Ascididemin and meridine stabilise G-quadruplexes and inhibit telomerase in vitro

Biochimica et Biophysica Acta - General Subjects

Volumn 1724, Issue 3, 2005, Pages 375-384

  Guittat, Lionel ^a   De Cian, Anne ^a   Rosu, Frédéric ^b   Gabelica, Valérie ^b   De Pauw, Edwin ^b   Delfourne, Evelyne ^c   Mergny, Jean Louis ^a  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^b UNIVERSITY OF LIÈGE   (Belgium)

^c UPS)   (France)

Author keywords

DNA ligands; G quadruplex; G Quartet; Telomerase inhibitor; Telomeres

Indexed keywords

ALKALOID; ASCIDIDEMIN; DNA; DOUBLE STRANDED DNA; MERIDINE; SINGLE STRANDED DNA; TELOMERASE; TELOMERASE INHIBITOR; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; ASSAY; BINDING AFFINITY; CONCENTRATION RESPONSE; DIALYSIS; DIALYSIS COMPETITION ASSAY; DNA BINDING; DRUG DNA INTERACTION; ENZYME INHIBITION; IN VITRO STUDY; MASS SPECTROMETRY; MOLECULAR RECOGNITION; PRIORITY JOURNAL;

ALKALOIDS; DIALYSIS; DNA; INTERCALATING AGENTS; LIGANDS; MASS SPECTROMETRY; PHENANTHROLINES; QUINOLINES; SPECTROMETRY, FLUORESCENCE; TELOMERASE;

EID: 23144458156     PISSN: 03044165     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbagen.2005.04.023     Document Type: Article

References (67)

