Neuropilin-1 is expressed by endothelial and tumor cells as an isoform- specific receptor for vascular endothelial growth factor

Cell

Volumn 92, Issue 6, 1998, Pages 735-745

  Soker, Shay ^a   Takashima, Seiji ^a,c   Miao, Hua Quan ^a   Neufeld, Gera ^b   Klagsbrun, Michael ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^c OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROPILIN; RECEPTOR SUBTYPE; VASCULOTROPIN; VASCULOTROPIN RECEPTOR;

ANGIOGENESIS; ARTICLE; CANCER; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR BLOOD FLOW; VASCULAR ENDOTHELIUM;

EID: 0032549799     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81402-6     Document Type: Article

References (61)

1. Barbacid, M. (1995). Neurotrophic factors and their receptors. Curr. Opin. Cell Biol. 7, 148-155.
2. Barleon, B., Sozzani, S., Zhou, D., Weich, H.A., Mantovani, A., and Marme, D. (1996). Migration of human monocytes in response to vascular endothelial growth factor (VEGF) is mediated via the VEGF receptor flt-1. Blood 87, 3336-3343.
3. Breier, G., Albrecht, U., Sterrer, S., and Risau, W. (1992). Expression of vascular endothelial growth factor during embryonic angiogenesis and endothelial cell differentiation. Development 114, 521-532.
4. 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.
5. Chen, H., Chedotal, A., He, Z., Goodman, C.S., and Tessier-Lavigne, M. (1997). Neuropilin-2, a novel member of the neuropilin family, is a high affinity receptor for the semaphorins Sema E and Sema IV but not Sema III. Neuron 19, 547-559.
6. Cohen, T., Gitay, G.H., Neufeld, G., and Levi, B.Z. (1992). High levels of biologically active vascular endothelial growth factor (VEGF) are produced by the baculovirus expression system. Growth Factors 7, 131-138.
7. de Vries, C., Escobedo, J.A., Ueno, H., Houck, K., Ferrara, N., and Williams, L.T. (1992). The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science 255, 989-991.
8. Dvorak, H.F., Sioussat, T.M., Brown, L.F., Berse, B., Nagy, J.A., Sotrel, A., Manseau, E.J., Van de Water, L., and Senger, D.R. (1991). Distribution of vascular permeability factor (vascular endothelial growth factor) in tumors: concentration in tumor blood vessels. J. Exp. Med. 174, 1275-1278.
9. Dvorak, H.F., Brown, L.F., Detmar, M., and Dvorak, A.M. (1995). Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am. J. Path. 146, 1029-1039.
10. Elenius, K., Paul, S., Allison, G., Sun, J., and Klagsbrun, M. (1997). Activation of HER4 by heparin-binding EGF-likegrowth factor stimulates chemotaxis but not proliferation. EMBO J. 16, 1268-1278.
11. Enomoto, T., Okamoto, T., and Sato, J.D. (1994). Vascular endothelial growth factor induces the disorganization of actin stress fibers accompanied by protein tyrosine phosphorylation and morphological change in Balb/C3T3 cells. Biochem. Biophys. Res. Commun. 202, 1716-1723.
12. Feiner, L., Koppel, A.M., Kobayashi, H., and Raper, J.A. (1997). Secreted chick semaphorins bind recombinant neuropilin with similar affinities but bind different subsets of neurons in situ. Neuron 19, 539-545.
13. Ferrara, N., and Davis-Smith, T. (1997). The biology of vascular endothelial growth factor. Endocrine Rev. 18, 4-25.
14. 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.
15. Flamme, I., Breier, G., and Risau, W. (1995). Vascular endothelial growth factor (VEGF) and VEGF receptor 2 (flk-1) are expressed during vasculogenesis and vascular differentiation in the quail embryo. Dev. Biol. 169, 699-712.
16. Fong, G.H., Rossant, J., Gertsenstein, M., and Breitman, M.L. (1995). Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376, 66-70.
17. Fujisawa, H., Takagi, S., and Hirata, T. (1995). Growth-associated expression of a membrane protein, neuropilin, in Xenopus optic nerve fibers. Dev. Neurosci. 17, 343-349.
18. Gearing, D.P., King, J.A., Gough, N.M., and Nicola, N.A. (1989). Expression cloning of a receptor for human granulocyte-macrophage colony-stimulating factor. EMBO J. 8, 3667-3676.
