Nitric oxide and tumor biology

Nitric Oxide, Cell Signaling, and Gene Expression

Volumn , Issue , 2005, Pages 395-420

  Sonveaux, Pierre ^a   Feron, Olivier ^a  

^a UCL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 40249092194     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (105)

1. Stuehr, D.J., Cho, H.J., Kwon, N.S., Weise, M.F., and Nathan, C.F. Purification and characterization of the cytokine-induced macrophage nitric oxide synthase: an FAD- and FMN-containing flavoprotein. Proc. Natl. Acad. Sci. USA 88: 7773-7 (1991).
2. Markewitz, B.A., Michael, J.R., and Kohan, D.E. Cytokine-induced expression of a nitric oxide synthase in rat renal tubule cells. J. Clin. Invest. 91: 2138-43 (1993).
3. Koide, M., Kawahara, Y., Tsuda, T., and Yokoyama, M. Cytokine-induced expression of an inducible type of nitric oxide synthase gene in cultured vascular smooth muscle cells. FEBS Lett. 318: 213-7 (1993).
4. Amaro, M.J., Bartolome, J., and Carreno, V. Hepatitis B virus X protein transactivates the inducible nitric oxide synthase promoter. Hepatology 29: 915-23 (1999).
5. Elmore, L.W. et al. Hepatitis B virus X protein and p53 tumor suppressor interactions in the modulation of apoptosis. Proc. Natl. Acad. Sci. U S A 94: 14707-12 (1997).
6. Szabo, C., Zingarelli, B., O’Connor, M., and Salzman, A.L. DNA strand breakage, activation of poly (ADP-ribose) synthetase, and cellular energy depletion are involved in the cytotoxicity of macrophages and smooth muscle cells exposed to peroxynitrite. Proc. Natl. Acad. Sci. USA 93: 1753-8 (1996).
7. Szabo, C. and Salzman, A.L. Inhibition of terminal calcium overload protects against peroxynitrite-induced cellular injury in macrophages. Immunol. Lett. 51: 163-7 (1996).
8. Xia, Y. and Zweier, J.L. Superoxide and peroxynitrite generation from inducible nitric oxide synthase in macrophages. Proc. Natl. Acad. Sci. USA 94: 6954-8 (1997).
9. Hofseth, L.J., Hussain, S.P., Wogan, G.N., and Harris, C.C. Nitric oxide in cancer and chemoprevention. Free Radic. Biol. Med. 34: 955-68 (2003).
10. Hanahan, D. and Weinberg, R.A. The hallmarks of cancer. Cell 100: 57-70 (2000).
11. Black, W.C. and Welch, H.G. Advances in diagnostic imaging and overestimations of disease prevalence and the benefits of therapy. N. Engl. J. Med. 328: 1237-43 (1993).
12. Dachs, G.U. and Tozer, G.M. Hypoxia modulated gene expression: angiogenesis, metastasis and therapeutic exploitation. Eur. J. Cancer 36: 1649-60 (2000).
13. Vaupel, P., Kelleher, D.K., and Hockel, M. Oxygen status of malignant tumors: pathogenesis of hypoxia and significance for tumor therapy. Semin. Oncol. 28: 29-35 (2001).
14. Folkman, J. Tumor angiogenesis: therapeutic implications. N. Engl. J. Med. 285: 1182-6 (1971).
15. Bergers, G. and Benjamin, L.E. Tumorigenesis and the angiogenic switch. Nat. Rev. Cancer 3: 401-10 (2003).
16. Fukumura, D., Yuan, F., Endo, M., and Jain, R.K. Role of nitric oxide in tumor microcirculation. Blood flow, vascular permeability, and leukocyte-endothelial interactions. Am. J. Pathol. 150: 713-25 (1997).
17. Lubbe, A.S. and Huhnt, W. Microvessel diameters of human colon adenocarcinoma during acute treatment with serotonin. Int. J. Microcirc. Clin. Exp. 14: 218-25 (1994).
18. Huhnt, W. and Lubbe, A.S. Venules and arterioles in xenotransplanted human colon adenocarcinoma critically constrict with hyperthermia and serotonin. J. Cancer Res. Clin. Oncol. 121: 267-74 (1995).
19. Thews, O., Kelleher, D.K., and Vaupel, P.W. Modulation of spatial O2 tension distribution in experimental tumors by increasing arterial O2 supply. Acta Oncol. 34, 291-5 (1995).
