Induction of apoptosis without redox catastrophe by thioredoxin-inhibitory compounds

Biochemical Pharmacology

Volumn 66, Issue 9, 2003, Pages 1695-1705

  Pallis, Monica ^a   Bradshaw, Tracey D ^a   Westwell, Andrew D ^a   Grundy, Martin ^a   Stevens, Malcolm F G ^a   Russell, Nigel ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Apoptosis; AW 464; Diamide; Phenylarsine oxide; Thioredoxin

Indexed keywords

ARSENOSOBENZENE; AW 464; CYTOCHROME C; DIAMIDE; DITHIOL DERIVATIVE; DNA; FREE RADICAL; HYDROGEN PEROXIDE; LIGAND; PHOSPHATIDYLSERINE; PROTEIN BAK; PROTEIN INHIBITOR; REACTIVE OXYGEN METABOLITE; THIOREDOXIN INHIBITOR; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL ACTIVITY; CELL FREE SYSTEM; CELL STRAIN; CHROMATIN CONDENSATION; CONTROLLED STUDY; DETOXIFICATION; HUMAN; HUMAN CELL; MITOCHONDRION; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL;

EID: 0141922903     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-2952(03)00471-4     Document Type: Article

References (40)

1. Webb J. Enzyme and metabolic inhibitors, vol. III. New York: Academic press, 1966.
2. Marchetti P., Decaudin D., Macho A., Zamzami N., Hirsch T., Susin S.A., Kroemer G. Redox regulation of apoptosis: impact of thiol oxidation status on mitochondrial function. Eur. J. Immunol. 27:1997;289-296.
3. Costantini P., Jacotot E., Decaudin D., Kroemer G. Mitochondrion as a novel target of anticancer chemotherapy. J. Natl. Cancer Inst. 92:2000;1042-1053.
4. Pallis M., Grundy M., Turzanski J., Kofler R., Russell N. Mitochondrial membane sensitivity to depolarisation in acute myeloblastic leukemia is associated with spontaneous in vitro apoptosis, wild-type TP53 and vicinal thiol/disulfide status. Blood. 98:2001;405-413.
5. Zamzami N., Marzo I., Susin S.A., Brenner C., Larochette N., Marchetti P., Reed J., Kofler R., Kroemer G. The thiol crosslinking agent diamide overcomes the apoptosis-inhibitory effect of Bcl-2 by enforcing mitochondrial permeability transition. Oncogene. 16:1998;1055-1063.
6. Nakamura H., Nakamura K., Yodoi J. Redox regulation of cellular activation. Annu. Rev. Immunol. 15:1997;351-369.
7. Powis G., Mustacich D., Coon A. The role of the redox protein thioredoxin in cell growth and cancer. Free Radic Biol. Med. 29:2000;312-322.
8. Nordberg J., Arner E.S. Reactive oxygen species, antioxidants, and the mammalian thioredoxin system (1). Free Radic. Biol. Med. 31:2001;1287-1312.
9. Holmgren A. Reduction of disulfides by thioredoxin. Exceptional reactivity of insulin and suggested functions of thioredoxin in mechanism of hormone action. J. Biol. Chem. 254:1979;9113-9119.
10. Yokomizo A., Ono M., Nanri H., Makino Y., Ohga T., Wada M., Okamoto T., Yodoi J., Kuwano M., Kohno K. Cellular levels of thioredoxin associated with drug sensitivity to cisplatin, mitomycin C, doxorubicin, and etoposide. Cancer Res. 55:1995;4293-4296.
11. Baker A., Payne C.M., Briehl M.M., Powis G. Thioredoxin, a gene found overexpressed in human cancer, inhibits apoptosis in vitro and in vivo. Cancer Res. 57:1997;5162-5167.
12. Becker K., Gromer S., Schirmer R.H., Muller S. Thioredoxin reductase as a pathophysiological factor and drug target. Eur. J. Biochem. 267:2000;6118-6125.
13. Lenaz G. Role of mitochondria in oxidative stress and ageing. Biochim. Biophys. Acta. 1366:1998;53-67.
14. Nicotera P., Leist M., Ferrando-May E. Intracellular ATP, a switch in the decision between apoptosis and necrosis. Toxicol. Lett. 102/103:1998; 139-142.
15. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 341:1999;233-249.
16. 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 (ASK) 1. Embo. J. 17:1998;2596-2606.
17. Wells G., Bradshaw T.D., Diana P., Seaton A., Shi D.F., Westwell A.D., Stevens M.F.G. Antitumour benzothiazoles. Part 10. The synthesis and antitumour activity of benzothiazole substituted quinol derivatives. Bioorg. Med. Chem. Lett. 10:2000;513-515.
18. Wells G., Berry J.M., Bradshaw T.D., Burger A.M., Seaton A., Wang B., Westwell A.D., Stevens M.F.G. 4-Substituted 4-hydroxycyclohexa-2-5-dien-1-ones with selective activities against colon and renal cancer cell lines. J. Med. Chem. 46:2003;532-541.
19. Park E.M., Thomas J.A. The mechanisms of reduction of protein mixed disulfides (dethiolation) in cardiac tissue. Arch. Biochem. Biophys. 274:1989;47-54.
20. Sato N., Iwata S., Nakamura K., Hori T., Mori K., Yodoi J. Thiol-mediated redox regulation of apoptosis. Possible roles of cellular thiols other than glutathione in T cell apoptosis. J. Immunol. 154:1995;3194-3203.
