., Nilsson, I., et al. Vascular endothelial growth factor B controls endothelial fatty acid uptake. Nature 464:7290 (2010), 917–921.
27. [27] Autiero, M., Waltenberger, J., Communi, D., Kranz, A., Moons, L., Lambrechts, D., et al. Role of PlGF in the intra- and intermolecular cross talk between the VEGF receptors Flt1 and Flk1. Nat. Med. 9:7 (2003), 936–943.
28. [28] Anisimov, A., Leppanen, V.M., Tvorogov, D., Zarkada, G., Jeltsch, M., Holopainen, T., et al. The basis for the distinct biological activities of vascular endothelial growth factor receptor-1 ligands. Sci Signal., 6(282), 2013, ra52.
29. [29] Shalaby, F., Rossant, J., Yamaguchi, T.P., Gertsenstein, M., Wu, X.F., Breitman, M.L., et al. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376:6535 (1995), 62–66.
30. [30] Faivre, S., Demetri, G., Sargent, W., Raymond, E., Molecular basis for sunitinib efficacy and future clinical development. Nat. Rev. 6:9 (2007), 734–745.
31. [31] Matsumoto, T., Bohman, S., Dixelius, J., Berge, T., Dimberg, A., Magnusson, P., et al. VEGF receptor-2 Y951 signaling and a role for the adapter molecule TSAd in tumor angiogenesis. EMBO J. 24:13 (2005), 2342–2353.
32. [32] Sun, Z., Li, X., Massena, S., Kutschera, S., Padhan, N., Gualandi, L., et al. VEGFR2 induces c-Src signaling and vascular permeability in vivo via the adaptor protein TSAd. J. Exp. Med. 209:7 (2012), 1363–1377.
33. [33] Weis, S., Shintani, S., Weber, A., Kirchmair, R., Wood, M., Cravens, A., et al. Src blockade stabilizes a Flk/cadherin complex, reducing edema and tissue injury following myocardial infarction. J. Clin. Invest. 113:6 (2004), 885–894.
34. [34] Gavard, J., Gutkind, J.S., VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin. Nat. Cell Biol. 8:11 (2006), 1223–1234.
35. [35] Claesson-Welsh, L., Vascular permeability–the essentials. Ups. J. Med. Sci. 120:3 (2015), 135–143.
36. [36] Sakurai, Y., Ohgimoto, K., Kataoka, Y., Yoshida, N., Shibuya, M., Essential role of Flk-1 (VEGF receptor 2) tyrosine residue 1173 in vasculogenesis in mice. Proc. Natl. Acad. Sci. U. S. A. 102:4 (2005), 1076–1081.
37. [37] 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. 20:11 (2001), 2768–2778.
38. [38] Holmqvist, K., Cross, M.J., Rolny, C., Hagerkvist, R., Rahimi, N., Matsumoto, T., et al. The adaptor protein shb binds to tyrosine 1175 in vascular endothelial growth factor (VEGF) receptor-2 and regulates VEGF-dependent cellular migration. J. Biol. Chem. 279:21 (2004), 22267–22275.
39. [39] Warner, A.J., Lopez-Dee, J., Knight, E.L., Feramisco, J.R., Prigent, S.A., The Shc-related adaptor protein, Sck, forms a complex with the vascular-endothelial-growth-factor receptor KDR in transfected cells. Biochem. J. 347:Pt 2 (2000), 501–509.
40. [40] Lamalice, L., Houle, F., Jourdan, G., Huot, J., Phosphorylation of tyrosine 1214 on VEGFR2 is required for VEGF-induced activation of Cdc42 upstream of SAPK2/p38. Oncogene 23:2 (2004), 434–445.
41. [41] Lamalice, L., Houle, F., Huot, J., Phosphorylation of Tyr1214 within VEGFR-2 triggers the recruitment of Nck and activation of Fyn leading to SAPK2/p38 activation and endothelial cell migration in response to VEGF. J. Biol. Chem. 281:45 (2006), 34009–34020.
42. [42] Ridley, A.J., Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol. 16:10 (2006), 522–529.
43. [43] Ruan, G.X., Kazlauskas, A., VEGF-A engages at least three tyrosine kinases to activate PI3K/Akt. Cell Cycle 11:11 (2012), 2047–2048.