20. Emerich, D.F. et al. Bradykinin modulation of tumor vasculature: I. Activation of B2 receptors increases delivery of chemotherapeutic agents into solid peripheral tumors, enhancing their efficacy. J. Pharmacol. Exp. Ther. 296: 623-31 (2001).
21. Song, C.W. Blood perfusion and microenvironment of human tumors. (Molls, M. and Vaupel, P., eds.), pp. 193-208 (Springer-Verlag, Berlin, 1998).
22. Kiani, M.F., Pries, A.R., Hsu, L.L., Sarelius, I.H., and Cokelet, G.R. Fluctuations in microvascular blood flow parameters caused by hemodynamic mechanisms. Am. J. Physiol. 266, H1822-8 (1994).
23. Dewhirst, M.W. et al. Microvascular studies on the origins of perfusion-limited hypoxia. Br. J. Cancer Suppl. 27, S247-51 (1996).
24. Kimura, H. et al. Fluctuations in red cell flux in tumor microvessels can lead to transient hypoxia and reoxygenation in tumor parenchyma. Cancer Res. 56: 5522-8 (1996).
25. Feron, O. Targeting the tumor vascular compartment to improve conventional cancer therapy. Trends Pharmacol. Sci. 25: 536-42 (2004).
26. Thomsen, L.L. et al. Nitric oxide synthase activity in human gynecological cancer. Cancer Res. 54: 1352-4 (1994).
27. Thomsen, L.L. et al. Nitric oxide synthase activity in human breast cancer. Br. J. Cancer 72: 41-4 (1995).
28. Ambs, S. et al. Frequent nitric oxide synthase-2 expression in human colon adenomas: implication for tumor angiogenesis and colon cancer progression. Cancer Res. 58: 334-41 (1998).
29. Ambs, S. et al. Relationship between p53 mutations and inducible nitric oxide synthase expression in human colorectal cancer. J. Natl. Cancer. Inst. 91: 86-8 (1999).
30. Tschugguel, W. et al. Inducible nitric oxide synthase (iNOS) expression may predict distant metastasis in human melanoma. Br. J. Cancer 79: 1609-12 (1999).
31. Chen, T. and Stoner, G.D. Inducible nitric oxide synthase expression in Nnitrosomethylbenzylamine (NMBA)-induced rat esophageal tumorigenesis. Mol. Carcinog. 40: 232-40 (2004).
32. Chen, T., Nines, R.G., Peschke, S.M., Kresty, L.A., and Stoner, G.D. Chemopreventive effects of a selective nitric oxide synthase inhibitor on carcinogen-induced rat esophageal tumorigenesis. Cancer Res. 64: 3714-7 (2004).
33. Takahashi, M., Mutoh, M., Kawamori, T., Sugimura, T., and Wakabayashi, K. Altered expression of beta-catenin, inducible nitric oxide synthase and cyclooxygenase-2 in azoxymethane-induced rat colon carcinogenesis. Carcinogenesis 21: 1319-27 (2000).
34. Komatsu, S., Watanabe, H., Oka, T., Tsuge, H., and Kat, N. Dietary vitamin B6 suppresses colon tumorigenesis, 8-hydroxyguanosine, 4-hydroxynonenal, and inducible nitric oxide synthase protein in azoxymethane-treated mice. J. Nutr. Sci Vitaminol (Tokyo) 48: 65-8 (2002).
35. Murakami, A. et al. Inhibitory effect of citrus nobiletin on phorbol ester-induced skin inflammation, oxidative stress, and tumor promotion in mice. Cancer Res. 60, 5059-66 (2000).
36. Kampa, M. et al. Wine antioxidant polyphenols inhibit the proliferation of human prostate cancer cell lines. Nutr. Cancer 37: 223-33 (2000).
37. Martinez, J. and Moreno, J.J. Effect of resveratrol, a natural polyphenolic compound, on reactive oxygen species and prostaglandin production. Biochem. Pharmacol. 59, 865-70 (2000).
38. Trikha, P., Sharma, N., and Athar, M. Nitroglycerin: an NO donor inhibits TPAmediated tumor promotion in murine skin. Carcinogenesis 22: 1207-11 (2001).
39. Schleiffer, R., Duranton, B., Gosse, F., Bergmann, C., and Raul, F. Nitric oxide synthase inhibition promotes carcinogen-induced preneoplastic changes in the colon of rats. Nitric Oxide 4: 583-9 (2000).
40. Inano, H., Suzuki, K., Ishii-Ohba, H., Ikeda, K., and Wakabayashi, K. Pregnancydependent initiation in tumorigenesis of Wistar rat mammary glands by 60Coirradiation. Carcinogenesis 12: 1085-90 (1991).
