Elevation of Mitochondrial transmembrane potential and reactive oxygen intermediate levels are early events and occur independently from activation of caspases in Fas signaling

Journal of Immunology

Volumn 162, Issue 3, 1999, Pages 1466-1479

  Banki, Katalin ^a   Hutter, Eliza ^a   Gonchoroff, Nick J ^a   Perl, Andras ^a  

^a SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; CASPASE 3; CASPASE INHIBITOR; FAS ANTIGEN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PEPTIDE; PHOSPHATIDYLSERINE; REACTIVE OXYGEN METABOLITE; TRANSALDOLASE;

APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; OXIDATION REDUCTION REACTION; PENTOSE PHOSPHATE CYCLE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANTIGENS, CD95; APOPTOSIS; CASPASES; CYSTEINE PROTEINASE INHIBITORS; ENZYME ACTIVATION; HUMANS; JURKAT CELLS; MEMBRANE POTENTIALS; MITOCHONDRIA; PHOSPHATIDYLSERINES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TRANSALDOLASE;

EID: 0033083310     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (86)

1. Wyllie, A. H., J. F. R. Kerr, and A. E. Currie. 1980. Cell death: the significance of apoptosis. Int. Rev. Cytol. 68:251.
2. Nagata, S., and P. Golstein. 1995. The Fas death factor. Science 267:1449.
3. Thompson, C. B., 1995. Apoptosis in the pathogenesis and treatment of disease. Science 267:1456.
4. Nagata, S., 1997. Apoptosis by death factor. Cell 88:355.
5. Itoh, N., and S. Nagata. 1993. A novel prolein domain required for apoptosis: mutational analysis of human Fas antigen. J. Biol. Chem. 268:10932.
6. Tanaglia, L. A., T. M. Ayres, G. H. W. Wong, and G. V. Goeddel. 1993. A novel domain within the 55 kd TNF receptor signals cell death. Cell 74:845.
7. Tewari, M., and V. M. Dixit. 1995. Fas- and tumor necrosis factor-induced apoptosis is inhibited by the Poxvirus crmA gene product. J. Biol. Chem. 270:3255.
8. Los, M., M. Van de Craen, L. S. Penning, H. Schenk, M. Westendorp, P. A. Baeuerle, W. Droge, P. H. Krammer, W. Flers, and K. Schulze-Osthoff. 1995. Requirement of an ICE/CED-3 protease for Fas/Apo-1-mediated apoptosis. Nature 375:81.
9. Enari, M., H. Hug, and S. Nagata. 1995. Involvement of an ICE-like protease in Fas-mediated apoptosis. Nature 375:78.
10. Martin, S. J., and D. R. Green. 1995. Protease activation during apoptosis: death by a thousand cuts. Cell 82:349.
11. Boldin, M. P., T. M. Goncharov, Y. V. Goltsev, and D. Wallach. 1996. Involvement of MACH, a novel MORT1/FADD-imeracting protease. in Fas/Apo-1- and TNF receptor-induced cell death. Cell 85:803.
12. Muzio, M., A. M. Chinnaiyan, F. C. Kischkel, K. O'Rourke, A. Shevchenko, J. Ni, K. Scaffidi, I. D. Bretz, M. Zhang, R. Gentz, et al. 1996. FLICE, a novel FADD-homologous ICE/CED-3-like prolease, is recruited to the CD95 (Fas/Apo 1) death-inducing signaling complex. Cell 85:817.
13. Miyawaki, T., T. Uehara, R. Nibu, T. Tsuji, A. Yachie, S. Yonehara, and N, Taniguchi. 1992. Differential expression of apoptosis related Fas antigen on lymphocyte subpopulations in human peripheral blood. J. Immunol. 149:3753.
14. Alderson, M. K., R. J. Armitage, E. Maraskovsky, T. W. Tough, E. Roux, K. Schooley, F. Ramsdell, and D. H. Lynch. 1993. Fas transduces activation signals in normal human T lymphocytes. J. Exp. Med. 178:2231.
