A small molecule that induces reactive oxygen species via cellular glutathione depletion

Biochemical Journal

Volumn 463, Issue 1, 2014, Pages 53-63

  Kawamura, Tatsuro ^a   Kondoh, Yasumitsu ^a,b   Muroi, Makoto ^a,b   Kawatani, Makoto ^a   Osada, Hiroyuki ^a,b  

^a RIKEN   (Japan)

^b Elements Chemistry Laboratory   (Japan)

Author keywords

Cancer therapy; Chemical biology; Glutathione; GST; KRAS; Reactive oxygen species (ROS)

Indexed keywords

CAMPTOTHECIN; DAUNORUBICIN; ETOPOSIDE; GLUTATHIONE; MITOMYCIN; NPD 926; REACTIVE OXYGEN METABOLITE; SMALL MOLECULE TRANSPORT AGENT; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; ANTIPORTER; KRAS PROTEIN, HUMAN; ONCOPROTEIN; RAS PROTEIN;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER STEM CELL; CANCER THERAPY; CELL DEATH; CONJUGATION; CONTROLLED STUDY; CYTOTOXICITY; DRUG MECHANISM; FEMALE; FIBROBLAST; GLUTATHIONE METABOLISM; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; ONCOGENE K RAS; OXIDATIVE STRESS; PROTEOMICS; TRANSFORMED CELL; CHEMISTRY; DRUG ANTAGONISM; DRUG EFFECT; HL 60 CELL LINE; JURKAT CELL LINE; K562 CELL LINE; METABOLISM; PATHOLOGY; TRANSFORMED CELL LINE; U937 CELL LINE;

ANTINEOPLASTIC AGENTS; ANTIPORTERS; CELL DEATH; CELL LINE, TRANSFORMED; GLUTATHIONE; HL-60 CELLS; HUMANS; JURKAT CELLS; K562 CELLS; NEOPLASTIC STEM CELLS; PROTO-ONCOGENE PROTEINS; RAS PROTEINS; REACTIVE OXYGEN SPECIES; U937 CELLS;

EID: 84906990892     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20140669     Document Type: Article

References (54)

