VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia

Journal of Cell Biology

Volumn 161, Issue 6, 2003, Pages 1163-1177

  Gerhardt, Holger ^a   Golding, Matthew ^b   Fruttiger, Marcus ^c   Ruhrberg, Christiana ^b   Lundkvist, Andrea ^a   Abramsson, Alexandra ^a   Jeltsch, Michael ^d   Mitchell, Christopher ^e   Alitalo, Kari ^d   Shima, David ^b,f   Betsholtz, Christer ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d Ludwig Institute Cancer Research   (Finland)

^e UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^f Eyetech Pharmaceuticals Inc   (United States)

Author keywords

Astrocyte; Endothelial cell; Filopodia; Migration; Proliferation; VEGF

Indexed keywords

VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL GROWTH; CELL MIGRATION; CELL POPULATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENDOTHELIUM CELL; FILOPODIUM; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; RETINA CELL;

ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; CELL DIFFERENTIATION; CELL DIVISION; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL GROWTH FACTORS; ENDOTHELIUM, VASCULAR; MICE; MICE, KNOCKOUT; NEOVASCULARIZATION, PHYSIOLOGIC; ORGAN CULTURE TECHNIQUES; PSEUDOPODIA; RETINA; RETINAL ARTERY; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

ANIMALIA;

EID: 0037815292     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200302047     Document Type: Article

References (44)