41. Inano, H. and Onoda, M. Role of nitric oxide in radiation-induced initiation of mammary tumorigenesis in rats. Nitric Oxide 8: 144-8 (2003).
42. Voevodskaya, N.V. and Vanin, A.F. Gamma-irradiation potentiates L-argininedependent nitric oxide formation in mice. Biochem. Biophys. Res. Commun. 186: 1423-8 (1992).
43. Onoda, M. and Inano, H. Localization of nitric oxide synthases and nitric oxide production in the rat mammary gland. J. Histochem. Cytochem. 46: 1269-78 (1998).
44. Ibuki, Y. and Goto, R. Enhancement of NO production from resident peritoneal macrophages by in vitro gamma-irradiation and its relationship to reactive oxygen intermediates. Free Radic. Biol. Med. 22: 1029-35 (1997).
45. Kisley, L.R. et al. Genetic ablation of inducible nitric oxide synthase decreases mouse lung tumorigenesis. Cancer Res. 62: 6850-6 (2002).
46. Ellies, L.G. et al. Mammary tumor latency is increased in mice lacking the inducible nitric oxide synthase. Int. J. Cancer 106: 1-7 (2003).
47. Ahn, B. and Ohshima, H. Suppression of intestinal polyposis in Apc(Min/+) mice by inhibiting nitric oxide production. Cancer Res. 61: 8357-60 (2001).
48. Scott, D.J. et al. Lack of inducible nitric oxide synthase promotes intestinal tumorigenesis in the Apc(Min/+) mouse. Gastroenterology 121: 889-99 (2001).
49. Ziesche, R. et al. Lipopolysaccharide and interleukin 1 augment the effects of hypoxia and inflammation in human pulmonary arterial tissue. Proc. Natl. Acad. Sci. USA 93: 12478-83 (1996).
50. Liao, J.K. et al. Regulation of bovine endothelial constitutive nitric oxide synthase by oxygen. J. Clin. Invest. 96: 2661-6 (1995).
51. Arnet, U.A., McMillan, A., Dinerman, J.L., Ballermann, B., and Lowenstein, C.J. Regulation of endothelial nitric-oxide synthase during hypoxia. J. Biol. Chem. 271, 15069-73 (1996).
52. Phelan, M.W. and Faller, D.V. Hypoxia decreases constitutive nitric oxide synthase transcript and protein in cultured endothelial cells. J. Cell Physiol. 167: 469-76 (1996).
53. Searles, C.D., Miwa, Y., Harrison, D.G., and Ramasamy, S. Posttranscriptional regulation of endothelial nitric oxide synthase during cell growth. Circ Res. 85: 588-95 (1999).
54. Liu, S.F., Adcock, I.M., Old, R.W., Barnes, P.J., and Evans, T.W. Differential regulation of the constitutive and inducible nitric oxide synthase mRNA by lipopolysaccharide treatment in vivo in the rat. Crit. Care Med. 24: 1219-25 (1996).
55. Kaku, Y. et al. Differential induction of constitutive and inducible nitric oxide synthases by distinct inflammatory stimuli in bovine aortic endothelial cells. Biochim. Biophys. Acta 1356: 43-52 (1997).
56. Inoue, N. et al. Molecular regulation of the bovine endothelial cell nitric oxide synthase by transforming growth factor-beta 1. Arterioscler. Thromb. Vasc. Biol. 15, 1255-61 (1995).
57. Kostyk, S.K. et al. Basic fibroblast growth factor increases nitric oxide synthase production in bovine endothelial cells. Am. J. Physiol. 269, H1583-9 (1995).
58. Kroll, J. and Waltenberger, J. VEGF-A induces expression of eNOS and iNOS in endothelial cells via VEGF receptor-2 (KDR). Biochem. Biophys. Res. Commun. 252, 743-6 (1998).
59. Brouet, A., Sonveaux, P., Dessy, C., Balligand, J.L., and Feron, O. Hsp90 ensures the transition from the early Ca2+-dependent to the late phosphorylation-dependent activation of the endothelial nitric-oxide synthase in vascular endothelial growth factor-exposed endothelial cells. J. Biol. Chem. 276: 32663-9 (2001).
60. He, H. et al. Vascular endothelial growth factor signals endothelial cell production of nitric oxide and prostacyclin through flk-1/KDR activation of c-Src. J. Biol. Chem. 274: 25130-5 (1999).
61. Michell, B.J. et al. The Akt kinase signals directly to endothelial nitric oxide synthase. Curr. Biol. 9: 845-8 (1999).
