Interaction of G-quadruplexes with nonintercalating duplex-DNA minor groove binding ligands

Bioconjugate Chemistry

Volumn 22, Issue 12, 2011, Pages 2355-2368

  Jain, Akash K ^a   Bhattacharya, Santanu ^a,b  

^a INDIAN INSTITUTE OF SCIENCE   (India)

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

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; DISEASES; DNA SEQUENCES; LIGANDS; ONCOGENIC VIRUSES;

BINDING LIGANDS; CANCER CELLS; DNA STRANDS; DUPLEX DNA; G-QUADRUPLEX STRUCTURE; G-QUADRUPLEXES; GROOVE-BINDING; MINOR GROOVES; TELOMERASE; TELOMERES;

DNA;

CONGOCIDINE; CYANINE DYE; DISTAMYCIN A; DNA BINDING PROTEIN; DOUBLE STRANDED DNA; GUANINE QUADRUPLEX; MINOR GROOVE BINDING LIGAND; OLIGODEOXYNUCLEOTIDE; POLYAMIDE; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANISOTROPY; BINDING AFFINITY; BINDING SITE; CHEMICAL STRUCTURE; DNA DRUG COMPLEX; DNA HELIX; DNA REPLICATION; DNA SEQUENCE; DNA STRUCTURE; DNA TRANSCRIPTION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION; GENE MUTATION; HUMAN; HYDROGEN BOND; IN VITRO STUDY; LIGAND BINDING; REVIEW; STOICHIOMETRY; TELOMERE; THERMODYNAMICS;

TETRA;

EID: 84555186973     PISSN: 10431802     EISSN: 15204812     Source Type: Journal    
DOI: 10.1021/bc200268a     Document Type: Review

References (114)

