5-N-methylated quindoline derivatives as telomeric G-quadruplex stabilizing ligands: Effects of 5-N positive charge on quadruplex binding affinity and cell proliferation

Journal of Medicinal Chemistry

Volumn 51, Issue 20, 2008, Pages 6381-6392

  Lu, Yu Jing ^a   Ou, Tian Miao ^a   Tan, Jia Heng ^a   Hou, Jin Qiang ^a   Shao, Wei Yan ^a   Peng, Dan ^a   Sun, Ning ^a   Wang, Xiao Dong ^a   Wu, Wei Bin ^a   Bu, Xian Zhang ^a   Huang, Zhi Shu ^a   Ma, Dik Lung ^b   Wong, Kwok Yin ^b   Gu, Lian Quan ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b HONG KONG POLYTECHNIC UNIVERSITY   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

CRYPTOLEPINE DERIVATIVE;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BINDING AFFINITY; CANCER CELL CULTURE; CANCER INHIBITION; CELL PROLIFERATION; CIRCULAR DICHROISM; CONTROLLED STUDY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; IC 50; MOLECULAR MODEL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POLYMERASE CHAIN REACTION; TELOMERE;

ALKALOIDS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL-FREE SYSTEM; CIRCULAR DICHROISM; DIALYSIS; ENZYME INHIBITORS; G-QUADRUPLEXES; HUMANS; INDOLES; LIGANDS; METHYLATION; MODELS, MOLECULAR; POTASSIUM; QUINOLINES; STRUCTURE-ACTIVITY RELATIONSHIP; TELOMERASE; TELOMERE; THERMODYNAMICS;

EID: 54549117013     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm800497p     Document Type: Article

References (67)

