Evidence for Pro-angiogenic Functions of VEGF-Ax

Cell

Volumn 167, Issue 1, 2016, Pages 275-284.e6

  Xin, Hong ^a   Zhong, Cuiling ^a   Nudleman, Eric ^a   Ferrara, Napoleone ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

angiogenesis; endothelium; readthrough translation; tyrosine kinase; VEGF

Indexed keywords

AMINO ACID; RECOMBINANT PROTEIN; TYROSINE; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL GROWTH FACTOR AX; VASCULOTROPIN 165; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2; ANGIOGENESIS INHIBITOR; ANGIOGENIC FACTOR; ISOPROTEIN; MESSENGER RNA; MITOGENIC AGENT; NEUROPILIN 1; VASCULOTROPIN RECEPTOR 1; VEGFA PROTEIN, HUMAN;

AMINO ACID SEQUENCE; ANGIOGENESIS; ANIMAL EXPERIMENT; ANTIANGIOGENIC ACTIVITY; ARTICLE; BLOOD VESSEL PERMEABILITY; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; COMPARATIVE STUDY; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; MALE; MITOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ALTERNATIVE RNA SPLICING; ANIMAL; CAPILLARY PERMEABILITY; CHEMOTAXIS; CYTOLOGY; DRUG EFFECTS; GENETICS; GUINEA PIG; HEK293 CELL LINE; METABOLISM; MITOSIS; MOLECULAR CLONING; PHYSIOLOGY; PROTEIN SYNTHESIS;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANGIOGENESIS INDUCING AGENTS; ANGIOGENESIS INHIBITORS; ANIMALS; CAPILLARY PERMEABILITY; CHEMOTAXIS; CLONING, MOLECULAR; ENDOTHELIAL CELLS; GUINEA PIGS; HEK293 CELLS; HUMANS; MICE; MITOGENS; MITOSIS; NEOVASCULARIZATION, PHYSIOLOGIC; NEUROPILIN-1; PROTEIN BIOSYNTHESIS; PROTEIN ISOFORMS; RECOMBINANT PROTEINS; RNA, MESSENGER; TYROSINE; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84988584464     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.08.054     Document Type: Article

References (49)

