Exploring the chemical space of G-quadruplex binders: Discovery of a novel chemotype targeting the human telomeric sequence

Journal of Medicinal Chemistry

Volumn 56, Issue 23, 2013, Pages 9646-9654

  Di Leva, Francesco Saverio ^a   Zizza, Pasquale ^b   Cingolani, Chiara ^b   D'Angelo, Carmen ^b   Pagano, Bruno ^c   Amato, Jussara ^c   Salvati, Erica ^b   Sissi, Claudia ^d   Pinato, Odra ^d   Marinelli, Luciana ^c   Cavalli, Andrea ^a,e   Cosconati, Sandro ^f   Novellino, Ettore ^c   Randazzo, Antonio ^c   Biroccio, Annamaria ^b  

^a ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^b REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^d UNIVERSITY OF PADOVA   (Italy)

^e UNIVERSITY OF BOLOGNA   (Italy)

^f SECOND UNIVERSITY OF NAPLES   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; GUANINE QUADRUPLEX; HISTONE H2AX;

ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; BINDING AFFINITY; CELL SURVIVAL; CIRCULAR DICHROISM; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; DRUG DNA BINDING; DRUG SCREENING; DRUG STABILITY; DRUG TARGETING; FLUORESCENCE ANALYSIS; FLUORESCENT INTERCALATOR DISPLACEMENT ASSAY; HISTONE PHOSPHORYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; LIGAND BINDING; MELTING POINT; NUCLEAR MAGNETIC RESONANCE; TELOMERE; THERMOSTABILITY; TUMOR CELL LINE; VIRTUAL REALITY;

EID: 84890516811     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm401185b     Document Type: Article

References (42)

