Structure-specific recognition of quadruplex DNA by organic cations: Influence of shape, substituents and charge

Biophysical Chemistry

Volumn 126, Issue 1-3, 2007, Pages 140-153

  White, Elizabeth W ^a   Tanious, Farial ^a   Ismail, Mohamed A ^a   Reszka, Anthony P ^b   Neidle, Stephen ^b   Boykin, David W ^a   Wilson, W David ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

BIAcore; DNA quadruplex binding; G tetrad; ITC; Synthetic cations; Telomere

Indexed keywords

CATION; DOUBLE STRANDED DNA;

ARTICLE; BINDING AFFINITY; CIRCULAR DICHROISM; DNA STRUCTURE; ENTHALPY; ISOTHERMAL TITRATION CALORIMETRY; PRIORITY JOURNAL; SURFACE PLASMON RESONANCE;

CALORIMETRY; CIRCULAR DICHROISM; DNA; MOLECULAR STRUCTURE; NUCLEIC ACID CONFORMATION; ORGANIC CHEMICALS; SURFACE PLASMON RESONANCE;

EID: 33846569026     PISSN: 03014622     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bpc.2006.06.006     Document Type: Article

References (89)

1. Blackburn G.M., and Gait M.J. Nucleic Acids in Chemistry and Biology. second ed. (1996), Oxford University Press, New York
2. Dervan P.B., and Edelson B.S. Recognition of the DNA minor groove by pyrrole-imidazole polyamides. Curr. Opin. Struct. Biol. 13 (2003) 284-299
3. Lacy E.R., Madsen E.M., Lee M., and Wilson W.D. Polyamide stacking in the DNA minor groove and recognition of T-G mismatched base pairs in DNA. In: Demeunynck M., Bailly C., and Wilson W.D. (Eds). DNA and RNA Binders (2003), Wiley-VCH, Weinheim 384-413
4. Carter A.P., Clemons W.M., Brodersen D.E., Morgan-Warren R.J., Wimberly B.T., and Ramakrishnan V. Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 407 (2000) 340-348
5. Kaul M., Barbieri C.M., and Pilch D.S. Aminoglycoside-induced reduction in nucleotide mobility at the ribosomal RNA A-site as a potentially key determinant of antibacterial activity. J. Am. Chem. Soc. 128 (2006) 1261-1271
6. Moazed D., and Noller H.F. Interaction of antibiotics with functional sites in 16S ribosomal RNA. Nature 327 (1987) 389-394
7. Tucker B.J., and Breaker R.R. Riboswitches as versatile gene control elements. Curr. Opin. Struct. Biol. 15 (2005) 342-348
8. Gold L. Globular Oligonucleotide Screening via the SELEX Process: Aptamers as High-Affinity, High-Specificity Compounds for Drug Development and Proteomic Diagnostics (1999), Dekker, New York
9. Liu B., Liu Y., Motyka S.A., Agbo E.E., and Englund P.T. Fellowship of the rings: the replication of kinetoplast DNA. Trends Parasitol. 21 (2005) 363-369
10. Shapiro T.A., and Englund P.T. The structure and replication of kinetoplast DNA. Annu. Rev. Microbiol. 49 (1995) 117-143
11. Shlomai J. The structure and replication of kinetoplast DNA. Curr. Mol. Med. 4 (2004) 623-647
12. Marini J.C., Levene S.D., Crothers D.M., and Englund P.T. Bent helical structure in kinetoplast DNA. Proc. Natl. Acad. Sci. U. S. A. 79 (1982) 7664-7668
13. Wilson W.D., Nguyen B., Tanious F.A., Mathis A., Hall J.E., Stephens C.E., and Boykin D.W. Dications that target the DNA minor groove: compound design and preparation, DNA interactions, cellular distribution and biological activity. Curr. Med. Chem. Anticancer Agents 5 (2005) 389-408
14. Cech T.R. G-strings at chromosome ends. Nature 332 (1988) 777-778
15. Sen D., and Gilbert W. Formation of parallel four-stranded complexes by guanine-rich motifs in DNA and its implications for meiosis. Nature 334 (1988) 364-366
16. Catasti P., Chen X., Moyzis R.K., Bradbury E.M., and Gupta G. Structure-function correlations of the insulin-linked polymorphic region. J. Mol. Biol. 264 (1996) 534-545
17. Siddiqui-Jain A., Grand C.L., Bearss D.J., and 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. U. S. A. 99 (2002) 11593-11598
