The hormonal peptide Elabela guides angiob lasts to the midline during vasculogenesis

eLife

Volumn 4, Issue MAY, 2015, Pages

  Helker, Christian S M ^a   Schuermann, Annika ^a   Pollmann, Cathrin ^b   Chng, Serene C ^c   Kiefer, Friedemann ^a,b   Reversade, Bruno ^c   Herzog, Wiebke ^a,b  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^c INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

Author keywords

Angioblast migration; Apelin receptor; Chemoattractant; Dorsal aorta; Endothelial cell migration; Notochord; Vegf; Zebrafish

Indexed keywords

APELIN RECEPTOR; CHEMOATTRACTANT; ELABELA; MESSENGER RNA; PEPTIDE HORMONE; PLASMID DNA; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2; APELA PROTEIN, ZEBRAFISH; APELIN PROTEIN, ZEBRAFISH; CHEMOKINE; PRIMER DNA; ZEBRAFISH PROTEIN;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL MIGRATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EMBRYO; ENDOTHELIUM CELL; GENE OVEREXPRESSION; GENETIC CODE; HEMANGIOBLAST; IN SITU HYBRIDIZATION; MICROINJECTION; MUTATION; NONHUMAN; NOTOCHORD; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TIME LAPSE IMAGING; TRANSPLANTATION; ZEBRA FISH; ANIMAL; BIOLOGICAL MODEL; CELL MOTION; CYTOLOGY; ENDOTHELIAL PROGENITOR CELL; GENETICS; HUMAN; METABOLISM; MOLECULAR CLONING; MUTAGENESIS; PHYSIOLOGY;

DANIO RERIO;

ANIMALS; CELL MOVEMENT; CHEMOKINES; CLONING, MOLECULAR; DNA PRIMERS; ENDOTHELIAL CELLS; ENDOTHELIAL PROGENITOR CELLS; HUMANS; IN SITU HYBRIDIZATION; MODELS, BIOLOGICAL; MUTAGENESIS; NEOVASCULARIZATION, PHYSIOLOGIC; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84930666161     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.06726     Document Type: Article

References (34)

