Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis

Journal of Clinical Investigation

Volumn 99, Issue 11, 1997, Pages 2625-2634

  Ziehe, Marina ^a,d   Morbidelli, Lucia ^a   Choudhuri, Rangana ^b   Zhang, Hua Tang ^b   Donnini, Sandra ^a   Granger, Harris J ^c   Bicknell, Roy ^b  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c TEXAS A M COLLEGE OF MEDICINE   (United States)

^d Department of Pharmacology ^*  (Italy)

Author keywords

Endothelium; Neovascularization; Nitric oxide; Vascular endothelial growth factor

Indexed keywords

6 ANILINO 5,8 QUINOLINEQUINONE; BASIC FIBROBLAST GROWTH FACTOR; INTEGRIN; NITRIC OXIDE SYNTHASE; VASCULOTROPIN;

ANGIOGENESIS; ARTICLE; BREAST CARCINOMA; CARCINOMA CELL; CELL GROWTH; CELL MIGRATION; CORNEA; ENDOTHELIUM CELL; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; NEOVASCULARIZATION (PATHOLOGY); PRIORITY JOURNAL;

EID: 0031008458     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/jci119451     Document Type: Article

References (45)

1. Ferrara, N., and W.J. Henzel. 1989. Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem. Biophys. Res. Commun. 161:851-858.
2. Keck, P.J., S.D. Hauser, G. Krivi, K. Sanzo, T. Warren, J. Feder, and D.T. Conolly. 1989. Vascular permeability factor, an endothelial cell mitogen related to PDGF. Science (Wash. DC). 246:1309-1312.
3. Houck, K.A., N. Ferrara, J. Winer, G. Cachianes, B. Li, and D.W. Leung. 1991. The vascular endothelial growth factor family: identification of a fourth molecular species and characterization of alternative splicing of RNA. Mol. Endocrinol. 5:1806-1814.
4. Shweiki, D., A. Hin, D. Soffer, and E. Keshet. 1992. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis, Nature (Lond.). 359:843-845.
5. Plate, K.H., G. Breier, H.A. Weich, and W. Risau. 1992. Vascular endothelial growth factor is a potential tumor angiogenesis factor in human gliomas in vivo. Nature (Lond.). 359:845-848.
6. Brown, L.F., B. Berse, R.W. Jackman, K. Tognazzi, E.J. Manseau, H.F. Dvorak, and D.R. Senger. 1993. Increased expression of vascular permeability factor (vascular endothelial growth factor) and its receptors in kidney and bladder carcinomas. Am. J. Pathol. 143:1255-1262.
7. O'Brien, T., D. Cranston, S. Fuggle, R. Bicknell, and A.L. Harris. 1996. Different angiogenic pathways characterize superficial and invasive bladder cancer. Cancer Res. 55:510-513.
8. Toi, M., S. Kondo, H. Suzuki, Y. Yamamoto, K. Inada, T. Imazawa, T. Taniguchi, and T. Tominaga. 1996. Quantitative analyses of vascular endothelial growth factor in primary breast cancer. Cancer Res. 77:1101-1105.
9. Zhang, H.-T., P. Craft, P.A.E. Scott, M. Ziehe, H.A. Weich, A.L. Harris, and R. Bicknell. 1995. Enhancement of tumor growth and vascular density by transfection of vascular endothelial cell growth factor into MCF-7 human breast carcinoma cells. J. Natl. Cancer Inst. 87:213-217.
10. Claffey, K.P., L.F. Brown, L.F. del Aguila, K. Tognazzi, K.-T. Yeo. E.J. Manseau, and H.F. Dvorak. 1996. Expression of vascular permeability factor/ vascular endothelial growth factor by melanoma cells increases tumor growth, angiogenesis, and experimental metastasis. Cancer Res. 56:172-181.
11. Kim, K.J., B. Li, J. Winer, M. Armanini, N. Gillet, H.S. Phillips, and N. Ferrara. 1993. Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature (Lond.). 262:841-844.