18. Simonsson T., Pecinka P., and Kubista M. DNA tetraplex formation in the control region of c-myc. Nucleic Acids Res. 26 (1998) 1167-1172
19. Incles C.M., Schultes C.M., and Neidle S. Telomerase inhibitors in cancer therapy: current status and future directions. Curr. Opin. Investig. Drugs 4 (2003) 675-685
20. Kelland L.R. Overcoming the immortality of tumour cells by telomere and telomerase based cancer therapeutics-current status and future prospects. Eur. J. Cancer 41 (2005) 971-979
21. Mergny J.L., Riou J.F., Mailliet P., Teulade-Fichou M.P., and Gilson E. Natural and pharmacological regulation of telomerase. Nucleic Acids Res. 30 (2002) 839-865
22. Olaussen K.A., Dubrana K., Domont J., Spano J.P., Sabatier L., and Soria J.C. Telomeres and telomerase as targets for anticancer drug development. Crit. Rev. Oncol./Hematol. 57 (2006) 191-214
23. Rezler E.M., Bearss D.J., and Hurley L.H. Telomeres and telomerases as drug targets. Curr. Opin. Pharmacol. 2 (2002) 415-423
24. Rezler E.M., Bearss D.J., and Hurley L.H. Telomere inhibition and telomere disruption as processes for drug targeting. Annu. Rev. Pharmacol. Toxicol. 43 (2003) 359-379
25. Saretzki G. Telomerase inhibition as cancer therapy. Cancer Lett. 194 (2003) 209-219
26. Shin-Ya K. Novel antitumor and neuroprotective substances discovered by characteristic screenings based on specific molecular targets. Biosci. Biotechnol. Biochem. 69 (2005) 867-872
27. Parkinson G.N., Lee M.P., and Neidle S. Crystal structure of parallel quadruplexes from human telomeric DNA. Nature 417 (2002) 876-880
28. Wang Y., and Patel D.J. Solution structure of the human telomeric repeat d[AG3(T2AG3)3] G-tetraplex. Structure 1 (1993) 263-282
29. Fang G., and Cech T.R. The beta subunit of Oxytricha telomere-binding protein promotes G-quartet formation by telomeric DNA. Cell 74 (1993) 875-885
30. Fang G., and Cech T.R. Characterization of a G-quartet formation reaction promoted by the beta-subunit of the Oxytricha telomere-binding protein. Biochemistry 32 (1993) 11646-11657
31. Giraldo R., Suzuki M., Chapman L., and Rhodes D. Promotion of parallel DNA quadruplexes by a yeast telomere binding protein: a circular dichroism study. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 7658-7662
32. Granotier C., Pennarun G., Riou L., Hoffschir F., Gauthier L.R., de Cian A., Gomez D., Mandine E., Riou J.-F., Mergny J.-L., Mailliet P., Dutrillaux B., and Boussin F.D. Preferential binding of a G-quadruplex ligand to human chromosome ends. Nucleic Acids Res. 33 (2005) 4182-4190
33. Harley C.B., Futcher A.B., and Greider C.W. Telomeres shorten during ageing of human fibroblasts. Nature 345 (1990) 458-460
34. Kim N.W., Piatyszek M.A., Prowse K.R., Harley C.B., West M.D., Ho P.L., Coviello G.M., Wright W.E., Weinrich S.L., and Shay J.W. Specific association of human telomerase activity with immortal cells and cancer. Science 266 (1994) 2011-2015
35. Zahler A.M., Williamson J.R., Cech T.R., and Prescott D.M. Inhibition of telomerase by G-quartet DNA structures. Nature 350 (1991) 718-720
36. Sun D., Thompson B., Cathers B.E., Salazar M., Kerwin S.M., Trent J.O., Jenkins T.C., Neidle S., and Hurley L.H. Inhibition of human telomerase by a G-quadruplex-interactive compound. J. Med. Chem. 40 (1997) 2113-2116
37. Fedoroff O.Y., Salazar M., Han H., Chemeris V.V., Kerwin S.M., and Hurley L.H. NMR-Based model of a telomerase-inhibiting compound bound to G-quadruplex DNA. Biochemistry 37 (1998) 12367-12374
38. Han F.X., Wheelhouse R.T., and Hurley L.H. Interactions of TMPyP4 and TMPyP2 with quadruplex DNA. Structural basis for the differential effects on telomerase inhibition. J. Am. Chem. Soc. 121 (1999) 3561-3570
