Inducible nitric oxide synthase (iNOS) activity could be responsible for resistance or sensitivity to IFNγ-induced apoptosis in several human hepatoma cell lines

Journal of Interferon and Cytokine Research

Volumn 26, Issue 12, 2006, Pages 901-913

  Vadrot, Nathalie ^a   Legrand, Agnès ^a   Nello, Elisabeth ^a   Bringuier, Annie France ^a   Guillot, Raymonde ^a   Feldmann, Gérard ^a  

^a CENTRE DE RECHERCHE BIOMÉDICALE BICHAT BEAUJON CRB3   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; N(G) NITROARGININE METHYL ESTER; SMALL INTERFERING RNA; STAT1 PROTEIN;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; HEPATOMA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; TRANSACTIVATION;

EID: 33845903327     PISSN: 10799907     EISSN: None     Source Type: Journal    
DOI: 10.1089/jir.2006.26.901     Document Type: Article

References (50)

1. Stark GR, Kerr IM, Williams BRG, Silverman RH, Schreiber RD. How cells respond to interferons. Annu. Rev. Biochem. 1998;67:227-264.
2. Schiller JH, Witt PL, Storer B, Alberti D, Tombes MB, Arzoomanian R, Brown RR, Proctor RA, Voss SD, Spriggs DR. Clinical and biological effects of combination therapy with gamma-interferon and tumor necrosis factor. Cancer 1992;69:562-571.
3. Kim CJ, Tautenberger JK, Simonis TB, White DE, Rosenberg SA, Marincola FM. Combination therapy with interferon-gamma and interleukin-2 for the treatment of metastatic melanoma. J. Immunother. Emphasis Tumor Immunol. 1996;19:50-58.
4. Koshiji M, Adachi Y, Sogo S, Taketani S, Oyaizu N, Than S, Inaba M, Phawa S, Hioki K, Ikehara S. Apoptosis of colorectal adenocarcinoma (COLO 201) by tumour necrosis factor-alpha (TNF-α) and/or interferon-gamma (IFN-γ), resulting from down-modulation of Bcl-2 expression. Clin. Exp. Immunol. 1998;111:211-218.
5. Schindler C. STATs as activators of apoptosis. Trends Cell. Biol. 1998;8:97-98.
6. Lamboley C, Bringuier AF, Feldmann G. Apoptotic behavior of hepatic and extra hepatic tumor cell lines differs after Fas stimulation. Cell. Mol. Biol. 2000;46:13-28.
7. Darnell JE. Stats and gene regulation. Science 1997;277:1630-1635.
8. Schindler C, Darnell JE. Transcriptional response to polypeptide ligands: the JAK-STAT pathway. Annu. Rev. Biochem. 1995;64:621-651.
9. Ihle JN. The STAT family in cytokine signaling. Curr. Opin. Cell Biol. 2001;13:211-217.
10. 2-dependent activation of nuclear factor κB. J. Biol. Chem. 2001;276:8918-8923.
11. Moreau R. Are nitric oxide synthases new players in the pathophysiology of fulminant hepatic failure? J. Hepatol. 2002;37:678-680.
12. Kim YM, De Vera ME, Watkins SC, Billiar TR. Nitric oxide protects cultured rat hepatocytes from tumor necrosis factor-α-induced apoptosis by inducing heat shock protein 70 expression. J. Biol. Chem. 1997:272:1402-1411.
13. Mosser DD, Caron AW, Bourget L, Denis-Larose C, Massie B. Role of the human heat shock protein HSP70 in protection against stress-induced apoptosis. Mol. Cell Biol. 1997;17:5317-5327.
14. Jolly C, Morimoto RI. Role of the heat shock response and molecular chaperones in oncogenesis and cell death. J. Natl. Cancer Inst. 2000;92:1564-1572.
15. Der SD, Zhou A, Williams BRG, Silverman RH. Identification of genes differentially regulated by interferon α, β or γ using oligonucleotide arrays. Proc. Natl. Acad. Sci. USA 1998;95:15623-15628.
16. Spanaus KS, Schlapbach R, Fontana A. TNF-α and IFN-γ render microglia sensitive to Fas ligand-induced apoptosis by induction of Fas expression and down-regulation of Bcl-2 and Bcl-xL. Eur. J. Immunol. 1998;28:4398-4408.
