Supramolecular Iron Cylinder with Unprecedented DNA Binding Is a Potent Cytostatic and Apoptotic Agent without Exhibiting Genotoxicity

Chemistry and Biology

Volumn 15, Issue 12, 2008, Pages 1258-1267

  Hotze, Anna C G ^a   Hodges, Nikolas J ^a   Hayden, Rachel E ^a   Sanchez Cano, Carlos ^a   Paines, Christopher ^a   Male, Natalia ^a   Tse, Man Kit ^a   Bunce, Chris M ^a   Chipman, J Kevin ^a   Hannon, Michael J ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

CHEMBIO; DNA

Indexed keywords

CISPLATIN; CYTOSTATIC AGENT; DNA; FERROUS ION;

APOPTOSIS; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; DOUBLE STRANDED DNA BREAK; DRUG EFFECT; HUMAN; IC 50; METABOLISM; MITOCHONDRION; MUTAGEN TESTING; NEOPLASM; SYNTHESIS; TUMOR CELL LINE;

APOPTOSIS; CELL LINE, TUMOR; CISPLATIN; CYTOSTATIC AGENTS; DNA; DNA BREAKS, DOUBLE-STRANDED; FERROUS COMPOUNDS; HUMANS; INHIBITORY CONCENTRATION 50; MITOCHONDRIA; MODELS, MOLECULAR; MUTAGENICITY TESTS; NEOPLASMS;

EID: 57649152998     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2008.10.016     Document Type: Article

References (59)