1. Blackburn, E. H. and Gall, J. G. (1978) A tandemly repeated sequence at the termini of the extrachromosomal ribosomal RNA genes in Tetrahymena J. Mol. Biol. 120, 33-53 (Pubitemid 8312910)
2. Morin, G. B. (1989) The human telomere terminal transferase enzyme is a ribonucleoprotein that synthesizes TTAGGG repeats Cell 59, 521-529 (Pubitemid 19284465)
3. Griffith, J. D., Comeau, L., Rosenfield, S., Stansel, R. L., Bianchi, A., Moss, H., and Lange, Tde. (1999) Mammalian telomeres end in a large duplex loop Cell 97, 503-514 (Pubitemid 29231173)
4. Lingner, J., Cooper, J. P., and Cech, T. R. (1995) Telomerase and DNA end replication: no longer a lagging strand problem? Science 269, 1533-1534
5. Greider, C. W. and Blackburn, E. H. (1985) Identification of a specific telomere terminal transferase activity in tetrahymena extracts Cell 43, 405-413 (Pubitemid 16213265)
6. Yu, G. L., Bradley, J. D., Attardi, L. D., and Blackburn, E. H. (1990) In vivo alteration of telomere sequences and senescence caused by mutated tetrahymena telomerase RNAs Nature 344, 126-132
7. Cech, T. R. (2000) Life at the end of the chromosome: Telomeres and telomerase Angew. Chem., Int. Ed. 39, 34-43
8. Chen, H., Li, Y., and Tollefsbol, T. O. (2009) Strategies targeting telomerase inhibition Mol. Biotechnol. 41, 194-199
9. Phatak, P. and Burger, A. M. (2007) Telomerase and its potential for therapeutic intervention Br. J. Pharmacol. 152, 1003-1011 (Pubitemid 350166039)
10. Balasubramanian., S. and Neidle, S. (2009) G-quadruplex nucleic acids as therapeutic targets Curr. Opin. Chem. Biol. 13, 345-353
11. McEachern, M. J., Krauskopf, A., and Blackburn, E. H. (2000) Telomeres and their control Annu. Rev. Genet. 34, 331-358 (Pubitemid 32065925)
12. Hurley, L. H. (2002) DNA and its associated processes as targets for cancer therapy Nat. Rev. Cancer 2, 188-200 (Pubitemid 37328788)
13. Sen, D. and Gilbert, W. (1988) Formation of parallel four-stranded complexes by guanine-rich motifs in DNA and its implications for meiosis Nature 334, 364-366
14. Catasti, P., Chen, X., Moyzis, R. K., Bradbury, E. M., and Gupta, G. (1996) Structure-function correlations of the insulin-linked polymorphic region J. Mol. Biol. 264, 534-545 (Pubitemid 27010743)
15. Siddiqui-Jain, A., Grand, C. L., Bearss, D. J., and Hurley, L. H. (2002) 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, 11593-11598 (Pubitemid 34994444)
16. Todd, A. K., Haider, S. M., Parkinson, G. N., and Neidle, S. (2007) Sequence occurrence and structural uniqueness of a G-quadruplex in the human c-kit promoter Nucleic Acids Res. 35, 5799-5808 (Pubitemid 47506295)
17. Huppert, J. L. and Balasubramanian, S. (2007) G-quadruplexes in promoters throughout the human genome Nucleic Acids Res. 35, 406-413 (Pubitemid 46232058)
18. Balasubramanian, S., Hurley, L. H., and Neidle, S. (2011) Targrtting G-quadruplexes in gene promoters: a novel anticancer strategy Nat. Rev. Drug Discovery 10, 261-275
19. Ou, T.-M., Lu, Y.-J., Zhang, C., Huang, Z.-S., Wang, X.-D., Tan, J.-H., Chen, Y., Ma, D.-L., Wong, K.-Y., Tang, J. C-O., Chan, A. S-C., and Gu, L.-Q. (2007) Stabilization of G-quadruplex DNA and down-regulation of oncogene c-myc by quindoline derivatives J. Med. Chem. 50, 1465-1474 (Pubitemid 46566333)
20. Davis, J. T. (2004) G-Quartets 40 Years Later: From 5? -GMP to molecular biology and supramolecular chemistry Angew. Chem., Int. Ed. 43, 668-669
21. Phan, A. T., Kuryavyi, V., Burge, S., Neidle, S., and Patel, D. J. (2007) Structure of an unprecedented G-quadruplex scaffold in the human c-kit promoter J. Am. Chem. Soc. 129, 4386-4392 (Pubitemid 46595454)
22. Pedroso, I. M., Duarte, L. F., Yanez, G., Burkewitz, K., and Fletcher., T. M. (2007) Sequence specificity of inter- and intramolecular G-quadruplex formation by human telomeric DNA Biopolymers 87, 74-84 (Pubitemid 47401783)
