Rapid Copper Acquisition by Developing Murine Mesothelioma: Decreasing Bioavailable Copper Slows Tumor Growth, Normalizes Vessels and Promotes T Cell Infiltration

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Crowe, Andrew ^a   Jackaman, Connie ^a   Beddoes, Katie M ^a   Ricciardo, Belinda ^a   Nelson, Delia J ^a  

^a CURTIN UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CHELATING AGENT; CISPLATIN; COPPER; INTERCELLULAR ADHESION MOLECULE 1; KI 67 ANTIGEN; PENICILLAMINE; TETRATHIOMOLYBDIC ACID; TRIENTINE; VASCULOTROPIN; VASCULOTROPIN ANTIBODY; VASCULOTROPIN RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; ATOMIC ABSORPTION SPECTROMETRY; CANCER STAGING; CD4+ T LYMPHOCYTE; CELL PROLIFERATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; FLOW CYTOMETRY; IN VIVO STUDY; LYMPHOCYTIC INFILTRATION; MESOTHELIOMA; MOUSE; NONHUMAN; TREATMENT OUTCOME; TUMOR GROWTH;

ANIMALS; CELL PROLIFERATION; CHELATING AGENTS; COPPER; ENDOTHELIAL CELLS; FEMALE; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; KI-67 ANTIGEN; MESOTHELIOMA; MICE; NEOPLASM PROTEINS; NEOVASCULARIZATION, PATHOLOGIC; T-LYMPHOCYTES;

EID: 84883179964     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073684     Document Type: Article

References (48)

