Structural probes in quadruplex nucleic acid structure determination by NMR

Molecules

Volumn 17, Issue 11, 2012, Pages 13073-13086

  Karsisiotis, Andreas Ioannis ^a   Da Silva, Mateus Webba ^a  

^a UNIVERSITY OF ULSTER   (United Kingdom)

Author keywords

2,6 diaminopurine; 5 bromouracil; 8 bromoguanosine; 8 methylguanine; 8 O methylguanine; Chemical modifications; Inosine; LNA; Quadruplex; Riboguanosine

Indexed keywords

DNA; GUANINE QUADRUPLEX; RNA;

BASE PAIRING; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; DNA ADDUCT; HYDROGEN BOND; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE SEQUENCE; REVIEW; SYNTHESIS;

BASE PAIRING; BASE SEQUENCE; DNA; DNA ADDUCTS; G-QUADRUPLEXES; HYDROGEN BONDING; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; RNA;

EID: 84870190030     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules171113073     Document Type: Review

References (61)

1. Webba da Silva, M. NMR methods for studying quadruplex nucleic acids. Methods 2007, 43, 264-277.
2. Adrian, M.; Heddi, B.; Phan, A.T. NMR spectroscopy of G-quadruplexes. Methods 2012, 57, 11-24.
3. Musumeci, D.; Montesarchio, D. Polyvalent nucleic acid aptamers and modulation of their activity: A focus on the thrombin binding aptamer. Pharmacol. Ther. 2012, 136, 202-215.
4. Avino, A.; Fabrega, C.; Tintore, M.; Eritja, R. Thrombin Binding Aptamer, More than a Simple Aptamer: Chemically Modified Derivatives and Biomedical Applications. Curr. Pharm. Des. 2012, 18, 2036-2047.
5. Webba da Silva, M. Geometric formalism for DNA quadruplex folding. Chem. Eur. J. 2007, 13, 9738-9745.
6. Lech, C.J.; Lim, J.K.C.; Lim, J.M.W.; Amrane, S.; Heddi, B.; Phan, A.T. Effects of Site-Specific Guanine C8-Modifications on an Intramolecular DNA G-Quadruplex. Biophys. J. 2011, 101, 1987-1998.
7. Kuryavyi, V.; Majumdar, A.; Shallop, A.; Chernichenko, N.; Skripkin, E.; Jones, R.; Patel, D.J. A double chain reversal loop and two diagonal loops define the architecture of a unimolecular DNA quadruplex containing a pair of stacked G(syn)center dot G(syn)center dot G(anti)center dot G(anti) tetrads flanked by a G center dot(T-T) triad and a T center dot T center dot T triple. J. Mol. Biol. 2001, 310, 181-194.
8. + solution. Nucleic Acids Res. 2007, 35, 6517-6525.
9. + solution. FEBS J. 2007, 274, 3545-3556.
10. + Solution: A Stable Basket-Type G-Quadruplex with Only Two G-Tetrad Layers. J. Am. Chem. Soc. 2009, 131, 4301-4309.
11. Sugiyama, H.; Kawai, K.; Matsunaga, A.; Fujimoto, K.; Saito, I.; Robinson, H.; Wang, A.H.J. Synthesis, structure and thermodynamic properties of 8-methylguanine-containing oligonucleotides: Z-DNA under physiological salt conditions. Nucleic Acids Res. 1996, 24, 1272-1278.
12. Krawczyk, S.H.; Bischofberger, N.; Griffin, L.C.; Law, V.S.; Shea, R.G.; Swaminathan, S. Structure-activity study of oligodeoxynucleotides which inhibit thrombin. Nucleosides Nucleotides 1995, 14, 1109-1116.
13. He, G.X.; Krawczyk, S.H.; Swaminathan, S.; Shea, R.G.; Dougherty, J.P.; Terhorst, T.; Law, V.S.; Griffin, L.C.; Coutre, S.; Bischofberger, N. N-2- and C-8-substituted oligodeoxynucleotides with enhanced thrombin inhibitory activity in vitro and in vivo. J. Med. Chem. 1998, 41, 2234-2242.