39. Read M., Harrison R.J., Romagnoli B., Tanious F.A., Gowan S.H., Reszka A.P., Wilson W.D., Kell L.R., and Neidle S. Structure-based design of selective and potent G quadruplex-mediated telomerase inhibitors. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 4844-4849
40. Teulade-Fichou M.P., Carrasco C., Guittat L., Bailly C., Alberti P., Mergny J.L., David A., Lehn J.M., and Wilson W.D. Selective recognition of G-quadruplex telomeric DNA by a bis(quinacridine) macrocycle. J. Am. Chem. Soc. 125 (2003) 4732-4740
41. Neidle S. DNA minor-groove recognition by small molecules. Nat. Prod. Rep. 18 (2001) 291-309
42. Wang L., Bailly C., Kumar A., Ding D., Bajic M., Boykin D.W., and Wilson W.D. Specific molecular recognition of mixed nucleic acid sequences: an aromatic dication that binds in the DNA minor groove as a dimer. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 12-16
43. Wang L., Carrasco C., Kumar A., Stephens C.E., Bailly C., Boykin D.W., and Wilson W.D. Evaluation of the influence of compound structure on stacked-dimer formation in the DNA minor groove. Biochemistry 40 (2001) 2511-2521
44. Kerwin S.M. G-quadruplex DNA as a target for drug design. Curr. Pharm. Des. 6 (2000) 441-478
45. Chen Q., Kuntz I.D., and Shafer R.H. Spectroscopic recognition of guanine dimeric hairpin quadruplexes by a carbocyanine dye. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 2635-2639
46. Cheng J.-Y., Lin S.-H., and Chang T.-C. Vibrational investigation of DODC cation for recognition of guanine dimeric hairpin quadruplex studied by satellite holes. J. Phys. Chem. 102 (1998) 5542-5546
47. Chiang C.-C., Cheng J.-Y., and Chang T.-C. Satellite hole spectral method and its applications to dye-DNA complexes. Proc. Natl. Sci. Counc. Repub. China, Part A 23 (1999) 679-694
48. Kerwin S.M., Sun D., Kern J.T., Rangan A., and Thomas P.W. G-quadruplex DNA binding by a series of carbocyanine dyes. Bioorg. Med. Chem. Lett. 11 (2001) 2411-2414
49. Rodger A., and Norden B. Circular Dichroism and Linear Dichroism (1997), Oxford University Press, New York
50. Li J., Correia J.J., Wang L., Trent J.O., and Chaires J.B. Not so crystal clear: the structure of the human telomere G-quadruplex in solution differs from that present in a crystal. Nucleic Acids Res. 33 (2005) 4649-4659
51. Harrison R.J., Gowan S.M., Kell L.R., and Neidle S. Human telomerase inhibition by substituted acridine derivatives. Bioorg. Med. Chem. Lett. 9 (1999) 2463-2468
52. Perry P.J., Gowan S.M., Read M.A., Kell L.R., and Neidle S. Design, synthesis and evaluation of human telomerase inhibitors based upon a tetracyclic structural motif. Anticancer Drug Des. 14 (1999) 373-382
53. Perry P.J., Gowan S.M., Reszka A.P., Polucci P., Jenkins T.C., Kell L.R., and Neidle S. 1,4- and 2,6-disubstituted amidoanthracene-9,10-dione derivatives as inhibitors of human telomerase. J. Med. Chem. 41 (1998) 3253-3260
54. Perry P.J., Reszka A.P., Wood A.A., Read M.A., Gowan S.M., Dosanjh H.S., Trent J.O., Jenkins T.C., Kell L.R., and Neidle S. Human telomerase inhibition by regioisomeric disubstituted amidoanthracene-9,10-diones. J. Med. Chem. 41 (1998) 4873-4884
55. Read M.A., Wood A.A., Harrison J.R., Gowan S.M., Kelland L.R., Dosanjh H.S., and Neidle S. Molecular modeling studies on G-quadruplex complexes of telomerase inhibitors: structure-activity relationships. J. Med. Chem. 42 (1999) 4538-4546
56. Moore M.J., Schultes C.M., Cuesta J., Cuenca F., Gunaratnam M., Tanious F.A., Wilson W.D., and Neidle S. Trisubstituted acridines as G-quadruplex telomere targeting agents. Effects of extensions of the 3,6- and 9-side chains on quadruplex binding, telomerase activity, and cell proliferation. J. Med. Chem. 49 (2006) 582-599
