Nitric oxide induces tyrosine nitration and release of cytochrome c preceding an increase of mitochondrial transmembrane potential in macrophages

FASEB Journal

Volumn 13, Issue 15, 1999, Pages 2311-2317

  Hortelano, Sonsoles ^a   Alvarez, Alberto M ^b   Boscá, Lisardo ^a,b  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Apoptosis; Mitochondria; Nitric oxide synthase; NO

Indexed keywords

3 NITROTYROSINE; CASPASE; CYTOCHROME C; NITRIC OXIDE; PEROXYNITRITE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CHEMICAL MODIFICATION; CONTROLLED STUDY; MACROPHAGE; MEMBRANE PERMEABILITY; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MOUSE; NITRATION; NONHUMAN; PRIORITY JOURNAL;

EID: 0032808057     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fasebj.13.15.2311     Document Type: Article

References (51)

1. Thompson, C. B. (1995) Apoptosis in the pathogenesis and treatment of disease. Science 267, 1456-1462
2. Nagata, S. (1997) Apoptosis by death factor. Cell 88, 355-365
3. Green, D. R. (1998) Apoptotic pathways: the roads to ruin. Cell 94, 695-698
4. Kroemer, G., Petit, P., Zamzami, N., Vayssiere, J. L., and Mignotte, B. (1995). The biochemistry of programmed cell death. FASEB J. 9, 1277-1287
5. MacMicking, J., Xie, Q. W., and Nathan, C. (1997) Nitric oxide and macrophage function. Annu. Rev. Immunol. 15, 323-50, 323-350
6. Nathan, C. (1995) Natural resistance and nitric oxide. Cell 82, 873-876
7. Dugas, B., Debre, P., and Moncada, S. (1995) Nitric oxide, a vital poison inside the immune and inflammatory network. Res. Immunol. 146, 664-670
8. Stamler, J. S. (1995) S-nitrosothiols and the bioregulatory actions of nitrogen oxides through reactions with thiol groups. Curr. Top. Microbiol. Immunol. 196, 19-36
9. Girard, P., and Potier, P. (1993) NO, thiols and disulfides. FEBS Lett. 320, 7-8
10. Simon, D. I., Mullins, M. E., Jia, L., Gaston, B., Singel, D. J., and Stamler, J. S. (1996) Polynitrosylated proteins: characterization, bioactivity, and functional consequences. Prof. Natl. Acad. Sci. USA 93, 4736-4741
11. Terenzi, F., Diaz-Guerra, M. J., Casado, M., Hortelano, S., Leoni, S., and Bosca, L. (1995) Bacterial lipopeptides induce nitric oxide synthase and promote apoptosis through nitric oxide-independent pathways in rat macrophages. J. Biol. Chem. 270, 6017-6021
12. Hashimoto, S., Ochs, R. L., Rosen, F., Quach, J., McCabe, G., Solan, J., Seegmiller, J. E., Terkeltaub, R., and Lotz, M. (1998) Chondrocyte-derived apoptotic bodies and calcification of articular cartilage. Proc. Natl. Acad. Sci. USA 95, 3094-3099
13. Guh, J. H., Hwang, T. L., Ko, F. N., Chueh, S. C., Lai, M. K., and Teng, C. M. (1998) Antiproliferative effect in human prostatic smooth muscle cells by nitric oxide donor. Mol. Pharmacol. 53, 467-474
14. Albina, J. E., and Reichner, J. S. (1998) Role of nitric oxide in mediation of macrophage cytotoxicity and apoptosis. Cancer Metastasis Rev. 17, 39-53
15. Velasco, M., Diaz-Guerra, M. J., Diaz-Achirica, P., Andreu, D., Rivas, L., and Bosca, L. (1997) Macrophage triggering with cecropin A and melittin-derived peptides induces type II nitric oxide synthase expression. J. Immunol. 158, 4437-4443
16. Anderson, G. P. (1996) Resolution of chronic inflammation by therapeutic induction of apoptosis. Trends Pharmacol. Sci. 17, 438-442
