Multiple and cooperative binding of fluorescence light-up probe thioflavin t with human telomere DNA G-quadruplex

Cooperative binding; Dissociation constant; Electrospray ionization mass spectrometry; Fluorescence titrations; Fluorescent probes; G-quadruplex structure; Human telomere DNA; Telomeric sequences; Biochemistry; Dissociation; Fluorescence; Ligands; Mass spectrometry; Probes; DNA sequences; DNA; DNA sequence; Algorithms; Binding Sites; Circular Dichroism; Fluorescent Dyes; G-Quadruplexes; Humans; Kinetics; Models, Molecular; Molecular Structure; Spectrometry, Mass, Electrospray Ionization; Telomere; Thiazoles

Abstract :

[en] Thioflavin T (ThT), a typical probe for protein fibrils, also binds human telomeric G-quadruplexes with a fluorescent light-up signal change and high specificity against DNA duplexes. Cell penetration and low cytotoxicity of fibril probes having been widely established, modifying ThT and other fibril probes is an attractive means of generating new G-quadruplex ligands. Thus, elucidating the binding mechanism is important for the design of new drugs and fluorescent probes based on ThT. Here, we investigated the binding mechanism of ThT with several variants of the human telomeric sequence in the presence of monovalent cations. Fluorescence titrations and electrospray ionization mass spectrometry (ESI-MS) analyses demonstrated that each G-quadruplex unit cooperatively binds to several ThT molecules. ThT brightly fluoresces when a single ligand is bound to the G-quadruplex and is quenched as ligand binding stoichiometry increases. Both the light-up signal and the dissociation constants are exquisitely sensitive to the base sequence and to the G-quadruplex structure. These results are crucial for the sensible design and interpretation of G-quadruplex detection assays using fluorescent ligands in general and ThT in particular. © 2013 American Chemical Society.

Disciplines :

Chemistry

Author, co-author :

Gabelica, Valerie ; Université de Liège - ULiège

Maeda, R.; Faculty of Frontiers of Innovative Research in Science and Technology (FIRST), Japan

Fujimoto, T.; Faculty of Frontiers of Innovative Research in Science and Technology (FIRST), Japan

Yaku, H.; Faculty of Frontiers of Innovative Research in Science and Technology (FIRST), Japan, Frontier Institute for Biomolecular Engineering Research (FIBER), Konan University, 7-1-20 minatojima-minamimachi, Chuo-ku, Kobe 650-0047, Japan, Advanced Technology Research Laboratories, Panasonic Corporation, 3-4 Hikaridai, Seika-cho, Soraku-gun, Kyoto 619-0237, Japan

Murashima, T.; Faculty of Frontiers of Innovative Research in Science and Technology (FIRST), Japan, Frontier Institute for Biomolecular Engineering Research (FIBER), Konan University, 7-1-20 minatojima-minamimachi, Chuo-ku, Kobe 650-0047, Japan

Sugimoto, N.; Faculty of Frontiers of Innovative Research in Science and Technology (FIRST), Japan, Frontier Institute for Biomolecular Engineering Research (FIBER), Konan University, 7-1-20 minatojima-minamimachi, Chuo-ku, Kobe 650-0047, Japan

Miyoshi, D.; Faculty of Frontiers of Innovative Research in Science and Technology (FIRST), Japan, Frontier Institute for Biomolecular Engineering Research (FIBER), Konan University, 7-1-20 minatojima-minamimachi, Chuo-ku, Kobe 650-0047, Japan

Title :

Multiple and cooperative binding of fluorescence light-up probe thioflavin t with human telomere DNA G-quadruplex

Publication date :

2013

Journal title :

Biochemistry

ISSN :

0006-2960

eISSN :

1520-4995

Publisher :

American Chemical Society, Washington, United States - District of Columbia

Volume :

Issue :

Pages :

5620-5628

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 28 October 2016

Statistics

Number of views

127 (4 by ULiège)

Number of downloads

309 (1 by ULiège)

