Bz-423 superoxide signals apoptosis via selective activation of JNK, Bak, and Bax

Free Radical Biology and Medicine

Volumn 45, Issue 9, 2008, Pages 1232-1242

  Blatt, Neal B ^a   Boitano, Anthony E ^b   Lyssiotis, Costas A ^b   Opipari Jr , Anthony W ^a   Glick, Gary D ^b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Apoptosis; Bak; Bax; Bcl 2; Benzodiazepine; Bz 423; JNK; Mitochondria; Superoxide

Indexed keywords

ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; APOPTOSIS SIGNAL REGULATING KINASE 1; BENZODIAZEPINE DERIVATIVE; BZ 423; CYTOCHROME C; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN BAK; PROTEIN BAX; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE INHIBITOR; SUPEROXIDE; THIOREDOXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL TYPE; DRUG SELECTIVITY; EMBRYO; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; MEMBRANE PERMEABILITY; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN TRANSPORT; RESPIRATORY CHAIN; SIGNAL TRANSDUCTION; TREATMENT RESPONSE;

ANIMALS; APOPTOSIS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; BENZODIAZEPINES; DIPLOIDY; DNA; MAP KINASE KINASE 4; MAP KINASE KINASE KINASE 5; MEMBRANE POTENTIALS; MICE; MICE, TRANSGENIC; MITOCHONDRIA; MODELS, BIOLOGICAL; SUPEROXIDES;

MURINAE;

EID: 53449087685     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2008.07.022     Document Type: Article

References (73)

