G-quadruplex; thiazole orange; fluorescence; noncovalent; mass spectrometry; DNA
Abstract :
[en] We report here the details of G4-FID (G-quadruplex fluorescent intercalator displacement), a simple method aiming at evaluating quadruplex DNA binding affinity and quadruplex- over duplex-DNA selectivity of putative ligands. This assay is based on the loss of fluorescence upon displacement of thiazole orange from quadruplex and duplex-DNA matrices. The original protocol was tested using various quadruplex and
duplex-DNA targets, and with a wide panel of G-quadruplex ligands belonging to different families (i.e. from quinacridines to metalloorganic ligands) likely to display various binding modes. The reliability of the assay is further supported by comparisons with FRET-melting and ESI-MS assays.
Research Center/Unit :
Giga-Systems Biology and Chemical Biology - ULiège
Monchaud, David; Institut Curie, Section Recherche, CNRS UMR176, Centre Universitaire Paris XI, Bat. 110, 91405 Orsay, France
Allain, C.; Institut Curie, Section Recherche, CNRS UMR176, Centre Universitaire Paris XI, Bat. 110, 91405 Orsay, France
Bertrand, Hélène; Institut Curie, Section Recherche, CNRS UMR176, Centre Universitaire Paris XI, Bat. 110, 91405 Orsay, France
Smargiasso, Nicolas ; Université de Liège - ULiège > Département de chimie (sciences) > Chimie physique, spectrométrie de masse
Rosu, Frédéric ; Université de Liège - ULiège > Département de chimie (sciences) > Chimie physique, spectrométrie de masse
Gabelica, Valérie ; Université de Liège - ULiège > Département de chimie (sciences) > Chimie physique, spectrométrie de masse
De Cian, Anne; INSERM, U565, Acides Nucle´iques: Dynamique, Ciblage et Fonctions Biologiques, Muse´um National d’histoire Naturelle USM 503, 43, Rue Cuvier, 75005 Paris, France
Mergny, Jean-Louis; INSERM, U565, Acides Nucléques: Dynamique, Ciblage et Fonctions Biologiques, Musém National d’histoire Naturelle USM 503, 43, Rue Cuvier, 75005 Paris, France
Teulade-Fichou, Marie-Paule; Institut Curie, Section Recherche, CNRS UMR176, Centre Universitaire Paris XI, Bat. 110, 91405 Orsay, France
Language :
English
Title :
Ligands playing musical chairs with G-quadruplex DNA: A rapid and simple displacement assay for identifying selective G-quadruplex binders
Publication date :
2008
Journal title :
Biochimie
ISSN :
0300-9084
eISSN :
1638-6183
Publisher :
Elsevier, Paris, France
Special issue title :
Special issue: Targeting DNA, part II
Volume :
90
Issue :
8
Pages :
1207-1223
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique FRIA - Fonds pour la Formation à la Recherche dans l'Industrie et dans l'Agriculture
Commentary :
The final version of this article has been published by Elsevier as: D. Monchaud, C. Allain, H. Bertrand, N. Smargiasso, F. Rosu, V. Gabelica, A. De Cian, J.-L. Mergny, and M.-P. Teulade-Fichou, "Ligands playing musical chairs with G-quadruplex DNA: A rapid and simple displacement assay for identifying selective G-quadruplex binders", Biochimie (2008), 90(8), Special issue "Targeting DNA Part II", 1207-1223
Neidle S., and Balasubramanian S. Quadruplex Nucleic Acid (2006), RSC Publishing, Cambridge 301
Patel D.J., Phan A.T., and Kuryavyi V. Human telomere, oncogenic promoter and 5′-UTR G-quadruplexes: diverse higher order DNA and RNA targets for cancer therapeutics. Nucleic Acids Res. 35 (2007) 7429-7455
Pagano B., and Giancola C. Energetics of quadruplex-drug recognition in anticancer therapy. Current Cancer Drug Targets 7 (2007) 520-540
Davis J.T. G-quartets 40 years later: from 5′-GMP to molecular biology and supramolecular chemistry. Angew. Chem. Int. Ed. 43 (2004) 668-698
Monchaud D., and Teulade-Fichou M.-P. A hitchhiker's guide to G-quadruplex ligands. Org. Biomol. Chem. 6 (2008) 627-636
Hurley L.H. DNA and its associated processes as targets for cancer therapy. Nature Reviews Cancer 2 (2002) 188-200
Neidle S., and Parkinson G. Telomere maintenance as a target for anticancer drug discovery. Nature Reviews Drug Discovery 1 (2002) 383-393
