Nitric oxide synthase expression, enzyme activity and NO production during angiogenesis in the chick chorioallantoic membrane

British Journal of Pharmacology

Volumn 129, Issue 1, 2000, Pages 207-213

  Pipili Synetos, Eva ^a   Kritikou, Sosanna ^a   Papadimitriou, Evangelia ^a,b   Athanassiadou, Aglaia ^a   Flordellis, C ^a   Maragoudakis, M E ^a  

^a UNIVERSITY OF PATRAS   (Greece)

^b UNIVERSITY OF PATRAS   (Greece)

Author keywords

Angiogenesis; Chick chorioallantoic membrane; Nitric oxide; Nitric oxide synthase

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CALCIUM; CITRULLINE; MESSENGER RNA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRITE;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CHICK EMBRYO; CHORIOALLANTOIS; CONTROLLED STUDY; DOSE RESPONSE; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; MESSENGER RNA SYNTHESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

EID: 0033983606     PISSN: 00071188     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.bjp.0702986     Document Type: Article

References (37)

1. Ahmed, A., Dunk, C., Kniss, D. & Wilkes, M. (1997). Role of VEGF receptor-1 (Flt-1) in mediating calcium-dependent nitric oxide release and limiting DNA synthesis in human trophoblast cells. Lab. Invest., 76, 779-791.
2. Babaei, S., Teichert-Kuliszewska, K., Monge, J.C., Mohamed, F., Bendeck, M.P. & Stewart, D.J. (1998). Role of nitric oxide in the angiogenic response in vitro to basic fibroblast growth factor. Circ. Res., 82, 1007-1015.
3. Bradford, M. (1976). A rapid and sensitive method for quantities of proteins, utilising the principle of protein-dye binding. Anal. Biochem., 72, 248-253.
4. Chomczynski, P. & Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium-thiocyanate phenol chloroform extraction. Analyt. Biochem., 162, 156-159.
5. Folkman, J. (1985). Tumor angiogenesis. Adv. Cancer Res., 43, 172-203.
6. Fukuo, K., Inoue, T., Morimoto, S., Nakahashi, T., Yasuda, O., Kitano, S., Sasada, R. & Ogihara, T. (1995). Nitric oxide mediates cytotoxicity and basic fibroblast growth factor release in cultured vascular smooth muscle cells. A possible mechanism of neovascularization in atherosclerotic plaques. J. Clin. Invest., 95, 669-676.
7. Gallo, O., Masini, E., Morbidelli, L., Franchi, A., FiniStorchi, I., Vergari, W.A. & Ziche, M. (1998). Role of nitric oxide in angiogenesis and tumor progression in head and neck cancer. J. Natl. Cancer Inst., 90, 587-596.
8. Goureau, O., Lepoivre, M. & Courtois, Y. (1992). Lipopolysaccharide and cytokines induce a macrophage-type nitric oxide synthase in bovine retinal pigmented epithelial cells. Biochem. Biophys. Res. Commun., 186, 854-859.
9. Hood, J. & Granger, H.J. (1998). Protein kinase G mediates vascular endothelial growth factor-induced Raf-I activation and proliferation in human endothelial cells. J. Biol. Chem., 273, 23504-23508.
10. Hood, J.D., Meininger, C.J., Ziche, M. & Granger, H.J. (1998). VEGF upregulates ecNOS message, protein and NO production in human endothelial cells. Am. J. Physiol., 274, H1054-H1058.
11. Kroll, J. & Waltenberger, J. (1998). VEGF-A induces expression of eNOS and iNOS in endothelial cells via VEGF receptor-2 (KDR). Biochem. Biophys. Res. Commun., 252, 743-746.
12. Lala, P.K. & Orucevic, A. (1998). Role of nitric oxide in tumor progression: lessons from experimental tumors. Cancer Metastasis Rev., 17, 91-106.
13. Lin, A.W., Chang, C.C. & McCormick, C.C. (1996). Molecular cloning and expression of an avian macrophage nitric-oxide synthase cDNA and the analysis of the genomic 5'-flanking region. J. Biol. Chem., 271, 11911-11919.
14. Liu, Y., Christou, H., Morita, T., Laughner, E., Semenza, G.L. & Kourembanas, S. (1998). Carbon monoxide and nitric oxide suppress the hypoxic induction of vascular endothelial growth factor gene via the 5' enhancer. J. Biol. Chem., 273, 15257-15262.
15. Maragoudakis, M.E. (1993). Angiogenesis. In: Yakoub, M. & Pepper J. (eds.). Annual of Cardiac surgery, pp 13-19. London: Current Science.
16. Maragoudakis, M.E., Sarmonica, M. & Panoutsakopoulou, M. (1988). Rate of basement membrane biosynthesis as an index to angiogenesis. Tissue Cell., 20, 531-539.
17. Morbidelli, V., Chang, C.-H., Douglas, J.G. Granger, H.J., Ledda, F. & Ziche, M. (1996). Nitric oxide mediates mitogenic effect of VEGF on coronary venular endothelium. Am. J. Physiol. 270, H411-H415.
18. Oh, S.-J., Jeltsch, M.M., Birkenhager, R., McCarthy, J.E.G., Weich, H.A., Christ, B., Alitalo, K. & Wilting, J. (1997). VEGF and VEGF-C: Specific induction of angiogenesis and lymphangiogenesis in the differentiated avian chorioallantoic membrane. Dev. Biol., 188, 96-109.
