Nitric oxide-mediated regulation of hypoxia-induced B16F10 melanoma metastasis

International Journal of Cancer

Volumn 108, Issue 1, 2004, Pages 47-53

  Postovit, Lynne Marie ^a   Adams, Michael A ^a   Lash, Gendie E ^a,b   Heaton, Jeremy P W ^a   Graham, Charles H ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

B16F10; CGMP; Hypoxia; Invasion; Metastasis; Nitric oxide; Nitroglycerin

Indexed keywords

8 BROMO CYCLIC AMP; CYCLIC GMP; DIETHYLENETRIAMINE; DIETHYLENETRIAMINE NITRIC OXIDE; GLYCERYL TRINITRATE; GUANYLATE CYCLASE; NITRIC OXIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CELL CULTURE; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; HYPOXIA; INCUBATION TIME; LUNG METASTASIS; LUNG NODULE; MELANOMA CELL; METASTASIS; METASTASIS POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SOLUBILITY;

ANIMALS; ANOXIA; CYCLIC GMP; FEMALE; LUNG NEOPLASMS; MELANOMA, EXPERIMENTAL; MICE; NEOPLASM METASTASIS; NEOPLASM TRANSPLANTATION; NITRIC OXIDE; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED; TUMOR STEM CELL ASSAY;

EID: 0344825132     PISSN: 00207136     EISSN: None     Source Type: Journal    
DOI: 10.1002/ijc.11556     Document Type: Article

References (52)