1. Trachootham, D., Alexandre, J. and Huang, P. (2009) Targeting cancer cells by ROS-mediated mechanisms: A radical therapeutic approach? Nat. Rev. Drug Discov. 8, 579-591 CrossRef PubMed.
2. D'Autréaux, B. and Toledano, M. B. (2007) ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell Biol. 8, 813-824 CrossRef PubMed.
3. Downward, J. (2003) Targeting RAS signalling pathways in cancer therapy. Nat. Rev. Cancer 3, 11-22 CrossRef PubMed.
4. Mascaux, C., Iannino, N., Martin, B., Paesmans, M., Berghmans, T., Dusart, M., Haller, A., Lothaire, P., Meert, A. P., Noel, S. et al. (2005) The role of RAS oncogene in survival of patients with lung cancer: A systematic review of the literature with meta-analysis. Br. J. Cancer 92, 131-139 CrossRef PubMed.
5. Winton, T., Livingston, R., Johnson, D., Rigas, J., Johnston, M., Butts, C., Cormier, Y., Goss, G., Inculet, R., Vallieres, E. et al. (2005) Vinorelbine plus cisplatin vs. observation in resected non-small-cell lung cancer. N. Engl. J. Med. 352, 2589-2597 CrossRef PubMed.
6. Mitsushita, J., Lambeth, J. D. and Kamata, T. (2004) The superoxide-generating oxidase Nox1 is functionally required for Ras oncogene transformation. Cancer Res. 64, 3580-3585 CrossRef PubMed.
7. Hu, Y., Lu, W., Chen, G., Wang, P., Chen, Z., Zhou, Y., Ogasawara, M., Trachootham, D., Feng, L., Pelicano, H. et al. (2012) K-ras(G12V) transformation leads to mitochondrial dysfunction and a metabolic switch from oxidative phosphorylation to glycolysis. Cell Res. 22, 399-412 CrossRef PubMed.
8. Hu, Y., Rosen, D. G., Zhou, Y., Feng, L., Yang, G., Liu, J. and Huang, P. (2005) Mitochondrial manganese-superoxide dismutase expression in ovarian cancer: role in cell proliferation and response to oxidative stress. J. Biol. Chem. 280, 39485-39492 CrossRef PubMed.
9. Radisky, D. C., Levy, D. D., Littlepage, L. E., Liu, H., Nelson, C. M., Fata, J. E., Leake, D., Godden, E. L., Albertson, D. G., Nieto, M. A. et al. (2005) Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature 436, 123-127 CrossRef PubMed.
10. Xia, C., Meng, Q., Liu, L. Z., Rojanasakul, Y., Wang, X. R. and Jiang, B. H. (2007) Reactive oxygen species regulate angiogenesis and tumor growth through vascular endothelial growth factor. Cancer Res. 67, 10823-10830 CrossRef PubMed.
11. Luo, J., Solimini, N. L. and Elledge, S. J. (2009) Principles of cancer therapy: oncogene and non-oncogene addiction. Cell 136, 823-837 CrossRef PubMed.
12. Shaw, A. T., Winslow, M. M., Magendantz, M., Ouyang, C., Dowdle, J., Subramanian, A., Lewis, T. A., Maglathin, R. L., Tolliday, N. and Jacks, T. (2011) Selective killing of K-ras mutant cancer cells by small molecule inducers of oxidative stress. Proc. Natl. Acad. Sci. U.S.A. 108, 8773-8778 CrossRef PubMed.
13. Dolma, S., Lessnick, S. L., Hahn, W. C. and Stockwell, B. R. (2003) Identification of genotype-selective antitumor agents using synthetic lethal chemical screening in engineered human tumor cells. Cancer Cell 3, 285-296 CrossRef PubMed.
14. Yagoda, N., von Rechenberg, M., Zaganjor, E., Bauer, A. J., Yang, W. S., Fridman, D. J., Wolpaw, A. J., Smukste, I., Peltier, J. M., Boniface, J. J. et al. (2007) RAS-RAF-MEK-dependent oxidative cell death involving voltage-dependent anion channels. Nature 447, 864-868 CrossRef PubMed.
15. Couzin, J. (2002) Cancer drugs. Smart weapons prove tough to design. Science 298, 522-525 CrossRef PubMed.
16. Frantz, S. (2006) Drug approval triggers debate on future direction for cancer treatments. Nat. Rev. Drug Discov. 5, 91 CrossRef PubMed.
17. Trachootham, D., Zhou, Y., Zhang, H., Demizu, Y., Chen, Z., Pelicano, H., Chiao, P. J., Achanta, G., Arlinghaus, R. B., Liu, J. and Huang, P. (2006) Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by β-phenylethyl isothiocyanate. Cancer Cell 10, 241-252 CrossRef PubMed.
18. Raj, L., Ide, T., Gurkar, A. U., Foley, M., Schenone, M., Li, X., Tolliday, N. J., Golub, T. R., Carr, S. A., Shamji, A. F. et al. (2011) Selective killing of cancer cells by a small molecule targeting the stress response to ROS. Nature 475, 231-234 CrossRef PubMed.
