Copper as a target for prostate cancer therapeutics: Copper-ionophore pharmacology and altering systemic copper distribution

Oncotarget

Volumn 7, Issue 24, 2016, Pages 37064-37080

  Denoyer, Delphine ^a   Pearson, Helen B ^b,c   Clatworthy, Sharnel A S ^a   Smith, Zoe M ^d   Francis, Paul S ^d   Llanos, Roxana M ^a   Volitakis, Irene ^c   Phillips, Wayne A ^b,c   Meggyesy, Peter M ^a   Masaldan, Shashank ^a   Cater, Michael A ^a,c  

^a DEAKIN UNIVERSITY   (Australia)

^b PETER MACCALLUM CANCER CENTRE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d DEAKIN UNIVERSITY   (Australia)

Author keywords

Atp7b; Copper; Ionophore; Prostate cancer; TRAMP

Indexed keywords

CERULOPLASMIN; CLIOQUINOL; COPPER IONOPHORE; DISULFIRAM; GLUTATHIONE; GLYOXALBIS(N4 METHYLTHIOSEMICARBAZONATO)COPPER; IONOPHORE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; WILSON DISEASE PROTEIN; ZINC ION; ANTINEOPLASTIC AGENT; ATP7B PROTEIN, MOUSE; COPPER; COPPER EXPORTING ADENOSINE TRIPHOSPHATASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CHEMOTHERAPY; CONTROLLED STUDY; COPPER BLOOD LEVEL; DRUG SAFETY; DRUG TARGETING; ENZYME ACTIVITY; IN VITRO STUDY; INTRACELLULAR SPACE; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROSTATE CANCER; PROSTATE EPITHELIUM CELL; TISSUE LEVEL; TRAMP MOUSE; TRANSGENIC MOUSE; ZINC BLOOD LEVEL; ADENOCARCINOMA; ANIMAL; GENETICS; METABOLISM; PROSTATE TUMOR;

ADENOCARCINOMA; ANIMALS; ANTINEOPLASTIC AGENTS; COPPER; COPPER-TRANSPORTING ATPASES; IONOPHORES; MALE; MICE; MICE, TRANSGENIC; PROSTATIC NEOPLASMS;

EID: 84978132469     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.9245     Document Type: Article

References (75)

