Crystal structure of a c-kit promoter quadruplex reveals the structural role of metal ions and water molecules in maintaining loop conformation

Nucleic Acids Research

Volumn 40, Issue 10, 2012, Pages 4691-4700

  Wei, Dengguo ^a   Parkinson, Gary N ^a   Reszka, Anthony P ^a   Neidle, Stephen ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE QUADRUPLEX; MAGNESIUM ION; METAL ION; POTASSIUM ION; STEM CELL FACTOR; WATER;

ARTICLE; CLUSTER ANALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA CONFORMATION; DNA DETERMINATION; DNA SEQUENCE; DNA STRUCTURE; GENE REARRANGEMENT; GENE REGULATORY NETWORK; GENETIC STABILITY; NUCLEAR MAGNETIC RESONANCE; ONCOGENE C KIT; PRIORITY JOURNAL; PROMOTER REGION; X RAY;

CATIONS; CRYSTALLOGRAPHY, X-RAY; DNA; G-QUADRUPLEXES; MAGNESIUM; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; POTASSIUM; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-KIT; WATER;

EID: 84861564071     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks023     Document Type: Article

References (57)

1. Davies, J.T. (2004) G-quartets 40 years later: from 50-GMP to molecular biology and supramolecular chemistry. Angew. Chem. Intl. Edit., 43, 668-698.
2. Burge, S., Parkinson, G.N., Hazel, P., Todd, A.K. and Neidle, S. (2006) Quadruplex DNA: sequence, topology and structure. Nucleic Acids Res., 34, 5402-5415.
3. 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.
4. Phan, A.T. (2010) Human telomeric G-quadruplex: structures of DNA and RNA sequences. FEBS J., 277, 1107-1117.
5. Todd, A.K., Johnston, M. and Neidle, S. (2005) Highly prevalent putative quadruplex sequence motifs in human DNA. Nucleic Acids Res., 33, 2901-2907.
6. Huppert, J.L. and Balasubramanian, S. (2005) Prevalence of quadruplexes in the human genome. Nucleic Acids Res., 33, 2908-2916.
7. Huppert, J.L. and Balasubramanian, S. (2007) G-quadruplexes in promoters throughout the human genome. Nucleic Acids Res., 35, 406-413.
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. Balasubramanian, S., Hurley, L.H. and Neidle, S. (2011) Targeting G-quadruplexes in gene promoters: a novel anticancer strategy? Nature Rev. Drug Discov., 10, 261-275.
10. Kumari, S., Bugaut, A., Huppert, J.L. and Balasubramanian, S. (2007) An RNA G-quadruplex in the 5' UTR of the NRAS proto-oncogene modulates translation. Nature Chem. Biol., 3, 218-221.
11. Huppert, J.L., Bugaut, A., Kumari, S. and Balasubramanian, S. (2008) G-quadruplexes: the beginning and end of UTRs. Nucleic Acids Res., 36, 6260-6268.
12. Halder, K., Wieland, M. and Hartig, J.S. (2009) Predictable suppression of gene expression by 5'-UTR-based RNA quadruplexes. Nucleic Acids Res., 37, 6811-6817.
13. Howard, F.B. and Miles, H.T. (1982) Poly(inosinic acid) helices: essential chelation of alkali metal ions in the axial channel. Biochemistry, 21, 6736-6745.
14. Hardin, C.C., Henderson, E., Watson, T. and Prosser, J.K. (1991) Monovalent cation induced structural transitions in telomeric DNAs: G-DNA folding intermediates. Biochemistry, 30, 4460-4472.
15. Williamson, J.R., Raghuraman, M.K. and Cech, T.R. (1989) Monovalent cation-induced structure of telomeric DNA: the G-quartet model. Cell, 45, 167-176.
16. Smith, F.W. and Feigon, J. (1992) Quadruplex structure of Oxytricha telomeric DNA oligonucleotides. Nature, 356, 164-168.
17. Rovnak, D., Baldus, M., Wu, G., Hud, N.V., Feigon, J. and Griffin, R.G. (2000) Localization of 23Na+ in a DNA quadruplex by high-field solid-state NMR. J. Am. Chem. Soc., 122, 11423-11429.
