Netrin-4 acts as a pro-angiogenic factor during zebrafish development

Journal of Biological Chemistry

Volumn 287, Issue 6, 2012, Pages 3987-3999

  Lambert, Elise ^a,b   Coissieux, Marie May ^a   Laudet, Vincent ^b   Mehlen, Patrick ^a  

^a UNIVERSITÉ DE LYON   (France)

^b UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS; BIOLOGICAL EFFECTS; CELL-BASED; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; IN-VITRO; LAMININ; MULTIFUNCTIONAL ACTIVITY; PROTEIN KINASE; TRANSGENICS; UMBILICAL ARTERY; VASCULAR ACTIVITY; VASCULAR DEVELOPMENT; VASCULAR SYSTEM; VESSEL FORMATION; WILD TYPES; ZEBRAFISH; ZEBRAFISH DEVELOPMENT;

CHEMICAL ACTIVATION; DRUG DELIVERY; ENDOTHELIAL CELLS; ENZYMES;

BLOOD VESSELS;

MESSENGER RNA; NETRIN; NETRIN 4; PHOSPHOTRANSFERASE; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR SYSTEM; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; ENDOTHELIUM CELL; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HUMAN UMBILICAL ARTERY ENDOTHELIAL CELL; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSGENIC ANIMAL; UMBILICAL VEIN ENDOTHELIAL CELL; WILD TYPE; ZEBRA FISH;

ANGIOGENESIS INDUCING AGENTS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELLS, CULTURED; ENDOTHELIAL CELLS; ENZYME ACTIVATION; HUMANS; MORPHOLINOS; NEOVASCULARIZATION, PHYSIOLOGIC; NERVE GROWTH FACTORS; PROTEIN KINASES; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 84856718520     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.289371     Document Type: Article

References (41)

