Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells

Journal of Clinical Investigation

Volumn 100, Issue 12, 1997, Pages 3131-3139

  Papapetropoulos, Andreas ^a   García Cardeña, Guillermo ^a   Madri, Joseph A ^b   Sessa, William C ^a,c  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c YALE UNIVERSITY   (United States)

Author keywords

Angiogenesis; CGMP; Endothelium; Nitric oxide; Vascular endothelial growth factor

Indexed keywords

CYCLIC GMP; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PROTEIN TYROSINE KINASE; VASCULOTROPIN;

ANGIOGENESIS; ARTICLE; CALCIUM CELL LEVEL; CELL PROLIFERATION; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UMBILICAL VEIN;

EID: 2642597076     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119868     Document Type: Article

References (64)

1. Brown, L.F., M. Detmar, K. Claffey, J.A. Nagy, D. Feng, A.M. Dvorak, and H.F. Dvorak. 1997. Vascular permeability factor/vascular endothelial growth factor: a multifunctional angiogenic cytokine. Exs. 79:233-269.
2. Ferrara, N., K. Houck, L. Jakeman, and D.W. Leung. 1992. Molecular and biological properties of the vascular endothelial growth factor family of proteins. Endocr. Rev. 13:18-32.
3. Ferrara, N. 1996. Vascular endothelial growth factor. Eur. J. Cancer. 32A:2413-2422.
4. Thomas, K.A. 1996. Vascular endothelial growth factor, a potent and selective angiogenic agent. J. Biol. Chem. 271:603-606.
5. Terman, B.I., M. Dougher-Vermazen, M.E. Carrion, D. Dimitrov, D.C. Armellino, D. Gospodarowicz, and P. Bohlen. 1992. Identification of the KDR tyrosine kinase as a receptor for vascular endothelial cell growth factor. Biochem. Biophys. Res. Commun. 187:1579-1586.
6. de Vries, C, J.A. Escobedo, H. Ueno, K. Houck, N. Ferrara, and L.T. Williams. 1992. The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science. 255:989-991.
7. Rooman, I., F. Schuit, and L. Bouwens. 1997. Effect of vascular endothelial growth factor on growth and differentiation of pancreatic ductal epithelium. Lab. Invest. 76:225-232.
8. Clauss, M., H. Weich, G. Breier, U. Knies, W. Rockl, J. Waltenberger, and W. Risau. 1996. The vascular endothelial growth factor receptor Flt-1 mediates biological activities. Implications for a functional role of placenta growth factor in monocyte activation and chemotaxis. J. Biol. Chem. 271:17629-17634.
9. Brown, L.F., M. Detmar, K. Tognazzi, G. Abu-Jawdeh, and M.L. Iruela-Arispe. 1997. Uterine smooth muscle cells express functional receptors (flt-1 and KDR) for vascular permeability factor/vascular endothelial growth factor. Lab. Invest. 76:245-255.
10. Fong, G.H., J. Rossant, M. Gertsenstein, and M.L. Breitman. 1995. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature. 376:66-70.
11. Ferrara, N., K. Carver-Moore, H. Chen, M. Dowd. L. Lu, K.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.
12. 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.
13. 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.
14. Shibuya, M. 1995. Role of VEGF-flt receptor system in normal and tumor angiogenesis. Adv. Cancer Res. 67:281-316.
15. Wu, H.M., Q. Huang, Y. Yuan, and H.J. Granger. 1996. VEGF induces NO-dependent hyperpermeability in coronary venules. Am. J. Physiol. 271: H2735-H2739.
