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Angiogenesis pp 307-319 | Cite as

Nitric Oxide: A Promoter or Inhibitor of Angiogenesis

  • Eva Pipili-Synetos
  • Michael E. Maragoudakis
Chapter
Part of the NATO ASI Series book series (NSSA, volume 298)

Abstract

Nitric oxide (NO) has been shown in the last decade to be an ubiquitous messenger with a remarkably wide diversity of biological actions. Its role as a major regulator in the nervous immune and cardiovascular systems as well as in pathophysiological states (septic shock, hypertension, stroke and neurodegenerative diseases) is increasingly appreciated (Gross & Wolin, 1995).

Keywords

Nitric Oxide Nitric Oxide Hank Balance Salt Solution Lewis Lung Carcinoma Isosorbide Dinitrate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Albina, J.E., Abate, J.A., & Henry, W.L. (1991). Nitric oxide production is required for murine resident peritonei macrophages to suppress mitogen-stimulated T cell proliferation. J. Immunol. 147, 144–148.PubMedGoogle Scholar
  2. 2.
    Assender, J. W., Southgate, K.M., Hallett, M.B. & Newby, A.C. (1992). Inhibition of proliferation, but not of Ca2+ mobilization by cyclic AMP and GMP in rabbit aortic smooth muscle cells. Biochem. J., 288, 527–532.Google Scholar
  3. 3.
    Bath, P.M.W., Hassel, D.G., & Gladwin, A.M. (1991). Nitric oxide and prostacyclin: Divergence of inhibitory effects on monocyte Chemotaxis and adhesion to endothelium in vitro. Arterioscler. Thromb., 11, 254–260.CrossRefPubMedGoogle Scholar
  4. 4.
    Beckman, J.S., Beckman, T.W., Chen, J., Marshall, P.A. & Freeman, B.A. & (1990). Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. U.S.A., 87, 1620–1624.CrossRefPubMedGoogle Scholar
  5. 5.
    Brooks, P.C., Montgomery, A. M., Rosenfeld, M., Reisfeld, RA., Hu, T., Klier, G. & Cheresh, D.A. (1994). Integrin alpha v beta 3 antagonists, promote tumour regression by inducing apoptosis of angiogenic blood vessels. Cell, 79, 1157–1164.CrossRefPubMedGoogle Scholar
  6. 6.
    Cornwell, TL., Arnold, E., Boerth, N.L. & Lincoln, T.M., (1994). Inhibition of smooth muscle cell growth by nitric oxide and activation of cAMP-dependent protein kinase by cGMP. Am. J. Physiol., 267, C1405–1413.Google Scholar
  7. 7.
    Delikonstantinos, G., Villiotou, V. & Stavrides, J. C (1995). Release by ultraviolet B (u. v. B) radiation of nitric oxide (NO) from human keratinocytes: a potential role for nitric oxide in erythema production. Br. J. Pharmacol., 114, 1257–1265.CrossRefGoogle Scholar
  8. 8.
    Edwards, P., Cendan, J.C., Topping, D.B., Moldawer, L.L., Mackay, S., Copeland, E.M. & Lind, D.S. (1996). Tumour cell nitric oxide inhibits cell growth in virtro but stimulates tumourigenesis and experimental lung metastasis in vivo. J. Surg. Res., 63 (1), 49–52.CrossRefPubMedGoogle Scholar
  9. 9.
    Efron, D.T., Kirk, S.J. Regan M.C., Wasserkrug, H.L. & Barbul, A. (1991). Nitric oxide generation from L-arginine is required for optimal human peripheral blood lymphocyte DNA synthesis. Surgery, 110,327–334.PubMedGoogle Scholar
  10. 10.
    Filep, J.G., Baron, C, Lachance, S., Perreault, C. & Chan, J.S.D.(1996). Involvement of nitric oxide in target-cell lysis and DNA fragmentation induced by murine natural killer cells. Blood, 87, 5136–5143.PubMedGoogle Scholar
  11. 11.
    Folkman, J. & Shing, Y. (1992). Angiogenesis. J. Biol. Chem. 267, 10931–10934.PubMedGoogle Scholar
  12. 12.
    Folkman, J. (1985). Tumor angiogenesis. Adv. Cancer. Res., 43,172–203.Google Scholar
