Quadruplex ligands may act as molecular chaperones for tetramolecular quadruplex formation

Nucleic Acids Research

Volumn 35, Issue 8, 2007, Pages 2483-2493

  Cian, Anne De ^a   Mergny, Jean Louis ^a  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDE; CHAPERONE; G QUADRUPLEX; LIGAND; PROTEIN 360A; UNCLASSIFIED DRUG; 2,6 N,N' METHYL QUINOLINIO 3 YL PYRIDINE DICARBOXAMIDE; 2,6-N,N'-METHYL-QUINOLINIO-3-YL-PYRIDINE DICARBOXAMIDE; DNA; PHOSPHATE; PYRIDINE DERIVATIVE; QUADRUPLEX DNA; QUINOLINE DERIVATIVE;

ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; KINETICS; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; CHEMISTRY; CONFORMATION; METABOLISM;

DNA; KINETICS; LIGANDS; MOLECULAR CHAPERONES; NUCLEIC ACID CONFORMATION; PHOSPHATES; PYRIDINES; QUINOLINES;

EID: 34250333423     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkm098     Document Type: Article

References (65)

1. Williamson,J.R. (1994) G-quartet structures in telomeric DNA. Annu. Rev. Biophys. Biomol. Struc., 23, 703-730.
2. Davis J.T. (2004) G-quartets 40 years later: From 5′-GMP to molecular biology and supramolecular chemistry. Angew. Chem. Int. Ed., 43 668-698.
3. Henderson,E., Hardin,C.C., Walk, S.K., Tinoco, I.Jr. and Blackburn,E.H. (1987) Telomeric DNA oligonucleotides form novel intramolecular structures containing guanine-guanine base pairs. Cell, 51, 899-908.
4. Oka,Y. and Thomas,C.A.Jr. (1987) The cohering telomeres of Oxytricha. Nucleic Acids Res., 15, 8877-8898.
5. Sundquist,W.I. and Klug,A. (1989) Telomeric DNA dimerizes by formation of guanine tetrads between hairpin loops. Nature, 342, 825-829.
6. Williamson, J.R., Raghuraman, M.K. and Cech,T.R. (1989) Monovalent cation induced structure of telomeric DNA: The G-quartet model. Cell 59, 871-880.
7. Zahler,A.M., Williamson, J.R., Cech,T.R. and Prescott,D.M. (1991) Inhibition of telomerase by G-quartet DNA structures. Nature, 350, 718-720.
8. 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. USA, 99, 11593-11598.
9. Grand,C.L., Powell,T.J., Nagle,R.B., Bearss,D.J., Tye,D., Gleason-Guzman,M. and Hurley,L.H. (2004) Mutations in the G-quadruplex silencer element and their relationship to c-MYC overexpression, NM23 repression, and therapeutic rescue. Proc. Natl. Acad. Sci. USA, 101, 6140-6145.
10. Schaffitzel,C., Berger,I., Postberg,J., Hanes,J., Lipps,H.J. and Plückthun,A. (2001) In vitro generated antibodies specific for telomeric guanine quadruplex DNA react with Stylonychia lemnae macronuclei. Proc. Natl. Acad. Sci. USA, 98, 8572-8577.
11. Duquette,M.L., Handa,P., Vincent,J.A., Taylor,A.F. and Maizels,N. (2004) Intracellular transcription of G-rich DNAs induces formation of G-loops, novel structures containing G4 DNA. Genes Dev., 18, 1618-1629.
12. Paeschke,K., Simonsson,T., Postberg,J., Rhodes,D. and Lipps,H. (2005) Telomere end-binding proteins control the formation of G-quadruplex DNA structures in vivo. Nat. Struct. Mol. Biol., 12, 847-854.
13. Li,J.J. and Tan,W. (2002) A single DNA molecule nanomotor. nano Lett. 2, 315-318.
14. Alberti,P. and Mergny,J.L. (2003) DNA duplex-quadruplex exchange as the basis for a nanomolecular machine. Proc. Natl. Acad. Sci. USA, 100, 1569-1573.
