Inhibition of mitochondrial ATP generation by nitric oxide switches apoptosis to necrosis

Experimental Cell Research

Volumn 249, Issue 2, 1999, Pages 396-403

  Leist, Marcel ^a   Single, Barbara ^a   Naumann, Heike ^a   Fava, Eugenio ^a   Simon, Bernadett ^a   Kühnle, Simone ^a   Nicotera, Pierluigi ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

Apoptosis; Caspase; Cytochrome c; Mitochondria; Nitric oxide

Indexed keywords

ADENOSINE TRIPHOSPHATE; GLUTATHIONE; NITRIC OXIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROTENONE;

APOPTOSIS; ARTICLE; CELL CULTURE; CELL DEATH; CELL METABOLISM; CONTROLLED STUDY; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; MITOCHONDRION; PRIORITY JOURNAL;

EID: 0033563776     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1006/excr.1999.4514     Document Type: Article

References (45)

1. Moncada S., Palmer R. M. J., Higgs E. A. Nitric oxide: Physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 43:1991;109-142.
2. Vallance P., Moncada S. Nitric oxide - From mediator to medicines. J. R. Coll. Physicians London. 28:1994;209-219.
3. Nicotera P., Bonfoco E., Brüne B. Mechanisms for nitric oxide-induced cell death: Involvement of apoptosis. Adv. Neuroimmunol. 5:1995;411-420.
4. Zhang J., Snyder S. H. Nitric oxide in the nervous system. Annu. Rev. Pharmacol. Toxicol. 35:1995;213-233.
5. Albina J. E., Cui S., Mateo R. B., Reichner J. S. Nitric oxide-mediated apoptosis in murine peritoneal macrophages. J. Immunol. 150:1993;5080-5085.
6. Messmer U. K., Ankarcrona M., Nicotera P., Brüne B. p53 expression in nitric-oxide-induced apoptosis. FEBS Lett. 355:1994;23-26.
7. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P., Lipton S. A. Apoptosis and necrosis: Two distinct events induced respectively by mild and intense insults with NMDA or nitric oxide/superoxide in cortical cell cultures. Proc. Natl. Acad. Sci. USA. 92:1995;72162-72166.
8. Mohr S., Zech B., Lapetina E. G., Brüne B. Inhibition of caspase-3 by S-nitrosation and oxidation caused by nitric oxide. Biochem. Biophys. Res. Commun. 238:1997;387-391.
9. Brockhaus F., Brüne B. U937 apoptotic cell death by nitric oxide: bcl-2 downregulation and caspase activation. Exp. Cell Res. 238:1998;33-41.
10. Cohen G. M. Caspases: The executioners of apoptosis. Biochem. J. 326:1997;1-16.
11. Harbrecht B. G., Stadler J., Demetris A. J., Simmons R. L., Billiar T. R. Nitric oxide and prostaglandins interact to prevent hapatic damage during murine endotoxemia. Am. J. Physiol. 266:1994;G1004-G1010.
12. Bohlinger I., Leist M., Barsig J., Uhlig S., Tiegs G., Wendel A. Interleukin-1 and nitric oxide protect against tumor necrosis-factor alpha-induced liver injury through distinct pathways. Hepatology. 22:1995;1829-1837.
13. Mannick J. B., Asano K., Izumi K., Kleff E., Stamler J. S. Nitric oxide produced by human B lymphocytes inhibits apoptosis and Epstein-Barr virus reactivation. Cell. 79:1994;1137-1146.
14. Mannick J. B., Miao X. Q., Stamler J. S. Nitric oxide inhibits Fas-induced apoptosis. J. Biol. Chem. 272:1997;24125-24128.
15. Melino G., Bernassola F., Knight R. A., Corasaniti M. T., Nistico G., Finazzi-Agro A. S-nitrosylation regulates apoptosis. Nature. 388:1997;432-433.
16. Ren Y., Savill J. Apoptosis: The importance of being eaten. Cell Death Differ. 5:1998;563-568.
17. Dimmeler S., Haendeler J., Nehls M., Zeiher A. M. 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. 185:1997;601-607.
18. Kim Y.-M., Talanian R. V., Billiar T. R. Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms. J. Biol. Chem. 272:1997;31138-31148.
19. Hebesteit H., Dibbert B., Balatti I., Braun D., Schapowal A., Blaser K., Simon H-U. Disruption of fas receptor signaling by nitric oxide in eosinophils. J. Exp. Med. 187:1998;415-425.
20. Green D., Kroemer G. The central executioners of apoptosis: Caspases or mitochondria. Trends Cell Biol. 8:1998;267-271.
21. Leist M., Single B., Castoldi A. F., Kühnle S., Nicotera P. Intracellular ATP concentration: A switch deciding between apoptosis and necrosis. J. Exp. Med. 185:1997;1481-1486.
22. Hirsch T., Marchetti P., Susin S. A., Dallaporta B., Zamzami N., Marzo I., Geuskens M., Kroemer G. The apoptosis-necrosis paradox. Apoptogenic proteases activated after mitochondrial permeability transition determine the mode of cell death. Oncogene. 15:1997;1573-1581.
