Hsp90 cleavage by an oxidative stress leads to its client proteins degradation and cancer cell death

Biochemical Pharmacology

Volumn 77, Issue 3, 2009, Pages 375-383

  Beck, Raphael ^a   Verrax, Julien ^a   Gonze, Thomas ^a   Zappone, Marianne ^a   Pedrosa, Rozangela Curi ^b   Taper, Henryk ^a   Feron, Olivier ^a   Calderon, Pedro Buc ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

Author keywords

Ascorbate driven menadione redox cycling; Bcr Abl oncogene; Chronic myeloid leukemia (CML); K562 cells; Oxidative stress; Protein chaperone Hsp90

Indexed keywords

ANTIBODY; ASCORBIC ACID; BCR ABL PROTEIN; GLUCOSE; GLUCOSE OXIDASE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 ALPHA; HEAT SHOCK PROTEIN 90 BETA; HYDROGEN PEROXIDE; ISOPROTEIN; MENADIONE; PROTEIN DERIVATIVE; PROTEIN KINASE B; RECEPTOR INTERACTING PROTEIN; TANESPIMYCIN; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; CANCER CELL CULTURE; CELL DEATH; CELL STRAIN K 562; CHRONIC MYELOID LEUKEMIA; DOWN REGULATION; HUMAN; HUMAN CELL; LEUKEMIA CELL; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DOMAIN; WESTERN BLOTTING;

APOPTOSIS; ASCORBIC ACID; BLOTTING, WESTERN; HSP90 HEAT-SHOCK PROTEINS; HUMANS; HYDROLYSIS; K562 CELLS; OXIDATIVE STRESS; VITAMIN K 3;

EID: 58649121962     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2008.10.019     Document Type: Article

References (39)