15. Owen-Schaub, L. B., R. Radinsky, E. Kruzel, K. Berry, and S. Yonehara. 1992. Anti-Fas on nonhemopoietic tumors: levels of Fas/Apo-1 and Bcl-2 are not predictive of biological responses. Cancer Res. 54:1580.
16. Lipton, S. A., Y. Choi, Z. Pan, S. Z. Lei, H. V. Chen, N. J. Sucher, J. Loscalzo, D. J. Singel, and J. S. Stamler. 1993. A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature 364:626.
17. Halliwell, B., and J. M. Gutteridge. 1990. Role of free radicals and catalytic metal tons in human disease: an overview. Methods Enzymol. 186:1.
18. Stamler, J. S. 1994. Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell 78:931.
19. Korsmeyer, S. J., 1995. Regulators of cell death. Trends Genet. 11:101.
20. Buttke, T. M., and P. A. Sandstrom. 1994. Oxidative stress as a mediator or apoptosis. Immunol. Today 15:7.
21. Hamilos, D. L., and H. J. Wedner. 1985. The role of glulathione in lymphocyte activation. I. Comparison of inhibitory effects of buthionine sulfoximine and 2-cyclohexene-1-one by nuclear size transformation. J. Immunol. 135:2740.
22. Los, M., W. Droge, K. Stricker, P. A. Bauerle, and K. Schulze-Osthoff. 1995. Hydrogen peroxide as a potent activator of T lymphocyte functions. Eur. J. Immunol. 25:159.
23. Jacobson, M. D., and M. C. Raff. 1995. Programmed cell death and bcl-2 protection in very low oxygen. Nature 374:814.
24. Meier, B., H. H. Radeke, S. Selle, M. Younes, H. Sies, K. Resch, and G. G. Habermehl. 1989. Human fibroblasts release reactive oxygen species in response to interleukin-1 or tumor necrosis factor-α. Biochem. J. 263:539.
25. Hennet, T., C. Richter, and E. Peterhans. 1993. Tumor necrosis factor-α induces superoxide anion generation in mitochondria of L929 cells. Biochem. J. 289:587.
26. Schulze-Osthoff, K., P. H. Krammer, and W. Droge. 1994. Divergent signaling via APO-1/Fas and the TNF receptor, two homologous molecules involved in physiological cell death. EMBO J. 13:4587.
27. Banki, K., E. Hutter, E. Colombo, N. J. Gonchoroff, and A. Perl. 1996. Glutathione levels and sensitivity to apoptosis are regulated by changes in transaldolase expression. J. Biol. Chem. 271:32994.
28. Xiang, J., D. T. Chao, and S. J. Korsmeyer. 1996. BAX-induced cell death may not require interleukin 1β-converting enzyme-like proteases. Proc. Natl. Acad. Sci. USA 93:14559.
29. Kasahara, Y., K. Iwai, A. Yachie, K. Ohta, A. Konno, H. Seki, and T. Miyawaki, 1997. Involvement of reactive oxygen intermediates in spontaneous and CD95 (Fas/APO-1)-mediated apoptosis of neutrophils. Blood 89:1748.
30. Williams, M. S., and P. A. Henkart. 1996. Role of reactive oxygen intermediates in TCR-induced death of T cell blasts and hybridomas. J. Immunol. 157:2395.
31. 2-synthesis. Immunology 89:205.
32. Um, H. D., J. M. Orenstein, and S. M. Wahl. 1996. Fas mediates apoptosis in human monocytes by a reactive oxygen intermediate dependent pathway. J. Immunol. 156:3469.