23. + solution: insights into structure polymorphism of the human telomeric sequence Nucleic Acids Res. 35, 4927-4940
24. + solution Nucleic Acids Res. 34, 5715-5719 (Pubitemid 44742458)
25. Dai, J., Carver, M., and Yang, D. (2008) Polymorphism of human telomeric quadruplex structures Biochimie 90, 1172-1183
26. Parkinson, G. N., Lee, M. P., and Neidle, S. (2002) Crystal structure of parallel quadruplex from human telomeric DNA Nature 417, 876-880 (Pubitemid 34670337)
27. Phan, A. T., Kuryavyi, V., and Patel, D. J. (2006) DNA architecture: from G to Z Curr. Opin. Struct. Biol. 16, 288-298 (Pubitemid 43831655)
28. Petraccone, L., Trent, J. O., and Chaires, J. B. (2008) The tail of the telomere J. Am. Chem. Soc. 130, 16530-16532
29. Yang, D. and Okamoto, K. (2010) Structural insights into G-quadruplexes: towards new anticancer drugs Future Med. Chem. 2, 619-646
30. 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
31. Jain, A. K. and Bhattacharya, S. (2010) Groove binding ligands for interaction with non B-DNA duplex and triplex DNA Bioconjugate Chem. 21, 1389-1403
32. Fuertes, M. A., Castilla, J., Alonso, C., and Perez, J. M. (2002) Novel concepts in the development of platinum antitumor drugs Curr. Med. Chem.-Anti-Cancer Agents 2, 539-551 (Pubitemid 34649888)
33. Neidle, S. (1981) The molecular bases for the action of some DNA-binding drugs Prog. Med. Chem. 16, 151-221
34. Thomas, M., Varshney, U., and Bhattacharya, S. (2002) Distamycin analogs without leading amide at the N-terminus: Comparative binding properties to AT and GC rich DNA sequences Eur. J. Org. Chem. 3604-3615
35. Bhattacharya, S. and Thomas, M. (2000) Facile synthesis of oligopeptide distamycin analogs devoid of hydrogen 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 (Pubitemid 30481670)
36. Bhattacharya, S. and Thomas, M. (2001) DNA recognition by the first tail-to-tail linked distamycin-like oligopeptide dimers Chem. Commun. 1464-1465 (Pubitemid 32747801)
37. Tawar, U., Jain, A. K., Dwarakanath, B. S., Chandra, R., Singh, Y., Chaudhury, N. K., Khaitan, D., and Tandon, V. (2003) Influence on phenyl ring disubstitution on bisbenzimidazole and terbenzimidazole cytotoxicity: Synthesis and biological evaluation as radioprotectors J. Med. Chem. 46, 3785-3792 (Pubitemid 37038092)
38. Tawar, U., Jain, A. K., Chandra, R., Singh, Y., Dwarakanath, B. S., Chaudhury, N. K., Good, L., and Tandon, V. (2003) Minor groove binding DNA ligands with expanded A/T sequence length recognition, selective binding to bent DNA regions and enhanced fluorescent properties Biochemistry 42, 13339-13346 (Pubitemid 37420686)
39. Jain, A. K., Gupta, S. K., and Tandon, V. (2009) Evaluation of electronic effect of phenyl ring substituents on the DNA minor groove binding properties of novel bis and terbenzimidazoles: Synthesis and spectroscopic studies of ligand-DNA interaction Oligonucleotides 19, 329-340
40. Ghosh, S., Usharani, D., Paul, A., De, S., Jemmis, E. D., and Bhattacharya, S. (2008) Design, synthesis, and DNA binding properties of photoisomerizable azobenzene-distamycin conjugates: An experimental and computational study Bioconjugate Chem. 19, 2332-2345
41. 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 (Pubitemid 38657857)
42. Bhattacharya, S. and Thomas, M. (2000) DNA binding properties of novel distamycin analogs that lack the leading amide unit at the N-terminus Biochem. Biophys. Res. Commun. 267, 139-144 (Pubitemid 30072521)
43. Jain, A. K., Awasthi, S. K., and Tandon, V. (2006) Triple helix stabilization by covalently linked DNA-bisbenzimidazole conjugate synthesized by maleimide-thiol coupling chemistry Bioorg. Med. Chem. 14, 6444-6452 (Pubitemid 44224067)