1. Bates, D.O., Cui, T.G., Doughty, J.M., Winkler, M., Sugiono, M., Shields, J.D., Peat, D., Gillatt, D., Harper, S.J., VEGF165b, an inhibitory splice variant of vascular endothelial growth factor, is down-regulated in renal cell carcinoma. Cancer Res. 62 (2002), 4123–4131.
2. Beier, H., Grimm, M., Misreading of termination codons in eukaryotes by natural nonsense suppressor tRNAs. Nucleic Acids Res. 29 (2001), 4767–4782.
3. Carmeliet, P., Jain, R.K., Molecular mechanisms and clinical applications of angiogenesis. Nature 473 (2011), 298–307.
4. Carmeliet, P., Ferreira, V., Breier, G., Pollefeyt, S., Kieckens, L., Gertsenstein, M., Fahrig, M., Vandenhoeck, A., Harpal, K., Eberhardt, C., et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380 (1996), 435–439.
5. Carmeliet, P., Ng, Y.-S., Nuyens, D., Theilmeier, G., Brusselmans, K., Cornelissen, I., Ehler, E., Kakkar, V.V., Stalmans, I., Mattot, V., et al. Impaired myocardial angiogenesis and ischemic cardiomyopathy in mice lacking the vascular endothelial growth factor isoforms VEGF164 and VEGF188. Nat. Med. 5 (1999), 495–502.
6. 165b are weakly angiogenic isoforms of VEGF-A. Mol. Cancer, 9, 2010, 320.
7. Clark, H.F., Gurney, A.L., Abaya, E., Baker, K., Baldwin, D., Brush, J., Chen, J., Chow, B., Chui, C., Crowley, C., et al. The secreted protein discovery initiative (SPDI), a large-scale effort to identify novel human secreted and transmembrane proteins: a bioinformatics assessment. Genome Res. 13 (2003), 2265–2270.
8. Eswarappa, S.M., Potdar, A.A., Koch, W.J., Fan, Y., Vasu, K., Lindner, D., Willard, B., Graham, L.M., DiCorleto, P.E., Fox, P.L., Programmed translational readthrough generates antiangiogenic VEGF-Ax. Cell 157 (2014), 1605–1618.
9. Ferrara, N., Vascular endothelial growth factor: basic science and clinical progress. Endocr. Rev. 25 (2004), 581–611.
10. Ferrara, N., Binding to the extracellular matrix and proteolytic processing: two key mechanisms regulating vascular endothelial growth factor action. Mol. Biol. Cell 21 (2010), 687–690.
11. Ferrara, N., Adamis, A.P., Ten years of anti-vascular endothelial growth factor therapy. Nat. Rev. Drug Discov. 15 (2016), 385–403.
12. Ferrara, N., Kerbel, R.S., Angiogenesis as a therapeutic target. Nature 438 (2005), 967–974.
13. Ferrara, N., Carver-Moore, K., Chen, H., Dowd, M., Lu, L., O'Shea, K.S., Powell-Braxton, L., Hillan, K.J., Moore, M.W., Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380 (1996), 439–442.
14. Ferrara, N., Gerber, H.P., LeCouter, J., The biology of VEGF and its receptors. Nat. Med. 9 (2003), 669–676.
15. Firth, A.E., Brierley, I., Non-canonical translation in RNA viruses. J. Gen. Virol. 93 (2012), 1385–1409.
16. Folkman, J., Klagsbrun, M., Angiogenic factors. Science 235 (1987), 442–447.
17. Fuh, G., Wu, P., Liang, W.C., Ultsch, M., Lee, C.V., Moffat, B., Wiesmann, C., Structure-function studies of two synthetic anti-vascular endothelial growth factor Fabs and comparison with the Avastin Fab. J. Biol. Chem. 281 (2006), 6625–6631.
18. Gille, H., Kowalski, J., Li, B., LeCouter, J., Moffat, B., Zioncheck, T.F., Pelletier, N., Ferrara, N., Analysis of biological effects and signaling properties of Flt-1 (VEGFR-1) and KDR (VEGFR-2). A reassessment using novel receptor-specific vascular endothelial growth factor mutants. J. Biol. Chem. 276 (2001), 3222–3230.
19. Harris, S., Craze, M., Newton, J., Fisher, M., Shima, D.T., Tozer, G.M., Kanthou, C., Do anti-angiogenic VEGF (VEGFxxxb) isoforms exist? A cautionary tale. PLoS ONE, 7, 2012, e35231.
20. Herbert, S.P., Stainier, D.Y., Molecular control of endothelial cell behaviour during blood vessel morphogenesis. Nat. Rev. Mol. Cell Biol. 12 (2011), 551–564.
21. Houck, K.A., Ferrara, N., Winer, J., Cachianes, G., Li, B., Leung, D.W., The vascular endothelial growth factor family: identification of a fourth molecular species and characterization of alternative splicing of RNA. Mol. Endocrinol. 5 (1991), 1806–1814.
22. Houck, K.A., Leung, D.W., Rowland, A.M., Winer, J., Ferrara, N., Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms. J. Biol. Chem. 267 (1992), 26031–26037.
23. Kawamura, H., Li, X., Harper, S.J., Bates, D.O., Claesson-Welsh, L., Vascular endothelial growth factor (VEGF)-A165b is a weak in vitro agonist for VEGF receptor-2 due to lack of coreceptor binding and deficient regulation of kinase activity. Cancer Res. 68 (2008), 4683–4692.
24. Kerbel, R.S., Tumor angiogenesis. N. Engl. J. Med. 358 (2008), 2039–2049.
25. Keyt, B.A., Berleau, L.T., Nguyen, H.V., Chen, H., Heinsohn, H., Vandlen, R., Ferrara, N., The carboxyl-terminal domain (111-165) of vascular endothelial growth factor is critical for its mitogenic potency. J. Biol. Chem. 271 (1996), 7788–7795.
26. LeCouter, J., Kowalski, J., Foster, J., Hass, P., Zhang, Z., Dillard-Telm, L., Frantz, G., Rangell, L., DeGuzman, L., Keller, G.-A., et al. Identification of an angiogenic mitogen selective for endocrine gland endothelium. Nature 412 (2001), 877–884.