19. O'Reilly, M.S., Holmgren, L., Shing, Y., Chen, C., RoSenthal, R.A., Moses, M., Lane, W.S., Cao, Y., Sage, E.H. & Folkman, J. (1994). Angiostatin: A novel angiogenesis inhibitor that mediates the suppression of metastasis by a Lewis lung carcinoma. Cell, 79, 315-328.
20. Papapetropoulos, A., Desai, M.K., Rudic, R.D., Mayer, B., Zhang, R., Ruiz-Torres, M.P., Garcia-Gardena, G., Madri, J.A. & Sessa, W.C. (1997). Nitric synthase inhibitors attenuate transforming growth factor-B1-stimulated capillary organisation in vitro. Am. J. Pathol., 150, 1835-1844.
21. Parenti, A., Morbidelli, L., Cui, X.L., Douglas, J.C., Hood, J.D., Granger, H.J., Ledda, F. & Ziche, M. (1998). Nitric oxide is an upstream signal of vascular endothelial growth factor induced extracellular signal regulated kinase 1/2 activation in post capillary endothelium. J. Biol. Chem., 273, 4220-4226.
22. Pipili-Synetos, E., Papageorgiou, A., Sakkoula, E., Sotiropoulou, G., Fotsis, T., Karakioulakis, G. & Maragoudakis, M.E. (1995). Inhibition of angiogenesis, tumour growth and metastasis by the NO-releasing vasodilators, isosorbide mononitrate and dinitrate. Br. J. Pharmacol., 116, 1829-1834.
23. Pipili-Synetos, E., Sakkoula, E., Haralabopoulos, G., Andriopoulou, P., Peristeris, P. & Maragoudakis, M.E. (1994). Evidence that nitric oxide is an endogenous antiangiogenic mediator. Br. J. Pharmacol., 11, 894-902.
24. Pipili-Synetos, E., Sakkoula, E. & Maragoudakis, M.E. (1993). Nitric oxide is involved in the regulation of angiogenesis. Br. J. Pharmacol., 108, 855-857.
25. Rachel, L., Handy, C. & Moore, P.K. (1998). A comparison of the effects of L-NAME, 7-NI and L-NIL on corrageenan-induced hindpaw oedema and NOS activity, Br. J. Pharmacol., 123, 1119-1126.
26. Raychaudhury, A., Frischer, H. & Malik, A.B. (1996). Inhibition of endothelial cell proliferation and bFGF-induced phenotypic modulation by nitric oxide. J. Cell. Biochem., 63, 125-134.
27. Sakkoula, E., Pipili-Synetos, E. & Maragoudakis, M.E. (1997). Involvement of nitric oxide in the inhibition of angiogenesis by interleukin-2. Br. J. Pharmacol., 122, 793-798.
28. Shen, B.-Q., Lee, D.Y., Gerber, H.-P., Keyt, B.A., Ferrara, N. & Zioncheck, T.F. (1998). Homologous up-regulation of KDR/ Flk-1 receptor expression by vascular endothelial growth factor in vitro. J. Biol. Chem., 273, 29979-29985.
29. Shimizu, T., Kinugawa, K., Sugishita, Y., Sugishita, K., Harada, K., Matsui, H., Kohmoto, O., Serizawa, T. & Takahashi, T. (1998). Molecular cloning and expression of inducible nitric oxide synthase in chick embryonic ventricular myocytes. Cardiovasc. Res., 38, 405-413.
30. Stone, E.M., Rothblun, K.N., Alevy, M.C., Kuo, T.M. & Schwartz, R.J. (1985). Complete sequence of the chicken glyceraldehyde-3-phosphate dehydrogenase gene. Proc. Natl. Acad. Sci. U.S.A., 82, 1628-1632.
31. Szabo, C., Southan, G.J. & Thiemermann, C. (1994). Beneficial effects and improved survival in rodent models of septic shock with S-methyl-isothiourea sulfate, a novel, potent and selective inhibitor of inducible nitric oxide synthase. Proc. Natl. Acad. Sci. U.S.A., 91, 12472-12476.
32. Tsurumi, Y., Murohara, T., Krasinski, K., Chen, D., Witzen-Bichler, B., Kearney, M., Couffinhal, T. & Isner, J.M. (1997). Reciprocal relation between VEGF and NO in the regulation of endothelial integrity. Nature Med., 3, 879-886.
33. Tuder, R.M., Floor, B.E. & Voelkel, N.F. (1995). Increased gene expression for VEGF and the VEGF receptors KDR/Flk and Flt in lungs exposed to acute or to chronic hypoxia. Modulation of gene expression by nitric oxide. J. Clin. Invest., 95, 1798-1807.
34. Yang, W., Ando, J., Korenaga, R., Toyo-Oka, T. & Kamiya, A. (1994). Exogenous nitric oxide inhibits proliferation of cultured vascular endothelial cells. Biochem. Biophys. Res. Commun., 203, 1160-1167.
35. Ziche, M., Morbidelli, L., Choudhuri, R., Zhang, H-T., Donnini, S., Granger, H.J. & Bicknell, R. (1997). Nitric oxide lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis. J. Clin. Invest., 99, 2625-2634.
36. Ziche, M., Morbidelli, E., Masini, H., Amerini, H.J., Granger, H.J., Maggi, C.A., Geppetti, P. & Ledda, F. (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.
37. Ziche, M., Morbidelli, L., Masini, E., Granger, H.J., Geppetti, P. & Ledda, F. (1993). Nitric oxide promotes DNA synthesis and cyclic GMP formation in endothelial cells from postcapillary venules. Biochem. Biophys. Res. Commun., 192, 1198-1203.