15. Bourdoncle,A., Estévez Torres,A., Gosse,C., Lacroix,L., Vekhoff,P., Le Saux,T., Jullien,L. and Mergny,J.L. (2006) Quadruplex-based molecular beacons as tunable DNA probes. J. Am. Chem. Soc., 128, 11094-11105.
16. Maizels,N. (2006) Dynamic roles for G4 DNA in the biology of eukaryotic cells. Nature Struct. Mol. Biol., 13, 1055-1059.
17. Oganesian,L. and Bryan,T.M. (2007) Physiological relevance of telomeric G-quadruplex formation: A potential drug target. Bioessays, 29 155-165.
18. Sun,D., Thompson,B., Cathers,B.E., Salazar,M., Kerwin,S.M., Trent,J.O., Jenkins,T.C., Neidle,S. and Hurley,L.H. (1997) Inhibition of human telomerase by a G-quadruplex-interactive compound. J. Med. Chem., 40, 2113-2116.
19. Mergny,J.L. and Hélène,C. (1998) G-quadruplex DNA: A target for drug design. Nature Med., 4, 1366-1367.
20. Guittat,L., Alberti,P., Rosu,F., Van Miert,S., Thetiot,E., Pieters,L., Gabelica,V., De Pauw,E., Ottaviani,A. et al. (2003) Interactions of cryptolepine and neocryptolepine with unusual DNA structures. Biochimie, 85, 535-547.
21. Franceschin,M., Rossetti,L., Dambrosio,A., Schirripa,S., Bianco,A., Ortaggi,G., Savino,M., Schultes,C. and Neidle,S. (2006) Natural and synthetic G-quadruplex interactive berberine derivatives. Bioorg. Medicinal Chem. Lett., 16, 1707-1711.
22. Shin-ya,K., Wierzba,K., Matsuo,K., Ohtani,T., Yamada,Y., Furihata,K., Hayakawa,Y. and Seto,H. (2001) Telomestatin, a novel telomerase inhibitor from Streptomyces anulatus. J. Am. Chem. Soc., 123 1262-1263.
23. 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.
24. Gowan,S., Heald,R., Stevens,M. and Kelland,L. (2001) Potent inhibition of telomerase by small-molecule pentacyclic acridines capable of interacting with G-quadruplexes. Mol. Pharmacol., 60, 981-988.
25. Han, F.X.G., Wheelhouse,R.T. and Hurley,L.H. (1999) Interactions of TMPyP4 and TMPyP2 with quadruplex DNA. Structural basis for the differential effects on telomerase inhibition. J. Am. Chem. Soc., 121, 3561-3570.
26. Pennarun,G., Granotier,C., Gauthier,L.R., Gomez,D., Hoffschir,F., Mandine,E., Riou,J.F., Mergny,J.L., Mailliet,P. et al. (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.
27. De Cian,A., DeLemos,E., Mergny,J.L., Teulade-Fichou,M.P. and Monchaud, D. (2007) Highly efficient G-Quadruplex recognition by bisquinolinium compounds. J. Am. Chem. Soc., 129, 1856-1857.
28. Riou,J.F., Guittat,L., Mailliet,P., Laoui,A., Petigenet,O., Megnin-Chanet,F., Héleène, C. and Mergny,J.L. (2002) Cell senescence and telomere shortening induced by a new series of specific G-quadruplex DNA ligands. Proc. Natl. Acad. Sci. USA, 99, 2672-2677.
29. Han,H.Y., Cliff, C.L. and Hurley,L.H. (1999) Accelerated assembly of G-quadruplex structures by a small molecule. Biochemistry, 38 6981-6986.
30. Kern,J.T. and Kerwin,S.M. (2002) The aggregation and G-quadruplex DNA selectivity of charged 3,4,9,10-perylenetetracarboxylic acid diimides. Bioorg. Med. Chem. Lett., 12, 3395-3398.
31. Harrison,R.J., Cuesta,J., Chessari,G., Read,M.A., Basra,S.K., Reszka,A.P., Morrell,J., Gowan,S.M., Incles,C.M. et al. (2003) Trisubstituted acridine derivatives as potent and selective telomerase inhibitors. J. Med. Chem., 46, 4463-4476.
32. Burger,A.M., Dai,F.P., 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 growih, consistent with telomere targeting and interference with telomerase function. Cancer Res., 65, 1489-1496.
