Vegfa signals through ERK to promote angiogenesis, but not artery differentiation

Development (Cambridge)

Volumn 143, Issue 20, 2016, Pages 3796-3805

  Shin, Masahiro ^a   Beane, Timothy J ^a   Quillien, Aurelie ^a,b   Male, Ira ^a,c   Zhu, Lihua J ^a   Lawson, Nathan D ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b UNIVERSITÉ DE TOULOUSE   (France)

^c UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

Angiogenesis; Artery differentiation; ERK; Vegfa; Zebrafish

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; NOTCH RECEPTOR; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 3;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTERY ENDOTHELIUM; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CONTROLLED STUDY; ECTOPIC EXPRESSION; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL CELL; ZEBRA FISH; ANIMAL; ARTERY; CYTOLOGY; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; PHYSIOLOGY; TRANSGENIC ANIMAL; WESTERN BLOTTING;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ARTERIES; BLOTTING, WESTERN; CELL DIFFERENTIATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; IN SITU HYBRIDIZATION; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3; ZEBRAFISH;

EID: 84991783867     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.137919     Document Type: Article

References (40)

1. Anderson, M. J., Pham, V. N., Vogel, A. M., Welnsteln, B. M. and Roman, B. L. (2008). Loss of unc45a precipitates arteriovenous shunting in the aortic arches. Dev. Biol. 318, 258-267.
2. Asakawa, K. and Kawakaml, K. (2008). Targeted gene expression by the Gal4-UAS system in zebrafish. Dev. Growth Differ. 50, 391-399.
3. Bussmann, J., Lawson, N., Zon, L., Schulte-Merker, S. and Zebraflsh Nomenclature Commlttee. (2008). Zebrafish VEGF receptors: a guideline to nomenclature. PLoS Genet. 4, e1000064.
4. Bussmann, J., Wolfe, S. A. and Slekmann, A. F. (2011). Arterial-venous network formation during brain vascularization involves hemodynamic regulation of chemokine signaling. Development 138, 1717-1726.
5. Carmellet, P., Ferrelra, V., Breler, G., Pollefeyt, S., Kleckens, L., Gertsensteln, M., Fahrlg, M., Vandenhoeck, A., Harpal, K., Eberhardt, C. et al. (1996). Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380, 435-439.
6. Cleaver, O. and Krleg, P. A. (2010). Vascular development. In Heart Development and Regeneration (ed. N. Rosenthal and R. P. Harvey), pp. 487-528. London, UK: Elsevier Inc.
7. Covassln, L. D., Vlllefranc, J. A., Kacergls, M. C., Welnsteln, B. M. and Lawson, N. D. (2006). Distinct genetic interactions between multiple Vegf receptors are required for development of different blood vessel types in zebrafish. Proc. Natl. Acad. Sci. USA 103, 6554-6559.
8. Covassln, L. D., Slekmann, A. F., Kacergls, M. C., Laver, E., Moore, J. C., Vlllefranc, J. A., Welnsteln, B. M. and Lawson, N. D. (2009). A genetic screen for vascular mutants in zebrafish reveals dynamic roles for Vegf/Plcg1 signaling during artery development. Dev. Biol. 329, 212-226.
9. Duarte, A., Hlrashlma, M., Benedlto, R., Trlndade, A., Dlnlz, P., Bekman, E., Costa, L., Henrlque, D. and Rossant, J. (2004). Dosage-sensitive requirement for mouse Dll4 in artery development. Genes Dev. 18, 2474-2478.
10. Gerber, H.-P., McMurtrey, A., Kowalskl, J., Yan, M., Keyt, B. A., Dlxlt, V. and Ferrara, N. (1998). Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J. Biol. Chem. 273, 30336-30343.
11. Goll, M. G., Anderson, R., Stalnler, D. Y. R., Spradllng, A. C. and Halpern, M. E. (2009). Transcriptional silencing and reactivation in transgenic zebrafish. Genetics 182, 747-755.
12. Graupera, M., Gulllermet-Gulbert, J., Foukas, L. C., Phng, L.-K., Caln, R. J., Salpekar, A., Pearce, W., Meek, S., Mlllan, J., Cutlllas, P. R. et al. (2008). Angiogenesis selectively requires the p110alpha isoform of PI3K to control endothelial cell migration. Nature 453, 662-666.
13. Hellstrom, M., Phng, L.-K., Hofmann, J. J., Wallgard, E., Coultas, L., Llndblom, P., Alva, J., Nllsson, A.-K., Karlsson, L., Galano, N. et al. (2007). Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445, 776-780.
14. Hogan, B. M., Herpers, R., Wltte, M., Helotera, H., Alltalo, K., Duckers, H. J. and Schulte-Merker, S. (2009). Vegfc/Flt4 signalling is suppressed by Dll4 in developing zebrafish intersegmental arteries. Development 136, 4001-4009.
15. Hong, C. C., Peterson, Q. P., Hong, J.-Y. and Peterson, R. T. (2006). Artery/vein specification is governed by opposing phosphatidylinositol-3 kinase and MAP kinase/ERK signaling. Curr. Biol. 16, 1366-1372.
16. Isogal, S., Lawson, N. D., Torrealday, S., Horlguchl, M. and Welnsteln, B. M. (2003). Angiogenic network formation in the developing vertebrate trunk. Development 130, 5281-5290.
17. Itoh, M., Klm, C.-H., Palardy, G., Oda, T., Jlang, Y.-J., Maust, D., Yeo, S.-Y., Lorlck, K., Wrlght, G. J., Arlza-McNaughton, L. et al. (2003). Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta. Dev. Cell 4, 67-82.