1. Blatt N.B., Bednarski J.J., Warner R.E., Leonetti F., Johnson K.M., Boitano A., Yung R., Richardson B.C., Johnson K.J., Ellman J.A., Opipari A.W., and Glick G.D. Benzodiazepine-induced superoxide signals B cell apoptosis: mechanistic insight and potential therapeutic utility. J. Clin. Invest. 110 (2002) 1123-1132
2. Bednarski J.J., Warner R.E., Rao T., Leonetti F., Yung R., Richardson B.C., Johnson K.J., Ellman J.A., Opipari A.W., and Glick G.D. Attenuation of autoimmune disease in Fas-deficient mice by treatment with a cytotoxic benzodiazepine. Arthritis Rheum. 48 (2003) 757-766
3. Bhagavathula N., Nerusu K.C., Hanosh A., Aslam M.N., Sundberg T.B., Opipari A.W., Johnson K., Kang S., Glick G.D., and Varani J. Bz-423, a benzodiazepine, suppresses keratinocyte proliferation and has anti-psoriatic activity in the human skin-SCID mouse transplant model. J. Pharmacol. Exp. Ther. 324 (2008) 938-947
4. 0-ATPase as the molecular target of the immunomodulatory benzodiazepine Bz-423. Chem. Biol. 12 (2005) 485-496
5. Green D.R., and Kroemer G. Pharmacological manipulation of cell death: clinical applications in sight?. J. Clin. Invest. 115 (2005) 2610-2617
6. Wei M.C., Zong W.-X., Cheng E.H.-Y., Lindsten T., Panoutsakopoulou V., Ross A.J., Roth K.A., MacGregor G.R., Thompson C.B., and Korsmeyer S.J. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292 (2001) 727-730
7. Bunin B.A., Plunkett M.J., and Ellman J.A. The combinatorial synthesis and chemical and biological evaluation of a 1,4-benzodiazepine library. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 4708-4712
8. Fink B., Laude K., McCann L., Doughan A., Harrison D.G., and Dikalov S. Detection of intracellular superoxide formation in endothelial cells and intact tissues using dihydroethidium and an HPLC-based assay. Am. J. Physiol. Cell. Physiol. 287 (2004) C895-C902
9. Bouchier-Hayes L., Lartrigue L., and Newmeyer D.D. Mitochondria: pharmacological manipulation of cell death. J. Clin. Invest. 115 (2005) 2640-2647
10. Patel M., and Day B.J. Metalloporphyrin class of therapeutic catalytic antioxidants. Trends Pharmacol. Sci. 20 (1999) 359-364
11. Beckman J.S., Minor R.L., White C.W., Repine J.E., Rosen G.M., and Freeman B.A. Superoxide dismutase and catalase conjugated to polyethylene glycol increases endothelial enzyme activity and oxidant resistance. J. Biol. Chem. 263 (1988) 6884-6892
12. Giles G.I. The redox regulation of thiol dependent signaling pathways in cancer. Curr. Pharm. Des. 12 (2006) 4427-4443
13. Bailey H.H. L-S,R-buthionine sulfoximine: historical development and clinical issues. Chem. Biol. Interact. 111-112 (1998) 239-254
14. 2-terminal kinase and up-regulation of death receptors. Cancer Res. 66 (2006) 11416-11423
15. Morales M., Perez-Yarza G., Nieto-Rementeria N., Boyano M.D., Jangi M., Atencia R., and Asumendi A. Intracellular glutathione levels determine cell sensitivity to apoptosis induced by the antineoplastic agent N-(4-hydroxyphenyl) retinamide. Anticancer Res. 25 (2005) 1945-1951
16. Chipuk J.E., Bouchier-Hayes L., and Green D.R. Mitochondrial outer membrane permeabilization during apoptosis: the innocent bystander scenario. Cell Death Differ. 13 (2006) 1396-1402
17. Festjens N., Vanden Berghe T., and Vandenabeele P. Necrosis, a well-orchestrated form of cell demise: signalling cascade, important mediators and concomitant immune response. Biochim. Biophys. Acta 1757 (2006) 1371-1387
18. Weston C.R., and Davis R.J. The JNK signal transduction pathway. Curr. Opin. Cell Biol. 19 (2006) 142-149
19. Shen H.-M., and Liu Z. JNK signaling is a key modulator in cell death mediated by reactive oxygen and nitrogen species. Free Radic. Biol. Med. 40 (2006) 928-939
20. Matsuzawa, A.; Ichijo, H., Redox control of cell fate by MAP kinase: physiological roles of ASK1-MAP kinase pathway in stress signaling. Biochim. Biophys. Acta:doi:10.1016/j.bbagen.2007.1012.1011; 2008.
21. Davis R.J. Signal transduction by the JNK group of MAP kinases. Cell 103 (2000) 239-252
22. Tobiume K., Matsuzawa A., Takahashi T., Nishitoh H., Morita K., Takeda K., Minowa O., Miyazono K., Noda T., and Ichijo H. ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep. 2 (2001) 222-228
23. Bennett B.L., Sasaki D.T., Murray B.W., O'Leary E.C., Sakata S.T., Xu W., Leisten J.C., Motiwala A., Pierce S., Satoh Y., Bhagwat S.S., Manning A.M., and Anderson D.W. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 13681-13686