17. Williams, G. T. (1994) Programmed cell death: a fundamental protective response to pathogens. Trends Microbiol. 2, 463-464
18. Molloy, A., Laochumroonvorapong, P., and Kaplan, G. (1994) Apoptosis, but not necrosis, of infected monocytes is coupled with killing of intracellular bacillus Calmette-Guerin. J. Exp. Med. 180, 1499-1509
19. Savill, J. (1997). Apoptosis in resolution of inflammation. J. Leukoc. Biol. 61, 375-380
20. Sarti, P., Lendaro, E., Ippoliti, R., Bellelli, A., Benedetti, P. A., and Brunori, M. (1999) Modulation of mitochondrial respiration by nitric oxide: investigation by single cell fluorescence microscopy. FASEB J. 13, 191-197
21. Clementi, K., Brown, G. C., Feelisch, M., and Moncada, S. (1998) Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylalion of mitochondrial complex I and protective action of glutathione. Proc. Natl. Acad. Sci. USA 95, 7631-7636
22. Kroemer, G., Dallaporta, B., and Resche-Rigon, M. (1998) The mitochondrial death/life regulator in apoptosis and necrosis. Annu. Rev. Physiol. 60, 619-642
23. Hortelano, S., Dallaporta, B., Zamzami, N., Hirsch, T., Susin, S. A., Marzo, I., Bosca, L., and Kroemer, G. (1997) Nitric oxide induces apoptosis via triggering mitochondrial permeability transition. FEBS Lett. 410, 373-377
24. Packer, M. A., and Murphy, M. P. (1994) Peroxynitrite causes calcium efflux from mitochondria which is prevented by cyclosporin A. FEBS Lett. 345, 237-240
25. Susin, S. A., Zamzami, N., Castedo, M., Hirsch, T., Marchetti, P., Macho, A., Daugas, E., Geuskens, M., and Kroemer, G. (1996) Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J. Exp. Med. 184, 1331-1341
26. Marzo, I., Brenner, C., Zamzami, N., Jurgensmeier, J. M., Susin, S. A., Vieira, H. L., Prevost, M. C., Xie, Z., Matsuyama, S., Reed, J. G., and Kroemer, G. (1998) Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281, 2027-2031
27. Kroemer, G., Zamzami, N., and Susin, S. A. (1997) Mitochondrial control of apoptosis. Immunol. Today 18, 44-51
28. Bossy-Wetzel, E., Newmeyer, D. D., and Green, D. R. (1998) Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J. 17, 37-49
29. Liu, X., Kim, C. N., Yang, J., Jemmerson, R., and Wang, X. (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86, 147-157
30. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S. M., Ahmad, M., Alnemri, E. S., and Wang, X. (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91, 479-489
31. Yoshida, H., Kong, Y. Y., Yoshida, R., Elia, A. J., Hakem, A., Hakem, R., Penninger, J. M., and Mak, T. W. (1998) Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell 94, 739-750
32. Kroemer, G., Boscá, L., Zamzami, N., Hortelano, S., and Martinez-A., C. (1997) Detection of apoptosis and apoptosis associated alterations. In The immunological Methods Manual(Lefkovitz, R., ed) Vol. 14.2, pp. 1111-1125
33. Hortelano, S., López-Collazo, A., and Boscá, L. (1999) Protective effect of cyclosporin A and FK506 from nitric oxide-dependent apoptosis in activated macrophages. Br. J. Pharmacol. 126, 1139-1146
34. Genaro, A. M., Hortelano, S., Alvarez, A., Martinez, C., and Bosca, L. (1995) Splenic B lymphocyte programmed cell death is prevented by nitric oxide release through mechanisms involving sustained Bcl-2 levels. J. Clin. Invest. 95, 1884-1890
35. Moro, M. A., Darley-Usmar, V. M., Goodwill, D. A., Read, N. G., Zamora-Pino, R., Feelisch, M., Radomski, M. W., and Moncada, S. (1994) Paradoxical fate and biological action of peroxynitrite on human platelets. Proc. Natl. Acad. Sci. USA 91, 6702-6706