1. Blackburn, E. H. Structure and function of telomeres. Nature 1991, 350, 569-573.
2. Blackburn, E. H. Switching and signaling at the telomere. Cell 2001, 106, 661-673.
3. Harley, C. B.; Futcher, A. B.; Greider, C. W. Telomeres shorten during aging of human Fibroblasts. Nature 1990, 345, 458-460.
4. Greider, C. W.; Blackburn, E. H. Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 1985, 43, 405-413.
5. Feng, J.; Funk, W.; Wang, S.-S.; Weinrich, S. L.; Avilion, A. A.; Chiu, C.-P.; Adam, R. R.; Chang, E. The RNA component of human telomerase. Science 1995, 269, 1236.
6. 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.; Shay, J. W. Specific association of human telomerase activity with immortal cell and cancer. Science 1994, 266, 2011-2015.
7. Bryan, T. M.; Cech, T. R. Telomerase and maintenance of chromosome ends. Curr. Opin. Cell Biol. 1999, 11, 318-322.
8. Masutomi, K.; Yu, E. Y.; Khurts, S.; Ben-Porath, I.; Currier, J. L.; Metz, G. B.; Brooks, M. W.; Kaneko, S.; Murakami, S.; DeCaprio, J. A.; Weinberg, R. A.; Stewart, S. A.; Hahn, W. C. Telomerase maintains telomere structure in normal human cells. Cell 1999, 114, 241-253.
9. Herbert, B. S.; Pitts, A. E.; Baker, S. I.; Hamilton, S. E.; Wright, W. E.; Shay, J. W.; Corey, D. R. Inhibition of human telomerase in immortal human cells leads to progressive telomere shortening and cell death. Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 14276-14281.
10. Neidle, S.; Parkinson, G. Telomere maintenance as a target for anticancer drug discovery. Nat. Rev. Drug Discovery 2002, 1, 383-393.
11. Herbert, B. S.; Pitts, A. E.; Baker, S. I.; Hamilton, S. E.; Wright, W. E.; Shay, J. W.; Corey, D. R. Inhibition of human telomerase in immortal human cells leads to progressive telomere shortening and cell death. Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 14276-14281.
12. Mergny, J.-L.; Riou, J.-F.; Mailliet, P.; Teulade-Fichou, M.-P.; Gilson, E. Natural and pharmacological regulation of telomerase. Nucleic Acids Res. 2002, 30, 839-865.
13. Rezler, E. M.; Rearss, D. J.; Hurley, L. H. Telomeres and telomerases as drug targets. Curr. Opin. Pharmacol. 2002, 2, 415-423.
14. De Cian, A.; Lacroix, L.; Douarre, C.; Temime-Smaali, N.; Trentesaux, C.; Riou, J.-F.; Mergny, J.-L. Targeting telomeres and telomerase. Biochime 2008, 90, 131-155.
15. Ou, T.-M.; Lu, Y.-J.; Tan, J.-H.; Huang, Z.-S.; Wong, K.-Y.; Gu, L.-Q. G-quadruplexes: targets in anticancer drug design ChemMedChem 2008, DOI:10.1002/cmdc.200700300.
16. Neidle, S.; Parkinson, G. N. The structure of telomeric DNA. Curr. Opin. Struct. Biol. 2003, 13, 275-283.
17. Kim, M.-Y.; Vankayalapati, H.; Shin-ya, K.; Wierzba, K.; Hurley, L. H. Telomestatin, a Potent Telomerase Inhibitor That Interacts Quite Specifically with the Human Telomeric Intramolecular G-Quadruplex. J. Am. Chem. Soc. 2002, 124, 2098-2099.
18. 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.
19. Read, M. A.; Wood, A. A.; Harrison, J. R.; Gowan, S. M.; Kelland, L. R.; Dosanjh, H. S.; Neidle, S. Molecular Modeling Studies on G-Quadruplex Complexes of Telomerase Inhibitors: Structure-Activity Relationships. J. Med. Chem. 1999, 42, 4538-4546.
20. Read, M.; Harrison, R. J.; Romagnoli, B.; Tanious, F. A.; Gowan, S. H.; Reszka, A. P.; Wilson, W. D.; Kelland, L. R.; Neidle, S. Structure-based design of selective and potent G quadruplex-mediated telomerase inhibitors. Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 4844-4849.
21. Moore, M. J. B.; Schultes, C. M.; Cuesta, J.; Cuenca, F.; Gunaratnam, M.; Tanious, F. A.; Wilson, W. D.; 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. 2006, 49, 582-599.
22. Cookson, J. C.; Heald, R. A.; Stevens, M. F. G. Antitumor polycyclic acridines. 17. Synthesis and pharmaceutical profiles of pentacyclic acridinium salts designed to destabilize telomeric integrity. J. Med. Chem. 2005, 48, 7198-7207.
23. Fedoroff, O. Y.; Salazar, M.; Han, H.; Chemeris, V. V.; Kerwin, S. M.; Hurley, L. H. NMR-based model of a telomerase-inhibiting compound bound to G-quadruplex DNA. Biochemistry 1998, 37, 12367-12374.
24. Kern, J. T.; Wang, T. P.; Kerwin, S. M. The relationship between ligand aggregation and G-quadruplex DNA selectivity in a series of 3,4,9,10- perylenetetracarboxylic acid diimides. Biochemistry 2002, 41, 11379-11389.