1. Cirulli, V., and Yebra, M. (2007) Netrins. Beyond the brain. Nat. Rev. Mol. Cell Biol. 8, 296-306
2. Barallobre, M. J., Pascual, M., Del Río, J. A., and Soriano, E. (2005) The Netrin family of guidance factors. Emphasis on Netrin-1 signalling. Brain Res. Brain Res. Rev. 49, 22-47 (Pubitemid 40803502)
3. Koch, M., Murrell, J. R., Hunter, D. D., Olson, P. F., Jin, W., Keene, D. R., Brunken, W. J., and Burgeson, R. E. (2000) A novel member of the netrin family, β-netrin, shares homology with the b chain of laminin. Identification, expression, and functional characterization. J. Cell Biol. 151, 221-234
4. Carmeliet, P., and Tessier-Lavigne, M. (2005) Common mechanisms of nerve and blood vessel wiring. Nature 436, 193-200 (Pubitemid 41021263)
5. Suchting, S., Bicknell, R., and Eichmann, A. (2006) Neuronal clues to vascular guidance. Exp. Cell Res. 312, 668-675 (Pubitemid 43290343)
6. Larrivée, B., Freitas, C., Suchting, S., Brunet, I., and Eichmann, A. (2009) Guidance of vascular development. Lessons from the nervous system. Circ. Res. 104, 428-441
7. Castets, M., and Mehlen, P. (2010) Netrin-1 role in angiogenesis. To be or not to be a pro-angiogenic factor? Cell Cycle 9, 1466-1471
8. Folkman, J. (1995) Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat. Med. 1, 27-31
9. Carmeliet, P. (2005) Angiogenesis in life, disease and medicine. Nature 438, 932-936
10. Provis, J. M., Leech, J., Diaz, C. M., Penfold, P. L., Stone, J., and Keshet, E. (1997) Development of the human retinal vasculature. Cellular relations and VEGF expression. Exp. Eye Res. 65, 555-568 (Pubitemid 27454955)
11. Tammela, T., Zarkada, G., Wallgard, E., Murtomäki, A., Suchting, S., Wirzenius, M., Waltari, M., Hellström, M., Schomber, T., Peltonen, R., Freitas, C., Duarte, A., Isoniemi, H., Laakkonen, P., Christofori, G., Ylä-Herttuala, S., Shibuya, M., Pytowski, B., Eichmann, A., Betsholtz, C., and Alitalo, K. (2008) Blocking VEGFR-3 suppresses angiogenic sprouting and vascular network formation. Nature 454, 656-660
12. Olsson, A. K., Dimberg, A., Kreuger, J., and Claesson-Welsh, L. (2006) VEGF receptor signaling - in control of vascular function. Nat. Rev. Mol. Cell Biol. 7, 359-371
13. Zachary, I. (2005) Neuroprotective role of vascular endothelial growth factor. Signalling mechanisms, biological function, and therapeutic potential. Neurosignals 14, 207-221
14. Nguyen, A., and Cai, H. (2006) Netrin-1 induces angiogenesis via a DCC-dependent ERK1/2-eNOS feed-forward mechanism. Proc. Natl. Acad. Sci. U.S.A. 103, 6530-6535
15. Castets, M., Coissieux, M. M., Delloye-Bourgeois, C., Bernard, L., Delcros, J. G., Bernet, A., Laudet, V., and Mehlen, P. (2009) Inhibition of endothelial cell apoptosis by netrin-1 during angiogenesis. Dev. Cell 16, 614-620
16. Hoang, S., Liauw, J., Choi, M., Guzman, R. G., and Steinberg, G. K. (2009) Netrin-4 enhances angiogenesis and neurologic outcome after cerebral ischemia. J. Cereb. Blood Flow Metab. 29, 385-397
17. Lejmi, E., Leconte, L., Pédron-Mazoyer, S., Ropert, S., Raoul, W., Lavalette, S., Bouras, I., Feron, J. G., Maitre-Boube, M., Assayag, F., Feumi, C., Alemany, M., Jie, T. X., Merkulova, T., Poupon, M. F., Ruchoux, M. M., Tobelem, G., Sennlaub, F., and Plouët, J. (2008) Netrin-4 inhibits angiogenesis via binding to neogenin and recruitment of Unc5B. Proc. Natl. Acad. Sci. U.S.A. 105, 12491-12496
18. Nacht, M., St Martin, T. B., Byrne, A., Klinger, K. W., Teicher, B. A., Madden, S. L., and Jiang, Y. (2009) Netrin-4 regulates angiogenic responses and tumor cell growth. Exp. Cell Res. 315, 784-794
19. Wilson, B. D., Ii, M., Park, K. W., Suli, A., Sorensen, L. K., Larrieu-Lahargue, F., Urness, L. D., Suh, W., Asai, J., Kock, G. A., Thorne, T., Silver, M., Thomas, K. R., Chien, C. B., Losordo, D. W., and Li, D. Y. (2006) Netrins promote developmental and therapeutic angiogenesis. Science 313, 640-644 (Pubitemid 44201136)
20. Larrieu-Lahargue, F., Welm, A. L., Thomas, K. R., and Li, D. Y. (2010) Netrin-4 induces lymphangiogenesis in vivo. Blood 115, 5418-5426