  13. 13.
    Friedlander, M., Brooks, P.C., Shaffer, R.W., Kincaid, M, Varner, J. A. & Cheresh, D.A. (1995). Definition of two angiogenic pathways by distinct av integrins. Science 270,1500–1502.CrossRefPubMedGoogle Scholar
  14. 14.
    Garg, U.C. & Hassid, A. (1989). Nitric oxide-generating vasodilators and 8-bromo-cyclic GMP inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells. J. Clin Invest., 83, 1774–1777.CrossRefPubMedGoogle Scholar
  15. 15.
    Gasic, E.J., Gasic, T.B., Galanti, N., Johnson, T. & Murphy, S. (1973). Platelet tumour interaction in mice. The role of platelet in the spread of malignant disease. Int. J. Cancer, 11,704–708.CrossRefPubMedGoogle Scholar
  16. 16.
    Gasic, G.J., Gasic, T.B. & Stewart, C.C. (1968). Antimetastatic effects associated with platelet reduction. Proc. Natl. Acad. Sci. USA. 61, 45–62.CrossRefGoogle Scholar
  17. 17.
    Grant, D.S., Tashiro, K.I., Segui-Real, B., Yamada, Y, Martin, G.R. & Kleinman, H.K. (1989).Two different laminin domains mediate the differentiation of human endothelial cells into capillary-like structures in vitro. Cell, 58, 933–943.CrossRefPubMedGoogle Scholar
  18. 18.
    Gross, S.S. & Wolin, M.S. (1995). Nitric oxide: Pathophysiological mechanism. Ann. Rev. Physiol 57, 737–769.CrossRefGoogle Scholar
  19. 19.
    Harris-Hooker, S.A., Gajdusec, C.M., Wight, T.N. & Schwartz, S.M. (1983). Neovascular response induced by cultured aortic endothelial cells. J. Cell Physiol., 114,302–310.CrossRefPubMedGoogle Scholar
  20. 20.
    Hibbs, J. B., Taintor, R.R. , Vavrin, Z., Granger, D.L., Drapier, J-C, Aber, I.J. & Lancaster, J.R., jr. (1990). Synthesis of nitric oxide from a terminal guanidino nitrogen atom of L-arginine: a molecular mechanism regulating cellular proliferation that targets intracellular iron. In: Nitric oxide from L-arginine: A cellular Bioregulatory system, ed. S. Moncada, J.B. Hibbs, p. p. 189–223, Amsterdam: Elsevier Sci.Google Scholar
  21. 21.
    Hidetsugu, S., Kurose, I., Ebinuma, H., Fukumura, D. , Higuchi, H., Atsukawa, K., Tada, S., Kimura, H., Yonei, Y., Masuda, T., Mura, S. & Ishii, H. (1996). Kupffer cell-mediated cytotoxicity against hepatoma cells occur through production of nitric oxide and adhesion via ICAM-1/CD18. Intern. Immunol. 8 (7), 1165–1172.CrossRefGoogle Scholar
  22. 22.
    Hirata, M & Murad, F. (1994). Interrelationships of cyclic GMP, inositol phosphates and calcium. Adv. Pharmacol. 26, 195–216.CrossRefPubMedGoogle Scholar
  23. 23.
    Hogg, N., Darley-Usmar, V., Wilson, M.T. & Moncada, S. (1992). Production of hydroxyl-radicals from the simultaneous generation of superoxide and nitric oxide. Biochem. J. 281, 419–424.PubMedGoogle Scholar
  24. 24.
    Honn, K. V., Tang, D. G. & Chen, Y.Q. (1992). Platelets and cancer metastasis: more than an epiphenomenon. Semin. Thromb. Hemostas., 18, 392–415.CrossRefGoogle Scholar
  25. 25.
    Jaffe, E.A., Grulich, J, Welksler, B.B., Hampel, G. & Watanabe, K., (1987). Correlation between thrombin-induced prostacyclin production and inositol triphosphate and cytosolic free calcium levels in cultured human endothelial cells. J. Biol. Chem., 262, 8557–8565.PubMedGoogle Scholar
  26. 26.
    Jenkins, D.C., Charles, I.G, Thompson, L.L., Moss, D.W., Holnes, L.S., Bayliss, S.A., Rhodes, P., Westmore, K., Emson, P.C. & Moncada, S. (1995). Roles of nitric oxide in tumour growth. Proc. Natl. Acad. Sci. U.S.A. 92, 4392–4396.CrossRefPubMedGoogle Scholar