19. Guzman, M. L., Rossi, R. M., Neelakantan, S., Li, X., Corbett, C. A., Hassane, D. C., Becker, M. W., Bennett, J. M., Sullivan, E., Lachowicz, J. L. et al. (2007) An orally bio available parthenolide analog selectively eradicates acute myelogenous leukemia stem and progenitor cells. Blood 110, 4427-4435 CrossRef PubMed.
20. Huang, P., Feng, L., Oldham, E. A., Keating, M. J. and Plunkett, W. (2000) Superoxide dismutase as a target for the selective killing of cancer cells. Nature 407, 390-395 CrossRef PubMed.
21. Sun, X., Ai, M., Wang, Y., Shen, S., Gu, Y., Jin, Y., Zhou, Z., Long, Y. and Yu, Q. (2013) Selective induction of tumor cell apoptosis by a novel P450-mediated reactive oxygen species (ROS) inducer methyl 3-(4-nitrophenyl) propiolate. J. Biol. Chem. 288, 8826-8837 CrossRef PubMed.
22. Schenone, M., Dančík, V., Wagner, B. K. and Clemons, P. A. (2013) Target identification and mechanism of action in chemical biology and drug discovery. Nat. Chem. Biol. 9, 232-240 CrossRef PubMed.
23. Ziegler, S., Pries, V., Hedberg, C. and Waldmann, H. (2013) Target identification for small bioactive molecules: finding the needle in the haystack. Angew. Chem. Int. Ed. Engl. 52, 2744-2792 CrossRef PubMed.
24. Muroi, M., Kazami, S., Noda, K., Kondo, H., Takayama, H., Kawatani, M., Usui, T. and Osada, H. (2010) Application of proteomic profiling based on 2D-DIGE for classification of compounds according to the mechanism of action. Chem. Biol. 17, 460-470 CrossRef PubMed.
25. Kawatani, M., Takayama, H., Muroi, M., Kimura, S., Maekawa, T. and Osada, H. (2011) Identification of a small-molecule inhibitor of DNA topoisomerase II by proteomic profiling. Chem. Biol. 18, 743-751 CrossRef PubMed.
26. Futamura, Y., Kawatani, M., Muroi, M., Aono, H., Nogawa, T. and Osada, H. (2013) Identification of a molecular target of a novel fungal metabolite, pyrrolizilactone, by phenotypic profiling systems. ChemBioChem 14, 2456-2463 CrossRef PubMed.
27. Kanoh, N., Honda, K., Simizu, S., Muroi, M. and Osada, H. (2005) Photo-cross-linked small-molecule affinity matrix for facilitating forward and reverse chemical genetics. Angew. Chem. Int. Ed. Engl. 44, 3559-3362 CrossRef PubMed.
28. Kawatani, M., Okumura, H., Honda, K., Kanoh, N., Muroi, M., Dohmae, N., Takami, M., Kitagawa, M., Futamura, Y., Imoto, M. and Osada, H. (2008) The identification of an osteoclastogenesis inhibitor through the inhibition of glyoxalase I. Proc. Natl. Acad. Sci. U.S.A. 105, 11691-11696 CrossRef PubMed.
29. Eva, A., Tronick, S. R., Gol, R. A., Pierce, J. H. and Aaronson, S. A. (1983) Transforming genes of human hematopoietic tumors: frequent detection of ras-related oncogenes whose activation appears to be independent of tumor phenotype. Proc. Natl. Acad. Sci. U.S.A. 80, 4926-4930 CrossRef PubMed.
30. Osada, H. (2010) Introduction of new tools for chemical biology research on microbial metabolites. Biosci. Biotechnol. Biochem. 74, 1135-1140 CrossRef PubMed.
31. Watabe, M., Kakeya, H. and Osada, H. (1999) Requirement of protein kinase (Krs/MST) activation for MT-21-induced apoptosis. Oncogene 18, 5211-5220 CrossRef PubMed.
32. Maruyama, M., Sudo, T., Kasuya, Y., Shiga, T., Hu, B. and Osada, H. (2000) Immunolocalization of p38 MAP kinase in mouse brain. Brain Res. 887, 350-358 CrossRef PubMed.
33. Awasthi, Y. C., Garg, H. S., Dao, D. D., Partridge, C. A. and Srivastava, S. K. (1981) Enzymatic conjugation of erythrocyte glutathione with 1-chloro-2, 4-dinitrobenzene: The fate of glutathione conjugate in erythrocytes and the effect of glutathione depletion on hemoglobin. Blood 58, 733-738 PubMed.
34. Huang, J. and Philbert, M. A. (1996) Cellular responses of cultured cerebellar astrocytes to ethacrynic acid-induced perturbation of subcellular glutathione homeostasis. Brain Res. 711, 184-192 CrossRef PubMed.
35. Garrido, C., Schmitt, E., Cande, C., Vahsen, N., Parcellier, A. and Kroemer, G. (2003) HSP27 and HSP70: Potentially oncogenic apoptosis inhibitors. Cell Cycle 2, 579-584 CrossRef PubMed.
36. Dolado, I., Swat, A., Ajenjo, N., De Vita, G., Cuadrado, A. and Nebreda, A. R. (2007) p38α MAP kinase as a sensor of reactive oxygen species in tumorigenesis. Cancer Cell 11, 191-205 CrossRef PubMed.
