Loop residues of thrombin-binding DNA aptamer impact G-quadruplex stability and thrombin binding

Biochimie

Volumn 93, Issue 8, 2011, Pages 1231-1238

  Nagatoishi, Satoru ^a   Isono, Noburu ^a   Tsumoto, Kouhei ^b   Sugimoto, Naoki ^a  

^a KONAN UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

Aptamer; G quadruplex; Thrombin

Indexed keywords

ADENINE; APTAMER; DNA; OLIGONUCLEOTIDE; POTASSIUM ION; THROMBIN; THYMIDINE;

ARTICLE; BINDING AFFINITY; DNA PROTEIN COMPLEX; ISOTHERMAL TITRATION CALORIMETRY; MOLECULAR INTERACTION; PROTEIN DNA BINDING; PROTEIN STABILITY; PROTEIN STRUCTURE; THERMODYNAMICS;

APTAMERS, NUCLEOTIDE; G-QUADRUPLEXES; HYDROGEN BONDING; THROMBIN;

EID: 79960699716     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2011.03.013     Document Type: Article

References (73)

1. S. Neidle, and S. Balasubramanian Quadruplex Nucleic Acids 2006 RSC Biomolecular Sciences Cambridge
2. C.C. Hardin, A.G. Perry, and K. White Thermodynamic and kinetic characterization of the dissociation and assembly of quadruplex nucleic acids Biopolymers 56 2000 147 194 (Pubitemid 33115750)
3. A.N. Lane, J.B. Chaires, R.D. Gray, and J.O. Trent Stability and kinetics of G-quadruplex structures Nucleic Acids Res. 36 2008 5482 5515
4. H.M. Wong, L. Payet, and J.L. Huppert Function and targeting of G-quadruplexes Curr. Opin. Mol. Ther. 11 2009 146 155
5. S. Neidle The structures of quadruplex nucleic acids and their drug complexes Curr. Opin. Struct. Biol. 19 2009 239 250
6. J.B. Chaires Human telomeric G-quadruplex: thermodynamic and kinetic studies of telomeric quadruplex stability FEBS J. 277 2009 1098 1106
7. 2+ Nucleic Acids Res. 31 2003 1156 1163 (Pubitemid 36284956)
8. W. Li, D. Miyoshi, S. Nakano, and N. Sugimoto Structural competition involving G-quadruplex DNA and its complement Biochemistry 42 2003 11736 11744 (Pubitemid 37243634)
9. D.H. Zhang, T. Fujimoto, S. Saxena, H.Q. Yu, D. Miyoshi, and N. Sugimoto Monomorphic RNA G-quadruplex and polymorphic DNA G-quadruplex structures responding to cellular environmental factors Biochemistry 49 2010 4554 4563
10. Z.Y. Kan, Y. Yao, P. Wang, X.H. Li, Y.H. Hao, and Z. Tan Molecular crowding induces telomere G-quadruplex formation under salt-deficient conditions and enhances its competition with duplex formation Angew. Chem. Int. Ed. 45 2006 1629 1632 (Pubitemid 44105287)
11. D. Miyoshi, and N. Sugimoto Molecular crowding effects on structure and stability of DNA Biochimie 90 2008 1040 1051
12. K.W. Zheng, Z. Chen, Y.H. Hao, and Z. Tan Molecular crowding creates an essential environment for the formation of stable G-quadruplexes in long double-stranded DNA Nucleic Acids Res. 38 2009 327 338
13. J. Zhou, C. Wei, G. Jia, X. Wang, Z. Feng, and C. Li Formation and stabilization of G-quadruplex in nanosized water pools Chem. Commun. 46 2010 1700 1702
14. K. Paeschke, T. Simonsson, J. Postberg, D. Rhodes, and H.J. Lipps Telomere end-binding proteins control the formation of G-quadruplex DNA structures in vivo Nat. Struct. Mol. Biol. 12 2005 847 854 (Pubitemid 41486707)
15. N. Maizels Dynamic roles for G4 DNA in the biology of eukaryotic cells Nat. Struct. Mol. Biol. 13 2006 1055 1059 (Pubitemid 44885914)
16. H.J. Lipps, and D. Rhodes G-quadruplex structures: in vivo evidence and function Trends Cell Biol. 19 2009 414 422
17. T.A. Brooks, and L.H. Hurley The role of supercoiling in transcriptional control of MYC and its importance in molecular therapeutics Nat. Rev. Cancer 9 2009 849 861
