Lysosomal release of Cathepsin D precedes relocation of Cytochrome C and loss of mitochondrial transmembrane potential during apoptosis induced by oxidative stress

Free Radical Biology and Medicine

Volumn 27, Issue 11-12, 1999, Pages 1228-1237

  Roberg, Karin ^a   Johansson, Uno ^a   Öllinger, Karin ^a  

^a LINKÖPING UNIVERSITY   (Sweden)

Author keywords

Apoptosis; Cathepsin D; Cytochrome c; Free radicals; Lysosomes; Mitochondria; Oxidative stress

Indexed keywords

CATHEPSIN D; CYTOCHROME C; NAPHTHAZARIN; PEPSTATIN;

APOPTOSIS; ARTICLE; CELL VIABILITY; CONFOCAL MICROSCOPY; FIBROBLAST; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; LYSOSOME; MEMBRANE POTENTIAL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

APOPTOSIS; CATHEPSIN D; CELL LINE; CYTOCHROME C GROUP; FIBROBLASTS; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; LYSOSOMES; MALE; MEMBRANE POTENTIALS; MICROSCOPY, ELECTRON; MITOCHONDRIA; NAPHTHOQUINONES; OXIDATIVE STRESS; PEPSTATINS; PROTEASE INHIBITORS;

EID: 0033436344     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0891-5849(99)00146-X     Document Type: Article

References (38)