1. Neckers L. Development of small molecule Hsp90 inhibitors: utilizing both forward and reverse chemical genomics for drug identification. Curr Med Chem 10 (2003) 733-739
2. Bonvini P., Dalla R.H., Vignes N., and Rosolen A. Ubiquitination and proteasomal degradation of nucleophosmin-anaplastic lymphoma kinase induced by 17-allylamino-demethoxygeldanamycin: role of the co-chaperone carboxyl heat shock protein 70-interacting protein. Cancer Res 64 (2004) 3256-3264
3. Neckers L. Heat shock protein 90: the cancer chaperone. J Biosci 32 (2007) 517-530
4. Neckers L., and Ivy S.P. Heat shock protein 90. Curr Opin Oncol 15 (2003) 419-424
5. Banerji U., O'Donnell A., Scurr M., Pacey S., Stapleton S., Asad Y., et al. Phase I pharmacokinetic and pharmacodynamic study of 17-allylamino, 17-demethoxygeldanamycin in patients with advanced malignancies. J Clin Oncol 23 (2005) 4152-4161
6. Goetz M.P., Toft D., Reid J., Ames M., Stensgard B., Safgren S., et al. Phase I trial of 17-allylamino-17-demethoxygeldanamycin in patients with advanced cancer. J Clin Oncol 23 (2005) 1078-1087
7. Grem J.L., Morrison G., Guo X.D., Agnew E., Takimoto C.H., Thomas R., et al. Phase I and pharmacologic study of 17-(allylamino)-17-demethoxygeldanamycin in adult patients with solid tumors. J Clin Oncol 23 (2005) 1885-1893
8. Ramanathan R.K., Trump D.L., Eiseman J.L., Belani C.P., Agarwala S.S., Zuhowski E.G., et al. Phase I pharmacokinetic-pharmacodynamic study of 17-(allylamino)-17-demethoxygeldanamycin (17AAG, NSC 330507), a novel inhibitor of heat shock protein 90, in patients with refractory advanced cancers. Clin Cancer Res 11 (2005) 3385-3391
9. Pantano C., Shrivastava P., McElhinney B., and Janssen-Heininger Y. Hydrogen peroxide signaling through tumor necrosis factor receptor 1 leads to selective activation of c-Jun N-terminal kinase. J Biol Chem 278 (2003) 44091-44096
10. 2 production as a mechanism for cell type-specific inhibition of tumor necrosis factor alpha-induced but not interleukin-1beta-induced IkappaB kinase complex/nuclear factor-kappaB activation. J Biol Chem 280 (2005) 2912-2923
11. Shen S.C., Yang L.Y., Lin H.Y., Wu C.Y., Su T.H., and Chen Y.C. Reactive oxygen species-dependent HSP90 protein cleavage participates in arsenical As(+3)- and MMA(+3)-induced apoptosis through inhibition of telomerase activity via JNK activation. Toxicol Appl Pharmacol 229 (2008) 239-251
12. Verrax J., Vanbever S., Stockis J., Taper H., and Buc Calderon P. Role of glycolysis inhibition and poly(ADP-ribose) polymerase activation in necrotic-like cell death caused by ascorbate/menadione-induced oxidative stress in K562 human chronic myelogenous leukemic cells. Int J Cancer 120 (2007) 1192-1197
13. Prodromou C., Roe S.M., O'Brien R., Ladbury J.E., Piper P.W., and Pearl L.H. Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 90 (1997) 65-75
14. Schneider C., Sepp-Lorenzino L., Nimmesgern E., Ouerfelli O., Danishefsky S., Rosen N., et al. Pharmacologic shifting of a balance between protein refolding and degradation mediated by Hsp90. Proc Natl Acad Sci USA 93 (1996) 14536-14541
15. Bartholomeusz G.A., Talpaz M., Kapuria V., Kong L.Y., Wang S., Estrov Z., et al. Activation of a novel Bcr/Abl destruction pathway by WP1130 induces apoptosis of chronic myelogenous leukemia cells. Blood 109 (2007) 3470-3478
16. Pearl L.H., and Prodromou C. Structure and mechanism of the Hsp90 molecular chaperone machinery. Annu Rev Biochem 75 (2006) 271-294
17. Racker E., and Krimsky I. The mechanism of oxidation of aldehydes by glyceralde-hyde-3-phosphate dehydrogenase. J Biol Chem 198 (1952) 731-743
18. Verrax J., Cadrobbi J., Delvaux M., Jamison J.M., Gilloteaux J., Summers J.L., et al. The association of vitamins C and K3 kills cancer cells mainly by autoschizis, a novel form of cell death. Basis for their potential use as coadjuvants in anticancer therapy. Eur J Med Chem 38 (2003) 451-457
19. Verrax J., Cadrobbi J., Marques C., Taper H., Habraken Y., Piette J., et al. Ascorbate potentiates the cytotoxicity of menadione leading to an oxidative stress that kills cancer cells by a non-apoptotic caspase-3 independent form of cell death. Apoptosis 9 (2004) 223-233