16. Yang, R., G.R. Thomas, S. Bunting, A. Ko, N. Ferrara, B. Keyt, J. Ross, and H. Jin. 1996. Effects of vascular endothelial growth factor on hemodynamics and cardiac performance. J. Cardiovasc. Pharmacol. 27:838-844.
17. 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.
18. Brock, T.A., H.F. Dvorak, and D.R. Senger. 1991. Tumor-secreted vascular permeability factor increases cytosolic Ca2+ and von Willebrand factor release in human endothelial cells. Am. J. Pathol. 138:213-221.
19. Moncada, S., R.M. Palmer, and E.A. Higgs. 1991. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 43:109-142.
20. Morbidelli, L., C.H. Chang, J.G. Douglas, H.J. Granger, F. Ledda, and M. Ziehe. 1996. Nitric oxide mediates milogenic effect of VEGF on coronary venular endothelium. Am. J. Physiol. 270:H411-H415.
21. van der Zee, R., T. Murohara, Z. Luo, F. Zollmann, J. Passeri, C. Lekutat, and J.M. Isner. 1997. Vascular endothelial growth factor/vascular permeability factor augments nitric oxide release from quiescent rabbit and human vascular endothelium. Circulation. 95:1030-1037.
22. 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.
23. Noiri, E., Y. Hu, W.F. Bahou, C.R. Keese, I. Giaever, and M.S. Goligorsky. 1997. Permissive role of nitric oxide in endothelin-induced migration of endothelial cells. J. biol. Chem. 272:1747-1752.
24. Pipili-Synetos, E., E. Sakkoula, G. Haralabopoulos, P. Andriopoulou, P. Peristeris, and M.E. Maragoudakis. 1994. Evidence that nitric oxide is an endogenous antiangiogenic mediator. Br. J. Pharmacol. 111:894-902.
25. Leibovich, S.J., P.J. Polverini, T.W. Fong, L.A. Harlow, and A.E. Koch. 1994. Production of angiogenic activity by human monocytes requires an L-arginine/nitric oxide-synthase-dependent effector mechanism. Proc Natl. Acad. Sci. USA. 91:4190-4194.
26. Jenkins, D.C., I.G. Charles, L.L. Thomsen, D.W. Moss, L.S. Holmes, S.A. Baylism P. Rhodesm K. Westmorem P.C. Emson, and S. Moncada. 1995. Roles of nitric oxide in tumor growth. Proc. Natl. Acad. Sci. USA. 92:4392-4396.
27. Papapetropoulos, A., K.M. Desai, R.D. Rudic, B. Mayer, R. Zhang, M.P. Ruiz-Torres, G. García-Cardeña, J.A. Madri, and W.C. Sessa. 1997. Nitric oxide synthase inhibitors attenuate transforming-growth-factor-beta1-stimulated capillary organization in vitro. Am. J. Pathol. 150:1835-1844.
28. Rosenkranz-Weiss, P., W.C. Sessa, S. Milstien, S. Kaufman, C.A. Watson, and J.S. Pober. 1994. Regulation of nitric oxide synthesis by proinflammatory cytokines in human umbilical vein endothelial cells. Elevations in tetrahydrobiopterin levels enhance endothelial nitric oxide synthase specific activity. J. Clin. Invest. 93:2236-2243.
29. Sankar. S., N. Mahooti-Brooks, L. Bensen, T.L. McCarthy, M. Centrella, and J.A. Madri. 1996. Modulation of transforming growth factor beta receptor levels on microvascular endothelial cells during in vitro angiogenesis. J. Clin. Invest. 97:1436-1446.
30. Papapetropoulos, A., A. Cziraki, J.W. Rubin, C.D. Stone, and J.D. Catravas. 1996. cGMP accumulation and gene expression of soluble guanylate cyclase in human vascular tissue. J. Cell. Physiol. 167:213-221.
31. Papapetropoulos, A., N. Marczin, M.D. Snead, C. Cheng, A. Milici, and J.D. Catravas. 1994. Smooth muscle cell responsiveness to nitrovasodilators in hypertensive and normotensive rats. Hypertension (Dallas). 23:476-484.
