Modulation of Wnt/Β-catenin signaling and proliferation by a ferrous iron chelator with therapeutic efficacy in genetically engineered mouse models of cancer

Oncogene

Volumn 31, Issue 2, 2012, Pages 213-225

  Coombs, G S ^a   Schmitt, A A ^b   Canning, C A ^c   Alok, A ^a   Low, I C C ^d   Banerjee, N ^e   Kaur, S ^a   Utomo, V ^a   Jones, C M ^c   Pervaiz, S ^d   Toone, E J ^b   Virshup, D M ^a,d,f  

^a DUKE NUS MEDICAL SCHOOL   (Singapore)

^b DUKE UNIVERSITY   (United States)

^c INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^f DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

drug therapy; iron; iron chelator; mouse models of cancer; Wnt b catenin

Indexed keywords

BENZAMIDE DERIVATIVE; BETA CATENIN; IRON CHELATING AGENT; N [(8 HYDROXY 7 QUINOLINYL)(4 METHYLPHENYL)METHYL]BENZAMIDE; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER GROWTH; CANCER INHIBITION; CANCER MODEL; CELL PROLIFERATION; CHICK EMBRYO; CONTROLLED STUDY; DISSOCIATION CONSTANT; DRUG DOSE COMPARISON; DRUG MECHANISM; EMBRYO; FEMALE; GENETIC ENGINEERING; HUMAN; HUMAN CELL; MOUSE; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; BETA CATENIN; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; FERROUS COMPOUNDS; GENETIC ENGINEERING; IRON CHELATING AGENTS; MICE; NEOPLASMS; SIGNAL TRANSDUCTION; WNT PROTEINS;

MOUSE MAMMARY TUMOR VIRUS; MUS;

EID: 84855758079     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.228     Document Type: Article

References (33)