18. Smirnov, I.V., Kotch, F.W., Pickering, I.J., Davis, J.T. and Shafer, R.H. (2002) Pb EXAFS studies on DNA quadruplexes: identification of metal ion binding site. Biochemistry, 41, 12133-12139.
19. Sen, D. and Gilbert, W. (1990) A sodium-potassium switch in the formation of four-stranded G4-DNA. Nature, 344, 410-414.
20. Schultze, P., Hud, N.V., Smith, F.W. and Feigon, J. (1994) The effect of sodium, potassium and ammonium ions on the conformation of the dimeric quadruplex formed by the Oxytricha nova telomere repeat oligonucleotide d(G4T4G4). Nucleic Acids Res., 27, 3018-3028.
21. Marincola, F.C., Virno, A., Randazzo, A., Mocci, F., Saba, G. and Lai, A. (2009) Competitive binding exchange between alkali metal ions (K+, Rb+, and Cs+) and Na+ ions bound to the dimeric quadruplex [d(G4T4G4)]2: a 23Na and 1H NMR study. Magn. Reson. Chem., 47, 1036-1042.
22. Ida, R., Kwan, I.C. and Wu, G. (2007) Direct 23Na NMR observation of mixed cations residing inside a G-quadruplex channel. Chem. Commun., 795-797.
23. Ida, R. and Wu, G. (2008) Direct NMR detection of alkali metal ions bound to G-quadruplex DNA. J. Am. Chem. Soc., 130, 3590-3602.
24. Hud, N.V., Schultze, P. and Feigon, J. (1998) Ammonium ion as an NMR probe for monovalent cation coordination sites of DNA quadruplexes. J. Am. Chem. Soc., 120, 6403-6404.
25. Olson, C.M., Gmeimer, W.H. and Marky, L.A. (2006) Unfolding of G-quadruplexes: energetic, and ion and water contributions of G-quartet stacking. J. Phys. Chem., 110, 6962-6969.
26. Snoussi, K. and Halle, B. (2008) Internal sodium ions and water molecules in guanine quadruplexes: magnetic relaxation dispersion studies of [d(G3T4G3)]2 and [d(G4T4G4)]2. Biochemistry, 47, 12219-12229.
27. Mergny, J.-L., De Cian, A., Ghelab, A., Saccà, B. and Lacroix, L. (2005) Kinetics of tetramolecular quadruplexes. Nucleic Acids Res., 33, 81-94.
28. Yan, Y.Y., Lin, J., Ou, T.-M., Tan, J.-H., Li, D., Gu, L.-Q. and Huang, Z.-S. (2010) Selective recognition of oncogene promoter G-quadruplexes by Mg2+. Biochem. Biophys. Res. Comm., 402, 614-618.
29. Parkinson, G.N., Lee, M.P.H. and Neidle, S. (2002) Crystal structure of parallel quadruplexes from human telomeric DNA. Nature, 417, 876-880.
30. Haider, S.M., Parkinson, G.N. and Neidle, S. (2003) Structure of a G-quadruplex-ligand complex. J. Mol. Biol., 326, 117-125.
31. Campbell, N.H., Patel, M., Tofa, A.B., Ghosh, R., Parkinson, G.N. and Neidle, S. (2009) Selectivity in ligand recognition of G-quadruplex loops. Biochemistry, 48, 1675-1680.
32. Parkinson, G.N., Ghosh, R. and Neidle, S. (2007) Structural basis for binding of porphyrin to human telomeres. Biochemistry, 46, 2390-2397.
33. Parkinson, G.N., Cuenca, F. and Neidle, S. (2008) Topology conservation and loop flexibility in quadruplex-drug recognition: crystal structures of inter-and intramolecular telomeric DNA quadruplex-drug complexes. J. Mol. Biol., 381, 1145-1156.
34. 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.
35. Gray, R.D. and Chaires, J.B. (2011) Linkage of cation binding and folding in human telomeric quadruplex DNA. Biophysical Chem., 159, 205-209.
36. Wang, Y. and Patel, D.J. (1993) Solution structure of the human telomeric repeat d[AG3(T2AG3)3] G-tetraplex. Structure, 1, 263-282.
37. 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.
38. Dai, J., Carver, M., Punchihewa, C., Jones, R.A. and Yang, D. (2007) 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, 4927-4940.
