Suppression of the pro-apoptotic function of cytochrome c by singlet oxygen via a haem redox state-independent mechanism

Biochemical Journal

Volumn 392, Issue 2, 2005, Pages 399-406

  Suto, Daisuke ^a   Sato, Kazuaki ^b   Ohba, Yoshihiro ^b   Yoshimura, Tetsuhiko ^c   Fujii, Junichi ^a  

^a YAMAGATA UNIVERSITY   (Japan)

^b YAMAGATA UNIVERSITY   (Japan)

^c Yamagata Promotional Organization for Industrial Technology   (Japan)

Author keywords

Caspase; Cytochrome c; Haem; Redox state; Singlet oxygen

Indexed keywords

AMINO ACIDS; CELLS; CONFORMATIONS; OXYGEN; PROTEINS; REDOX REACTIONS;

CASPASE; CYTOCHROME C; HAEM; REDOX STATE; SINGLET OXYGEN;

PIGMENTS;

AMINO ACID; APOPTOSOME; APOPTOTIC PROTEASE ACTIVATING FACTOR 1; CARBONYL DERIVATIVE; CASPASE; CYSTEINE; CYTOCHROME C; ENDOPEROXIDE; GLUTATHIONE; HEME; SINGLET OXYGEN;

AMINO ACID SYNTHESIS; APOPTOSIS; ARTICLE; CELL FREE SYSTEM; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME CONFORMATION; ENZYME INHIBITION; HEME SYNTHESIS; HUMAN; HUMAN CELL; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN MODIFICATION;

ANIMALS; APOPTOSIS; CASPASES; CELL LINE, TUMOR; CYSTEINE; CYTOCHROMES C; ENZYME ACTIVATION; GLUTATHIONE; HEME; HORSES; HUMANS; OXIDATION-REDUCTION; SINGLET OXYGEN;

EID: 29144432723     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20050580     Document Type: Article

References (49)