33. Wyatt,J.R., Davis,P.W. and Freier,S.M. (1996) Kinetics of G-quartet-mediated tetramer formation. Biochemistry, 35, 8002-8008.
34. Mergny,J.L., De Cian,A., Ghelab,A., Saccà,B. and Lacroix,L. (2005) Kinetics of tetramolecular quadruplexes. Nucleic Acids Res., 33 81-94.
35. Mergay,J.L., De Cian,A., Amrane,S. and Webba da Silva,M. (2006) Kinetics of double-chain reversals bridging contiguous quartets in tetramolecular quadruplexes. Nucleic Acids Res., 34, 2386-2397.
36. Petraccone,L., Pagano,B., Esposito,V., Randazzo,A., Piccialli,G., Barone,G., Mattia,C.A. and Giancola,C. (2005) Thermodynamics and kinetics of PNA-DNA quadruplex-forming chimeras. J. Am. Chem. Soc. 127, 16215-16223.
37. Petraccone,L., Erra,E., Randazzo,A. and Giancola,C. (2006) Energetic aspects of locked nucleic acids quadruplex association and dissociation. Biopolymers, 83, 584-594.
38. Sen,D. and Gilbert,W. (1988) Formation of parallel four-stranded complexes by guanine-rich motifs in DNA and its applications for meiosis. Nature, 334, 364-366.
39. Sen,D. and Gilbert,W. (1990) A sodium-potassium switch in the formation of four-stranded G4-DNA. Nature, 344, 410-414.
40. Cantor,C.R., Warshaw,M.M. and Shapiro,H. (1970) Oligonucleotide interactions. 3. Circular dichroism studies of the conformation of deoxyoligonucleotides. Biopolymers, 9, 1059-1077.
41. Kejnovska,J., Kypr,J. and Vorlickova,M. (2007) Oligo(dT) is not a correct native PAGE marker for single-stranded DNA. Biochem. Biophys. Res. Commun., 353, 776-779.
42. Mergny,J.L., Phan,A.T. and Lacroix,L. (1998) Following G-quartet formation by UV-spectroscopy. FEBS Lett., 435, 74-78.
43. Petraccone,L., Erra,E., Esposito,V., Randazzo,A., Galeone,A., Barone,G. and Giancola,C. (2005) Biophysical properties of quadruple helices of modified human telomeric DNA. Biopolymers, 77, 75-85.
44. Guo,Q., Lu, M., Marky,L.A. and Kallenbach,N.R. (1992) Interaction of the dye ethidium bromide with DNA containing guanine repeats. Biochemistry, 31, 2451-2455.
45. Koeppel,F., Riou,J.F., Laoui,A., Mailliet,P., Arimondo,P.B., Labit,D., Petigenet,O., Hélène,C. and Mergny,J.L. (2001) Ethidium derivatives bind to G-quartets, inhibit telomerase and act as fluorescent probes for quadruplexes. Nucleic Acids Res., 29, 1087-1096.
46. Rosu,F., Pauw,E.D., Guittat,L., Alberti,P., Lacroix,L., Mailliet,P., Riou,J.-F. and Mergny,J.-L. (2003) Selective interaction of ethidium derivatives with quadruplexes. Biochemistry, 42, 10361-10371.
47. Lemarteleur,T., Gomez,D., Paterski,R., Mandine,E., Maitliet,P. and Riou,J.-F. (2004) Stabilization of the c-myc gene promoter quadruplex by specific ligands inhibitors of telomerase. Biochem. Biophys. Res. Com., 323, 802-808.
48. Granotier,C., Pennarun,G., Riou,L., Hoffschir,F., Gauthier,L.R., DeCian,A., Gomez,D., Mandine,E., Riou,J.F. et al. (2005) Preferential binding of a G-quadruplex ligand to human chromosome ends. Nucl Acid Res., 33, 4182-4190.
49. Uddin,M.K., Kato,Y., Takagi,Y., Mikuma,T. and Taira,K. (2004) Phosphorylation at 5′ end of guanosine stretches inhibits dimerization of G-quadruplexes and formation of a G-quadruplex interferes with the enzymatic activities of DNA enzymes. Nucleic Acids Res., 32, 4618-4629.
