Separation of cytochrome c-dependent caspase activation from thiol- disulfide redox change in cells lacking mitochondrial DNA

Free Radical Biology and Medicine

Volumn 29, Issue 3-4, 2000, Pages 334-342

  Cai, Jiyang ^a   Wallace, Douglas C ^a   Zhivotovsky, Boris ^b   Jones, Dean P ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Adenylate kinase; Apoptosis; Cytochrome c; Free radicals; Mitochondria; Redox

Indexed keywords

CASPASE; CYTOCHROME C OXIDASE; GLUTATHIONE; MITOCHONDRIAL DNA; STAUROSPORINE;

APOPTOSIS; ARTICLE; ELECTRON TRANSPORT; ENZYME ACTIVATION; HUMAN; HUMAN CELL; LYMPHOCYTE; MITOCHONDRIAL RESPIRATION; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL;

ADENYLATE KINASE; ANTIGENS, CD95; APOPTOSIS; CASPASES; CELL LINE; CYTOCHROME C; DISULFIDES; DNA FRAGMENTATION; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT; ENZYME ACTIVATION; GLUTATHIONE; GLUTATHIONE DISULFIDE; HUMAN; IMMUNOHISTOCHEMISTRY; JURKAT CELLS; KINETICS; MICROSCOPY, FLUORESCENCE; MITOCHONDRIA; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; STAUROSPORINE; SUPPORT, U.S. GOV'T, P.H.S.;

EID: 0033805327     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0891-5849(00)00312-9     Document Type: Article

References (54)

