Vegfc/Flt4 signalling is suppressed by Dll4 in developing zebrafish intersegmental arteries

Development

Volumn 136, Issue 23, 2009, Pages 4001-4009

  Hogan, Benjamin M ^a,b   Herpers, Robert ^a,b,c   Witte, Merlijn ^a,b   Heloterä, Hanna ^d   Alitalo, Kari ^d   Duckers, Henricus J ^c   Schulte Merker, Stefan ^a,b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b Centre for Biomedical Genetics   (Netherlands)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Arterial; Dll4; Flt4; Lymphatics; Vegfc; Zebrafish

Indexed keywords

GENE PRODUCT; PROTEIN DLL4; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 3;

ANGIOGENESIS; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENDOTHELIUM CELL; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCUS; GENE MAPPING; GENE MUTATION; GENE OVEREXPRESSION; GENETIC ANALYSIS; GENETIC SCREENING; GENOTYPE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ARTERIES; EMBRYO, NONMAMMALIAN; MEMBRANE PROTEINS; MUTATION; NEOVASCULARIZATION, PHYSIOLOGIC; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR C; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3; ZEBRAFISH;

DANIO RERIO;

EID: 70450195982     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.039990     Document Type: Article

References (42)

1. Bahary, N., Goishi, K., Stuckenholz, C., Weber, G., Leblanc, J., Schafer, C. A., Berman, S. S., Klagsbrun, M. and Zon, L. I. (2007). Duplicate VegfA genes and orthologues of the KDR receptor tyrosine kinase family mediate vascular development in the zebrafish. Blood 110, 3627-3636.
2. Baldwin, M. E., Catimel, B., Nice, E. C., Roufail, S., Hall, N. E., Stenvers, K. L., Karkkainen, M. J., Alitalo, K., Stacker, S. A. and Achen, M. G. (2001). The specificity of receptor binding by vascular endothelial growth factor-d is different in mouse and man. J. Biol. Chem. 276, 19166-19171.
3. Benedito, R., Roca, C., Sorensen, I., Adams, S., Gossler, A., Fruttiger, M. and Adams, R. H. (2009). The notch ligands Dll4 and Jagged1 have opposing effects on angiogenesis. Cell 137, 1124-1135.
4. Bussmann, J., Bakkers, J. and Schulte-Merker, S. (2007). Early endocardial morphogenesis requires Scl/Tal1. PLoS Genet. 3, e140.
5. Bussmann, J., Lawson, N., Zon, L. and Schulte-Merker, S.; Zebrafish Nomenclature Committee. (2008). Zebrafish VEGF receptors: a guideline to nomenclature. PLOS Genet. 4, e1000064.
6. Covassin, L. D., Villefranc, J. A., Kacergis, M. C., Weinstein, 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.
7. Covassin, L. D., Siekmann, A. F., Kacergis, M. C., Laver, E., Moore, J. C., Villefranc, J. A., Weinstein, 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.
8. Dumont, D. J., Jussila, L., Taipale, J., Lymboussaki, A., Mustonen, T., Pajusola, K., Breitman, M. and Alitalo, K. (1998). Cardiovascular failure in mouse embryos deficient in VEGF receptor-3. Science 282, 946-949.
9. Geling, A., Steiner, H., Willem, M., Bally-Cuif, L. and Haass, C. (2002). A gamma-secretase inhibitor blocks Notch signaling in vivo and causes a severe neurogenic phenotype in zebrafish. EMBO Rep. 3, 688-694.
10. Habeck, H., Odenthal, J., Walderich, B., Maischein, H. and Schulte-Merker, S. (2002). Analysis of a zebrafish VEGF receptor mutant reveals specific disruption of angiogenesis. Curr. Biol. 12, 1405-1412.
