Cardiolipin-Specific Peroxidase Reactions of Cytochrome c in Mitochondria During Irradiation-Induced Apoptosis

International Journal of Radiation Oncology Biology Physics

Volumn 69, Issue 1, 2007, Pages 176-186

  Belikova, Natalia A ^a   Jiang, Jianfei ^a   Tyurina, Yulia Y ^a   Zhao, Qing ^a   Epperly, Michael W ^a   Greenberger, Joel ^a,b   Kagan, Valerian E ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Cardiolipin; Cytochrome c; Irradiation induced apoptosis

Indexed keywords

CELL MEMBRANES; ENZYMES; IRRADIATION; MASS SPECTROMETRY; PHOTOOXIDATION; RNA;

CARDIOLIPIN; CYTOCHROME C; IRRADIATION-INDUCED APOPTOSIS;

CELL DEATH;

CARDIOLIPIN; CASPASE 3; CASPASE 7; CYTOCHROME C; HYDROPEROXIDE; PEROXIDASE; PHOSPHATIDYLSERINE; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; SMALL INTERFERING RNA;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; ENZYME ACTIVATION; ENZYME MECHANISM; GAMMA IRRADIATION; HELA CELL; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IRRADIATION; LIPID OXIDATION; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN SECRETION; WESTERN BLOTTING;

APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BLOTTING, WESTERN; CARDIOLIPINS; CASPASE 3; CASPASE 7; CYTOCHROMES C; ENZYME ACTIVATION; FLUORESCENCE; GAMMA RAYS; HELA CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPID PEROXIDATION; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; OXIDATION-REDUCTION; PHOSPHATIDYLSERINES; RADIATION TOLERANCE; RNA, SMALL INTERFERING;

EID: 34547850187     PISSN: 03603016     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijrobp.2007.03.043     Document Type: Article

References (41)

