Quadruplex DNA: A Promising Drug Target for the Medicinal Inorganic Chemist

Current Topics in Medicinal Chemistry

Volumn 11, Issue 5, 2011, Pages 572-590

  Ralph, Stephen F ^a  

^a UNIVERSITY OF WOLLONGONG   (Australia)

Author keywords

Metal complex; Porphyrin; Quadruplex dna; Telomerase

Indexed keywords

DIPYRIDO[3,2 A:2',3']PHENAZINE LIGAND; GUANINE QUADRUPLEX; MANGANESE; METAL COMPLEX; NICKEL; PALLADIUM COMPLEX; PHENANTHROLINE; PLATINUM COMPLEX; PLATINUM QUINACRIDINE; PLATINUM(II)PHENANTHROIMIDAZOLE COMPLEX; PORPHYRIN; SCHIFF BASE; TELOMERASE; UNCLASSIFIED DRUG; ZINC;

ARTICLE; BINDING AFFINITY; DNA BINDING; DNA STRUCTURE; DRUG TARGETING; HUMAN; HYDROGEN BOND; MONONUCLEAR CELL; NONHUMAN; STRUCTURE ACTIVITY RELATION; SUPRAMOLECULAR CHEMISTRY; TELOMERE;

APOPTOSIS; DNA, SINGLE-STRANDED; DRUG SCREENING ASSAYS, ANTITUMOR; ENZYME INHIBITORS; G-QUADRUPLEXES; HUMANS; HYPOGLYCEMIC AGENTS; NEOPLASMS; ORGANOMETALLIC COMPOUNDS; TELOMERASE;

EID: 79952749516     PISSN: 15680266     EISSN: None     Source Type: Journal    
DOI: 10.2174/156802611794785208     Document Type: Article

References (80)