19. Gitay-Goren, H., Soker, S., Vlodavsky, I., and Neufeld, G. (1992). The binding of vascular endothelial growth factor to its receptors is dependent on cell surface-associated heparin-like molecules. J. Biol. Chem. 267, 6093-6098
20. 121 to one of the three VEGF receptors of vascular endothelial cells. J. Biol. Chem. 267, 6093-6098.
21. He, Z., and Tessier-Lavigne, M. (1997). Neuropilin is a receptor for the axonal chemorepellent Semaphorin III. Cell 90, 739-751.
22. Houck, K.A., Leung, D.W., Rowland, A.M., Winer, J., and Ferrara, N. (1992). Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms. J. Biol. Chem. 267, 26031-26037.
23. 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, 1751.
24. Kawakami, A., Kitsukawa, T., Takagi, S., and Fujisawa, H. (1995). Developmentally regulated expression of a cell surface protein, neuropilin, in the mouse nervous system. J. Neurobiol. 29, 1-17.
25. Keck, P.J., Hauser, S.D., Krivi, G., Sanzo, K., Warren, T., Feder, J., and Connolly, D.T. (1989). Vascular permeability factor, an endothelial cell mitogen related to PDGF. Science 246, 1309-1312.
26. Kendall, R.L., and Thomas, K.A. (1993). Inhibition of vascular endothelial growth factor activity by endogenously encoded soluble receptor. Proc. Natl. Acad. Sci. USA 90, 10705-10709.
27. Keyt, B.A., Nguyen, H.V., Berleau, L.T., Duarte, C.M., Park, J., Chen, H., and Ferrara, N. (1996a). Identification of vascular endothelial growth factor determinants for binding KDR and FLT-1 receptors. Generation of receptor-selective VEGF variants by site-directed mutagenesis. J. Biol. Chem. 271, 5638-5646.
28. Keyt, B.A., Berleau, L.T., Nguyen, H.V., Chen, H., Heinsohn, H., Vandlen, R., and Ferrara, N. (1996b). The carboxyl-terminal domain (111-165) of vascular endothelial growth factor is critical for its mitogenic potency. J. Biol. Chem. 271, 7788-7795.
29. Kim, K.J., Li, B., Winer, J., Armanini, M., Gillett, N., Phillips, H.S., and Ferrara, N. (1993). Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumor growth in vivo. Nature 362, 841-844.
30. Kitsukawa, T., Shimono, A., Kawakami, A., Kondoh, H., and Fujisawa, H. (1995). Overexpression of a membrane protein, neuropilin, in chimeric mice causes anomalies in the cardiovascular system, nervous system and limbs. Development 121, 4309-4318.
31. Kitsukawa, T., Shimizu, M., Sanbo, M., Hirata, T., Taniguchi, M., Bekku, Y., Yagi, T., and Fujisawa, H. (1997). Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron 19, 995-1005.
32. Klagsbrun, M., and Soker, S. (1993). VEGF/VPF: the angiogenic factor found? Curr. Biol. 3, 699-702.
33. Klagsbrun, M., and D'Amore, P.A. (1996). Vascular endothelial growth factor and its receptors. Cytokine Growth Factor Rev. 7, 259-270.
34. Kolodkin, A.L., Matthes, D.J., and Goodman, C.S. (1993). The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 75, 1389-1399.
35. Kolodkin, A.L., Levengood, D.V., Rowe, E.G., Tai, Y.-T., Giger, R.J., and Ginty, D.D. (1997). Neuropilin is a Semaphorin III receptor. Cell 90, 753-762.
36. Leung, D.L., Cachianes, G., Kuang, W.-J., Goeddel, D.V., and Ferrara, N. (1989). Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246, 1306-1309.
37. Lopez-Casillas, F., Wrana, J.L., and Massague, J. (1993). Betaglycan presents ligand to the TGFβ signaling receptor. Cell 73, 1435-1444.
38. Midy, V., and Plouet, J. (1994). Vasculotropin/vascular endothelial growth factor induces differentiation in cultured osteoblasts. Biochem. Biophys. Res. Commun. 199, 380-386.
39. Millauer, B., Wizigmann-Voos, S., Schnurch, H., Martinez, R., Moller, N.P., Risau, W., and Ullrich, A. (1993). High affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell 72, 835-846.
40. Millauer, B., Shawver, L.K., Plate, K.H., Risau, W., and Ullrich, A. (1994). Glioblastoma growth inhibited in vivo by a dominant-negative Flk-1 mutant. Nature 367, 576-579.
41. Munson, P.J., and Rodbard, D. (1980). Ligand: a versatile computerized approach for characterization of ligand-binding systems. Anal. Biochem. 107, 220-239.