12. 121. Cancer Res. 55:5296-5301.
13. Millauer, B., L.K. Shawver, K.H. Plate, W. Risau, and A. Ullrich. 1994. Glioblastoma growth inhibited in vivo by a dominant-negative Flk-1 mutant. Nature (Lond.). 367:576-579.
14. Klagsbrun, M., J. Sasse, R. Sullivan, and J.A. Smith. 1986. Human tumor cells synthesize an endothelial cell growth factor that is structurally related to basic fibroblast growth factor. Proc. Natl. Acad. Sci. USA. 83:2448-2452.
15. Kandel, J., E. Bossy-Wetzel, F. Radvanyi, M. Kiagsbrun, J. Folkman, and D. Hanahan. 1991. Neovascularization is associated with a switch to the export of bFGF in the multistep development of fibrosarcoma. Cell. 66:1095-1104.
16. 2+ and von Willebrand factor release in human endothelial cells. Am. J. Pathol. 138:213-221.
17. Myoken, Y., Y. Kayada, T. Okamoto, M. Kan, G.H. Sato, and J.D. Sato. 1991. Vascular endothelial growth factor (VEGF) produced by A-431 human epidermoid carcinoma cells and identification of VEGF membrane binding sites. Proc. Natl. Acad. Sci. USA. 88:5819-5823.
18. Ku, D.D., J.K. Zaleski, S. Liu, and T.A. Brock. 1993. Vascular endothelial growth factor induces EDRF-dependent relaxation in coronary arteries. Am. J. Physiol. 265:H586-H592.
19. Wu, H.M., H. Qiaobing, Y. Yuan, and H.J. Granger. 1996. VEGF induces NO-dependent hyperpermeability in coronary venules. Am. J. Physiol. 271:H2735-H2739.
20. Morbidelli, L., C.-H. Chang, J.G. Douglas, H.J. Granger, F. Ledda, and M. Ziehe. 1996. Nitric oxide mediates the mitogenic effect of VEGF on coronary venular endothelium. Am. J. Physiol. 270:H411-H415.
21. Moncada, S., and A. Higgs, 1993. The L-arginine-nitric oxide pathway. N. Engl. J. Med. 329:2002-2012.
22. Ziehe, M., L. Morbidelli, E. Masini, H.J. Granger, G. Geppetti, and F. Ledda. 1993. Nitric oxide promotes DNA synthesis and cyclic GMP formation in endothelial cells from postcapillary venules. Biochem. Biophys. Res. Commun. 192:1198-1203.
23. Ziehe, M., L. Morbidelli, E. Masini, S. Amerini, H.J. Granger, C.A. Maggi, P. Geppetti, and F. Ledda. 1994. Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by substance P. J. Clin. Invest. 94:2036-2044.
24. Leibovich, S.J., P.J. Polverini, T.W. Fong, L.A. Harlow, and A.E. Koch. 1994. Production of angiogenic activity by human monocytcs requires an L-arginine/nitric oxide-synthase-dependent effector mechanism. Proc. Natl. Acad. Sci. USA. 91:4190-4194.
25. Schelling, M.E., C.J. Meininger, J.R. Hawker, and H.J. Granger. 1988. Venular endothelial cells from bovine heart. Am. J. Physiol. 254:H1211-H1217.
26. Bradford, M. 1976. A rapid and sensitive method for quantities of proteins, utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-253.
27. Taraboletti, G., D. Roberts, L.A. Liotta, and R. Giavazzi. 1990. Platelet thrombospondin modulates endothelial cell adhesion, motility, and growth: a potential angiogenesis regulatory factor. J. Cell Biol 111:765-772.
28. Parenti, A., S. Amerini, F. Ledda, C.A. Maggi, and M. Ziehe. 1996. The tachykinin NK-1 receptor mediates the migration-promoting effect of substance P on human skin fibroblasts in culture. Naunyn-Schmiedebergs Arch. Pharmakol. 353:475-481.
29. Ziehe, M., J. Jones, and P.M. Gullino. 1982. Role of prostaglandin E1 and copper in angiogenesis. J. Natl. Cancer Inst. 69:475-482.
30. Ziehe, M., and P.M. Gullino. 1982. Angiogenesis and neoplastic progression in vitro. J. Natl. Cancer Inst. 69:483-487.