1. Kim, N. W.; Piatyszek, M. A.; Prowse, K. R.; Harley, C. B.; West, M. D.; Ho, P. L. C.; Coviello, G. M.; Wright, W. E.; Weinrich, S. L.; Shay, J. W. Specific association of human telomerase activity with immortal cells and cancer. Science, 1994, 266, 2011-2015.
2. Bang, I. Untersuchungen uber die guanylsaure. Biochem. Z., 1910, 26, 293-311.
3. Gellert, M; Lipsett M. N.; Davies, D. R. Helix formation by guanylic acid. Proc. Natl. Acad. Sci. USA, 1962, 48, 2013-2018.
4. Oxford, S. F.; Gillespie, R. G. Evolution and ecology of spider coloration. Annu. Rev. Entomol., 1998, 43, 619-643.
5. Douglas, R. H.; Partridge, J. C.; Marshall, N. J. The eyes of deepsea fish I: Lens pigmentation, tapeta and visual pigments. Prog. Retinal Eye Res., 1998, 17, 597-636.
6. Sen, D.; Gilbert W. Formation of parallel four-stranded complexes by guanine-rich motifs in DNA and its implications for meiosis. Nature, 1988, 334, 364-366.
7. Sundquist, W. I.; Klug, A. Telomeric DNA dimerises by formation of guanine tetrads between hairpin loops. Nature, 1989, 342, 825-829.
8. Neidle, S.: Parkinson, G. Telomere maintenance as a target for anticancer drug discovery. Nat. Rev. Drug Discov., 2002, 1, 383-393.
9. Hahn, W. C.; Counter, C. M.; Lundberg, A. S.; Beijersbergen, R. L.; Brooks, M. W.; Weinberg, R. A. Creation of human tumour cells with defined genetic elements. Nature, 1999, 400, 464-468.
10. Hahn, W. C.; Stewart, S. A.; Brooks, M. W.; York, S. G.; Eaton, E.; Kurachi, A.; Beijersbergen, R. L.; Knoll, J. H. M.; Meyerson, M.; Weinberg, R. A. Inhibition of telomerase limits the growth of human cancer cells. Nat. Med., 1999, 5, 1164-1170.
11. Gilbert, D. E.; Feigon, J. Multistranded DNA structures. Curr. Opin. Struct. Biol., 1999, 9, 305-314.
12. Keniry, M. A. Quadruplex structures in nucleic acids. Biopolymers, 2001, 56, 123-146.
13. Simonsson, T. G-quadruplex DNA structures - variations on a theme. Biol. Chem., 2001, 382, 621-628.
14. Suhnel, J. Beyond nucleic acid base pairs: from triads to heptads. Biopolymers, 2002, 61, 32-51.
15. Burge, S.; Parkinson, G. N.; Hazel, P.; Todd, A. K.; Neidle, S. Quadruplex DNA: sequence, topology and structure. Nucleic Acids Res., 2006, 34, 5402-5415.
16. Sun, D.; Thompson, B.; Cathers, B. E.; Salazar, M.; Kerwin, S. M.; Trent, J. O.; Jenkins, T. C.; Neidle, S.; Hurley, L. H. Inhibition of human telomerase by a g-quadruplex-interactive compound. J. Med. Chem., 1997, 40, 2113-2116.
17. Han, H.; Hurley, L. H. G-quadruplex DNA: A potential target for anti-cancer drug design. Trends Pharmacol. Sci., 2000, 21, 136-142.
18. Kerwin, S. M. G-quadruplex DNA as a target for drug design. Curr. Pharm. Des., 2000, 6, 441-471.
19. Balasubramanian, S.; Neidle, S. G-quadruplex nucleic acids as therapeutic targets. Curr. Opin. Chem. Biol., 2009, 13, 345-353.
20. Arola, A.; Vilar, R. Stabilisation of G-quadruplex DNA by small molecules. Curr. Top. Med. Chem., 2008, 8, 1405-1415.
21. Huppert J. L.; Balasubramanian, S. G-quadruplexes in promoters throughout the human genome. Nucleic Acids Res., 2007, 35, 406-413.
22. Verma, A.; Halder, K.; Yadav, V. K.; Rawal, P.; Thakur, R. K.; Mohd, F.; Sharma, A.; Chowdhury, S. Genome-wide computational and expression analyses reveal g-quadruplex dna motifs as conserved cis-regulatory elements in human and related species. J. Med. Chem., 2008, 51, 5641-5649.
23. Siddiqui-Jain, A.; Grand, C. L.; Bearss, D J.; Hurley, L. H. Direct evidence for a g-quadruplex in a promoter region and its targeting with a small molecule to repress c-myc transcription. Proc. Natl. Acad. Sci. USA, 2002, 99, 11593-11598.