17. Ossina NK, Cannas A, Powers VC, Fitzpatrick PA, Knight JD, Gilbert JR, Shekhtman EM, Tomei LD, Umansky SR, Kiefer MC. Interferon-γ modulates a p53-independent apoptotic pathway and apoptosis-related gene expression. J. Biol. Chem. 1997;272:16351-16357.
18. Legrand A, Vadrot N, Lardeux B, Bringuier AF, Guillot R, Feldmann G. Study of the effects of interferon α on several human hepatoma cell lines: analysis of the signalling pathway of the cytokine and of its effects on apoptosis and cell proliferation. Liver Int. 2004;24:149-160.
19. Andrews NC, Faller DV. A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res. 1991;19:2499-2500.
20. Sadowski HB, Gilman MZ. Cell-free activation of a DNA-binding protein by epidermal growth factor. Nature 1993;362:79-83.
21. Nadori F, Lardeux B, Rahmani M, Bringuier A, Durand-Schneider AM, Bernuau D. Presence of distinct AP-1 dimers in normal and transformed rat hepatocytes under basal conditions and after epidermal growth factor stimulation. Hepatology 1997;26:1477-1483.
22. Le Cam A. Electroporation-mediated gene transfer into hepatocytes. Methods Mol. Biol. 1995;48:141-150.
23. Rahmani M, Nadori F, Durand-Schneider AM, Lardeux B, Bernuau D. Hepatocyte growth factor activates the AP-1 complex: a comparison between normal and transformed rat hepatocytes. J. Hepatol. 1999;30:916-925.
24. Seed B, Sheen JY. A simple phase-extraction assay for chloramphenicol acetyltransferase activity. Gene 1988:67:271-277.
25. Kaabache T, Barraud B, Feldmann G, Bernuau D, Lardeux B. Direct solution hybridization of guanidine thiocyanate-solubilized cells for quantitation of mRNAs in hepatocytes. Anal. Biochem. 1995;232:225-230.
26. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidine thiocyanate-phenol-chloroform. Anal. Biochem. 1987;162:156-159.
27. Chin YE, Kitagawa M, Kuida K, Flavell RA, Fu XY. Activation of the STAT signaling pathway can cause expression of caspase 1 and apoptosis. Mol. Cell. Biol. 1997;17:5328-5337.
28. Karlsen AE, Pavlovic D, Nielsen K, Jensen J, Andersen HU, Pociot F, Mandrup-Poulsen T, Eizirik DL, Nerup J. Interferon-gamma induces interleukin-1 converting enzyme expression in pancreatic islets by an interferon regulatory factor-1-dependent mechanism. J. Clin. Endocrinol. Metab. 2000;85:830-836.
29. O'Connell J, Bennett MW, Nally K, O'Sullivan GC, Collins JK, Shanahan F. Interferon-γ sensitizes colonie epithelial cell lines to physiological and therapeutic inducets of colonocyte apoptosis. J. Cell. Physiol. 2000;185:331-338.
30. Detjen KM, Farwig K, Welzel M, Wiedenmann B, Rosewicz S. Interferon gamma inhibits growth of human pancreatic carcinoma cells via caspase-1 dependent induction of apoptosis. Gut 2001;49:251-262.
31. Dai C, Krantz SB. Interferon-γ induces upregulation and activation of caspases 1, 3 and 8 to produce apoptosis in human erythroid progenitor cells. Blood 1999;93:3309-3316.
32. Ruiz-Ruiz C, Munoz-Pinedo C, Lopez-Rivas A. Interferon γ treatment elevates caspase 8 expression and sensitizes human breast tumor cells to a death receptor-induced mitochondria-operated apoptotic program. Cancer Res. 2000;60:5673-5680.
33. Fulda S, Debatin KM. IFN-γ sensitizes for apoptosis by upregulating caspase-8 expression through the Stat1 pathway. Oncogene 2002;21:2295-2308.
34. Choi C, Park JY, Lee J, Lim JH, Shin EC, Ahn YS, Kim CH, Kim SJ, Kim JD, Choi IS, Choi IH. Fas ligand and Fas are expressed constitutively in human astrocytes and the expression increases with IL-1, IL-6, TNF-alpha, or IFN-gamma. J. Immunol. 1999;162:1889-1895.