1. Sandell, L. L.; Zakian, V. A. Loss of a yeast telomere: Arrest, recovery and chromosome loss Cell 1993, 75, 729-739
2. De Cian, A.; Lacroix, L.; Douarre, C.; Temime-Smaali, N.; Trentesaux, C.; Riou, J.-F.; Mergny, J.-L. Targeting telomeres and telomerase Biochimie 2008, 90, 131-155
3. Paeschke, K.; Simonsson, T.; Postberg, J.; Rhodes, D.; Lipps, H. J. Telomere end-binding proteins control the formation of G-quadruplex DNA structures in vivo Nat. Struct. Mol. Biol. 2005, 12, 847-854
4. Biffi, G.; Tannahill, D.; McCafferty, J.; Balasubramanian, S. Quantitative visualization of DNA G-quadruplex structures in human cells Nat. Chem. 2013, 5, 182-186
5. 1H-NMR study Nucleosides, Nucleotides Nucleic Acids 2007, 26, 1133-11337
6. Virno, A.; Randazzo, A.; Giancola, C.; Bucci, M.; Cirino, G.; Mayol, L. A novel thrombin binding aptamer containing a G-LNA residue Bioorg. Med. Chem. 2007, 15, 5710-5718
7. Limongelli, V.; De Tito, S.; Cerofolini, L.; Fragai, M.; Pagano, B.; Trotta, R.; Cosconati, S.; Marinelli, L.; Novellino, E.; Bertini, I.; Randazzo, A.; Luchinat, C.; Parrinello, M. The G-triplex DNA Angew. Chem., Int. Ed. 2013, 52, 2269-2273
8. 4 J. Am. Chem. Soc. 2007, 129, 15950-15956
9. Cosconati, S.; Marinelli, L.; Trotta, R.; Virno, A.; Mayol, L.; Novellino, E.; Olson, A. J.; Randazzo, A. Tandem application of virtual screening and NMR experiments in the discovery of brand new DNA quadruplex groove binders J. Am. Chem. Soc. 2009, 131, 16336-16337
10. Cosconati, S.; Marinelli, L.; Trotta, R.; Virno, A.; De Tito, S.; Romagnoli, R.; Pagano, B.; Limongelli, V.; Giancola, C.; Baraldi, P. G.; Mayol, L.; Novellino, E.; Randazzo, A. Structural and conformational requisites in DNA quadruplex groove binding: Another piece to the puzzle J. Am. Chem. Soc. 2010, 132, 6425-64333
11. Trotta, R.; De Tito, S.; Lauri, I.; La Pietra, V.; Marinelli, L.; Cosconati, S.; Martino, L.; Conte, M. R.; Mayol, L.; Novellino, E.; Randazzo, A. Biochimie 2011, 93, 1280-1287
12. Cosconati, S.; Rizzo, A.; Trotta, R.; Pagano, B.; Iachettini, S.; De Tito, S.; Lauri, I.; Fotticchia, I.; Giustiniano, M.; Marinelli, L.; Giancola, C.; Novellino, E.; Biroccio, A.; Randazzo, A. Shooting for selective drug-like G-quadruplex binders: evidence for telomeric DNA damage and tumor cell death J. Med. Chem. 2012, 55, 9785-9792
13. Dai, J.; Carver, M.; Yang, D. Polymorphism of human telomeric quadruplex structures Biochimie 2008, 90, 1172-1183
14. Alcaro, S.; Musetti, C.; Distinto, S.; Casatti, M.; Zagotto, G.; Artese, A.; Parrotta, L.; Moraca, F.; Costa, G.; Ortuso, F.; Maccioni, E.; Sissi, C. Identification and characterization of new DNA G-quadruplex binders selected by a combination of ligand and structure-based virtual screening approaches J. Med. Chem. 2013, 56, 843-855
15. Balagurumoorthy, P.; Brahmachari, S. K. Structure and stability of human telomeric sequence J. Biol. Chem. 1994, 269, 21858-21869
16. Ying, L. M.; Green, J. J.; Li, H. T.; Klenerman, D.; Balasubramanian, S. Studies on the structure and dynamics of the human telomeric G-quadruplex by single-molecule fluorescence resonance energy transfer Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 14629-14634
17. + solutions Nucleic Acids Res. 2003, 31, 1605-1613
18. Phan, A. T.; Patel, D. J. 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. 2003, 125, 15021-15027
19. Luu, K. N.; Phan, A. T.; Kuryavyi, V.; Lacroix, L.; Patel, D. J. Structure of the human telomere in K+ solution: An intramolecular (3 + 1) G-quadruplex scaffold J. Am. Chem. Soc. 2006, 128, 9963-9970
20. 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
21. Huey, R.; Morris, G. M.; Olson, A. J.; Goodsell, D. S. A semiempirical free energy force field with charge-based desolvation J. Comput. Chem. 2007, 28, 1145-1152
22. Irwin, J. J.; Shoichet, B. K. ZINC-A Free Database of Commercially Available Compounds for Virtual Screening J. Chem. Inf. Model. 2005, 45, 177-182
