Cellular and molecular analyses of vascular tube and lumen formation in zebrafish

Development

Volumn 132, Issue 23, 2005, Pages 5199-5209

  Jin, Suk Won ^a   Beis, Dimitris ^a,c   Mitchell, Tracy ^a,d   Chen, Jau Nian ^b   Stainier, Didier Y R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Academy of Athens Biomedical Research Foundation   (Greece)

^d OSI Eyetech   (United States)

Author keywords

Angioblast; Endoderm; Endothelial cell; Migration; VEGF; Zebrafish

Indexed keywords

GREEN FLUORESCENT PROTEIN; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL JUNCTION; CELL LINE; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; ENDODERM; ENDOTHELIUM CELL; GENE MUTATION; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSGENE; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BLOOD VESSELS; BODY PATTERNING; CELL MOVEMENT; EMBRYO, NONMAMMALIAN; ENDODERM; ENDOTHELIAL CELLS; GREEN FLUORESCENT PROTEINS; INTERCELLULAR JUNCTIONS; PROMOTER REGIONS (GENETICS); STEM CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; ZEBRAFISH;

ANIMALIA; AVES; DANIO RERIO;

EID: 29644439510     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02087     Document Type: Article

References (62)

1. Alexander, J. and Stainier, D. Y. (1999). A molecular pathway leading to endoderm formation in zebrafish. Curr. Biol. 9, 1147-1157.
2. Alexander, J., Rothenberg, M., Henry, G. L. and Stainier, D. Y. (1999). casanova plays an early and essential role in endoderm formation in zebrafish. Dev. Biol. 215, 343-357.
3. Bielinska, M., Narita, N., Heikinheimo, M., Porter, S. B. and Wilson, D. B. (1996). Erythropoiesis and vasculogenesis in embryoid bodies lacking visceral yolk sac endoderm. Blood 88, 3720-3730.
4. Carmeliet, P. and Storkebaum, E. (2002). Vascular and neuronal effects of VEGF in the nervous system: implications for neurological disorders. Semin. Cell Dev. Biol. 13, 39-53.
5. Carmeliet, P., Ferreira, V., Breier, G., Pollefeyt, S., Kieckens, L., Gertsenstein, M., Fahrig, 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. Chan, J., Mably, J. D., Serluca, F. C., Chen, J. N., Goldstein, N. B., Thomas, M. C., Cleary, J. A., Brennan, C., Fishman, M. C. and Roberts, T. M. (2001). Morphogenesis of prechordal plate and notochord requires intact Eph/ephrin B signaling. Dev. Biol. 234, 470-482.
7. Chan, J., Bayliss, P. E., Wood, J. M. and Roberts, T. M. (2002). Dissection of angiogenic signaling in zebrafish using a chemical genetic approach. Cancer Cell 1, 257-267.
8. Childs, S., Chen, J. N., Garrity, D. M. and Fishman, M. C. (2002). Patterning of angiogenesis in the zebrafish embryo. Development 129, 973-982.
9. Cleaver, O. and Krieg, P. A. (1998). VEGF mediates angioblast migration during development of the dorsal aorta in Xenopus. Development 125, 3905-3914.
10. Cleaver, O., Tonissen, K. F., Saba, M. S. and Krieg, P. A. (1997). Neovascularization of the Xenopus embryo. Dev. Dyn. 210, 66-77.
11. Cross, L. M., Cook, M. A., Lin, S., Chen, J. N. and Rubinstein, A. L. (2003). Rapid analysis of angiogenesis drugs in a live fluorescent zebrafish assay. Arterioscler. Thromb. Vasc. Biol. 23, 911-912.
12. Eichmann, A., Corbel, C., Jaffredo, T., Breant, C., Joukov, V., Kumar, V., Alitalo, K. and le Douarin, N. M. (1998). Avian VEGF-C: cloning, embryonic expression pattern and stimulation of the differentiation of VEGFR2-expressing endothelial cell precursors. Development 125, 743-752.
13. Ferrara, N., Carver-Moore, K., Chen, H., Dowd, M., Lu, L., O'Shea, K. S., Powell-Braxton, L., Hillan, K. J. and Moore, M. W. (1996). Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380, 439-442.
14. Fong, T. A., Shawver, L. K., Sun, L., Tang, C., App, H., Powell, T. J., Kim, Y. H., Schreck, R., Wang, X., Risau, W. et al. (1999). SU5416 is a potent and selective inhibitor of the vascular endothelial growth factor receptor (Flk-1/KDR) that inhibits tyrosine kinase catalysis, tumor vascularization, and growth of multiple tumor types. Cancer Res. 59, 99-106.
15. Fouquet, B., Weinstein, B. M., Serluca, F. C. and Fishman, M. C. (1997). Vessel patterning in the embryo of the zebrafish: guidance by notochord. Dev. Biol. 183, 37-48.
