Increasing intracellular bioavailable copper selectively targets prostate cancer cells

ACS Chemical Biology

Volumn 8, Issue 7, 2013, Pages 1621-1631

  Cater, Michael A ^a,b   Pearson, Helen B ^a,b   Wolyniec, Kamil ^a   Klaver, Paul ^a   Bilandzic, Maree ^d,e   Paterson, Brett M ^b,c   Bush, Ashley I ^b   Humbert, Patrick O ^a,b   La Fontaine, Sharon ^e   Donnelly, Paul S ^b,c   Haupt, Ygal ^a,b,f  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^e DEAKIN UNIVERSITY   (Australia)

^f MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CHYMOTRYPSIN; COPPER; COPPER COMPLEX; CUPRIC ION; DIACETYLBIS [N 4 METHYLTHIOSEMICARBAZONATO]CUPRIC ION; GLYOXALBIS[N 4 METHYLTHIOSEMICARBAZONATO]CUPRIC ION; IONOPHORE; LIGAND; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CELL CULTURE; CONTROLLED STUDY; DISEASE SEVERITY; EPITHELIUM CELL; EXPERIMENTAL MODEL; HUMAN; HUMAN CELL; INTERSTITIAL NEPHRITIS; MALE; MOUSE; NEPHROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROSTATE ADENOCARCINOMA; PROSTATE CANCER CELL; STOMACH DISTENSION;

ANIMALS; BIOLOGICAL AVAILABILITY; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL SURVIVAL; COPPER; DRUG DELIVERY SYSTEMS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MOLECULAR STRUCTURE; ORGANOMETALLIC COMPOUNDS; PROSTATIC NEOPLASMS;

EID: 84880553409     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb400198p     Document Type: Article

References (40)