  27. 27.
    Kariya, K., Kawahara, Y., Araki, S., Fukuzaki, H. & Takai, Y., (1989). Antiprolifarative action of cGMP-elevating vasodilators in cultured rabbit aortic smooth muscle cells. Atherosklerosis, 80, 143–147.CrossRefGoogle Scholar
  28. 28.
    Karpatkin, S., Pearlstein, E., Ambrogio, C. & Coller, B.S. (1988). Role of adhesive proteins on platelet tumour interaction in vitro and metastasis formation in vitro. J. Clin Invest, 81, 1012–1019.CrossRefPubMedGoogle Scholar
  29. 29.
    Katsuki, S., Arnold, W., Mittal, C. & Mural, F. (1977). Stimulation of guanylate cyclase by sodium nitroprusside, nitroglycerin and nitric oxide in various tissue preparation and comparison to the effects of sodium azide and hydroxylamine. J. Cyclic Nucleotide Res. 3, 23–35.PubMedGoogle Scholar
  30. 30.
    Koch, A.E., Halloram, M.M., Haskell, C.J., Shah, M.R. & Polverini, P.J. (1995). Angiogenesis mediated by soluble forms of E-selectin and vascular cell adhesion molecule-1. Nature, 376, 517–519.CrossRefPubMedGoogle Scholar
  31. 31.
    Kubota, Y., Kleinman, H.K., Martin, G.R. & Lawley, T.J. (1988). The role of laminin and basement membrane in the morphological differentiation of human endothelial cells into capillary-like structures. J.Cell Biol., 107, 1589–1598.CrossRefPubMedGoogle Scholar
  32. 32.
    Lee, Y.S. & Wurster, R.D. (1994). Potentiation on anti-proliferative effect of nitroprusside by ascorbate in human brain tumour cells. Cancer Letters, 78 (1–3), 19–23.CrossRefPubMedGoogle Scholar
  33. 33.
    Leibovich, S.J., Polverini, P.J., Fong, T.W., Hardow, L.A. & Koch, A.E., (1994). Production of angiogenic activity by human monocytes requires an L-arginine-nitric oxide synthase dependent effector mechanism. Proc. Natl. Acad. Sei. USA., 91, 4190–4194.CrossRefGoogle Scholar
  34. 34.
    Lejeune, P., Lagadec, P., Onier, N., Pinad, D., Ohshima, H. & Jeannin, J.F. (1994). Nitric oxide involvement in tumour-induced immunosuppression. J. Immunol., 152, 5077–5083.PubMedGoogle Scholar
  35. 35.
    Liotta, LA., Steeg, P.S. & Stetler-Stevenson, W.G. (1991). Cancer metastasis and angiogenesis: An imbalance of positive and megative regulation. Cell, 64, 327–336.CrossRefPubMedGoogle Scholar
  36. 36.
    Maragoudakis, ME., Sarmonika, M., & Panoutsakopoulou, M., (1988). Rate of basement membrane biosynthesis as an index to angiogenesis. Tissue & Cell, 20, 531–539.CrossRefGoogle Scholar
  37. 37.
    McDonald, C.J. (1991). Cardiovascular complications of psoriasis. In: Psoriasis, ed. Roenigk, H.H. & Mailbach, H.J., p. p. 97–11, New York, Basel, Hong-Kong: Marcel Dekker Inc.Google Scholar
  38. 38.
    McDonald, L.J. & Murad, F. (1996). Nitric oxide and cyclic GMP signalling. Proc. Soc. Exp. Biol. Med. 211 (1), 1–6.PubMedGoogle Scholar
  39. 39.
    Miki, W., Kawabe, Y., & Kurijama, K. (1977). Activation of cerebral guanylate cyclase by nitric oxide. Biochem. Biophys. Res. Commun., 75, 851–856.CrossRefPubMedGoogle Scholar
  40. 40.
    Moncada, S., Radomski, M.W. & Palmer, R.M. (1988). Endothelium derived relaxing factor: identification as nitric oxide and role in the control of vascular tone and platelet function. Biochem. Pharmacol., 37, 2495–2501.CrossRefPubMedGoogle Scholar
  41. 41.
    Morbidelli, V., Chang, C-H, Douglas, J.G., Granger, HJ., Ledda, F. & Ziche, M. (1996). Nitric oxide mediates mitogenic effect of VEGF on coronary renular endothelium. Am. J. Physiol, 270 (Heart Circ. Physiol. 39): H411-H415.Google Scholar