1. Finkel T. Oxygen radicals and signaling. Curr. Opin. Cell. Biol. 19:1998;248-253.
2. Nakamura H., Nakamura K., Yodoi J. Redox regulation of cellular activation. Annu. Rev. Immunol. 15:1997;351-369.
3. Ma L.C., Anderson S. Correlation between disulfide reduction and conformational unfolding in bovine pancreatic trypsin inhibitor. Biochemistry. 36:1997;3728-3736.
4. Gorlatov S.N., Stadtman T.C. Human thioredoxin reductase from HeLa cells selective alkylation of selenocysteine in the protein inhibits enzyme activity and reduction with NADPH influences affinity to heparin . Proc. Natl. Acad. Sci. USA. 95:1998;8520-8525.
5. Hirota K., Matsui M., Iwata S., Nishiyama A., Mori K., Yodoi J. AP-1 transcriptional activity is regulated by a direct association between thioredoxin and Ref-1. Proc. Natl. Acad. Sci. USA. 94:1997;3633-3638.
6. Bains J.S., Shaw C.A. Neurodegenerative disorders in humans the role of glutathione in oxidative stress-mediated neuronal death . Brain Res. Brain Res. Rev. 25:1997;335-358.
7. Saitoh M., Nishitoh H., Fujii M., Takeda K., Tobiume K., Sawada Y., Kawabata M., Miyazono K., Ichijo H. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (AKS) 1. Eur. Mol. Biol. Organ. J. 17:1998;2596-2606.
8. Smith C.V., Jones D.P., Guenthner T.M., Lash L.H., Lauterburg B.H. Compartmentation of glutathione implications for the study of toxicity and disease . Toxicol. Appl. Pharmacol. 140:1996;1-12.
9. Bjornstedt M., Kumar S., Bjorkhem L., Spyrou G., Holmgren A. Selenium and the thioredoxin and glutaredoxin systems. Biomed. Environ. Sci. 10:1997;271-279.
10. Powis G., Briehl M., Oblong J. Redox signaling and the control of cell growth and death. Pharmacol. Ther. 68:1995;149-173.
11. Thornberry N.A., Lazebnik Y. Caspases enemies within . Science. 281:1998;1312-11316.
12. Slater A.F., Stefan C., Nobel I., van den Dobbelsteen D.J., Orrenius S. Signaling mechanisms and oxidative stress in apoptosis. Toxicol. Lett. 82:1995;149-153.
13. Cai J., Jones D.P. Superoxide in apoptosis; mitochondrial generation triggered by cytochrome c loss. J. Biol. Chem. 273:1998;11401-11404.
14. Hockenbery D.M., Oltvai Z.N., Yin X.M., Milliman C.L., Korsmeyer S.J. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell. 75:1993;241-251.
15. Suzuki Y., Ono Y., Hirabayashi Y. Rapid and specific reactive oxygen species generation via NADPH oxidase activation during Fas-mediated apoptosis. FEBS Lett. 425:1998;209-212.
16. Majima H.J., Oberely T.D., Furukawa K., Mattson M.P., Yen H.-C., Szweda L.I., St. Clair D.K. Prevention of mitochondrial injury by manganese superoxide dismutase reveals a primary mechanism for alkaline-induced cell death. J. Biol. Chem. 273:1998;8217-8224.
17. Zhang P., Liu B., Kang S.W., Seo M.S., Rhee S.G., Obeid L.M. Thioredoxin peroxidase is a novel inhibitor of apoptosis with a mechanism distinct from that of Bcl-2. J. Biol. Chem. 272:1997;30615-30618.
18. Mayer M., Noble M. N-acetyl-L-cysteine is a pluripotent protector against cell death and enhancer of trophic factor-mediated cell survival in vitro. Proc. Natl. Acad. Sci. USA. 91:1994;7496-7500.
19. Holguin F., Moss I., Brown L.A., Guidot D.M. Chronic ethanol ingestion imparis alveolar type II cells glutathione homeostasis and function and predisposes to endotoxin-mediated acute edematous lung injury in rats. . J. Clin. Invest. 101:1998;761-768.
20. Li P., Nijhawan D., Budihardjo I., Srinivasula S.M., Ahmad M., Alnemri E.S., Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apototic protease cascade. Cell. 91:1998;479-489.
21. Hampton M.B., Zhivotovsky B., Slater A.F., Burgess D.H., Orrenius S. Importance of the redox state of cytochrome c during caspase activation in cytosolic extracts. Biochem. J. 329:1998;95-99. [part 1].
22. Susin A.S., Zamzami N., Kroemer G. Mitochondria as regulators of apoptosis doubt no more . Biochim. Biophys. Acta. 1366:1998;151-165.
23. Chu Z.L., McKinsey T.A., Liu L., Gentry J.J., Malim M.H., Ballard D.W. Suppression of tumor necrosis factor-induced cell death by inhibitor of apoptosis c-IAP2 is under NF-kappaB control. Proc. Natl. Acad. Sci. USA. 94:1997;10057-10062.
24. Hampton M.B., Orrenius S. Redox regulation of apoptotic cell death in the immune system. Toxicol. Lett. 102-103:1998;355-358.
25. Hampton M.B., Fadeel B., Orrenius S. Redox regulation of the caspases during apoptosis. Ann. NY Acad. Sci. 854:1998;328-335.
26. Van den Dobbelsteen D.J., Nobel C.S.I., Schlegel J., Cotgreave I.A., Orrenius S., Slater A.F. Rapid and specific efflux of reduced glutathione during apoptosis induced by anti-Fas/APO-1 antibody. J. Biol. Chem. 271:1996;15420-15427.