14. Virgilio, A.; Esposito, V.; Citarella, G.; Pepe, A.; Mayol, L.; Galeone, A. The insertion of two 8-methyl-2′-deoxyguanosine residues in tetramolecular quadruplex structures: Trying to orientate the strands. Nucleic Acids Res. 2012, 40, 461-475.
15. Phong, L.T.T.; Virgilio, A.; Esposito, V.; Citarella, G.; Mergny, J.L.; Galeone, A. Effects of 8-methylguanine on structure, stability and kinetics of formation of tetramolecular quadruplexes. Biochimie 2011, 93, 399-408.
16. Cosconati, S.; Marinelli, L.; Trotta, R.; Virno, A.; de Tito, S.; Romagnoli, R.; Pagano, B.; Limongelli, V.; Giancola, C.; Baraldi, P.G.; et al. Structural and Conformational Requisites in DNA Quadruplex Groove Binding: Another Piece to the Puzzle. J. Am. Chem. Soc. 2010, 132, 6425-6433.
17. Martino, L.; Virno, A.; Pagano, B.; Virgilio, A.; Di Micco, S.; Galeone, A.; Giancola, C.; Bifulco, G.; Mayol, L.; Randazzo, A. Structural and thermodynamic studies of the interaction of distamycin a with the parallel quadruplex structure d(TGGGGT) (4). J. Am. Chem. Soc. 2007, 129, 16048-16056.
18. Xu, Y.; Sugiyama, H. Formation of the G-quadruplex and i-motif structures in retinoblastoma susceptibility genes (Rb). Nucleic Acids Res. 2006, 34, 949-954.
19. Kuryavyi, V.; Kettani, A.; Wang, W.M.; Jones, R.; Patel, D.J. A diamond-shaped zipper-like DNA architecture containing triads sandwiched between mismatches and tetrads. J. Mol. Biol. 2000, 295, 455-469.
20. Virgilio, A.; Esposito, V.; Randazzo, A.; Mayol, L.; Galeone, A. Effects of 8-methyl-2′-deoxyadenosine incorporation into quadruplex forming oligodeoxyribonucleotides. Bioorg. Med. Chem. 2005, 13, 1037-1044.
21. 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.
22. Amrane, S.; Ang, R.W.L.; Tan, Z.M.; Li, C.; Lim, J.K.C.; Lim, J.M.W.; Lim, K.W.; Phan, A.T. A novel chair-type G-quadruplex formed by a Bombyx mori telomeric sequence. Nucleic Acids Res. 2009, 37, 931-938.
23. Cevec, M.; Plavec, J. Role of loop residues and cations on the formation and stability of dimeric DNA G-quadruplexes. Biochemistry 2005, 44, 15238-15246.
24. Rachwal, P.A.; Brown, T.; Fox, K.R. Sequence effects of single base loops in intramolecular quadruplex DNA. FEBS Lett. 2007, 581, 1657-1660.
25. Esposito, V.; Martino, L.; Citarella, G.; Virgilio, A.; Mayol, L.; Giancola, C.; Galeone, A. Effects of abasic sites on structural, thermodynamic and kinetic properties of quadruplex structures. Nucleic Acids Res. 2010, 38, 2069-2080.
26. Skolakova, P.; Bednarova, K.; Vorlickova, M.; Sagi, J. Quadruplexes of human telomere dG(3)(TTAG(3))(3) sequences containing guanine abasic sites. Biochem. Biophys. Res. Commun. 2010, 399, 203-208.
27. Virgilio, A.; Petraccone, L.; Esposito, V.; Citarella, G.; Giancola, C.; Galeone, A. The abasic site lesions in the human telomeric sequence d[TA(G(3)T(2)A)(3)G(3)]: A thermodynamic point of view. Biochim. Biophys. Acta 2012, 1820, 2037-2043.
28. Tang, C.F.; Shafer, R.H. Engineering the quadruplex fold: Nucleoside conformation determines both folding topology and molecularity in guanine quadruplexes. J. Am. Chem. Soc. 2006, 128, 5966-5973.
29. + Solution. J. Am. Chem. Soc. 2009, 131, 2570-2578.