1. Höckel M, Schlenger K, Aral B, Mitze M, Schaffer U, Vaupel P. Association between tumor hypoxia and malignant progression in advanced cancer of the uterine cervix. Cancer Res 1996;56:4509-15.
2. Brizel DM, Scully SP, Harrelson JM, Layfield LJ, Bean JM, Prosnitz LR, Dewhirst MW. Tumor oxygenation predicts for the likelihood of distant metastases in human soft tissue sarcoma. Cancer Res 1996; 56:941-3.
3. Brizel DM, Sibley GS, Prosnitz LR, Scher RL, Dewhirst MW. Tumor hypoxia adversely affects the prognosis of carcinoma of the head and neck. Int J Radiat Oncol Biol Phys 1997;38:285-9.
4. Lartigau E, Randrianarivelo H, Avril MF, Margulis A, Spatz A, Eschwege F, Guichard M. Intratumoral oxygen tension in metastatic melanoma. Melanoma Res 1997;7:400-6.
5. Brown JM. The hypoxic cell: a target for selective cancer therapy-eighteenth Bruce F. Cain Memorial Award lecture. Cancer Res 1999; 59:5863-70.
6. Teicher BA. Hypoxia and drug resistance. Cancer Metastasis Rev 1998;13:139-68.
7. Young SD, Marshall RS, Hill RP. Hypoxia induces DNA over replication and enhances metastatic potential of murine tumor cells. Proc Natl Acad Sci USA 1988;85:9533-7.
8. Cairns RA, Kalliomaki T, Hill RP. Acute (cyclic) hypoxia enhances spontaneous metastasis of KHT murine tumors. Cancer Res 2001;61: 8903-8.
9. Matthews NE, Adams MA. Maxwell LR, Gofton TE, Graham CH. Nitric oxide-mediated regulation of chemosensitivity in cancer cells. J Natl Cancer Inst 2001;93:1879-85.
10. Postovit LM, Adams MA, Lash GE, Heaton JP, Graham CH. Oxygen-mediated regulation of tumour cell invasiveness: involvement of a nitric oxide signaling pathway. J Biol Chem 2002;277:35730-7.
11. Huang LE, Willmore WG, Gu J, Goldberg MA, Bunn HF. Inhibition of hypoxia-inducible factor I activation by carbon monoxide and nitric oxide. Implications for oxygen sensing and signaling. J Biol Chem 1999;274:9038-44.
12. Schobersberger W, Hoffmann G, Fandrey J, Nitric oxide donors suppress erythropoietin production in vitro. Pflugers Arch 1996;432: 980-5.
13. Kourembanas S, McQuillan LP, Leung GK, Faller DV. Nitric oxide regulates the expression of vasoconstrictors and growth factors by vascular endothelium under both normoxia and hypoxia. J Clin Invest 1993;92:99-104.
14. Smith AP, Demoncheaux EA, Higenbottam TW. Nitric oxide gas decreases endothelin-1 mRNA in cultured pulmonary artery endothelial cells. Nitric Oxide 2002;6:153-9.
15. Liu Y, Christou H, Morita T, Laughner E, Semenza GL, Kourembanas S. Carbon monoxide and nitric oxide suppress the hypoxic induction of vascular endothelial growth factor gene via the 5′ enhancer. J Biol Chem 1998;273:15257-62.
16. Sogawa K, Numayama-Tsuruta K. Ema M, Abe M, Abe H, Fujii-Kuriyama Y. Inhibition of hypoxia-inducible factor I activity by nitric oxide donors in hypoxia. Proc Natl Acad Sci USA 1998:95:7368-73.
17. Denninger JW, Marletta MA. Guanylate cyclase and the NO/cGMP signaling pathway. Biochim Biophys Acta 1999;1411:334-50.
18. Sogo N, Magid KS, Shaw CA, Webb DJ, Megson IL. Inhibition of human platelet aggregation by nitric oxide donor drugs: relative contribution of cGMP-independent mechanisms. Biochem Biophys Res Commun 2000;279:412-9.
19. Forslund T, Nilsson HM, Sundqvist T. Nitric oxide regulates the aggregation of stimulated human neutrophils. Biochem Biophys Res Commun 2000;274:482-7.
20. Nicolson GL, Brunson KW, Fidler IJ. Specificity of arrest, survival, and growth of selected metastatic variant cell lines. Cancer Res 1978;38:4105-11.
21. Bennett BM, McDonald BJ, Nigam R, Simon WC. Biotransformation of organic nitrates and vascular smooth muscle cell function. Trends Pharmacol Sci 1994; 15:245-9.
22. Diodati JG, Quyyumi AA, Hussain N, Keefer LK. Complexes of nitric oxide with nucleophiles as agents for the controlled biological release of nitric oxide: antiplatelet effect. Thromb Haemost 1993;70:654-8.
23. Tharaux PL, Chatziantoniou C, Casellas D, Fouassier L, Ardaillou R, Dussaule JC. Vascular endothelin-1 gene expression and synthesis and effect on renal type I collagen synthesis and nephroangiosclerosis during nitric oxide synthase inhibition in rats. Circulation 1999;99: 2185-91.
24. Faller DV. Endothelial cell responses to hypoxic stress. Clin Exp Pharmacol Physiol 1999;26:74-84.
25. Qiu H, Orr FW, Jensen D, Wang HH, McIntosh AR, Hasinoff BB, Nance DM, Pylypas S, Qi K, Song C, Muschel RJ, Al Mehdi AB. Arrest of B16 melanoma cells in the mouse pulmonary microcirculation induces endothelial nitric oxide synthase-dependent nitric oxide release that is cytotoxic to the tumor cells. Am J Pathol 2003; 162: 403-12.
26. Yamamoto T, Terada N, Nishizawa Y, Tanaka H, Akedo H, Seiyama A, Shiga T, Kosaka H. Effects of NG-nitro-L-arginine and/or L-arginine on experimental pulmonary metastasis in mice. Cancer Lett 1994;87:115-20.