37. Townsend, D. M. and Tew, K. D. (2003) The role of glutathione-S -transferase in anti-cancer drug resistance. Oncogene 22, 7369-7375 CrossRef PubMed.
38. Laborde, E. (2010) Glutathione transferases as mediators of signaling pathways involved in cell proliferation and cell death. Cell Death Differ. 17, 1373-1380 CrossRef PubMed.
39. Meyer, D. J., Crease, D. J. and Ketterer, B. (1995) Forward and reverse catalysis and product sequestration by human glutathione S-transferases in the reaction of GSH with dietary aralkyl isothiocyanates. Biochem. J. 306, 565-569 PubMed.
40. Oude Elferink, R. P., Bakker, C. T. and Jansen, P. L. (1993) Glutathione-conjugate transport by human colon adenocarcinoma cells (Caco-2 cells). Biochem. J. 290, 759-764 PubMed.
41. Xu, K. and Thornalley, P. J. (2001) Involvement of glutathione metabolism in the cytotoxicity of the phenethyl isothiocyanate and its cysteine conjugate to human leukaemia cells in vitro. Biochem. Pharmacol. 61, 165-177 CrossRef PubMed.
42. Rosenbluth, M. J., Lam, W. A. and Fletcher, D. A. (2006) Force microscopy of nonadherent cells: A comparison of leukemia cell deformability. Biophys. J. 90, 2994-3003 CrossRef PubMed.
43. Adams, D. J., Dai, M., Pellegrino, G., Wagner, B. K., Stern, A. M., Shamji, A. F. and Schreiber, S. L. (2012) Synthesis, cellular evaluation, and mechanism of action of piperlongumine analogs. Proc. Natl. Acad. Sci. U.S.A. 109, 15115-15120 CrossRef PubMed.
44. Basu, A., Bodycombe, N. E., Cheah, J. H., Price, E. V., Liu, K., Schaefer, G. I., Ebright, R. Y., Stewart, M. L., Ito, D., Wang, S. et al. (2013) An interactive resource to identify cancer genetic and lineage dependencies targeted by small molecules. Cell 154, 1151-1161 CrossRef PubMed.
45. Watabe, M., Kakeya, H., Onose, R. and Osada, H. (2000) Activation of MST/Krs and c-Jun N-terminal kinases by different signaling pathways during cytotrienin A-induced apoptosis. J. Biol. Chem. 275, 8766-8771 CrossRef PubMed.
46. Recktenwald, C. V., Kellner, R., Lichtenfels, R. and Seliger, B. (2008) Altered detoxification status and increased resistance to oxidative stress by K-ras transformation. Cancer Res. 68, 10086-10093 CrossRef PubMed.
47. DeNicola, G. M., Karreth, F. A., Humpton, T. J., Gopinathan, A., Wei, C., Frese, K., Mangal, D., Yu, K. H., Yeo, C. J., Calhoun, E. S. et al. (2011) Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature 475, 106-109 CrossRef PubMed.
48. Pei, S., Minhajuddin, M., Callahan, K. P., Balys, M., Ashton, J. M., Neering, S. J., Lagadinou, E. D., Corbett, C., Ye, H., Liesveld, J. L. et al. (2013) Targeting aberrant glutathione metabolism to eradicate human acute myelogenous leukemia cells. J. Biol. Chem. 288, 33542-33558 CrossRef PubMed.
49. Adams, D. J., Boskovic, Z. V., Theriault, J. R., Wang, A. J., Stern, A. M., Wagner, B. K., Shamji, A. F. and Schreiber, S. L. (2013) Discovery of small-molecule enhancers of reactive oxygen species that are nontoxic or cause genotype-selective cell death. ACS Chem. Biol. 8, 923-929 CrossRef PubMed.
50. Dixon, S. J., Lemberg, K. M., Lamprecht, M. R., Skouta, R., Zaitsev, E. M., Gleason, C. E., Patel, D. N., Bauer, A. J., Cantley, A. M., Yang, W. S., Morrison, B. and Stockwell, B. R. (2012) Ferroptosis: An iron-dependent form of nonapoptotic cell death. Cell 149, 1060-1072 CrossRef PubMed.
51. c- cystine transporter: A new action for an old drug. Leukemia 15, 1633-1640 CrossRef PubMed.
52. c- And thereby promotes tumor growth. Cancer Cell 19, 387-400 CrossRef PubMed.
53. Drayton, R. M., Dudziec, E., Peter, S., Bertz, S., Hartmann, A., Bryant, H. E. and Catto, J. W. (2014) Reduced expression of miRNA-27a modulates cisplatin resistance in bladder cancer by targeting the cystine/glutamate exchanger SLC7A11. Clin. Cancer Res. 20, 1990-2000 CrossRef PubMed.
54. Timmerman, L. A., Holton, T., Yuneva, M., Louie, R. J., Padŕo, M., Daemen, A., Hu, M., Chan, D. A., Ethier, S. P., van 't Veer, L. J. et al. (2013) Glutamine sensitivity analysis identifies the xCT antiporter as a common triple-negative breast tumor therapeutic target. Cancer Cell 24, 450-465 CrossRef PubMed.