18. S. Balasubramanian, and S. Neidle G-quadruplex nucleic acids as therapeutic targets Curr. Opin. Chem. Biol. 13 2009 345 353
19. L.A. Cahoon, and H.S. Seifert An alternative DNA structure is necessary for pilin antigenic variation in Neisseria gonorrhoeae Science 325 2009 764 767
20. J.L. Huppert, and S. Balasubramanian Prevalence of quadruplexes in the human genome Nucleic Acids Res. 33 2005 2908 2916 (Pubitemid 41511230)
21. J.L. Huppert, and S. Balasubramanian G-quadruplexes in promoters throughout the human genome Nucleic Acids Res. 35 2007 406 413 (Pubitemid 46232058)
22. A. Verma, K. Halder, R. Halder, V.K. Yadav, P. Rawal, R.K. Thakur, F. Mohd, A. Sharma, and S. Chowdhury Genome-wide computational and expression analyses reveal G-quadruplex DNA motifs as conserved cis-regulatory elements in human and related species J. Med. Chem. 51 2008 5641 5649
23. S. Kumari, A. Bugaut, J.L. Huppert, and S. Balasubramanian An RNA G-quadruplex in the 5′ UTR of the NRAS proto-oncogene modulates translation Nat. Chem. Biol. 3 2007 218 221 (Pubitemid 46440536)
24. J. Eddy, and N. Maizels Gene function correlates with potential for G4 DNA formation in the human genome Nucleic Acids Res. 34 2006 3887 3896 (Pubitemid 44391004)
25. Z. Du, Y. Zhao, and N. Li Genome-wide analysis reveals regulatory role of G4 DNA in gene transcription Genome Res. 18 2008 233 241 (Pubitemid 351240733)
26. K. Halder, M. Wieland, and J.S. Hartig Predictable suppression of gene expression by 5′-UTR-based RNA quadruplexes Nucleic Acids Res. 37 2009 6811 6817
27. H. Fernando, S. Sewitz, J. Darot, S. Tavare, J.L. Huppert, and S. Balasubramanian Genome-wide analysis of a G-quadruplex-specific single-chain antibody that regulates gene expression Nucleic Acids Res. 37 2009 6716 6722
28. 1: function and regulation Annu. Rev. Pharmacol. Toxicol. 50 2010 111 129
29. A. Verma, V.K. Yadav, R. Basundra, A. Kumar, and S. Chowdhury Evidence of genome-wide G4 DNA-mediated gene expression in human cancer cells Nucleic Acids Res. 37 2009 4194 4204
30. S. Neidle, and G. Parkinson Telomere maintenance as a target for anticancer drug discovery Nat. Rev. Drug Discov. 1 2002 383 393 (Pubitemid 37361468)
31. D. Yang, and K. Okamoto Structural insights into G-quadruplexes: towards new anticancer drugs Future Med. Chem. 2 2010 619 646
32. A. De Cian, L. Lacroix, C. Douarre, N. Temime-Smaali, C. Trentesaux, J.F. Riou, and J.L. Mergny Targeting telomeres and telomerase Biochimie 90 2008 131 155 (Pubitemid 350245369)
33. D. Monchaud, and M.P. Teulade-Fichou A hitchhiker's guide to G-quadruplex ligands Org. Biomol. Chem. 6 2008 627 636 (Pubitemid 351972601)
34. T.M. Ou, Y.J. Lu, J.H. Tan, Z.S. Huang, K.Y. Wong, and L.Q. Gu G-quadruplexes: targets in anticancer drug design ChemMedChem 3 2008 690 713
35. H. Yaku, T. Murashima, D. Miyoshi, and N. Sugimoto Anionic phthalocyanines targeting G-quadruplexes and inhibiting telomerase activity in the presence of excessive DNA duplexes Chem. Commun. 46 2010 5740 5742
36. T.M. Bryan, and M.B. Jarstfer Interrogation of G-quadruplex-protein interactions Methods 43 2007 332 339 (Pubitemid 47633207)
37. M. Fry Tetraplex DNA and its interacting proteins Front. Biosci. 12 2007 4336 4351