1. Ahmad AS, Ormiston-Smith N and Sasieni PD. Trends in the lifetime risk of developing cancer in Great Britain: comparison of risk for those born from 1930 to 1960. British Journal of Cancer. 2015; 112:943-947.
2. Berger NA, Savvides P, Koroukian SM, Kahana EF, Deimling GT, Rose JH, Bowman KF and Miller RH. Cancer in the elderly. Transactions of the American Clinical and Climatological Association. 2006; 117:147-155; discussion 155-146.
3. Gallick GE, Corn PG, Zurita AJ and Lin SH. Smallmolecule protein tyrosine kinase inhibitors for the treatment of metastatic prostate cancer. Future Medicinal Chemistry. 2012; 4:107-119.
4. Caino MC and Altieri DC. Molecular Pathways: Mitochondrial Reprogramming in Tumor Progression and Therapy. Clinical Cancer Research. 2016; 22:540-545.
5. Dassie JP, Hernandez LI, Thomas GS, Long ME, Rockey WM, Howell CA, Chen Y, Hernandez FJ, Liu XY, Wilson ME, Allen LA, Vaena DA, Meyerholz DK and Giangrande PH. Targeted inhibition of prostate cancer metastases with an RNA aptamer to prostate-specific membrane antigen. Molecular Therapy. 2014; 22:1910-1922.
6. Logothetis CJ, Gallick GE, Maity SN, Kim J, Aparicio A, Efstathiou E and Lin SH. Molecular classification of prostate cancer progression: foundation for marker-driven treatment of prostate cancer. Cancer Discovery. 2013; 3:849-861.
7. Cater MA and Haupt Y. Clioquinol induces cytoplasmic clearance of the X-linked inhibitor of apoptosis protein (XIAP): therapeutic indication for prostate cancer. The Biochemical Journal. 2011; 436:481-491.
8. Cater MA, Pearson HB, Wolyniec K, Klaver P, Bilandzic M, Paterson BM, Bush AI, Humbert PO, La Fontaine S, Donnelly PS and Haupt Y. Increasing intracellular bioavailable copper selectively targets prostate cancer cells. ACS Chemical Biology. 2013; 8:1621-1631.
9. Denoyer D, Masaldan S, La Fontaine S and Cater MA. Targeting copper in cancer therapy: 'Copper That Cancer'. Metallomics. 2015; 7:1459-1476.
10. Helsel ME and Franz KJ. Pharmacological activity of metal binding agents that alter copper bioavailability. Dalton Transactions. 2015; 44:8760-8770.
11. Ding WQ and Lind SE. Metal ionophores-an emerging class of anticancer drugs. LUBMB Life. 2009; 61:1013-1018.
12. Linder MC and Hazegh-Azam M. Copper biochemistry and molecular biology. The American Journal of Clinical Nutrition. 1996; 63:797S-811S.
13. Santini C, Pellei M, Gandin V, Porchia M, Tisato F and Marzano C. Advances in copper complexes as anticancer agents. Chemical Reviews. 2014; 114:815-862.
14. Allensworth JL, Evans MK, Bertucci F, Aldrich AJ, Festa RA, Finetti P, Ueno NT, SafiR, McDonnell DP, Thiele DJ, Van Laere S and Devi GR. Disulfiram (DSF) acts as a copper ionophore to induce copper-dependent oxidative stress and mediate anti-tumor efficacy in inflammatory breast cancer. Molecular Oncology. 2015; :1155-1168.
15. Brar SS, Grigg C, Wilson KS, Holder WD, Jr., Dreau D, Austin C, Foster M, Ghio AJ, Whorton AR, Stowell GW, Whittall LB, Whittle RR, White DP and Kennedy TP. 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. Molecular Cancer Therapeutics. 2004; 3:1049-1060.
16. Chen D, Cui QC, Yang H, Barrea RA, Sarkar FH, Sheng S, Yan B, Reddy GP and Dou QP. 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 Research. 2007; 67:1636-1644.
17. SafiR, Nelson ER, Chitneni SK, Franz KJ, George DJ, Zalutsky MR and McDonnell DP. Copper signaling axis as a target for prostate cancer therapeutics. Cancer Research. 2014; 74:5819-5831.
18. Cai H, Wu JS, Muzik O, Hsieh JT, Lee RJ and Peng F. Reduced 64Cu uptake and tumor growth inhibition by knockdown of human copper transporter 1 in xenograft mouse model of prostate cancer. Journal of Nuclear Medicine. 2014; 55:622-628.
19. Fleshner NE and Klotz LH. Diet, androgens, oxidative stress and prostate cancer susceptibility. Cancer Metastasis Reviews. 1998; 17:325-330.
20. Fair WR, Fleshner NE and Heston W. Cancer of the prostate: a nutritional disease? Urology. 1997; 50:840-848.
