Topology Conservation and Loop Flexibility in Quadruplex-Drug Recognition: Crystal Structures of Inter- and Intramolecular Telomeric DNA Quadruplex-Drug Complexes

Journal of Molecular Biology

Volumn 381, Issue 5, 2008, Pages 1145-1156

  Parkinson, Gary N ^a   Cuenca, Francisco ^a   Neidle, Stephen ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

ligand interaction; quadruplex; telomeric DNA; topology; X ray structures

Indexed keywords

DNA; NUCLEIC ACID;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; DNA DETERMINATION; DNA SEQUENCE; GENE EXPRESSION; HUMAN; PRIORITY JOURNAL;

TETRA;

EID: 48749109524     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.06.022     Document Type: Article

References (52)

1. n, present at the telomeres of human chromosomes. Proc. Natl Acad. Sci. USA 85 (1988) 6622-6626
2. Burge S., Parkinson G.N., Hazel P., Todd A.K., and Neidle S. Quadruplex DNA: sequence, topology and structure. Nucleic Acids Res. 34 (2006) 5402-5415
3. Sun D., Thompson B., Cathers B.E., Salazar M., Kerwin S.M., Trent J.O., et al. Inhibition of human telomerase by a G-quadruplex-interactive compound. J. Med. Chem. 40 (1997) 2113-2116
4. Autexier C., and Lue N.F. The structure and function of telomerase reverse transcriptase. Annu. Rev. Biochem. 75 (2006) 493-517
5. Hahn W.C., Stewart S.A., Brooks M.W., York S.G., Eaton E., Kurachi A., et al. Inhibition of telomerase limits the growth of human cancer cells. Nat. Med. 5 (1999) 1164-1170
6. Kim N.W., Piatyszek M.A., Prowse K.R., Harley C.B., West M.D., Ho P.L.C., et al. Specific association of human telomerase activity with immortal cells and cancer. Science 266 (1994) 2011-2015
7. Xu L., and Blackburn E.H. Human cancer cells harbor T-stumps, a distinct class of extremely short telomeres. Mol. Cell 28 (2007) 315-327
8. Verdun R.E., and Karlseder J. Replication and protection of telomeres. Nature 447 (2007) 924-931
9. de Lange T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19 (2005) 2100-2110
10. Neidle S., and Parkinson G.N. Telomere maintenance as a target for anticancer drug discovery. Nat. Rev. Drug Discov. 1 (2002) 383-393
11. Shay J.W., and Wright W.E. Telomerase therapeutics for cancer: challenges and new directions. Nat. Rev. Drug Discov. 5 (2006) 577-584
12. Oganesian L., and Bryan T.M. Physiological relevance of telomeric G-quadruplex formation: a potential drug target. BioEssays 29 (2007) 155-165
13. De Cian A., Lacroix L., Douarre C., Temime-Smaali N., Trentesaux C., Riou J.-F., and Mergny J.-L. Targeting telomeres and telomerase. Biochimie 90 (2008) 131-155
14. Monchaud D., and Teulade-Fichou M.P. A hitchhiker's guide to G-quadruplex ligands. Org. Biomol. Chem. 6 (2008) 627-636
15. Gomez D., Wenner T., Brassart B., Douarre C., O'Donohue M.-F., El Khoury V., et al. Telomestatin-induced telomere uncapping is modulated by POT1 through G-overhang extension in HT1080 human tumor cells. J. Biol. Chem. 281 (2006) 38721-38729
16. Gomez D., O'Donohue M.-F., Wenner T., Douarre C., Macadré J., Koebel P., et al. The G-quadruplex ligand telomestatin inhibits POT1 binding to telomeric sequences in vitro and induces GFP-POT1 dissociation from telomeres in human cells. Cancer Res. 66 (2006) 6908-6912
17. Kim M.Y., Vankayalapati H., Shin-Ya K., Wierzba K., and Hurley L.H. Telomestatin, a potent telomerase inhibitor that interacts quite specifically with the human telomeric intramolecular G-quadruplex. J. Am. Chem. Soc. 124 (2002) 2098-2099
18. 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
19. 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
20. Gunaratnam M., Greciano O., Martins C., Reszka A.P., Schultes C.M., Morjani H., et al. Mechanism of acridine-based telomerase inhibition and telomere shortening. Biochem. Pharmacol. 74 (2007) 679-689
21. Leonetti C., Amodei S., D'Angelo C., Rizzo A., Benassi B., Antonelli A., et al. 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
22. Burger A.M., Dai F., Schultes C.M., Reszka A.P., Moore M.J., Double J.A., and Neidle S. The G-quadruplex-interactive molecule BRACO-19 inhibits tumor growth, consistent with telomere targeting and interference with telomerase function. Cancer Res. 65 (2005) 1489-1496
23. Pilch D.S., Barbieri C.M., Rzuczek S.G., LaVoie E.J., and Rice J.E. Targeting human telomeric G-quadruplex DNA with oxazole-containing macrocyclic compounds. Biochimie (2008) 10.1016/j.biochi.2008.03.011
