Flt1 acts as a negative regulator of tip cell formation and branching morphogenesis in the zebrafish embryo

Development

Volumn 138, Issue 10, 2011, Pages 2111-2120

  Krueger, Janna ^a,b   Liu, Dong ^a   Scholz, Katja ^a   Zimmer, Anja ^a   Shi, Yu ^a   Klein, Christian ^a   Siekmann, Arndt ^c   Schulte Merker, Stefan ^d   Cudmore, Melissa ^e   Ahmed, Asif ^e   le Noble, Ferdinand ^a,b  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^d HUBRECHT INSTITUTE   (Netherlands)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Angiogenesis; Flt1; Nerves; Notch; Tip cells; VEGF; Zebrafish

Indexed keywords

NOTCH RECEPTOR; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 3;

ANIMAL TISSUE; ARTICLE; BLOOD FLOW; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; LOSS OF FUNCTION MUTATION; MACROPHAGE; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASE SEQUENCE; BLOOD VESSELS; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MACROPHAGES; NEOVASCULARIZATION, PHYSIOLOGIC; NERVOUS SYSTEM; OLIGODEOXYRIBONUCLEOTIDES, ANTISENSE; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; SOLUBILITY; TISSUE DISTRIBUTION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 79955555428     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.063933     Document Type: Article

References (46)