33. Ames, B. N., 1989. Endogenous oxidative DNA damage, aging, and cancer. Free Rad. Res. Common. 7:121.
34. Sarafian, T. A., and D. E. Bredesen. 1994. Is apoptosis mediated by reactive oxygen species?. Free Rad. Res. 21:1.
35. Mayes, P., 1993. The pentose phosphate pathway & other pathways of hexose metabolism. In Harper's Biochemistry. 23th Ed. R. Murray, D. Granner, P. Mayes, and V. Rodwell, eds. Appleton & Lange, Norwalk, CT, p. 201.
36. Wood, T. 1985. The Pentose Phosphate Pathway. Academic Press, New York.
37. Heinrich, P. C., H. P. Morris, and G. Weber. 1976. Behavior of transaldolase (EC 2.2.1.2.) and transketolase (EC 2.2.1.1.) in normal neoplastic, differentiating, and regenerating liver. Cancer Res. 36:3189.
38. Banki, K., D. Halladay, and A. Perl. 1994. Cloning and expression of the human gene for transaldolase: a novel highly repetitive element constitutes an integral part of the coding sequence. J. Biol. Chem. 269:2847.
39. Novello, F., and P. McLean. 1968. The pentosc phosphate pathway of glucose metabolism: measurements of the nonoxidative reactions of the cycle. Biochem. J. 107:775.
40. Banki, K., E. Colombo, F. Sia, D. Halladay, D. Mattson, A. Tatum, P. Massa, P. E. Phillips, and A. Perl. 1994. Oligodendrocyte-specific expression and auloantigenicity of transaldolase in multiple sclerosis. J. Exp. Med. 180:1649.
41. Baquer, N. Z., J. S. Hothersall, P. McLean, and A. L. Greenbaum. 1977. Aspects of carbohydrate metabolism in developing brain. Dev. Med. Child Neurol. 19:81.
42. Ni, T., and M. A. Savageau. 1996. Application of biochemical systems theory to metabolism in human red blood cells: signal propagation and accuracy of representation. J. Biol. Chem. 271:7927.
43. + T-cell subsets in lectin-dependent cell-mediated cytotoxicity against adherent HEp-2 cells. Cell. Immunol. 84:185.
44. Yonehara, S., A. Ishii, and M. Yonehara. 1989. A cell-killing monoclonal antibody (anti-Fas) to a cell surface antigen co-downregulated with the receptor of tumor necrosis factor. J. Exp. Med. 169:1747.
45. Itoh, N., S. Yonehara, A. Ashii, M. Yonehara, S. Mizushima, M. Sameshima, A. Hase, Y. Seto, and S. Nagata. 1991. The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell 66:233.
46. Trauth, B. C., C. Klas, A. M. J. Peters, S. Matzku, P. Moller, W. Falk, K. Debatin, and P. H. Krammer. 1989. Monoclonal antibody-mediated tumor regression by induction of apoptosis. Science 245:301.
47. Vermes, I., C. Haanen, H. Steffens-Nakken, and C. Reutelingsperger. 1995. A novel assay for apoptosis: flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled annexin V. J. Immunol. Methods 184:39.
48. Martin, S. J., C. P. M. Reutelingsperger, A. J. McGahon, J. A. Rader, C. A. A. van Schie, D. M. LaFace, and D. R. Green. 1995 Early redistribution of plasma membrane pbosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J. Exp. Med. 182:1545.
49. Burow, S., and G. Valet. 1987. Flow-cytometric characterization, free radical formation, peroxidase activity and phagocytosis of human granulocytes with 2,7-dichlorofluorescein (DCF). Eur. J. Cell. Biol. 43:128.
50. 2 in cultured endothelial cells. Arch. Biochem. Biophys. 302:348.
51. Petit, P. X., J. E. O'Connor, D. Grunwald, and S. C. Brown. 1990. Analysis of the membrane potential of rat- and mouse-liver mitochondria by flow cytometry and possible applications. Eur. J. Biochem. 194:389.
52. Tanner, M. K., S. R. Wellhausen, and J. B. Klein. 1993. Flow cytometric analysis of altered mononuclear cell transmembrane potential induced by cyclosporin. Cytometry 14:59.