50. Wheelhouse,R.T., Sun,D., Han,H., Han,F.X. and Hurley,L.H. (1998) Cationic porphyrins as telomerase inhibitors: The interaction of tetra (N-methyl-4-pyridyl) porphyrin with quadruplex DNA. J. Am. Chem. Soc. 120, 3261-3262.
51. Fedoroff,O.Y., Salazar,M., Han,H., Chemeris,V.V., Kerwin,S.M. and Hurley,L.H. (1998) NMR-based model of a telomerase inhibiting compound bound to G-quadruplex DNA. Biochemistry, 37, 12367-12374.
52. Perry,P.J., Read,M.A., Davies,R.T., Gowan,S.M., Reszka,A.P., Wood,A.A., Kelland,L.R. and Neidle,S. (1999) 2,7-disubstituted amidofluorenone derivatives as inhibitors of human telomerase. J. Med. Chem., 42, 2679-2684.
53. Harrison,R.J., Gowan,S.M., Kelland,L.R. and Neidle,S. (1999) Human telomerase inhibition by substituted acridine derivatives. Bioorg. Med. Chem. Lett., 9, 2463-2468.
54. Neidle,S., Harrison,R.J., Reszka,A.P. and Read,M.A. (2000) Structure-activity relationships among guanine-quadruplex telomerase inhibitors. Pharmacol. Ther., 85, 133-139.
55. Caprio,V., Guyen,B., Opoku-Boahen,Y., Mann,J., Gowan,S.M., Kelland,L.M., Read,M.A. and Neidle,S. (2000) A novel inhibitor of human telomerase derived from 10H-indolo[3,2-b]quinoline. Bioorg. Med. Chem. Lett., 10, 2063-2066.
56. Mergny,J.L., Lacroix,L., Teulade-Fichou,M.P., Hounsou,C., Guittat,L., Hoarau,M., Arimondo,P.B., Vigneron,J.P., Lehn,J.M. et al. (2001) Telomerase inhibitors based on quadruplex ligands selected by a fluorescent assay. Proc. Natl. Acad. Sci. USA, 98, 3062-3067.
57. Alberti,P., Schmidt,P., Nguyen,C.H., Hoarau,M., Grierson,D. and Mergny,J.L. (2002) Benzoindoloquinolines interact with DNA quadruplexes and inhibit telomerase. Bioorg. Med. Chem. Lett., 12, 1071-7074.
58. Shi,D.F., Wheelhouse,R.T., Sun,D.Y. and Hurley,L.H. (2001) Quadruplex-interactive agents as telomerase inhibitors: Synthesis of porphyrins and structure-activity relationship for the inhibition of telomerase. J. Med. Chem., 44, 4509-4523.
59. Heald,R.A., Modi,C., Cookson,J.C., Hutchinson,I., Laughton,C.A., Gowan,S.M., Kelland,L.R. and Stevens,M.F.G. (2002) Antitumor polycyclic acridines. 8. Synthesis and telomerase-inhibitory activity of methylated pentacyclic acridinium salts. J. Med. Chem., 45, 590-597.
60. Gowan,S.M., Harrison,J.R., Patterson,L., Valenti,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.
61. Rossetti,L., Franceschin,M., Bianco,A., Ortaggi,G. and Savino,M. (2002) Perylene diimides with different side chains are selective in inducing different G-quadruplex DNA structures and in inhibiting telomerase. Bioorg. Med. Chem. Lett., 12, 2527-2533.
62. Read,M., 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. USA, 98, 4844-4849.
63. Maraval,A., Franco,S., Vialas,C., Pratviel,G., Blasco,M.A. and Meunier,B. (2003) Porphyrin-aminoquinoline conjugates as telomerase inhibitors. Org. Biomol. Chem., 1, 921-927.
64. Rosu,F., Gabelica,V., Shin-ya,K. and DePauw,E. (2003) Telomestatin induced stabilization of the human telomeric DNA quadruplex monitored by electrospray mass spectrometry. Chem. Commun., 34, 2702-2703.
65. Green,J.J., Ladame,S., Ying,L., Klenerman,D. and Balasubramanian,S. (2006) Investigating a quadruplex-ligand interaction by unfolding kinetics. J. Am. Chem. Soc., 128, 9809-9812.