  42. 42.
    Murad, F. (1986). Cyclic guanosine monophosphate as a mediator of vasodilatation. J. Clin. Invest. 78, 1–5.CrossRefPubMedGoogle Scholar
  43. 43.
    Nathan, C. & Hibbs, J.B. Jr. (1991). Role of nitric oxide synthesis in macrophage antimicrobial activity. Curr. Opin. Immunol., 3, 65–70.CrossRefPubMedGoogle Scholar
  44. 44.
    Nierodzik, ML., Kajumo, F. & Karpatkin, S. (1992). Effect of thrombin tretament of tumour cell on adhesion of tumour cells to platelets in vitro and tumour metastasis in vivo. Cancer Res., 52, 3267–3272.PubMedGoogle Scholar
  45. 45.
    Nierodzik, M., Plotkin, A., Kajumo, F. & Karpatkin, S., (1991). Thrombin stimulates tumour-platelet adhesion in vitro and metastasis in vivo. J. Clin. Invest., 87, 229–236.CrossRefPubMedGoogle Scholar
  46. 46.
    Nishio, E., Fukushima, K., Shiozaki, M. & Watanabe, Y (1996). Nitric oxide donor SNAP induces apoptosis in smooth muscle cells through cGMP-independent mechanisms. Biochem. Bophys. Res. Commun., 221, 163–168.CrossRefGoogle Scholar
  47. 47.
    Page, C.P. (1988). The involvement of platelet in non thrombotic processes. Trends in Pharmacol. Sci., 9, 66–71.CrossRefGoogle Scholar
  48. 48.
    Pearlstein, E., Ambrogio, C. & Karpatkin, S. (1984). Effect of antiplatelet antibody on the development of pulmonary metastasis following injection of CT26 colon adenosarcinoma, Lewis Lung carcinoma and CT16 a melanotic melanoma tumour cells into mice. Cancer Res. 44, 3384–3387Google Scholar
  49. 49.
    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.CrossRefGoogle Scholar
  50. 50.
    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 mononiitrate and dinitrate. Br. J. Pharmacol., 116, 1829–1834.CrossRefPubMedGoogle Scholar
  51. 51.
    Radomski, M.W., & Moncada, S. (1991). Biological role of nitric oxide in platelet function In: Clinical Relevance of nitric oxide in the cardiovascular system e.d. Moncada, S., Higgs, E.A. & Berrazueta, J.R., p. p. 45–56. Madrid: Edicomplet.Google Scholar
  52. 52.
    Rickles, F.R. & Edwards, R.L. (1983). Activation of blood coagulation in cancer: Trousseau’s syndrome revised. Blood, 62, 14–31.PubMedGoogle Scholar
  53. 53.
    Robertson, F.M., Long, B.W., Tober, K.L., Ross, M.S. & A Oberyszyn. (1996). Gene expression and cellular sources of inducible nitric oxide synthase during tumour promotion. Carcinogenesis, 17 (9), 2053–2059CrossRefPubMedGoogle Scholar
  54. 54.
    Rodeberg, A.D., CHaet, M.S., Bass, R.C., Arkovitz, M.S. & Garcia, V.F. (1995). Nitric oxide: An overview. Am. J. Surgery, 170, 292–303CrossRefGoogle Scholar
  55. 55.
    Rollo, E.E., Laskin, D.E., & Denhardt, D.T., (1996). Osteopontin inhibits nitric oxide production and cytotoxicity by activated RAW 264.7 macrophages. J. Leucocyte Biology 60 (3), 397–404.Google Scholar
  56. 56.
    Sanchez Bueno, A., Verkhusha, V., Tanaka, Y., Takikawa, D. & Yoshida, R. (1996). Interferon-gamma-dependent expression of inducible nitric oxide synthase, interleukin-12 and interferon-gamma-inducing factor in macrophages elicited by allografted tumour cells. Biochem. Biophys. Res. Commun., 224 (2), 555–563.CrossRefGoogle Scholar
  57. 57.
    Schmidt, H.H.H.W., Lohmann, S. M. & Walter, U. (1993). The nitric oxide and cGMP signal transduction system. Regulation and mechanism of action. Biochim. Biophys. Acta, 1178, 153–175.CrossRefPubMedGoogle Scholar
  58. 58.
    Stuher, D.J. & Griffith, D.W. (1992). Mammalian nitric oxide synthases. Adv. Enzymol, Relat. Areas. Mol. Biol. 65, 287–346Google Scholar