57. Seenisamy J., Bashyam S., Gokhale V., Vankayalapati H., Sun D., Siddiqui-Jain A., Streiner N., Shin-Ya K., White E., Wilson W.D., and Hurley L.H. Design and synthesis of an expanded porphyrin that has selectivity for the c-MYC G-quadruplex structure. J. Am. Chem. Soc. 127 (2005) 2944-2959
58. Cookson J.C., Heald R.A., and Stevens M.F. Antitumor polycyclic acridines. 17. Synthesis and pharmaceutical profiles of pentacyclic acridinium salts designed to destabilize telomeric integrity. J. Med. Chem. 48 (2005) 7198-7207
59. Lacy E.R., Le N.M., Price C.A., Lee M., and Wilson W.D. Influence of a terminal formamido group on the sequence recognition of DNA by polyamides. J. Am. Chem. Soc. 124 (2002) 2153-2163
60. Mazur S., Tanious F.A., Ding D., Kumar A., Boykin D.W., Simpson I.J., Neidle S., and Wilson W.D. A thermodynamic and structural analysis of DNA minor-groove complex formation. J. Mol. Biol. 300 (2000) 321-337
61. Nguyen B., Tardy C., Bailly C., Colson P., Houssier C., Kumar A., Boykin D.W., and Wilson W.D. Influence of compound structure on affinity, sequence selectivity, and mode of binding to DNA for unfused aromatic dications related to furamidine. Biopolymers 63 (2002) 281-297
62. Burger A.M., Dai F., Schultes C.M., Reszka A.P., Moore M.J., Double J.A., and Neidle S. The G-quadruplex-interactive molecule BRACO-19 inhibits tumor growth, consistent with telomere targeting and interference with telomerase function. Cancer Res. 65 (2005) 1489-1496
63. Harrison R.J., Cuesta J., Chessari G., Read M.A., Basra S.K., Reszka A.P., Morrell J., Gowan S.M., Incles C.M., Tanious F.A., Wilson W.D., Kell L.R., and Neidle S. Trisubstituted acridine derivatives as potent and selective telomerase inhibitors. J. Med. Chem. 46 (2003) 4463-4476
64. Schultes C.M., Guyen B., Cuesta J., and 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. 14 (2004) 4347-4351
65. Han H., Langley D.R., Rangan A., and Hurley L.H. Selective interactions of cationic porphyrins with G-quadruplex structures. J. Am. Chem. Soc. 123 (2001) 8902-8913
66. Anantha N.V., Azam M., and Sheardy R.D. Porphyrin binding to quadruplex T4G4. Biochemistry 37 (1998) 2709-2714
67. Arthanari H., Basu S., Kawano T.L., and Bolton P.H. Fluorescent dyes specific for quadruplex DNA. Nucleic Acids Res. 26 (1998) 3724-3728
68. Izbicka E., Wheelhouse R.T., Raymond E., Davidson K.K., Lawrence R.A., Sun D., Windle B.E., Hurley L.H., and Von Hoff D.D. Effects of cationic porphyrins as G-quadruplex interactive agents in human tumor cells. Cancer Res. 59 (1999) 639-644
69. Hurley L.H., Wheelhouse R.T., Sun D., Kerwin S.M., Salazar M., Fedoroff O.Y., Han F.X., Han H., Izbicka E., and Von Hoff D.D. G-quadruplexes as targets for drug design. Pharmacol. Ther. 85 (2000) 141-158
70. Rezler E.M., Seenisamy J., Bashyam S., Kim M.Y., White E., Wilson W.D., and Hurley L.H. Telomestatin and diseleno sapphyrin bind selectively to two different forms of the human telomeric G-quadruplex structure. J. Am. Chem. Soc. 127 (2005) 9439-9447
71. Mazzitelli C.L., Brodbelt J.S., Kern J.T., Rodriguez M., and Kerwin S.M. Evaluation of binding of perylene diimide and benzannulated perylene diimide ligands to DNA by electrospray ionization mass spectrometry. J. Am. Soc. Mass Spectrom. (2006)
72. Alberti P., Schmitt P., Nguyen C.H., Rivalle C., Hoarau M., Grierson D.S., and Mergny J.L. Benzoindoloquinolines interact with DNA tetraplexes and inhibit telomerase. Bioorg. Med. Chem. Lett. 12 (2002) 1071-1074
73. Cookson J.C., Dai F., Smith V., Heald R.A., Laughton C.A., Stevens M.F., and Burger A.M. Pharmacodynamics of the G-quadruplex-stabilizing telomerase inhibitor 3,11-difluoro-6,8,13-trimethyl-8H-quino[4,3,2-kl]acridinium methosulfate (RHPS4) in vitro: activity in human tumor cells correlates with telomere length and can be enhanced, or antagonized, with cytotoxic agents. Mol. Pharmacol. 68 (2005) 1551-1558