24. Korshunov S.S., Skulachev V.P., and Starkov A.A. High protonic potential actuates a mechanism of production of reactive oxygens species in mitochondria. FEBS Lett. 416 (1997) 15-18
25. Tirosh O., Aronis A., and Melendez J.A. Mitochondrial state 3 to 4 respiration transition during Fas-mediated apoptosis controls cellular redox balance and rate of cell death. Biochem. Pharmacol. 66 (2003) 1331-1334
26. 2+ signaling. Am. J. Physiol. Cell. Physiol. 291 (2006) C1082-C1088
27. Skulachev V.P. Bioenergetic aspects of apoptosis, necrosis, and mitoptosis. Apoptosis 11 (2006) 473-485
28. Turrens J.F. Mitochondrial formation of reactive oxygen species. J. Physiol. 552 (2003) 335-344
29. Valko M., Leibfritz D., Moncol J., Cronin M.T.D., Mazur M., and Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 39 (2007) 44-84
30. Schumacker P.T. Reactive oxygen species in cancer cells: live by the sword, die by the sword. Cancer Cell 10 (2006) 175-176
31. Liu Q., Wilkins B.J., Lee Y.J., Ichijo H., and Molkentin J.D. Direct interaction and reciprocal regulation between ASK1 and calcineurin-NFAT control cardiomyocyte death and growth. Mol. Cell. Biol. 26 (2006) 3785-3797
32. Fujino G., Noguchi T., Matsuzawa A., Yamauchi S., Saitoh M., Takeda K., and Ichijo H. Thioredoxin and TRAF family proteins regulate reactive oxygen species-dependent activation of ASK1 through reciprocal modulation of the N-terminal homophilic interaction of ASK1. Mol. Cell. Biol. 27 (2007) 8152-8163
33. Matsukawa J., Matsuzawa A., Takeda K., and Ichijo H. The ASK1-MAP kinase cascades in mammalian stress response. J. Biochem. (Tokyo) 136 (2004) 261-265
34. Hansen J.M., Zhang H., and Jones D.P. Differential oxidation of thioredoxin-1, thioredoxin-2, and glutathione by metal ions. Free Radic. Biol. Med. 40 (2006) 138-145
35. Hsieh C.-C., and Papaconstantinou J. Thioredoxin-ASK1 complex levels regulate ROS-mediated p38 MAPK pathway activity in livers of aged and long-lived Snell dwarf mice. FASEB J. 20 (2006) 259-268
36. Matsuura H., Nishitoh H., Takeda K., Matsuzawa A., Amagasa T., Ito M., Yoshioka K., and Ichijo H. Phosphorylation-dependent scaffolding role of JSAP1/JIP3 in the ASK1-JNK signaling pathway. J. Biol. Chem. 277 (2002) 40703-40709
37. 2-terminal kinase signaling pathway by the WD-repeat protein Gemin5. Cell Death Differ. 14 (2007) 1518-1528
38. Owens D.M., and Keyse S.M. Differential regulation of MAP kinase signalling by dual-specificity protein phosphatases. Oncogene 26 (2007) 3203-3213
39. Mendelson K.G., Contois L.-R., Tevosian S.G., Davis R.J., and Paulson K.E. Independent regulation of JNK/p38 mitogen-activated protein kinases by metabolic oxidative stress in the liver. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 12908-12913
40. Rebouças J.S., Spasojevic I., and Batinic-Haberle I. Pure manganse(III) 5,10,15,20-tetrakis(4-benzoic acid)porphyrin (MnTBAP) is not a superoxide dismutase mimic in aqueous systems: a case of structure-activity relationship as a watchdog mechanism in experimental therapeutics and biology. J. Biol. Inorg. Chem. 13 (2008) 289-302
41. Benrahmoune M., Therond P., and Abendinzadeh Z. The reaction of superoxide radical with N-acetylcysteine. Free Radic. Biol. Med. 29 (2000) 775-782
42. Winterbourn C.C., and Metodiewa D. Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxide. Free Radic. Biol. Med. 27 (1999) 322-328
43. Du J., Suzuki H., Nagase F., Akhand A.A., Ma X.-Y., Yokoyama T., Miyata T., and Nakashima I. Superoxide-mediated early oxidation and activation of ASK1 are important for initiating methylglyoxal-induced apoptosis process. Free Radic. Biol. Med. 31 (2001) 469-478
44. Chiang E., Dang O., Anderson K., Matsuzawa A., Ichijo H., and David M. Apoptosis-regulating signal kinase 1 is required for reactive oxygen species-mediated activation of IFN regulatory factor 3 by lipopolysaccharide. J. Immunol. 176 (2006) 5720-5724
45. Liu H., Zhang H., Iles K.E., Rinna A., Merrill G., Yodoi J., Torres M., and Forman H.J. The ADP-stimulated NADPH oxidase activates the ASK-1/MKK4/JNK pathway in alveolar macrophages. Free Radic. Res. 40 (2006) 865-874
46. Han D., Antunes F., Canali R., Rettori D., and Cadenas E. Voltage-dependent anion channels control the release of the superoxide anion from mitochondria to cytosol. J. Biol. Chem. 278 (2003) 5557-5563
47. Tsuruta F., Sunayama J., Mori Y., Hattori S., Shimizu S., Tsujimoto Y., Yoshioka K., Masuyama N., and Gotoh Y. JNK promotes Bax translocation to mitochondria through phosphorylation of 14-3-3 proteins. EMBO J. 23 (2004) 1889-1899
