Induction of endothelial nitric oxide synthase expression by melanoma sensitizes endothelial cells to tumor necrosis factor-driven cytotoxicity

Clinical Cancer Research

Volumn 10, Issue 20, 2004, Pages 6879-6886

  Mocellin, Simone ^a   Provenzano, Maurizio ^b   Rossi, Carlo Riccardo ^a   Pilati, Pierluigi ^a   Scalerta, Romano ^a   Lise, Mario ^a   Nitti, Donato ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; CITRULLINE; COMPLEMENTARY DNA; MESSENGER RNA; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; TUMOR NECROSIS FACTOR;

APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL VIABILITY; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DNA SYNTHESIS; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME ASSAY; GENE EXPRESSION; HUMAN; HUMAN CELL; MELANOMA; METASTASIS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SKIN BIOPSY; SKIN TUMOR;

BIOPSY; CELL CULTURE TECHNIQUES; ENDOTHELIAL CELLS; GENE EXPRESSION PROFILING; HUMANS; MELANOMA; NEOPLASM METASTASIS; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE III; POLYMERASE CHAIN REACTION; PROGNOSIS; SKIN NEOPLASMS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 6044234745     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-04-0791     Document Type: Article

References (58)

1. Cars well EA, Old LJ, Kassel RL, Green S, Fiore N, Williamson B. An endotoxin-induced serum factor that causes necrosis of tumors. Proc Natl Acad Sci USA 1975;72:3666-70.
2. Rossi CR, Foletto M, Pilati P, Mocellin S, Lise M. Isolated limb perfusion in locally advanced cutaneous melanoma. Semin Oncol 2002;29:400-9.
3. Rossi CR, Mocellin S, Pilati P, Foletto M, Nitti D, Lise M. TNFalpha-based isolated perfusion for limb-threatening soft tissue sarcomas: state of the art and future trends. J Immunother 2003;26:291-300.
4. Alexander HR, Bartlett DL, Libutti SK, Fraker DL, Moser T, Rosenberg SA. Isolated hepatic perfusion with tumor necrosis factor and melphalan for unresectable cancers confined to the liver. J Clin Oncol 1998;16:1479-89.
5. Duerksen-Hughes PJ, Day DB, Laster SM, Zachariades NA, Aquino L, Gooding LR. Both tumor necrosis factor and nitric oxide participate in lysis of simian virus 40-transformed cells by activated macrophages. J Immunol 1992;149:2114-22.
6. Kwak JY, Man MK, Choi KS, et al. Cytokines secreted by lymphokine-activated killer cells induce endogenous nitric oxide synthesis and apoptosis in DLD-1 colon cancer cells. Cell Immunol 2000;203:84-94.
7. Lotzova E, Savary CA. Human natural killer cell development from bone marrow progenitors: analysis of phenotype, cytotoxicity and growth. Nat Immun 1993;12:209-17.
8. Lu G, Janjic BM, Janjic J, Whiteside TL, Storkus WJ, Vujanovic NL. Innate direct anticancer effector function of human immature dendritic cells. II. Role of TNF, lymphotoxin-alpha(1)beta(2), Fas ligand, and TNF-related apoptosis-inducing ligand. J Immunol 2002;168:1831-9.
9. de Wilt JH, ten Hagen TL, de Boeck G, van Tiel ST, de Bruijn EA, Eggermont AM. Tumour necrosis factor alpha increases melphalan concentration in tumour tissue after isolated limb perfusion. Br J Cancer 2000;82:1000-3.
10. van der Veen AH, de Wilt JH, Eggermont AM, van Tiel ST, Seynhaeve AL, ten Hagen TL. TNF-alpha augments intratumoural concentrations of doxorubicin in TNF-alpha-based isolated limb perfusion in rat sarcoma models and enhances anti-tumour effects. Br J Cancer 2000;82:973-80.
11. Stoelcker B, Ruhland B, Hehlgans T, Bluethmann H, Luther T, Mannel DN. Tumor necrosis factor induces tumor necrosis via tumor necrosis factor receptor type 1-expressing endothelial cells of the tumor vasculature. Am J Pathol 2000;156:1171-6.
12. Gnant MF, Berger AC, Huang J, et al. Sensitization of tumor necrosis factor alpha-resistant human melanoma by tumor-specific in vivo transfer of the gene encoding endothelial monocyte-activating polypeptide II using recombinant vaccinia virus. Cancer Res 1999;59:4668-74.
13. Lejeune FJ, Ruegg C, Lienard D. Clinical applications of TNF-alpha in cancer. Curr Opin Immunol 1998;10:573-80.