Mergny J.-L., Riou J.-F., Mailliet P., Teulade-Fichou M.-P., and Gilson E. Natural and Pharmacological regulation of telomerase. Nucleic Acids Res. 30 (2002) 839-865
Rezler E.M., Bearss D.J., and Hurley L.H. Telomere inhibition and telomere disruption as processes for drug targeting. Annu. Rev. Pharmacol. Toxicol. 43 (2003) 359-379
Neidle S., and Thurston D.E. Chemical approaches to the discovery and development of cancer therapies. Nature Reviews Cancer 5 (2005) 285-296
Oganesian L., and Bryan T.M. Physiological relevance of telomeric G-quadruplex formation: a potential drug target. BioEssays 29 (2007) 155-165
Maizels N. Dynamic roles for G4 DNA in the biology of eukaryotic cells. Nat. Struct. Biol. 13 (2006) 1055-1059
Fry M. Tetraplex DNA and its interacting proteins. Front. Biosci. 12 (2007) 4336-4351
Kelland L. Targeting the limitless replicative potential of cancer: the telomerase/telomere pathway. Clin. Cancer Res. 13 (2007) 4960-4963
De Cian A., Lacroix L., Douarre C., Temine-Smaali N., Trentesaux C., Riou J.-F., and Mergny J.-L. Targeting telomeres and telomerase. Biochimie 90 (2008) 131-155
Mergny J.-L., and Maurizot J.-C. Fluorescence resonance energy transfer as a probe for G-quartet formation by a telomeric repeat. ChemBioChem 2 (2001) 124-132
De Cian A., Guittat L., Kaiser M., Saccà B., Amrane S., Bourdoncle A., Alberti P., Teulade-Fichou M.-P., Lacroix L., and Mergny J.-L. Fluorescence-based melting assays for studying quadruplex ligands. Methods 42 (2007) 183-195
White E.W., Tanious F., Ismail M.A., Reszka A.P., Neidle S., Boykin D.W., and Wilson W.D. Structure-specific recognition of quadruplex DNA by organic cations: influence of shape, substituents and charge. Biophys. Chem. 126 (2007) 140-153
Nguyen B., Tanious F.A., and Wilson W.D. Biosensor-surface plasmon resonance: quantitative analysis of small molecule-nucleic acid interactions. Methods 42 (2007) 150-161
Redman J.E. Surface plasmon resonance for probing quadruplex folding and interactions with proteins and small molecules. Methods 43 (2007) 302-312
Gabelica V., Baker E.S., Teulade-Fichou M.-P., De Pauw E., and Bowers M.T. Stabilization and structure of telomeric and c-myc region intramolecular G-quadruplexes: the role of central cations and small planar ligands. J. Am. Chem. Soc. 129 (2007) 895-904
Guittat L., De Cian A., Rosu F., Gabelica V., De Pauw E., Delfourne E., and Mergny J.-L. Ascididemin and meridine stabilise G-quadruplexes and inhibit telomerase in vivo. Biochim. Biophys. Acta 1724 (2005) 375-384
Rosu F., Gabelica V., Shin-ya K., and De Pauw E. Telomestatin-induced stabilization of the human telomeric DNA quadruplex monitored by electrospray mass spectrometry. Chem. Commun. (2003) 2702-2703
Carrasco C., Rosu F., Gabelica V., Houssier C., De Pauw E., Garbay-Jaureguiderty C., Roques B., Wilson W.D., Chaires J.B., Waring M.J., and Bailly C. The binding of the antitumor drug ditercalinium to quadruplex DNA. ChemBioChem 3 (2002) 1235-1241
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., and Hélène C. Telomerase inhibitors based on quadruplex ligands selected by a fluorescence assay. Proc. Natl. Acad. Sci. USA 98 (2001) 3062-3067
Teulade-Fichou M.-P., Carrasco C., Guittat L., Bailly C., Alberti P., Mergny J.-L., David A., Lehn J.-M., and Wilson W.D. Selective recognition of G-quadruplex telomeric DNA by a bis(quinacridine) macrocycle. J. Am. Chem. Soc. 125 (2003) 4732-4740
Ren J., and Chaires J.B. Sequence and structural selectivity of nucleic acid binding ligands. Biochemistry 38 (1999) 16067-16075
Ragazzon P.A., Garbett N.C., and Chaires J.B. Competition dialysis: a method for the study of structural selective nucleic acid binding. Methods 42 (2007) 173-182
Ragazzon P.A., and Chaires J.B. Use of competition dialysis in the discovery of G-quadruplex selective ligands. Methods 43 (2007) 313-323
