Nitric oxide donors inhibit formation of the Apaf-1/caspase-9 apoptosome and activation of caspases

Biochemical Journal

Volumn 371, Issue 3, 2003, Pages 1055-1064

  Zech, Birgit ^a   Köhl, Roman ^a   Von Knethen, Andreas ^a   Brüne, Bernhard ^a  

^a Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

Author keywords

Caspase processing; Cytochrome c; Fas; Nitric oxide; Nitrosation

Indexed keywords

CELLS; ENZYME INHIBITION; METABOLITES; NITROGEN COMPOUNDS;

MITOCHONDRIA;

ENZYMES;

APOPTOTIC PROTEASE ACTIVATING FACTOR 1; CASPASE; CASPASE 3; CASPASE 8; CASPASE 9; CYTOCHROME C; DNA FRAGMENT; ETOPOSIDE; FAS ANTIGEN; NITRIC OXIDE DONOR;

APOPTOSIS; ARTICLE; DNA DETERMINATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; GEL FILTRATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE; NITROSATION; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN INTERACTION; WESTERN BLOTTING;

APOPTOSIS; APOPTOTIC PROTEASE-ACTIVATING FACTOR 1; CASPASES; CELL-FREE SYSTEM; ENZYME ACTIVATION; ETOPOSIDE; HUMANS; JURKAT CELLS; MITOCHONDRIA; NITRIC OXIDE DONORS; PROTEINS; S-NITROSO-N-ACETYLPENICILLAMINE;

EID: 0037907637     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20021720     Document Type: Article

References (46)