44. [44] Lanahan, A.A., Hermans, K., Claes, F., Kerley-Hamilton, J.S., Zhuang, Z.W., Giordano, F.J., et al. VEGF receptor 2 endocytic trafficking regulates arterial morphogenesis. Dev. Cell 18:5 (2010), 713–724.
45. [45] Hayashi, M., Majumdar, A., Li, X., Adler, J., Sun, Z., Vertuani, S., et al. VE-PTP regulates VEGFR2 activity in stalk cells to establish endothelial cell polarity and lumen formation. Nat. Commun., 4, 2013, 1672.
46. [46] Pitulescu, M.E., Adams, R.H., Regulation of signaling interactions and receptor endocytosis in growing blood vessels. Cell Adhes. Migr. 8:4 (2014), 366–377.
47. [47] Kuppers, V., Vockel, M., Nottebaum, A.F., Vestweber, D., Phosphatases and kinases as regulators of the endothelial barrier function. Cell Tissue Res. 355:3 (2014), 577–586.
48. [48] Tammela, T., Zarkada, G., Nurmi, H., Jakobsson, L., Heinolainen, K., Tvorogov, D., et al. VEGFR-3 controls tip to stalk conversion at vessel fusion sites by reinforcing notch signalling. Nat. Cell Biol. 13:10 (2011), 1202–1213.
49. [49] Tammela, T., Alitalo, K., Lymphangiogenesis: molecular mechanisms and future promise. Cell 140:4 (2010), 460–476.
50. [50] Dumont, D.J., Jussila, L., Taipale, J., Lymboussaki, A., Mustonen, T., Pajusola, K., et al. Cardiovascular failure in mouse embryos deficient in VEGF receptor-3. Science 282:5390 (1998), 946–949.
51. [51] Galvagni, F., Pennacchini, S., Salameh, A., Rocchigiani, M., Neri, F., Orlandini, M., et al. Endothelial cell adhesion to the extracellular matrix induces c-Src-dependent VEGFR-3 phosphorylation without the activation of the receptor intrinsic kinase activity. Circ. Res. 106:12 (2010), 1839–1848.
52. [52] Planas-Paz, L., Strilic, B., Goedecke, A., Breier, G., Fassler, R., Lammert, E., Mechanoinduction of lymph vessel expansion. EMBO J. 31:4 (2012), 788–804.
53. [53] Salameh, A., Galvagni, F., Bardelli, M., Bussolino, F., Oliviero, S., Direct recruitment of CRK and GRB2 to VEGFR-3 induces proliferation, migration, and survival of endothelial cells through the activation of ERK, AKT, and JNK pathways. Blood 106:10 (2005), 3423–3431.
54. [54] Zarkada, G., Heinolainen, K., Makinen, T., Kubota, Y., Alitalo, K., VEGFR3 does not sustain retinal angiogenesis without VEGFR2. Proc. Natl. Acad. Sci. U. S. A. 112:3 (2015), 761–766.
55. [55] Stanczuk, L., Martinez-Corral, I., Ulvmar, M.H., Zhang, Y., Lavina, B., Fruttiger, M., et al. cKit Lineage Hemogenic Endothelium-Derived Cells Contribute to Mesenteric Lymphatic Vessels. Cell Reports. 2015.
56. [56] Makinen, T., Veikkola, T., Mustjoki, S., Karpanen, T., Catimel, B., Nice, E.C., et al. Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF-C/D receptor VEGFR-3. EMBO J. 20:17 (2001), 4762–4773.
57. [57] Zhou, F., Chang, Z., Zhang, L., Hong, Y.K., Shen, B., Wang, B., et al. Akt/protein kinase B is required for lymphatic network formation, remodeling, and valve development. Am. J. Pathol. 177:4 (2010), 2124–2133.
58. [58] Koltowska, K., Paterson, S., Bower, N.I., Baillie, G.J., Lagendijk, A.K., Astin, J.W., et al. mafba is a downstream transcriptional effector of Vegfc signaling essential for embryonic lymphangiogenesis in zebrafish. Genes Dev. 29:15 (2015), 1618–1630.
59. [59] Irrthum, A., Karkkainen, M.J., Devriendt, K., Alitalo, K., Vikkula, M., Congenital hereditary lymphedema caused by a mutation that inactivates VEGFR3 tyrosine kinase. Am. J. Hum. Genet. 67:2 (2000), 295–301.