21. Gupta-Elera G, Garrett AR, Robison RA and O'Neill KL. The role of oxidative stress in prostate cancer. European Journal of Cancer Prevention. 2012; 21:155-162.
22. Arsova-Sarafinovska Z, Eken A, Matevska N, Erdem O, Sayal A, Savaser A, Banev S, Petrovski D, Dzikova S, Georgiev V, Sikole A, Ozgok Y, Suturkova L, Dimovski AJ and Aydin A. Increased oxidative/nitrosative stress and decreased antioxidant enzyme activities in prostate cancer. Clinical Biochemistry. 2009; 42:1228-1235.
23. Stefani C, Al-Eisawi Z, Jansson PJ, Kalinowski DS and Richardson DR. Identification of differential anti-neoplastic activity of copper bis(thiosemicarbazones) that is mediated by intracellular reactive oxygen species generation and lysosomal membrane permeabilization. Journal of Inorganic Biochemistry. 2015; 152:20-37.
24. Xiao Y, Chen D, Zhang X, Cui Q, Fan Y, Bi C and Dou QP. Molecular study on copper-mediated tumor proteasome inhibition and cell death. International Journal of Oncology. 2010; 37:81-87.
25. Festa RA and Thiele DJ. Copper: An essential metal in biology. Curr Biol. 2011; 21:R877-R883.
26. Denoyer D, Clatworthy SA, Masaldan S, Meggyesy PM and Cater MA. Heterogeneous copper concentrations in cancerous human prostate tissues. Prostate. 2015; 75:1510-1517.
27. Petering HG, Buskirk HH and Underwood GE. The Anti-Tumor Activity of 2-Keto-3-Ethoxybutyraldehyde Bis(Thiosemicarbazone) and Related Compounds. Cancer Research. 1964; 24:367-372.
28. Barry VC, Conalty ML and O'Sullivan JF. Anticancer activity of bisthiosemicarbazones of methylglyoxal. Cancer Research. 1966; 26:2165-2168.
29. French FA and Freedlander BL. Carcinostatic action of polycarbonyl compounds and their derivatives. IV. Glyoxal bis (thiosemicarbazone) and derivatives. Cancer Research. 1958; 18:1290-1300.
30. Schweizer MT, Lin J, Blackford A, Bardia A, King S, Armstrong AJ, Rudek MA, Yegnasubramanian S and Carducci MA. Pharmacodynamic study of disulfiram in men with non-metastatic recurrent prostate cancer. Prostate Cancer and Prostatic Diseases. 2013; 16:357-361.
31. Peng F, Lu X, Janisse J, Muzik O and Shields AF. PET of human prostate cancer xenografts in mice with increased uptake of 64CuCl2. Journal of Nuclear Medicine. 2006; 47:1649-1652.
32. Hurwitz AA, Foster BA, Allison JP, Greenberg NM and Kwon ED. The TRAMP mouse as a model for prostate cancer. Curr Protoc Immunol. 2001; Chapter 20:Unit 20 25.
33. Costello LC, Franklin RB, Zou J, Feng P, Bok R, Swanson MG and Kurhanewicz J. Human prostate cancer ZIP1/zinc/citrate genetic/metabolic relationship in the TRAMP prostate cancer animal model. Cancer Biology & Therapy. 2011; 12:1078-1084.
34. Greenberg NM, DeMayo F, Finegold MJ, Medina D, Tilley WD, Aspinall JO, Cunha GR, Donjacour AA, Matusik RJ and Rosen JM. Prostate cancer in a transgenic mouse. Proceedings of the National Academy of Sciences of the United States of America. 1995; 92:3439-3443.
35. Kaplan-Lefko PJ, Chen TM, Ittmann MM, Barrios RJ, Ayala GE, Huss WJ, Maddison LA, Foster BA and Greenberg NM. Pathobiology of autochthonous prostate cancer in a pre-clinical transgenic mouse model. Prostate. 2003; 55:219-237.
36. Costello LC, Guan Z, Kukoyi B, Feng P and Franklin RB. Terminal oxidation and the effects of zinc in prostate versus liver mitochondria. Mitochondrion. 2004; 4:331-338.
37. Kuvibidila S, Gauthier T, Warrier RP and Rayford W. Increased levels of serum transferrin receptor and serum transferrin receptor/log ferritin ratios in men with prostate cancer and the implications for body-iron stores. Journal of Laboratory and Clinical Medicine. 2004; 144:176-182.
38. Foster BA, Gingrich JR, Kwon ED, Madias C and Greenberg NM. Characterization of prostatic epithelial cell lines derived from transgenic adenocarcinoma of the mouse prostate (TRAMP) model. Cancer Research. 1997; 57:3325-3330.
39. Frohlich DA, McCabe MT, Arnold RS and Day ML. The role of Nrf2 in increased reactive oxygen species and DNA damage in prostate tumorigenesis. Oncogene. 2008; 27:4353-4362.
