Nitric oxide inhibits apoptosis via AP-1-dependent CD95L transactivation

Cancer Research

Volumn 60, Issue 9, 2000, Pages 2377-2383

  Melino, Gerry ^a   Bernassola, Francesca ^a   Catani, Maria Valeria ^a   Rossi, Antonello ^a   Corazzari, Marco ^a   Sabatini, Stefania ^a   Vilbois, Francis ^b   Green, Douglas R ^c  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b SERONO PHARMACEUTICAL RES INSTITUTE   (Switzerland)

^c LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; ETOPOSIDE; FAS ANTIGEN; NITRIC OXIDE; PROTEIN C JUN; TRANSCRIPTION FACTOR AP 1;

AMINO ACID SEQUENCE; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; DNA BINDING; DOSE RESPONSE; ENZYME ACTIVATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; PRIORITY JOURNAL; PROMOTER REGION; TRANSACTIVATION; WESTERN BLOTTING;

AMINO ACID SEQUENCE; APOPTOSIS; BLOTTING, WESTERN; CELL NUCLEUS; CERAMIDES; DNA FRAGMENTATION; DOSE-RESPONSE RELATIONSHIP, DRUG; ETOPOSIDE; FAS LIGAND PROTEIN; HUMANS; JURKAT CELLS; MEMBRANE GLYCOPROTEINS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; NITRIC OXIDE; NITRIC OXIDE DONORS; NUCLEIC ACID SYNTHESIS INHIBITORS; PENICILLAMINE; POLY(ADP-RIBOSE) POLYMERASES; PROTO-ONCOGENE PROTEINS C-JUN; TIME FACTORS; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTOR AP-1; TRANSFECTION;

EID: 0034194327     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (50)