24. Bejugam M.; Sewitz, S.; Shirude, P.S.; Rodriguez, R.; Shahid, R.; Balasubramanian, S. trisubstituted isoalloxazines as a new class of g-quadruplex binding ligands: small molecule regulation of c-kit oncogene expression. J. Am. Chem. Soc., 2007, 129, 12926-12927.
25. Cogoi, S.; Xodo, L.E. G-quadruplex formation within the promoter of the kras proto-oncogene and its effect on transcription. Nucleic Acids Res., 2006, 34, 2536-2549.
26. Aboul-ela, F.; Murhie, A. I.; Lilley, D. M. NMR study of parallelstranded tetraplex formation by the hexadeoxynucleotide d(TG4T). Nature, 1992, 360, 280-282.
27. Phillips, K.; Dauter, Z.; Murchie, A. I.; Lilley, D. M.; Luisi, B. The crystal structure of a parallel-stranded guanine tetraplex at 0.95 Å resolution. J. Mol. Biol. 1997, 273, 171-182.
28. 3] G-tetraplex. Structure, 1993, 1, 263-282.
29. Parkinson, G. N.; Lee, M. P. H.; Neidle, S. Crystal structure of parallel quadruplexes from human telomeric DNA. Nature, 2002, 417, 876-880.
30. Campbell, N. H.; Parkinson, G. N.; Reszka, A. P.; Neidle, S. Structural basis of DNA quadruplex recognition by an acridine drug. J. Am. Chem. Soc., 2008, 130, 6722-6724.
31. Wheelhouse, R. T.; Sun, D.; Han, H.; Han, F. X.; Hurley, L. H. Cationic porphyrins as telomerase inhibitors: the interaction of tetra(N-methyl-4-pyridyl)porphine with quadruplex DNA. J. Am. Chem. Soc., 1998, 120, 3261-3262.
32. Shi, D.-F.; Wheelhouse, R. T.; Sun D.; Hurley, L. H. Quadruplexinteractive agents as telomerase inhibitors: synthesis of porphyrins and structure-activity relationship for the inhibition of telomerase. J. Med. Chem., 2001, 44, 4509-4523.
33. Vialas, C.; Pratviel, G.; Meunier, B. Oxidative damage generated by an oxo-metalloporphyrin onto the human telomeric sequence. Biochemistry, 2000, 39, 9514-9522.
34. Maraval, A.; Franco, S.; Vialas, C.; Pratviel, G.; Blasco, M. A.; Meunier, B. Porphyrin-aminoquinoline conjugates as telomerase inhibitors. Org. Biomol. Chem., 2003, 1, 921-927.
35. Keating, L. R.; Szalai, V.A. Parallel-stranded guanine quadruplex interactions with a copper cationic porphyrin. Biochemistry, 2004, 43, 15891-15900.
36. Goncalves, D. P. N.; Rodriquez, R.; Balasubramanian, S.; Sanders, J. K. M. Tetramethylpyridiniumporphyrazines - a new class of Gquadruplex inducing and stabilising ligands. Chem. Commun., 2006, 4685-4687.
37. Dixon, I. M.; Lopez, F.; Esteve, J.-P.; Tejera, A. M.; Blasco, M. A.; Pratviel, G.; Meunier, B. Porphyrin derivatives for telomere binding and telomerase inhibition. ChemBioChem, 2005, 6, 123-132.
38. Haq, I.; Trent, J. O.; Chowdhry, B. Z.; Jenkins, T. C. Intercalative g-tetraplex stabilization of telomeric DNA by a cationic porphyrin. J. Am. Chem. Soc., 1999, 121, 1768-1779.
39. Ren, L.; Zhang, A.; Huang, J.; Wang, P.; Weng, X.; Zhang, L.; Liang, F.; Tan, Z.; Zhou, X. Quaternary ammonium zinc phthalocyanine: inhibiting telomerase by stabilizing G quadruplexes and inducing g-quadruplex structure transition and formation. ChemBioChem, 2007, 8, 775-780.
40. Dixon, I. M.; Lopez, F.; Tejera, A. M.; Esteve, J.-P.; Blasco, M. A.; Prativiel, G.; Meunier, B. A G-quadruplex ligand with 10000-fold selectivity over duplex DNA. J. Am. Chem. Soc., 2007, 129, 1502-1503.
41. Shin-ya, K.; Wierzba, K.; Matsuo, K.; Ohtani, T.; Yamada, Y.; Furihata, K.; Hayakawa, Y.; Seto, H. Telomestatin, a novel telomerase inhibitor from Streptomyces anulatus. J. Am. Chem. Soc., 2001, 123, 1262-1263.
42. Reed, J.E.; Neidle, S.; Vilar, R. Stabilisation of human telomeric quadruplex DNA and inhibition of telomerase by a platinumphenanthroline complex. Chem. Commun., 2007, 4366-4368.
