Manganese superoxide dismutase inactivation during Fas (CD95)-mediated apoptosis in Jurkat T cells

Free Radical Biology and Medicine

Volumn 41, Issue 12, 2006, Pages 1795-1806

  Pardo, Michal ^a   Melendez, J Andres ^b   Tirosh, Oren ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b ALBANY MEDICAL COLLEGE   (United States)

Author keywords

Apoptosis; Caspase activity; Mitochondria; Redox state

Indexed keywords

BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CALCIUM; CASPASE 3; CYCLOHEXIMIDE; FAS ANTIGEN; HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; PROTEIN SYNTHESIS INHIBITOR; RECOMBINANT ENZYME; SUPEROXIDE;

APOPTOSIS; ARTICLE; CALCIUM MOBILIZATION; CELL DEATH; CONTROLLED STUDY; CYTOSOLIC FRACTION; ENZYME DEGRADATION; ENZYME INACTIVATION; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN INTERACTION; STEADY STATE; T LYMPHOCYTE;

AMINO ACID SEQUENCE; ANTIBODIES; ANTIGENS, CD95; APOPTOSIS; CALCIUM; CASPASES; HUMANS; JURKAT CELLS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PROTEIN DENATURATION; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE;

EID: 33751548294     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2006.08.027     Document Type: Article

References (66)