14. Madge LA, Pober JS. TNF signaling in vascular endothelial cells. Exp Mol Pathol 2001;70:317-25.
15. Ruegg C, Yilmaz A, Bieler G, Bamat J, Chaubert P, Lejeune FJ. Evidence for the involvement of endothelial cell integrin alphaVbeta3 in the disruption of the tumor vasculature induced by TNF and IFN-gamma. Nat Med 1998;4:408-14.
16. Ashkenazi A. Targeting death and decoy receptors of the tumour-necrosis factor superfamily. Nat Rev Cancer 2002;2:420-30.
17. Aggarwal B. Signaling pathways of the TNF superfamily: a double edged sword. Nat Rev Immunol 2003;3:745-56.
18. Maianski NA, Roos D, Kuijpers TW. Tumor necrosis factor alpha induces a caspase-independent death pathway in human neutrophils. Blood 2003;101:1987-95.
19. Leist M, Jaattela M. Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev Mol Cell Biol 2001;2:589-98.
20. Dimmeler S, Zeiher AM. Nitric oxide and apoptosis: another paradigm for the double-edged role of nitric oxide. Nitric Oxide 1997;1:275-81.
21. Salerno L, Sorrenti V, Di Giacomo C, Romeo G, Siracusa MA. Progress in the development of selective nitric oxide synthase (NOS) inhibitors. Curr Pharm Des 2002;8:177-200.
22. Estrada C, Gomez C, Martin C, Moncada S, Gonzalez C. Nitric oxide mediates tumor necrosis factor-alpha cytotoxicity in endothelial cells. Biochem Biophys Res Commun 1992;186:475-82.
23. Maciejewski JP, Selleri C, Sato T, et al. Nitric oxide suppression of human hematopoiesis in vitro. Contribution to inhibitory action of interferon-gamma and tumor necrosis factor-alpha. J Clin Investig 1995;96:1085-92.
24. Binder C, Schulz M, Hiddemann W, Oellerich M. Induction of inducible nitric oxide synthase is an essential part of tumor necrosis factor-alpha-induced apoptosis in MCF-7 and other epithelial tumor cells. Lab Investig 1999;79:1703-12.
25. De Nadai C, Sestili P, Cantoni O, et al. Nitric oxide inhibits tumor necrosis factor-alpha-induced apoptosis by reducing the generation of ceramide. Proc Natl Acad Sci USA 2000;97:5480-5.
26. Kim YM, Talanian RV, Billiar TR. Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms. J Biol Chem 1997;272:31138-48.
27. Dimmeler S, Haendeler J, Nehls M, Zeiher AM. Suppression of apoptosis by nitric oxide via inhibition of interleukin-1beta-converting enzyme (ICE)-like and cysteine protease protein (CPP)-32-like proteases. J Exp Med 1997;185:601-7.
28. Bulotta S, Barsacchi R, Rotiroti D, Borgese N, Clementi E. Activation of the endothelial nitric-oxide synthase by tumor necrosis factor-alpha. A novel feedback mechanism regulating cell death. J Biol Chem 2001;276:6529-36.
29. Rossi CR, Foletto M, Mocellin S, Pilati P, Lise M. Hyperthermic isolated limb perfusion with low-dose tumor necrosis factor-alpha and melphalan for bulky in-transit melanoma metastases. Ann Surg Oncol 2004;11:173-7.
30. Bredt DS, Snyder SH. Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. Proc Natl Acad Sci USA 1989;86:9030-3.
31. Mocellin S, Rossi C, Pilati P, Nitti D, Marincola F. Quantitative real time PCR: a powerful ally in cancer research. Trends Mol Med 2003;9:189-195.
32. Mocellin S, Provenzano M, Lise M, Nitti D, Rossi CR. Increased TIA-1 gene expression in the tumor microenvironment after locoregional administration of tumor necrosis factor-alpha to patients with soft tissue limb sarcoma. Int J Cancer 2003;107:317-22.
33. de la Taille A, Katz AE, Bagiella E, et al. Microvessel density as a predictor of PSA recurrence after radical prostatectomy. A comparison of CD34 and CD31. Am J Clin Pathol 2000;113:555-62.
34. Koukourakis MI, Giatromanolaki A, Thorpe PE, et al. Vascular endothelial growth factor/KDR activated microvessel density versus CD31 standard microvessel density in non-small cell lung cancer. Cancer Res 2000;60:3088-95.
35. Wieberdink J, Benckhuysen C, Braat RP, van Slooten EA, Olthuis GA. Dosimetry in isolation perfusion of the limbs by assessment of perfused tissue volume and grading of toxic tissue reactions. Eur J Cancer Clin Oncol 1982;18:905-10.