74. Gavathiotis E., Heald R.A., Stevens M.F., and Searle M.S. Recognition and stabilization of quadruplex DNA by a potent new telomerase inhibitor: NMR studies of the 2:1 complex of a pentacyclic methylacridinium cation with d(TTAGGGT)(4). Angew. Chem., Int. Ed. Engl. 40 (2001) 4749-4751
75. Gavathiotis E., Heald R.A., Stevens M.F., and Searle M.S. Drug recognition and stabilisation of the parallel-stranded DNA quadruplex d(TTAGGGT)4 containing the human telomeric repeat. J. Mol. Biol. 334 (2003) 25-36
76. Gowan S.M., Heald R., Stevens M.F., and Kelland L.R. Potent inhibition of telomerase by small-molecule pentacyclic acridines capable of interacting with G-quadruplexes. Mol. Pharmacol. 60 (2001) 981-988
77. Heald R.A., Modi C., Cookson J.C., Hutchinson I., Laughton C.A., Gowan S.M., Kell L.R., and Stevens M.F. Antitumor polycyclic acridines. 8.(1) Synthesis and telomerase-inhibitory activity of methylated pentacyclic acridinium salts. J. Med. Chem. 45 (2002) 590-597
78. Leonetti C., Amodei S., D'Angelo C., Rizzo A., Benassi B., Antonelli A., Elli R., Stevens M.F., D'Incalci M., Zupi G., and Biroccio A. Biological activity of the G-quadruplex ligand RHPS4 (3,11-difluoro-6,8,13-trimethyl-8H-quino[4,3,2-kl]acridinium methosulfate) is associated with telomere capping alteration. Mol. Pharmacol. 66 (2004) 1138-1146
79. Carrasco C., Rosu F., Gabelica V., Houssier C., De Pauw E., Garbay-Jaureguiberry C., Roques B., Wilson W.D., Chaires J.B., Waring M.J., and Bailly C. Tight binding of the antitumor drug ditercalinium to quadruplex DNA. ChemBioChem 3 (2002) 1235-1241
80. Dias N., Jacquemard U., Baldeyrou B., Tardy C., Lansiaux A., Colson P., Tanious F., Wilson W.D., Routier S., Merour J.Y., and Bailly C. Targeting DNA with novel diphenylcarbazoles. Biochemistry 43 (2004) 15169-15178
81. Koeppel F., Riou J.F., Laoui A., Mailliet P., Arimondo P.B., Labit D., Petitgenet O., Helene C., and Mergny J.L. Ethidium derivatives bind to G-quartets, inhibit telomerase and act as fluorescent probes for quadruplexes. Nucleic Acids Res. 29 (2001) 1087-1096
82. Neidle S., and Read M.A. G-quadruplexes as therapeutic targets. Biopolymers 56 (2001) 195-208
83. Randazzo A., Galeone A., Esposito V., Varra M., and Mayol L. Interaction of distamycin A and netropsin with quadruplex and duplex structures: a comparative 1H-NMR study. Nucleosides Nucleotides Nucleic Acids 21 (2002) 535-545
84. Cocco M.J., Hanakahi L.A., Huber M.D., and Maizels N. Specific interactions of distamycin with G-quadruplex DNA. Nucleic Acids Res. 31 (2003) 2944-2951
85. Cao R., Venezia C.F., and Armitage B.A. Investigation of DNA binding modes for a symmetrical cyanine dye trication: effect of DNA sequence and structure. J. Biomol. Struct. Dyn. 18 (2001) 844-856
86. Garoff R.A., Litzinger E.A., Connor R.E., Fishman I., and Armitage B.A. Helical aggregation of cyanine dyes on DNA templates: effect of dye structure on formation of homo- and heteroaggregates. Langmuir 18 (2002) 6330-6337
87. Wang M., Silva G.L., and Armitage B.A. DNA-templated formation of a helical cyanine dye J-aggregate. J. Am. Chem. Soc. 122 (2000) 9977-9986
88. Rosu F., De Pauw E., Guittat L., Alberti P., Lacroix L., Mailliet P., Riou J.F., and Mergny J.L. Selective interaction of ethidium derivatives with quadruplexes: an equilibrium dialysis and electrospray ionization mass spectrometry analysis. Biochemistry 42 (2003) 10361-10371
89. Tidwell R.R., and Boykin W.D. DNA and RNA Binders: From Small Molecules to Drugs (2003), Wiley-VCH