1. Aung L., Gorlick R.G., Shi W., Thaler H., Shorter N.A., Healey J.H., Huvos A.G., and Meyers P.A. Second malignant neoplasms in long-term survivors of osteosarcoma: Memorial Sloan-Kettering Cancer Center Experience. Cancer 95 (2002) 1728-1734
2. Baraldi P.G., Bovero A., Fruttarolo F., Preti D., Tabrizi M.A., Pavani M.G., and Romagnoli R. DNA minor groove binders as potential antitumor and antimicrobial agents. Med. Res. Rev. 24 (2004) 475-528
3. Cerasino L., Hannon M.J., and Sletten E. DNA three-way junction with a dinuclear iron(II) supramolecular helicate at the center: a NMR structural study. Inorg. Chem. 46 (2007) 6245-6251
4. Charbonniere L.J., Williams A.F., Piguet C., Bernardinelli G., and Rivara-Minten E. Structural, magnetic, and electrochemical properties of dinuclear triple helices: comparison with their mononuclear analogues. Chem. Eur. J. 4 (1998) 485-493
5. Childs L.J., and Hannon M.J. Helices and helicates. Supramol. Chem. 16 (2004) 7-22
6. Cohen S.M., and Lippard S.J. Cisplatin: from DNA damage to cancer therapy. Prog. Nucleic Acid Res. Mol. Biol. 67 (2001) 93-130
7. Da Ros T., Spalluto G., Prato M., Saison-Behmoaras T., Boutorine A., and Cacciari B. Oligonucleotides and oligonucleotide conjugates: a new approach for cancer treatment. Curr. Med. Chem. 12 (2005) 71-88
8. Dervan P.B. Molecular recognition of DNA by small molecules. Bioorg. Med. Chem. 9 (2001) 2215-2235
9. Duez P., Dehon G., Kumps A., and Dubois J. Statistics of the Comet assay: a key to discriminate between genotoxic effects. Mutagenesis 18 (2003) 159-166
10. Escudero M.C., Lassaletta A., Sevilla J., Fernandez-Plaza S., Pérez A., Diaz M.A., and Madero L. Chemotherapy-related secondary acute myeloid leukemia in patients diagnosed with osteosarcoma. J. Pediatr. Hematol. Oncol. 26 (2004) 454-456
11. Fadeel B., and Orrenius S. Apoptosis: a basic biological phenomenon with wide-ranging implications in human disease. J. Intern. Med. 6 (2005) 479-517
12. Fisher D.M., Bednarski P.J., Grunert R., Turner P., Fenton R.R., and Aldrich-Wright J.R. Chiral platinum(II) metallointercalators with potent in vitro cytotoxic activity. ChemMedChem 2 (2007) 488-495
13. Fogh J., and Orfeo T. One hundred and twenty seven cultured human tumour cell lines producing tumours in nude mice. J. Natl. Cancer Inst. 59 (1977) 221-226
14. Fogh J., Wright W., and Loveless J. Absence of HeLa cell contamination in 169 cell lines derived from human tumours. J. Natl. Cancer Inst. 58 (1977) 209-214
15. Freake H., Marcocci C., Iwasaki J., and MacIntyre I. 1,25-dihydroxyvitamin D3 specifically binds to a human breast cancer cell line (T47D) and stimulates growth. Biochem. Biophys. Res. Commun. 101 (1981) 1131-1138
16. Gallagher R., Collins S., Trujillo J., McCredie K., Ahearn M., Tsai S., Metzgar R., Aulakh G., Ting R., Ruscett F., and Gallo R. Characterization of the continuous, differentiating myeloid cell line (HL-60) from a patient with acute promyelocytic leukemia. Blood 54 (1979) 713-733
17. Gebel T., Lantzsch H., Plessow K., and Dunkelberg H. Genotoxicity of platinum and palladium compounds on human and bacterial cells. Mutat. Res. 389 (1997) 183-190
18. Guo Z.J., and Sadler P.J. Medicinal inorganic chemistry. Adv. Inorg. Chem. 49 (2000) 183-306
19. Hannon M.J. Supramolecular DNA recognition. Chem. Soc. Rev. 36 (2007) 280-295
20. Hannon M.J. Metal-based anticancer drugs: from a past anchored in platinum chemistry to a post-genomic future of diverse chemistry and biology. Pure Appl. Chem. 79 (2007) 2243-2261
21. Hannon M.J., Moreno V., Prieto M.J., Molderheim E., Sletten E., Meistermann I., Isaac C.J., Sanders K.J., and Rodger A. Intramolecular DNA coiling mediated by a metallo-supramolecular cylinder. Angew. Chem. Int. Ed. Engl. 40 (2001) 879-884
22. Hannon M.J., Meistermann I., Isaac C.J., Blomme C., Rodger A., and Aldrich-Wright J.R. A cheap yet effective chiral stationary phase for chromatographic resolution of metallo-supramolecular helicates. Chem. Commun. (2001) 1078-1079
23. Harris A.L., Yang X., Hegmans A., Povirk L., Ryan J., Kelland L., and Farrell N.P. Synthesis, characterization, and cytotoxicity of a novel highly charged trinuclear platinum compound. Enhancement of cellular uptake with charge. Inorg. Chem. 44 (2005) 9598-9600
24. 4+ (BBR 3464) with its noncovalent congeners. Mol. Pharmacol. 69 (2005) 666-672
25. Heffeter P., Jakupec M.A., Korner W., Wild S., von Keyserlingk N.G., Elbling L., Zorbas H., Korynevska A., Knasmuller S., Sutterluty H., et al. Multidrug-resistant cancer cells are preferential targets of the new antineoplastic lanthanum compound KP772 (FFC24). Biochem. Pharmacol. 71 (2006) 426-440
26. 2(L′, L″ = 2-phenylazopyridine, 2,2′-bipyridine). Eur. J. Inorg. Chem. 2005 (2005) 2648-2657
27. Hotze A.C.G., Kariuki B.M., and Hannon M.J. Dinuclear double-stranded metallosupramolecular ruthenium complexes: potential anticancer drugs. Angew. Chem. Int. Ed. Engl. 45 (2006) 4839-4842
28. Jacobs J.P. A simple medium for the propagation and maintenance of human diploid cell strains. Nature 210 (1966) 100-101
29. Jacobs J.P., Jones C., and Baille J.P. Characteristics of a human diploid cell designated MRC-5. Nature 227 (1970) 168-170
30. Kerckhoffs J.M.C.A., Peberdy J.C., Meistermann I., Childs L.J., Isaac C.J., Pearmund C.R., Reudegger V., Khalid S., Alcock N.W., Hannon M.J., and Rodger A. Enantiomeric resolution of supramolecular helicates with different surface topographies. Dalton Trans. (2007) 734-742