11. Haiko, P., Makinen, T., Keskitalo, S., Taipale, J., Karkkainen, M. J., Baldwin, M. E., Stacker, S. A., Achen, M. G. and Alitalo, K. (2008). Deletion of vascular endothelial growth factor C (VEGF-C) and VEGF-D is not equivalent to VEGF receptor 3 deletion in mouse embryos. Mol. Cell. Biol. 28, 4843-4850.
12. He, Y., Kozaki, K., Karpanen, T., Koshikawa, K., Yla-Herttuala, S., Takahashi, T. and Alitalo, K. (2002). Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling. J. Natl. Cancer Inst. 94, 819-825.
13. Hellstrom, M., Phng, L. K., Hofmann, J. J., Wallgard, E., Coultas, L., Lindblom, P., Alva, J., Nilsson, A. K., Karlsson, L., Gaiano, N. et al. (2007). Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445, 776-780.
14. Herpers, R., van de Kamp, E., Duckers, H. J. and Schulte-Merker, S. (2008). Redundant roles for sox7 and sox18 in arteriovenous specification in zebrafish. Circ. Res. 102, 12-15.
15. Hogan, B. M., Bos, F. L., Bussmann, J., Witte, M., Chi, N. C., Duckers, H. J. and Schulte-Merker, S. (2009). Ccbe1 is required for embryonic lymphangiogenesis and venous sprouting. Nat. Genet. 41, 396-398.
16. Isogai, S., Lawson, N. D., Torrealday, S., Horiguchi, M. and Weinstein, B. M. (2003). Angiogenic network formation in the developing vertebrate trunk. Development 130, 5281-5290.
17. Karkkainen, M. J., Ferrell, R. E., Lawrence, E. C., Kimak, M. A., Levinson, K. L., McTigue, M. A., Alitalo, K. and Finegold, D. N. (2000). Missense mutations interfere with VEGFR-3 signalling in primary lymphoedema. Nat. Genet. 25, 153-159.
18. Karkkainen, M. J., Haiko, P., Sainio, K., Partanen, J., Taipale, J., Petrova, T. V., Jeltsch, M., Jackson, D. G., Talikka, M., Rauvala, H. et al. (2004). Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat. Immunol. 5, 74-80.
19. Karpanen, T., Egeblad, M., Karkkainen, M. J., Kubo, H., Yla-Herttuala, S., Jaattela, M. and Alitalo, K. (2001). Vascular endothelial growth factor C promotes tumor lymphangiogenesis and intralymphatic tumor growth. Cancer Res. 61, 1786-1790.
20. Kawakami, K. (2005). Transposon tools and methods in zebrafish. Dev. Dyn. 234, 244-254.
21. Kuchler, A. M., Gjini, E., Peterson-Maduro, J., Cancilla, B., Wolburg, H. and Schulte-Merker, S. (2006). Development of the zebrafish lymphatic system requires VEGFC signaling. Curr. Biol. 16, 1244-1248.
22. Lawson, N. D. and Weinstein, B. M. (2002). In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 248, 307-318.
23. Lawson, N. D., Scheer, N., Pham, V. N., Kim, C. H., Chitnis, A. B., Campos- Ortega, J. A. and Weinstein, B. M. (2001). Notch signaling is required for arterial-venous differentiation during embryonic vascular development. Development 128, 3675-3683.
24. Lawson, N. D., Mugford, J. W., Diamond, B. A. and Weinstein, B. M. (2003). phospholipase C gamma-1 is required downstream of vascular endothelial growth factor during arterial development. Genes Dev. 17, 1346-1351.
25. Leslie, J. D., Ariza-McNaughton, L., Bermange, A. L., McAdow, R., Johnson, S. L. and Lewis, J. (2007). Endothelial signalling by the Notch ligand Delta-like 4 restricts angiogenesis. Development 134, 839-844.
26. Lyons, M. S., Bell, B., Stainier, D. and Peters, K. G. (1998). Isolation of the zebrafish homologues for the tie-1 and tie-2 endothelium-specific receptor tyrosine kinases. Dev. Dyn. 212, 133-140.