1. Bergeron RJ, Streiff RR, Creary EA, Daniels Jr RD, King W, Luchetta G et al. (1993). A comparative study of the iron-clearing properties of desferrithiocin analogues with desferrioxamine B in a Cebus monkey model. Blood 81: 2166-2173. (Pubitemid 23106734)
2. Bergeron RJ, Wiegand J, Weimar WR, Vinson JR, Bussenius J, Yao GW et al. (1999). Desazadesmethyldesferrithiocin analogues as orally effective iron chelators. J Med Chem 42: 95-108. (Pubitemid 29056492)
3. BrookesMJ, Boult J, Roberts K, Cooper BT, Hotchin NA, Matthews G et al. (2008). A role for iron in Wnt signalling. Oncogene 27: 966-975. (Pubitemid 351225389)
4. Canning CA, Lee L, Irving C, Mason I, Jones CM. (2007). Sustained interactive Wnt and FGF signaling is required to maintain isthmic identity. Dev Biol 305: 276-286. (Pubitemid 46589418)
5. Coombs GS, Covey TM, Virshup DM. (2008). Wnt signaling in development, disease and translational medicine. Curr Drug Targets 9: 513-531.
6. Coombs GS, Yu J, Canning CA, Veltri CA, Covey TM, Cheong JK et al. (2010). WLS-dependent secretion of WNT3A requires Ser209 acylation and vacuolar acidification. J Cell Sci 123: 3357-3367.
7. DiTusa CA, Christensen T, McCall KA, Fierke CA, Toone EJ. (2001). Thermodynamics of metal ion binding. 1. Metal ion binding by wild-type carbonic anhydrase. Biochemistry 40: 5338-5344. (Pubitemid 32458233)
8. Eberhard Y, McDermott SP, Wang X, Gronda M, Venugopal A, Wood TE et al. (2009). Chelation of intracellular iron with the antifungal agent ciclopirox olamine induces cell death in leukemia and myeloma cells. Blood 114: 3064-3073.
9. Guy CT, Cardiff RD, Muller WJ. (1992). Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol Cell Biol 12: 954-961.
10. Henderson WR, Chi EY, Ye X, Nguyen C, Tien Y-T, Zhou B et al. (2010). Inhibition of Wnt/beta-catenin/CREB binding protein (CBP) signaling reverses pulmonary fibrosis. Proc Natl Acad Sci USA 107: 14309-14314.
11. Herschkowitz JI, Simin K, Weigman VJ, Mikaelian I, Usary J, Hu Z et al. (2007). Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biol 8: R76.
12. Hodges YK, Antholine WE, Horwitz LD. (2004). Effect on ribonucleotide reductase of novel lipophilic iron chelators: the desferri-exochelins. Biochem Biophys Res Commun 315: 595-598. (Pubitemid 38229385)
13. Jaakkola P, Mole DR, Tian YM, Wilson MI, Gielbert J, Gaskell SJ et al. (2001). Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292: 468-472. (Pubitemid 32335942)
14. Jansson PJ, Hawkins CL, Lovejoy DB, Richardson DR. (2010). The iron complex of Dp44mT is redox-active and induces hydroxyl radical formation: an EPR study. J Inorg Biochem 104: 1224-1228.
15. Keberle H. (1964). The biochemistry of desferrioxamine and its relation to iron metabolism. Ann N Y Acad Sci 119: 758-768.
16. Lamb J, Crawford ED, Peck D, Modell JW, Blat IC, Wrobel MJ et al. (2006). The Connectivity Map: using gene-expression signatures to connect small molecules, genes, and disease. Science 313: 1929-1935. (Pubitemid 44497995)
17. Lamb J. (2007). The Connectivity Map: a new tool for biomedical research. Nat Rev Cancer 7: 54-60. (Pubitemid 46020847)
18. Lucero OM, Dawson DW, Moon RT, Chien AJ. (2010). A reevaluation of the 'oncogenic' nature of Wnt/beta-catenin signaling in melanoma and other cancers. Curr Oncol Rep 12: 314-318.
19. McCulloch MW, Bugni TS, Concepcion GP, Coombs GS, Harper MK, Kaur S et al. (2009a). Carteriosulfonic acids A-C, GSK-3beta inhibitors from a Carteriospongia sp. J Nat Prod 72: 1651-1656.
20. McCulloch MW, Coombs GS, Banerjee N, Bugni TS, Cannon KM, Harper MK et al. (2009b). Psammaplin A as a general activator of cell-based signaling assays via HDAC inhibition and studies on some bromotyrosine derivatives. Bioorg Med Chem 17: 2189-2198.
21. Mosimann C, Hausmann G, Basler K. (2009). Beta-catenin hits chromatin: regulation of Wnt target gene activation. Nat Rev Mol Cell Biol 10: 276-286.
22. Pang H, Bartlam M, Zeng Q, Miyatake H, Hisano T, Miki K et al. (2004). Crystal structure of human pirin: an iron-binding nuclear protein and transcription cofactor. J Biol Chem 279: 1491-1498. (Pubitemid 38082678)
23. Phelps RA, Chidester S, Dehghanizadeh S, Phelps J, Sandoval IT, Rai K et al. (2009). A two-step model for colon adenoma initiation and progression caused by APC loss. Cell 137: 623-634.
24. Rai K, Sarkar S, Broadbent TJ, Voas M, Grossmann KF, Nadauld LD et al. (2010). DNA demethylase activity maintains intestinal cells in an undifferentiated state following loss of APC. Cell 142: 930-942.
25. Richardson DR, Kalinowski DS, Lau S, Jansson PJ, Lovejoy DB. (2009). Cancer cell iron metabolism and the development of potent iron chelators as anti-tumour agents. Biochim Biophys Acta 1790: 702-717.
26. Rutherford JC, Bird AJ. (2004). Metal-responsive transcription factors that regulate iron, zinc, and copper homeostasis in eukaryotic cells. Eukaryot Cell 3: 1-13. (Pubitemid 38237293)
27. Sheftel A, Stehling O, Lill R. (2010). Iron-sulfur proteins in health and disease. Trends Endocrinol Metab 21: 302-314.
28. Sigurskjold BW. (2000). Exact analysis of competition ligand binding by displacement isothermal titration calorimetry. Anal Biochem 277: 260-266. (Pubitemid 30055877)
29. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y et al. (2009). Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324: 930-935.
30. Teo JL, Kahn M. (2010). The Wnt signaling pathway in cellular proliferation and differentiation: a tale of two coactivators. Adv Drug Deliv Rev 62: 1149-1155.
31. Tian J, Peehl DM, Zheng W, Knox SJ. (2010). Anti-tumor and radiosensitization activities of the iron chelator HDp44mT are mediated by effects on intracellular redox status. Cancer Lett 298: 231-237.
32. Tomayko MM, Reynolds CP. (1989). Determination of subcutaneous tumor size in athymic (nude) mice. Cancer Chemother Pharmacol 24: 148-154. (Pubitemid 19163397)
33. Zhou H, Shen T, Luo Y, Liu L, Chen W, Xu B et al. (2010). The antitumor activity of the fungicide ciclopirox. Int J Cancer 127: 2467-2477.