1. Steller H. Mechanisms and genes of cellular suicide. Science. 267:1995;1445-1449.
2. Cai J., Yang J., Jones D.P. Mitochondrial control of apoptosis the role of cytochrome c . Biochem. Biophys. Acta. 1366:1998;139-149.
3. Chen B.L., Smiley S.T. Probing mitochondrial membrane potential in living cell by a J-aggregate-forming dye. Manson W.T. Fluorescent and luminescent probes for biological activity. 1993;124-132 Academic Press, London.
4. Reers M., Smith T.W., Chen B.L. J-aggregate formation of a carbocyanine as a quantitative fluorescent indicator of membrane potential. Biochemistry. 30:1991;4480-4486.
5. Zamzami N., Marchetti P., Castedo M., Zanin C., Vayssiére J.-L., Petit P.X., Kroemer G. Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in vivo. J. Exp. Med. 181:1995;1661-1672.
6. Kroemer G., Zamzami N., Susin S.A. Mitochondrial control of apoptosis. Immunol. Today. 18:1997;3861-3870.
7. Buttke T.M., Sandstrom P.A. Oxidative stress as a mediator of apoptosis. Immunol. Today. 15:1994;7-10.
8. Gardner A.M., Xu F., Fady C., Jacoby F.J., Duffey D.C., Tu Y., Lichtenstein A. Apoptotic vs nonapoptotic cytotoxicity induced by hydrogen peroxide. Free Radic. Biol. Med. 22:1997;73-83.
9. Forrest V.J., Kang Y.-H., McClain D.E., Robinson D.H., Ramakrishnan N. Oxidative stress-induced apoptosis prevented by trolox. Free Radic. Biol. Med. 16:1994;675-684.
10. Slater A.F.G., Nobel C.S.I., Orrenius S. The role of intracellular oxidants in apoptosis. Biochim. Biophys. Acta. 1271:1995;59-62.
11. Hockenburg D.M., Oltovoi Z.N., Yin X.M. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell. 75:1993;241-251.
12. Kane D.J., Sarafian T.A., Antonio R., Hahn H., Gralla E.B., Valentine J.S., Ord T., Bredesen D.E. BCL-2 inhibition of neutral death decreased generation of reactive oxygen species . Science. 262:1993;1274-1277.
13. Hennet T., Richter C., Peterhans E. Tumour necrosis factor-alpha induces superoxide anion production in mitochondria of L929 cells. Biochem. J. 289:1993;587-592.
14. Minn A.J., Rudin C.M., Boise L.H., Thompson B. Expression of bcl-xl can confer a multidrug resistance phenotype. Blood. 86:1995;1903-1910.
15. Ohkuma S., Poole B. Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. Proc. Natl. Acad. Sci. USA. 75:1978;3327-3331.
16. Yamamoto K. Cathepsin E, Cathepsin D biosynthesis, processing and subcellular location . Takahashi K. Aspartic proteases structure, function, biology and biomedical implications . 1995;223-229 Plenum Press, New York.
17. Peters P.J., Neefjes J.J., Oorschot V., Ploegh H.L., Geuze H.J. Segregation of MHC class II molecules from MHC class I molecules in the Golgi complex for transport to lysosomal compartments. Nature. 349:1991;669-676.
18. Cantor A.B., Kornfeld S. Phosphorylation of Asn-linked oligosaccharides located at novel sites on the lysosomal enzyme cathepsin D. J. Biol. Chem. 267:1992;23357-23363.
19. Rochefort H., Liaudet E., Garcia M. Alterations and role of human cathepsin D in cancer metastasis. Enzyme Protein. 49:1996;106-116.
20. Öllinger K., Brunk U.T. Oxidative stress-induced cellular injury is mediated through lysosomal damage. Free Radic. Biol. Med. 19:1995;565-574.
21. 2-mediated damage to lysosomal membranes of J774-cells. Free Radic. Res. Commun. 18:1993;71-73.
22. Brunk U.T., Zhang H., Roberg K., Öllinger K. Lethal hydrogen peroxide toxicity involves lysosomal iron-catalyzed reactions with membrane damage. Redox Report. 1:1995;267-277.
23. Roberg K., Öllinger K. Oxidative stress causes relocation of the lysosomal enzyme cathepsin D with ensuing apoptosis in neonatal rat cardiomyocytes. Am. J. Pathol. 152:1998;1151-1156.
24. Deiss L.P., Galinka H., Barissi H., Cohen O., Kimichi A. Cathepsin D protease mediates programmed cell death induced by interferon-gamma, Fas/APO-1 and TNF-alpha. EMBO J. 15:1996;3861-3870.
25. Wu G.S., Saftig P., Peters C., El-Deiry W.S. Potential role for cathepsin D in p53-dependent tumor suppression and chemosensitivity. Oncogene. 16:1998;2177-2183.
26. Vancompernolle K., van Herreweghe F., Pynaert G., van der Craen M., de Vos K., Totty N., Sterling A., Fiers. W.; Vandenabeele P., Grooten J. Atractyloside-induced release of cathepsin B, a protease with caspase-processing activity. FEBS Lett. 438:1998;150-158.
27. Brunk U.T., Dalen H., Roberg K., Hellquist H.B. Photo-oxidative disruption of lysosomal membranes causes apoptosis of culture human fibroblasts. Free Radic. Biol. Med. 23:1997;616-626.
28. Shields P.P., Gonzales T.A., Charles D., Gilligfan J.P., Stern W. Accumulation of pepstatin in cultured endothelial cells and its effect on endothelial processing. Biochem. Biophys. Res. Commun. 177:1991;1006-1012.
29. Öllinger K., Brunmark A. Effect of different oxygen pressure and DPPD on adriamycin toxicity to neonatal rat heart myocytes. Biochem. Pharmacol. 48:1994;1707-1715.
30. Öllinger, K. Inhibition of cathepsin D prevents free radical induced apoptosis in rat cardiomyocytes. Arch. Biochem. Biophys. in press; 1999.
31. Zdolsek J., Olsson M., Brunk U.T. Photooxidative damage to lysosomes of cultured macrophages by acridine orange. Photochem. Photobiol. 51:1990;67-76.
32. Scarlett J.L., Murphy M.P. Release of apoptogenic proteins from the mitochondrial intermembrane space during the mitochondrial permeability transition. FEBS Lett. 418:1997;282-286.
33. Yang J.C., Cortopassi G.A. Induction of mitochondrial permeability transition causes release of the apoptogenic factor cytochrome C. Free Radic. Biol. Med. 24:1998;624-631.
34. Zhivotovsky B., Orrenius S., Brustugun O.T., Doskeland S.O. Injected cytochrome c induces apoptosis. Nature. 391:1998;449-450.
35. Cossarizza A., Kalashnikova G., Grassilli E., Chiappelli F., Salvioli S., Capri M., Barbieri D., Troiano L., Monti D., Franceschi C. Mitochondrial modifications during rat thymocyte apoptosis a study at single cell level. Exp. Cell Res. 214:1994;323-330.
36. Smiley S.T., Reers M., Mottola-Hartshorn C., Lin M., Chen A., Smith T.W., Steele G.D., Chen L.B. Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc. Natl. Acad. Sci. USA. 88:1991;3671-3675.
37. Ankarcrona M., Dypbukt J.M., Bonfoco E., Zhivovsk B., Orrenius S., Lipton S.A., Nicotera P. Glutamate-induced neuronal death a succession of necrosis or apoptosis depending on mitochondrial function . Neuron. 15:1995;961-973.
38. Richter C., Schweizer M., Cossarizza A., Franceschi C. Control of apoptosis by cellular ATP level. FEBS Lett. 378:1996;107-110.