  59. 59.
    Stuher, D.J. & Nathan, C. (1989). Nitric oxide. A macrophage product responsible for cytostasis and respiratory inhibition in tumour cells. J. Exp. Med. 169, 1543–1555.CrossRefGoogle Scholar
  60. 60.
    Thomsen, L.L., Lawton, F.G., Knowles, R.G., Beesly, J.E., Riveros-Moreno, V. & Moncada, S. (1994). Nitric oxide synthase activity in human gynaecological cancer. Cancer Res., 54, 1352–1354.PubMedGoogle Scholar
  61. 61.
    Thomsen, L.L., Miles, D.W., Happerfield, L., Bobrow, L.G., Knowles, R.G. & Moncada, S. (1995). Nitric oxide synthase activity in human breast cancer. Br. J. Cancer, 72,41–44.CrossRefPubMedGoogle Scholar
  62. 62.
    Timpl, R., Rhode, H., Gehron Robey, P., Rennard, S.I., Foidart, J.M. & Martin, G.R. (1979). Laminin a glycoprotein from basement membranes. J. Biol. Chem., 254, 9933–9937.PubMedGoogle Scholar
  63. 63.
    Tsopanoglou, N.E., Pipili-Synetos, Eva & Maragoudakis, M.E. (1993a). Thrombin promotes angiogenesis by a mechanism independent of fibrin formation. Amer. J. Pysiol. 264 (Cell Physiol.33): C:1302-C1307.Google Scholar
  64. 64.
    Umansky, V., Rocha, M. & Schirrmacher, V. (1996a). Liver endothelial cells: Participation in most response to lymphoma metastasis. Cancer & Metastas. Rev. 15, 273–279.CrossRefGoogle Scholar
  65. 65.
    Umansky, V., Schirrmacher, V., & Rocha, M. (1996b). New insights into tumour-host interactions in lymphoma metastasis. J. Mol. Med. 74, 353–363.CrossRefPubMedGoogle Scholar
  66. 66.
    Xie, K., Dong, Z. & Filder, I.J. (1996). Activation of nitric oxide synthase gene for inhibition of cancer metastasis. J. Leucoc. Biol., 59, 797–803Google Scholar
  67. 67.
    Xie, K. P., Huang, S.Y., Dong, Z.Y., Juang, S.H., Gutman, M, Xie, Q.W., Nathan, C. & Fidler, I.J. (1995). Transfection with the inducible nitric-oxide synthase gene suppresses tumourigenicity and abrogates metastasis by M-1735 murine melanoma cells. J. Exp. Med., 181, 1333–1343.CrossRefPubMedGoogle Scholar
  68. 68.
    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.CrossRefPubMedGoogle Scholar
  69. 69.
    Yim, C.Y., Bastian, N.R., Smith, J.C., Hibbs, J.B. & A Samlowski (1993). Macrophage nitric oxide synthesis delays progression of ultra-violet light-induced murine skin cancers. Cancer Res., 53 (22), 5507–5511.PubMedGoogle Scholar
  70. 70.
    Yu, W.G., Yamamoto, N, Takenaka, H., Mu, J., Tai, X.G., Zou, J.P., Ogawa M, Tsutsui, T., Nijesuriya R., Yoshida, R., Herrman, S., Fujuvara, H. & Hamaoka, T. (1996). Molecular mechanisms underlying tumour immunotherapy with IL-12. International Immunol., 8 (6) 855–865.CrossRefGoogle Scholar
  71. 71.
    Yuang, F., Leuing, M., Berk, D.A. & Jain, R.K. (1993). Microvascular permeability of albumin, vascular surface area and vascular volume measured in human adenocarcinoma, LS174T using dorsal chamber in SCID mice. Microvasc. Res. 45, 269–289.CrossRefGoogle Scholar
  72. 72.
    Ziche, M., Morbidelli, L., Masini, E., Amerini, S., Granger HJ., Maggi, CA., Geppetti, P. & Ledola, 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.CrossRefGoogle Scholar
  73. 73.
    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.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1998

Authors and Affiliations

  • Eva Pipili-Synetos
    • 1
  • Michael E. Maragoudakis
    • 1
  1. 1.Department of Pharmacolgy, Medical SchoolUniversity of PatrasPatrasGreece

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