20. Verrax J., Stockis J., Tison A., Taper H.S., and Buc Calderon P. Oxidative stress by ascorbate/menadione association kills K562 human chronic myelogenous leukaemia cells and inhibits its tumour growth in nude mice. Biochem Pharmacol 72 (2006) 671-680
21. Fader C.M., and Colombo M.I. Multivesicular bodies and autophagy in erythrocyte maturation. Autophagy 2 (2006) 122-125
22. Verrax J., Delvaux M., Beghein N., Taper H., Gallez B., and Buc Calderon P. Enhancement of quinone redox cycling by ascorbate induces a caspase-3 independent cell death in human leukaemia cells. An in vitro comparative study. Free Radic Res 39 (2005) 649-657
23. Trachootham D., Zhou Y., Zhang H., Demizu Y., Chen Z., Pelicano H., et al. Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by beta-phenylethyl isothiocyanate. Cancer Cell 10 (2006) 241-252
24. Guo F., Rocha K., Bali P., Pranpat M., Fiskus W., Boyapalle S., et al. Abrogation of heat shock protein 70 induction as a strategy to increase antileukemia activity of heat shock protein 90 inhibitor 17-allylamino-demethoxy geldanamycin. Cancer Res 65 (2005) 10536-10544
25. Hostetter D.R., Loeb C.R., Chu F., and Craik C.S. Hip is a pro-survival substrate of granzyme B. J Biol Chem 282 (2007) 27865-27874
26. Soti C., Racz A., and Csermely P. A Nucleotide-dependent molecular switch controls ATP binding at the C-terminal domain of Hsp90. N-terminal nucleotide binding unmasks a C-terminal binding pocket. J Biol Chem 277 (2002) 7066-7075
27. Buc Calderon P., Cadrobbi J., Marques C., Hong-Ngoc N., Jamison J.M., Gilloteaux J., et al. Potential therapeutic application of the association of vitamins C and K3 in cancer treatment. Curr Med Chem 9 (2002) 2271-2285
28. Noto V., Taper H.S., Jiang Y.H., Janssens J., Bonte J., and De Loecker W. Effects of sodium ascorbate (vitamin C) and 2-methyl-1,4-naphthoquinone (vitamin K3) treatment on human tumor cell growth in vitro. I. Synergism of combined vitamin C and K3 action. Cancer 63 (1989) 901-906
29. Sakagami H., Satoh K., Hakeda Y., and Kumegawa M. Apoptosis-inducing activity of vitamin C and vitamin K. Cell Mol Biol (Noisy-le-grand) 46 (2000) 129-143
30. Jamison J.M., Gilloteaux J., Nassiri M.R., Venugopal M., Neal D.R., and Summers J.L. Cell cycle arrest and autoschizis in a human bladder carcinoma cell line following vitamin C and vitamin K3 treatment. Biochem Pharmacol 67 (2004) 337-351
31. Kassouf W., Highshaw R., Nelkin G.M., Dinney C.P., and Kamat A.M. Vitamins C and K3 sensitize human urothelial tumors to gemcitabine. J Urol 176 (2006) 1642-1647
32. Vera J.C., Rivas C.I., Fischbarg J., and Golde D.W. Mammalian facilitative hexose transporters mediate the transport of dehydroascorbic acid. Nature 364 (1993) 79-82
33. Agus D.B., Vera J.C., and Golde D.W. Stromal cell oxidation: a mechanism by which tumors obtain vitamin C. Cancer Res 59 (1999) 4555-4558
34. Sun Y., Oberley L.W., Elwell J.H., and Sierra-Rivera E. Antioxidant enzyme activities in normal and transformed mouse liver cells. Int J Cancer 44 (1989) 1028-1033
35. Kamal A., Thao L., Sensintaffar J., Zhang L., Boehm M.F., Fritz L.C., et al. A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature 425 (2003) 407-410
36. Csermely P., Kajtar J., Hollosi M., Jalsovszky G., Holly S., Kahn C.R., et al. ATP induces a conformational change of the 90-kDa heat shock protein (hsp90). J Biol Chem 268 (1993) 1901-1907
37. Casciari J.J., Riordan N.H., Schmidt T.L., Meng X.L., Jackson J.A., and Riordan H.D. Cytotoxicity of ascorbate, lipoic acid, and other antioxidants in hollow fibre in vitro tumours. Br J Cancer 84 (2001) 1544-1550
38. Margolin K.A., Akman S.A., Leong L.A., Morgan R.J., Somlo G., Raschko J.W., et al. Phase I study of mitomycin C and menadione in advanced solid tumors. Cancer Chemother Pharmacol 36 (1995) 293-298
39. Tareen B., Summers J.L., Jamison J.M., Neal D.R., McGuire K., Gerson L., et al. A 12 week, open-label, phaseI/IIa study using Apatone for the treatment of prostate cancer patients who have failed standard therapy. Int J Med Sci 5 (2008) 62-67