1. Folkman J, (2007) Angiogenesis: an organizing principle for drug discovery? Nat Rev Drug Discov 6: 273-286. doi:10.1038/nrd2115. PubMed: 17396134.
2. Sun S, Schiller JH, (2007) Angiogenesis inhibitors in the treatment of lung cancer. Crit Rev Oncol/Hematol 62: 93-104. doi:10.1016/j.critrevonc.2007.01.002.
3. Rosen LS, (2005) VEGF-targeted therapy: therapeutic potential and recent advances. Oncologist 10: 382-391. doi:10.1634/theoncologist.10-6-382. PubMed: 15967832.
4. Brewer GJ, (2005) Copper lowering therapy with tetrathiomolybdate as an antiangiogenic strategy in cancer. Curr Cancer Drug Targets 5: 195-202. doi:10.2174/1568009053765807. PubMed: 15892619.
5. Pan Q, Kleer CG, van Golen KL, Irani J, Bottema KM, et al. (2002) Copper deficiency induced by tetrathiomolybdate suppresses tumor growth and angiogenesis. Cancer Res 62: 4854-4859. PubMed: 12208730.
6. Hassouneh B, Islam M, Nagel T, Pan Q, Merajver SD, et al. (2007) Tetrathiomolybdate promotes tumor necrosis and prevents distant metastases by suppressing angiogenesis in head and neck cancer. Mol Cancer Ther 6: 1039-1045. doi:10.1158/1535-7163.MCT-06-0524. PubMed: 17363496.
7. Montenegro MA, Sanchez Negrette M, Gimeno EJ, Borda JT, (2002) Effects of high molybdenum intake on 1,2-dimethylhydrazine-induced intestinal tumors in rats. Biocell: official journal of the Sociedades Latinoamericanas de Microscopia Electronica et al 26: 339-345.
8. Cox C, Merajver SD, Yoo S, Dick RD, Brewer GJ, et al. (2003) Inhibition of the growth of squamous cell carcinoma by tetrathiomolybdate-induced copper suppression in a murine model. Arch Otolaryngol Head Neck Surg 129: 781-785. doi:10.1001/archotol.129.7.781. PubMed: 12874082.
9. Gartner EM, Griffith KA, Pan Q, Brewer GJ, Henja GF, et al. (2009) A pilot trial of the anti-angiogenic copper lowering agent tetrathiomolybdate in combination with irinotecan, 5-flurouracil, and leucovorin for metastatic colorectal cancer. Invest New Drugs 27: 159-165. doi:10.1007/s10637-008-9165-9. PubMed: 18712502.
10. Redman BG, Esper P, Pan Q, Dunn RL, Hussain HK, et al. (2003) Phase II trial of tetrathiomolybdate in patients with advanced kidney cancer. Clin Cancer Res Off J Am Assoc Cancer Res 9: 1666-1672. PubMed: 12738719.
11. Pass HI, Brewer GJ, Dick R, Carbone M, Merajver S, (2008) A phase II trial of tetrathiomolybdate after surgery for malignant mesothelioma: final results. Ann Thorac Surg 86: 383-389; discussion 390 doi:10.1016/j.athoracsur.2008.03.016. PubMed: 18640301.
12. Brem SS, Zagzag D, Tsanaclis AM, Gately S, Elkouby MP, et al. (1990) Inhibition of angiogenesis and tumor growth in the brain. Suppression of endothelial cell turnover by penicillamine and the depletion of copper, an angiogenic cofactor. Am J Pathol 137: 1121-1142. PubMed: 1700617.
13. Jain RK, (2005) Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 307: 58-62. doi:10.1126/science.1104819. PubMed: 15637262.
14. Carmeliet P, Jain RK, (2011) Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases. Nat Rev Drug Discov 10: 417-427. doi:10.1038/nrd3455. PubMed: 21629292.
15. Hamzah J, Jugold M, Kiessling F, Rigby P, Manzur M, et al. (2008) Vascular normalization in Rgs5-deficient tumours promotes immune destruction. Nature 453: 410-414. doi:10.1038/nature06868. PubMed: 18418378.
16. Robinson BW, Musk AW, Lake RA, (2005) Malignant mesothelioma. Lancet 366: 397-408. doi:10.1016/S0140-6736(05)67025-0. PubMed: 16054941.
17. Jackaman C, Bundell CS, Kinnear BF, Smith AM, Filion P, et al. (2003) IL-2 intratumoral immunotherapy enhances CD8+ T cells that mediate destruction of tumor cells and tumor-associated vasculature: a novel mechanism for IL-2. J Immunol 171: 5051-5063. PubMed: 14607902.
18. Klein D, Lichtmannegger J, Heinzmann U, Summer KH, (2000) Dissolution of copper-rich granules in hepatic lysosomes by D-penicillamine prevents the development of fulminant hepatitis in Long-Evans cinnamon rats. J Hepatol 32: 193-201. doi:10.1016/S0168-8278(00)80063-X. PubMed: 10707858.
19. Goodman VL, Brewer GJ, Merajver SD, (2004) Copper deficiency as an anti-cancer strategy. Endocr Relat Cancer 11: 255-263. doi:10.1677/erc.0.0110255. PubMed: 15163301.
20. Siegemund R, Lössner J, Günther K, Kühn HJ, Bachmann H, (1991) Mode of action of triethylenetetramine dihydrochloride on copper metabolism in Wilson's disease. Acta Neurol Scand 83: 364-366. doi:10.1111/j.1600-0404.1991.tb03964.x. PubMed: 1887758.
21. Hou G, Dick R, Zeng C, Brewer GJ, (2006) Comparison of lowering copper levels with tetrathiomolybdate and zinc on mouse tumor and doxorubicin models. Transl Res 148: 309-314. doi:10.1016/j.trsl.2006.06.005. PubMed: 17162252.
22. Hou G, Dick R, Zeng C, Brewer GJ, (2007) Antitumor and antiinflammatory effects of tetrathiotungstate in comparison with tetrathiomolybdate. Transl Res J Lab Clin Med 149: 260-264. doi:10.1016/j.trsl.2006.12.003. PubMed: 17466925.
23. Prewett M, Huber J, Li Y, Santiago A, O'Connor W, et al. (1999) Antivascular endothelial growth factor receptor (fetal liver kinase 1) monoclonal antibody inhibits tumor angiogenesis and growth of several mouse and human tumors. Cancer Res 59: 5209-5218. PubMed: 10537299.
24. Crowe A, Morgan EH, (1996) Iron and copper interact during their uptake and deposition in the brain and other organs of developing rats exposed to dietary excess of the two metals. J Nutr 126: 183-194. PubMed: 8558300.