44. Jain, A. K.; Bhattacharya, S. Recent developments in the chemistry and biology of G-quadruplexes with reference to the DNA groove binders.. Curr. Pharm. Des. 2011, in press.
45. 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 (Pubitemid 351990958)
46. 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 0.95Å resolution J. Mol. Biol. 273, 171-182 (Pubitemid 27460223)
47. Han, H., Langley, D. R., Rangan, A., and Hurley, L. H. (2001) Selective interactions of cationic porphyrins with G-quadruplex structures J. Am. Chem. Soc. 123, 8902-8913 (Pubitemid 32884711)
48. 4) form parallel-stranded potassium cation stabilized G-quadruplexes with anti glycosidic torsion angles in solution Biochemistry 31, 8112-8119
49. Wang, Y. and Patel, D. J. (1993) Solution structure of a parallel-stranded G-quadruplex DNA J. Mol. Biol. 234, 1171-1183 (Pubitemid 24027245)
50. Read, M. A., Harrison, R. J., Romagnoli, B., Tanious, F. A., Gowan, S. H., Reszka, A. P., Wilson, W. D., Kelland, L. R., and Neidle, S. (2001) Structure-based design of selective and potent G quadruplex-mediated telomerase inhibitors Proc. Natl. Acad. Sci. U.S.A. 98, 4844-4849 (Pubitemid 32397044)
51. Yang, D.-Y., Chang, T.-C., and Sheu, S.-Y. (2007) Interaction between human telomere and a carbazole derivative: A molecular dynamics simulation of a quadruplex stabilizer and telomerase inhibitor J. Phys. Chem. A 111, 9224-9232 (Pubitemid 47548309)
52. Nambiar, M., Goldsmith, G., Moorthy, B. T., Lieber, M. R., Joshi, M. V., Choudhary, B., Hosur, R. V., and Raghavan, S. C. (2011) Formation of a G-quadruplex at the BCL2 major breakpoint region of the t(14;18) translocation in follicular lymphoma. 936-948 Nucleic Acids Res. 39, 936-948
53. Rawal, P., Kummarasetti, V. B. R., Ravindran, J., Kumar, N., Halder, K., Sharma, R., Mukerji, M., Das, S. K., and Chowdhury, S. (2006) Genome-wide prediction of G4 DNA as regulatory motifs: Role in Escherichia coli global regulation Genome Res. 16, 644-655
54. Du, Z., Zhao, Y., and Li, N. (2009) Genome-wide colonization of gene regulatory elements by G4 DNA motifs Nucleic Acids Res. 37, 6784-6798
55. Verma, A., Yadav, V. K., Basundra, R., Kumar, A., and Chowdhury, S. (2009) Evidence of genome-wide G4 DNA-mediated gene expression in human cancer cells. 4194-4204 Nucleic Acids Res. 37, 4194-4204
56. Du, Z., Zhao, Y., and Li, N. (2008) Genome-wide analysis reveals regulatory role of G4 DNA in gene transcription Genome Res. 18, 233-241 (Pubitemid 351240733)
57. Cogoi, S., Paramasivam, M., Filichev, V., Geci, I., Pedersen, E. B., and Xodo, L. E. (2009) Identification of a new G-quadruplex motif in the KRAS promoter and design of pyrene-modified G4-decoys with antiproliferative activity in pancreatic cancer cells J. Med. Chem. 52, 564-568
58. Fry, M. (2007) Tetraplex DNA and its interacting proteins Front. Biosci. 12, 4336-4351
59. Paramasivam, M., Membrino, A., Cogoi, S., Fukuda, H., Nakagama, H., and Xodo, L. E. (2009) Protein hnRNP A1 and its derivative Up1 unfold quadruplex DNA in the human KRAS promoter: implications for transcription Nucleic Acids Res. 37, 2841-2853
60. Thakur, R. K., Kumar, P., Halder, K., Verma, A., Kar, A., Parent, J.-L., Basundra, R., Kumar, A., and Chowdhury, S. (2009) Metastases suppressor NM23-H2 interaction with G-quadruplex DNA within c-MYC promoter nuclease hypersensitive element induces c-MYC expression Nucleic Acids Res. 37, 172-183
61. Phan, A. T., Kuryavyi, V., Ma, J. B., Faure, A., Andreola, M. L., and Patel, D. J. (2005) An interlocked dimeric parallel-stranded DNA quadruplex: a potent inhibitor of HIV-1 integrase Proc. Natl. Acad. Sci. U.S.A. 102, 634-639 (Pubitemid 40282717)
62. Kerwin, S. M. (2000) G-quadruplex DNA as a target for drug design Curr. Pharm. Des. 6, 441-478
63. 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 (Pubitemid 46418395)