More statistics

Scopus citations^®

102

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

104

Bibliography

Cer, R. Z., Bruce, K. H., Mudunuri, U. S., Yi, M., Volfovsky, N., Luke, B. T., Bacolla, A., Collins, J. R., and Stephens, R. M. (2011) Non-B DB: a database of predicted non-B DNA-forming motifs in mammalian genomes Nucleic Acids Res. 39, D383-D391
Gellert, M., Lipsett, M. N., and Davies, D. R. (1962) Helix formation by guanylic acid Proc. Natl. Acad. Sci. U.S.A. 48, 2013-2018
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
Phan, A. T., Kuryavyi, V., Luu, K. N., and Patel, D. J. (2007) Structure of two intramolecular G-quadruplexes formed by natural human telomere sequences in K+ solution Nucleic Acids Res. 35, 6517-6525
Greider, C. W. and Blackburn, E. H. (1985) Identification of a specific telomere terminal transferase activity in Tetrahymena extracts Cell 43, 405-413
Moyzis, R. K., Buckingham, J. M., Cram, L. S., Dani, M., Deaven, L. L., Jones, M. D., Meyne, J., Ratliff, R. L., and Wu, J.-R. (1988) A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes Proc. Natl. Acad. Sci. U.S.A. 85, 6622-6626
Huppert, J. L. and Balasubramanian, S. (2007) G-quadruplexes in promoters throughout the human genome Nucleic Acids Res. 35, 406-413
Todd, A. K., Johnston, M., and Neidle, S. (2005) Highly prevalent putative quadruplex sequence motifs in human DNA Nucleic Acids Res. 33, 2901-2907
Eddy, J. and Maizels., N. (2006) Gene function correlates with potential for G4 DNA formation in the human genome Nucleic Acids Res. 34, 3887-3896
Balasubramanian, S., Hurley, L. H., and Neidle, S. (2011) Targeting G-quadruplexes in gene promoters: a novel anticancer strategy? Nat. Rev. Drug Discovery 10, 261-275
Dixon, I. M., Lopez, F., Tejera, A. M., Estève, J. P., Blasco, M. A., Pratviel, G., and Meunier, B. (2007) A G-quadruplex ligand with 10000-fold selectivity over duplex DNA J. Am. Chem. Soc. 129, 1502-1503
Yaku, H., Murashima, T., Miyoshi, D., and Sugimoto, N. (2010) Anionic phthalocyanines targeting G-quadruplexes and inhibiting telomerase activity in the presence of excessive DNA duplexes Chem. Commun. 46, 5740-5742
Haudecoeur, R., Stefan, L., Denat, F., and Monchaud, D. (2013) A model of smart g-quadruplex ligand J. Am. Chem. Soc. 135, 550-553
Biffi, G., Tannahill, D., McCafferty., J., and Balasubramanian, S. (2013) Quantitative visualization of DNA G-quadruplex structures in human cells Nat. Chem. 5, 182-186
Largy, E., Granzhan, A., Hamon, F., Verga, D., and Teulade-Fichou, M. P. (2013) Visualizing the quadruplex: From fluorescent ligands to light-up probes Top. Curr. Chem. 330, 111-177
Bhasikuttan, A. C., Mohanty, J., and Pal, H. (2007) Interaction of malachite green with guanine-rich single-stranded DNA: Preferential binding to a G-quadruplex Angew. Chem., Int. Ed. 46, 9305-9307
Iida, K., Tera, M., Hirokawa, T., Shin-ya, K., and Nagasawa, K. (2009) G-quadruplex recognition by macrocyclic hexaoxazole (6OTD) dimer: Greater selectivity than monomer Chem. Commun. 6481-6483
Meguellati, K., Koripelly, G., and Ladame, S. (2010) DNA-templated synthesis of trimethine cyanine dyes: a versatile fluorogenic reaction for sensing G-quadruplex formation Angew. Chem., Int. Ed. 49, 2738-2742
Tran, P. L., Largy, E., Hamon, F., Teulade-Fichou, M. P., and Mergny, J. L. (2011) Fluorescence intercalator displacement assay for screening G4 ligands towards a variety of G-quadruplex structures Biochimie 93, 1288-1296