30. Koshkin, A.A.; Singh, S.K.; Nielsen, P.; Rajwanshi, V.K.; Kumar, R.; Meldgaard, M.; Olsen, C.E.; Wengel, J. LNA (Locked Nucleic Acids): Synthesis of the adenine, cytosine, guanine, 5-methylcytosine, thymine and uracil bicyclonucleoside monomers, oligomerisation, and unprecedented nucleic acid recognition. Tetrahedron 1998, 54, 3607-3630.
31. Singh, S.K.; Nielsen, P.; Koshkin, A.A.; Wengel, J. LNA (locked nucleic acids): Synthesis and high-affinity nucleic acid recognition. Chem. Commun. 1998, 455-456.
32. + Solution. Chem. Eur. J. 2011, 17, 2405-2413.
33. Braasch, D.A.; Corey, D.R. Locked nucleic acid (LNA): Fine-tuning the recognition of DNA and RNA. Chem. Biol. 2001, 8, 1-7.
34. Dominick, P.K.; Jarstfer, M.B. A conformationally constrained nucleotide analogue controls the folding topology of a DNA G-quadruplex. J. Am. Chem. Soc. 2004, 126, 5050-5051.
35. Randazzo, A.; Esposito, V.; Ohlenschlager, O.; Ramachandran, R.; Mayol, L. NMR solution structure of a parallel LNA quadruplex. Nucleic Acids Res. 2004, 32, 3083-3092.
36. Nielsen, J.T.; Arar, K.; Petersen, M. NMR solution structures of LNA (locked nucleic acid) modified quadruplexes. Nucleic Acids Res. 2006, 34, 2006-2014.
37. Virno, A.; Randazzo, A.; Giancola, C.; Bucci, M.; Cirinoc, G.; Mayol, L. A novel thrombin binding aptamer containing a G-LNA residue. Bioorg. Med. Chem. 2007, 15, 5710-5718.
38. Nielsen, J.T.; Arar, K.; Petersen, M. Solution Structure of a Locked Nucleic Acid Modified Quadruplex: Introducing the V4 Folding Topology. Angew. Chem. Int. Ed. Engl. 2009, 48, 3099-3103.
39. Smith, F.W.; Feigon, J. Strand orientation in the DNA quadruplex formed from the Oxytricha telomere repeat oligonucleotide d(G4T4G4) in solution. Biochemistry 1993, 32, 8682-8692.
40. Wang, Y.; Patel, D.J. Solution structure of the tetrahymena telomeric repeat d(T(2)G(4))(4) G-tetraplex. Structure 1994, 2, 1141-1156.
41. Do, N.Q.; Lim, K.W.; Teo, M.H.; Heddi, B.; Phan, A.T. Stacking of G-quadruplexes: NMR structure of a G-rich oligonucleotide with potential anti-HIV and anticancer activity. Nucleic Acids Res. 2011, 39, 9448-9457.
42. Mukundan, V.T.; Ngoc Quang, D.; Phan, A.T. HIV-1 integrase inhibitor T30177 forms a stacked dimeric G-quadruplex structure containing bulges. Nucleic Acids Res. 2011, 39, 8984-8991.
43. + Solution: Effect of Loop Length and Sequence on the Folding Topology. J. Am. Chem. Soc. 2009, 131, 16824-16831.
44. Lim, K.W.; Lacroix, L.; Yue, D.J.E.; Lim, J.K.C.; Lim, J.M.W.; Phan, A.T. Coexistence of Two Distinct G-Quadruplex Conformations in the hTERT Promoter. J. Am. Chem. Soc. 2010, 132, 12331-12342.
45. Yue, D.J.E.; Lim, K.W.; Phan, A.T. Formation of (3+1) G-Quadruplexes with a Long Loop by Human Telomeric DNA Spanning Five or More Repeats. J. Am. Chem. Soc. 2011, 133, 11462-11465.
46. Zhang, N.; Gorin, A.; Majumdar, A.; Kettani, A.; Chernichenko, N.; Skripkin, E.; Patel, D.J. V-shaped scaffold: A new architectural motif identified in an A center dot(G center dot G center dot G center dot G) pentad-containing dimeric DNA quadruplex involving stacked G(anti)center dot G(anti)center dot G(anti)center dot G(syn) tetrads. J. Mol. Biol. 2001, 311, 1063-1079.