32. Fleming, I., B. Fisslthaler, and R. Busse. 1996. Interdependence of calcium signaling and protein tyrosine phosphorylation in human endothelial cells. J. Biol. Chem. 271:11009-11015.
33. Akiyama, T., J. Ishida, S. Nakagawa, H. Ogawara, S. Watanabe, N. Itoh, M. Shibuya, and Y. Fukami. 1987. Genistein, a specific inhibitor of tyrosine-specific protein kinases. J. Biol. Chem. 262:5592-5595.
34. Xia, P., L.P. Aiello, H. Ishii, Z.Y. Jiang, D.J. Park, G.S. Robinson, H. Takagi, W.P. Newsome, M.R. Jirousek, and G.L. King. 1996. Characterization of vascular endothelial growth factor's effect on the activation of protein kinase C, its isoforms, and endothelial cell growth. J. Clin. Invest. 98:2018-2026.
35. Guo, D., Q. Jia, H.Y. Song, R.S. Warren, and D.B. Donner. 1995. Vascular endothelial cell growth factor promotes tyrosine phosphorylation of mediators of signal transduction that contain SH2 domains. Association with endothelial cell proliferation. J. Biol. Chem. 270:6729-6733.
36. Ziehe, M., L. Morbidelli, R. Choudhuri, H.T. Zhang, S. Donnini, H.J. Granger, and R. Bicknell. 1997. Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis. J. Clin. Invest. 99:2625-2634.
37. Andrade, S.P., I.R. Hart, and P.J. Piper. 1992. Inhibitors of nitric oxide synthase selectively reduce flow in tumor-associated neovasculature. Br. J. Pharmacol. 107:1092-1095.
38. Konturek, S.J., T. Brzozowski, J. Majka, J. Pytko-Polonczyk, and J. Stachura. 1993. Inhibition of nitric oxide synthase delays healing of chronic gastric ulcers. Eur. J. Pharmacol. 239:215-217.
39. Goto, F., K. Goto, K. Weindel, and J. Folkman. 1993. Synergistic effects of vascular endothelial growth factor and basic fibroblast growth factor on the proliferation and cord formation of bovine capillary endothelial cells within collagen gels. Lab. Invest. 69:508-517.
40. Montesano, R., and L. Orci. 1985. Tumor-promoting phorbol esters induce angiogenesis in vitro. Cell. 42:469-477.
41. Sessa, W.C. 1994. The nitric oxide synthase family of proteins. J. Vasc. Res. 31:131-143.
42. Kanno, K., Y. Hirata, T. Imai, M. Iwashina, and F. Marumo. 1994. Regulation of inducible nitric oxide synthase gene by interleukin-1 beta in rat vascular endothelial cells. Am. J. Physiol. 267:H2318-H2324.
43. Zeng, G., and M.J. Quon. 1996. Insulin-stimulated production of nitric oxide is inhibited by wortmannin. Direct measurement in vascular endothelial cells. J. Clin. Invest. 98:894-898.
44. Tsukahara, H., D.V. Gordienko, B. Tonshoff, M.C. Gelato, and M.S. Goligorsky. 1994. Direct demonstration of insulin-like growth factor-I-induced nitric oxide production by endothelial cells. Kidney Int. 45:598-604.
45. Ayajiki, K., M. Kindermann, M. Hecker, I. Fleming, and R. Busse. 1996. Intracellular pH and tyrosine phosphorylation but not calcium determine shear stress-induced nitric oxide production in native endothelial cells. Circ. Res. 78: 750-758.
46. Inoue, N., R.C. Venema, H.S. Sayegh, Y. Ohara, T.J. Murphy, and D.G. Harrison. 1995. Molecular regulation of the bovine endothelial cell nitric oxide synthase by transforming growth factor-beta 1. Arterioscler. Thromb. Vasc. Biol. 15:1255-1261.
