Symmetrical bisbenzimidazoles with benzenediyl spacer: The role of the shape of the ligand on the stabilization and structural alterations in telomeric g-quadruplex dna and telomerase inhibition

Bioconjugate Chemistry

Volumn 21, Issue 7, 2010, Pages 1148-1159

  Bhattacharya, Santanu ^a,b   Chaudhuri, Padmaparna ^a   Jain, Akash K ^a   Paul, Ananya ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

2,2' (1,3 PHENYLENE) BIS [5 [4 (2 HYDROXYETHYL) 1 PIPERAZINYL] 1H BENZIMIDAZOLE]; 2,2' (1,4 PHENYLENE) BIS [5 [4 (2 HYDROXYETHYL) 1 PIPERAZINYL] 1H BENZIMIDAZOLE]; ANTINEOPLASTIC AGENT; GUANINE QUADRUPLEX; PIBENZIMOL; SODIUM ION; TELOMERASE; UNCLASSIFIED DRUG;

ARTICLE; CIRCULAR DICHROISM; COMPUTER MODEL; CONTROLLED STUDY; DNA DRUG COMPLEX; DRUG DESIGN; DRUG DNA BINDING; ENZYME INHIBITION; ENZYME SPECIFICITY; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; MOLECULAR MODEL; MOLECULAR STABILITY; STRUCTURE ACTIVITY RELATION; TELOMERE; TELOMERIC REPEAT AMPLIFICATION PROTOCOL;

EID: 77954881060     PISSN: 10431802     EISSN: 15204812     Source Type: Journal    
DOI: 10.1021/bc9003298     Document Type: Article

References (67)