64. Maiti, S., Chaudhury, N. K., and Chowdhury, S. (2003) Hoechst 33258 binds to G-quadruplex in the promoter region of human c-myc Biochem. Biophys. Res. Commun. 310, 505-512 (Pubitemid 37163693)
65. Phan, A. T., Kuryavyi, V., Gaw, H. Y., and Patel, D. J. (2005) Small-molecule interaction with a five-guanine-tract G-quadruplex structure from the human MYC promoter Nat. Chem. Biol. 1, 167-163
66. Chen, Z., Zheng, K-w., Hao, Y-h., and Tan, Z. (2009) Reduced or diminished stabilization of the telomere G-quadruplex and inhibition of telomerase by small chemical ligands under molecular crowding condition J. Am. Chem. Soc. 131, 10430-10438
67. Li, G., Huang, J., Zhang, M., Zhou, Y., Zhang, D., Wu, Z., Wang, S., Weng, X., Zhou, X., and Yang, G. (2008) Bis(benzimidazole)pyridine derivative as a new class of G-quadruplex inducing and stabilizing ligand Chem. Commun. 4564-4566
68. Huang, J., Li, G., Wu, Z., Song, Z., Zhou, Y., Shuai, L., Weng, X., Zhou, X., and Yang, G. (2009) Bisbenzimidazole to benzobisimidazole: from binding B-form duplex DNA to recognizing different modes of telomere G-quadruplex Chem. Commun. 902-904
69. Bhattacharya, S., Chaudhuri, P., Jain, A. K., and Paul, A. (2010) 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 Chem. 21, 1148-1159
70. Jain, A. K., Reddy, V. V., Paul, A., Muniyappa, K., and Bhattacharya, S. (2009) The synthesis and evaluation of a novel class of G-quadruplex stabilizing small molecules based on 1, 3-Phenylene-bis (piperazinyl benzimidazole) system Biochemistry 48, 10693-10704
71. Randazzo, A., Galeone, A., Esposito, V., Varra, M., and Mayol, L. (2002) Interaction of distamycin A and netropsin with quadruplex and duplex structures: a comparative 1H-NMR study Nucleosides, Nucleotides, Nucleic Acids 21, 535-545 (Pubitemid 35417090)
72. 4 Chem. Commun. 11, 1030-1031 (Pubitemid 32521850)
73. 4 J. Am. Chem. Soc. 129, 16048-16056
74. Cocco, M. J., Hanakahi, L. A., Huber, M. D., and Maizels, N. (2003) Specific interactions of distamycin with G-quadruplex DNA Nucleic Acids Res. 31, 2944-2951 (Pubitemid 37442137)
75. David, W. M., Brodbelt, J., Kerwin, S. M, and Thomas, P. W. (2002) Investigation of quadruplex oligonucleotide-Drug interactions by electrospray ionization mass spectrometry Anal. Chem. 74, 2029-2033 (Pubitemid 34465398)
76. Pagano, B., Fotticchia, I., Tito, S., De Mattia, C. A., Mayol, L., Novellino, E., Randazzo, A., and Giancola, C. (2010) Selective binding of distamycin A derivative to G-quadruplex structure [d(TGGGGT)]4. J. Nucleic. Acids, doi: 10.4061/2010/247137.
77. 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
78. Pagano, B., Mattia, C. A., Virno, A., Randazzo, A., Mayol, L., and Giancola, C. (2007) Thermodynamic analysis of quadruplex DNA-drug interaction Nucleosides, Nucleotides, Nucleic Acids 26, 761-765 (Pubitemid 350239210)
79. Moore, M. J. B., Cuenca, F., Searcey, M., and Neidle, S. (2006) Synthesis of distamycin A polyamides targeting G-quadruplex DNA Org. Biomol. Chem. 4, 3479-3488 (Pubitemid 44319636)
80. Zhou, J., Yuan, G., Liu, J., and Zhan, C.-G. (2007) Formation and stability of G-quadruplexes self-assembled from guanine-rich strands Chem. - Eur. J. 13, 945-949 (Pubitemid 46144570)
81. Li, H., Liu, Y., Lin, S., and Yuan, G. (2009) Spectroscopy probing of the formation, recognition, and conversion of a G-quadruplex in the promoter region of the bcl-2 oncogene Chem. - Eur. J. 15, 2445-2452
82. Zaffaroni, N., Lualdi, S., Villa, R., Bellarosa, D., Cermele, C., Felicetti, P., Rossi, C., Orlandi, L., and Daidone, M. G. (2002) Inhibition of telomerase activity by a distamycin derivative: effects on cell proliferation and induction of apoptosis in human cancer cells Eur. J. Cancer 38, 1792-1801