48. Kim B.-J., Ryu S.-W., and Song B.-J. JNK- and p38 kinase-mediated phosphorylation of Bax leads to its activation and mitochondrial translocation and to apoptosis of human hepatoma HepG2 cells. J. Biol. Chem. 281 (2006) 21256-21265
49. Zoratti M., and Szabo I. The mitochondrial permability transition. Biochim. Biophys. Acta 1241 (1995) 139-176
50. Madesh M., and Hajnóczky G. VDAC-dependent permeabilization of the outer mitochondrial membrane by superoxide induces rapid and massive cytochrome c release. J. Cell Biol. 155 (2001) 1003-1015
51. Costantini P., Belzacq A.-S., Vieira H.L.A., Larochette N., de Pablo M.A., Zamzami N., Susin S.A., Brenner C., and 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
52. Watabe M., and Nakaki T. ATP depletion does not account for apoptosis induced by inhibition of mitochondrial electron transport chain in human dopaminergic cells. Neuropharmacology 52 (2007) 536-541
53. Lim P.L., Liu J., and Boelsterli U.A. The mitochondrial superoxide/thioredoxin-2/Ask1 signaling pathway is critically involved in troglitazone-induced cell injury to human hepatocytes. Toxicol. Sci. 101 (2008) 341-349
54. Dvorakova K., Payne C.M., Tome M.E., Briehl M.M., McClure T., and Dorr R.T. Induction of oxidative stress and apoptosis in myeloma cells by the aziridine-containing agent imexon. Biochem. Pharmacol. 60 (2000) 749-758
55. Dvorakova K., Waltmire C.N., Payne C.M., Tome M.E., Briehl M.M., and Dorr R.T. Induction of mitochondrial changes in myeloma cells by imexon. Blood 97 (2001) 3544-3551
56. Iyengar B.S., Dorr R.T., and Remers W.A. Chemical basis for the biological activity of imexon and related cyanoaziridines. J. Med. Chem. 47 (2004) 218-223
57. 0 part of H+-ATP-synthase, suppresses the TNF-induced apoptosis. Oncogene 21 (2002) 8149-8157
58. +-ATPase. J. Biol. Chem. 280 (2005) 33115-33122
59. Homareda H., Ishii T., and Takeyasu K. Binding domain of oligomycin on Na(+),K(+)-ATPase. Eur. J. Pharmacol. 400 (2000) 177-183
60. 0-ATPase. ACS Chem. Biol. 1 (2006) 304-308
61. Saito Y., Nishio K., Ogawa Y., Kimata J., Kinumi T., Yoshida Y., Noguchi N., and Niki E. Turning point in apoptosis/necrosis induced by hydrogen peroxide. Free Radic. Res. 40 (2006) 619-630
62. Eguchi Y., Shimizu S., and Tsujimoto Y. Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res. 57 (1997) 1835-1840
63. Gong Y., Sohn H., Xue L., Firestone G.L., and Bjeldanes L.F. 3,3′-diindolylmethane is a novel mitochondrial H+-ATP synthase inhibitor that can induce p21Cip1/Waf1 expression by induction of oxidative stress in human breast cancer cells. Cancer Res. 66 (2006) 4880-4887
64. Nachshon-Kedmi M., Yannai S., and Fares F.A. Induction of apoptosis in human prostate cancer cell line, PC3, by 3,3′-diindolylmethane through the mitochondrial pathway. Br. J. Cancer 91 (2004) 1358-1363
65. Chen I., McDougal A., Wang F., and Safe S. Aryl hydrocarbon receptor-mediated antiestrogenic and antitumorigenic activity of diindolylmethane. Carcinogenesis 19 (1998) 1631-1639
66. Wattenberg L.W., and Loub W.D. Inhibition of polycyclic aromatic hydrocarbon-induced neoplasia by naturally occurring indoles. Cancer Res. 38 (1978) 1410-1413
67. Armstrong J.S. Mitochondrial medicine: pharmacological targeting of mitochondria in disease. Br. J. Pharmacol. 151 (2007) 1154-1165
68. Van Remmen H., Salvador C., Yang H., Huang T.T., Epstein C.J., and Richardson A. Characterization of the antioxidant status of the heterozygous manganese superoxide dismutase knockout mouse. Arch. Biochem. Biophys. 363 (1999) 91-97
69. 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
70. Davison K., Cote S., Mader S., and Miller W.H. Glutathione depletion overcomes resistance to arsenic trioxide in arsenic-resistant cell lines. Leukemia 17 (2003) 931-940
71. Maeda H., Hori S., Ohizumi H., Segawa T., Kakehi Y., Ogawa O., and Kakizuka A. Effective treatment of advanced solid tumors by the combination of arsenic trioxide and L-buthionine-sulfoximine. Cell Death Differ. 11 (2004) 737-746
72. Aouadi M., Binetruy B., Caron L., Le Marchand-Brustel Y., and Bost F. Role of MAPKs in development and differentiation: lessons from knockout mice. Biochimie 88 (2006) 1091-1098
73. Bednarski J.J., Lyssiotis C.A., Roush R., Boitano A., Glick G.D., and Opipari A.W. A novel benzodiazepine increase the sensitivity of B cells to receptor stimulation with synergistic effects on calcium signaling and apoptosis. J. Biol. Chem. 279 (2004) 29615-29621