1. Blackburn, E. H. (1991) Structure and function of telomeres Nature 350, 569-573
2. Harley, C. B., Futcher, A. B., and Greider, C. W. (1990) Telomeres shorten during ageing of human fibroblasts Nature 345, 458-460
3. Gowan, S. M., Harrison, J. R., Patterson, Valenti, L. M., Read, M. A., Neidle, S., and Kelland, L. R. (2002) A G-quadruplex-interactive potent small-molecule inhibitor of telomerase exhibiting in vitro and in vivo antitumor activity Mol. Pharmacol. 61, 1154-1162
4. Cech, T. R. (2000) Life at the end of the chromosome: Telomeres and telomerase Angew. Chem. Int. Ed. 39, 34-43
5. Kerwin, S. M. (2000) G-quadruplex DNA as a target for drug design Curr. Pharmacol. Des. 6, 441-478
6. Perry, P. J. and Kell, L. R. (1998) Telomeres and telomerase: targets for cancer chemotherapy Exp. Opin. Ther. Patents 8, 1567-1586
7. Franceschin, M. (2009) G-Quadruplex DNA structures and organic chemistry: More than one connection Eur. J. Org. Chem. 2225-2238
8. Kim, M. Y., Vankayalapati, H., Shin-Ya, K., Wierzba, K., and Hurley, L. H. (2002) Telomestatin, a potent telomerase inhibitor that interacts quite specifically with the human telomeric intramolecular G-quadruplex J. Am. Chem. Soc. 124, 2098-2099
9. Barbieri, C. M., Srinivasan, A. R., Rzuczek, S. G., Rice, J. E., LaVoie, E. J., and Pilch, D. S. (2007) Defending the mode, energetic and specificity with which a macrocyclic hexaoxazole binds to human telomeric G-quadruplex DNA Nucleic Acids Res. 35, 3272-3286
10. Hurley, L. H. (2002) DNA and its associated processes as targets for cancer therapy Nat. Rev. Cancer 2, 188-200
11. Pindur, U. and Fischer, G. A. (1996) DNA complexing minor groove-binding ligands: Antitumour and antimicrobial drug design Curr. Med. Chem. 3, 379-406
12. Phillips, K., Dauter, Z., Murchie, A. I. H., Lilley, D. M. J., and Luisi, B. (1997) The crystal structure of a parallel-stranded guanine tetraplex at 0.95 resolution J. Mol. Biol. 273, 171-182
13. Tang, C. F. and Shafer, R. H. (2006) Engineering the quadruplex fold: Nucleoside conformation determines both folding topology and molecularity in guanine quadruplexes J. Am. Chem. Soc. 128, 5966-5973
14. Rodriguez, R., Pantos, G. D., Goncalvs, D. P. N., Sanders, J. K. M., and Balasubramanian, S. (2007) Ligand induced-driven G-quadruplex conformational switching by using an unusual mode of interaction Angew. Chem. Int. Ed. 46, 5405-5407
15. Mergny, J. L., Phan, A. T., and Lacroix, L. (1998) Following G-quartet formation by UV-spectroscopy FEBS Lett. 435, 74-78
16. Han, H. and Hurley, L. H. (2000) G-quadruplex DNA: A potential target for anti-cancer drug design Trends Pharmacol. Sci. 21, 136-141
17. Burger, A. M., Schultes, Dai, F., Reszka, C. M., Moore, A. P., Double, J. A., and Neidle, S. (2005) The G-Quadruplex-interactive molecule BRACO-19 inhibits tumour growth, consistent with telomere targeting and interference with telomerase function Cancer Res. 65, 1489-1496
18. Moorehouse, A. D., Santos, A. M., Gunaratnam, M., Moore, M., Neidle, S., and Mosses, J. E. (2006) Stabilization of G-quadruplex DNA by highly selective ligands via click chemistry J. Am. Chem. Soc. 128, 15972-15973
19. Dash, J., Shirude, P. S., and Balasubramanian, S. (2008) Quadruplex recognition by bis-indole carboxamides Chem. Commun. 3055-3057
20. Li, G., Huang, J., Zhang, M., Zhou, Y., Zhang, D., Wu, Z., Wang, S., Weng, X., and Zhou, X. Y. (2008) G. Bis(benzimidazole)pyridine derivative as a new class of G-quadruplex inducing and stabilizing ligand Chem. Commun. 4564-4566
21. Monchaud, D., Yang, P., Lacroix, L., Teulade-Fichou, M. P., and Mergny, J. L. (2008) A metal-mediated conformational switch controls G-quadruplex binding affinity Angew. Chem., Int. Ed. 47, 4858-4861
22. Bhattacharya, S. and Thomas, M. (2000) Facile synthesis of oligopeptide distmycin analogs devoid of hydogen bond donors or acceptors at the N-terminus: Sequence-specific duplex DNA binding as a function of peptide chain length Tetrahedron Lett. 41, 5571-5575
23. Thomas, M., Varshney, U., and Bhattacharya, S. (2002) Distamycin analogs without leading amide at their N-termini comparative binding properties to AT- and GC-rich DNA sequences Eur. J. Org. Chem. 3604-3615
