Arteries are formed by vein-derived endothelial tip cells

Nature Communications

Volumn 5, Issue , 2014, Pages

  Xu, Cong ^a   Hasan, Sana S ^a   Schmidt, Inga ^a   Rocha, Susana F ^a   Pitulescu, Mara E ^a   Bussmann, Jeroen ^a   Meyen, Dana ^b   Raz, Erez ^b   Adams, Ralf H ^a,b   Siekmann, Arndt F ^a  

^a MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR CXCR4; ENDOTHELIAL SPECIFIC MOLECULE 1 PROTEIN; MESSENGER RNA; PROTEIN; STROMAL CELL DERIVED FACTOR 1; UNCLASSIFIED DRUG; CXCR4 PROTEIN, MOUSE; CXCR4A PROTEIN, ZEBRAFISH; ZEBRAFISH PROTEIN;

CELL ORGANELLE; GENE EXPRESSION; LIGAND; MUTATION; NUMERICAL MODEL;

ANGIOGENESIS; ANIMAL TISSUE; ARTERY; ARTICLE; BONE TISSUE; CELL MIGRATION; CELL TRANSPLANTATION; CONTROLLED STUDY; ENDOTHELIUM CELL; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RETINA; TIME LAPSE IMAGING; VASCULARIZATION; VEIN; WILD TYPE; ZEBRA FISH; ANIMAL; CELL LINEAGE; CELL MOTION; CYTOLOGY; FIN (ORGAN); GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; SIGNAL TRANSDUCTION; TRANSGENIC ANIMAL; VASCULAR ENDOTHELIUM; VIDEORECORDING;

DANIO RERIO;

ANIMAL FINS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ARTERIES; CELL LINEAGE; CELL MOVEMENT; CHEMOKINE CXCL12; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTORS, CXCR4; RETINA; SIGNAL TRANSDUCTION; TIME-LAPSE IMAGING; VEINS; VIDEO RECORDING; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84923281901     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6758     Document Type: Article

References (53)