1. E. Delfourne, and J. Bastide Marine pyridoacridine alkaloids and synthetic analogues as antitumour agents Med. Res. Rev. 23 2003 234 252
2. F.J. Schmitz, F.S. De Guzman, M.B. Hossain, and D. van der Helm Cytotoxic aromatic alkaloid from the ascidian Amphicarpa meridiana and Leptoclinides sp.: Meridine and 11-hydroxyascididemin J. Org. Chem. 56 1991 804 808
3. J. Kobayashi, J. Cheng, H. Nakamura, and Y. Ohizumi Ascididemin, a novel pentacyclic aromatic alkaloid with potent antileukemic activity from the okinawan tunicate Didemnum sp. Tetrahedron Lett. 29 1988 1177 1180
4. S.S. Matsumoto, M.H. Sidford, J.A. Holden, L.R. Barrows, and B.R. Copp Mechanism of action studies of cytotoxic marine alkaloids: ascididemin exhibits thiol-dependant oxidative DNA cleavage Tetrahedron Lett. 41 2000 1667 1670
5. I. Bonnard, N. Bontemps, S. Lahmi, B. Banaigs, G. Combaut, C. Francisco, P. Colson, C. Houssier, M. Waring, and C. Bailly Binding to DNA and cytotoxic evaluation of ascididemin, the major alkaloid from the Mediterranean ascidian Cystodytes dellechiajei Anti-Cancer Drug Des. 10 1995 333 346
6. A. Rich DNA comes in many forms Gene 135 1993 99 109
7. M. Mills, L. Lacroix, P. Arimondo, J.L. Leroy, J.C. François, H.H. Klump, and J.L. Mergny Unusual DNA conformations: implications for telomeres Curr. Med. Chem., Anti-Cancer Agents 2 2002 627 644
8. J.R. Williamson G-quartet structures in telomeric DNA Annu. Rev. Biophys. Biomol. Struct. 23 1994 703 730
9. J.T. Davis G-quartets 40 years later: from 5′-GMP to molecular biology and supramolecular chemistry Angew. Chem., Int. Ed. 43 2004 668 698
10. K. Masutomi, E.Y. Yu, S. Khurts, I. BenPorath, J.L. Currier, G.B. Metz, M.W. Brooks, S. Kaneko, S. Murakami, J.A. DeCaprio, R.A. Weinberg, S.A. Stewart, and W.C. Hahn Telomerase maintains telomere structure in normal human cells Cell 114 2003 241 253
11. Y. Wang, and D.J. Patel Solution structure of the human telomeric repeat d[AG3(T2AG3)3] G-Tetraplex Structure 1 1993 263 282
12. G.N. Parkinson, M.P.H. Lee, and S. Neidle Crystal structure of parallel quadruplexes from human telomeric DNA Nature 417 2002 876 880
13. A.M. Zahler, J.R. Williamson, T.R. Cech, and D.M. Prescott Inhibition of telomerase by G-quartet DNA structures Nature 350 1991 718 720
14. D. Sun, B. Thompson, B.E. Cathers, M. Salazar, S.M. Kerwin, J.O. Trent, T.C. Jenkins, S. Neidle, and L.H. Hurley Inhibition of human telomerase by a G-quadruplex-interactive compound J. Med. Chem. 40 1997 2113 2116
15. J.L. Mergny, and C. Hélène G-quadruplex DNA: a target for drug design Nat. Med. 4 1998 1366 1367
16. J.L. Mergny, J.F. Riou, P. Mailliet, M.P. Teulade-Fichou, and E. Gilson Natural and pharmacological regulation of telomerase Nucleic Acids Res. 30 2002 839 865
17. G. Saretzki Telomerase inhibition as cancer therapy Cancer Lett. 194 2003 209 219
18. E.M. Rezler, D.J. Bearss, and L.H. Hurley Telomere inhibition and telomere disruption as processes for drug targeting Annu. Rev. Pharmacol. Toxicol. 43 2003 359 379
19. J. Cuesta, M. Read, and S. Neidle The design of G-quadruplex ligands as telomerase inhibitors Mini Rev. Med. Chem. 3 2003 11 21
20. L.K. White, W.E. Wright, and J.W. Shay Telomerase inhibitors Trends Biotech. 19 2001 114 120
21. P.T. Rowley Development of telomerase inhibitors Expert Opin. Ther. Pat. 11 2001 1815 1823
22. S.M. Kerwin G-quadruplex DNA as a target for drug design Curr. Pharm. Des. 6 2000 441 471
23. L. Guittat, P. Alberti, D. Gomez, A. de Cian, G. Pennarun, T. Lemarteleur, C. Belmokhtar, R. Paterski, H. Morjani, C. Trentesaux, E. Mandine, F. Boussin, P. Mailliet, L. Lacroix, J.-F. Riou, and J.-L. Mergny Targeting human telomerase for cancer therapeutics Cytotechnomogy 45 2004 75 90
24. L. Guittat, P. Alberti, F. Rosu, S. Van Miert, E. Thetiot, L. Pieters, V. Gabelica, E. De Pauw, A. Ottaviani, J.F. Riou, and J.-L. Mergny Interactions of cryptolepine and neocryptolepine with unusual DNA structures Biochimie 85 2003 535 547
25. K. Shin-ya, K. Wierzba, K. Matsuo, T. Ohtani, Y. Yamada, K. Furihata, Y. Hayakawa, and H. Seto Telomestatin, a novel telomerase inhibitor from Streptomyces anulatus J. Am. Chem. Soc. 123 2001 1262 1263