24. Ghosh, S., Defrancq, E., Lhomme, J. H., Dumy, P., and Bhattacharya, S. (2004) Efficient conjugation and characterization of distamycin based peptides with selected oligonucleotide stretches Bioconjugate Chem. 15, 520-529
25. Bhattacharya, S. and Mandal, S. S. (1995) Ambient oxygen activating water soluble cobalt-salen complex for DNA cleavage J. Chem. Soc. Chem. Commun. 2489-2490
26. Mandal, S. S., Kumar, N. V., Varshney, U., and Bhattacharya, S. (1996) Metal-ion dependent oxidative DNA cleavage by transition metal complex of a new water soluble salen derivative J. Inorg. Biochem. 63, 265-272
27. Bhattacharya, S. and Mandal, S. S. (1996) DNA cleavage by intercalatable cobalt-bispicolylamine complexes activated by visible light Chem. Commun. 1515-1516
28. Mandal, S. S., Varshney, U., and Bhattacharya, S. (1997) Role of central metal ion and ligand charge in the DNA binding and modification by metallosalen complexes Bioconjugate Chem. 8, 798-812
29. Chaudhuri, P., Majumder, H. K., and Bhattacharya, S. (2007) Synthesis, DNA binding, and Leishmania topoisomerase inhibition activities of a novel series of anthra[1, 2 d ]imidazole-6,11-dione derivatives J. Med. Chem. 50, 2536-2540
30. Jain, A. K., Reddy, V. V., Paul, A., Muniyappa, K., and Bhattacharya, S. (2009) Synthesis and evaluation of a novel class of G-quadruplex-stabilizing small molecules based on the 1,3-phenylene-bis(piperazinyl benzimidazole) system Biochemistry 48, 10693-10704
31. Drewe, W. C., Nanjunda, R., Gunaratnam, M., Beltran, M., Parkinson, G. N., Reszka, A. P., Wilson, D., and Neidle, S. (2008) Rational design of substituted diarylureas: A scaffold for binding to G-quadruplex motifs J. Med. Chem. 51, 7751-7767
32. Muller, S., Pantos, G. D., Rodriguez, R., and Balasubramanian, S. (2009) Controlled-folding of a small molecule modulates DNA G-quadruplex recognition Chem. Commun. 80-82
33. Bathini, Y., Rao, K. E., Shea, R. G., and Lown, W. (1990) Molecular recognition between ligands and nucleic acids: novel pyridine- and benzoxazole-containing agents related to Hoechst 33258 that exhibit altered DNA sequence specificity deduced from footprinting analysis and spectroscopic studies Chem. Res. Toxicol. 3, 268-280
34. Hori, Y., Bichenkova, E. V., Wilton, A. N., El-Attug, M. N., Sadat-Ebrahimi, S., Tanaka, T., Kikuchi, Y., Araki, M., Sugiura, Y., and Douglas, K. T. (2001) Synthetic inhibitors of the processing of pretransfer RNA by the ribonuclease P ribozyme: Enzyme inhibitors which act by binding to substrate Biochemistry 40, 603-608
35. Hardin, C. C., Henderson, E., Watson, T., and Prosser, J. K. (1991) Monovalent cation induced structural transitions in telomeric DNAs: G-DNA folding intermediates Biochemistry 30, 4460-4472
36. +) facilitates intermolecular G-quadruplex formation of telomeric sequences Biochemistry 31, 3769-3776
37. Murashima, Sakiyama, T. D., Miyoshi, D., Kuriyama, M., Yamada, T., Miyazawa, T. and, and Sugimoto, N. (2008) Cationic porphyrin induced a telomeric DNA to G-quadruplex form in water Bioinorg. Chem. Appl. 1-5
38. 4 G-tetraplex Structure 2, 1141-1156
39. Peacocke, A. R. and Skerrett, J. N. H. (1956) The interaction of aminoacridines with nucleic acids J. Chem. Soc., Faraday Trans. 52, 261-279
40. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Montgomery, J. A., Vreven, T., Kudin, K. N., Burant, J. C., and Milliam, J. M. Gaussian 03, Gaussian, Inc., Wallingford, CT.
41. Morris, G. M., Goodsell, D. S., Halliday, R. S., Huey, R., Hart, W. E., Belew, R. K., and Olson, A. J. (1998) Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function J. Comput. Chem. 19, 1639-1662
42. Sanner, M. F. (1999) Python: a programming language for software integration and development J. Mol. Graph. Model. 17, 57-61
43. Cornell, W. D., Cieplak, P., Bayly, C. I., Gould, I. R., Merz, K. M., Jr., Ferguson, D. M., Spellmeyer, D. C., Fox, T., Caldwell, J. W., and Kollman, P. A. (1995) A second generation force field for the simulation of proteins, nucleic acids, and organic molecules J. Am. Chem. Soc. 117, 5179-5197
44. Wang, J., Wolf, R. M., Caldwell, J. W., Kollman, P. A., and Case, D. A. (2004) Development and testing of a general Amber force field J. Comput. Chem. 25, 1157-1174