31. Gasparini, G., N. Weidner, P. Bevilacqua, S. Maluta, P. Dalla Palma, O. Caffo, M. Barbareschi, P. Boracchi, E. Marubini, and F. Pozza. 1994. Tumor microvessel density, p53 expression, tumor size and peritumoral lymphatic vessel invasion are relevant prognostic markers in node-negative breast carcinoma. J. Clin. Oncol. 12:454-466.
32. Mulsh, A., R. Buse, S. Liebau, and U. Fostermann. 1988. LY 83583 interferes with the release of endothelium-derived relaxing factor and inhibits soluble guanylate cyclase. J. Pharmacol. Exp. Ther. 247:283-288.
33. Harris, D.M., M.M. Asaad, M.B. Phillips, H.J. Goldberg, and M.J. Antonaccio. 1979. Inhibition of adenylate cyclase in human blood platelets by 9-substituted adenine derivatives. J. Cyclic Nucleotide Res. 5:125-134.
34. v integrins. Science (Wash. DC). 270:1500-1502.
35. Brzozowski, T., S.J. Kounturek, D. Drozdowicz, A. Dembinski, and J. Stachura. 1995. Healing of chronic gastric ulcerations by L-arginine. Digestion. 56:463-471.
36. Pipili-Synetos, E., E. Sakkoula, G. Haralabopoulos, P. Andiopuolou, P. Peristeris, and M.E. Maragoudakis. 1994. Evidence that nitric oxide is an endogenous antiangiogenic mediator. Br. J. Pharmacol. 111:894-902.
37. Pipili-Synetos, E., A. Papageorgiu, E. Sakkoula, G. Sotiropoulou, T. Fotsis, G. Karskiulakis, and M.E. Maragoudakis. 1995. Inhibition of angiogenesis, tumour growth and metastasis by the NO-releasing vasodilators, isosorbide mononitrate and dinitrate. Br. J. Pharmacol. 116:1829-1834.
38. Ziehe, M., L. Morbidelli, M. Pacini, P. Geppetti, G. Alessandri, and C.A. Maggi. 1990. Substance P stimulates neovascularization in vivo and proliferation of cultured endothelial cells. Microvasc. Res. 40:264-278.
39. Thomsen, L.L., F.G. Lawton, R.G. Knowles, J.E. Beesley, V. Riveros-Moreno, and S. Moncada. 1994. Nitric oxide synthase activity in human gynecological cancer. Cancer Res. 54:1352-1354.
40. Cobbs, C.S., J.E. Brenman, K.D. Alpade, D.S. Bredt, and M.A. Israel. 1995. Expression of nitric oxide synthase in human central nervous system tumors. Cancer Res. 55:727-730.
41. Jenkins, D.C., I.G. Charles, L.L. Thomsen, D.W. Moss, L.S. Holmes, S.A. Baylis, P. Rhodes, K. Westmore, P.C. Emson, and S. Moncada. 1995. Role of nitric oxide in tumor angiogenesis. Proc. Natl. Acad. Sci. USA. 92:4392-4396.
42. Kennovin, G.D., D.G. Hirst, M.R.L. Stratford, and F.W. Flitney. 1994. Inducible nitric oxide synthase is expressed in tumor associated vasculature; inhibition retards tumor growth in vivo. In Biology of Nitric Oxide. Vol. 4: Enzymology, Biochemistry and Immunology. S. Moncada. M. Feelish, R. Busse, and E.A. Higgs, editors. Portland Press Ltd., London. 473-479.
43. G-nitro-L-arginine methyl ester, an inhibitor of nitric oxide synthesis, ameliorates interleukin 2-induced capillary leakage and reduces tumour growth in adenocarcinoma-bearing mice. Br. J. Cancer 73:189-196.
44. Doi, K., T. Akaike, H. Horie, Y. Noguchi, S. Fuji, T. Beppu, M. Ogawa, and H. Maeda. 1996. Excessive production of NO in rat solid tumor and its implication in rapid tumor growth. Cancer. 77:1598-1604.
45. Wolff, J.E.A., C. Guerin, J. Laterra, J. Bressler, R.R. Indurti, H. Brem, and G.W. Goldstein. 1993. Dexamethasone reduces vascular density and plasminogen activator activity in 9L rat brain tumors. Brain Res. 604:79-85.