26. M.Y. Kim, H. Vankayalapati, K. Shin-Ya, K. Wierzba, and L.H. Hurley Telomestatin, a potent telomerase inhibitor that interacts quite specifically with the human telomeric intramolecular G-quadruplex J. Am. Chem. Soc. 124 2002 2098 2099
27. S. Gowan, R. Heald, M. Stevens, and L. Kelland Potent inhibition of telomerase by small-molecule pentacyclic acridines capable of interacting with G-quadruplexes Mol. Pharmacol. 60 2001 981 988
28. F. Bracher Total synthesis of the pentacyclic alkaloid ascididemin Heterocycles 29 1989 2093 2095
29. N. Bontemps, E. Delfourne, J. Bastide, C. Francisco, and F. Bracher Total synthesis of the marine pentacyclic alkaloid meridine Tetrahedron 53 1997 1743 1750
30. C.R. Cantor, M.M. Warshaw, and H. Shapiro Oligonucleotide interactions. 3. Circular dichroism studies of the conformation of deoxyoligonucleotides Biopolymers 9 1970 1059 1077
31. J.S. Ren, and J.B. Chaires Sequence and structural selectivity of nucleic acid binding ligands Biochemistry 38 1999 16067 16075
32. J.S. Ren, and J.B. Chaires Rapid screening of structurally selective ligand binding to nucleic acids J.B. Chaires M.J. Waring Drug Nucleic Acid Interaction 2001 Academic Press Inc. 525 B Street, Suite 1900, San Diego, CA 92101-4495, USA 99 108
33. J.B. Chaires, J. Ren, D. Hamelberg, A. Kumar, V. Pandya, D.W. Boykin, and W.D. Wilson Structural selectivity of aromatic diamidines J. Med. Chem. 47 2004 5729 5742
34. F. Rosu, E.D. Pauw, L. Guittat, P. Alberti, L. Lacroix, P. Mailliet, J.-F. Riou, and J.-L. Mergny Selective interaction of ethidium derivatives with quadruplexes Biochemistry 42 2003 10361 10371
35. J.L. Mergny, and J.C. Maurizot Fluorescence resonance energy transfer as a probe for G-quartet formation by a telomeric repeat ChemBioChem 2 2001 124 132
36. J.L. Mergny, L. Lacroix, M.P. Teulade-Fichou, C. Hounsou, L. Guittat, M. Hoarau, P.B. Arimondo, J.P. Vigneron, J.M. Lehn, J.F. Riou, T. Garestier, and C. Hélène Telomerase inhibitors based on quadruplex ligands selected by a fluorescent assay Proc. Natl. Acad. Sci. U. S. A. 98 2001 3062 3067
37. J. Beck, M.L. Colgrave, S.F. Ralph, and M.M. Sheil Electrospray ionization mass spectrometry of oligonucleotide complexes with drugs, metals, and proteins Mass Spectrom. Rev. 20 2001 61 87
38. V. Gabelica, E. DePauw, and F. Rosu Interaction between antitumor drugs and a double-stranded oligonucleotide studied by electrospray ionization mass spectrometry J. Mass Spectrom. 34 1999 1328 1337
39. F. Rosu, V. Gabelica, C. Houssier, P. Colson, and E. De Pauw Triplex and quadruplex DNA structures studied by electrospray mass spectrometry Rapid Commun. Mass Spectrom. 16 2002 1729 1736
40. J.L. Mergny, A.T. Phan, and L. Lacroix Following G-quartet formation by UV-spectroscopy FEBS Lett. 435 1998 74 78
41. J.S. Ren, and J.B. Chaires Preferential binding of 3,3′- diethyloxadicarbocyanine to triplex DNA J. Am. Chem. Soc. 122 2000 424 425
42. A.T. Phan, and D.J. Patel Two-repeat human telomeric d(TAGGGTTAGGGT) sequence forms interconverting parallel and antiparallel G-quadruplexes in solution: distinct topologies, thermodynamic properties, and folding/unfolding kinetics J. Am. Chem. Soc. 125 2003 15021 15027
43. P. Balagurumoorthy, and S.K. Brahmachari Structure and stability of human telomeric sequence J. Biol. Chem. 269 1994 21858 21869
44. R.T. Wheelhouse, D. Sun, H. Han, F.X. Han, and L.H. Hurley Cationic porphyrins as telomerase inhibitors: the interaction of tetra (N-methyl-4-pyridyl) porphyrin with quadruplex DNA J. Am. Chem. Soc. 120 1998 3261 3262
45. O.Y. Fedoroff, M. Salazar, H. Han, V.V. Chemeris, S.M. Kerwin, and L.H. Hurley NMR-based model of a telomerase inhibiting compound bound to G-quadruplex DNA Biochemistry 37 1998 12367 12374
46. P.J. Perry, M.A. Read, R.T. Davies, S.M. Gowan, A.P. Reszka, A.A. Wood, L.R. Kell, and S. Neidle 2,7-disubstituted amidofluorenone derivatives as inhibitors of human telomerase J. Med. Chem. 42 1999 2679 2684
47. R.J. Harrison, S.M. Gowan, L.R. Kell, and S. Neidle Human telomerase inhibition by substituted acridine derivatives Bioorg. Med. Chem. Lett. 9 1999 2463 2468
48. S. Neidle, R.J. Harrison, A.P. Reszka, and M.A. Read Structure-activity relationships among guanine-quadruplex telomerase inhibitors Pharmacol. Ther. 85 2000 133 139