1. Fadeel, B., Orrenius, S. and Zhivotovsky, B. (1999) Apoptosis in human disease: a new skin for the old ceremony? Biochem. Biophys. Res. Commun. 266, 699-717
2. Green, D. R. (1998) Apoptotic pathways: the roads to ruin. Cell 94, 695-698
3. Ashkenazi, A. and Dixit, V. M. (1998) Death receptors: signaling and modulation. Science 281, 1305-1308
4. Evan, G. and Littlewood, T. (1998) A matter of life and cell death. Science 281, 1317-1322
5. Scaffidi, C., Fulda, S., Srinivasan, A., Friesen, C., Li, F., Tomaselli, K. J., Debatin, K. M., Krammer, P. H. and Peter, M. E. (1998) Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 17, 1675-1687
6. Scaffidi, C., Schmitz, I., Zha, J., Korsmeyer, S. J., Krammer, P. H. and Peter, M. E. (1999) Differential modulation of apoptosis sensitivity in CD95 type I and type II cells. J. Biol. Chem. 274, 22532-22538
7. Johnstone, R. W., Ruefli, A. A. and Lowe, S. W. (2002) Apoptosis: a link between cancer genetics and chemotherapy. Cell 108, 153-164
8. Debatin, K.-M., Poncet, D. and Kroemer, G. (2002) Chemotherapy: targeting the mitochondrial cell death pathway. Oncogene 21, 8786-8803
9. Cecconi, F. (1999) Apaf1 and the apoptotic machinery. Cell Death Differ. 6, 1087-1098
10. Salvesen, G. S. and Dixit, V. M. (1999) Caspase activation: the induced-proximity model. Proc. Natl. Acad. Sci. U.S.A. 96, 10964-10967
11. Zou, H., Li, Y., Liu, X. and Wang, X. (1999) An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J. Biol. Chem. 274, 11549-11556
12. Ekert, P. G., Silke, J. and Vaux, D. L. (1999) Caspase inhibitors. Cell Death Differ. 6, 1081-1086
13. Tschopp, J., Irmler, M. and Thome, M. (1998) Inhibition of fas death signals by FLIPs. Curr. Opin. Immunol. 10, 552-558
14. Brüne, B., von Knethen, A. and Sandau, K. B. (1999) Nitric oxide (NO): an effector of apoptosis. Cell Death Differ. 6, 969-975
15. Liu, L. and Stamler, J. S. (1999) NO: an inhibitor of cell death. Cell Death Differ. 6, 937-942
16. Stamler, J. S. (1994) Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell 78, 931-936
17. Li, J., Billiar, T. R., Talanian, R. V. and Kim, Y. M. (1997) Nitric oxide reversibly inhibits seven members of the caspase family via S-nitrosylation. Biochem. Biophys. Res. Commun. 240, 419-424
18. Zech, B., Wilm, M., van Eldik, R. and Brüne, B. (1999) Mass spectrometric analysis of nitric oxide-modified caspase-3. J. Biol. Chem. 274, 20931-20936
19. Polte, T., Oberle, S. and Schroder, H. (1997) The nitric oxide donor SIN-1 protects endothelial cells from tumor necrosis factor-α-mediated cytotoxicity: possible role for cyclic GMP and heme oxygenase. J. Mol. Cell. Cardiol. 29, 3305-3310
20. 2+ concentration. Arch. Biochem. Biophys. 269, 365-370
21. Burton, K. (1956) A study of the conditions and mechanism of the diphenylamine reaction for the estimation of deoxyribonucleic acid. Biochem. J. 62, 315-323
22. Leist, M., Volbracht, C., Fava, E. and Nicotera, P. (1998) 1-Methyl-4-phenylpyridinium induces autocrine excitotoxicity, protease activation, and neuronal apoptosis. Mol. Pharmacol. 54, 789-801
23. Messmer, U. K., Ankarcrona, M., Nicotera, P. and Brüne, B. (1994) p53 expression in nitric oxide-induced apoptosis. FEBS Lett. 355, 23-26
24. Shiozaki, E. N., Chai, J. and Shi, Y. (2002) Oligomerization and activation of caspase-9, induced by Apaf-1 CARO. Proc. Natl. Acad. Sci. U.S.A. 99, 4197-4202
25. Cain, K., Bratton, S. B., Langlais, C., Walker, G., Brown, D. G., Sun, X. M. and Cohen, G. M. (2000) Apaf-1 oligomerizes into biologically active approximately 700-kDa and inactive approximately 1.4-MDa apoptosome complexes. J. Biol. Chem. 275, 6067-6070
26. Bratton, S. B., Walker, G., Srinivasula, S. M., Sun, X. M., Butterworth, M., Alnemri, E. S. and Cohen, G. M. (2001) Recruitment, activation and retention of caspases-9 and -3 by Apaf-1 apoptosome and associated XIAP complexes. EMBO J. 20, 998-1009
27. Qin, H., Srinivasula, S. M., Wu, G., Fernandes-Alnemri, T., Alnemri, E. S. and Shi, Y. (1999) Structural basis of procaspase-9 recruitment by the apoptotic protease-activating factor 1. Nature (London) 399, 549-557
28. Bratton, S. B., Walker, G., Roberts, D. L., Cain, K. and Cohen, G. M. (2001) Caspase-3 cleaves Apaf-1 into an 30 kDa fragment that associates with an inappropriately oligomerized and biologically inactive 1.4 MDa apoptosome complex. Cell Death Differ. 8, 425-433
29. Lily, Y. L., Xu, L. and Wang, X. (2001) Endonuclease G is an apoptotic DNase when released from mitochondria. Nature (London) 412, 95-99
30. Dimmeler, S., Haendeler, J., Sause, A. and Zeiher, A. M. (1998) Nitric oxide inhibits APO-1/Fas-mediated cell death. Cell Growth Differ. 9, 415-422
31. Kim, Y. M., Talanian, R. V. and Billiar, T. R. (1997) Nitric oxide inhibits apoptosis by preventing increases in caspase-3 like activity via two distinct mechanisms. J. Biol. Chem. 272, 31138-31148
32. Melino, G., Bernassola, F., Knight, R. A., Corasaniti, M. T., Nistico, G. and Finazzi-Agro, A. (1997) S-nitrosylation regulates apoptosis. Nature (London) 388, 432-433
33. Li, J., Bombeck, C. A., Yang, S., Kim, Y. M. and Billiar, T. R. (1999) Nitric oxide suppresses apoptosis via interrupting caspase activation and mitochondrial dysfunction in cultured hepatocytes. J. Biol. Chem. 274, 17328-17333
34. Dimmeler, S., Haendeler, J. Nehls, M. and Zeiher, A. M. (1997) Suppression of apoptosis by nitric oxide via inhibition of interleukin-1β-converting enzyme (ICE)-like and cysteine protease protein (CPP)-32-like proteases. J. Exp. Med. 185, 601-607
35. Mannick, J. B., Miao, X. Q. and Stamler, J. S. (1997) Nitric oxide inhibits Fas-induced apoptosis. J. Biol. Chem. 272, 24128-24128
36. Rodriguez, J. and Lazebnik, Y. (1999) Caspase-9 and APAF-1 form an active holoenzyme. Genes Dev. 13, 3179-3184
37. Leist, M., Single, B., Castoldi, A. F., Kuhnle, S. and Nicotera, P. (1997) Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J. Exp. Med. 185, 1481-1486
38. Mannick, J. B., Hausladen, A., Liu, L., Hess, L., Zeng, M., Miao, Q. X., Kane, L. S., Gow, A. J. and Stamler, J. S. (1999) Fas-induced caspase denitrosylation. Science 284, 651-654
39. Török, N. J., Higuchi, H., Bronk, S. and Gores, G. J. (2002) Nitric oxide inhibits apoptosis downstream of cytochrome c release by nitrosylating caspase-9. Cancer Res. 62, 1648-1653
40. Beere, H. M., Wolf, B. B., Cain, K., Mosser, D. D., Mahboubi, A., Kuwana, T., Tailor, P., Morimoto, R. I., Cohen, G. M. and Green, D. R. (2000) Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the apaf-1 apoptosome. Nat. Cell. Biol. 2, 469-475
41. Saleh, A., Srinivasula, S. M., Balkir, L., Robbins, P. D. and Alnemri, E. S. (2000) Negative regulation of the apaf-1 apoptosome by hsp70. Nat. Cell. Biol. 2, 476-483
42. Nicholson, D. W. (1999) Caspase structure, proteolytic substrates, and function during apoptotic cell death. Cell Death Differ. 6, 1028-1042
43. Benedict, M. A., Hu, Y., Inohara, N. and Nunez, G. (2000) Expression and functional analysis of apaf-1 isoforms. Extra Wd-40 repeat is required for cytochrome c binding and regulated activation of procaspase-9. J. Biol. Chem. 275, 8461-8468
44. Bratton, S. B., MacFarlane, M., Cain, K. and Cohen, G. M. (2000) Protein complexes activate distinct caspase cascades in death receptor and stress-induced apoptosis. Exp. Cell Res. 256, 27-33
45. Kim, Y. M., Bombeck, C. A. and Billiar, T. R. (1999) Nitric oxide as a bifunctional regulator of apoptosis. Circ. Res. 84, 253-256
46. Kim, Y. M., Chung, H. T., Simmons, R. L. and Billiar, T. R. (2000) Cellular non-haem iron content is a determinant of nitric oxide-mediated apoptosis, necrosis, and caspase inhibition. J. Biol. Chem. 275, 10954-10961