1. Bussmann, J., Bos, F. L., Urasaki, A., Kawakami, K., Duckers, H. J. and Schulte- Merker, S. (2010), Arteries provide essential guidance cues for lymphatic endothelial cells in the zebrafish trunk. Development 137, 2653-7.
2. Cermak, T., Doyle, E. L., Christian, M., Wang, L., Zhang, Y., Schmidt, C., Baller, J. A., Somia, N. V., Bogdanove, A. J. and Voytas, D. F. (2011). Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res 39, e82.
3. Charo, D. N., Ho, M., Fajardo, G., Kawana, M., Kundu, R. K., Sheikh, A. Y., Finsterbach, T. P., Leeper, N. J., Ernst, K. V., Chen, M. M. et al. (2009). Endogenous regulation of cardiovascular function by apelin-APJ. Am J Physiol Heart Circ Physiol 297, H1904-13.
4. Chng, S. C., Ho, L., Tian, J. and Reversade, B. (2013). ELABELA: a hormone essential for heart development signals via the apelin receptor. Dev Cell 27, 672-80.
5. Cleaver, O. and Krieg, P. A. (1998). VEGF mediates angioblast migration during development of the dorsal aorta in Xenopus. Development 125, 3905-14.
6. Coultas, L., Chawengsaksophak, K. and Rossant, J. (2005). Endothelial cells and VEGF in vascular development. Nature 438, 937-45.
7. 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, 439-42.
8. 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.
9. Gordon, K., Schulte, D., Brice, G., Simpson, M. A., Roukens, M. G., van Impel, A., Connell, F., Kalidas, K., Jeffery, S., Mortimer, P. S. et al. (2013). Mutation in vascular endothelial growth factor-C, a ligand for vascular endothelial growth factor receptor-3, is associated with autosomal dominant milroy-like primary lymphedema. Circ Res 112, 956-60.
10. Gore, A. V., Monzo, K., Cha, Y. R., Pan, W. and Weinstein, B. M. (2012). Vascular development in the zebrafish. Cold Spring Harb Perspect Med 2, a006684.
11. Halpern, M. E., Ho, R. K., Walker, C. and Kimmel, C. B. (1993). Induction of muscle pioneers and floor plate is distinguished by the zebrafish no tail mutation. Cell 75, 99111.
12. Helker, C. S., Schuermann, A., Karpanen, T., Zeuschner, D., Belting, H. G., Affolter, M., Schulte-Merker, S. and Herzog, W. (2013). The zebrafish common cardinal veins develop by a novel mechanism: lumen ensheathment. Development 140, 2776-86.
13. Hesselson, D., Anderson, R. M., Beinat, M. and Stainier, D. Y. (2009). Distinct populations of quiescent and proliferative pancreatic beta-cells identified by HOTcre mediated labeling. Proc Natl Acad Sci U S A 106, 14896-901.
14. 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, 396-8.
15. Hwang, W. Y., Fu, Y. F., Reyon, D., Maeder, M. L., Tsai, S. Q., Sander, J. D., Peterson, R. T., Yeh, J. R. J. and Joung, J. K. (2013). Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol 31, 227-229.
16. Jao, L. E., Wente, S. R. and Chen, W. (2013). Efficient multiplex biallelic zebrafish genome editing using a CRISPR nuclease system. Proc Natl Acad Sci U S A 110, 139049.
17. Kawakami, K., Takeda, H., Kawakami, N., Kobayashi, M., Matsuda, N. and Mishina, M. (2004). A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Dev Cell 7, 133-44.
18. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev Dyn 203, 253-310.
19. Larson, J. D., Wadman, S. A., Chen, E., Kerley, L., Clark, K. J., Eide, M., Lippert, S., Nasevicius, 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, 204-13.
20. 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, 127-36.
21. Lawson, N. D. and Weinstein, B. M. (2002). In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol 248, 307-18.
22. Nasevicius, A. and Ekker, S. C. (2000). Effective targeted gene 'knockdown' in zebrafish. Nat Genet 26, 216-20.
23. Nicoli, S., Tobia, C., Gualandi, L., De Sena, G. and Presta, M. (2008). Calcitonin receptor-like receptor guides arterial differentiation in zebrafish. Blood 111, 4965-72.
24. 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.
25. Odenthal, J., Haffter, P., Vogelsang, E., Brand, M., van Eeden, F. J., Furutani-Seiki, M., Granato, M., Hammerschmidt, M., Heisenberg, C. P., Jiang, Y. J. et al. (1996). Mutations affecting the formation of the notochord in the zebrafish, Danio rerio. Development 123, 103-15.
26. Pauli, A., Norris, M. L., Valen, E., Chew, G. L., Gagnon, J. A., Zimmerman, S.,Mitchell, A., Ma, J., Dubrulle, J., Reyon, D. et al. (2014). Toddler: an embryonic signal that promotes cell movement via Apelin receptors. Science 343, 1248636.
27. Santoro, M. M., Samuel, T., Mitchell, T., Reed, J. C. and Stainier, D. Y. (2007). Birc2 [Iap1] regulates endothelial cell integrity and blood vessel homeostasis. Nat Genet 39, 1397-402.
28. Scott, I. C., Masri, B., D'Amico, L. A., Jin, S. W., Jungblut, B., Wehman, A. M., Baier, H., Audigier, Y. and Stainier, D. Y. (2007). The g protein-coupled receptor agtrl1b regulates early development of myocardial progenitors. Dev Cell 12, 403-13.
29. Shalaby, F., Rossant, J., Yamaguchi, T. P., Gertsenstein, M., Wu, X. F., Breitman, M. L. and Schuh, A. C. (1995). Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376, 62-6.
30. Sumoy, L., Keasey, J. B., Dittman, T. D. and Kimelman, D. (1997). A role for notochord in axial vascular development revealed by analysis of phenotype and the expression of VEGR-2 in zebrafish flh and ntl mutant embryos. Mech Dev 63, 15-27.
31. Verma, A., Bhattacharya, R., Remadevi, I., Li, K., Pramanik, K., Samant, G. V., Horswill, M., Chun, C. Z., Zhao, B., Wang, E. et al. (2010). Endothelial cell-specific chemotaxis receptor (ecscr) promotes angioblast migration during vasculogenesis and enhances VEGF receptor sensitivity. Blood 115, 4614-22.
32. Westerfield, M. (1993). The Zebrafish Book. University of Oregon press.
33. Zeng, X. X., Wilm, T. P., Sepich, D. S. and Solnica-Krezel, L. (2007). Apelin and its receptor control heart field formation during zebrafish gastrulation. Dev Cell 12, 391402.
34. Zhang, S., Cao, Z., Tian, H., Shen, G., Ma, Y., Xie, H., Liu, Y., Zhao, C., Deng, S., Yang, Y. et al. (2011). SKLB1002, a novel potent inhibitor of VEGF receptor 2 signaling, inhibits angiogenesis and tumor growth in vivo. Clin Cancer Res 17, 4439-50.