25. Zowczak M, Iskra M, Paszkowski J, Mańczak M, Torliński L, et al. (2001) Oxidase activity of ceruloplasmin and concentrations of copper and zinc in serum of cancer patients. J Trace Elem Med Biol 15: 193-196. doi:10.1016/S0946-672X(01)80066-3. PubMed: 11787988.
26. Wei H, Frei B, Beckman JS, Zhang WJ, (2011) Copper Chelation by Tetrathiomolybdate Inhibits Lipopolysaccharide-Induced Inflammatory Responses in Vivo. Am J Physiol Heart Circ Physiol, 301: H712-20. PubMed: 21724870.
27. Brewer GJ, Dick RD, Grover DK, LeClaire V, Tseng M, et al. (2000) Treatment of metastatic cancer with tetrathiomolybdate, an anticopper, antiangiogenic agent: Phase I study. Clin Cancer Res 6: 1-10. PubMed: 10656425.
28. Tanaka F, Otake Y, Yanagihara K, Kawano Y, Miyahara R, et al. (2001) Evaluation of angiogenesis in non-small cell lung cancer: comparison between anti-CD34 antibody and anti-CD105 antibody. Clin Cancer Res Off J Am Assoc Cancer Res 7: 3410-3415. PubMed: 11705856.
29. Youdim MB, Grünblatt E, Mandel S, (2007) The copper chelator, D-penicillamine, does not attenuate MPTP induced dopamine depletion in mice. J Neural Transm 114: 205-209. doi:10.1007/s00702-006-0499-1. PubMed: 16736232.
30. Brewer GJ, (2005) Anticopper therapy against cancer and diseases of inflammation and fibrosis. Drug Discov Today 10: 1103-1109. doi:10.1016/S1359-6446(05)03541-5. PubMed: 16182195.
31. Deering TB, Dickson ER, Fleming CR, Geall MG, McCall JT, et al. (1977) Effect of D-penicillamine on copper retention in patients with primary billiary cirrhosis. Gastroenterology 72: 1208-1212. PubMed: 870369.
32. Yoshii J, Yoshiji H, Kuriyama S, Ikenaka Y, Noguchi R, et al. (2001) The copper-chelating agent, trientine, suppresses tumor development and angiogenesis in the murine hepatocellular carcinoma cells. Int J Cancer 94: 768-773. doi:10.1002/ijc.1537. PubMed: 11745476.
33. Kadowaki S, Endoh D, Okui T, Hayashi M, (2009) Trientine, a copper-chelating agent, induced apoptosis in murine fibrosarcoma cells by activation of the p38 MAPK pathway. J Vet Med Sci 71: 1541-1544. doi:10.1292/jvms.001541. PubMed: 19959910.
34. Hayashi M, Nishiya H, Chiba T, Endoh D, Kon Y, et al. (2007) Trientine, a copper-chelating agent, induced apoptosis in murine fibrosarcoma cells in vivo and in vitro. J Vet Med Sci 69: 137-142. doi:10.1292/jvms.69.137. PubMed: 17339757.
35. Khan G, Merajver S, (2009) Copper chelation in cancer therapy using tetrathiomolybdate: an evolving paradigm. Expert Opin Investig Drugs 18: 541-548. doi:10.1517/13543780902845622. PubMed: 19335282.
36. Brewer GJ, (2009) The use of copper-lowering therapy with tetrathiomolybdate in medicine. Expert Opin Investig Drugs 18: 89-97. doi:10.1517/13543780802621859. PubMed: 19053885.
37. Goodman VL, Brewer GJ, Merajver SD, (2005) Control of copper status for cancer therapy. Curr Cancer Drug Targets 5: 543-549. doi:10.2174/156800905774574066. PubMed: 16305350.
38. Nasulewicz A, Mazur A, Opolski A, (2004) Role of copper in tumour angiogenesis--clinical implications. J Trace Elem Med Biol Organ Soc Miner Trace Elem 18: 1-8. doi:10.1016/j.jtemb.2004.02.004. PubMed: 15487757.
39. Brewer GJ, (2001) Copper control as an antiangiogenic anticancer therapy: lessons from treating Wilson's disease. Exp Biol Med 226: 665-673. PubMed: 11444102.
40. Richards MP, (1999) Zinc, copper, and iron metabolism during porcine fetal development. Biol Trace Elem Res 69: 27-44. doi:10.1007/BF02783913. PubMed: 10383097.
41. Lowndes SA, Harris AL, (2005) The role of copper in tumour angiogenesis. J Mammary Gland Biol Neoplasia 10: 299-310. doi:10.1007/s10911-006-9003-7. PubMed: 16924372.
42. Bachmanov AA, Reed DR, Beauchamp GK, Tordoff MG, (2002) Food intake, water intake, and drinking spout side preference of 28 mouse strains. Behav Genet 32: 435-443. doi:10.1023/A:1020884312053. PubMed: 12467341.
43. Brem S, (1999) Angiogenesis and Cancer Control: From Concept to Therapeutic Trial. Cancer Contr J Moffitt Cancer Center 6: 436-458. PubMed: 10758576.
44. Henry NL, Dunn R, Merjaver S, Pan Q, Pienta KJ, et al. (2006) Phase II trial of copper depletion with tetrathiomolybdate as an antiangiogenesis strategy in patients with hormone-refractory prostate cancer. Oncology 71: 168-175. doi:10.1159/000106066. PubMed: 17641535.
45. Schuschke DA, Reed MW, Saari JT, Olson MD, Ackermann DM, et al. (1992) Short-term dietary copper deficiency does not inhibit angiogenesis in tumours implanted in striated muscle. Br J Cancer 66: 1059-1064. doi:10.1038/bjc.1992.410. PubMed: 1280989.
46. Omari KM, Dorovini-Zis K, (2003) CD40 expressed by human brain endothelial cells regulates CD4+ T cell adhesion to endothelium. J Neuroimmunol 134: 166-178. doi:10.1016/S0165-5728(02)00423-X. PubMed: 12507785.
47. Hamzah J, Nelson D, Moldenhauer G, Arnold B, Hämmerling GJ, et al. (2008) Vascular targeting of anti-CD40 antibodies and IL-2 into autochthonous tumors enhances immunotherapy in mice. J Clin Invest 118: 1691-1699. doi:10.1172/JCI33201. PubMed: 18398504.
48. Liu L, Abken H, Pföhler C, Rappl G, Tilgen W, et al. (2000) Accumulation of CD4+CD7- T cells in inflammatory skin lesions: evidence for preferential adhesion to vascular endothelial cells. Clin Exp Immunol 121: 94-99. doi:10.1046/j.1365-2249.2000.01260.x. PubMed: 10886244.