Nikan, M., Di Antonio, M., Abecassis, K., McLuckie, K., and Balasubramanian, S. (2013) An acetylene-bridged 6,8-purine dimer as a fluorescent switch-on probe for parallel G-quadruplexes Angew. Chem., Int. Ed. 52, 1428-1431
Vummidi, B. R., Alzeer, J., and Luedtke, N. W. (2013) Fluorescent probes for g-quadruplex structures ChemBioChem 14, 540-558
Mohanty, J., Barooah, N., Dhamodharan, V., Harikrishna, S., Pradeepkumar, P. I., and Bhasikuttan, A. C. (2013) Thioflavin T as an efficient inducer and selective fluorescent sensor for the human telomeric G-quadruplex DNA J. Am. Chem. Soc. 135, 367-376
Richard, E. G., Ed. (1975) Handbook of Biochemistry and Molecular Biology, CRC Press, Cleveland, OH.
Groenning, M. (2010) Binding mode of Thioflavin T and other molecular probes in the context of amyloid fibrils-current status J. Chem. Biol. 3, 1-18
Risitano., A. and Fox, K. R. (2004) Influence of loop size on the stability of intramolecular DNA quadruplexes Nucleic Acids Res. 32, 2598-2606
Lim, K. W., Amrane, S., Bouaziz, S., Xu, W., Mu, Y., Patel, D. J., Luu, K. N., and Phan, A. T. (2009) Structure of the Human Telomere in K+ Solution: A Stable Basket-Type G-Quadruplex with Only Two G-Tetrad Layers J. Am. Chem. Soc. 131, 4301-4309
Gabelica, V., Rosu, F., and De Pauw, E. (2009) A simple method to determine electrospray response factors of noncovalent complexes Anal. Chem. 81, 6708-6715
Kuzmic, P. (1996) Program DYNAFIT for the analysis of enzyme kinetic data: Application to HIV proteinase Anal. Biochem. 237, 260-273
Jan, A., Gokce, O., Luthi-Carter, R., and Lashuel, H. A. (2008) The ratio of monomeric to aggregated forms of Abeta40 and Abeta42 is an important determinant of amyloid-beta aggregation, fibrillogenesis, and toxicity J. Biol. Chem. 283, 28176-28189
Maskevich, A. A., Stsiapura, V. I., Kuzmitsky, V. A., Kuznetsova, I. M., Povarova, O. I., Uversky, V. N., and Turoverov, K. K. (2007) Spectral properties of thioflavin T in solvents with different dielectric properties and in a fibril-incorporated form J. Proteome Res. 6, 1392-1401
Sulatskaya, A. I., Kuznetsova, I. M., and Turoverov, K. K. (2012) Interaction of thioflavin T with amyloid fibrils: fluorescence quantum yield of bound dye J. Phys Chem B 116, 2538-2544
Ambrus, A., Chen, D., Dai, J., Bialis, T., Jones, R. A., and Yang, D. (2006) Human telomeric sequence forms a hybrid-type intramolecular G-quadruplex structure with mixed parallel/antiparallel strands in potassium solution Nucleic Acids Res. 34, 2723-2735
Miyoshi, D., Inoue, M., and Sugimoto, N. (2006) DNA logic gates based on structural polymorphism of telomere DNA molecules responding to chemical input signals Angew. Chem., Int. Ed. 45, 7716-7719
Wang, Y. and Patel, D. J. (1993) Solution structure of the human telomeric repeat d[AG3(T2AG3)3] G-tetraplex Structure 1, 263-282
Lombardo, C. M., Martínez, I. S., Haider, S., Gabelica, V., De Pauw, E., Moses, J. E., and Neidle, S. (2010) Structure-based design of selective high-affinity telomeric quadruplex-binding ligands Chem. Commun. 46, 9116-9118
Gabelica, V. (2010) Determination of equilibrium association constants of ligand-DNA complexes by electrospray mass spectrometry Methods Mol. Biol. 613, 89-101
Rosu, F., Gabelica, V., De Pauw, E., Mailliet, P., and Mergny, J. L. (2008) Cooperative 2:1 binding of a bisphenothiazine to duplex DNA ChemBioChem 9, 849-852