16. Gering, M., Rodaway, A. R., Gottgens, B., Patient, R. K. and Green, A. R. (1998). The SCL gene specifies haemangioblast development from early mesoderm. EMBO J. 17, 4029-4045.
17. 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.
18. Hashimoto, T., Zhang, X. M. and Yang, X. J. (2003). Expression of the Flk1 receptor and its ligand VEGF in the developing chick central nervous system. Gene Expr. Patterns 3, 109-113.
19. Horne-Badovinac, S., Lin, D., Waldron, S., Schwarz, M., Mbamalu, G., Pawson, T., Jan, Y., Stainier, D. Y. and Abdelilah-Seyfried, S. (2001). Positional cloning of heart and soul reveals multiple roles for PKC lambda in zebrafish organogenesis. Curr. Biol. 11, 1492-1502.
20. Horne-Badovinac, S., Rebagliati, M. and Stainier, D. Y. (2003). A cellular framework for gut-looping morphogenesis in zebrafish. Science 302, 662-665.
21. Isogai, S., Horiguchi, M. and Weinstein, B. M. (2001). The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development. Dev. Biol. 230, 278-301.
22. Joukov, V., Pajusola, K., Kaipainen, A., Chilov, D., Lahtinen, I., Kukk, E., Saksela, O., Kalkkinen, N. and Alitalo, K. (1996). A novel vascular endothelial growth factor, VEGF-C, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases. EMBO J. 15, 290-298.
23. Kataoka, H., Ochi, M., Enomoto, K. and Yamaguchi, A. (2000). Cloning and embryonic expression patterns of the zebrafish Runt domain genes, runxa and runxb. Mech. Dev. 98, 139-143.
24. Kikuchi, Y., Trinh, L. A., Reiter, J. F., Alexander, J., Yelon, D. and Stainier, D. Y. (2000). The zebrafish bonnie and clyde gene encodes a Mix family homeodomain protein that regulates the generation of endodermal precursors. Genes Dev. 14, 1279-1289.
25. Kikuchi, Y., Agathon, A., Alexander, J., Thisse, C., Waldron, S., Yelon, D., Thissue, B. and Stainier, D. Y. (2001). casanova encodes a novel Sox-related protein necessary and sufficient for early endoderm formation in zebrafish. Genes Dev. 15, 1493-1505.
26. Larson, J. D., Wadman, S. A., Chen, E., Kerley, L., Clark, K. J., Eide, M., Lippert, S., Nasevicious, A., Ekker, S. C., Hackett, P. B. et al. (2004). Expression of VE-cadherin in zebrafish embryos: a new tool to evaluate vascular development. Dev. Dyn. 231, 204-213.
27. Lawson, N. D. and Weinstein, B. M. (2002). In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 248, 307-318.
28. 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.
29. 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.
30. 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.
31. Liang, D., Xu, X., Chin, A. J., Balasubramaniyan, N. V., Teo, M. A., Lam, T. J., Weinberg, E. S. and Ge, R. (1998). Cloning and characterization of vascular endothelial growth factor (VEGF) from zebrafish, Danio rerio. Biochim. Biophys. Acta 1397, 14-20.
32. Liao, E. C., Paw, B. H., Oates, A. C., Pratt, S. J., Postlethwait, J. H. and Zon, L. I. (1998). SCL/Tal-1 transcription factor acts downstream of cloche to specify hematopoietic and vascular progenitors in zebrafish. Genes Dev. 12, 621-626.
33. 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.
34. 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.
35. Motoike, T., Loughna, S., Perens, E., Roman, B. L., Liao, W., Chau, T. C., Richardson, C. D., Kawate, T., Kuno, J., Weinstein, B. M. et al. (2000). Universal GFP reporter for the study of vascular development. Genesis 28, 75-81.
36. Nasevicius, A. and Ekker, S. C. (2000). Effective targeted gene 'knockdown' in zebrafish. Nat. Genet. 26, 216-220.
37. 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.
38. Oomman, S., Finckbone, V., Dertien, J., Attridge, J., Henne, W., Medina, M., Mansouri, B., Singh, H., Strahlendorf, H. and Strahlendorf, J. (2004). Active caspase-3 expression during postnatal development of rat cerebellum is not systematically or consistently associated with apoptosis. J. Comp. Neurol. 476, 154-173.
39. Palis, J., McGrath, K. E. and Kingsley, P. D. (1995). Initiation of hematopoiesis and vasculogenesis in murine yolk sac explants. Blood 86, 156-163.
40. Pardanaud, L., Altmann, C., Kitos, P., Dieterlen-Lievre, F. and Buck, C. A. (1987). Vasculogenesis in the early quail blastodisc as studied with a monoclonal antibody recognizing endothelial cells. Development 100, 339-349.