1. Ferlini C., D'Amelio R., and Scambia G. Apoptosis induced by ionizing radiation. The biological basis of radiosensitivity. Subcell Biochem 36 (2002) 171-186
2. Zhou L., Yuan R., and Serggio L. Molecular mechanisms of irradiation-induced apoptosis. Front Biosci 8 (2003) d9-d19
3. Epperly M.W., Gretton J.E., Sikora C.A., et al. Mitochondrial localization of superoxide dismutase is required for decreasing radiation-induced cellular damage. Radiat Res 160 (2003) 568-578
4. Li P., Nijhawan D., Budihardjo I., et al. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91 (1997) 479-489
5. Zou H., Li Y., Liu X., et al. An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J Biol Chem 274 (1999) 11549-11556
6. Purring-Koch C., and McLendon G. Cytochrome c binding to Apaf-1: The effects of dATP and ionic strength. Proc Natl Acad Sci U S A 97 (2000) 11928-11931
7. Chen Q., Gong B., and Almasan A. Distinct stages of cytochrome c release from mitochondria: Evidence for a feedback amplification loop linking caspase activation to mitochondrial dysfunction in genotoxic stress induced apoptosis. Cell Death Differ 7 (2000) 227-233
8. Gilmore K.J., Quinn H.E., and Wilson M.R. Pinocytic loading of cytochrome c into intact cells specifically induces caspase-dependent permeabilization of mitochondria: Evidence for a cytochrome c feedback loop. Cell Death Differ 8 (2001) 631-639
9. Luo X., Budihardjo I., Zou H., et al. 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
10. Li H., Zhu H., Xu C.J., et al. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94 (1998) 491-501
11. Kagan V.E., Tyurin V.A., Jiang J., et al. Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nat Chem Biol 1 (2005) 223-232
12. Zhivotovsky B., Hanson K.P., and Orrenius S. Back to the future: The role of cytochrome c in cell death. Cell Death Differ 5 (1998) 459-460
13. Fire A., Xu S., Montgomery M.K., et al. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391 (1998) 806-811
14. Zhao H., Kalivendi S., Zhang H., et al. Superoxide reacts with hydroethidine but forms a fluorescent product that is distinctly different from ethidium: Potential implications in intracellular fluorescence detection of superoxide. Free Radic Biol Med 34 (2003) 1359-1368
15. Folch J., Lees M., and Sloane Stanley G.H. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226 (1957) 497-509
16. Kagan V.E., Ritov V.B., Tyurina Y.Y., et al. Sensitive and specific fluorescent probing of oxidative stress in different classes of membrane phospholipids in live cells using metabolically integrated cis-parinaric acid. Methods Mol Biol 108 (1998) 71-87
17. Chalvardjian A., and Rudnicki E. Determination of lipid phosphorus in the nanomolar range. Anal Biochem 36 (1970) 225-226
18. Alpen E.L. Radiation biophysics. 2nd ed. (1998), Academic Press, San Diego (CA)
19. Green D.R., and Reed J.C. Mitochondria and apoptosis. Science 281 (1998) 1309-1312
20. Wei M.C., Zong W.X., Cheng E.H., et al. Proapoptotic BAX and BAK: A requisite gateway to mitochondrial dysfunction and death. Science 292 (2001) 727-730
21. Liu X., Kim C.N., Yang J., et al. Induction of apoptotic program in cell-free extracts: Requirement for dATP and cytochrome c. Cell 86 (1996) 147-157
22. Fadok V.A., Voelker D.R., Campbell P.A., et al. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol 148 (1992) 2207-2216
23. Tyurina Y.Y., Kawai K., Tyurin V.A., et al. The plasma membrane is the site of selective phosphatidylserine oxidation during apoptosis: Role of cytochrome C. Antioxid Redox Signal 6 (2004) 209-225
24. Armstrong J.S., and Jones D.P. Glutathione depletion enforces the mitochondrial permeability transition and causes cell death in Bcl-2 overexpressing HL60 cells. FASEB J 16 (2002) 1263-1265
25. Jiang X.J., and Wang X.D. Cytochrome C-mediated apoptosis. Annu Rev Biochem 73 (2004) 87-106
26. Hampton M.B., Zhivotovsky B., Slater A.F., et al. Importance of the redox state of cytochrome c during caspase activation in cytosolic extracts. Biochem J 329 Pt 1 (1998) 95-99
27. Cai J., and Jones D.P. Mitochondrial redox signaling during apoptosis. J Bioenerg Biomembr 31 (1999) 327-334
28. Kirkland R.A., and Franklin J.L. Evidence for redox regulation of cytochrome C release during programmed neuronal death: Antioxidant effects of protein synthesis and caspase inhibition. J Neurosci 21 (2001) 1949-1963
29. Hampton M.B., and Orrenius S. Redox regulation of apoptotic cell death. Biofactors 8 (1998) 1-5
30. Kagan V.E. Lipid peroxidaton in biomembranes (1988), CRC Press, Boca Raton, FL
31. Polyak K., Xia Y., Zweier J.L., et al. A model for p53-induced apoptosis. Nature 389 (1997) 300-305
32. Ostrander D.B., Sparagna G.C., Amoscato A.A., et al. Decreased cardiolipin synthesis corresponds with cytochrome c release in palmitate-induced cardiomyocyte apoptosis. J Biol Chem 276 (2001) 38061-38067
33. McMillin J.B., and Dowhan W. Cardiolipin and apoptosis. Biochim Biophys Acta 1585 (2002) 97-107
34. Paradies G., Petrosillo G., Pistolese M., et al. The effect of reactive oxygen species generated from the mitochondrial electron transport chain on the cytochrome c oxidase activity and on the cardiolipin content in bovine heart submitochondrial particles. FEBS Lett 466 (2000) 323-326
35. Lesnefsky E.J., Slabe T.J., Stoll M.S., et al. Myocardial ischemia selectively depletes cardiolipin in rabbit heart subsarcolemmal mitochondria. Am J Physiol Heart Circ Physiol 280 (2001) H2770-H2778
36. Ott M., Robertson J.D., Gogvadze V., et al. Cytochrome c release from mitochondria proceeds by a two-step process. Proc Natl Acad Sci U S A 99 (2002) 1259-1263
37. Nomura K., Imai H., Koumura T., et al. 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 (2000) 183-193
38. Jiang J., Serinkan B.F., Tyurina Y.Y., et al. Peroxidation and externalization of phosphatidylserine associated with release of cytochrome c from mitochondria. Free Radic Biol Med 35 (2003) 814-825
39. Tyurina Y.Y., Shvedova A.A., Kawai K., et al. Phospholipid signaling in apoptosis: Peroxidation and externalization of phosphatidylserine. Toxicology 148 (2000) 93-101
40. Hahn S.M., Krishna C.M., Samuni A., et al. Potential use of nitroxides in radiation oncology. Cancer Res 54 (1994) 2006s-2010s
41. Wipf P., Xiao J., Jiang J., et al. Mitochondrial targeting of selective electron scavengers: Synthesis and biological analysis of hemigramicidin-TEMPO conjugates. J Am Chem Soc 127 (2005) 12460-12461