27. Yamamoto T, Terada N, Seiyama A, Nishizawa Y, Akedo H, Kosaka H. Increase in experimental pulmonary metastasis in mice by L-arginine under inhibition of nitric oxide production by NG-nitro-L-arginine methyl ester. Int J Cancer 1998;75:140-4.
28. Taylor CT, Lisco SJ, Awtrey CS, Colgan SP. Hypoxia inhibits cyclic nucleotide-stimulated epithelial ion transport: role for nucleotide cyclases as oxygen sensors. J Pharmacol Exp Ther 1998;284:568-75.
29. Adachi T, Shinomura T, Nakao S, Kurata J, Murakawa M, Shichino T, Seo N, Mori K. Chronic treatment with nitric oxide synthase (NOS) inhibitor profoundly reduces cerebellar NOS activity and cyclic guanosine monophosphate but does not modify minimum alveolar anesthetic concentration. Anesth Analg 1995;81:862-5.
30. Alderton WK, Cooper CE, Knowles RG. Nitric oxide synthases: structure, function and inhibition. Biochem J 2001;357:593-615.
31. Dweik RA, Laskowski D, Abu-Soud HM, Kaneko F, Hutte R, Stuehr DJ, Erzurum SC. Nitric oxide synthesis in the lung. Regulation by oxygen through a kinetic mechanism. J Clin Invest 1998;101:660-6.
32. Whorton AR, Simonds DB, Piantadosi CA. Regulation of nitric oxide synthesis by oxygen in vascular endothelial cells, Am J Physiol 1997;272:L1161-6.
33. Palmer LA, Semenza GL, Stoler MH, Johns RA. Hypoxia induces type II NOS gene expression in pulmonary artery endothelial cells via HIF-1. Am J Physiol 1998;274:L212-9.
34. Inoue T, Kwon AH, Oda M, Kaibori M, Kamiyama Y, Nishizawa M, Ito S, Okumura T. Hypoxia and heat inhibit inducible nitric oxide synthase gene expression by different mechanisms in rat hepatocytes. Hepatology 2000;32:1037-44.
35. Zulueta JJ, Sawhney R, Kayyali U, Fogel M, Donaldson C, Huang H, Lanzillo JJ, Hassoun PM. Modulation of inducible nitric oxide synthase by hypoxia in pulmonary artery endothelial cells. Am J Respir Cell Mol Biol 2002;26:22-30.
36. Takemoto M, Sun J, Hiroki J, Shimokawa H, Liao JK. Rho-kinase mediates hypoxia-induced downregulation of endothelial nitric oxide synthase. Circulation 2002;106:57-62.
37. Kashiwagi K, Iizuka Y, Mochizuki S, Tsumamoto Y, Mishima HK, Araie M, Suzuki Y, Tsukahara S. Differences in nitric oxide production: a comparison of retinal ganglion cells and retinal glial cells cultured under hypoxic conditions. Brain Res Mol Brain Res 2003; 112:126-34.
38. Cuvier C, Jang A, Hill RP. Exposure to hypoxia, glucose starvation and acidosis: effect on invasive capacity of murine tumor cells and correlation with cathepsin (L + B) secretion. Clin Exp Metastasis 1997;15:19-25.
39. Rofstad EK, Rasmussen H, Galappathi K, Mathiesen B, Nilsen K, Graff BA. Hypoxia promotes lymph node metastasis in human melanoma xenografts by up-regulating the urokinase-type plasminogen activator receptor. Cancer Res 2002;62:1847-53.
40. Couzin J. Medicine. Tracing the steps of metastasis, cancer's menacing ballet. Science 2003;299:1002-6.
41. Herzig M, Christofori G. Recent advances in cancer research: mouse models of tumorigenesis. Biochim Biophys Acta 2002;1602:97-113.
42. Chambers AF, Naumov GN, Varghese HJ, Nadkarni KV, MacDonald IC, Groom AC. Critical steps in hematogenous metastasis: an overview. Surg Oncol Clin N Am 2001;10:243-55, vii.
43. Wong CW, Song C, Grimes MM, Fu W, Dewhirst MW, Muschel RJ, Al Mehdi AB. Intravascular location of breast cancer cells after spontaneous metastasis to the lung. Am J Pathol 2002:161:749-53.
44. Graham CH, Forsdike J, Fitzgerald CF, Macdonald-Goodfellow S. Hypoxia-mediated stimulation of carcinoma cell invasiveness via upregulation of urokinase receptor expression. Int J Cancer 1999;80: 617-23.
45. Maity A, Solomon D. Both increased stability and transcription contribute to the induction of the urokinase plasminogen activator receptor (uPAR) message by hypoxia. Exp Cell Res 2000:255:250-7.
46. Minchenko A, Bauer T, Salceda S, Caro J. Hypoxic stimulation of vascular endothelial growth factor expression in vitro and in vivo. Lab Invest 1994:71:374-9.
47. Toi M, Matsumoto T, Bando H. Vascular endothelial growth factor: its prognostic, predictive, and therapeutic implications. Lancet Oncol 2001;2:667-73.
48. Memarzadeh S, Kozak KR, Chang L, Natarajan S, Shintaku P, Reddy ST, Farias-Eisner R, Memarzedeh S. Urokinase plasminogen activator receptor: Prognostic biomarker for endometrial cancer. Proc Natl Acad Sci USA 2002;99:10647-52.
49. Xing RH, Rabbani SA. Overexpression of urokinase receptor in breast cancer cells results in increased tumor invasion, growth and metastasis. Int J Cancer 1996;67:423-9.
50. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1995;1:27-31.
51. Aguirre-Ghiso JA, Liu D, Mignatti A, Kovalski K, Ossowski L. Urokinase receptor and fibronectin regulate the ERK(MAPK) to p38(MAPK) activity ratios that determine carcinoma cell proliferation or dormancy in vivo. Mol Biol Cell 2001;12:863-79.
52. Aguirre Ghiso JA, Kovalski K, Ossowski L. Tumor dormancy induced by downregulation of urokinase receptor in human carcinoma involves integrin and MAPK signaling. J Cell Biol 1999; 147:89-104.