53. Zamzami, N., P. Marchetti, M. Castedo, D. Decaudin, A. Macho, T. Hirsch, S. A. Susin, P. X. Petit, B. Mignotte, and G. Kroemer. 1995. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J. Exp. Med. 182:367.
54. L regulates the membrane potential and volume homeostasis of mitochondria. Cell 91:627.
55. Smiley, S. T., M. Reers, C. Mottola-Hartshorn, M. Lin, A. Chen, T. W. Smith, G. D. Steele, Jr., and L. Bo Chen. 1991. Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming cation JC-1. Proc. Natl. Acad. Sci. USA 88:3671.
56. Cossarizza, A., C. Franceschi, D. Monti, S. Salvioli, E. Bellesia, R. Rivabene, L. Biondo, G. Rainaldi, A. Tinari, and W. Malorni. 1995. Protective effect of N-acetylcysteine in tumor necrosis factor-α-induced apoptosis in U937 cells: the role of mitochondria. Exp. Eye Res. 220:232.
57. Brauner, T., D. F. Hulser, and R. J. Strasser. 1984. Comparative measurements of membrane potentials with microelectrodes and voltage-sensitive dyes. Biochim. Biophys. Acta 771:208.
58. Pontremoli, S., D. B. Prandini, A. Bonsignore, and B. L. Horecker. 1961. The preparation of crystalline transaldolase from Candida utilis. Proc. Natl. Acad. Sci. USA 47:1942.
59. Rudack, D., E. M. Chisholm, and D. Holten. 1971. Rat liver glucose 6-phosphate dehydrogenase. J. Biol. Chem. 246:1249.
60. Tietze, F. 1969. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal. Biochem. 27:502.
61. Lowry, O. H., N. J. Rosebrough, A. L. Fair, and R. J. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265.
62. Nicholson, D. W., A. Ali, N. A. Thornberry, J. P. Vaillancourt, C. K. Ding, M. Gallant, Y. Gareau, P. R. Griffin, M. Labelle, Y. A. Lazebnik, et al. 1995. Identification and inhibition of ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376:37.
63. Kluck, R. M., E. Bossy-Wetzel, D. R. Green, and D. D. Newmeyer. 1997. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoplosis. Science 275:1132.
64. Armstrong, R. C., T. Aja, J. Xiang, S. Gaur, J. F. Krebs, K. Hoang, X. Bai, S. J. Korsmeyer, D. S. Karanevsky, L. C. Fritz, et al. 1996. Fas-induced activation of the cell death-related protease CPP32 is inhibited by Bcl-2 and by ICE family protease inhibitors. J. Biol. Chem. 271:16850.
65. Towbin, H. H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylarnide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76:4350.
66. Lamarre, D., B. Talbot, G. De Murcia, C. LaPlante, Y. LeDuc, A. Mazen, and G. G. Poirier. 1988. Structural and functional analysis of poly(ADP-ribose) polymerase: an immunological study. Biochim. Biophys. Acta 950:147.
67. Packham, G., R. A. Ashmun, and J. L. Cleveland. 1996. Cytokines suppress apoptosis independent of increases in reactive oxygen levels. J. Immunol. 156: 2792.
68. Susin, S. A., N. Zamzami, M. Castedo, E. Daugas, H. Wang, S. Geley, F. Fassy, R. C. Reed, and G. Kroemer. 1997. The central executioner of apoptosis: multiple connections between protease activation and mitochondria in Fas/Apo-1/CD95- and ceramide-induced apoptosis. J. Exp. Med. 186:25.
69. Enari, M., R. V. Talanian, W. W. Wong, and S. Nagata. 1996. Sequential activation of ICE-like and CPP32-like proteases during Fas-mediated apoptosis. Nature 380:723.
70. Constantini, P., B. V. Chernyak, V. Petronilli, and P. Bernardt. 1996. Modulation of the mitochondrial permeability transition pore by pyridine nucleotides and dithiol oxidation at two separate sites. J. Biol. Chem. 271:6746.