1. Stamler, J. S., Singel, D. J., and Loscalzo, J. Biochemistry of nitric oxide and its redox-activated forms. Science (Washington DC), 258: 1898-1902, 1992.
2. Stamler, J. S., Simon, D. I., Osborne, J. A., Mullins, M. E., Jaraki, O., Michel, T., Singel, D. J., and Loscalzo, J. S-nitrosylation of proteins with nitric oxide: synthesis and characterization of biologically active compounds. Proc. Natl. Acad. Sci. USA, 89: 444-448, 1992.
3. Lipton, S. A., Choi, Y. B., Pan, Z. H., Lei, S. Z., Chen, H. S., Sucher, N. J., Loscalzo, J., Singel, D. J., and Stamler, J. S. A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature (Lond.), 364: 626-632, 1993.
4. Xu, L., Eu, J. P., Meissner, G., and Stamler, J. S. Activation of the cardiac calcium release channel (ryanodine receptor) by poly-S-nitriosylation. Science (Washington DC), 279: 234-237, 1998.
5. Lander, H. M., Ogiste, J. S., Pearce, S. F., Levi, R., and Novogrodsky, A. Nitric oxide-stimulated guanine nucleotide exchange on p21 Ras. J. Biol. Chem., 270: 7017-7020, 1995.
6. So, H. S., Park, R. K., Kim, M. S., Lee, S. R., Jung, B. H., Chung, S. Y., Jun, C. D., and Chung, H. T. Nitric oxide inhihits c-Jun N-terminal kinase 2 (JNK2) via S-nitrosylation. Biochem. Biophys. Res. Commun., 247: 809-813, 1998.
7. Mohr, S., Stamler, J. S., and Brüne, B. Posttranslational modifications of glyceral-dehyde-3-phosphate dehydrogenase by S-nitrosylation and subsequent NADH attachment. J. Biol. Chem., 271: 4209-4214, 1996.
8. Jia, L., Bonaventura, C., Bonaventura, J., and Stamler, J. S. S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature (Lond.), 380: 221-226, 1996.
9. Gow, A., and Stamler, J. S. Reactions between nitric oxide and haemoglobin under physiological conditions. Nature (Lond.), 391: 169-173, 1998.
10. Melino, G., Bernassola, F., Knight, R. A., Corasaniti, M. T., Nisticò, G., and Finazzi-Agrò, A. S-nitrosylation regulates apoptosis. Nature (Lond.), 388: 432-433, 1997.
11. Dimmeler, S., Haendeler, J., Nehls, M., and Zeiher, A. M. Suppression of apoptosis by nitric oxide by inhibition of ICE-like and CPP32-like proteases. J. Exp. Med., 185: 601-608, 1997.
12. Matthews, J. R., Botting, C. H., Panico, M., Morris, H. R., and Hay, R. T. Inhibition of NF-κB DNA binding by nitric oxide. Nucleic Acids Res., 24: 2236-2242, 1996.
13. Hausladen, A., Privalle, C. T., Keng, T., DeAngelo, J., and Stamler, J. S. Nitrosative stress: activation of the transcription factor Oxy R. Cell, 86: 719-729, 1996.
14. Brendeford, E. M., Andersson, K. B., and Gabrielsen, O. S. Nitric oxide (NO) disrupts specific DNA binding of the transcription factor c-Myb in vitro. FEBS Lett., 425: 52-56, 1998.
15. Tabuchi, A., Sano, K., Oh, E., Tsuchiya, T., and Tsuda, M. Modulation of AP-1 activity by nitric oxide (NO) in vitro: NO-mediated modulation of AP-1. FEBS Lett., 351: 123-127, 1994.
16. Stamler, J. S., and Hausladen, A. Oxidative modifications in nitrosative stress. Nat. Struct. Biol., 5: 247-249, 1998.
17. Nicotera, P., and Leist, M. Energy supply and the shape of death in neurons and lymphoid cells. Cell Death Differ., 4: 435-442, 1997.
18. Ankarcrona, M., Dypbuki, J. M., Bonfoco, E., Zhivotovsky, B., Orrenius, S., Lipton, S. A., and Nicotera, P. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron, 15: 1-13, 1995.
19. Leist, M., Single, B., Castoldi, A. F., Kühnle, S., and Nicotera, P. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J. Exp. Med., 185: 1481-1486, 1997.
20. Li, J., and Billiar, T. R. The anti-apoptotic actions of nitric oxide in hepatocytes. Cell Death Differ., 6: 952-955, 1999.
21. Liu, L., and Stamler, J. S. NO: an inhibitor of cell death. Cell Death Differ., 6: 937-942, 1999.
22. Li, J., Billiar T. R., Talanian, R. V., and Kim, Y. M. Nitric oxide reversibly inhibits seven members of the caspase family via S-nitrosylation. Biochem. Biophys. Res. Commun., 240: 419-424, 1997.
23. Mannick, J. B., Hausladen, A., Liu, L., Hess, D. T., Zeng, M., Miao, Q. X., Kane, L. S., Gow, A. J., and Stamler, J. S. Fas-induced caspase denitrosylation. Science (Washington DC), 284: 651-654, 1999.
24. Curran, T., and Franza, B. R. Fos, and Jun. the AP-1 connection. Cell, 55: 395-397, 1988.
25. Kyriakis, J., Banergee, P., Nikolakaki, E., Dai, T., Rubie, E., Ahmad, M., Avruch, J., and Woodgett, J. The stress-activated protein kinase subfamily of c-Jun kinases. Nature (Lond.), 369: 156-160, 1994.
26. Liu, Z. G., Hsu, H., Goeddel, D. V., and Karin, M. Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NFkB activation prevents cell death. Cell, 87: 565-576, 1996.
27. Lenczowsky, J. M., Dominguez, L., Eder, A. M., King, L. B., Zacharchuk, C. M., and Ashwell, J. D. Lack of a role for Jun kinase and AP-1 in Fas-induced apoptosis. Mol. Cell. Biol., 17: 170-181, 1997.