40. Circu ML and Aw TY. Glutathione and modulation of cell apoptosis. Biochim Biophys Acta. 2012; 1823:1767-1777.
41. Kalinina EV, Chernov NN and Novichkova MD. Role of glutathione, glutathione transferase, and glutaredoxin in regulation of redox-dependent processes. Biochemistry Biokhimiia. 2014; 79:1562-1583.
42. Tripathy D, Choudhary A, Banerjee UC, Singh IP and Chatterjee A. Induction of Apoptosis and Reduction of Endogenous Glutathione Level by the Ethyl-Acetate Soluble Fraction of the Methanol Extract of the Roots of Potentilla fulgens in Cancer Cells. PloS One. 2015; 10:e0135890.
43. Cheah DM, Deal YJ, Wright PF, Buck NE, Chow CW, Mercer JF and Allen KJ. Heterozygous tx mice have an increased sensitivity to copper loading: implications for Wilson's disease carriers. Biometals. 2007; 20:751-757.
44. Theophilos MB, Cox DW and Mercer JF. The toxic milk mouse is a murine model of Wilson disease. Human Molecular Genetics. 1996; 5:1619-1624.
45. Rauch H. Toxic milk, a new mutation affecting copper metabolism in the mouse. The Journal of Heredity. 1983; 74:141-144.
46. Cater MA, La Fontaine S, Shield K, Deal Y and Mercer JF. ATP7B mediates vesicular sequestration of copper: insight into biliary copper excretion. Gastroenterology. 2006; 130:493-506.
47. Allen KJ, Buck NE, Cheah DM, Gazeas S, Bhathal P and Mercer JF. Chronological changes in tissue copper, zinc and iron in the toxic milk mouse and effects of copper loading. Biometals. 2006; 19:555-564.
48. Howell JM and Mercer JF. The pathology and trace element status of the toxic milk mutant mouse. Journal of Comparative Pathology. 1994; 110:37-47.
49. Cherny RA, Atwood CS, Xilinas ME, Gray DN, Jones WD, McLean CA, Barnham KJ, Volitakis I, Fraser FW, Kim Y, Huang X, Goldstein LE, Moir RD, Lim JT, Beyreuther K, Zheng H, et al. Treatment with a copper-zinc chelator markedly and rapidly inhibits beta-amyloid accumulation in Alzheimer's disease transgenic mice. Neuron. 2001; 30:665-676.
50. Faux NG, Ritchie CW, Gunn A, Rembach A, Tsatsanis A, Bedo J, Harrison J, Lannfelt L, Blennow K, Zetterberg H, Ingelsson M, Masters CL, Tanzi RE, Cummings JL, Herd CM and Bush AI. PBT2 rapidly improves cognition in Alzheimer's Disease: additional phase II analyses. JAD. 2010; 20:509-516.
51. Bush AI. Drug development based on the metals hypothesis of Alzheimer's disease. Journal of Alzheimer's disease. 2008; 15:223-240.
52. Williams JR, Trias E, Beilby PR, Lopez NI, Labut EM, Bradford CS, Roberts BR, McAllum EJ, Crouch PJ, Rhoads TW, Pereira C, Son M, Elliott JL, Franco MC, Estevez AG, Barbeito L, et al. Copper delivery to the CNS by CuATSM effectively treats motor neuron disease in SOD mice co-expressing the Copper-Chaperone-for-SOD. Neurobiology of Disease. 2016; 89:1-9.
53. Donnelly PS, Liddell JR, Lim S, Paterson BM, Cater MA, Savva MS, Mot AI, James JL, Trounce IA, White AR and Crouch PJ. An impaired mitochondrial electron transport chain increases retention of the hypoxia imaging agent diacetylbis(4-methylthiosemicarbazonato)copperII. Proceedings of the National Academy of Sciences of the United States of America. 2012; 109:47-52.
54. Roberts BR, Lim NK, McAllum EJ, Donnelly PS, Hare DJ, Doble PA, Turner BJ, Price KA, Lim SC, Paterson BM, Hickey JL, Rhoads TW, Williams JR, Kanninen KM, Hung LW, Liddell JR, et al. Oral treatment with Cu(II)(atsm) increases mutant SOD1 in vivo but protects motor neurons and improves the phenotype of a transgenic mouse model of amyotrophic lateral sclerosis. The Journal of Neuroscience. 2014; 34:8021-8031.
55. Zaichick V, Sviridova TV and Zaichick SV. Zinc in the human prostate gland: normal, hyperplastic and cancerous. International Urology and Nephrology. 1997; 29:565-574.
56. Kolenko V, Teper E, Kutikov A and Uzzo R. Zinc and zinc transporters in prostate carcinogenesis. Nature Reviews Urology. 2013; 10:219-226.
57. Costello LC, Franklin RB, Zou J and Naslund MJ. Evidence that Human Prostate Cancer is a ZIP1-Deficient Malignancy that could be Effectively Treated with a Zinc Ionophore (Clioquinol) Approach. Chemotherapy (Los Angel). 2015; 4.