45. Hazel, P., Huppert, J., Balasubramanian, S., and Neidle, S. (2004) Loop-length-dependent folding of G-quadruplex J. Am. Chem. Soc. 126, 16405-16415
46. Hazel, P., Parkinson, G. N., and Neidle, S. (2006) Predictive modelling of topology and loop variations in dimeric DNA quadruplex structures Nucleic Acids Res. 34, 2117-2127
47. Darden, T., York, D., and Pedersen, L. (1993) Particle mesh Ewald: an N log(N) method for Ewald sums in large systems J. Chem. Phys. 98, 10089-10092
48. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79, 926-935
49. Ryckaert, J. P., Ciccotti, G., and Berendsen, H. J. C. (1977) Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n -alkanes J. Comput. Phys. 23, 327-41
50. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: visual molecular dynamics J. Mol. Graph. 14, 33-8 plates 27-28
51. Pagano, B., Virno, A., Mattia, C. A., Mayol, L., Randazzo, A., and Giancola, C. (2008) Targeting DNA quadruplexes with distamycin A and its derivatives: An ITC and NMR study Biochimie 90, 1224-1232
52. 4 G-quadruplex: Spectroscopic evidence Biophys. Chem. 143, 79-84
53. Rezler, E. M., Seenisamy, J., Bashyam, J. S., Kim, M. Y., White, E., Wilson, W. D., and Hurley, L. H. (2005) Telomestatin and diseleno sapphyrin bind selectively to two different forms of the human telomeric G-quadruplex structure J. Am. Chem. Soc. 127, 9439-9447
54. Bhattacharya, S. and Chaudhuri, P. (2008) Medical implications of benzimidazole derivatives as drugs designed for targeting DNA and DNA associated processes Curr. Med. Chem. 15, 1762-1777
55. Stokke, T. and Steen, H. B. (1985) Multiple binding modes for Hoechst 33258 to DNA J. Histochem. Cytochem. 33, 333-338
56. Latt, S. A. and Wohlleb, J. C. (1975) Optical studies of the interaction of 33258 Hoechst with DNA, chromatin, and metaphase chromosomes Chromosoma 52, 297-316
57. Chaudhuri, P., Ganguly, B., and Bhattacharya, S. (2007) An experimental and computational analysis on the differential role of the positional isomers of symmetric bis-2-(pyridyl)-1 H -benzimidazoles as DNA binding agents J. Org. Chem. 72, 1912-1923
58. Tawar, U., Jain, A. K., Dwarakanath, B. S., Chandra, R., Singh, Y., Chaudhury, N. K., Khaitan, D., and Tandon, V. (2003) Influence of phenyl ring disubstitution on bisbenzimidazole and terbenzimidazole cytotoxicity: synthesis and biological evaluation as radioprotectors J. Med. Chem. 46, 3785-3792
59. Kieltyka, R., Fakhoury, J., Moitessier, N., and Sleiman, H. F. (2008) Platinum phenanthroimidazole complexes as G-quadruplex DNA selective binders Chem. - Eur. J. 14, 1145-1154
60. Arora, A., Balasubramanian, C., Kumar, N., Agrawal, S., Ojha, R. P., and Maiti, S. (2008) Binding of berberine to human telomeric quadruplex- spectroscopic, calorimetric and molecular modeling studies FEBS J. 275, 3971-3983
61. De. Cian, A., Guittat, L., Kaiser, M., Sacca, B., Amrane, S., Bourdoncle, A., Albrtti, P., Teulade-Fichou, M. P., Lacriox, L., and Mergny, J. L. (2007) Fluorescence-based melting assays for studying quadruplex ligands Methods 42, 183-195
62. + solution under molecular crowding condition J. Am. Chem. Soc. 129, 11185-11191
63. Haider, S. M., Parkinson, G. N., and Neidle, S. (2003) Structure of a G-quadruplex-ligand complex J. Mol. Biol. 326, 117-125
64. Campbell, N. H., Parkinson, G. N., Reszka, A. P., and Neidle, S. (2008) Structural basis of DNA quadruplex recognition by an acridine drug J. Am. Chem. Soc. 130, 6722-6724
65. Gomez, D., Aouali, N., Renaud, A., Douarre, Ce.-T., Shin-ya, K., Tazi, J., Martinez, S., Trentesaux, C., Morjani, H., and ois Riou, J.-F. (2003) Resistance to senescence induction and telomere shortening by a G-quadruplex ligand inhibitor of telomerase Cancer Res. 63, 6149-6153
66. Mikami-Terao, Y., Akiyama, M., Yuza, Y., Yanagisawa, T., Yamada, O., and Yamada, H. (2008) Antitumor activity of G-quadruplex-interactive agent TMPyP4 in K562 leukemic cells Cancer Lett. 261, 226-234
67. Read, M. J., Gunaratnam, M., Beltran, A. P., Reszka, R. V., and Neidle, S. (2008) TRAP-LIG, a modified telomere repeat amplification protocol assay to quantitate telomerase inhibition by small molecules Anal. Biochem. 380, 99-105