21. 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. U.S.A. 103, 6554-6559
22. Martyn, U., and Schulte-Merker, S. (2004) Zebrafish neuropilins are differentially expressed and interact with vascular endothelial growth factor during embryonic vascular development. Dev. Dyn. 231, 33-42 (Pubitemid 39095195)
23. 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 (Pubitemid 37369685)
24. Lawson, N. D., and Weinstein, B. M. (2002) Arteries and veins. Making a difference with zebrafish. Nat. Rev. Genet. 3, 674-682 (Pubitemid 34984256)
25. 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
26. Thisse, C., and Thisse, B. (2008) High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat. Protoc. 3, 59-69
27. Ekker, S. C. (2000) Morphants. A new systematic vertebrate functional genomics approach. Yeast 17, 302-306
28. Draper, B. W., Morcos, P. A., and Kimmel, C. B. (2001) Inhibition of zebrafish fgf8 pre-mRNA splicing with morpholino oligos. A quantifiable method for gene knockdown. Genesis 30, 154-156 (Pubitemid 32730763)
29. Robu, M. E., Larson, J. D., Nasevicius, A., Beiraghi, S., Brenner, C., Farber, S. A., Ekker, S. C. (2007) p53 activation by knockdown technologies. Plos Genet. 3, e78
30. Sugiyama, N., Konoki, K., and Tachibana, K. (2007) Isolation and characterization of okadaic acid binding proteins from the marine sponge Halichondria okadai. Biochemistry 46, 11410-11420 (Pubitemid 47556768)
31. Fujiki, H., and Suganuma, M. (1993) Tumor promotion by inhibitors of protein phosphatases 1 and 2A. The okadaic acid class of compounds. Adv. Cancer Res. 61, 143-194 (Pubitemid 23266387)
32. Atkinson, T., Whitfield, J., and Chakravarthy, B. (2009) The phosphatase inhibitor, okadaic acid, strongly protects primary rat cortical neurons from lethal oxygen-glucose deprivation. Biochem. Biophys. Res. Commun. 378, 394-398
33. Milman, G., Maor, Y., Abu-Lafi, S., Horowitz, M., Gallily, R., Batkai, S., Mo, F. M., Offertaler, L., Pacher, P., Kunos, G., and Mechoulam, R. (2006) N-Arachidonoyl L-serine, an endocannabinoid-like brain constituent with vasodilatory properties. Proc. Natl. Acad. Sci. U.S.A. 103, 2428-2433 (Pubitemid 43271686)
34. Zhang, X., Maor, Y., Wang, J. F., Kunos, G., and Groopman, J. E. (2010) Endocannabinoid-like N-arachidonoyl serine is a novel pro-angiogenic mediator. Br. J. Pharmacol. 160, 1583-1594
35. Yang, Y., Zou, L., Wang, Y., Xu, K. S., Zhang, J. X., and Zhang, J. H. (2007) Axon guidance cue Netrin-1 has dual function in angiogenesis. Cancer Biol. Ther. 6, 743-748 (Pubitemid 47328356)
36. Ivy, S. P., Wick, J. Y., and Kaufman, B. M. (2009) An overview of small-molecule inhibitors of VEGFR signaling. Nat. Rev. Clin. Oncol. 6, 569-579
37. Salameh, A., Galvagni, F., Bardelli, M., Bussolino, F., and Oliviero, S. (2005) Direct recruitment of CRK and GRB2 to VEGFR-3 induces proliferation, migration, and survival of endothelial cells through the activation of ERK, AKT, and JNK pathways. Blood 106, 3423-3431 (Pubitemid 41609177)
38. Lu, X., Le Noble, F., Yuan, L., Jiang, Q., De Lafarge, B., Sugiyama, D., Bréant, C., Claes, F., De Smet, F., Thomas, J. L., Autiero, M., Carmeliet, P., Tessier-Lavigne, M., and Eichmann, A. (2004) The netrin receptor UNC5B mediates guidance events controlling morphogenesis of the vascular system. Nature 432, 179-186 (Pubitemid 39545842)
39. Navankasattusas, S., Whitehead, K. J., Suli, A., Sorensen, L. K., Lim, A. H., Zhao, J., Park, K. W., Wythe, J. D., Thomas, K. R., Chien, C. B., and Li, D. Y. (2008) The netrin receptor UNC5B promotes angiogenesis in specific vascular beds. Development 135, 659-667 (Pubitemid 351405019)
40. Larrieu-Lahargue, F., Welm, A. L., Thomas, K. R., and Li, D. Y. (2011) Netrin-4 activates endothelial integrin α6b1. Circ. Res. 109, 770-774
41. Yebra, M., Diaferia, G. R., Montgomery, A. M., Kaido, T., Brunken, W. J., Koch, M., Hardiman, G., Crisa, L., and Cirulli, V. (2011) Endotheliumderived Netrin-4 supports pancreatic epithelial cell adhesion and differentiation through integrins α2β 1 and α3β 1. PLoS One 6, e22750