18. Koch, S. and Claesson-Welsh, L. (2012). Signal transduction by vascular endothelial growth factor receptors. Cold Spring Harb. Perspect. Med. 2, a006502.
19. Lawson, N. D. and Welnsteln, B. M. (2002). In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 248, 307-318.
20. Lawson, N. D., Scheer, N., Pham, V. N., Klm, C. H., Chltnls, A. B., Campos-Ortega, J. A. and Welnsteln, B. M. (2001). Notch signaling is required for arterial-venous differentiation during embryonic vascular development. Development 128, 3675-3683.
21. Lawson, N. D., Vogel, A. M. and Welnsteln, B. M. (2002). sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation. Dev. Cell 3, 127-136.
22. Lawson, N. D., Mugford, J. W., Dlamond, B. A. and Welnsteln, B. M. (2003). phospholipase C gamma-1 is required downstream of vascular endothelial growth factor during arterial development. Genes Dev. 17, 1346-1351.
23. Leslle, J. D., Arlza-McNaughton, L., Bermange, A. L., McAdow, R., Johnson, S. L. and Lewls, J. (2007). Endothelial signalling by the Notch ligand Delta-like 4 restricts angiogenesis. Development 134, 839-844.
24. Marchettl, S., Glmond, C., Chambard, J.-C., Touboul, T., Roux, D., Pouyssegur, J. and Pages, G. (2005). Extracellular signal-regulated kinases phosphorylate mitogen-activated protein kinase phosphatase 3/DUSP6 at serines 159 and 197, two sites critical for its proteasomal degradation. Mol. Cell. Biol. 25, 854-864.
25. Moore, J. C., Sheppard, S., Shestopalov, I. A., Chen, J. K. and Lawson, N. D. (2013). Post-transcriptional mechanisms contribute to Etv2 repression during vascular development. Dev. Biol. 384, 128-140.
26. Muda, M., Theodoslou, A., Rodrlgues, N., Boschert, U., Camps, M., Glllleron, C., Davles, K., Ashworth, A. and Arklnstall, S. (1996). The dual specificity phosphatases M3/6 and MKP-3 are highly selective for inactivation of distinct mitogen-activated protein kinases. J. Biol. Chem. 271, 27205-27208.
27. Pajusola, K., Aprellkova, O., Pellccl, G., Welch, H., Claesson-Welsh, L. and Alltalo, K. (1994). Signalling properties of FLT4, a proteolytically processed receptor tyrosine kinase related to two VEGF receptors. Oncogene 9, 3545-3555.
28. Potente, M., Gerhardt, H. and Carmellet, P. (2011). Basic and therapeutic aspects of angiogenesis. Cell 146, 873-887.
29. Qullllen, A., Moore, J. C., Shln, M., Slekmann, A. F., Smlth, T., Pan, L., Moens, C. B., Parsons, M. J. and Lawson, N. D. (2014). Distinct Notch signaling outputs pattern the developing arterial system. Development 141, 1544-1552.
30. Sakural, Y., Ohglmoto, K., Kataoka, Y., Yoshlda, N. and Shlbuya, M. (2005). Essential role of Flk-1 (VEGF receptor 2) tyrosine residue 1173 in vasculogenesis in mice. Proc. Natl. Acad. Sci. USA 102, 1076-1081.
31. Scheer, N. and Campos-Ortega, J. A. (1999). Use of the Gal4-UAS technique for targeted gene expression in the zebrafish. Mech. Dev. 80, 153-158.
32. Shalaby, F., Ho, J., Stanford, W. L., Flscher, K.-D., Schuh, A. C., Schwartz, L., Bernsteln, A. and Rossant, J. (1997). A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell 89, 981-990.
33. Shln, M., Male, I., Beane, T. J., Vlllefranc, J. A., Kok, F. O., Zhu, L. J. and Lawson, N. D. (2016). Vegfc acts through ERK to induce sprouting and differentiation of trunk lymphatic progenitors. Development 143, 3785-3795.
34. Slekmann, A. F. and Lawson, N. D. (2007). Notch signalling limits angiogenic cell behaviour in developing zebrafish arteries. Nature 445, 781-784.
35. Srlnlvasan, R., Zabuawala, T., Huang, H., Zhang, J., Gulatl, P., Fernandez, S., Karlo, J. C., Landreth, G. E., Leone, G. and Ostrowskl, M. C. (2009). Erk1 and Erk2 regulate endothelial cell proliferation and migration during mouse embryonic angiogenesis. PLoS ONE 4, e8283.
36. Stalmans, I., Ng, Y.-S., Rohan, R., Fruttlger, M., Bouche, A., Yuce, A., Fujlsawa, H., Hermans, B., Shanl, M., Jansen, S. et al. (2002). Arteriolar and venular patterning in retinas of mice selectively expressing VEGF isoforms. J. Clin. Invest. 109, 327-336.
37. Takahashl, T., Yamaguchl, S., Chlda, K. and Shlbuya, M. (2001). 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, 2768-2778.
38. Vlllefranc, J. A., Amlgo, J. and Lawson, N. D. (2007). Gateway compatible vectors for analysis of gene function in the zebrafish. Dev. Dyn. 236, 3077-3087.
39. Vlllefranc, J. A., Nlcoll, S., Bentley, K., Jeltsch, M., Zarkada, G., Moore, J. C., Gerhardt, H., Alltalo, K. and Lawson, N. D. (2013). A truncation allele in vascular endothelial growth factor c reveals distinct modes of signaling during lymphatic and vascular development. Development 140, 1497-1506.
40. Wythe, J. D., Dang, L. T. H., Devlne, W. P., Boudreau, E., Artap, S. T., He, D., Schachterle, W., Stalnler, D. Y. R., Oettgen, P., Black, B. L. et al. (2013). ETS factors regulate Vegf-dependent arterial specification. Dev. Cell 26, 45-58.