Yao Y., Wang Q., Hao Y.-H., and Tan Z. An exonuclease I hydrolysis assay for evaluating G-quadruplex stabilization by small molecules. Nucleic Acids Res. 35 (2007) e68
Monchaud D., Allain C., and Teulade-Fichou M.-P. Development of a fluorescent intercalator displacement assay (G4-FID) for establishing quadruplex-DNA affinity and selectivity of putative ligands. Bioorg. Med. Chem. Lett. 16 (2006) 4842-4845
Burge S., Parkinson G.N., Hazel P., Todd A.K., and Neidle S. Quadruplex DNA: sequence, topology and structure. Nucleic Acid Res. 34 (2006) 5402-5415
Phan A.T., Kuryavyi V., and Patel D.J. DNA architecture: from G to Z. Curr. Opin. Struct. Biol. 16 (2006) 288-298
Macaya R.F., Schultze P., Smith F.W., Roe J.A., and Feigon J. Thrombin-binding DNA aptamer forms a unimolecular quadruplex structure in solution. Proc. Natl. Acad. Sci. USA 90 (1993) 3745-3749
Marathias V.M., and Bolton P.H. Structure of the potassium-saturated, 2:1, and intermediate, 1:1, forms of a quadruplex DNA. Nucleic Acids Res. 28 (2000) 1969-1977
Nygren J., Svanvik N., and Kubista M. The interactions between the fluorescent dye thiazole orange and DNA. Biopolymers 46 (1998) 39-51
Boger D.L., Fink B.E., Brunette S.R., Tse W.C., and Hedrick M.P. A simple, high-resolution method for establishing DNA binding affinity and sequence selectivity. J. Am. Chem. Soc. 123 (2001) 5878-5891
Rosu F., Gabelica V., Houssier C., and De Pauw E. Determination of affinity, stoichiometry and sequence selectivity of minor groove binder complexes with double-stranded oligodeoxynucleotides by electrospray ionization mass spectrometry. Nucleic Acids Res. 30 (2002) e82
Hounsou C., Guittat L., Monchaud D., Jourdan M., Saettel N., Mergny J.-L., and Teulade-Fichou M.-P. G-quadruplex recognition by quinacridines: a SAR, NMR and biological study. ChemMedChem 2 (2007) 655-666
Allain C., Monchaud D., and Teulade-Fichou M.-P. FRET templated by G-quadruplex DNA: a specific ternary interaction using an original pair of donor/acceptor partners. J. Am. Chem. Soc. 128 (2006) 11890-11893
Lemarteleur T., Gomez D., Paterski R., Mandine E., Mailliet P., and Riou J.-F. Stabilization of the c-myc gene promoter quadruplex by specific ligands' inhibitors of telomerase. Biochem. Biophys. Res. Commun. 323 (2004) 802-808
Pennarun G., Granotier C., Gauthier L.R., Gomez D., Hoffschir F., Mandine E., Riou J.-F., Mergny J.-L., Mailliet P., and Boussin F.D. Apoptosis related to telomere instability and cell cycle alterations in human glioma cells treated by new highly selective G-quadruplex ligands. Oncogene 24 (2005) 2917-2928
Granotier C., Pennarun G., Riou L., Hoffshir F., Gauthier L.R., De Cian A., Gomez D., Mandine E., Riou J.-F., Mergny J.-L., Mailliet P., Dutrillaux B., and Boussin F.D. Preferential binding of a G-quadruplex ligand to human chromosomes ends. Nucleic Acids Res. 33 (2005) 4182-4190
De Cian A., and Mergny J.-L. Quadruplex ligands may act as molecular chaperones for tetramolecular quadruplex formation. Nucleic Acids Res. 35 (2007) 2483-2493
De Cian A., DeLemos E., Mergny J.-L., Teulade-Fichou M.-P., and Monchaud D. Highly efficient G-quadruplex recognition by bisquinolinium compounds. J. Am. Chem. Soc. 129 (2007) 1856-1857
De Cian A., Cristofari G., Reichenbach P., De Lemos E., Monchaud D., Teulade-Fichou M.-P., Shin-ya K., Lacroix L., Lingner J., and Mergny J.-L. Reevaluation of telomerase inhibition by quadruplex ligands and their mechanisms of action. Proc. Natl. Acad. Sci. USA 104 (2007) 17347-17352
Bertrand H., Monchaud D., De Cian A., Guillot R., Mergny J.-L., and Teulade-Fichou M.-P. The importance of the metal geometry in the recognition of G-quadruplex-DNA by metal-terpyridine complexes. Org. Biomol. Chem. 5 (2007) 2555-2559
Vialas C., Pratviel G., and Meunier B. Oxidative damage generated by an oxo-metalloporphyrin onto the human telomeric sequence. Biochemistry 39 (2000) 9514-9522
Shi D.-F., Wheelhouse R.T., Sun D., and Hurley L.H. 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