62. Kupatt, C., Dessy, C., Hinkel, R., Raake, P., Daneau, G., Bouzin, C., Boekstegers, P., and Feron O. Heat shock protein 90 transfection reduces ischemia-reperfusioninduced myocardial dysfunction via reciprocal endothelial NO synthase serine 1177 phosphorylation and threonine 495 dephosphorylation. Arterioscler. Thromb. Vasc. Biol. 24: 1435-41 (2004).
63. Murata, T., Sato, K., Hori, M., Ozaki, H., and Karaki, H. Decreased endothelial nitric-oxide synthase (eNOS) activity resulting from abnormal interaction between eNOS and its regulatory proteins in hypoxia-induced pulmonary hypertension. J. Biol. Chem. 277: 44085-92 (2002).
64. Arena, S. et al. Nitric oxide production stimulated by the basic fibroblast growth factor requires the synthesis of ceramide. Ann. NY Acad. Sci. 973: 94-104 (2002).
65. Barsacchi, R. et al. Activation of endothelial nitric-oxide synthase by tumor necrosis factor-alpha: a novel pathway involving sequential activation of neutral sphingomyelinase, phosphatidylinositol-3' kinase, and Akt. Mol. Pharmacol. 63: 886-95 (2003).
66. Carmeliet, P. Mechanisms of angiogenesis and arteriogenesis. Nat. Med. 6: 389-95 (2000).
67. Six, I., Kureishi, Y., Luo, Z., and Walsh, K. Akt signaling mediates VEGF/VPF vascular permeability in vivo. FEBS Lett. 532: 67-9 (2002).
68. Albina, J.E., Mills, C.D., Henry, W.L., Jr., and Caldwell, M.D. Temporal expression of different pathways of 1-arginine metabolism in healing wounds. J. Immunol. 144, 3877-80 (1990).
69. Ziche, M. et al. Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by substance P. J. Clin. Invest. 94: 2036-44 (1994).
70. Kirk, S.J. et al. Arginine stimulates wound healing and immune function in elderly human beings. Surgery 114, 155-9; discussion 160 (1993).
71. Lee, P.C. et al. Impaired wound healing and angiogenesis in eNOS-deficient mice. Am. J. Physiol. 277, H1600-8 (1999).
72. Papapetropoulos, A., Garcia-Cardena, G., Madri, J.A., and Sessa, W.C. Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J. Clin. Invest. 100: 3131-9 (1997).
73. Ziche, M. et al. Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis. J. Clin. Invest. 99: 2625-34 (1997).
74. Murohara, T. et al. Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J. Clin. Invest. 101: 2567-78 (1998).
75. Fukumura, D. et al. Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proc. Natl. Acad. Sci. USA 98: 2604-9 (2001).
76. Yamasaki, K. et al. Reversal of impaired wound repair in iNOS-deficient mice by topical adenoviral-mediated iNOS gene transfer. J. Clin. Invest. 101: 967-71 (1998).
77. Kimura, H. et al. Hypoxia response element of the human vascular endothelial growth factor gene mediates transcriptional regulation by nitric oxide: control of hypoxia-inducible factor-1 activity by nitric oxide. Blood 95: 189-97 (2000).
78. Jadeski, L.C. and Lala, P.K. Nitric oxide synthase inhibition by N(G)-nitro-Larginine methyl ester inhibits tumor-induced angiogenesis in mammary tumors. Am. J. Pathol. 155: 1381-90 (1999).
79. Dong, Z., Staroselsky, A.H., Qi, X., Xie, K., and Fidler, I.J. Inverse correlation between expression of inducible nitric oxide synthase activity and production of metastasis in K-1735 murine melanoma cells. Cancer Res. 54: 789-93 (1994).
80. Juang, S.H. et al. Suppression of tumorigenicity and metastasis of human renal carcinoma cells by infection with retroviral vectors harboring the murine inducible nitric oxide synthase gene. Hum. Gene Ther. 9: 845-54 (1998).
81. Gratton, J.P. et al. Selective inhibition of tumor microvascular permeability by cavtratin blocks tumor progression in mice. Cancer Cell 4: 31-9 (2003).
82. Sonveaux, P. et al. Irradiation-induced angiogenesis through the up-regulation of the nitric oxide pathway: implications for tumor radiotherapy. Cancer Res. 63: 1012-9 (2003).
83. Folkman, J. and Camphausen, K. Cancer. What does radiotherapy do to endothelial cells? Science 293: 227-8 (2001).
84. d’Uscio, L.V. and Luscher, T.F. Nitric oxide: biology and pathobiology. (Ignarro, L.J., ed.), pp. 609-20 (Academic Press, San Diego, 2000).