39. 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.
40. Phan, A.T., Luu, K.N. and Patel, D.J. (2006) Different loop arrangements of intramolecular human telomeric (3+1) G-quadruplexes in K+ solution. Nucleic Acids Res., 34, 5715-5719.
41. Luu, K.N., Phan, A.T., Kuryavyi, V., Lacroix, L. and Patel, D.J. (2006) Structure of the human telomere in K+ solution: an intramolecular (3+1) G-quadruplex scaffold. J. Am. Chem. Soc., 128, 9963-9970.
42. Rankin, S., Reszka, A.P., Huppert, J., Zloh, M., Parkinson, G.N., Todd, A.K., Ladame, S., Balasubramanian, S. and Neidle, S. (2005) Putative DNA quadruplex formation within the human c-kit oncogene. J. Am. Chem. Soc., 127, 10584-10589.
43. Phan, A.T., Kuryavyi, V., Burge, S., Neidle, S. and Patel, D.J. (2007) Structure of an unprecedented G-quadruplex scaffold in the human c-kit promoter. J. Am. Chem. Soc., 129, 4386-4392.
44. Gunaratnam, M., Swank, S., Haider, S.M., Galesa, K., Reszka, A.P., Beltran, M., Cuenca, F., Fletcher, J.A. and Neidle, S. (2009) Targeting human gastrointestinal stromal tumor cells with a quadruplex-binding small molecule. J. Med. Chem, 52, 3774-3783.
45. McLuckie, K.I., Waller, Z.A., Sanders, D.A., Alves, D., Rodriguez, R., Dash, J., McKenzie, G.J., Venkitaraman, A.R. and Balasubramanian, S. (2011) G-quadruplex-binding benzo[a]phenoxazines down-regulate c-KIT expression in human gastric carcinoma cells. J. Am. Chem. Soc., 133, 2658-2663.
46. Todd, A.K., Haider, S.M., Parkinson, G.N. and Neidle, S. (2007) Sequence occurrence and structural uniqueness of a G-quadruplex in the human c-kit promoter. Nucleic Acids Res., 35, 5799-5808.
47. Sheldrick, G.M. (2010) Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr., D66, 479-485.
48. CCP4. (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr., D50, 760-763.
49. Emsley, P., Lohkamp, B., Scott, W.G. and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr., D66, 486-501.
50. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C. and Read, R.J. (2007) Phaser crystallographic software. J. Appl. Crystallogr., 40, 658-674.
51. Vagin, A.A., Steiner, R.A., Lebedev, A.A., Potterton, L., McNicholas, S., Long, F. and Murshudov, G.N. (2004) REFMAC5 dictionary: organization of prior chemical knowledge and guidelines for its use. Acta Crystallogr., D60, 2184-2195.
52. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C. and Ferrin, T.E. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J. Comp. Chem, 25, 1605-1612.
53. DeLano, W.L. (2008) The PyMOL Molecular Graphics System, Version 0.99beta37, Schro?dinger, LLC.
54. Woods, K.K., Maehigashi, T., Howerton, S.B., Sines, C.C., Tannenbaum, S. and Williams, L.D. (2004) High-resolution structure of an extended A-tract: [d(CGCAAATTTGCG)]2. J. Am. Chem. Soc., 126, 15530-15531.
55. Cang, X., Sponer, J. and CheathamIII, T.E. (2011) Insight into G-DNA structural polymorphism and folding from sequence and loop connectivity through free energy analysis. J. Am. Chem. Soc., 133, 14270-14279.
56. Cang, X., Sponer, J. and CheathamIII, T.E. (2011) Explaining the varied glycosidic conformational, G-tract length and sequence preferences for anti-parallel G-quadruplexes. Nucleic Acids Res., 39, 4499-4512.
57. Reshetnikov, R.V., Sponer, J., Rassokhina, O.I., Kopylov, A.M., Tsvetkov, P.O., Makarov, A.A. and Govolin, A.V. (2011) Cation binding to 15-TBA quadruplex DNA is a multiple-pathway cation-dependent process. Nucleic Acids Res., 39, 9789-9802.