43. Schultes, C.M.; Guyen, B.; Cuesta J.; Neidle, S. Synthesis, biophysical and biological evaluation of 3,6-bis-amidoacridines with extended 9-anilino substituents as potent g-quadruplex-binding telomerase inhibitors. Bioorg. Med. Chem. Lett., 2004, 14, 4347-4351.
44. Reed, J.E.; White, A.J.P.; Neidle, S.; Vilar, R. Effect of metal coordination on the interaction of substituted phenanthroline and pyridine ligands with quadruplex DNA. Dalton Trans., 2009, 2558-2568.
45. Suntharalingam, K.; White, A.J.P.; Vilar, R. Synthesis, structural characterisation and quadruplex DNA binding studies of platinum(II)-terpyridine complexes. Inorg. Chem., 2009, 48, 9427-9435.
46. Ma, D.-L.; Che, C.-M.; Yan, S.-Y. Platinum(II) complexes with dipyridophenazine ligands as human telomerase inhibitors and luminescent probes for G-quadruplex DNA. J. Am. Chem. Soc., 2009, 131, 1835-1846.
47. Talib, J.; Green, C.; Davis, K. J.; Urathamakul, T.; Beck, J. L.; Aldrich-Wright, J.R.; Ralph, S.F. A comparison of the binding of metal complexes to duplex and quadruplex DNA. Dalton Trans., 2008, 1018-1026.
48. Kieltyka, R.; Fakhoury, J.; Moitessier, N.; Sleiman, H. F. Platinum phenanthroimidazole complexes as g-quadruplex DNA selective binders. Chem. Eur. J., 2008, 14, 1145-1154.
49. Pierce, S.E.; Kieltyka, R.; Sleiman, H. F.; Brodbelt, J.S. Evaluation of binding selectivities and affinities of platinum-based quadruplex interactive complexes by electrospray ionization mass spectrometry. Biopolymers, 2009, 91, 233-243.
50. Erkkila, K.E.; Odom, D.T.; Barton, J. K. Recognition and reaction of metallointercalators with DNA. Chem. Rev., 1999, 99, 2777-2795.
51. 2+. J. Am. Chem. Soc., 1990, 112, 4960-4962.
52. 2+ with DNA: A calorimetric and equilibrium binding study. J. Am. Chem. Soc., 1995, 117, 4788-4796.
53. Kieltyka, R.; Englebienne, P.; Fakhoury, J.; Autexier, C.; Moitessier, N.; Sleiman, H.F. A Platinum supramolecular square as an effective g-quadruplex binder and telomerase inhibitor. J. Am. Chem. Soc., 2008, 130, 10040-10041.
54. 1 which Recognizes an organic molecule in aqueous media. J. Am. Chem. Soc., 1990, 112, 5645-5647.
55. Bertrand, H.; Bombard, S.; Monchaud, D.; Teulade-Fichou, M.-P. A platinum-quinacridine hybrid as a g-quadruplex ligand. J. Biol. Inorg. Chem., 2007, 12, 1003-1014.
56. Szalai, V.A.; Thorp, H.H. Electron transfer in tetrads: adjacent guanines are not hole traps in g quartets. J. Am. Chem. Soc., 2000, 122, 4524-4525.
57. Delaney, S.; Barton, J. K. Charge transport in DNA duplex/quadruplex conjugates. Biochemistry, 2003, 42, 14159-14165.
58. Tuntiwechapikul, W.; Salazar, M. Cleavage of telomeric Gquadruplex DNA with perylene-EDTA-Fe(II). Biochemistry, 2001, 40, 13652-13658.
59. Muller, J.G.; Kayser, L. A.; Paikoff, S. J.; Duarte, V.; Tang, N.; Perez, R. J.; Rokita, S. E.; Burrows, C. J. Formation of DNA adducts using nickel(II) complexes of redox-active ligands: A comparison of salen and peptide complexes. Coord. Chem. Rev., 1999, 185-186, 761-774.
60. Routier, S.; Cotelle, N.; Catteau, J-P.; Bernier, J-L.; Waring, M. J.; Riou, J-F.; Bailly, C. Salen-anthraquinone conjugates. Synthesis, DNA-binding and cleaving properties, effects on topoisomerases and cytotoxicity. Bioorg. Med. Chem., 1996, 4, 1185-1196.
61. Reed, J.E.; Arnal, A.A.; Neidle, S.; Vilar, R. Stabilisation of Gquadruplex DNA and inhibition of telomerase activity by squareplanar nickel(II) complexes. J. Am. Chem. Soc., 2006, 128, 5992-5993.