83. Cosconati, S., Marinelli, L., Trotta, R., Virno, A., Tito, S. D., Romagnoli, R., Pagano, B., Limongelli, V., Giancola, C., Baraldi, P. G., Mayol, L., Novellino, E., and Randazzo, A. (2010) Structural and conformational requisites in DNA quadruplex groove binding: Another piece to the puzzle J. Am. Chem. Soc. 132, 6425-6433
84. Han, X., Li, C., Mosher, M. D., Rider, K. C., Zhou, P., Crawford, R. L., Fusco, W., Paszczynski, A., and Natale, N. R. (2009) Design, synthesis and biological evaluation of a novel class of anticancer agents: Anthracenylisoxazole lexitropsin conjugates Bioorg. Med. Chem. 17, 1671-1680
85. Rahman, K. M., Reszka, A. P., Gunaratnam, M., Haider, S. M., Howard, P. W., Fox, K. R., Neidle, S., and Thurston, D. E. (2009) Biaryl polyamides as a new class of DNA quadruplex-binding ligands Chem. Commun. 4097-4099
86. Garoff, R. A., Litzinger, E. A., Connor, R. E., Fishman, I., and Armitage, B. A. (2002) Helical aggregation of cyanine dyes on DNA templates: effect of dye structure on formation of homo- and heteroaggregates Langmuir 18, 6330-6337 (Pubitemid 35383368)
87. Chen, Q., Kuntz, I. D., and Shafer, R. H. (1996) Spectroscopic recognition of guanine dimeric hairpin quadruplexes by a carbocyanine dye Proc. Natl. Acad. Sci. U.S.A. 93, 2635-2639 (Pubitemid 26114300)
88. Cheng, J.-Y., Lin, S.-H., and Chang, T.-C. (1998) Vibrational investigation of DODC cation for recognition of guanine dimeric hairpin quadruplex studied by satellite holes J. Phys. Chem. B 102, 5542-5546 (Pubitemid 128602339)
89. Chiang, C.-C., Cheng, J.-Y., and Chang, T.-C. (1999) Satellite hole spectral method and its applications to dye-DNA complexes Proc. Natl. Sci. Counc. Repub. China, Part A 23, 679-694
90. Kerwin, S. M., Sun, D., Kern., J. T., Rangan, A., and Thomas, P. W. (2001) G-quadruplex DNA binding by a series of carbocyanine dyes Bioorg. Med. Chem. Lett. 11, 2411-2414 (Pubitemid 32823322)
91. White, E. W., Tanious, F., Ismail, M. A., Reszka, A. P., Neidle, S., Boykin, D. W., and Wilson, W. D. (2007) Structure-specific recognition of quadruplex DNA by organic cations: influence of shape, substituents and charge Biophys. Chem. 126, 140-153 (Pubitemid 46186645)
92. Paramasivan, S. and Bolton, P. H. (2008) Mix and measure fluorescence screening for selective quadruplex binders Nucleic Acids Res. 36, e106
93. Yang, Q., Xiang, J., Yang, S., Zhou, Q., Li, Q., Tang, Y., and Xu, G. (2009) Verification of specific G-quadruplex structure by using a novel cyanine dye supramolecular assembly: I. recognizing mixed G-quadruplex in human telomeres Chem. Commun. 1103-1105
94. Yang, Q., Xiang, J., Yang, S., Li, Q., Zhou, Q., Guan, A., Zhang, X., Zhang, H., Tang, Y., and Xu, G. (2010) Verification of specific G-quadruplex structure by using a novel cyanine dye supramolecular assembly: II. The binding characterization with specific intramolecular G-quadruplex and the recognizing mechanism Nucleic Acids Res. 38, 1022-1033
95. Tuesuwan, B., Kern, J. T, Thomas, P. W., Rodriguez, M., Li., J., David, W. M., and Kerwin, S. M. (2008) Simian virus 40 large T-antigen G-quadruplex DNA helicase inhibition by G-quadruplex DNA-interactive agents Biochemistry 47, 1896-1909 (Pubitemid 351287115)
96. Fu, W., Begley, J. G., Killen, M. W., and Mattson, M. P. (1999) Anti-apoptotic role of telomerase in pheochromocytoma cells J. Biol. Chem. 274, 7264-7271
97. Li, C. P., Huang, J. H, Chang, A. C., Hung, Y. M., Lin, C. H., Chao, Y., Lee, S. D., Whang-Peng, J., and Huang, T. S. (2004) A G-quadruplex ligand 3, 30-diethyloxadicarbocyanine iodide induces mitochondrionmediated apoptosis but not decrease of telomerase activity in nasopharyngeal carcinoma NPC-TW01 cells Pharm. Res. 21, 93-100 (Pubitemid 38122296)
98. Yao, Y., Wang, Q., Hao, Yu-h., and Tan, Z. (2007) An exonuclease I hydrolysis assay for evaluating G-quadruplex stabilization by small molecules Nucleic Acids Res. 35, e68