23. Adjei P. N., Kaufmann S. H., Leung W.-Y., Mao F., Gores G. J. Selective induction of apoptosis in Hep 3B cells by toposiomerase I inhibitors: Evidence for a protease-dependent pathway that does not activate cysteine protease P32. J. Clin. Invest. 98:1996;2588-2596.
24. McCarthy N. J., Whyte M. K. B., Gilbert C. S., Evan G. I. Inhibition of Ced-3/ICE-related proteases does not prevent cell death induced by oncogenes, DNA damage, or the bcl-2 homologue bak. J. Cell Biol. 136:1997;215-227.
25. Eguchi Y., Shimizu S., Tsujimoto Y. Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res. 57:1997;1835-1840.
26. Nicotera P., Leist M. Energy supply and the shape of death in neurons and lymphoid cells. Cell Death Differ. 4:1997;435-442.
27. Stadler J., Curran R. D., Ochoa J. B., Harbrecht B. G., Hoffman R. A., Simmons R. L., Billiar T. R. Effect of endogenous nitric oxide on mitochondrial respiration of rat hepatocytes in vitro and in vivo. Arch. Surg. 126:1991;186-191.
28. Schweizer M., Richter C. Nitric oxide potently and reversibly deenergizes mitochondria at low oxygen tension. Biochem. Biophys. Res. Commun. 204:1994;169-175.
29. Clementi E., Brown G. C., Feelisch M., Moncada S. Persistent inhibition of cell respiration by nitric oxide: Crucial role of S-nitrosylation of mitochondria complex I and protective action of glutathione. Proc. Natl. Acad. Sci. USA. 95:1998;7631-7636.
30. Koopman G., Reutelingsperger C. P. M., Kuijten G. A. M., Keehnen R. M. J., Pals S. T., van Oers M. H. J. Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood. 84:1994;1415-1420.
31. Leist M., Volbracht C., Fava E., Nicotera P. Caspase-mediated apoptosis in neuronal excitotoxicity triggered by nitric oxide. Mol. Pharmacol. 54:1998;789-801.
32. Single B., Leist M., Nicotera P. Simultaneous release of adenylate kinase and cytochrome c in cell death. Cell Death Differ. 5:1998;1001-1003.
33. Bergmeyer H.-U. Methods of Enzymatic Analysis. 1983;Verlag Chemie, Weinheim. p. 545-549.
34. Tietze F. Enzymatic method for quantitative determination of nanogram amounts of total and oxidised glutathione: Application to mammalian blood and other tissues. Anal. Biochem. 27:1969;502-522.
35. Ichas F., Jouaville L. S., Mazat J. P. Mitochondria are excitable organelles capable of generating and conveying electrical and calcium signals. Cell. 89:1997;1145-1153.
36. Leist M., Single B., Naumann H., Fava E., Simon B., Kühnle S., Nicotera P. Nitric oxide inhibits execution of apoptosis at two distinct ATP-dependent steps upstream and downstream of mitochondrial cytochrome c release. Biochem. Biophys. Res. Commun. 1999.
37. Zamzami N., Susin S. A., Marchetti P., Hirsch T., Gómez-Monterrey I., Castedo M., Kroemer G. Mitochondrial control of nuclear apoptosis. J. Exp. Med. 183:1996;1533-1544.
38. Ghibelli L., Fanelli C., Rotilio G., Lafavia E., Coppola S., Colussi C., Civitareale P., Cirioloo M. R. Rescue of cells from apoptosis by inhibition of active GSH extrusion. FASEB J. 12:1998;479-486.
39. Schraufstatter I. U., Hyslop P. A., Hinshaw D. B., Spragg R. G., Sklar L. A., Cochrane C. G. Hydrogen peroxide-induced injury of cells and its prevention by inhibitors of poly(ADP-ribose) polymerase. Proc. Natl. Acad. Sci. USA. 83:1986;4908-4912.
40. Medema J. P., Scaffidi C., Kischkel F. C., Shevchenko A., Mann M., Krammer P. H., Peter M. E. FLICE is activated by association with the CD95 death-inducing signaling complex (DISC). EMBO J. 16:1997;2794-2804.
41. Scaffidi C., Fulda S., Srinivasan A., Friesen C., Li F., Tomaselli K. J., Debatin K. M., Krammer P. H., Peter M. E. Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 17:1998;1675-1687.
42. Marzo I., Susin S. A., Petit P. X., Ravagnan L., Brenner C., Larochette N., Zamzami N., Kroemer G. Caspases disrupt mitochondrial membrane barrier function. FEBS Lett. 427:1998;198-202.
43. Lipton S. A., Choi Y.-B., Pan Z.-H., Lei S. Z., Chen H.-S. V., Sucher N. J., Loscalzo J., Singel D. J., Stamler J. S. A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature. 364:1993;626-632.
44. Tenneti L., D'Emilia D. M., Lipton S. A. Suppression of neuronal apoptosis by S-nitrosylation of caspases. Neurosci. Lett. 236:1997;139-142.
45. Estévez A. G., Spear N., Thompson J. A., Cornwell T. L., Radi R., Barbeito L., Beckman J. S. Nitric oxide-dependent production of cGMP supports the survival of rat embryonic motor neurons cultured with brain-derived neurotrophic factor. J. Neurosci. 18:1998;3708-3714.