1. Nagata S. Apoptosis by death factor. Cell 88 (1997) 355-365
2. Steller H. Mechanisms and genes of cellular suicide. Science 267 (1995) 1445-1449
3. Ashkenazi A., and Dixit V.M. Death receptors: signaling and modulation. Science 281 (1998) 1305-1308
4. Green D.R., and Reed J.C. Mitochondria and apoptosis. Science 281 (1998) 1309-1312
5. Li H., Zhu H., Xu C.J., and Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94 (1998) 491-501
6. Luo X., Budihardjo I., Zou H., Slaughter C., and 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
7. Robertson J.D., Enoksson M., Suomela M., Zhivotovsky B., and Orrenius S. Caspase-2 acts upstream of mitochondria to promote cytochrome c release during etoposide-induced apoptosis. J. Biol. Chem. 277 (2002) 29803-29809
8. Robertson J.D., Gogvadze V., Kropotov A., Vakifahmetoglu H., Zhivotovsky B., and Orrenius S. Processed caspase-2 can induce mitochondria-mediated apoptosis independently of its enzymatic activity. EMBO Rep. 5 (2004) 643-648
9. Kroemer G., and Martin S.J. Caspase-independent cell death. Nat. Med. 11 (2005) 725-730
10. French L.E., Hahne M., Viard I., Radlgruber G., Zanone R., Becker K., et al. Fas and Fas ligand in embryos and adult mice: ligand expression in several immune-privileged tissues and coexpression in adult tissues characterized by apoptotic cell turnover. J. Cell Biol. 133 (1996) 335-343
11. Lee J., Richburg J.H., Younkin S.C., and Boekelheide K. The Fas system is a key regulator of germ cell apoptosis in the testis. Endocrinology 138 (1997) 2081-2088
12. Lynch D.H., Ramsdell F., and Alderson M.R. Fas and FasL in the homeostatic regulation of immune responses. Immunol. Today 16 (1995) 569-574
13. Suzuki A., Enari M., Eguchi Y., Matsuzawa A., Nagata S., Tsujimoto Y., et al. Involvement of Fas in regression of vaginal epithelia after ovariectomy and during an estrous cycle. EMBO J. 15 (1996) 211-215
14. Kohno T., Yamada Y., Hata T., Mori H., Yamamura M., Tomonaga M., et al. Relation of oxidative stress and glutathione synthesis to CD95(Fas/APO-1)-mediated apoptosis of adult T cell leukemia cells. J. Immunol. 156 (1996) 4722-4728
15. Sato T., Machida T., Takahashi S., Iyama S., Sato Y., Kuribayashi K., et al. Fas-mediated apoptosome formation is dependent on reactive oxygen species derived from mitochondrial permeability transition in Jurkat cells. J. Immunol. 173 (2004) 285-296
16. Hayakawa M., Miyashita H., Sakamoto I., Kitagawa M., Tanaka H., Yasuda H., et al. Evidence that reactive oxygen species do not mediate NF-kappaB activation. EMBO J. 22 (2003) 3356-3366
17. Martinvalet D., Zhu P., and Lieberman J. Granzyme A induces caspase-independent mitochondrial damage, a required first step for apoptosis. Immunity 22 (2005) 355-370
18. Aronis A., Melendez J.A., Golan O., Shilo S., Dicter N., and Tirosh O. Potentiation of Fas-mediated apoptosis by attenuated production of mitochondria-derived reactive oxygen species. Cell Death Differ. 10 (2003) 335-344
19. Wong G.H., Elwell J.H., Oberley L.W., and Goeddel D.V. Manganous superoxide dismutase is essential for cellular resistance to cytotoxicity of tumor necrosis factor. Cell 58 (1989) 923-931
20. Wong G.H., and Goeddel D.V. Induction of manganous superoxide dismutase by tumor necrosis factor: possible protective mechanism. Science 242 (1988) 941-944
21. Kops G.J., Dansen T.B., Polderman P.E., Saarloos I., Wirtz K.W., Coffer P.J., et al. Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 419 (2002) 316-321
22. Li C., Wright M.M., and Jackson R.M. Reactive species mediated injury of human lung epithelial cells after hypoxia-reoxygenation. Exp. Lung Res. 28 (2002) 373-389
23. Pani G., Bedogni B., Anzevino R., Colavitti R., Palazzotti B., Borrello S., et al. Deregulated manganese superoxide dismutase expression and resistance to oxidative injury in p53-deficient cells. Cancer Res. 60 (2000) 4654-4660
24. Tanaka H., Matsumura I., Ezoe S., Satoh Y., Sakamaki T., and Albanese C. E2F1 and c-Myc potentiate apoptosis through inhibition of NF-kappaB activity that facilitates MnSOD-mediated ROS elimination. Mol. Cell 9 (2002) 1017-1029