41. Parker, L. H., Schmidt, M., Jin, S. W., Gray, A. M., Beis, D., Pham, T., Frantz, G., Palmieri, S., Hillan, K., Stainier, D. Y. et al. (2004). The endothelial-cell-derived secreted factor Egfl7 regulates vascular tube formation. Nature 428, 754-758.
42. Pham, V. N., Roman, B. L. and Weinstein, B. M. (2001). Isolation and expression analysis of three zebrafish angiopoietin genes. Dev. Dyn. 221, 470-474.
43. Quinn, T. P., Peters, K. G., De Vries, C., Ferrara, N. and Williams, L. T. (1993). Fetal liver kinase 1 is a receptor for vascular endothelial growth factor and is selectively expressed in vascular endothelium. Proc. Natl. Acad. Sci. USA 90, 7533-7537.
44. Sa, G., Murugesan, G., Jaye, M., Ivashchenko, Y. and Fox, P. L. (1995). Activation of cytosolic phospholipase A2 by basic fibroblast growth factor via a p42 mitogen-activated protein kinase-dependent phosphorylation pathway in endothelial cells. J. Biol. Chem. 270, 2360-2366.
45. Sehnert, A. J., Huq, A., Weinstein, B. M., Wakler, C., Fishman, M. and Stainier, D. Y. (2002). Cardiac troponin T is essential in sarcomere assembly and cardiac contractility. Nat. Genet. 31, 106-110.
46. Serbedzija, G. N., Flynn, E. and Willett, C. E. (1999). Zebrafish angiogenesis: a new model for drug screening. Angiogenesis 3, 353-359.
47. Shoji, W., Isogai, S., Sato-Maeda, M., Obinata, M. and Kuwada, J. Y. (2003). Semaphorin3a1 regulates angioblast migration and vascular development in zebrafish embryos. Development 130, 3227-3236.
48. Stainier, D. Y., Weinstein, B. M., Detrich, H. W., 3rd, Zon, L. I. and Fishman, M. C. (1995). Cloche, an early acting zebrafish gene, is required by both the endothelial and hematopoietic lineages. Development 121, 3141-3150.
49. Stainier, D. Y., Fouquet, B., Chen, J. N., Warren, K. S., Weinstein, B. M., Meiler, S. E., Mohideen, M. A., Neuhauss, S. C., Solnica-Krezel, L., Schier, A. F. et al. (1996). Mutations affecting the formation and function of the cardiovascular system in the zebrafish embryo. Development 123, 285-292.
50. Sun, L., Zou, Z., Collodi, P., Xu, F., Xu, X. and Zhao, Q. (2005). Identification and characterization of a second fibronectin gene in zebrafish. Matrix Biol. 24, 69-77.
51. Tallafuss, A. and Bally-Cuif, L. (2003). Tracing of her5 progeny in zebrafish transgenics reveals the dynamics of midbrain-hindbrain neurogenesis and maintenance. Development 130, 4307-4323.
52. Thommen, R., Humar, R., Misevic, G., Pepper, M. S., Hahn, A. W., John, M. and Battegay, E. J. (1997). PDGF-BB increases endothelial migration on cord movements during angiogenesis in vitro. J. Cell Biochem. 64, 403-413.
53. 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.
54. Torres-Vazquez, J., Kamei, M. and Weinstein, B. M. (2003). Molecular distinction between arteries and veins. Cell Tissue Res. 314, 43-59.
55. Torres-Vazquez, J., Gitler, A. D., Fraser, S. D., Berk, J. D., Van, N. P., Fishman, M. C., Childs, S., Epstein, J. A. and Weinstein, B. M. (2004). Semaphorin-plexin signaling guides patterning of the developing vasculature. Dev. Cell 7, 117-123.
56. Trinh, L. A. and Stainier, D. Y. (2004). Fibronectin regulates epithelial organization during myocardial migration in zebrafish. Dev. Cell 6, 371-382.
57. Vokes, S. A. and Krieg, P. A. (2002). Endoderm is required for vascular endothelial tube formation, but not for angioblast specification. Development 129, 775-785.
58. Vokes, S. A., Yatskievych, T. A., Heimark, R. L., McMahon, J., McMahon, A. P., Antin, P. B. and Krieg, P. A. (2004). Hedgehog signaling is essential for endothelial tube formation during vasculogenesis. Development 131, 4371-4380.
59. Walsh, E. C. and Stainier, D. Y. (2001). UDP-glucose dehydrogenase required for cardiac valve formation in zebrafish. Science 293, 1670-1673.
60. Westerfield, M. (1993). The Zebrafish Book. Eugene, OR: University of Oregon Press.
61. Yang, E. Y. and Moses, H. L. (1990). Transforming growth factor beta 1-induced changes in cell migration, proliferation, and angiogenesis in the chicken chorioallantoic membrane. J. Cell Biol. 111, 731-741.
62. Zhong, T. P., Childs, S., Leu, J. P. and Fishman, M. C. (2001). Gridlock signalling pathway fashions the first embryonic artery. Nature 414, 216-220.