47. Zhang, N.; Phan, A.T.; Patel, D.J. (3+1) assembly of three human telomeric repeats into an asymmetric dimeric G-quadruplex. J. Am. Chem. Soc. 2005, 127, 17277-17285.
48. Dai, J.X.; Chen, D.; Jones, R.A.; Hurley, L.H.; Yang, D.Z. NMR solution structure of the major G-quadruplex structure formed in the human BCL2 promoter region. Nucleic Acids Res. 2006, 34, 5133-5144.
49. Ambrus, A.; Chen, D.; Dai, J.X.; Jones, R.A.; Yang, D.Z. Solution structure of the biologically relevant G-quadruplex element in the human c-MYC promoter. Implications for G-quadruplex stabilization. Biochemistry 2005, 44, 2048-2058.
50. Ambrus, A.; Chen, D.; Dai, J.X.; Bialis, T.; Jones, R.A.; Yang, D.Z. Human telomeric sequence forms a hybrid-type intramolecular G-quadruplex structure with mixed parallel/antiparallel strands in potassium solution. Nucleic Acids Res. 2006, 34, 2723-2735.
51. Kettani, A.; Bouaziz, S.; Wang, W.; Jones, R.A.; Patel, D.J. Bombyx mori single repeat telomeric DNA sequence forms a G-quadruplex capped by base triads. Nat. Struct. Biol. 1997, 4, 382-389.
52. Kettani, A.; Bouaziz, S.; Gorin, A.; Zhao, H.; Jones, R.A.; Patel, D.J. Solution structure of a Na cation stabilized DNA quadruplex containing G center dot G center dot G center dot G and G center dot C center dot G center dot C tetrads formed by G-G-G-C repeats observed in adeno-associated viral DNA. J. Mol. Biol. 1998, 282, 619-636.
53. 15N NMR. J. Am. Chem. Soc. 1992, 114, 4047-4050.
54. 15N NMR To Probe Hoogsteen Hydrogen-Bonding at Guanine and Adenine N7 Atoms of a DNA Triplex. J. Am. Chem. Soc. 1995, 117, 12281-12283.
55. 1H]-NMR-spectroscopy: Combined use with isotope labeling for studies of macromolecular conformation and intermolecular interactions. Q. Rev. Biophys. 1990, 23, 39-96.
56. Zhang, N.; Gorin, A.; Majumdar, A.; Kettani, A.; Chernichenko, N.; Skripkin, E.; Patel, D.J. Dimeric DNA quadruplex containing major groove-aligned A center dot T center dot A center dot T and G center dot C center dot G center dot C tetrads stabilized by inter-subunit Watson-Crick A center dot T and G center dot C pairs. J. Mol. Biol. 2001, 312, 1073-1088.
57. Sotoya, H.; Matsugami, A.; Ikeda, T.; Ouhashi, K.; Uesugi, S.; Katahira, M. Method for direct discrimination of intra- and intermolecular hydrogen bonds, and characterization of the G(:A):G(:A):G(:A):G heptad, with scalar couplings across hydrogen bonds. Nucleic Acids Res. 2004, 32, 5113-5118.
58. Phan, A.T.; Patel, D.J. A site-specific low-enrichment N-15,C-13 isotope-labeling approach to unambiguous NMR spectral assignments in nucleic acids. J. Am. Chem. Soc. 2002, 124, 1160-1161.
59. Phan, A.T.; Patel, D.J. Differentiation between unlabeled and very-low-level fully N-15,C-13-labeled nucleotides for resonance assignments in nucleic acids. J. Biomol. NMR 2002, 23, 257-262.
60. Phan, A.T.; Modi, Y.S.; Patel, D.J. Propeller-type parallel-stranded g-quadruplexes in the human c-myc promoter. J. Am. Chem. Soc. 2004, 126, 8710-8716.
61. Phan, A.T.; Modi, Y.S.; Patel, D.J. Two-repeat Tetrahymena telomeric d(TGGGGTTGGGGT) sequence interconverts between asymmetric dimeric G-quadruplexes in solution. J. Mol. Biol. 2004, 338, 93-102.