58. Kumar B, Koul S, Khandrika L, Meacham RB and Koul HK. Oxidative stress is inherent in prostate cancer cells and is required for aggressive phenotype. Cancer Research. 2008; 68:1777-1785.
59. Freitas M, Baldeiras I, Proenca T, Alves V, Mota-Pinto A and Sarmento-Ribeiro A. Oxidative stress adaptation in aggressive prostate cancer may be counteracted by the reduction of glutathione reductase. FEBS Open Bio. 2012; 2:119-128.
60. Paschos A, Pandya R, Duivenvoorden WC and Pinthus JH. Oxidative stress in prostate cancer: changing research concepts towards a novel paradigm for prevention and therapeutics. Prostate Cancer and Prostatic Diseases. 2013; 16:217-225.
61. Zha J, Chen F, Dong H, Shi P, Yao Y, Zhang Y, Li R, Wang S, Li P, Wang W and Xu B. Disulfiram targeting lymphoid malignant cell lines via ROS-JNK activation as well as Nrf2 and NF-kB pathway inhibition. Journal of Translational Medicine. 2014; 12:163.
62. Mieyal JJ, Gallogly MM, Qanungo S, Sabens EA and Shelton MD. Molecular mechanisms and clinical implications of reversible protein S-glutathionylation. Antioxidants & Redox Signaling. 2008; 10:1941-1988.
63. Allen EM and Mieyal JJ. Protein-thiol oxidation and cell death: regulatory role of glutaredoxins. Antioxidants & Redox Signaling. 2012; 17:1748-1763.
64. Moskaluk CA, Duray PH, Cowan KH, Linehan M and Merino MJ. Immunohistochemical expression of pi-class glutathione S-transferase is down-regulated in adenocarcinoma of the prostate. Cancer. 1997; 79:1595-1599.
65. Traverso N, Ricciarelli R, Nitti M, Marengo B, Furfaro AL, Pronzato MA, Marinari UM and Domenicotti C. Role of glutathione in cancer progression and chemoresistance. Oxidative Medicine and Cellular Longevity. 2013; 2013:972913.
66. 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 and Differentiation. 2004; 11:737-746.
67. Voskoboinik I, Greenough M, La Fontaine S, Mercer JF and Camakaris J. Functional studies on the Wilson copper P-type ATPase and toxic milk mouse mutant. Biochemical and biophysical Research Communications. 2001; 281:966-970.
68. Chan HW, Liu T, Verdile G, Bishop G, Haasl RJ, Smith MA, Perry G, Martins RN and Atwood CS. Copper Induces Apoptosis of Neuroblastoma Cells Via Post-translational Regulation of the Expression of Bcl-2-family Proteins and the tx Mouse is a Better Model of Hepatic than Brain Cu Toxicity. International Journal of Clinical and Experimental Medicine. 2008; 1:76-88.
69. Meyer LA, Durley AP, Prohaska JR and Harris ZL. Copper transport and metabolism are normal in aceruloplasminemic mice. The Journal of Biological Chemistry. 2001; 276:36857-36861.
70. Gingras B, Suprunchuk T and Bayley C. The preparation of some thiosemicarbazones and their copper complexes: Part III. Canadian Journal of Chemistry. 1962; 40:1053-1059.
71. Schosinsky KH, Lehmann HP and Beeler MF. Measurement of ceruloplasmin from its oxidase activity in serum by use of o-dianisidine dihydrochloride. Clinical Chemistry. 1974; 20:1556-1563.
72. McDermott GP, Francis PS, Holt KJ, Scott KL, Martin SD, Stupka N, Barnett NW and Conlan XA. Determination of intracellular glutathione and glutathione disulfide using high performance liquid chromatography with acidic potassium permanganate chemiluminescence detection. Analyst. 2011; 136:2578-2585.
73. Smith ZM, Terry JM, Barnett NW, Gray LJ, Wright DJ and Francis PS. Enhancing permanganate chemiluminescence detection for the determination of glutathione and glutathione disulfide in biological matrices. Analyst. 2014; 139:2416-2422.
74. Terry JM, Adcock JL, Olson DC, Wolcott DK, Schwanger C, Hill LA, Barnett NW and Francis PS. Chemiluminescence detector with a serpentine flow cell. Analytical Chemistry. 2008; 80:9817-9821.
75. Llanos RM, Ke BX, Wright M, Deal Y, Monty F, Kramer DR and Mercer JF. Correction of a mouse model of Menkes disease by the human Menkes gene. Biochim Biophys Acta. 2006; 1762:485-493.