35. Moers C, Warskulat U, Muschen M, Even J, Niederacher D, Josien R, Koldovsky U, Beckmann MW, Haussinger D. Regulation of CD95 (Apo-1/Fas) ligand and receptor expression in squamous-cell carcinoma by interferon-gamma and cisplatin. Int. J. Cancer 1999;80:564-572.
36. Li JH, Kluger MS, Madge LA, Zheng L, Bothwell AL, Pober JS. Interferon-gamma augments CD95 (APO-1/Fas) and pro-caspase-8 expression and sensitizes human vascular endothelial cells to CD95-mediated apoptosis. Am. J. Pathol. 2002;161:1485-1495.
37. Ahn EY, Pan G, Vickers SM, McDonald JM. IFN-γ upregulates apoptosis-related molecules and enhances Fas-mediated apoptosis in human cholangiocarcinoma. Int. J. Cancer 2002;100:445-451.
38. Lamboley C, Bringuier AF, Camus E, Lardeux B, Groyer A, Feldmann G. Overexpression of the mouse Fas gene in Hep3B hepatoma cells overcomes their resistance to Fas-mediated apoptosis. J. Hepatol. 2002;36:385-394.
39. Locksin RA, Zakeri Z. Caspase-independent cell deaths. Curr. Opin. Cell. Biol. 2002;14:727-733.
40. Kano A, Haruyama T, Akaike T, Watanabe Y. IRF-1 is an essential mediator in IFN-gamma-induced cell cycle arrest and apoptosis of primary cultured hepatocytes. Biochem. Biophys. Res. Commun. 1999;257:672-677.
41. Scovassi AI, Poirier GG. Poly(ADP-ribosylation) and apoptosis. Mol. Cell. Biochem. 1999;199:125-137.
42. Adjei PN, Kaufmann SH, Leung WY, Mao F, Gores GJ. Selective induction of apoptosis in Hep3B cells by topoisomerase I inhibitors: evidence for a protease-dependent pathway that does not activate cysteine protease P32. J. Clin. Invest. 1996;98:2 588-2596.
43. Nagao M, Nakajima Y, Kanehiro H, Hisanaga M, Aomatsu Y, Ko S, Tatekawa Y, Ikeda N, Kanokogi H, Urizono Y, Kobayashi T, Shibaji T, Kanamura T, Ogawa S, Nakano H. The impact of interferon gamma receptor expression on the mechanism of escape from host immune surveillance in hepatocellular carcinoma. Hepatology 2000;32:491-500.
44. Lee KY, Anderson E, Madani K, Rosen GD. Loss of STAT1 expression confers resistance to IFNγ-induced apoptosis in ME180 cells. FEBS Lett. 1999;459:323-326.
45. McNaughton L, Puttagunta L, Martinez-Cuesta MA, Kneteman N, Mayers I, Moqbel R, Hamid Q, Radomski MW. Distribution of nitric oxide synthase in normal and cirrhotic human liver. Proc. Natl. Acad. Sci. USA 2002;94:17161-17166.
46. Ou J, Carlos TM, Watkins SC, Saavedra JE, Keefer LK, Kim YM, Harbrecht BG, Billiar TR. Differential effects of nonselective inaudible NOS inhibition on hepatic necrosis, apoptosis, ICAM-1 expression and neutrophil accumulation during endotoxemia. Nitric Oxide 1997;1:404-416.
47. Rai RM, Lee FY, Rosen A, Yang SQ, Lin HZ, Koteish A, Liew FY, Zaragoza C. Impaired liver regeneration in inducible nitric oxide synthase deficient mice. Proc. Natl. Acad. Sci. USA 1998;95:13829-13834.
48. Mojena M, Hortelano S, Castrillo A, Diaz-Guerra MJ, Garcia-Barchino MJ, Saez GT, Bosca L. Protection by nitric oxide against liver inflammatory injury in animals carrying a nitric oxide synthase-2 transgene. FASEB J. 2001;15:583-585.
49. Kim YM, Kim TH, Chung HT, Talanian RV, Yin XM, Billiar TR. Nitric oxide prevents tumor necrosis factor alpha-induced rat hepatocytes apoptosis by the interruption of mitochondrial apoptotic signaling through S-nitrosylation of caspase-8. Hepatology 2000;32:770-778.
50. Farghali H, Canova N, Kucera T, Martinek J, Masek K. Nitric oxide synthase inhibitors modulate lipopolysaccharide-induced hepatocyte injury: dissociation in vivo and in vitro effects. Int. Immunopharmacol. 2003;3:1627-1638.