1. Eilken, H. M. & Adams, R. H. Dynamics of endothelial cell behavior in sprouting angiogenesis. Curr. Opin. Cell. Biol. 22, 617-625 (2010).
2. Herbert, S. P. & Stainier, D. Y. Molecular control of endothelial cell behaviour during blood vessel morphogenesis. Nat. Rev. Mol. Cell. Biol. 12, 551-564 (2011).
3. Potente, M., Gerhardt, H. & Carmeliet, P. Basic and therapeutic aspects of angiogenesis. Cell 146, 873-887 (2011).
4. Wacker, A. & Gerhardt, H. Endothelial development taking shape. Curr. Opin. Cell. Biol. 23, 676-685 (2011).
5. DiPietro, L. A. Angiogenesis and scar formation in healing wounds. Curr. Opin. Rheumatol. 25, 87-91 (2013).
6. Isogai, S., Horiguchi, M. & Weinstein, B. M. The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development. Dev. Biol. 230, 278-301 (2001).
7. Mukouyama, Y. S., Shin, D., Britsch, S., Taniguchi, M. & Anderson, D. J. Sensory nerves determine the pattern of arterial differentiation and blood vessel branching in the skin. Cell 109, 693-705 (2002).
8. Stahl, A. et al. The mouse retina as an angiogenesis model. Invest. Ophthalmol. Vis. Sci. 51, 2813-2826 (2010).
9. Huang, C. C., Lawson, N. D., Weinstein, B. M. & Johnson, S. L. reg6 is required for branching morphogenesis during blood vessel regeneration in zebrafish caudal fins. Dev. Biol. 264, 263-274 (2003).
10. Machado, M. J. et al. Dynamics of angiogenesis during wound healing: a coupled in vivo and in silico study. Microcirculation 18, 183-197 (2011).
11. Siekmann, A. F., Affolter, M. & Belting, H. G. The tip cell concept 10 years after: New players tune in for a common theme. Exp. Cell. Res. 319, 1255-1263 (2013).
12. Geudens, I. & Gerhardt, H. Coordinating cell behaviour during blood vessel formation. Development 138, 4569-4583 (2011).
13. Jakobsson, L. et al. Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting. Nat. Cell Biol. 12, 943-953 (2010).
14. Arima, S. et al. Angiogenic morphogenesis driven by dynamic and heterogeneous collective endothelial cell movement. Development 138, 4763-4776 (2011).
15. Bussmann, J., Wolfe, S. A. & Siekmann, A. F. Arterial-venous network formation during brain vascularization involves hemodynamic regulation of chemokine signalling. Development 138, 1717-1726 (2011).
16. Ellertsdottir, E. et al. Vascular morphogenesis in the zebrafish embryo. Dev. Biol. 341, 56-65 (2010).
17. Fujita, M. et al. Assembly and patterning of the vascular network of the vertebrate hindbrain. Development 138, 1705-1715 (2011).
18. Lawson, N. D. & Weinstein, B. M. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 248, 307-318 (2002).
19. Bussmann, J. et al. Arteries provide essential guidance cues for lymphatic endothelial cells in the zebrafish trunk. Development 137, 2653-2657 (2010).
20. Roman, B. L. et al. Disruption of acvrl1 increases endothelial cell number in zebrafish cranial vessels. Development 129, 3009-3019 (2002).
21. Muzumdar, M. D., Tasic, B., Miyamichi, K., Li, L. & Luo, L. A global doublefluorescent Cre reporter mouse. Genesis 45, 593-605 (2007).
22. Rocha, S. F. et al. Esm1 modulates endothelial tip cell behavior and vascular permeability by enhancing VEGF bioavailability. Circ. Res. 115, 581-590 (2014).
23. del Toro, R. et al. Identification and functional analysis of endothelial tip cellenriched genes. Blood 116, 4025-4033 (2010).
24. Strasser, G. A., Kaminker, J. S. & Tessier-Lavigne, M. Microarray analysis of retinal endothelial tip cells identifies CXCR4 as a mediator of tip cell morphology and branching. Blood 115, 5102-5110 (2010).
25. Bussmann, J. & Schulte-Merker, S. Rapid BAC selection for tol2-mediated transgenesis in zebrafish. Development 138, 4327-4332 (2011).
26. Montes, G. S., Becerra, J., Toledo, O. M., Gordilho, M. A. & Junqueira, L. C. Fine structure and histochemistry of the tail fin ray in teleosts. Histochemistry 75, 363-376 (1982).
27. Siekmann, A. F., Standley, C., Fogarty, K. E., Wolfe, S. A. & Lawson, N. D. Chemokine signaling guides regional patterning of the first embryonic artery. Gene Dev. 23, 2272-2277 (2009).
28. Valentin, G., Haas, P. & Gilmour, D. The chemokine SDF1a coordinates tissue migration through the spatially restricted activation of Cxcr7 and Cxcr4b. Curr. Biol. 17, 1026-1031 (2007).
29. Rorth, P. Fellow travellers: emergent properties of collective cell migration. EMBO Rep. 13, 984-991 (2012).
30. Raz, E. & Mahabaleshwar, H. Chemokine signaling in embryonic cell migration: a fisheye view. Development 136, 1223-1229 (2009).
31. Bayliss, P. E. et al. Chemical modulation of receptor signaling inhibits regenerative angiogenesis in adult zebrafish. Nat. Chem. Biol. 2, 265-273 (2006).
32. Gerhardt, H. et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 161, 1163-1177 (2003).
33. Stratman, A. N., Davis, M. J. & Davis, G. E. VEGF and FGF prime vascular tube morphogenesis and sprouting directed by hematopoietic stem cell cytokines. Blood 117, 3709-3719 (2011).
34. Benedito, R. & Hellstrom, M. Notch as a hub for signaling in angiogenesis. Exp. Cell Res. 319, 1281-1288 (2013).
35. Li, W. et al. Peripheral nerve-derived CXCL12 and VEGF-A regulate the patterning of arterial vessel branching in developing limb skin. Dev. Cell 24, 359-371 (2013).
36. Mukouyama, Y. S., Gerber, H. P., Ferrara, N., Gu, C. & Anderson, D. J. Peripheral nerve-derived VEGF promotes arterial differentiation via neuropilin 1-mediated positive feedback. Development 132, 941-952 (2005).
37. Ehling, M., Adams, S., Benedito, R. & Adams, R. H. Notch controls retinal blood vessel maturation and quiescence. Development 140, 3051-3061 (2013).
38. Blum, Y. et al. Complex cell rearrangements during intersegmental vessel sprouting and vessel fusion in the zebrafish embryo. Dev. Biol. 316, 312-322 (2008).
39. Nicoli, S., Knyphausen, C. P., Zhu, L. J., Lakshmanan, A. & Lawson, N. D. miR-221 is required for endothelial tip cell behaviors during vascular development. Dev. Cell 22, 418-429 (2012).
40. Siekmann, A. F. & Lawson, N. D. Notch signalling limits angiogenic cell behaviour in developing zebrafish arteries. Nature 445, 781-784 (2007).
41. Sallusto, F. & Baggiolini, M. Chemokines and leukocyte traffic. Nat. Immunol. 9, 949-952 (2008).
42. Kiefer, F. & Siekmann, A. F. The role of chemokines and their receptors in angiogenesis. Cell Mol. Life Sci. 68, 2811-2830 (2011).
43. Nair, S. & Schilling, T. F. Chemokine signaling controls endodermal migration during zebrafish gastrulation. Science 322, 89-92 (2008).
44. Tiveron, M. C. & Cremer, H. CXCL12/CXCR4 signalling in neuronal cell migration. Curr. Opin. Neurobiol. 18, 237-244 (2008).
45. Boldajipour, B. et al. Control of chemokine-guided cell migration by ligand sequestration. Cell 132, 463-473 (2008).
46. Dona, E. et al. Directional tissue migration through a self-generated chemokine gradient. Nature 503, 285-289 (2013).
47. Venkiteswaran, G. et al. Generation and dynamics of an endogenous, selfgenerated signaling gradient across a migrating tissue. Cell 155, 674-687 (2013).
48. Chitnis, A. B., Nogare, D. D. & Matsuda, M. Building the posterior lateral line system in zebrafish. Dev. Neurobiol. 72, 234-255 (2012).
49. Haas, P. & Gilmour, D. Chemokine signaling mediates self-organizing tissue migration in the zebrafish lateral line. Dev. Cell 10, 673-680 (2006).
50. Poss, K. D., Shen, J. & Keating, M. T. Induction of lef1 during zebrafish fin regeneration. Dev. Dyn. 219, 282-286 (2000).
51. Knopf, F. et al. Bone regenerates via dedifferentiation of osteoblasts in the zebrafish fin. Dev. Cell 20, 713-724 (2011).
52. Miyasaka, N., Knaut, H. & Yoshihara, Y. Cxcl12/Cxcr4 chemokine signaling is required for placode assembly and sensory axon pathfinding in the zebrafish olfactory system. Development 134, 2459-2468 (2007).
53. Pitulescu, M. E., Schmidt, I., Benedito, R. & Adams, R. H. Inducible gene targeting in the neonatal vasculature and analysis of retinal angiogenesis in mice. Nat. Protoc. 5, 1518-1534 (2010).