85. Andrade, S.P., Hart, I.R., and Piper, P.J. Inhibitors of nitric oxide synthase selectively reduce flow in tumor-associated neovasculature. Br. J. Pharmacol. 107: 1092-5 (1992).
86. Meyer, R.E. et al. Nitric oxide synthase inhibition irreversibly decreases perfusion in the R3230Ac rat mammary adenocarcinoma. Br. J. Cancer 71: 1169-74 (1995).
87. Tozer, G.M., Prise, V.E., and Chaplin, D.J. Inhibition of nitric oxide synthase induces a selective reduction in tumor blood flow that is reversible with L-arginine. Cancer Res. 57: 948-55 (1997).
88. Wood, P.J. et al. Induction of hypoxia in experimental murine tumors by the nitric oxide synthase inhibitor, NG-nitro-L-arginine. Cancer Res. 54: 6458-63 (1994).
89. Jordan, B.F. et al. Changes in tumor oxygenation/perfusion induced by the NO donor, isosorbide dinitrate, in comparison with carbogen: monitoring by EPR and MRI. Int. J. Radiat. Oncol. Biol. Phys. 48: 565-70 (2000).
90. Jordan, B.F., Beghein, N., Aubry, M., Gregoire, V., and Gallez, B. Potentiation of radiation-induced regrowth delay by isosorbide dinitrate in FSaII murine tumors. Int. J. Cancer 103: 138-41 (2003).
91. Wood, P.J. et al. Modification of energy metabolism and radiation response of a murine tumour by changes in nitric oxide availability. Biochem. Biophys. Res. Commun. 192: 505-10 (1993).
92. Wood, P.J. et al. Changes in energy metabolism and X-ray sensitivity in murine tumours by the nitric oxide donor SIN-1. Br. J. Cancer Suppl. 27, S177-80 (1996).
93. Shan, S.Q. et al. Effects of diethylamine/nitric oxide on blood perfusion and oxygenation in the R3230Ac mammary carcinoma. Br. J. Cancer 76: 429-37 (1997).
94. Thews, O., Kelleher, D.K., and Vaupel, P. No improvement in perfusion and oxygenation of experimental tumors upon application of vasodilator drugs. Int. J. Oncol. 19: 1243-7 (2001).
95. Feelisch, M., Ostrowski, J., and Noack, E. On the mechanism of NO release from sydnonimines. J. Cardiovasc. Pharmacol. 14 Suppl 11, S13-22 (1989).
96. Stamler, J.S. et al. Blood flow regulation by S-nitrosohemoglobin in the physiological oxygen gradient. Science 276: 2034-7 (1997).
97. Dewhirst, M.W. et al. Quantification of longitudinal tissue pO2 gradients in window chamber tumours: impact on tumour hypoxia. Br. J. Cancer 79: 1717-22 (1999).
98. Mitchell, J.B. et al. Hypoxic mammalian cell radiosensitization by nitric oxide. Cancer Res. 53: 5845-8 (1993).
99. Mitchell, J.B. et al. Radiation sensitisation by nitric oxide releasing agents. Br. J. Cancer Suppl. 27, S181-4 (1996).
100. Jordan, B.F. et al. Insulin increases the sensitivity of tumors to irradiation: involvement of an increase in tumor oxygenation mediated by a nitric oxide-dependent decrease of the tumor cells oxygen consumption. Cancer Res. 62: 3555-61 (2002).
101. Drummond, G.R., Cai, H., Davis, M.E., Ramasamy, S., and Harrison, D.G. Transcriptional and posttranscriptional regulation of endothelial nitric oxide synthase expression by hydrogen peroxide. Circ. Res. 86: 347-54 (2000).
102. Thomas, S.R., Chen, K., and Keaney, J.F., Jr. Hydrogen peroxide activates endothelial nitric-oxide synthase through coordinated phosphorylation and dephosphorylation via a phosphoinositide 3-kinase-dependent signaling pathway. J. Biol. Chem. 277: 6017-24 (2002).
103. Sonveaux, P. et al. Endothelin-1 is a critical mediator of myogenic tone in tumor arterioles: implications for cancer treatment. Cancer Res. 64: 3209-14 (2004).
104. Sonveaux, P. et al. Modulation of the tumor vasculature functionality by ionizing radiation accounts for tumor radiosensitization and promotes gene delivery. FASEB J. 16: 1979-81 (2002).
105. Cai, H. and Harrison, D.G. Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ Res. 87: 840-4 (2000).