21. Bogumil R., Ullrich V. Phenylarsine oxide affinity chromatography to identify proteins involved in redox regulation: dithiol-disulfide equilibrium in serine/threonine phosphatase calcineurin. Methods Enzymol. 348:2002;271-280.
22. Kunkel M., Kirkpatrick D., Johnson J., Powis G. Cell-line-directed screening assay for inhibitors of thioredoxin reductase signaling as potential anti-cancer drugs. Anti Cancer Drug Design. 12:1997;659-670.
23. Rothe G., Valet G. Flow cytometric analysis of respiratory burst activity in phagocytes with hydroethidine and 2′,7′ -dichlorofluorescin. J. Leukoc. Biol. 47:1990;440-448.
24. Zamzami N., Marchetti P., Castedo M., Decaudin D., Macho A., Hirsch T., Susin S.A., Petit P.X., Mignotte B., Kroemer G. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J. Exp. Med. 182:1995;367-377.
25. 2 in cultured endothelial cells. Arch. Biochem. Biophys. 302:1993;348-355.
26. Griffiths G.J., Dubrez L., Morgan C.P., Jones N.A., Whitehouse J., Corfe B.M., Dive C., Hickman J.A. Cell damage-induced conformational changes of the pro-apoptotic protein Bak in vivo precede the onset of apoptosis. J. Cell. Biol. 144:1999;903-914.
27. Westwell A.D., Wells G., Berry J.M., Bradshaw T.D., Burger A.M., Matthews C.S., Monks A., Stevens M.F.G. Synthesis of heteroaromatic quinols, novel agents with selective activity clustered in colon and renal cell lines. Proc. Am. Assoc. Cancer Res. 43:2002;1034.
28. Collison M.W., Beidler D., Grimm L.M., Thomas J.A. A comparison of protein S-thiolation (protein mixed-disulfide formation) in heart cells treated with t-butyl hydroperoxide or diamide. Biochim. Biophys. Acta. 885:1986;58-67.
29. Waterhouse N.J., Goldstein J.C., von Ahsen O., Schuler M., Newmeyer D.D., Green D.R. Cytochrome c maintains mitochondrial transmembrane potential and ATP generation after outer mitochondrial membrane permeabilization during the apoptotic process. J. Cell. Biol. 153:2001;319-328.
30. Wang G.Q., Gastman B.R., Wieckowski E., Goldstein L.A., Gambotto A., Kim T.H., Fang B., Rabinovitz A., Yin X.M., Rabinowich H. A role for mitochondrial Bak in apoptotic response to anticancer drugs. J. Biol. Chem. 276:2001;34307-34317.
31. Hirota K., Murata M., Sachi Y., Nakamura H., Takeuchi J., Mori K., Yodoi J. Distinct roles of thioredoxin in the cytoplasm and in the nucleus. A two-step mechanism of redox regulation of transcription factor NF-kappaB. J. Biol. Chem. 274:1999;27891-27897.
32. Backway K.L., McCulloch E.A., Chow S., Hedley D.W. Relationships between the mitochondrial permeability transition and oxidative stress during ara-C toxicity. Cancer Res. 57:1997;2446-2451.
33. Gamen S., Anel A., Perez-Galan P., Lasierra P., Johnson D., Pineiro A., Naval J. Doxorubicin treatment activates, and apoptosis in Jurkat cells a Z-VAD-sensitive caspase, which causes deltapsim loss, caspase-9 activity. Exp. Cell. Res. 258:2000;223-235.
34. Liu F.T., Kelsey S.M., Newland A.C., Jia L. Generation of reactive oxygen species is not involved in idarubicin-induced apoptosis in human leukaemic cells. Br. J. Haematol. 115:2001;817-825.
35. Kantrow S.P., Piantadosi C.A. Release of cytochrome c from liver mitochondria during permeability transition. Biochem. Biophys. Res. Commun. 232:1997;669-671.
36. Freeman M.L., Meredith M.J. Modulation of diamide toxicity in thermotolerant cells by inhibition of protein synthesis. Cancer Res. 49:1989;4493-4498.
37. Halestrap A.P., Woodfield K.Y., Connern C.P. Oxidative stress, thiol reagents, and membrane potential modulate the mitochondrial permeability transition by affecting nucleotide binding to the adenine nucleotide translocase. J. Biol. Chem. 272:1997;3346-3354.
38. Costantini P., Belzacq A.S., Vieira H.L., Larochette N., de Pablo M.A., Zamzami N., Susin S.A., Brenner C., Kroemer G. Oxidation of a critical thiol residue of the adenine nucleotide translocator enforces Bcl-2-independent permeability transition pore opening and apoptosis. Oncogene. 19:2000;307-314.
39. Hirsch T., Marchetti P., Susin S.A., Dallaporta B., Zamzami N., Marzo I., Geuskens M., Kroemer G. The apoptosis-necrosis paradox. Apoptogenic proteases activated after mitochondrial permeability transition determine the mode of cell death. Oncogene. 15:1997;1573-1581.
40. Gurtu V., Kain S.R., Zhang G. Fluorometric and colorimetric detection of caspase activity associated with apoptosis. Anal. Biochem. 251:1997;98-102.