38. M.J. Law, K.M. Lower, H.P. Voon, J.R. Hughes, D. Garrick, V. Viprakasit, M. Mitson, M. De Gobbi, M. Marra, A. Morris, A. Abbott, S.P. Wilder, S. Taylor, G.M. Santos, J. Cross, H. Ayyub, S. Jones, J. Ragoussis, D. Rhodes, I. Dunham, D.R. Higgs, and R.J. Gibbons ATR-X syndrome protein targets tandem repeats and influences allele-specific expression in a size-dependent manner Cell 143 2010 367 378
39. V.A. Soldatenkov, A.A. Vetcher, T. Duka, and S. Ladame First evidence of a functional interaction between DNA quadruplexes and poly(ADP-ribose) polymerase-1 ACS Chem. Biol. 3 2008 214 219
40. J. Shklover, P. Weisman-Shomer, A. Yafe, and M. Fry Quadruplex structures of muscle gene promoter sequences enhance in vivo MyoD-dependent gene expression Nucleic Acids Res. 38 2010 2369 2377
41. V. Gonzalez, and L.H. Hurley The C-terminus of nucleolin promotes the formation of the c-MYC G-quadruplex and inhibits c-MYC promoter activity Biochemistry 49 2010 9706 9714
42. M. Melko, and B. Bardoni The role of G-quadruplex in RNA metabolism: involvement of FMRP and FMR2P Biochimie 92 2010 919 926
43. L. Menon, and M.-R. Mihailescu Interactions of the G-quartet forming semaphoring 3F RNA with the RGG box domain of the fragile X protein family Nucleic Acids Res. 35 2007 5379 5392 (Pubitemid 47423912)
44. K. Takahama, K. Kino, S. Arai, R. Kurokawa, and T. Oyoshi Identification of Ewing's sarcoma protein (EWS) as a G-quadruplex DNA- and RNA-binding protein FEBS J 278 2011 988 998
45. K. Padmanabhan, and A. Tulinsky An ambiguous structure of a DNA 15-mer thrombin complex Acta Crystallogr. D Biol. Crystallogr. 52 1996 272 282
46. M.J. Blandamer, J.B.F.N. Engberts, P.T. Gleeson, and J.C.R. Reis Activity of water in aqueous systems; a frequently neglected property Chem. Soc. Rev. 34 2005 440 458 (Pubitemid 40720489)
47. S. Nagatoishi, Y. Tanaka, and K. Tsumoto Circular dichroism spectra demonstrate formation of the thrombin-binding DNA aptamer G-quadruplex under stabilizing-cation-deficient conditions Biochem. Biophys. Res. Commun. 352 2007 812 817 (Pubitemid 44880327)
48. E.G. Richards Use of tables in calculation of absorption, optical rotatory dispersion and circular dichroism of polyribonucleotides G.D. Fasman, Handbook of Biochemistry and Molecular Biology third ed. 1975 CRC Press Cleveland, OH 596 603
49. D. Miyoshi, H. Karimata, and N. Sugimoto Hydration regulates thermodynamics of G-quadruplex formation under molecular crowding conditions J. Am. Chem. Soc. 128 2006 7957 7963 (Pubitemid 43945737)
50. T. Wiseman, S. Williston, J.F. Brandts, and L.N. Lin Rapid measurement of binding constants and heats of binding using a new titration calorimeter Anal. Biochem. 179 1989 131 137 (Pubitemid 19149635)
51. B.I. Kankia, and L.A. Marky Folding of the thrombin aptamer into a G-quadruplex with Sr(2+): stability, heat, and hydration J. Am. Chem. Soc. 123 2001 10799 10804 (Pubitemid 33041990)
52. M. Fialová, J. Kypr, and M. Vorlíčková The thrombin binding aptamer GGTTGGTGTGGTTGG forms a bimolecular guanine tetraplex Biochem. Biophys. Res. Commun. 344 2006 50 54
53. M. Trajkovski, P. Sket, and J. Plavec Cation localization and movement within DNA thrombin binding aptamer in solution Org. Biomol. Chem. 7 2009 4677 4684
54. C.M. Olsen, H.T. Lee, and L.A. Marky Unfolding thermodynamics of intramolecular G-quadruplexes: base sequence contributions of the loops J. Phys. Chem. B 113 2009 2587 2595
55. B. Pagano, L. Martino, A. Randazzo, and C. Giancola Stability and binding properties of a modified thrombin binding aptamer Biophys. J. 94 2008 562 569