27. Kirlin W.G., Cai J., Thompson S.A., Diaz D., Kavanagh T.J., Jones D.P. Glutathione redox potential during differentiation and enzyme induction. Free Radic. Biol. Med. 27:1999;1208-1218.
28. Melov S., Shoffner J.M., Kaufman A., Wallace D.C. Marked increase in the number and variety of mitochondrial DNA rearrangements in aging human skeletal muscle. Nucleic Acids Res. 23:1995;4122-4126.
29. Yakes F.M., van Houten B. Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc. Natl. Acad. Sci. USA. 94:1997;514-519.
30. Stridth H., Kimland M., Jones D.P., Orrenius S., Hampton M.B. Cytochrome c release and caspase activation in hydrogen peroxide- and tributyltin-induced apoptosis. FEBS Lett. 429:1998;351-355.
31. Yang J., Liu X., Bhalla K., Kim C.N., Ibrado A.M., Cai J., Peng T.-I., Jones D.P., Wang X. Prevention of apoptosis by Bcl-2 release of cytochrome c from mitochondria blocked . Science. 275:1997;1129-1132.
32. Bai C., Slife C.W., Aw T.Y., Jones D.P. Fractionation and analysis of mitochondria with polycarbonate membrane filters. Anal. Biochem. 179:1989;114-119.
33. Noma T., Song S., Yoon Y.S., Tanaka S., Nakazawa A. CDNA cloning and tissue-specific expression of the gene encoding human adenylate kinase isozyme 2. Biochim. Biophys. Acta. 1395:1998;34-39.
34. Jones D.P., Carlson J.C., Samiec P.S., Sternberg P., Reed R.L., Brown L.A.S. GSH measurement in human plasma. Evaluation of sample collection; storage and derivatization conditions for analysis of dansylderivatives by HPLC. Clin. Chim. Acta. 275:1998;175-184.
35. Bradford M.N. A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:1976;248-254.
36. Rost J., Rapoport S. Reduction potential of glutathione. Nature. 201:1964;185-187.
37. Park Y., Aw T.K., Jones D.P. ATP and other energetic parameters as indicators of cell injury. Tyson C.A., Frazier J. In vitro toxicity indicators (vol. 1B). 1994;140-151 Academic Press, London.
38. Marchetti P., Susin S.A., Decaudin D., Gamen S., Castedo M., Hirsch T., Zamzami N., Naval J., Senik A., Kroemer G. Apoptosis-associated derangement of mitochondrial function in cells lacking mitochondrial DNA. Cancer Res. 56:1996;2033-2038.
39. Green D.R., Reed J. Mitochondria and apoptosis. Science. 281:1998;1309-1312.
40. L regulates the membrane potential and volume homeostasis of mitochondria. Cell. 91:1997;627-637.
41. Li H., Zhu H., Xu C.-J., Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell. 94:1998;491-501.
42. Luo X., Imawati B., Zou H., Clive S., Wang X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell. 94:1998;481-490.
43. Enster L., Schatz G. Mitochondria a historical review [part 2] . J. Cell Biol. 91:1981;227s-255s.
44. Higuchi M., Aggarwai B.B., Yeh E.T.H. Activation of CPP32-like protease in tumor necrosis factor-induced apoptosis is dependent on mitochondrial function. J. Clin. Invest. 99:1997;1751-1758.
45. Reed J.C. Cytochrome c can't live with it-can't live without it . Cell. 91:1997;559-562.
46. Minn A.J., Velez P., Schendel S.L., Liang H., Muchmore S.W., Fesik S.W., Fill M., Thompson C.B. Bcl-x(L) forms an ion channel in synthetic lipid membranes. Nature. 385:1997;353-357.
47. Schlesinger P.H., Gross A., Yin X.M., Yamamoto K., Saito M., Waksman G., Korsmeyer S.J. Comparison of the ion channel characteristics of proapoptotic BAX and antiapoptotic Blc-2. Proc. Natl. Acad. Sci. USA. 94:1997;11357-11362.
48. Samali A., Cai J., Zhivotovsky B., Jones D.P., Orrenius S. Presence of a pre-apoptotic complex of pro-caspase-3, HSP 60 and HSP 10 in the mitochondrial fraction of Jurkat cells. EMBO J. 18:1999;2040-2048.
49. Kohler C., Gahm A., Noma T., Nakazawa A., Orrenius S., Zhivotovsky B. Release of adenylate kinase 2 from the mitochondrial intermembrane space during apoptosis. FEBS Lett. 447:1999;10-12.
50. Single B., Leist M., Nicotera P. Simultaneous release of adenylate kinase and cytochrome c in cell death. Cell Death Differ. 5:1998;1001-1003.
51. Susin S.A., Zamzami N., Castedo M., Hirsh T., Marchetti P., Macho A., Daugas E., Geuskens M., Kroemer G. Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J. Exp. Med. 184:1996;1331-1341.
52. Samali A., Zhivotovsky B., Jones D.P., Orrenius S. Detection of pro-caspase-3 in cytosol and mitochondria of various tissues. FEBS Lett. 431:1998;167-169.
53. Mancini M., Nicholson D.W., Roy S., Thornberry N.A., Peterson E.P., Casciola-Rosen L.A., Rosen A. The caspase-3 precursor has a cytosolic and mitochondrial distribution implications for apoptotic signaling . J. Cell. Biol. 140:1998;1485-1495.
54. Jiang S., Cai J., Wallace D.C., Jones D.P. Cytochrome c-mediated apoptosis in cells lacking mitochondrial DNA signaling pathway involving release and caspase 3 activation is conserved . J. Biol. Chem. 274:1999;29905-29911.