Tuntiwechapikul W., Lee J.T., and Salazar M. Design and synthesis of the G-quadruplex-specific cleaving reagent perylene-EDTA.iron(II). J. Am. Chem. Soc. 123 (2001) 5606-5607
Maraval A., Franco S., Vialas C., Pratviel G., Blasco M.A., and Meunier B. Porphyrin-aminoquinoline conjugates as telomerase inhibitors. Org. Biomol. Chem. 1 (2003) 921-927
Keating L.R., and Szalai V.A. Parallel-stranded guanine quadruplex interactions with a copper cationic porphyrin. Biochemistry 43 (2004) 15891-15900
Evans S.E., Mendez M.A., Turner K.B., Keating L.R., Grimes R.T., Melchior S., and Szalai V.A. End-stacking of copper cationic porphyrins on parallel-stranded guanine quadruplexes. J. Biol. Inorg. Chem. 12 (2007) 1235-1249
Sato S., Kondo H., Nojima T., and Takenaka S. Electrochemical telomerase assay with ferrocenylnaphthalene diimide as a tetraplex DNA-specific binder. Anal. Chem. 77 (2005) 7304-7309
Dixon I.M., Lopez F., Estève J.-P., Tejera A.M., Blasco M.A., Pratviel G., and Meunier B. Porphyrin derivatives for telomere binding and telomerase inhibition. ChemBioChem 6 (2005) 123-132
Reed J.E., Arnal A.A., Neidle S., and Vilar R. Stabilization of G-quadruplex DNA and inhibition of telomerase activity by square-planar nickel(II) complexes. J. Am. Chem. Soc. 128 (2006) 5992-5993
Gonçalves D.P.N., Rodriguez R., Balasubramanian S., and Sanders J.K.M. Tetramethylpyridinium porphyrazines-a new class of G-quadruplex inducing and stabilising ligands. Chem. Commun. (2006) 4685-4687
Ohyama T., Kato Y., Mita H., and Yamamoto Y. Exogenous ligand binding property of a heme-DNA coordination complex. Chem. Lett. 35 (2006) 126-127
Rajput C., Rutkaite R., Swanson L., Haq I., and Thomas J.A. Dinuclear monointercalating RuII complexes that display high affinity binding to duplex and quadruplex DNA. Chem. Eur. J. 12 (2006) 4611-4619
Dixon I.M., Lopez F., Tejera A.M., Estève J.-P., Blasco M.A., Pratviel G., and Meunier B. A G-quadruplex ligand with 10000-fold selectivity over duplex DNA. J. Am. Chem. Soc. 129 (2007) 1502-1503
Ren L., Zhang A., Huang J., Wang P., Weng X., Zhang L., Liang F., Tan Z., and Zhou X. Quaternary ammonium zinc phthalocyanine: inhibiting telomerase by stabilizing G quadruplexes and inducing G-quadruplex structure transition and formation. ChemBioChem 8 (2007) 775-780
Reed J.E., Neidle S., and Vilar R. Stabilisation of human telomeric quadruplex DNA and inhibition of telomerase by a platinum-phenanthroline complex. Chem. Commun. (2007) 4366-4368
Bertrand H., Bombard S., Monchaud D., and Teulade-Fichou M.-P. A platinum-quinacridine hybrid as a G-quadruplex ligand. J. Biol. Inorg. Chem. 12 (2007) 1003-1014
Kieltyka R., Fakhoury J., Moitessier N., and Sleiman M.F. Platinum phenanthroimidazole complexes as G-quadruplex DNA selective binders. Chem. Eur. J. 14 (2008) 1145-1154
Fialova M., Kypr J., and Vorlickova M. The thrombin binding aptamer GGTTGGTGTGGTTGG forms a bimolecular guanine tetraplex. Biochem. Biophys. Res. Commun. 344 (2006) 50-54
Wang Y., and Patel D.J. Solution structure of the human telomeric repeat d[AG3(T2AG3)3] G-tetraplex. Structure 1 (1993) 263-282
Ambrus A., Chen D., Dai J., Bialis T., Jones R.A., and Yang D. Human telomeric sequence forms a hybrid-type intramolecular G-quadruplex structure with mixed parallel/anti-parallel strands in potassium solution. Nucleic Acids Res. 34 (2006) 2723-2735
Dai J., Punchilhewa C., Ambrus A., Chen D., Jones R.A., and Yang D. Structure of the intramolecular human telomeric G-quadruplex in potassium solution: a novel adenine triple formation. Nucleic Acids Res. 35 (2007) 2440-2450
Dai J., Carver M., Punchilhewa C., Jones R.A., and Yang D. Structure of the hybrid-2 type intramolecular human telomeric G-quadruplex in K+ solution: insights into structure polymorphism of the human telomeric sequence. Nucleic Acids Res. 35 (2007) 4927-4940
Phan A.T., Kuryavyi V., Luu K.N., and Patel D.J. Structure of two intramolecular G-quadruplexes formed by natural human telomere sequences in K+ solution. Nucleic Acids Res. 35 (2007) 6517-6525