24. Shirude P.S., Gillies E.R., Ladame S., Godde F., Shin-Ya K., Huc I., and Balasubramanian S. Macrocyclic and helical oligoamides as a new class of G-quadruplex ligands. J. Am. Chem. Soc. 129 (2007) 11890-11891
25. Clark G.R., Pytel P.D., Squire C.J., and Neidle S. Structure of the first parallel DNA quadruplex-drug complex. J. Am. Chem. Soc. 125 (2003) 4066-4067
26. Haider S.M., Parkinson G.N., and Neidle S. Structure of a G-quadruplex-ligand complex. J. Mol. Biol. 326 (2003) 117-125
27. Parkinson G.N., Ghosh R., and Neidle S. Structural basis for binding of porphyrin to human telomeres. Biochemistry 46 (2007) 2390-2397
28. Campbell N.H., Parkinson G.N., Reszka A.R., and Neidle S. Structural basis of DNA quadruplex recognition by an acridine drug. J. Am. Chem. Soc. 130 (2008) 6722-6724
29. 4 containing the human telomeric repeat. J. Mol. Biol. 334 (2003) 25-36
30. Mehta A.K., Shayo Y., Vankayalapati H., Hurley L.H., and Schaefer J. Structure of a quinobenzoxazine-G-quadruplex complex by REDOR NMR. Biochemistry 43 (2004) 11953-11958
31. Phan A.T., Kuryavyi V., Gaw H.Y., and Patel D.J. Small-molecule interaction with a five-guanine-tract G-quadruplex structure from the human MYC promoter. Nat. Chem. Biol. 1 (2005) 167-173
32. Cuenca F., Greciano O., Gunaratnam M., Haider S., Munnur D., Nanjunda R., et al. Tri- and tetra-substituted naphthalene diimides as potent G-quadruplex ligands. Bioorg. Med. Chem. Lett. 18 (2008) 1668-1673
33. Parkinson G.N., Lee M.P.H., and Neidle S. Crystal structure of parallel quadruplexes from human telomeric DNA. Nature 417 (2002) 876-880
34. Schneider B., Neidle S., and Berman H.M. Conformations of the sugar-phosphate backbone in helical DNA crystal structures. Biopolymers 42 (1997) 113-124
35. Neidle S. Principles of Nucleic Acid Structure (2007), Elsevier/Academic Press, London, UK
36. Kettani A., Gorin A., Majumdar A., Hermann T., Skripkin E., Zhao H., et al. A dimeric DNA interface stabilized by stacked A•(G•G•G•G)•A hexads and coordinated monovalent cations. J. Mol. Biol. 297 (2000) 627-644
37. + solution. Nucleic Acids Res. 34 (2006) 5715-5719
38. + solution: an intramolecular (3 + 1) G-quadruplex scaffold. J. Am. Chem. Soc. 128 (2006) 9963-9970
39. 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/antiparallel strands in potassium solution. Nucleic Acids Res. 34 (2006) 2723-2735
40. + solution: insights into structure polymorphism of the human telomeric sequence. Nucleic Acids Res. 35 (2007) 4927-4940
41. + solution. Nucleic Acids Res. 35 (2006) 6517-6525
42. + solution under molecular crowding condition. J. Am. Chem. Soc. 129 (2007) 11185-11191
43. Paramasivan S., Rujan I., and Bolton P.H. Circular dichroism of quadruplex DNAs: applications to structure, cation effects and ligand binding. Methods 43 (2007) 324-331
44. Zagotto G., Sissi C., Moro S., Dal Ben D., Parkinson G.N., Fox K.R., et al. Amide bond direction modulates G-quadruplex recognition and telomerase inhibition by 2,6 and 2,7 bis-substituted anthracenedione derivatives. Bioorg. Med. Chem. 16 (2008) 354-361
45. Hurley L.H., Wheelhouse R.T., Sun D., Kerwin S.M., Salazar M., Fedoroff O.Y., et al. G-quadruplexes as targets for drug design. Pharmacol. Ther. 85 (2000) 141-158
46. Read M., Harrison R.J., Romagnoli B., Tanious F.A., Gowan S.H., Reszka A.P., et al. Structure-based design of selective and potent G-quadruplex-mediated telomerase inhibitors. Proc. Natl Acad. Sci. USA 98 (2001) 4844-4849
47. CrystalClear™: an integrated program for the collection and processing of area detector data, Rigaku Corporation, © 1997-2002.
48. Storoni L.C., McCoy A.J., and Read R.J. Likelihood-enhanced fast rotation functions. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 (2004) 432-438
49. Collaborative Computational Project, No. 4. The CCP4 Suite: programs for protein crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 (1995) 760-763
50. Winn M., Isupov M., and Murshudov G.N. Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr., Sect. D: Biol. Crystallogr. 57 (2001) 122-133
51. Cambillau C., and Horjales E.J. TOM: a FRODO subpackage for protein-ligand fitting with interactive energy minimization. J. Mol. Graphics 5 (1987) 175-177
52. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., and Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004) 1605-1612