Yu, H.-Q., Miyoshi, D., and Sugimoto, N. (2006) Characterization of structure and stability of long telomeric DNA G-quadruplexes J. Am. Chem. Soc. 128, 15461-15468
Petraccone, L., Spink, C., Trent, J. O., Garbett, N. C., Mekmaysy, C. S., Giancola, C., and Chaires, J. B. (2011) Structure and stability of higher-order human telomeric quadruplexes J. Am. Chem. Soc. 133, 20951-20961
Yu, H.-Q., Gu, X., Nakano, S., Miyoshi, D., and Sugimoto, N. (2012) Beads-on-a-string structure of long telomeric DNAs under molecular crowding conditions J. Am. Chem. Soc. 134, 20060-20069
Canter, C. R. and Schimmel, P. R. (1980) Biophysical Chemistry: Part III: The Behavior of Biological Macromolecules, W. H. Freeman and Company, New York.
Lockhart, A., Ye, L., Judd, D. B., Merritt, A. T., Lowe, P. N., Morgenstern, J. L., Hong, G., Gee, A. D., and Brown, J. (2005) Evidence for the presence of three distinct binding sites for the thioflavin T class of Alzheimer's disease PET imaging agents on beta-amyloid peptide fibrils J. Biol. Chem. 280, 7677-7684
LeVine, H., 3rd (2005) Multiple ligand binding sites on A beta(1-40) fibrils Amyloid 12, 5-14
Reinke, A. A. and Gestwicki, J. E. (2011) Insight into amyloid structure using chemical probes Chem. Biol. Drug Des. 77, 399-411
Harel, M., Sonoda, L. K., Silman, I., Sussman, J. L., and Rosenberry, T. L. (2008) Crystal structure of thioflavin T bound to the peripheral site of Torpedo californica acetylcholinesterase reveals how thioflavin T acts as a sensitive fluorescent reporter of ligand binding to the acylation site J. Am. Chem. Soc. 130, 7856-7861
Biancalana, M., Makabe, K., Koide, A., and Koide, S. (2009) Molecular mechanism of thioflavin-T binding to the surface of beta-rich peptide self-assemblies J. Mol. Biol. 385, 1052-1063
Haidekker, M. A. and Theodorakis, E. A. (2007) Molecular rotors - fluorescent biosensors for viscosity and flow Org. Biomol. Chem. 5, 1669-1678
Wolfe, L. S., Calabrese, M. F., Nath, A., Blaho, D. V., Miranker, A. D., and Xiong, Y. (2010) Protein-induced photophysical changes to the amyloid indicator dye thioflavin T Proc. Natl. Acad. Sci. U.S.A. 107, 16863-16868
Campbell, N. H., Parkinson, G. N., Reszka, A. P., and Neidle, S. (2008) Structural basis of DNA quadruplex recognition by an acridine drug J. Am. Chem. Soc. 130, 6722-6724
Collie, G. W., Promontorio, R., Hampel, S. M., Micco, M., Neidle, S., and Parkinson, G. N. (2012) Structural basis for telomeric G-quadruplex targeting by naphthalene diimide ligands J. Am. Chem. Soc. 134, 2723-2731
Clark, G. R., Pytel, P. D., Squire, C. J., and Neidle, S. (2003) Structure of the first parallel DNA quadruplex-drug complex J. Am. Chem. Soc. 125, 4066-4067
Bessi, I., Bazzicalupi, C., Richter, C., Jonker, H. R., Saxena, K., Sissi, C., Chioccioli, M., Bianco, S., Bilia, A. R., Schwalbe, H., and Gratteri, P. (2012) Spectroscopic, molecular modeling, and NMR-spectroscopic investigation of the binding mode of the natural alkaloids berberine and sanguinarine to human telomeric G-quadruplex DNA ACS Chem. Biol. 7, 1109-1119
Monchaud, D. and Teulade-Fichou, M. P. (2010) G4-FID: a fluorescent DNA probe displacement assay for rapid evaluation of quadruplex ligands Methods Mol. Biol. 608, 257-271
Cohen, A. D., Rabinovici, G. D., Mathis, C. A., Jagust, W. J., Klunk, W. E., and Ikonomovic, M. D. (2012) Using Pittsburgh compound B for in vivo PET imaging of fibrillar amyloid-beta Adv. Pharmacol. 64, 27-81