1. Achen, M.G., M. Jeltsch, E. Kukk, T. Makinen, A. Vitali, A.F. Wilks, K. Alitalo, and S.A. Stacker. 1998. Vascular endothelial growth factor D (VEGF-D) is a ligand for the tyrosine kinases VEGF receptor 2 (Flk1) and VEGF receptor 3 (Flt4). Proc. Natl. Acad. Sci. USA. 95:548-553.
2. Ausprunk, D.H., and J. Folkman. 1977. Migration and proliferation of endothelial cells in preformed and newly formed blood vessels during tumor angiogenesis. Microvasc. Res. 14:53-65.
3. Bär, T., and J.R. Wolff. 1972. The formation of capillary basement membranes during internal vascularization of the rat's cerebral cortex. Z Zellforsch Mikrosk. Anat. 133:231-248.
4. Benjamin, L.E., D. Golijanin, A. Itin, D. Pode, and E. Keshet. 1999. Selective ablation of immature blood vessels in established human tumors follows vascular endothelial growth factor withdrawal. J. Clin. Invest. 103:159-165.
5. Bonanno, E., M. Iurlato, J.A. Madri, and R.F. Nicosia. 2000. Type IV collagen modulates angiogenesis and neovessel survival in the rat aorta model. In Vitro Cell. Dev. Biol. Anim. 36:336-340.
6. Carmeliet, P. 2000. VEGF gene therapy: stimulating angiogenesis or angiomagenesis? Nat. Med. 6:1102-1103.
7. Carmeliet, P., and R.K. Jain. 2000. Angiogenesis in cancer and other diseases. Nature. 407:249-257.
8. Carmeliet, P., V. Ferreira, G. Breier, S. Pollefeyt, L. Kieckens, M. Gertsenstein, M. Fahrig, A. Vandenhoeck, K. Harpal, C. Eberhardt, et al. 1996. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature. 380:435-439.
9. Dorrell, I., E. Aguilar, and M. Friedlander. 2002. Retinal vascular development is mediated by endothelial filopodia, a preexisting astrocytic template and specific R-cadherin adhesion. Invest. Ophthalmol. Vis. Sci. 43:3500-3510.
10. Dumont, D.J., L. Jussila, J. Taipale, A. Lymboussaki, T. Mustonen, K. Pajusola, M. Breitman, and K. Alitalo. 1998. Cardiovascular failure in mouse embryos deficient in VEGF receptor-3. Science. 282:946-949.
11. Eriksson, U., and K. Alitalo. 1999. Structure, expression and receptor-binding properties of novel vascular endothelial growth factors. Curr. Top. Microbiol. Immunol. 237:41-57.
12. Ferrara, N. 1999. Vascular endothelial growth factor: molecular and biological aspects. Curr. Top. Microbiol. Immunol. 237:1-30.
13. Ferrara, N. 2000. VEGF: an update on biological and therapeutical aspects. Curr. Opin. Biotechnol. 11:617-624.
14. Ferrara, N., K. Carver-Moore, H. Chen, M. Dowd, L. Lu, S. O'Shea, L. Powell-Braxton, K.J. Hillan, and M.W. Moore. 1996. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature. 380:439-442.
15. Fruttiger, M. 2002. Development of the mouse retinal vasculature: angiogenesis versus vasculogenesis. Invest. Ophthalmol. Vis. Sci. 43:522-527.
16. Fruttiger, M., A.R. Calvet, W.H. Kruger, H.S. Mudhar, D. Michalovich, N. Takakura, S. Nishikawa, and W.D. Richardson. 1996. PDGF mediates a neuron-astrocyte interaction in the developing retina. Neuron. 17:1117-1131.
17. Fruttiger, M., A.R. Calver, and W.D. Richardson. 2000. Platelet-derived growth factor is constitutively secreted from neuronal cell bodies but not from axons. Curr. Biol. 10:1283-1286.
18. Joukov, V., V. Kumar, T. Sorsa, E. Arighi, H. Weich, O. Saksela, and K. Alitalo. 1998. A recombinant mutant vascular endothelial growth factor-C that has lost vascular endothelial growth factor receptor-2 binding, activation and vascular permeability activities. J. Biol. Chem. 273:6599-6602.
19. Kater, S.B., and V. Rehder. 1995. The sensory-motor role of growth cone filopodia. Curr. Opin. Neurobiol. 5:68-74.
20. Lawson, N.D., A.M. Vogel, and B.M. Weinstein. 2002. Sonic hedgehog and vascular endothelial growth factor act upstream of the notch pathway during arterial endothelial differentiation. Dev. Cell. 3:127-136.
21. Lindahl, P., B.R. Johansson, P. Levéen, and C. Betsholtz. 1997. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science. 277:242-245.
22. Marin-Padilla, M. 1985. Early vascularization of the embryonic cerebral cortex: Golgi and electron microscopic studies. J. Comp. Neurol. 241:237-249.
23. Mukouyama, Y., D. Shin, S. Britsch, M. Taniguchi, and D.J. Anderson. 2002. Sensory nerves determine the pattern of arterial differentiation and blood vessel branching in the skin. Cell. 109:693-705.
24. Nicosia, R.F., and A. Ottinetti. 1990. Growth of microvessels in serum-free matrix culture of rat aorta. A quantitative assay of angiogenesis in vitro. Lab. Invest. 63:115-122.
25. Ogawa, S., A. Oku, A. Sawano, S. Yamaguchi, Y. Yazaki, and M. Shibuya. 1998. A novel type of vascular endothelial growth factor: VEGF-E (NZ-7 VEGF) preferentially utilizes KDR/Flk-1 receptor and carries a potent mitotic activity without heparin-binding domain. J. Biol. Chem. 273:31273-31282.
26. Pierce, E.A., R.L. Avery, E.D. Foley, L.P. Aiello, and L.E. Smith. 1995. Vascular endothelial growth factor/vascular permeability factor expression in a mouse model of retinal neovascularization. Proc. Natl. Acad. Sci. USA. 92:905-909.
27. Provis, J.M., J. Leech, C.M. Diaz, P.L. Penfold, J. Stone, and E. Keshet. 1997. Development of the human retinal vasculature: cellular relations and VEGF expression. Exp. Eye Res. 65:555-568.
28. Ramirez-Weber, F.A., and T.B. Kornberg. 2000. Signaling reaches to new dimensions in Drosophila imaginal discs. Cell. 103:189-192.
29. Ribeiro, C., A. Ebner, and M. Affolter. 2002. In vivo imaging reveals different cellular functions for FGF and Dpp signaling in tracheal branching morphogenesis. Dev. Cell. 2:677-683.
30. Risau, W., and I. Flamme. 1995. Vasculogenesis. Annu. Rev. Cell Dev. Biol. 11:73-91.
31. Ruhrberg, C., H. Gerhardt, M. Golding, R. Watson, S. Ioannidou, H. Fujisawa, C. Bersholtz, and D. Shima. 2002. Spatially restricted patterning cues provided by heparin-binding VEGF-A control blood vessel branching morphogenesis. Genes Dev. 16:2684-2698.
32. Samakovlis, C., N. Hacohen, G. Manning, D.C. Sutherland, K. Guillemin, and M.A. Krasnow. 1996. Development of the Drosophila tracheal system occurs by a series of morphologically distinct but generically coupled branching events. Development. 122:1395-1407.
33. Senger, D.R., S.J. Galli, A.M. Dvorak, C.A. Perruzzi, V.S. Harvey, and H.F. Dvorak. 1983. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science. 219:983-985.
34. Shalaby, F., J. Rossant, T.P. Yamaguchi, M. Gertsenstein, X.-F. Wu, M.L. Breitman, and A.C. Schuh. 1995. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature. 376:62-66.
35. Shima, D., and C. Mailhos. 2000. Vascular developmental biology: getting nervous. Curr. Opin. Genet. Dev. 10:536-542.
36. Sholley, M.M., G.P. Ferguson, H.R. Seibel, J.L. Montour, and J.D. Wilson. 1984. Mechanisms of neovascularization. Vascular sprouting can occur without proliferation of endothelial cells. Lab. Invest. 51:624-634.
37. Soker, S., S. Takashima, H.Q. Miao, G. Neufeld, and M. Klagsbrun. 1998. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell. 92:735-745.
38. Stalmans, I., N. Yin-Shan, R. Rohan, M. Fruttiger, A. Bouché, A. Yuce, H. Fijusawa, B. Hermans, M. Shani, S. Jansen, et al. 2002. Arteriolar and venolar patterning in retinas of mice selectively expressing VEGF isoforms. J. Clin. Invest. 109:327-336.
39. Stone, J., and Z. Dreher. 1987. Relationship between astrocytes, ganglion cells and vasculature of the retina. J. Comp. Neurol. 255:35-49.
40. Stone, J., A. Itin, T. Alon, J. Peer, H. Gnessin, T. Chan-Ling, and E. Keshet. 1995. Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J. Neurosci. 15:4738-4747.
41. Tessier-Lavigne, M., and C.S. Goodman. 1996. The molecular biology of axon guidance. Science. 274:1123-1133.
42. Wise, L.M., T. Veikkola, A.A. Mercer, L.J. Savory, S.B. Fleming, C. Caesar, A. Vitali, T. Makinen, K. Alitalo, and S.A. Stacker. 1999. Vascular endothelial growth factor (VEGF)-like protein from orf virus NZ2 binds to VEGFR2 and neuropilin-1. Proc. Natl. Acad Sci. USA. 96:3071-3076.
43. Wood, W., and P. Martin. 2002. Structures in focus - filopodia. Int. J. Biochem. Cell Biol. 34:726-730.
44. Zelzer, E., and B.Z. Shilo. 2000. Cell fate choices in Drosophila trachela morphogenesis. Bioessays. 22:219-226.