1. Gupte, A. and Mumper, R. J. (2009) Elevated copper and oxidative stress in cancer cells as a target for cancer treatment Cancer Treat. Rev. 35, 32-46
2. Lin, J., Haffner, M. C., Zhang, Y., Lee, B. H., NathanielBrennen, W., Britton, J., Kachhap, S. K., Shim, J. S., Liu, J. O., Nelson, W., Yegnasubramanian, S., and Carducci, M. A. (2011) Disulfiram Is a DNA demethylating agent and inhibits prostate cancer cell growth Prostate 71, 333-343
3. Schimmer, A. D., Jitkova, Y., Gronda, M., Wang, Z., Brandwein, J., Chen, C., Gupta, V., Schuh, A., Yee, K., Chen, J., Ackloo, S., Booth, T., Keays, S., and Minden, M. D. A Phase I study of the metal ionophore clioquinol in patients with advanced hematologic malignancies. Clin. Lymphoma, Myeloma Leuk. 2012, in press
4. Daniel, K. G., Gupta, P., Harbach, R. H., Guida, W. C., and Dou, Q. P. (2004) Organic copper complexes as a new class of proteasome inhibitors and apoptosis inducers in human cancer cells Biochem. Pharmacol. 67, 1139-1151
5. Mao, X., Li, X., Sprangers, R., Wang, X., Venugopal, A., Wood, T., Zhang, Y., Kuntz, D. A., Coe, E., Trudel, S., Rose, D., Batey, R. A., Kay, L. E., and Schimmer, A. D. (2009) Clioquinol inhibits the proteasome and displays preclinical activity in leukemia and myeloma Leukemia 23, 585-590
6. Ding, W. Q., Liu, B., Vaught, J. L., Yamauchi, H., and Lind, S. E. (2005) Anticancer activity of the antibiotic clioquinol Cancer Res. 65, 3389-3395
7. Mao, X. and Schimmer, A. D. (2008) The toxicology of Clioquinol Toxicol. Lett. 182, 1-6
8. Chen, D., Cui, Q. C., Yang, H., Barrea, R. A., Sarkar, F. H., Sheng, S., Yan, B., Reddy, G. P., and Dou, Q. P. (2007) Clioquinol, a therapeutic agent for Alzheimer's disease, has proteasome-inhibitory, androgen receptor-suppressing, apoptosis-inducing, and antitumor activities in human prostate cancer cells and xenografts Cancer Res. 67, 1636-1644
9. Chen, D., Cui, Q. C., Yang, H., and Dou, Q. P. (2006) Disulfiram, a clinically used anti-alcoholism drug and copper-binding agent, induces apoptotic cell death in breast cancer cultures and xenografts via inhibition of the proteasome activity Cancer Res. 66, 10425-10433
10. Li, L., Yang, H., Chen, D., Cui, C., and Dou, Q. P. (2008) Disulfiram promotes the conversion of carcinogenic cadmium to a proteasome inhibitor with pro-apoptotic activity in human cancer cells Toxicol. Appl. Pharmacol. 229, 206-214
11. Navratilova, J., Jungova, P., Vanhara, P., Preisler, J., Kanicky, V., and Smarda, J. (2009) Copper ions regulate cytotoxicity of disulfiram to myeloid leukemia cells Int. J. Mol. Med. 24, 661-670
12. Brar, S. S., Grigg, C., Wilson, K. S., Holder, W. D., Jr., Dreau, D., Austin, C., Foster, M., Ghio, A. J., Whorton, A. R., Stowell, G. W., Whittall, L. B., Whittle, R. R., White, D. P., and Kennedy, T. P. (2004) Disulfiram inhibits activating transcription factor/cyclic AMP-responsive element binding protein and human melanoma growth in a metal-dependent manner in vitro, in mice and in a patient with metastatic disease Mol. Cancer Ther. 3, 1049-1060
13. Zhai, S. M., Yang, L., Cui, Q. C., Sun, Y., Dou, Q. P., and Yan, B. (2010) Tumor cellular proteasome inhibition and growth suppression by 8-hydroxyquinoline and clioquinol requires their capabilities to bind copper and transport copper into cells J. Biol. Inorg. Chem. 15, 259-269
14. Cen, D., Brayton, D., Shahandeh, B., Al-Ghazi, M., McNulty, S., Gidanian, S., Yang, S., Farmer, P., and Meyskens, F. (2004) Disulfiram facilitates intracellular copper transport that causes Oxidative stress and cell death in human Melanoma cells Pigment Cell Res. 17, 444-445
15. Cater, M. A. and Haupt, Y. (2011) Clioquinol induces cytoplasmic clearance of the X-linked inhibitor of apoptosis protein (XIAP): therapeutic indication for prostate cancer Biochem. J. 436, 481-491
16. Cvek, B. and Dvorak, Z. (2008) The value of proteasome inhibition in cancer. Can the old drug, disulfiram, have a bright new future as a novel proteasome inhibitor? Drug Discovery Today 13, 716-722
17. French, F. A. and Freedlander, B. L. (1958) Carcinostatic action of polycarbonyl compounds and their derivatives. IV. Glyoxal bis (thiosemicarbazone) and derivatives Cancer Res. 18, 1290-1300
18. French, F. A., Freedlander, B. L., Hosking, A., and French, J. (1960) Carcinostatic activity of some dicarbonyl compounds and their bis-hydrazones Acta Unio Int. Cancrum 16, 614-624
19. Petering, H. G., Buskirk, H. H., and Underwood, G. E. (1964) The anti-tumor activity of 2-keto-3-ethoxybutyraldehyde bis(thiosemicarbazone) and related compounds Cancer Res. 24, 367-372
20. Barry, V. C., Conalty, M. L., and O'Sullivan, J. F. (1966) Anticancer activity of bisthiosemicarbazones of methylglyoxal Cancer Res. 26, 2165-2168
21. Mihich, E., Simpson, C. L., and Mulhern, A. I. (1965) Kethoxal bis(thiosemicarbazone). II. Toxic and pathologic effects Cancer Res. 25, 1417-1431