31. Keydar I., Chen L., Karby S., Weiss F., Delarea J., Radu M., Chaitcik S., and Brenner H. Establishment and characterization of a cell line of human breast carcinoma origin. Eur. J. Cancer 15 (1979) 659-670
32. Khalid S., Hannon M.J., Rodger A., and Rodger P.M. Simulations of DNA coiling around a synthetic supramolecular cylinder that binds in the DNA major groove. Chem. Eur. J. 12 (2006) 3493-3506
33. Komeda S., Moulaei T., Woods K., Chikuma M., Farrell N.P., and Williams L.D. A third mode of DNA binding: phosphate clamps by a polynuclear platinum complex. J. Am. Chem. Soc. 128 (2006) 16092-16103
34. Kramer R., Lehn J.M., DeCian A., and Fischer J. Self-assembly, structure and spontaneous resolution of a trinuclear triple-helix form an oligobipyridine ligand and Ni(II) ions. Angew. Chem. Int. Ed. Engl. 32 (1993) 703-706
35. Lacroix M. Persistent use of "false" cell lines. Int. J. Cancer 122 (2008) 1-4
36. Lee A.J., Hodges N.J., and Chipman J.K. Interindividual variability in response to sodium dichromate-induced oxidative DNA damage: role of the Ser326Cys polymorphism in the DNA-repair protein of 8-oxo-7,8-dihydro-2′-deoxyguanosine DNA glycosylase 1 (OGG1). Cancer Epidemiol. Biomarkers Prev. 14 (2005) 497-505
37. Lincoln P., and Nordén B. Binuclear complex. Patent (April 1999) PCT/SE98/01655
38. In: Lippert B. (Ed). Cisplatin: Chemistry and Biochemistry of a Leading Anticancer Drug (1999), Wiley-VCH, Weinheim, Germany
39. Malina J., Hannon M.J., and Brabec V. Recognition of DNA three-way junctions by metallosupramolecular cylinders: gel electrophoresis studies. Chem. Eur. J. 13 (2007) 3871-3877
40. Maron D.M., and Ames B.N. Revised methods for the Salmonella mutagenicity test. Mutat. Res. 113 (1983) 173-215
41. Martínez R., and Chacón-García L. The search of DNA-intercalators as antitumoral drugs: what worked and what did not work. Curr. Med. Chem. 12 (2005) 127-151
42. Matsuba Y., Edatsugi E., Mita I., Matsunaga A., and Nakanishi O. A novel synthetic DNA minor groove binder, MS-247: antitumor activity and cytotoxic mechanism. Cancer Chemother. Pharmacol. 46 (2000) 1-9
43. Meistermann I., Moreno V., Prieto M.J., Moldrheim E., Sletten E., Khalid S., Rodger P.M., Peberdy J.C., Isaac C.J., Rodger A., and Hannon M.J. Intramolecular DNA coiling mediated by metallo-supramolecular cylinders: differential binding of P and M helical enantiomers. Proc. Natl. Acad. Sci. USA 99 (2002) 5069-5074
44. Moldrheim E., Hannon M.J., Meistermann I., Rodger A., and Sletten E. Interaction between a DNA oligonucleotide and a dinuclear iron(II) supramolecular cylinder; an NMR and molecular dynamics study. J. Biol. Inorg. Chem. 7 (2002) 770-780
45. Nielsen P.E. Targeting double stranded DNA with peptide nucleic acid (PNA). Curr. Med. Chem. 8 (2001) 545-550
46. Oleksi A., Blanco A.G., Boer R., Uson I., Aymami J., Rodger A., Hannon M.J., and Coll M. Molecular recognition of a three-way DNA junction by a metallosupramolecular helicate. Angew. Chem. Int. Ed. Engl. 45 (2006) 1227-1231
47. Olive P.L., and Durand R.E. Heterogeneity in DNA damage using the Comet assay. Cytometry A 66 (2005) 1-8
48. Önfelt B., Göstring L., Lincoln P., Nordén P., and Önfelt A. Cell studies of the DNA bis-intercalator δ-δ [μ-C4(cpdppz)(2)-(phen)(4)Ru(2)](4+): toxic effects and properties as a light emitting DNA probe in V79 Chinese hamster cells. Mutagenesis 17 (2002) 317-320
49. Pascu G.I., Hotze A.C.G., Sanchez Cano C., Kariuki B.M., and Hannon M.J. Dinuclear ruthenium(II) triple-stranded helicates: luminescent supramolecular cylinders that bind and coil DNA and exhibit activity against cancer cell lines. Angew. Chem. Int. Ed. Engl. 46 (2007) 4374-4378
50. Peberdy J.C., Malina J., Khalid S., Hannon M.J., and Rodger A. Influence of surface shape on DNA binding of bimetallo helicates. J. Inorg. Biochem. 101 (2007) 1937-1945
51. Reedijk J. Improved understanding in platinium antitumour chemistry. Chem. Commun. (1996) 801-806
52. Singh N.P. A simple method for accurate estimation of apoptotic cells. Exp. Cell Res. 256 (2000) 328-337
53. Singh N.P., McCoy M.T., Tice R.R., and Schneider E.L. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp. Cell Res. 175 (1988) 184-191
54. Takahara P.M., Rosenzweig A.C., Frederick C.A., and Lippard S.J. Crystal structure of double-stranded DNA containing the major adduct of the anticancer drug cisplatin. Nature 377 (1995) 649-652
55. Thuong N.T., and Helene C. Sequence-specific recognition and modification of double-helical DNA by oligonucleotides. Angew. Chem. Int. Ed. Engl. 32 (1993) 666-690
56. Uno Y., and Morita M. Mutagenic activity of some platinum and palladium complexes. Mutat. Res. 298 (1993) 269-275
57. Wang X., Cheung H.W., Chun A.C., Jin D.Y., and Wong Y.C. Mitotic checkpoint defects in human cancers and their implications to chemotherapy. Front. Biosci. 13 (2008) 2103-2114
58. Wheate N.J., Brodie C.R., Collins J.G., Kemp S., and Aldrich-Wright J.R. DNA intercalators in cancer therapy: organic and inorganic drugs and their spectroscopic tools of analysis. Mini Rev. Med. Chem. 7 (2007) 627-648
59. Wierecky J., Kollmannsberger C., Boehlke I., Kuczyk M., Schleicher J., Schleucher N., Metzner B., Kanz L., Hartmann J.T., and Bokemeyer C. Secondary leukemia after first-line high-dose chemotherapy for patients with advanced germ cell cancer. J. Cancer Res. Clin. Oncol. 131 (2005) 255-260