42. Omura,T., Miyazawa, K., Ostman, A., and Heldin, C.-H. (1997). Identification of a 190-kDa vascular endothelial growth factor165 cell surface binding protein on human glioma cell line. J. Biol. Chem. 272, 23317-23322.
43. Peters, K.G., DeVries C., and Williams L.T. (1993). Vascular endothelial growth factor expression during embryogenesis and tissue repair suggests a role in endothelial differentiation and blood vessel growth. Proc. Natl. Acad. Sci. USA 90, 8915-8919.
44. Plate, K.H., Breier, G., Weich, H.A., and Risau, W. (1992). Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature 359, 845-848.
45. Plouet, J., Schilling, J., and Gospodarowicz, D. (1989). Isolation and characterization of newly identified endothelial cell mitogen produced by AtT-20 cells. EMBO J. 8, 3801-3806.
46. 145, a secreted vascular endothelial growth factor isoform that binds to extracellular matrix. J. Biol. Chem. 272, 7151-7158.
47. 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, 62-66.
48. Shibuya, M., Yamaguchi, S., Yamane, A., Ikeda, T., Tojo, A., Matsushime, H., and Sato, M. (1990). Nucleotide sequence and expression of a novel human receptor-type tyrosine kinase gene (flt) closely related to the fms family. Oncogene 5, 519-524.
49. Shweiki, D., Itin, A., Neufeld, G., Gitay-Goren, H., and Keshet, E. (1993). Patterns of expression of vascular endothelial growth factor (VEGF) and VEGF receptors in mice suggest a role in hormonally regulated angiogenesis. J. Clin. Invest. 91, 2235-2243.
50. 165 via its exon 7-encoded domain. J. Biol. Chem. 271, 5761-5767.
51. 165. J. Biol. Chem. 272, 31582-31588.
52. Takagi, S., Tsuji, T., Amagai, T., Takamatsu, T., and Fujisawa, H. (1987). Specific cell surface labels in the visual centers of Xenopus laevis tadpole identified using monoclonal antibodies. Dev. Biol. 722, 90-100.
53. Takagi, S., Hirata, T., Agata, K., Mochii, M., Eguchi, G., and Fujisawa, H. (1991). The A5 antigen, a candidate for the neural recognition molecule, has homologies to complement components and coagulation factors. Neuron 7, 295-307.
54. Takagi, S., Kasuya, Y., Shimizu, M., Matsuura, T., Tsuboi, M., Kawakami, A., and Fujisawa, H. (1995). Expression of a cell adhesion molecule, neuropilin, in the developing chick nervous system. Dev. Biol. 770, 207-222.
55. Terman, B.I., Dougher-Vermazen, M., Carrion, M.E., Dimitrov, D., Armellino, D.C., Gospodarowicz, D., and Bohlen, P. (1992). Identification of the KDR tyrosine kinase as a receptor for vascular endothelial cell growth factor. Biochem. Biophys. Res. Commun. 187, 1579-1586.
56. Tischer, E., Gospodarowicz, D., Mitchell, R., Silva, M., Schilling, J., Lau, K., Crisp, T., Fiddes, J.C., and Abraham, J.A. (1989). Vascular endothelial growth factor: a new member of the platelet-derived growth factor gene family. Biochem. Biophys. Res. Commun. 165, 1198-1206.
57. Tischer, E., Mitchell, R., Hartman, T., Silva, M., Gospodarowicz, D., Fiddes, J.C., and Abraham, J.A. (1991). The human gene for vascular endothelial growth factor. Multiple protein forms are encoded through alternative exon splicing. J. Biol. Chem. 266, 11947-11954.
58. Waltenberger, J., Claesson-Welsh, L., Siegbahn, A., Shibuya, M., and Heldin, C.-H. (1994). Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor. J. Biol. Chem. 269, 26988-26995.
59. Wilchek, M., and Miron, T. (1982). Immobilization of enzymes and affinity ligands onto agarose via stable and uncharged carbamate linkages. Biochem. Int. 4, 629-635.
60. Yayon, A., Klagsbrun, M., Esko, J.D., Leder, P., and Ornitz, D.M. (1991). Cell surface, heparin-like molecules are required for binding basic fibroblast growth factor to its high affinity receptors. Cell 64, 841-848.
61. Yoshida, A., Anand-Apte, B., and Zetter, B.R. (1996). Differential endothelial migration and proliferation to basic fibroblast growth factor and vascular endothelial growth factor. Growth Factors 13, 57-64.