62. Arnal, A.A.; Benet-Buchholz, J.; Neidle, S.; Vilar, R. Effects of metal coordination geometry on stabilisation of human telomeric quadruplex DNA by square-planar and square-pyramidal metal complexes. Inorg. Chem., 2008, 47, 11910-11919.
63. Musetti, C.; Lucatello, L.; Bianco, S.; Krapcho, A. P.; Cadamuro, S. A.; Palumbo, M.; Sissi, C. Metal ion-mediated assembly of effective phenanthroline-based g-quadruplex ligands. Dalton Trans., 2009, 3657-3660.
64. Bertrand, H.; Monchaud, D.; De Cian, A.; Guillot, R.; Mergny, J.-L.; Teulade-Fichou, M.-P. The importance of metal geometry in the recognition of g-quadruplex-DNA by metal-terpyridine complexes. Org. Biomol. Chem., 2007, 5, 2555-2559.
65. Xu, H.; Zhang, H.; Qu, X. Interactions of the human telomeric DNA with terbim-amino acid complexes. J. Inorg. Biochem., 2006, 100, 1646-1652.
66. Rajput, C.; Rutkaite, R.; Swanson, L.; Haq, I.; Thomas, J.A. Dinuclear monointercalating RuII complexes that display high affinity binding to duplex and quadruplex DNA. Chem. Eur. J., 2006, 12, 4611-4619.
67. Gonzalez, V.; Wilson, T.; Kurihara, I.; Imai, A.; Thomas, J.A.; Otsuki, J. A Dinuclear Ruthenium(II) complex that functions as a label-free colorimetric sensor for DNA. Chem. Commun., 2008, 1868-1870.
68. Shi, S.; Liu, J.; Yao, T.; Geng, X.; Jiang, L.; Yang, Q.; Cheng, L.; Ji, L. Promoting the formation and stabilisation of g-quadruplexes by dinuclear RuII Complex Ru2(obip)L4. Inorg. Chem., 2008, 47, 2910-2912.
69. Yu, H.; Wang, X.; Fu, M.; Ren, J.; Qu, X. Chiral metallosupramolecular complexes selectively recognise human telomeric g-quadruplex DNA. Nucleic Acids Res., 2008, 36, 5695-5703.
70. Hannon, M.J.; Painting, C.L.; Jackson, A.; Hamblin, J.; Errington, W. An Inexpensive approach to supramolecular architecture. Chem. Commun., 1997, 1807-1808.
71. Barry, N. P. E.; Karim, N. H. A.; Vilar, R.; Therrien, B. Interactions of ruthenium coordination cubes with DNA. Dalton Trans., 2009, 10717-10719.
72. Xu, L.; Zhang, D.; Huang, J.; Deng, M.; Zhang, M.; Zhou, X. High fluorescene selectivity and visual detection of g-quadruplex structures by a novel dinuclear ruthenium complex. Chem. Commun., 2010, 46, 743-745.
73. Huppert, J. L. Hunting G-quadruplexes. Biochimie, 2008, 90, 1140-1148.
74. Suntharalingam, S.; White, A.J.P.; Vilar, R. Two metals are better than one: investigations on the interactions between dinuclear metal complexes and quadruplex DNA. Inorg. Chem., 2010, 49, 8371-8380.
75. 2+. Dalton Trans., 2010, 39, 2490-2493.
76. Rickling, S.; Ghisdavu, L.; Pierard, F.; Gerbaux, P.; Surin, M.; Murat, P.; Defrancq, E.; Moucheron, C.; Kirsch-De Mesmaeker, A. A rigid dinuclear ruthenium(II) complex as an efficient photoactive agent for bridging two guanine bases of a duplex or quadruplex oligonucleotide. Chem. Eur. J., 2010, 16, 3951-3961.
77. Seng, H.-L.; Von, S.-T.; Tan, K.-W.; Maah, M.J.; Ng, S.-W.; Rahman, R.J.Z.R.A.; Caracelli, I.; Ng, C.-H. Crystal structure, DNA inhibition studies, nucleolytic property and topoisomerase I inhibition of a zinc complex with 1,10-phenanthroline and 3-methylpicolinic acid. Biometals, 2010, 23, 99-118.
78. Bianco, S.; Musetti, C.; Waldeck, A.; Sparapani, S.; Seitz, J.D.; Krapcho, A.P.; Palumbo, M.; Sissi, C. Bis-phenanthroline derivatives as suitable scaffolds for effective g-quadruplex recognition. Dalton Trans., 2010, 39, 5833-5841.
79. Jiang, Y.-L.; Liu, Z.-P. Metallo-organic g-quadruplex ligands in anticancer drug design. Mini-rev. Med. Chem., 2010, 10, 726-736.
80. Georgiades, S.N.; Abd Karim, N.H.; Suntharalingam, K.; Vilar, R. Interaction of metal complexes with g-quadruplex DNA. Angew. Chem. Int. Ed. 2010, 49, 4020-4034.