1. Leist, M. and Jaattela, M. (2001) Four deaths and a funeral: from caspases to alternative mechanisms. Nat. Rev. Mol. Cell. Biol. 2, 589-598
2. Green, D. and Reed, J. C. (1998) Mitochondria and apoptosis. Science 281, 1309-1312
3. Hengartner, M. O. (2000) The biochemistry of apoptosis. Nature (London) 407, 770-776
4. 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
5. Kluck, R. M., Martin, S. J., Hoffman, B. M., Zhou, J. S., Green, D. R. and Newmeyer, D. D. (1997) Cytochrome c activation of CPP32-like proteolysis plays a critical role in a Xenopus cell-free apoptosis system. EMBO J. 16, 4639-4649
6. Dickerson, R. E. and Timkovich, R. (1975) Cytochromes c. In The Enzymes. XI: Oxidation-Reduction (Boyer, P. D., ed.), pp. 397-547, Academic Press, New York, NY
7. +-dependent isocitrate dehydrogenase. J. Biol. Chem. 276, 16168-16176
8. Kane, D. J., Sarafian, T. A., Anton, R., Hahn, H., Gralla, E. B., Valentine, J. S., Ord, T. and Bredesen, D. E. (1993) Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species. Science 262, 1274-1277
9. Backway, K. L., McCulloch, E. A., Chow, S. and Medley, D. W. (1997) Relationships between the mitochondrial permeability transition and oxidative stress during ara-C toxicity. Cancer Res. 57, 2446-2451
10. Voehringer, D. W., McConkey, D. J., McDonnell, T. J., Brisbay, S. and Meyn, R. E. (1998) Bcl-2 expression causes redistribution of glutathione to the nucleus. Proc. Natl. Acad. Sci. U.S.A. 95, 2956-2960
11. Mirkovic, N., Voehringer, D. W., Story, M. D., McConkey, D. J., McDonnell, T. J. and Meyn, R. E. (1997) Resistance to radiation-induced apoptosis in Bcl-2-expressing cells is reversed by depleting cellular thiols. Oncogene 15, 1461-1470
12. Hampton, M. B., Zhivotovsky, B., Slater, A. F., Burgess, D. H. and Orrenius, S. (1998) Importance of the redox state of cytochrome c during caspase activation in cytosolic extracts. Biochem. J. 329, 95-99
13. Hancock, J. T., Desikan, R. and Neill, S. J. (2001) Does the redox status of cytochrome c act as a fail-safe mechanism in the regulation of programmed cell death? Free Radical Biol. Med. 31, 697-703
14. Halliwell, B. and Gutteridge, J. M. C. (1999) Free Radical Biology and Medicine, 3rd edn., Clarendon Press, Oxford
15. Davies, M. J. (2005) The oxidative environment and protein damage. Biochim. Biophys. Acta. 1703, 93-109
16. Godar, D. E. (2000) Singlet oxygen-triggered immediate preprogrammed apoptosis. Methods Enzymol. 319, 309-330
17. Berneburg, M., Grether-Beck, S., Kurten, V., Ruzicka, T., Briviba, K., Sies, H. and Krutmann, J. (1999) Singlet oxygen mediates the UVA-induced generation of the photoaging-associated mitochondrial common deletion. J. Biol. Chem. 274, 15345-15349
18. 2 as the principal oxidant in myeloperoxidase-mediated bacterial killing in neutropnil phagosome. Biochem. Biophys. Res. Commun. 262, 647-650
19. Pellieux, C., Dewilde, A., Pierlot, C. and Aubry, J. M. (2000) Bactericidal and virucidal activities of singlet oxygen generated by thermolysis of naphthalene endoperoxides Methods Enzymol. 319, 197-207
20. Ahmad, N. and Mukhtar, H. (2000) Mechanism of photodynamic therapy-induced cell death. Methods Enzymol. 319, 342-358
21. Morita, A., Werfel, T., Stege, H., Ahrens, C., Karmann, K., Grewe, M., Grether-Beck, S., Ruzicka, T., Kapp, A., Klotz, L. O. et al. (1997) Evidence that singlet oxygen-induced human T helper cell apoptosis is the basic mechanism of ultraviolet-A radiation phototherapy. J. Exp. Med. 186, 1763-176
22. Kochevar, I. E., Lynch, M. C., Zhuang, S. and Lambert, C. R. (2000) Singlet oxygen, but not oxidizing radicals, induces apoptosis in HL-60 cells. Photochem. Photobiol. 72, 548-553
23. Klotz, L. O., Briviba, K. and Sies, H. (1997) Singlet oxygen mediates the activation of JNK by UVA radiation in human skin fibroblasts. FEBS Lett. 408, 289-291
24. Klotz, L. O., Pellieux, C., Briviba, K., Pierlot, C., Aubry, J. M. and Sies, H. (1999) Mitogen-activated protein kinase (p38-, JNK-, ERK-) activation pattern induced by extracellular and intracellular singlet oxygen and UVA. Eur J. Biochem. 260, 917-922
25. Zhuang, S., Demirs, J. T. and Kochevar, I. E. (2000) p38 mitogen-activated protein kinase mediates bid cleavage, mitochondrial dysfunction and caspase-3 activation during apoptosis induced by singlet oxygen but not by hydrogen peroxide. J. Biol. Chem. 275, 25939-25948
26. Chan, W. H., Yu J. S. and Yang, S. D. (2000) Apoptotic signalling cascade in photosensitized human epidermal carcinoma A431 cells: involvement of singlet oxygen, c-Jun N-terminal kinase, caspase-3 and p21-activated kinase 2. Biochem. J. 351, 221-232