47. Hewett, P.W., and J.C. Murray. 1996. Coexpression of flt-1, flt-4 and KDR in freshly isolated and cultured human endothelial cells. Biochem. Biophys. Res. Commun. 221:697-702.
48. Barleon, B., S. Hauser, C. Schollmann, K. Weindel, D. Marme, A. Yayon, and H.A. Weich. 1994. Differential expression of the two VEGF receptors flt and KDR in placenta and vascular endothelial cells. J. Cell. Biochem. 54: 56-66.
49. Pawson, T. 1988. Non-catalytic domains of cytoplasmic protein-tyrosine kinases: regulatory elements in signal transduction. Oncogene. 3:491-495.
50. Waltenberger, J., L. Claesson-Welsh, A. Siegbahn, M. Shibuya, and C.H. Heldin. 1994. Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor. J. Biol. Chem. 269:26988-23695.
51. Johnson, G.L., and R.R. Vaillanncourt. 1994. Sequential protein kinase reactions controlling cell growth and differentiation. Curr. Opin. Cell Biol. 6: 230-238.
52. Berridge, M.J., and R.F. Irvine. 1989. Inositol phosphates and cell signalling. Nature. 341:197-205.
53. Franke, T.F., D.R. Kaplan, and L.C. Cantley. 1997. PI3K: downstream AKTion blocks apoptosis. Cell. 88:435-437.
54. Carpenter, C.L., and L.C. Cantley. 1996. Phosphoinositide kinases. Curr. Opin. Cell Biol. 8:153-158.
55. Marczin, N., A. Papapetropoulos, and J.D. Catravas. 1993. Tyrosine kinase inhibitors suppress endotoxin- and IL-1 beta-induced NO synthesis in aortic smooth muscle cells. Am. J. Physiol. 265:H1014-H1018.
56. Muller, J.M., M.J. Davis, and W.M. Chilian. 1996. Coronary arteriolar flow-induced vasodilation signals through tyrosine kinase. Am. J. Physiol. 270: H1878-H1884.
57. Oikawa, T., H. Ashino, M. Shimamura, M. Hasegawa, I. Morita, S. Murota, M. Ishizuka, and T. Takeuchi. 1993. Inhibition of angiogenesis by erbstatin, an inhibitor of tyrosine kinase. J. Antibiot. (Tokyo). 46:785-790.
58. Fleming, I., B. Fisslthaler, and R. Busse. 1995. Calcium signaling in endothelial cells involves activation of tyrosine kinases and leads to activation of mitogen-activated protein kinases. Circ. Res. 76:522-529.
59. Abedi, H., and I. Zachary. 1997. Vascular endothelial growth factor stimulates tyrosine phosphorylation and recruitment to new focal adhesions of focal adhesion kinase and paxillin in endothelial cells. J. Biol. Chem. 272:15442-15451.
60. Derman, M.P., A. Toker, J.H. Hartwig, K. Spokes, J.R. Falck, C.-S. Chen, L.C. Cantley, and L.G. Cantley. 1997. The lipid products of phosphoinositide 3-kinase increase cell motility through protein kinase C. J. Biol. Chem. 272:6465-6470.
61. Oikawa, T., and M. Shimamura. 1996. Potent inhibition of angiogenesis by wortmannin, a fungal metabolite. Eur. J. Pharmacol. 318:93-96.
62. Sessa, W.C., G. Garcia-Cardena, J. Liu, A. Keh, J.S. Pollock, J. Bradley, S. Thiru, I.M. Braverman, and K.M. Desai. 1995. The Golgi association of endothelial nitric oxide synthase is necessary for the efficient synthesis of nitric oxide. J. Biol. Chem. 270:17641-17644.
63. Liu, J., G. Garcia-Cardena, and W.C. Sessa. 1996. Palmitoylation of endothelial nitric oxide synthase is necessary for optimal stimulated release of nitric oxide: implications for caveolae localization. Biochemistry. 35:13277-13281.
64. Carpenter, C.L., and L.C. Cantley. 1996. Phosphoinositide 3-kinase and the regulation of cell growth. Biochim. Biophys. Acta. 1288:M11-M16.