1. Alitalo, K., Tammela, T. and Petrova, T. V. (2005). Lymphangiogenesis in development and human disease. Nature 438, 946-953.
2. Ambati, B. K., Nozaki, M., Singh, N., Takeda, A., Jani, P. D., Suthar, T., Albuquerque, R. J., Richter, E., Sakurai, E., Newcomb, M. T. et al. (2006). Corneal avascularity is due to soluble VEGF receptor-1. Nature 443, 993-997.
3. Azzouz, M., Ralph, G. S., Storkebaum, E., Walmsley, L. E., Mitrophanous, K. A., Kingsman, S. M., Carmeliet, P. and Mazarakis, N. D. (2004). VEGF delivery with retrogradely transported lentivector prolongs survival in a mouse ALS model. Nature 429, 413-417.
4. 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.
5. Bussmann, J., Bakkers, J. and Schulte-Merker, S. (2007). Early endocardial morphogenesis requires Scl/Tal1. PLoS Genet. 3, e140.
6. Bussmann, J., Lawson, N., Zon, L. and Schulte-Merker, S. (2008). Zebrafish VEGF receptors: a guideline to nomenclature. PLoS Genet. 4, e1000064.
7. Carmeliet, P., De Smet, F., Loges, S. and Mazzone, M. (2009). Branching morphogenesis and antiangiogenesis candidates: tip cells lead the way. Nat. Rev. Clin. Oncol. 6, 315-326.
8. Chappell, J. C., Taylor, S. M., Ferrara, N. and Bautch, V. L. (2009). Local guidance of emerging vessel sprouts requires soluble Flt-1. Dev. Cell 17, 377-386.
9. Chi, N. C., Shaw, R. M., De Val, S., Kang, G., Jan, L. Y., Black, B. L. and Stainier, D. Y. (2008). Foxn4 directly regulates tbx2b expression and atrioventricular canal formation. Genes Dev. 22, 734-739.
10. 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.
11. 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.
12. Fantin, A., Vieira, J. M., Gestri, G., Denti, L., Schwarz, Q., Prykhozhij, S., Peri, F., Wilson, S. W. and Ruhrberg, C. (2010). Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction. Blood 116, 829-840.
13. Ferrara, N., Gerber, H. P. and LeCouter, J. (2003). The biology of VEGF and its receptors. Nat. Med. 9, 669-676.
14. Fong, G. H., Rossant, J., Gertsenstein, M. and Breitman, M. L. (1995). Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376, 66-70.
15. Gerhardt, H., Golding, M., Fruttiger, M., Ruhrberg, C., Lundkvist, A., Abramsson, A., Jeltsch, M., Mitchell, C., Alitalo, K., Shima, D. et al. (2003). VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 161, 1163-1177.
16. 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.
17. 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.
18. Hiratsuka, S., Minowa, O., Kuno, J., Noda, T. and Shibuya, M. (1998). Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice. Proc. Natl. Acad. Sci. USA 95, 9349-9354.
19. Hogan, B. M., Bos, F. L., Bussmann, J., Witte, M., Chi, N. C., Duckers, H. J. and Schulte-Merker, S. (2009a). Ccbe1 is required for embryonic lymphangiogenesis and venous sprouting. Nat. Genet. 41, 396-398.
20. Hogan, B. M., Herpers, R., Witte, M., Helotera, H., Alitalo, K., Duckers, H. J. and Schulte-Merker, S. (2009b). Vegfc/Flt4 signalling is suppressed by Dll4 in developing zebrafish intersegmental arteries. Development 136, 4001-4009.
21. Hsu, K., Traver, D., Kutok, J. L., Hagen, A., Liu, T. X., Paw, B. H., Rhodes, J., Berman, J. N., Zon, L. I., Kanki, J. P. et al. (2004). The pu.1 promoter drives myeloid gene expression in zebrafish. Blood 104, 1291-1297.
22. 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.
23. Jakobsson, L., Franco, C. A., Bentley, K., Collins, R. T., Ponsioen, B., Aspalter, I. M., Rosewell, I., Busse, M., Thurston, G., Medvinsky, A. et al. (2010). Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting. Nat. Cell Biol. 12, 943-953.
24. Jowett, T. and Lettice, L. (1994). Whole-mount in situ hybridizations on zebrafish embryos using a mixture of digoxigenin-and fluorescein-labelled probes. Trends Genet. 10, 73-74.
25. Lawson, N. D. and Weinstein, B. M. (2002). In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 248, 307-318.
26. Lawson, N. D., Vogel, A. M. and Weinstein, 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.
27. 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.
28. Liao, W., Bisgrove, B. W., Sawyer, H., Hug, B., Bell, B., Peters, K., Grunwald, D. J. and Stainier, D. Y. (1997). The zebrafish gene cloche acts upstream of a flk-1 homologue to regulate endothelial cell differentiation. Development 124, 381-389.
29. Lobov, I. B., Renard, R. A., Papadopoulos, N., Gale, N. W., Thurston, G., Yancopoulos, G. D. and Wiegand, S. J. (2007). Delta-like ligand 4 (Dll4) is induced by VEGF as a negative regulator of angiogenic sprouting. Proc. Natl. Acad. Sci. USA 104, 3219-3224.
30. Mukouyama, Y. S., Shin, D., Britsch, S., Taniguchi, M. and Anderson, D. J. (2002). Sensory nerves determine the pattern of arterial differentiation and blood vessel branching in the skin. Cell 109, 693-705.
31. Park, H. C., Kim, C. H., Bae, Y. K., Yeo, S. Y., Kim, S. H., Hong, S. K., Shin, J., Yoo, K. W., Hibi, M., Hirano, T. et al. (2000). Analysis of upstream elements in the HuC promoter leads to the establishment of transgenic zebrafish with fluorescent neurons. Dev. Biol. 227, 279-293.
32. Phng, L. K. and Gerhardt, H. (2009). Angiogenesis: a team effort coordinated by notch. Dev. Cell 16, 196-208.
33. Phng, L. K., Potente, M., Leslie, J. D., Babbage, J., Nyqvist, D., Lobov, I., Ondr, J. K., Rao, S., Lang, R. A., Thurston, G. et al. (2009). Nrarp coordinates endothelial Notch and Wnt signaling to control vessel density in angiogenesis. Dev. Cell 16, 70-82.
34. Poesen, K., Lambrechts, D., Van Damme, P., Dhondt, J., Bender, F., Frank, N., Bogaert, E., Claes, B., Heylen, L., Verheyen, A. et al. (2008). Novel role for vascular endothelial growth factor (VEGF) receptor-1 and its ligand VEGF-B in motor neuron degeneration. J. Neurosci. 28, 10451-10459.
35. Reyes, R., Haendel, M., Grant, D., Melancon, E. and Eisen, J. S. (2004). Slow degeneration of zebrafish Rohon-Beard neurons during programmed cell death. Dev. Dyn. 229, 30-41.
36. Roberts, D. M., Kearney, J. B., Johnson, J. H., Rosenberg, M. P., Kumar, R. and Bautch, V. L. (2004). The vascular endothelial growth factor (VEGF) receptor Flt-1 (VEGFR-1) modulates Flk-1 (VEGFR-2) signaling during blood vessel formation. Am. J. Pathol. 164, 1531-1535.
37. Roca, C. and Adams, R. H. (2007). Regulation of vascular morphogenesis by Notch signaling. Genes Dev. 21, 2511-2524.
38. Rottbauer, W., Just, S., Wessels, G., Trano, N., Most, P., Katus, H. A. and Fishman, M. C. (2005). VEGF-PLCgamma1 pathway controls cardiac contractility in the embryonic heart. Genes Dev. 19, 1624-1634.
39. Ruiz de Almodovar, C., Lambrechts, D., Mazzone, M. and Carmeliet, P. (2009). Role and therapeutic potential of VEGF in the nervous system. Physiol. Rev. 89, 607-648.
40. Sela, S., Itin, A., Natanson-Yaron, S., Greenfield, C., Goldman-Wohl, D., Yagel, S. and Keshet, E. (2008). A novel human-specific soluble vascular endothelial growth factor receptor 1, cell-type-specific splicing and implications to vascular endothelial growth factor homeostasis and preeclampsia. Circ. Res. 102, 1566-1574.
41. Siekmann, A. F. and Lawson, N. D. (2007). Notch signalling limits angiogenic cell behaviour in developing zebrafish arteries. Nature 445, 781-784.
42. Storkebaum, E., Lambrechts, D., Dewerchin, M., Moreno-Murciano, M. P., Appelmans, S., Oh, H., Van Damme, P., Rutten, B., Man, W. Y., De Mol, M. et al. (2005). Treatment of motoneuron degeneration by intracerebroventricular delivery of VEGF in a rat model of ALS. Nat. Neurosci. 8, 85-92.
43. 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.
44. Swendeman, S., Mendelson, K., Weskamp, G., Horiuchi, K., Deutsch, U., Scherle, P., Hooper, A., Rafii, S. and Blobel, C. P. (2008). VEGF-A stimulates ADAM17-dependent shedding of VEGFR2 and crosstalk between VEGFR2 and ERK signaling. Circ. Res. 103, 916-918.
45. 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.
46. Villefranc, J. A., Amigo, J. and Lawson, N. D. (2007). Gateway compatible vectors for analysis of gene function in the zebrafish. Dev. Dyn. 236, 3077-3087.