36. Lizasoain, I., Moro, M. A., Knowles, R. G., Darley-Usmar, V., and Moncada, S. (1996) Nitric oxide and peroxynitrite exert distinct effects on mitochondrial respiration which are differentially blocked by glutathione or glucose. Biochem. J. 314, 877-880
37. Yang, J., Liu, X., Bhalla, K., Kim, C. N., Ibrado, A. M., Cai, J., Peng, T. I., Jones, D. P., and Wang, X. (1997) Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275, 1129-1132
38. Macho, A., Decaudin, D., Castedo, M., Hirsch, T., Susin, S. A., Zamzami, N., and Kroemer, G. (1996) Chloromethyl-X-. Rosamine is an aldehyde-fixable potential-sensitive fluorochrome for the detection of early apoptosis. Cytometry 25, 333-340
39. Marzo, I., Brenner, C., Zamzami, N., Susin, S. A., Beutner, G., Brdiczka, D., Remy, R., Xie, Z. H., Reed, J. C., and Kroemer, G. (1998) The permeability transition pore complex: a target for apoptosis regulation by caspases and bcl-2-related proteins. J. Exp. Med. 187, 1261-1271
40. Jurgensmeier, J. M., Xie, Z., Deveraux, Q., Ellerby, L., Bredesen, D., and Reed, J. C. (1998) Bax directly induces release of cytochrome c from isolated mitochondria. Proc. Natl. Acad. Sci. USA 95, 4997-5002
41. Kluck, R. M., Bossy-Wetzel, E., Green, D. R., and Newmeyer, D. D. (1997) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275, 1132-1136
42. Green, D. R., and Reed, J. C. (1998) Mitochondria and apoptosis. Sience 281, 1309-1312
43. Ascenzi, P., Coletta, M., Santucci, R., Polizio, F., and Desideri, A. (1994) Nitric oxide binding to ferrous native horse heart cytochrome c and to its carboxymethylated derivative: a spectroscopic and thermodynamic study. J. Inorg. Biochem. 53, 273-280
44. Sharpe, M. A., and Cooper, C. E. (1998) Interaction of peroxynitrite with mitochondrial cytochrome oxidase. Catalytic production of nitric oxide and irreversible inhibition of enzyme activity. J. Biol. Chem. 273, 30961-30972
45. Brown, G. C. (1997) Nitric oxide inhibition of cytochrome oxidase and mitochondrial respiration: implications for inflammatory, neurodegenerative and ischaemic pathologies. Mol. Cell Biochem. 174, 189-192
46. Brookes, P. S., Bolanos, J. P., and Heales, S. J. (1999) The assumption that nitric oxide inhibits mitochondrial ATP synthesis is correct. FEBS Lett. 446, 261-263
47. Davey, G. P., and Clark, J. B. (1996) Threshold effects and control of oxidative phosphorylation in nonsynaptic rat brain mitochondria. J. Neurochem. 66, 1617-1624
48. Virag, L., Scott, G. S., Cuzzocrea, S., Manner, D., Salzman, A. L., and Szabo, C. (1998) Peroxynitrite-induccd thymocyte apoptosis: the role of caspases and poly (ADP-ribose) synthetase (PARS) activation, Immunology 94, 345-355
49. Limbach, K. J., and Wu, R. (1985) Characterization of a mouse somatic cytochrome c gene and three cytochrome c pseudogenes. Nucleic Acids Res. 13, 617-630
50. Finucane, D. M., Bossy-Wetzel, E., Waterhouse, N. J., Cotter, T. G., and Green, D. R. (1999) Bax-induced caspase activation and apoptosis via cytochrome c release from mitochondria is inhibitable by Bcl-xL. J. Biol Chem. 274, 2225-2233
51. Mallozzi, C., Di Stasi, A. M., and Minetti, M. (1997) Peroxynitrite modulates tyrosine-dependent signal transduction pathway of human erythrocyte band 3. FASEB J. 11, 1281-1290