99. Zhang, Y., Cao, E.-H., Liang, X.-Q., and Qin, J.-F. (2003) Increasing sensitivity to arsenic trioxide-induced apoptosis by altered telomere state Eur. J. Pharmacol. 474, 141-147 (Pubitemid 37281442)
100. Naasani, I., Seimiya, H., Yamori, T., and Tsuruo, T. (1998) Screening for antitelomerase agents with the aid of COMPARE analysis Proc. Am. Assoc. Cancer Res. 39, 3854
101. Huppert, J. L. and Balasubramanian, S. (2005) Prevalence of quadruplexes in the human genome Nucleic Acids Res. 33, 2908-2916 (Pubitemid 41511230)
102. Millar, K. M. and Rodriguez, R. (2011) G-quadruplexes: selective DNA targeting for cancer therapeutics? Expert Rev. Clin. Pharmacol. 4, 139-142
103. Folini, M., Venturini, L., Cimino-Reale, G., and Zaffaroni, N. (2011) Telomeres as targets for anticancer therapies Expert Opin. Ther. Targets 15, 579-593
104. Leonetti, C., Scarsella, M., Riggio, G., Rizzo, A., Salvati, E., DIncalci, M., Staszewsky, L., Frapolli, R., Stevens, M. F., Stoppacciaro, A., Mottolese, M., Antoniani, B., Gilson, E., Zupi, G., and Biroccio, A. (2008) G-Quadruplex ligand RHPS4 potentiates the antitumoractivity of camptothecins in preclinical models of solid tumors Clin. Cancer Res. 14, 7284-7291
105. Gomez, D., Wenner, T., Brassart, B., Douarre, C., ODonohue, M.-F., El Khoury, V., Shin-ya, K., Morjani, H., Trentesaux, C., and Riou, J.-F. (2006) Telomestatin-induced telomere uncapping is modulated by POT1 through G-overhang extension in HT1080 human tumor cells J. Biol. Chem. 281, 38721-38729 (Pubitemid 46041999)
106. Tsai, Y-C, Qi, H, Lin, C-P, Lin, C.-P., Lin, R.-K., Kerrigan, J. E., Rzuczek, S. G., Edmond J. LaVoie, E. J., Rice, J. E., Pilch, D. S., Lyu, Y. L., and Liu, L. F. (2009) A G-quadruplex stabilizer induces M-phase cell cycle arrest J. Biol. Chem. 284, 22535-22543
107. Burger, A. M., Dai, F., Schultes, C. M., Reszka, A. P., Moore, M. J., Double, J. A., and Neidle, S. (2005) The G-quadruplex-interactive molecule BRACO-19 inhibits tumor growth, consistent with telomere targeting and interference with telomerase function Cancer Res. 65, 1489-1496 (Pubitemid 40270178)
108. Drygin, D., Siddiqui-Jain, A., OBrien, S., Schwaebe, M., Lin, A., Bliesath, J., Ho, C. B., Proffitt, C., Trent, K., Whitten, J. P., Lim, J. K. C., Von Hoff, D., Anderes, K., and Rice, W. G. (2009) Anticancer activity of CX-3543: a direct inhibitor of rRNA biogenesis Cancer Res. 69, 7653-7661
109. Pennarun, G., Granotier, C., Gauthier, L. R., Gomez, D., and Boussin, F. D. (2005) Apoptosis related to telomere instability and cell cycle alterations in human glioma cells treated by new highly selective G-quadruplex ligands Oncogene 24, 2917-2928 (Pubitemid 40675523)
110. Riou, J. F., Guittat, L., Mailliet, P., Laoui, A., Renou, E., Petitgenet, O., Megnin-Chanet, F., Helene, C., and J. L. Mergny, J. L. (2002) Cell senescence and telomere shortening induced by a new series of specific G-quadruplex DNA ligands Proc. Natl. Acad. Sci. U.S.A. 99, 2672-2677 (Pubitemid 34240519)
111. Huppert, J. L. (2007) Four-stranded DNA: cancer, gene regulation and drug development Philos. Trans. R. Soc. A 365, 2969-2984
112. 2phi: A combination of shape selection and direct readout Biochemistry 37, 16093-16105 (Pubitemid 28536246)
113. Koya, K., Li, Y., Wang, H., Ukai, T., Tatsuta, N., Kawakami, M., Shishido, T., and Chen, L. B. (1996) MKT-077, a novel rhodacyanine dye in clinical trials, exhibits anticarcinoma activity in preclinical studies based on selective mitochondrial accumulation Cancer Res. 56, 538-543 (Pubitemid 26048603)
114. Kawakami, M., Koya, K., Ukai, T., Tatsuta, N., Ikegawa, A., Ogawa, K., Shishido, T., and Chen, L. B. (1998) Structure-activity of novel rhodacyanine dyes as antitumor agents J. Med. Chem. 41, 130-142 (Pubitemid 28070475)