23. Pagano, B.; Cosconati, S.; Gabelica, V.; Petraccone, L.; De Tito, S.; Marinelli, L.; La Pietra, V.; Di Leva, F. S.; Lauri, I.; Trotta, R.; Novellino, E.; Giancola, C.; Randazzo, A. State-of-the-art methodologies for the discovery and characterization of DNA G-quadruplex binders Curr. Pharm. Des. 2012, 18, 1880-1899
24. Mergny, J. L.; Maurizot, J. C. Fluorescence resonance energy transfer as a probe for G-quartet formation by a telomeric repeat ChemBioChem 2001, 2, 124-132
25. Giancola, C.; Pagano, B. Energetics of ligand binding to G-quadruplexes Top. Curr. Chem. 2013, 330, 211-242
26. Monchaud, D.; Allain, C.; 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. 2006, 16, 4842-4845
27. Vorlíčková, M.; Kejnovská, I.; Sagi, J.; Renčiuk, D.; Bednářová, K.; Motlová, J.; Kypr, J. Circular dichroism and guanine quadruplexes Methods 2012, 57, 64-75
28. Masiero, S.; Trotta, R.; Pieraccini, S.; De Tito, S.; Perone, R.; Randazzo, A.; Spada, G. P. A non-empirical chromophoric interpretation of CD spectra of DNA G-quadruplex structures Org. Biomol. Chem. 2010, 8, 2683-2692
29. Karsisiotis, A. I.; Hessari, N. M.; Novellino, E.; Spada, G. P.; Randazzo, A.; Webba da Silva, M. Topological characterization of nucleic acid G-quadruplexes by UV absorption and circular dichroism Angew. Chem., Int. Ed. 2011, 50, 10645-10646
30. Randazzo, A.; Spada, G. P.; da Silva, M. W. Circular dichroism of quadruplex structures Top. Curr. Chem. 2013, 330, 67-86
31. Martino, L.; Pagano, B.; Fotticchia, I.; Neidle, S.; Giancola, C. Shedding light on the interaction between TMPyP4 and human telomeric quadruplexes J. Phys. Chem. B 2009, 113, 14779-14786
32. Peduto, A.; Pagano, B.; Petronzi, C.; Massa, A.; Esposito, V.; Virgilio, A.; Paduano, F.; Trapasso, F.; Fiorito, F.; Florio, S.; Giancola, C.; Galeone, A.; Filosa, R. Design, synthesis, biophysical and biological studies of trisubstituted naphthalimides as G-quadruplex ligands Bioorg. Med. Chem. 2011, 19, 6419-6429
33. Thiriet, C.; Hayes, J. J. Chromatin in need of a fix: Phosphorylation of H2AX connects chromatin to DNA repair Mol. Cell 2005, 18, 617-622
34. Takai, H.; Smogorzewska, A.; de Lange, T. DNA damage foci at dysfunctional telomeres Curr. Biol. 2003, 13, 1549-1556
35. Morris, G. M.; Huey, R.; Lindstrom, W.; Sanner, M. F.; Belew, R. K.; Goodsell, D. S.; Olson, A. J. AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility J. Comput. Chem. 2009, 30, 2785-2791
36. Evans, D. A.; Neidle, S. Virtual screening of DNA minor groove binders J. Med. Chem. 2006, 49, 4232-4238
37. Cornell, W. D.; Cieplak, P.; Bayly, C. I.; Gould, I. R.; Merz, K. W., Jr.; 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
38. Hwang, T. L.; Shaka, A. J. Water suppression that works. Excitation sculpting using arbitrary waveforms and pulsed field gradients J. Magn. Reson. A 1995, 112, 275-279
39. Dalvit, C. Efficient multiple-solvent suppression for the study of the interactions of organic solvents with biomolecules J. Biomol. NMR 1998, 11, 437-444
40. Salvati, E.; Scarsella, M.; Porru, M.; Rizzo, A.; Iachettini, S.; Tentori, L.; Graziani, G.; D'Incalci, M.; Stevens, M. F.; Orlandi, A.; Passeri, D.; Gilson, E.; Zupi, G.; Leonetti, C.; Biroccio, A. PARP1 activated at telomeres upon G4 stabilization: possible target for telomere-based therapy Oncogene 2010, 29, 6280-6293
41. Biroccio, A.; Amodei, S.; Benassi, B.; Scarsella, M.; Cianciulli, A.; Mottolese, M.; Del Bufalo, D.; Leonetti, C.; Zupi, G. Reconstitution of hTERT restores tumorigenicity in melanoma-derived c-Myc low-expressing clones Oncogene 2002, 21, 3011-3019
42. Biroccio, A.; Benassi, B.; Filomeni, G.; Amodei, S.; Marchini, S.; Chiorino, G.; Rotilio, G.; Zupi, G.; Ciriolo, M. R. Glutathione influences c-Myc-induced apoptosis in M14 human melanoma cells J. Biol. Chem. 2002, 277, 43763-43770