27. Otsu, K., Sato, K., Ikeda, Y., Imai, H., Nakagawa, Y. Ohba, Y. and Fujii, J. (2005) Abortive apoptotic pathway by singlet oxygen due to the suppression of caspase activation. Biochem. J. 389, 197-206
28. Aubry, J. M., Cazin, B. and Duprat, F. (1989) Chemical sources of singlet oxygen. 3. Peroxidation of water-soluble singlet oxygen carriers with the hydrogen peroxide-molybdate system. J. Org. Chem. 54, 726-728
29. Liu, W., Ogata, T., Sato, K., Ohba, Y., Sakurai, K. and Igarashi, T. (2001) Syntheses of water-soluble endoperoxides as a singlet oxygen source. ITE Letters on Batteries, New Technol. Med. 2, 98-101
30. Stennicke, H. R. and Salvesen, G. S. (1997) Biochemical characteristics of caspases-3, -6, -7 and -8. J. Biol. Chem. 272, 25719-25723
31. Pan, Z., Voehringer, D. W. and Meyn, R. E. (1999) Analysis of redox regulation of cytochrome c-induced apoptosis in a cell-free system. Cell Death Differ. 6, 683-688
32. Jocelyn, P. C. (1967) The standard redox potential of cysteine-cystine from the thiol-disulphide exchange reaction with glutathione and lipoic acid. Eur. J. Biochem. 2, 327-331
33. Cassina, A. M., Hodara, R, Souza, J. M., Thomson, L., Castro, L., Ischiropoulos, H., Freeman, B. A. and Radi, R. (2000) Cytochrome c nitration by peroxynitrite. J. Biol. Chem. 275, 21409-21415
34. van den Dobbelsteen, D. J., Nobel, C. S., Schlegel, J., Cotgreave, I. A., Orrenius, S. and Slater, A. F. (1996) Rapid and specific efflux of reduced glutathione during apoptosis induced by anti-Fas/APO-1 antibody. J. Biol. Chem. 271, 15420-15427
35. Estevam, M, L., Nascimento, O. R., Baptista, M. S., Di Mascio, P., Prado, F. M., Faljoni-Alario, A., Zucchi Mdo, R. and Nantes, I. L. (2004) Changes in the spin state and reactivity of cytochrome C induced by photochemically generated singlet oxygen and tree radicals. J. Biol. Chem. 279, 39214-39222
36. Purring-Koch, C. and McLendon, G. (2000) Cytochrome c binding to Apaf-1: the effects of dATP and ionic strength. Proc. Natl. Acad. Sci. U.S.A. 97, 11928-11931
37. Kluck, R. M., Ellerby, L. M., Ellerby, H. M., Naiem, S., Yaffe, M. P., Margoliash, E., Bredesen, D., Mauk, A. G., Sherman, F. and Newmeyer, D. D. (2000) Determinants of cytochrome c pro-apoptotic activity. The role of lysine 72 trimethylation. J. Biol. Chem. 275, 16127-16133
38. Yu, T., Wang, X., Purring-Koch, C., Wei, Y. and McLendon, G. L. (2001) A mutational epitope for cytochrome c binding to the apoptosis protease activation factor-1. J. Biol. Chem. 276, 13034-13038
39. Nomura, K., Imai, H., Koumura, T., Kobayashi, T. and Nakagawa, Y. (2000) Mitochondrial phospholipid hydroperoxide glutathione peroxidase inhibits the release of cytochrome c from mitochondria by suppressing the peroxidation of cardiolipin in hypoglycaemia-induced apoptosis. Biochem. J. 351, 183-193
40. Kar, L., Sherman, S. and Johnson, M. E. (1994) Comparison of protein structures in solution using local conformations derived from NMR data: application to cytochrome c. J. Biomol. Struct. Dyn. 12, 527-558
41. Calvert, J. F., Hill, J. L. and Dong, A. (1997) Redox-dependent conformational changes are common structural features of cytochrome c from various species. Arch. Biochem. Biophys. 346, 287-293
42. Martin, A. G. and Fearnhead, H. O. (2002) Apocytochrome c blocks caspase-9 activation and Bax-induced apoptosis J. Biol. Chem. 277, 50834-50841
43. Martin, A. G., Nguyen, J., Wells, J. A. and Fearnhead, H. O. (2004) Apocytochrome c inhibits caspases by preventing apoptosome formation. Biochem. Biophys. Res Commun. 319, 944-950
44. Ascenzi, P., Salvati, L., Bolognesi, M., Colasanti, M., Polticelli, F. and Venturini, G. (2001) Inhibition of cysteine protease activity by NO-donors, Curr. Protein Pept. Sci. 2, 137-153
45. Percival, M. D., Quellet, M., Campagnolo, C., Claveau, D. and Li, C. (1999) Inhibition of cathepsin K by nitric oxide donors: evidence for the formation of mixed disulfides and a sulfenic acid. Biochemistry 38, 13574-13583
46. Nagaoka, Y., Otsu, K., Okada, F., Sato, K., Ohba, Y., Kotani, N. and Fujii, J. (2005) Specific inactivation of cysteine protease-type cathepsin by singlet oxygen generated from naphthalene endoperoxides. Biochem. Biophys. Res. Commun. 331, 215-223
47. Savill, J. and Fadok, V. (2000) Corpse clearance defines the meaning of cell death. Nature (London) 407, 784-788
48. Cline, A. M. and Radic, M. Z. (2004) Apoptosis, subcellular particles and autoimmunity. Clin. Immunol. 112, 175-182
49. Hanayama, R., Tanaka, M., Miyasaka, K., Aozasa, K., Koike, M., Uchiyama, Y. and Nagata, S. (2004) Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice. Science 304, 1147-1150