27. Makinen, T., Jussila, L., Veikkola, T., Karpanen, T., Kettunen, M. I., Pulkkanen, K. J., Kauppinen, R., Jackson, D. G., Kubo, H., Nishikawa, S. et al. (2001). Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor-3. Nat. Med. 7, 199-205.
28. Meng, X., Noyes, M. B., Zhu, L. J., Lawson, N. D. and Wolfe, S. A. (2008). Targeted gene inactivation in zebrafish using engineered zinc-finger nucleases. Nat. Biotechnol. 26, 695-701.
29. Nasevicius, A., Larson, J. and Ekker, S. C. (2000). Distinct requirements for zebrafish angiogenesis revealed by a VEGF-A morphant. Yeast 17, 294-301.
30. Noguera-Troise, I., Daly, C., Papadopoulos, N. J., Coetzee, S., Boland, P., Gale, N. W., Lin, H. C., Yancopoulos, G. D. and Thurston, G. (2006). Blockade of Dll4 inhibits tumour growth by promoting non-productive angiogenesis. Nature 444, 1032-1037.
31. Ober, E. A., Olofsson, B., Makinen, T., Jin, S. W., Shoji, W., Koh, G. Y., Alitalo, K. and Stainier, D. Y. (2004). Vegfc is required for vascular development and endoderm morphogenesis in zebrafish. EMBO Rep. 5, 78-84.
32. Petrova, T. V., Bono, P., Holnthoner, W., Chesnes, J., Pytowski, B., Sihto, H., Laakkonen, P., Heikkila, P., Joensuu, H. and Alitalo, K. (2008). VEGFR-3 expression is restricted to blood and lymphatic vessels in solid tumors. Cancer Cell 13, 554-556.
33. Saharinen, P., Ekman, N., Sarvas, K., Parker, P., Alitalo, K. and Silvennoinen, O. (1997). The Bmx tyrosine kinase induces activation of the Stat signaling pathway, which is specifically inhibited by protein kinase Cdelta. Blood 90, 4341-4353.
34. Siekmann, A. F. and Lawson, N. D. (2007). Notch signalling limits angiogenic cell behaviour in developing zebrafish arteries. Nature 445, 781-784.
35. Smithers, L., Haddon, C., Jiang, Y. J. and Lewis, J. (2000). Sequence and embryonic expression of deltaC in the zebrafish. Mech. Dev. 90, 119-123.
36. Suchting, S., Freitas, C., le Noble, F., Benedito, R., Breant, C., Duarte, A. and Eichmann, A. (2007). The Notch ligand Delta-like 4 negatively regulates endothelial tip cell formation and vessel branching. Proc. Natl. Acad. Sci. USA 104, 3225-3230.
37. Tammela, T., Zarkada, G., Wallgard, E., Murtomaki, A., Suchting, S., Wirzenius, M., Waltari, M., Hellstrom, M., Schomber, T., Peltonen, R. et al. (2008). Blocking VEGFR-3 suppresses angiogenic sprouting and vascular network formation. Nature 454, 656-660.
38. Thompson, M. A., Ransom, D. G., Pratt, S. J., MacLennan, H., Kieran, M. W., Detrich, H. W., 3rd, Vail, B., Huber, T. L., Paw, B., Brownlie, A. J. et al. (1998). The cloche and spadetail genes differentially affect hematopoiesis and vasculogenesis. Dev. Biol. 197, 248-269.
39. Veikkola, T., Jussila, L., Makinen, T., Karpanen, T., Jeltsch, M., Petrova, T. V., Kubo, H., Thurston, G., McDonald, D. M., Achen, M. G. et al. (2001). Signalling via vascular endothelial growth factor receptor-3 is sufficient for lymphangiogenesis in transgenic mice. EMBO J. 20, 1223-1231.
40. Wienholds, E., Schulte-Merker, S., Walderich, B. and Plasterk, R. H. (2002). Target-selected inactivation of the zebrafish rag1 gene. Science 297, 99-102.
41. Yaniv, K., Isogai, S., Castranova, D., Dye, L., Hitomi, J. and Weinstein, B. M. (2006). Live imaging of lymphatic development in the zebrafish. Nat. Med. 12, 711-716.
42. Zhong, T. P., Rosenberg, M., Mohideen, M. A., Weinstein, B. and Fishman, M. C. (2000). gridlock, an HLH gene required for assembly of the aorta in zebrafish. Science 287, 1820-1824.