25. Wong G.H. Protective roles of cytokines against radiation: induction of mitochondrial MnSOD. Biochim. Biophys. Acta 1271 (1995) 205-209
26. Kokoszka J.E., Coskun P., Esposito L.A., and Wallace D.C. Increased mitochondrial oxidative stress in the Sod2 (+/-) mouse results in the age-related decline of mitochondrial function culminating in increased apoptosis. Proc. Natl. Acad. Sci. USA 98 (2001) 2278-2283
27. Van Remmen H., Williams M.D., Guo Z., Estlack L., Yang H., Carlson E.J., et al. Knockout mice heterozygous for Sod2 show alterations in cardiac mitochondrial function and apoptosis. Am. J. Physiol. Heart Circ. Physiol. 281 (2001) H1422-H1432
28. Bruce-Keller A.J., Geddes J.W., Knapp P.E., McFall R.W., Keller J.N., Holtsberg F.W., et al. Anti-death properties of TNF against metabolic poisoning: mitochondrial stabilization by MnSOD. J. Neuroimmunol. 93 (1999) 53-71
29. Epperly M.W., Bernarding M., Gretton J., Jefferson M., Nie S., and Greenberger J.S. Overexpression of the transgene for manganese superoxide dismutase (MnSOD) in 32D cl 3 cells prevents apoptosis induction by TNF-alpha, IL-3 withdrawal, and ionizing radiation. Exp. Hematol. 31 (2003) 465-474
30. Epperly M.W., Sikora C.A., DeFilippi S.J., Gretton J.A., Zhan Q., Kufe D.W., et al. Manganese superoxide dismutase (SOD2) inhibits radiation-induced apoptosis by stabilization of the mitochondrial membrane. Radiat. Res. 157 (2002) 568-577
31. Manna S.K., Zhang H.J., Yan T., Oberley L.W., and Aggarwal B.B. Overexpression of manganese superoxide dismutase suppresses tumor necrosis factor-induced apoptosis and activation of nuclear transcription factor-kappaB and activated protein-1. J. Biol. Chem. 273 (1998) 13245-13254
32. Sen C.K., Sashwati R., and Packer L. Fas mediated apoptosis of human Jurkat T-cells: intracellular events and potentiation by redox-active alpha-lipoic acid. Cell Death Differ. 6 (1999) 481-491
33. Tirosh O., Sen C.K., Roy S., and Packer L. Cellular and mitochondrial changes in glutamate-induced HT4 neuronal cell death. Neuroscience 97 (2000) 531-541
34. Shishido S., Koga H., Harada M., Kumemura H., Hanada S., Taniguchi E., et al. Hydrogen peroxide overproduction in megamitochondria of troglitazone-treated human hepatocytes. Hepatology 37 (2003) 136-147
35. LeBel C.P., Ischiropoulos H., and Bondy S.C. Evaluation of the probe 2,7-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem. Res. Toxicol. 5 (1992) 227-231
36. Vanden Hoek T.L., Shao Z., Li C., Schumacker P.T., and Becker L.B. Mitochondrial electron transport can become a significant source of oxidative injury in cardiomyocytes. J. Mol. Cell. Cardiol. 29 (1997) 2441-2450
37. Zhao H., Kalivendi S., Zhang H., Joseph J., Nithipatikom K., and Vasquez-Vivar J. 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
38. Moini H., Guo Q., and Packer L. Enzyme inhibition and protein-binding action of the procyanidin-rich french maritime pine bark extract, pycnogenol: effect on xanthine oxidase. J. Agric. Food Chem. 48 (2000) 5630-5639
39. Tirosh O., Pardo M., Schwartz B., and Miskin R. Long-lived alphaMUPA transgenic mice show reduced SOD2 expression, enhanced apoptosis and reduced susceptibility to the carcinogen dimethylhydrazine. Mech. Ageing Dev. 126 (2005) 1262-1273
40. Gottlieb E., Armour S.M., Harris M.H., and Thompson C.B. Mitochondrial membrane potential regulates matrix configuration and cytochrome c release during apoptosis. Cell Death Differ. 10 (2003) 709-717
41. Zhang L., Himi T., Morita I., and Murota S. Inhibition of phosphatidylinositol-3 kinase/Akt or mitogen-activated protein kinase signaling sensitizes endothelial cells to TNF-alpha cytotoxicity. Cell Death Differ. 8 (2001) 528-536
42. Zhou A., Scoggin S., Gaynor R.B., and Williams N.S. Identification of NF-kappa B-regulated genes induced by TNFalpha utilizing expression profiling and RNA interference. Oncogene 22 (2003) 2054-2064
43. Hengartner M.O. The biochemistry of apoptosis. Nature 407 (2000) 770-776
44. Juo P., Woo M.S., Kuo C.J., Signorelli P., Biemann H.P., Hannun Y.A., et al. FADD is required for multiple signaling events downstream of the receptor Fas. Cell Growth Differ. 10 (1999) 797-804