49. V. Caprio, B. Guyen, Y. Opoku-Boahen, J. Mann, S.M. Gowan, L.M. Kelland, M.A. Read, and S. Neidle A novel inhibitor of human telomerase derived from 10 H-indolo[3,2-b]quinoline Bioorg. Med. Chem. Lett. 10 2000 2063 2066
50. F. Koeppel, J.F. Riou, A. Laoui, P. Mailliet, P.B. Arimondo, D. Labit, O. Petigenet, C. Hélène, and J.L. Mergny Ethidium derivatives bind to G-quartets, inhibit telomerase and act as fluorescent probes for quadruplexes Nucleic Acids Res. 29 2001 1087 1096
51. S. Missailidis, J. Stanslas, C. Modi, M.J. Ellis, R.A. Robins RA, C.A. Laughton, and M.F. Stevens 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. 13 2002 175 189
52. P. Alberti, P. Schmidt, C.H. Nguyen, M. Hoarau, D. Grierson, and J.L. Mergny Benzoindoloquinolines interact with DNA quadruplexes and inhibit telomerase Bioorg. Med. Chem. Lett. 12 2002 1071 7074
53. D.F. Shi, R.T. Wheelhouse, D.Y. Sun, and L.H. Hurley Quadruplex- interactive agents as telomerase inhibitors: synthesis of porphyrins and structure-activity relationship for the inhibition of telomerase J. Med. Chem. 44 2001 4509 4523
54. R.A. Heald, C. Modi, J.C. Cookson, I. Hutchinson, C.A. Laughton, S.M. Gowan, L.R. Kell, and M.F.G. Stevens Antitumor polycyclic acridines. 8. Synthesis and telomerase-inhibitory activity of methylated pentacyclic acridinium salts J. Med. Chem. 45 2002 590 597
55. S.M. Gowan, J.R. Harrison, L. Patterson, M. Valenti, M.A. Read, S. Neidle, and L.R. Kelland A G-quadruplex-interactive potent small-molecule inhibitor of telomerase exhibiting in vitro and in vivo antitumor activity Mol. Pharmacol. 61 2002 1154 1162
56. L. Rossetti, M. Franceschin, A. Bianco, G. Ortaggi, and M. Savino Perylene diimides with different side chains are selective in inducing different G-quadruplex DNA structures and in inhibiting telomerase Bioorg. Med. Chem. Lett. 12 2002 2527 2533
57. M. Read, R.J. Harrison, B. Romagnoli, F.A. Tanious, S.H. Gowan, A.P. Reszka, W.D. Wilson, L.R. Kell, and S. Neidle Structure-based design of selective and potent G quadruplex-mediated telomerase inhibitors Proc. Natl. Acad. Sci. U. S. A. 98 2001 4844 4849
58. A. Maraval, S. Franco, C. Vialas, G. Pratviel, M.A. Blasco, and B. Meunier Porphyrin-aminoquinoline conjugates as telomerase inhibitors Org. Biomol. Chem. 1 2003 921 927
59. R.J. Harrison, J. Cuesta, G. Chessari, M.A. Read, S.K. Basra, A.P. Reszka, J. Morrell, S.M. Gowan, C.M. Incles, F.A. Tanious, W.D. Wilson, L.R. Kell, and S. Neidle Trisubstituted acridine derivatives as potent and selective telomerase inhibitors J. Med. Chem. 46 2003 4463 4476
60. F. Rosu, V. Gabelica, K. Shin-ya, and E. DePauw Telomestatin induced stabilization of the human telomeric DNA quadruplex monitored by electrospray mass spectrometry Chem. Commun. 34 2003 2702 2703
61. T. Lemarteleur, D. Gomez, R. Paterski, E. Mandine, P. Mailliet, and J.-F. Riou Stabilization of the c-myc gene promoter quadruplex by specific ligands inhibitors of telomerase Biochem. Biophys. Res. Commun. 323 2004 802 808
62. D. Gomez, R. Paterski, T. Lemarteleur, K. Shinya, J.L. Mergny, and J.F. Riou Interaction of telomestatin with the telomeric single-strand overhang J. Biol. Chem. 279 2004 41487 41494
63. T. Tauchi, K. Shinya, G. Sashida, M. Sumi, A. Nakajima, T. Shimamoto, J.H. Ohyashiki, and K. Ohyashiki Activity of a novel G-quadruplex-interactive telomerase inhibitor, telomestatin (SOT-095), against human leukemia cells: involvement of ATM-dependent DNA damage response pathways Oncogene 22 2003 5338 5347
64. A. Nakajima, T. Tauchi, G. Sashida, M. Sumi, K. Abe, K. Yamamoto, J.H. Ohyashiki, and K. Ohyashiki Telomerase inhibition enhances apoptosis in human acute leukemia cells: possibility of antitelomerase therapy Leukemia 17 2003 560 567
65. J.F. Riou, L. Guittat, E. Renou, P. Mailliet, A. Laoui, O. Petigenet, C. Hélène, and J.L. Mergny Cell senescence and telomere shortening induced by a new series of specific quadruplex DNA ligands. Proc. Natl. Acad. Sci. U. S. A. 99 2002 2672 2677
66. C. Leonetti, S. Amodei, C. DAngelo, A. Rizzo, B. Benassi, A. Antonelli, R. Elli, M.F.G. Stevens, M. DIncalci, G. Zupi, and A. Biroccio 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
67. E. Gavathiotis, R.A. Heald, M.F.G. Stevens, and M.S. Searle 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