27. Lee, S., Jilani, S.M., Nikolova, G.V., Carpizo, D., Iruela-Arispe, M.L., Processing of VEGF-A by matrix metalloproteinases regulates bioavailability and vascular patterning in tumors. J. Cell Biol. 169 (2005), 681–691.
28. Leung, D.W., Cachianes, G., Kuang, W.J., Goeddel, D.V., Ferrara, N., Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246 (1989), 1306–1309.
29. Li, B., Fuh, G., Meng, G., Xin, X., Gerritsen, M.E., Cunningham, B., de Vos, A.M., Receptor-selective variants of human vascular endothelial growth factor. Generation and characterization. J. Biol. Chem. 275 (2000), 29823–29828.
30. Li, X., Padhan, N., Sjöström, E.O., Roche, F.P., Testini, C., Honkura, N., Sáinz-Jaspeado, M., Gordon, E., Bentley, K., Philippides, A., et al. VEGFR2 pY949 signalling regulates adherens junction integrity and metastatic spread. Nat. Commun., 7, 2016, 11017.
31. Liang, W.C., Wu, X., Peale, F.V., Lee, C.V., Meng, Y.G., Gutierrez, J., Fu, L., Malik, A.K., Gerber, H.P., Ferrara, N., et al. Cross-species vascular endothelial growth factor (VEGF)-blocking antibodies completely inhibit the growth of human tumor xenografts and measure the contribution of stromal VEGF. J. Biol. Chem. 281 (2006), 951–961.
32. Namy, O., Rousset, J.P., Napthine, S., Brierley, I., Reprogrammed genetic decoding in cellular gene expression. Mol. Cell 13 (2004), 157–168.
33. Neufeld, G., Cohen, T., Gengrinovitch, S., Poltorak, Z., Vascular endothelial growth factor (VEGF) and its receptors. FASEB J. 13 (1999), 9–22.
34. Neufeld, G., Cohen, T., Shraga, N., Lange, T., Kessler, O., Herzog, Y., The neuropilins: multifunctional semaphorin and VEGF receptors that modulate axon guidance and angiogenesis. Trends Cardiovasc. Med. 12 (2002), 13–19.
35. Olsson, A.K., Dimberg, A., Kreuger, J., Claesson-Welsh, L., VEGF receptor signalling - in control of vascular function. Nat. Rev. Mol. Cell Biol. 7 (2006), 359–371.
36. Park, J.E., Keller, G.-A., Ferrara, N., The vascular endothelial growth factor (VEGF) isoforms: differential deposition into the subepithelial extracellular matrix and bioactivity of extracellular matrix-bound VEGF. Mol. Biol. Cell 4 (1993), 1317–1326.
37. 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. USA 102 (2005), 1076–1081.
38. Schueren, F., Lingner, T., George, R., Hofhuis, J., Dickel, C., Gärtner, J., Thoms, S., Peroxisomal lactate dehydrogenase is generated by translational readthrough in mammals. eLife, 3, 2014, e03640.
39. Senger, D.R., Galli, S.J., Dvorak, A.M., Perruzzi, C.A., Harvey, V.S., Dvorak, H.F., Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219 (1983), 983–985.
40. Shalaby, F., Rossant, J., Yamaguchi, T.P., Gertsenstein, M., Wu, X.F., Breitman, M.L., Schuh, A.C., Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376 (1995), 62–66.
41. Shao, Z., Friedlander, M., Hurst, C.G., Cui, Z., Pei, D.T., Evans, L.P., Juan, A.M., Tahiri, H., Duhamel, F., Chen, J., et al. Choroid sprouting assay: an ex vivo model of microvascular angiogenesis. PLoS ONE, 8, 2013, e69552.
42. Shevchenko, A., Wilm, M., Vorm, O., Mann, M., Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68 (1996), 850–858.
43. Soker, S., Takashima, S., Miao, H.Q., Neufeld, G., Klagsbrun, M., Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 92 (1998), 735–745.
44. Soker, S., Miao, H.Q., Nomi, M., Takashima, S., Klagsbrun, M., VEGF165 mediates formation of complexes containing VEGFR-2 and neuropilin-1 that enhance VEGF165-receptor binding. J. Cell. Biochem. 85 (2002), 357–368.
45. Tischer, E., Mitchell, R., Hartman, T., Silva, M., Gospodarowicz, D., Fiddes, J.C., Abraham, J.A., The human gene for vascular endothelial growth factor. Multiple protein forms are encoded through alternative exon splicing. J. Biol. Chem. 266 (1991), 11947–11954.
46. Vander Kooi, C.W., Jusino, M.A., Perman, B., Neau, D.B., Bellamy, H.D., Leahy, D.J., Structural basis for ligand and heparin binding to neuropilin B domains. Proc. Natl. Acad. Sci. USA 104 (2007), 6152–6157.
47. Whitaker, G.B., Limberg, B.J., Rosenbaum, J.S., Vascular endothelial growth factor receptor-2 and neuropilin-1 form a receptor complex that is responsible for the differential signaling potency of VEGF(165) and VEGF(121). J. Biol. Chem. 276 (2001), 25520–25531.
48. Woolard, J., Wang, W.Y., Bevan, H.S., Qiu, Y., Morbidelli, L., Pritchard-Jones, R.O., Cui, T.G., Sugiono, M., Waine, E., Perrin, R., et al. VEGF165b, an inhibitory vascular endothelial growth factor splice variant: mechanism of action, in vivo effect on angiogenesis and endogenous protein expression. Cancer Res. 64 (2004), 7822–7835.
49. Yu, L., Wu, X., Cheng, Z., Lee, C.V., LeCouter, J., Campa, C., Fuh, G., Lowman, H., Ferrara, N., Interaction between bevacizumab and murine VEGF-A: a reassessment. Invest. Ophthalmol. Vis. Sci. 49 (2008), 522–527.