45. Fischer U., Janicke R.U., and Schulze-Osthoff K. Many cuts to ruin: a comprehensive update of caspase substrates. Cell Death Differ. 10 (2003) 76-100
46. Gao B., Flores S.C., Leff J.A., Bose S.K., and McCord J.M. Synthesis and anti-inflammatory activity of a chimeric recombinant superoxide dismutase: SOD2/3. Am. J. Physiol. Lung Cell. Mol. Physiol. 284 (2003) L917-L925
47. Boveris A., and Chance B. The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem. J. 134 (1973) 707-716
48. Cadenas E., and Davies K.J. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic. Biol. Med. 29 (2000) 222-230
49. Chance B., Sies H., and Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 59 (1979) 527-605
50. Van Remmen H., Ikeno Y., Hamilton M., Pahlavani M., Wolf N., Thorpe S.R., et al. Life-long reduction in MnSOD activity results in increased DNA damage and higher incidence of cancer but does not accelerate aging. Physiol. Genomics 16 (2003) 29-37
51. Epperly M.W., Gretton J.A., DeFilippi S.J., Greenberger J.S., Sikora C.A., Liggitt D., et al. Modulation of radiation-induced cytokine elevation associated with esophagitis and esophageal stricture by manganese superoxide dismutase-plasmid/liposome (SOD2-PL) gene therapy. Radiat. Res. 155 (2001) 2-14
52. Sen C.K. Cellular thiols and redox-regulated signal transduction. Curr. Top. Cell Regul. 36 (2000) 1-30
53. Ueda S., Nakamura H., Masutani H., Sasada T., Yonehara S., Takabayashi A., et al. Redox regulation of caspase-3(-like) protease activity: regulatory roles of thioredoxin and cytochrome c. J. Immunol. 161 (1998) 6689-6695
54. Hampton M.B., and Orrenius S. Dual regulation of caspase activity by hydrogen peroxide: implications for apoptosis. FEBS Lett. 414 (1997) 552-556
55. 2. Antioxid. Redox Signal. In press.
56. Krammer P.H. CD95's deadly mission in the immune system. Nature 407 (2000) 789-795
57. Chandra D., and Tang D.G. Mitochondrially localized active caspase-9 and caspase-3 result mostly from translocation from the cytosol and partly from caspase-mediated activation in the organelle. Lack of evidence for Apaf-1-mediated procaspase-9 activation in the mitochondria. J. Biol. Chem. 278 (2003) 17408-17420
58. Poncet D., Boya P., Metivier D., Zamzami N., and Kroemer G. Cytofluorometric quantitation of apoptosis-driven inner mitochondrial membrane permeabilization. Apoptosis 8 (2003) 521-530
59. Zhang Y., Haskins C., Lopez-Cruzan M., Zhang J., Centonze V., and Herman E. Detection of mitochondrial caspase activity in real time in situ in live cells. Microsc. Microanal. 10 (2004) 442-448
60. Krippner-Heidenreich A., Talanian R.V., Sekul R., Kraft R., Thole H., and Ottleben H. Targeting of the transcription factor Max during apoptosis: phosphorylation-regulated cleavage by caspase-5 at an unusual glutamic acid residue in position P1. Biochem. J. 358 (2001) 705-715
61. Charvet C., Alberti I., Luciano F., Jacquel A., Bernard A., Auberger P., et al. Proteolytic regulation of forkhead transcription factor FOXO3a by caspase-3-like proteases. Oncogene 22 (2003) 4557-4568
62. Jayaraman T., and Marks A.R. T cells deficient in inositol 1,4,5-trisphosphate receptor are resistant to apoptosis. Mol. Cell. Biol. 17 (1997) 3005-3012
63. Sugawara H., Kurosaki M., Takata M., and Kurosaki T. Genetic evidence for involvement of type 1, type 2 and type 3 inositol 1,4,5-trisphosphate receptors in signal transduction through the B-cell antigen receptor. EMBO J. 16 (1997) 3078-3088
64. Juin P., Pelletier M., Oliver L., Tremblais K., Gregoire M., Meflah K., et al. Induction of a caspase-3-like activity by calcium in normal cytosolic extracts triggers nuclear apoptosis in a cell-free system. J. Biol. Chem. 273 (1998) 17559-17564
65. Pelletier M., Oliver L., Meflah K., and Vallette F.M. Caspase-3 can be pseudo-activated by a Ca2+-dependent proteolysis at a non-canonical site. FEBS Lett. 579 (2005) 2364-2368
66. Wu Z., Tandon R., Ziembicki J., Nagano J., Hujer K.M., and Miller R.T. Role of ceramide in Ca2+-sensing receptor-induced apoptosis. J. Lipid Res. 46 (2005) 1396-1404