25. Gomez, D.; Aouali, N.; Renaud, A.; Douarre, C.; Shin-ya, K.; Tazi, J.; Martinez, S.; Trentesaux, C.; Morjani, H.; Riou, J.-F. Resistance to senescence induction and telomere shortening by a G-quadruplex ligand inhibitor of telomerase. Cancer Res. 2003, 63, 6149-6153.
26. Izbicka, E.; Wheelhouse, R. T.; Raymond, E.; Davidson, K. K.; Lawrence, R. A.; Sun, D.; Windle, B. E.; Hurley, L. H.; Von Hoff, D. D. Effects of cationic porphyrins as G-quadruplex interactive agents in human tumor cells. Cancer Res. 1999, 59, 639-644.
27. Missailidis, S.; Stanslas, J.; Modi, C.; Ellis, M. J.; Robins, R. A.; Laughton, C. A.; Stevens, M. F. G. Antitumor polycyclic acridines. Part 12. Physical and biological properties of 8,13-diethyl-6-methylquino[4,3,2-kl]acridinium iodide: a lead compound in anticancer drug design. Oncol. Res. 2002, 13, 175-189.
28. Gowan, S. M.; Heald, R.; Stevens, M. F. G.; Kelland, L. R. Potent inhibition of telomerase by small-molecule pentacyclic acridines capable of interacting with G-quadruplexes. Mol. Pharmacol. 2001, 60, 981-988.
29. Holt, S. J.; Petrow, V. Cabarzole, carbolines, and related compounds [Part 1]. J. Chem. Soc. 1947, 607-611.
30. Bierer, D. E.; Dubenko, L. G.; Zhang, P. Antihyperglycemic activities of cryptolepine analogues: an ethnobotanical lead structure from Cryptolepis sanguinolenta. J. Med. Chem. 1998, 41, 2754-2764.
31. Yang, S.-W.; Abdel-Kader, M.; Malone, S.; Werkhoven, M. C.; Wisse, J. H.; Bursuker, I.; Neddermann, K.; Fairchild, C.; Raventos-Suarez, C.; Menendez, A. T.; Lane, K.; Kingston, D. G. Synthesis and biological evaluation of analogues of cryptolepine, an alkaloid isolated from Suriname Rainforest. J. Nat.Prod 1999, 62, 976-983.
32. Lisgarten, J. N.; Coll, M.; Portugal, J. W. W. C.; Aymami, J. The antimalaral and cytotoxic drug cryptolepine intercalates into DNA at cytosine-cytosine sites. Nat. Struct. Biol. 2002, 9, 57-60.
33. Caprio, V.; Guyen, B.; Opoku-Boahen, Y.; Mann, J.; Gowan, S. M.; Kelland, L. M.; Read, M. A.; Neidle, S. A novel inhibitor of human telomerase derived from 10H-indolo-[3,2-b]quinoline. Bioorg. Med. Chem. Lett. 2000, 10, 2063-2066.
34. Guyen, B.; Schultes, C. M.; Hazel, P.; Mann, J.; Neidle, S. Synthesis and evaluation of analogs of 10H-indolo[3,2-b]quinoline as G-quadruplex stabilizing ligands and potential inhibitors of the enzyme telomerase. Org. Biomol. Chem. 2004, 2, 981-988.
35. LeSanna, C.; Huddlestona, J.; Mann, J. Synthesis and preliminary evaluation of novel analogues of quindolines as potential stabilisers of telomeric G-quadruplex DNA. Tetrahedron 2007, 63, 12903-12911.
36. Zhou, J.-L.; Lu, Y.-J.; Ou, T.-M.; Zhou, J.-M.; Huang, Z.-S.; Zhu, X.-F.; Du, C.-J.; Bu, X.-Z.; Ma, L.; Gu, L.-Q.; Li, Y.-M.; Chan, A. S.-C. Synthesis and evaluation of quindoline derivatives as G-quadruplex inducing and stabilizing ligands and potential inhibitors of telomerase. J. Med. Chem. 2005, 48, 7315-7321.
37. Zhou, J. M.; Zhu, X. F.; Lu, Y. J.; Deng, R.; Huang, Z. S.; Mei, Y. P.; Wang, Y.; Huang, W. L.; Liu, Z. C.; Gu, L. Q.; Zeng, Y. X. Senescence and telomere shortening induced by novel potent G-quadruplex interactive agents, quindoline derivatives, in human cancer cell lines. Oncogene 2006, 25, 503-511.
38. Monchaud, D.; Teulade-Fichou, M. P. A hitchhiker's guide to G-quadruplex ligands. Org. Biomol. Chem. 2008, 6, 627-636.
39. Fan, P.; Ablordeppey, S. Y. An alternative synthesis of 10-Indolo[3,2-b]quinoline and its selective N-alkylation. J. Heterocycl. Chem. 1997, 34, 1789-1794.
40. Li, W.; Wu, P.; Ohmichi, T.; Sugimoto, N. Characterization and thermodynamic properties of quadruplex/duplex competition. FEBS Lett. 2002, 526, 77-81.
41. Balagurumoorthy, P.; Brahmachari, S. K.; Mohanty, D.; Bansal, M.; Sasisekharan, V. Hairpin and parallel quartet structures for telomeric sequences. Nucleic Acids Res. 1992, 20, 4061-4067.
42. Rezler, E. M.; Seenisamy, J.; Bashyam, S.; Kim, M.-Y.; White, E.; Wilson, W. D.; Hurley, L. H. Telomestatin and diseleno sapphyrin bind selectively to two different forms of the human telomeric G-quadruplex structure. J. Am. Chem. Soc. 2005, 127, 9439-9447.
43. Paramasivan, S.; Rujan, I.; Bolton, P. H. Circular dichroism of quadruplex DNAs: applications to structure, cation effects and ligand binding. Methods 2007, 43, 324-331.