22. Dilanyan, E. R., Ovsepyan, T. R., Arsenyan, F. G., Stepanyan, G. M., and Garibdzhanyan, B. T. (2008) Antitumor activity of substituted methylglyoxal bisthiosemicarbazones and their copper(II) chelates Pharm. Chem. J. 49, 504-506
23. Paterson, B. M., Karas, J. A., Scanlon, D. B., White, J. M., and Donnelly, P. S. (2010) Versatile new bis(thiosemicarbazone) bifunctional chelators: synthesis, conjugation to bombesin(7-14)-NH(2), and copper-64 radiolabeling Inorg. Chem. 49, 1884-1893
24. Donnelly, P. S., Liddell, J. R., Lim, S., Paterson, B. M., Cater, M. A., Savva, M. S., Mot, A. I., James, J. L., Trounce, I. A., White, A. R., and Crouch, P. J. (2012) An impaired mitochondrial electron transport chain increases retention of the hypoxia imaging agent diacetylbis(4- methylthiosemicarbazonato)copperII Proc. Natl. Acad. Sci. U.S.A. 109, 47-52
25. Crouch, P. J., Hung, L. W., Adlard, P. A., Cortes, M., Lal, V., Filiz, G., Perez, K. A., Nurjono, M., Caragounis, A., Du, T., Laughton, K., Volitakis, I., Bush, A. I., Li, Q. X., Masters, C. L., Cappai, R., Cherny, R. A., Donnelly, P. S., White, A. R., and Barnham, K. J. (2009) Increasing Cu bioavailability inhibits Abeta oligomers and tau phosphorylation Proc. Natl. Acad. Sci. U.S.A. 106, 381-386
26. Hung, L. W., Villemagne, V. L., Cheng, L., Sherratt, N. A., Ayton, S., White, A. R., Crouch, P. J., Lim, S., Leong, S. L., Wilkins, S., George, J., Roberts, B. R., Pham, C. L., Liu, X., Chiu, F. C., Shackleford, D. M., Powell, A. K., Masters, C. L., Bush, A. I., O'Keefe, G., Culvenor, J. G., Cappai, R., Cherny, R. A., Donnelly, P. S., Hill, A. F., Finkelstein, D. I., and Barnham, K. J. (2012) The hypoxia imaging agent CuII(atsm) is neuroprotective and improves motor and cognitive functions in multiple animal models of Parkinson's disease J. Exp. Med. 209, 837-854
27. Van den Berghe, P. V., Folmer, D. E., Malingre, H. E., van Beurden, E., Klomp, A. E., van de Sluis, B., Merkx, M., Berger, R., and Klomp, L. W. (2007) Human copper transporter 2 is localized in late endosomes and lysosomes and facilitates cellular copper uptake Biochem. J. 407, 49-59
28. Hurwitz, A. A., Foster, B. A., Allison, J. P., Greenberg, N. M., and Kwon, E. D. (2001) The TRAMP mouse as a model for prostate cancer Curr. Protoc. Immunol. 10.1002/0471142735.im2005s45
29. Suttie, A., Nyska, A., Haseman, J. K., Moser, G. J., Hackett, T. R., and Goldsworthy, T. L. (2003) A grading scheme for the assessment of proliferative lesions of the mouse prostate in the TRAMP model Toxicol. Pathol. 31, 31-38
30. Mattsson, K., Pokrovskaja, K., Kiss, C., Klein, G., and Szekely, L. (2001) Proteins associated with the promyelocytic leukemia gene product (PML)-containing nuclear body move to the nucleolus upon inhibition of proteasome-dependent protein degradation Proc. Natl. Acad. Sci. U.S.A. 98, 1012-1017
31. Ogiso, Y., Tomida, A., and Tsuruo, T. (2002) Nuclear localization of proteasomes participates in stress-inducible resistance of solid tumor cells to topoisomerase II-directed drugs Cancer Res. 62, 5008-5012
32. Crim, J. A. and Petering, H. G. (1967) The antitumor activity of Cu(II)KTS, the copper (II) chelate of 3-ethoxy-2-oxobutyraldehyde bis(thiosemicarbazone) Cancer Res. 27, 1278-1285
33. Sunderman, F. W., Jr. (1995) The influence of zinc on apoptosis Ann. Clin. Lab. Sci. 25, 134-142
34. Truong-Tran, A. Q., Ho, L. H., Chai, F., and Zalewski, P. D. (2000) Cellular zinc fluxes and the regulation of apoptosis/gene-directed cell death J. Nutr. 130, 1459S-1466S
35. Yu, H., Zhou, Y., Lind, S. E., and Ding, W. Q. (2009) Clioquinol targets zinc to lysosomes in human cancer cells Biochem. J. 417, 133-139
36. Lovejoy, D. B., Jansson, P. J., Brunk, U. T., Wong, J., Ponka, P., and Richardson, D. R. (2011) Antitumor activity of metal-chelating compound Dp44mT is mediated by formation of a redox-active copper complex that accumulates in lysosomes Cancer Res. 71, 5871-5880
37. Richardson, P. G., Barlogie, B., Berenson, J., Singhal, S., Jagannath, S., Irwin, D., Rajkumar, S. V., Srkalovic, G., Alsina, M., Alexanian, R., Siegel, D., Orlowski, R. Z., Kuter, D., Limentani, S. A., Lee, S., Hideshima, T., Esseltine, D. L., Kauffman, M., Adams, J., Schenkein, D. P., and Anderson, K. C. (2003) A phase 2 study of bortezomib in relapsed, refractory myeloma N. Engl. J. Med. 348, 2609-2617
38. Hoeller, D. and Dikic, I. (2009) Targeting the ubiquitin system in cancer therapy Nature 458, 438-444
39. Siegel, D. S., Martin, T., Wang, M., Vij, R., Jakubowiak, A. J., Lonial, S., Trudel, S., Kukreti, V., Bahlis, N., Alsina, M., Chanan-Khan, A., Buadi, F., Reu, F. J., Somlo, G., Zonder, J., Song, K., Stewart, A. K., Stadtmauer, E., Kunkel, L., Wear, S., Wong, A. F., Orlowski, R. Z., and Jagannath, S. (2012) A phase 2 study of single-agent carfilzomib (PX-171-003-A1) in patients with relapsed and refractory multiple myeloma Blood 10.1182/blood-2012-05-425934
40. Gingras, B., Suprunchuk, T., and Bayley, C. (1962) The preparation of some thiosemicarbazones and their copper complexes: Part III Can. J. Chem. 40, 1053-1059