28. Verheij, M., Bose, R., Lin, X. H., Yao, B., Jarvis, W. D., Grant, S., Birrer, M. J., Szabo, E., Zon, L. I., Kyriakis, J. M., Haimovitz-Friedman, A., Fuks, Z., and Kolesnick, R. N. Requirement for ceramide-initiated SAPK-JNK signalling in stress-induced apoptosis. Nature (Lond.), 380: 75-79, 1996.
29. Wilson, D. J., Fortner, K. A., Lynch, D. H., Mattingly, R. R., Macara, I. G., Posada, J. A., and Budd, R. C. JNK, but not MAPK, activation is associated with Fas-mediated apoptosis in human T cells. Eur. J. Immunol., 26: 989-994, 1996.
30. Herr, I., Wilhelm, D., Meyer, E., Jeremias, I., Angel, P., and Debatin, K. M. TRAIL-induced JNK/SAPK activity depends on FADD/caspase-signaling in human lymphoid cells. Cell Death Differ., 6: 130-135, 1999.
31. Jacobs-Helber, S. M., Wickrema, A., Birrer, M. J., and Sawyer, S. T. AP-1 regulation of proliferation and initiation of apoptosis in erythropoietin-dependent erythroid cells. Mol. Cell. Biol., 18: 3699-3707, 1998.
32. Sawai, H., Okazaki, T., Yamamoto, H., Okano, H., Takeda, Y., Tashima, M., Sawada, H., Okuma, M., Ishikura, H., and Umehara, H. Requirement of AP-1 for ceramide-induced apoptosis in human leukemia HL-60 cells. J. Biol. Chem., 270: 27326-27331, 1995.
33. Chen, Y-R., Wang, X., Templeton, D., Davis, R., and Tan, T-H. The role of c-Jun N-terminal kinase (JNK) in apoptosis induced by ultraviolet C and γ radiation. J. Biol. Chem., 271: 31929-31936, 1996.
34. Ishikawa, Y., Yokoo, T., and Kitamura, M. c-Jun/AP-1, but not Nf-kB, is a mediator for oxidant-initiated apoptosis in glomerular mesangial cells. Biochem. Biophys. Res. Commun., 240: 496-501, 1997.
35. Herr, I., Wilhelm, D., Böhler, T., Angel, P., and Debatin, K. M. Activation of CD95 (APO-1/Fas) signaling by ceramide mediates cancer therapy-induced apoptosis. EMBO J., 16: 6200-6208, 1997.
36. Takahashi, T., Tanaka, M., Inazawa, J., Abe, T., Suda, T., and Nagata, S. Human Fas ligand. Gene structure, chromosomal localization and species specificity. Int. Immunol., 6: 1567-1574, 1994.
37. Kasibhatla, S., Brunner, T., Genestier, L., Echeverri, F., Mahboubi, A., and Green, D. R. DNA damaging agents induce expression of Fas-ligand and subsequent apoptosis in T lymphocytes via the activation of NF-kB and AP-1. Mol. Cell., 1: 543-551, 1998.
38. Faris, M., Kokot, N., Latinis, K., Kasibhatla, S., Green, D. R., Koretzky, G. A., and Nel, A. The c-jun N-terminal kinase cascade plays a role in stress-induced apoptosis in Jurkat cells by up-regulating Fas ligand expression. J. Immunol., 160: 134-144, 1998.
39. Piacentini, M., Fesus, L., and Melino, G. Multiple cell cycle access to the apoptotic death programme in human neuroblastoma cells. FEBS Lett., 320: 150-154, 1993.
40. Melino, G., Annicchiarico-Petruzzelli, M., Piredda, L., Candi, E., Gentile, V., Davies, P. J., and Piacentini, M. Tissue transglutaminase and apoptosis: sense and antisense transfection studies with human neuroblastoma cells. Mol. Cell. Biol., 14: 6584-6596, 1994.
41. Schreiber, E., Muller, M. M., and Schaffner, W. Rapid detection of octamer-binding proteins with "mini-extracts," prepared from a small number of cells. Nucleic Acids Res., 17: 6419, 1989.
42. Lee, J-H., Jang, S-I., Markova, N. G., and Steinert, P. M. The proximal promoter of the transglutaminase 3 gene. J. Biol. Chem., 271: 4561-4568, 1996.
43. Roda, A., Girotti, S., Motolese, G., Ghini, S., Ferri, E., Ursini, F., and Maiorino, M. In: A. A. Szalay, L. J. Kricka, and P. Stanley (eds.), Proceedings of the 7th International Symposium on Bioluminescence and Chemiluminescence, pp. 43-46. Chinchester, UK: John Wiley & Sons, 1993.
44. Sambrook, J., Fritsch, E. F., and Maniatis, T. Molecular Cloning. A Laboratory Manual, 2nd Ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 1989.
45. Wilm, M., and Mann, M. Analytical properties of the nano-electrospray ion source. Anal. Chem., 66: 1-8, 1996.
46. Martin, S. J., Takayama, S., McGahon, A. J., Miyashita, T., Corbeil, J., Kolesnick, R. N., Reed, J. C., and Green, D. R. Inhibition of ceramide-induced apoptosis by Bcl-2. Cell Death Differ., 2: 253-257, 1995.
47. Abate, C., Patel, L., Rauscher, F. J., and Curran, T. Redox regulation of fos and Jun DNA-binding activity in vitro. Science (Washington DC). 249: 1157-1161, 1990.
48. Nikitovic, D., Holmgren, A., and Spyrou, G. Inhibition of AP-1 DNA binding by nitric oxide involving conserved cysteine residues in Jun and Fos. Biochem. Biophys. Res. Commun., 242: 109-112, 1998.
49. Conant, K., Ahmed, U., Schwartz, J. P., and Major, E. O. IFN-γ inhibits AP-1 binding activity in human brain-derived cells through a nitric oxide dependent mechanism. J. Neuroimmunol., 88: 39-44, 1998.
50. Klatt, P., Molina, E. P., and Lamas, S. Nitric oxide inhibits c-Jun DNA binding by specifically targeted S-glutathionylation. J. Biol. Chem., 274: 15857-15864, 1999.