71. Muzio, M., B. R. Stockwell, H. R. Stennicke, G. S. Salvesen, and V. M. Dixit. 1998. An induced proximity model for caspase-8 activation. J. Biol. Chem. 273: 2926.
72. Tewari, M., L. T. Quan, K. O'Rourke, S. Desnoyers, Z. Zeng, D. R. Beidler, G. G. Poirier, G. S. Salvesen, and V. M. Dixit. 1995. Yama/CPP32β. a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 81:801.
73. Scaffidi, C., J. P. Medema, P. H. Krammer, and M. E. Peter. 1997. Flice is predominantly expressed as two functionally active isoforms, caspase-8/a and caspase-8/b. J. Biol. Chem. 272:26953.
74. Salvesen, G. S., and V. M. Dixit. 1997. Caspases: intracellular signaling by proteolysis. Cell 91:443.
75. Li, P., D. Nijhawan, I. Budihardjo, S. M. Srinivasula, M. Ahmad, E. S. Alnemri, and X. Wang. 1997. Cytochrome c and dATP-dependent formation of Apaf-1/ caspase-9 complex initiates and apoptotic protease cascade. Cell 91:479.
76. Casciola-Rosen, L. A., D. K. Miller, G. J. Anhalt, and A. Rosen. 1994. Specific cleavage of the 70 kDa prolein component of the U1 small nuclear ribonucleoprotein is a characteristic biochemical feature of apoptolic cell death. J. Biol. Chem. 269:30757.
77. Casciola-Rosen, L., D. W. Nicholson, T. Chong, K. R. Rowan, N. A. Thornberry, D. K. Miller, and A. Rosen. 1996. Apopain/CPP32 cleaves proteins that are essential for cellular repair: a fundamental principle of apoptotic cell death. J. Exp. Med. 183:1957.
78. Enari, M., H. Sakahira, H. Yokoyama, K. Okawa, A. Iwamatsu, and S. Nagata, 1998. A capase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 391:43.
79. Zoratti, M., and I. Szabo. 1995. The mitochondrial permeability transition. Biochim. Biophys. Acta 1241:139.
80. 6 or rhodamine 123, is a reliable fluorescent probe to assess Δψ changes in intact cells: implications for studies on mitochondrial functionality during apoptosis. FEBS Lett. 411:77.
81. Adachi, S., R. A. Gottlieb, and B. M. Babior. 1998. Lack of release of cytochrome c from mitochondria into cytosol early in the course of Fas-mediated apoptosis of Jurkat cells. J. Biol. Chem. 273:19892.
82. Mysler, E., P. Bini, J. Drappa, P. Ramos, S. M. Friedman, P. H. Krammer, and K. B. Elkon. 1994. The apoptosis-1/Fas protein in human systemic lupus crythematosus. J. Clin. Invest. 93:1029.
83. Suthanthiran, M., M. E. Anderson, V. K. Sharma, and A. Meister. 1990. Glutathione regulates activation-dependent DNA synthesis in highly purified normal human T lymphocytes stimulated via the CD2 and CD3 antigens. Proc. Natl. Acad. Sci. USA 87:3343.
84. Martin, D. A., R. M. Siegel, L. Zheng, and M. J. Lenardo. 1998. Membrane oligomerization and cleavage activates the caspase-8 (FLICE/MACHα1) death signal. J. Biol. Chem. 273:4345.
85. Banki, K., E. Hutler, N. J. Gonchoroff, and A. Perl. 1998. Molecular ordering in HIV-induced apoptosis: oxidative stress, activation of Caspases, and cell survival are regulated by transaldolase. J. Biol. Chem. 273:11944.
86. Berridge, M. V., A. S. Tan, K. D. McCoy, M. Kansara, and F. Rudert. 1996. CD95 (Fas/Apo-1)-induced apoptosis results in loss of glucose transporter function. J. Immunol. 156:4092.