56. L.C. Bock, L.C. Griffin, J.A. Latham, E.H. Vermaas, and J.J. Toole Selection of single-stranded-DNA molecules that bind and inhibit human thrombin Nature 355 1992 564 566
57. I. Smirnov, and R.H. Shafer Effect of loop sequence and size on DNA aptamer stability Biochemistry 39 2000 1462 1468 (Pubitemid 30090716)
58. + solution: effect of loop length and sequence on the folding topology J. Am. Chem. Soc. 131 2009 16824 16831
59. V.M. Marathias, and P.H. Bolton Determinants of DNA quadruplex structural type: sequence and potassium binding Biochemistry 38 1999 4355 4364
60. R.F. Macaya, J.A. Waldron, B.A. Beutel, H.T. Gao, M.E. Joesten, M.H. Yang, R. Patel, A.H. Bertelsen, and A.F. Cook Structural and functional-characterization of potent antithrombotic oligonucleotides possessing both quadruplex and Duplex Motifs Biochemistry 34 1995 4478 4492
61. A. Heckel, and G. Mayer Light regulation of aptamer activity: an anti-thrombin aptamer with caged thymidine nucleobases J. Am. Chem. Soc. 127 2005 822 823 (Pubitemid 40144269)
62. J. Muller, B. Wulffen, B. Potzsch, and G. Mayer Multidomain targeting generates a high-affinity thrombin-inhibiting bivalent aptamer ChemBioChem 8 2007 2223 2226
63. M. Tsiang, C.S. Gibbs, L.C. Griffin, K.E. Dunn, and L.L.K. Leung Selection of a suppressor mutation that restores affinity of an oligonucleotide inhibitor for thrombin using in-vitro genetics J. Biol. Chem. 270 1995 19370 19376
64. P. Hazel, G.N. Parkinson, and S. Neidle Predictive modelling of topology and loop variations in dimeric DNA quadruplex structures Nucleic Acids Res. 34 2006 2117 2127 (Pubitemid 44314209)
65. A. Risitano, and K.R. Fox Influence of loop size on the stability of intramolecular DNA quadruplexes Nucleic Acids Res. 32 2004 2598 2606 (Pubitemid 38854813)
66. S.M. Haider, G.N. Parkinson, and S. Neidle Structure of a G-quadruplex-ligand complex J. Mol. Biol. 326 2003 117 125 (Pubitemid 36279362)
67. H. Yu, C. Zhao, Y. Chen, M. Fu, J. Ren, and X. Qu DNA loop sequence as the determinant for chiral supramolecular compound G-quadruplex selectivity J. Med. Chem. 53 2010 492 498
68. J. Seenisamy, E.M. Rezler, T.J. Powell, D. Tye, V. Gokhale, C.S. Joshi, A. Siddiqui-Jain, and L.H. Hurley The dynamic character of the G-quadruplex element in the c-MYC promoter and modification by TMPyP4 J. Am. Chem. Soc. 126 2004 8702 8709 (Pubitemid 38955732)
69. E. Hatzakis, K. Okamoto, and D. Yang Thermodynamic stability and folding kinetics of the major G-quadruplex and its loop isomers formed in the nuclease hypersensitive element in the human c-Myc promoter: effect of loops and flanking segments on the stability of parallel-stranded intramolecular G-quadruplexes Biochemistry 49 2010 9152 9160
70. K.J. Zanotti, P.E. Lackey, G.L. Evans, and M.R. Mihailescu Thermodynamics of the fragile X mental retardation protein RGG box interactions with G quartet forming RNA Biochemistry 45 2006 8319 8330 (Pubitemid 44036538)
71. J.C. Darnell, K.B. Jensen, P. Jin, V. Brown, S.T. Warren, and R.B. Darnell Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function Cell 107 2001 489 499 (Pubitemid 33152784)
72. A. Ramos, D. Hollingworth, and A. Pastore G-quartet-dependent recognition between the FMRP RGG box and RNA RNA 9 2003 1198 1207 (Pubitemid 37151675)
73. K.A. Corbin-Lickfett, I.H. Chen, M.J. Cocco, and R.M. Sandri-Goldin The HSV-1 ICP27 RGG box specifically binds flexible, GC-rich sequences but not G-quartet structures Nucleic Acids Res. 37 2009 7290 7301