44. Mergny, J.-L.; Lacroix, L.; Teulade-Fichou, M.-P.; Hounsou, C.; Guittat, L.; Hoarau, M.; Arimondo, P. B.; Vigneron, J.-P.; Lehn J.-M.; Riou, J.-F.; Garestier, T.; Helene, C. Telomerase inhibitors based on quadruplex ligands selected by a fluorescence assay. Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 3062-3067.
45. De Cian, A.; Guittat, L.; Kaiser, M.; Sacca, B.; Amrane, S.; Bourdoncle, A.; Alberti, P.; Teulade-Fichou, M. P.; Lacroix, L.; Mergny, J. L. Fluorescence-based melting assays for studying quadruplex ligands. Methods 2007, 42, 183-95.
46. Han, H.; Hurley, L. H.; Salazar, M. A DNA polymerase stop assay for G-quadruplex-interactive compounds. Nucleic Acids Res. 1999, 27, 537-542.
47. Lemarteleur, T.; Gomez, D.; Paterski, R.; Mandine, E.; Mailliet, P.; Riou, J.-F. Stabilization of the c-myc gene promoter quadruplex by specific ligands' inhibitors of telomerase. Biochem. Biophys. Res. Commun. 2004, 323, 802-808.
48. Parkinson, G. N.; Lee, M. P. H.; Neidle, S. Crystal structure of parallel quadruplexes from human telomeric DNA. Nature 2002, 417, 876-880.
49. Bates, P.; Mergny, J. L; Yang, D. Quartets in G-major. EMBO Rep. 2007, 8, 1003-1010.
50. Ragazzon, P.; Chaires, J. B. Use of competition dialysis in the discovery of G-quadruplex selective ligands. Methods 2007, 43, 313-323.
51. Gomez, D.; Mergny, J.-L.; Riou, J.-F. Detection of telomerase inhibitors based on G-quadruplex ligands by a modified telomeric repeat amplification protocol assay. Cancer Res. 2002, 62, 3365-3368.
52. De Cian, A.; Cristofari, G.; Reichenbach, P.; De Lemos, E.; Monchaud, D.; Teulade-Fichou, M.-P.; Shin-ya, K.; Lacroix, L.; Lingner, J.; Mergny, J.-L. Reevaluation of telomerase inhibition by quadruplex ligands and their mechanisms of action. Proc. Natl. Acad. Sci. USA 2007, 104, 17347-17352.
53. Hwang, E. S. Replicative senescence and senescence-like state induced in cancer-derived cells. Mech. Aging Dev. 2002, 123, 1681-1694.
54. Roninson, I. B. Tumor senescence as a determinant of drug response in vivo. Drug Resist. Updates 2002, 5, 204-208.
55. Mita, H.; Ohyama, T.; Tanaka, Y.; Yamamoto, Y. Formation of a complex of 5,10,15,20-tetrakis(N-methyl-pyridinium-4-yl)-21H, 23H-porphyrin with G-quadruplex DNA. Biochemistry 2006, 45, 6765-6772.
56. Morris, G. M.; Goodsell, D. S.; Halliday, R. S.; Huey, R.; Hart, W. E.; Belew, R. K.; Olson, A. J. Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J. Comput. Chem. 1998, 19, 1639-1662.
57. Sanner, M. F. Python: a programming language for software integration and development. J. Mol. Graphics Modell. 1999, 17, 57-61.
58. Cornell, W. D.; Cieplak, C. I.; Bayly, I. R.; Gould, I. R.; Merz, K. M.; Ferguson, D. M.; Spellmeyer, D. C.; Fox, T.; Caldwell, J. W.; Kollman, P. A. A second generation force field for the simulation of proteins, nucleic acids and organic molecules. J. Am. Chem. Soc. 1995, 117, 5179-5197.
59. Wang, J.; Wolf, R. M.; Caldwell, J. W.; Kollman, P. A.; Case, D. A. Development and testing of a general amber force field. J. Comput. Chem. 2004, 25, 1157-1174.
60. Hazel, P.; Parkinson, G. N.; Neidle, S. Predictive modelling of topology and loop variations in dimeric DNA quadruplex structures. Nucleic Acids Res. 2006, 34, 21172127.
61. Darden, T.; York, D.; Pedersen, L. Particle mesh Ewald: An N log - (N) method for Ewald sums in large systems. J. Chem. Phys. 1993, 98, 10089-10092.
62. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 1983, 79, 926-935.
63. Ryckaert, J. P.; Ciccotti, G.; Berendsen, H. J. C. Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys. 1977, 23, 327-341.
64. Humphrey, W.; Dalke, A.; Schulten, K. VMD: visual molecular dynamics. J. Mol. Graphics 1996, 14, 33-38.
65. Kollman, P. A.; Massova, I.; Reyes, C.; Kuhn, B.; Huo, S. H.; Chong, L.; Lee, M.; Lee, T.; Duan, Y.; Wang, W.; Donini, O.; Cieplak, P.; Srinivasan, J.; Case, D. A.; Cheatham, T. E. Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models. Acc. Chem. Res. 2000, 33, 889-897.
66. Sitkoff, D.; Sharp, K. A.; Honig, B. Accurate calculation of hydration free energies using macroscopic solvent models. J. Phys. Chem. 1994, 98, 1978-1988.
67. Kottalam, J.; Case, D. A. Langevin modes of macromolecules - applications to Crambin and DNA hexamers. Biopolymers 1990, 29, 1409-1421.