36. Mocellin S, Provenzano M, Rossi CR, Pilati P, Nitti D, Lise M. Use of quantitative real-time PCR to determine immune cell density and cytokine gene profile in the tumor microenvironment. J Immunol Methods 2003;280:1-11.
37. Ziehe M, Morbidelli L, Choudhuri R, et al. Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis. J Clin Investig 1997;99:2625-34.
38. Moochhala S, Rajnakova A. Role of nitric oxide in cancer biology. Free Radic Res 1999;31:671-9.
39. Hegardt P, Widegren B, Sjogren HO. Nitric-oxide-dependent systemic immunosuppression in animals with progressively growing malignant gliomas. Cell Immunol 2000;200:116-27.
40. Kahn DA, Archer DC, Gold DP, Kelly CJ. Adjuvant immunotherapy is dependent on inducible nitric oxide synthase. J Exp Med 2001;193:1261-8.
41. Bogdan C. Nitric oxide and the immune response. Nat Immunol 2001;2:907-16.
42. Wink DA, Vodovotz Y, Laval J, Laval F, Dewhirst MW, Mitchell JB. The multifaceted roles of nitric oxide in cancer. Carcinogenesis (Lond.) 1998;19:711-21.
43. Thomsen LL, Miles DW. Role of nitric oxide in tumour progression: lessons from human tumours. Cancer Metastasis Rev 1998;17:107-18.
44. Xu W, Liu LZ, Loizidou M, Ahmed M, Charles IG. The role of nitric oxide in cancer. Cell Res 2002;12:311-20.
45. Ambs S, Merriam WG, Ogunfusika MO, et al. p53 and vascular endothelial growth factor regulate tumor growth of NOS2-expressing human carcinoma cells. Nat Med 1998;4:1371-6.
46. Konopka TE, Barker JE, Bamford TL, Guida E, Anderson RL, Stewart AG. Nitric oxide synthase II gene disruption: implications for tumor growth and vascular endothelial growth factor production. Cancer Res 2001;61:3182-7.
47. Jadeski LC, Hum KO, Chakraborty C, Lala PK. Nitric oxide promotes murine mammary tumour growth and metastasis by stimulating tumour cell migration, invasiveness and angiogenesis. Int J Cancer 2000;86:30-9.
48. Jadeski LC, Lala PK. Nitric oxide synthase inhibition by N(G)-nitro-L-arginine methyl ester inhibits tumor-induced angiogenesis in mammary tumors. Am J Pathol 1999;155:1381-90.
49. Vakkala M, Kahlos K, Lakari E, Paakko P, Kinnula V, Soini Y. Inducible nitric oxide synthase expression, apoptosis, and angiogenesis in in situ and invasive breast carcinomas. Clin Cancer Res 2000;6:2408-16.
50. Mocellin S, Riccardo Rossi C, Traldi P, Nitti D, Lise M. Molecular oncology in the post-genomic era: the challenge of proteomics. Trends Mol Med 2004;10:24-32.
51. Binder C, Binder L, Kroemker M, Schulz M, Hiddemann W. Influence of cycloheximide-mediated down-regulation of glucose transport on TNF alpha-induced apoptosis. Exp Cell Res 1997;236:223-30.
52. Slowik MR, Min W, Ardito T, Karsan A, Kashgarian M, Pober JS. Evidence that tumor necrosis factor triggers apoptosis in human endothelial cells by interleukin-1-converting enzyme-like protease-dependent and -independent pathways. Lab Investig 1997;77:257-67.
53. Carretero J, Obrador E, Esteve JM, et al. Tumoricidal activity of endothelial cells. Inhibition of endothelial nitric oxide production abrogates tumor cytotoxicity induced by hepatic sinusoidal endothelium in response to B16 melanoma adhesion in vitro. J Biol Chem 2001;276:25775-82.
54. Vercammen D, Beyaert R, Denecker G, et al. Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J Exp Med 1998;187:1477-85.
55. Cauwels A, Janssen B, Waeytens A, Cuvelier C, Brouckaert P. Caspase inhibition causes hyperacute tumor necrosis factor-induced shock via oxidative stress and phospholipase A2. Nat Immunol 2003;4:387-93.
56. Abe K, Shoji M, Chen J, et al. Regulation of vascular endothelial growth factor production and angiogenesis by the cytoplasmic tail of tissue factor. Proc Natl Acad Sci USA 1999;96:8663-8.
57. Graeven U, Rodeck U, Karpinski S, Jost M, Philippou S, Schmiegel W. Modulation of angiogenesis and tumorigenicity of human melanocytic cells by vascular endothelial growth factor and basic fibroblast growth factor. Cancer Res 2001;61:7282-90.
58. de Wilt JH, Manusama ER, van Etten B, et al. Nitric oxide synthase inhibition results in synergistic anti-tumour activity with melphalan and tumour necrosis factor alpha-based isolated limb perfusions. Br J Cancer 2000;83:1176-82.