Quadruplex DNA: Sequence, topology and structure

Nucleic Acids Research

Volumn 34, Issue 19, 2006, Pages 5402-5415

  Burge, Sarah ^a   Parkinson, Gary N ^a   Hazel, Pascale ^a   Todd, Alan K ^a   Neidle, Stephen ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; GENOMIC DNA; GUANINE; NUCLEASE; QUADRUPLEX DNA; UNCLASSIFIED DRUG;

ARTICLE; DNA SEQUENCE; DNA STRUCTURE; DRUG TARGETING; EUKARYOTE; GENE SEQUENCE; HUMAN; HYDROGEN BOND; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROMOTER REGION; RNA STRUCTURE; TELOMERE; X RAY CRYSTALLOGRAPHY;

ANIMALS; BASE SEQUENCE; DNA; GUANINE; HUMANS; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; TELOMERE;

EUKARYOTA;

EID: 33751020853     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkl655     Document Type: Article

References (107)

1. Gellert,M., Lipsett,M.N. and Davies,D.R. (1962) Helix formation by guanylic acid. Proc. Natl Acad. Sci. USA, 48, 2013-2018.
2. Zimmerman,S.B., Cohen,G.H. and Davies,D.R. (1975) X-ray fiber diffraction and model-building study of polyguanylic acid and polyinosinic acid. J. Mol. Biol., 92, 181-192.
3. Arnott,S., Chandrasekaran,R. and Marttila,C.M. (1974) Structures for polyinosinic acid and polyguanylic acid. Biochem. J., 141, 537-543.
4. Howard,F.B., Frazier,J. and Miles,H.T. (1977) Stable and metastable forms of poly(G). Biopolymers, 16, 791-809.
5. Williamson,J.R. (1994) G-tetrad structures in telomeric DNA. Ann. Rev. Biophys. Biomol. Struct., 23, 703-730.
6. Davies,J.T. (2004) G-tetrads 40 years later: From 50-GMP to molecular biology and supramolecular chemistry. Angew. Chem. Intl. Edit., 43, 668-698.
7. Sen,D. and Gilbert,W. (1988) Formation of parallel four-stranded complexes by guanine-rich motifs in DNA and its implications for meiosis. Nature, 334, 364-366.
8. Sundquist,W.I. and Klug,A. (1989) Telomeric DNA dimerizes by formation of guanine tetrads between hairpin loops. Nature, 342, 825-829.
9. Wright,W.E., Tesmer,V.M., Huffman,K.E., Levene,S.D. and Shay,J.W. (1997) Normal human chromosomes have long G-rich telomeric overhangs at one end. Genes Dev., 11, 2801-2809.
10. Sfeir,A.J., Chai,W., Shay,J.W. and Wright,W.E. (2005) Telomere-end processing the terminal nucleotides of human chromosomes. Mol. Cell, 18, 131-138.
11. Lei,M., Podell,E.M. and Cech,T.R. (2004) Structure of human POT1 bound to telomeric single-stranded DNA provides a model for chromosome end-protection. Nature Struct. Mol. Biol., 11, 1223-1229.
12. Zaug,A.J., Podell,E.R. and Cech,T.R. (2005) Human POT1 disrupts telomeric G-quadruplexes allowing telomerase extension in vitro. Proc. Natl Acad. Sci. USA, 102, 10864-10869.
13. Cech,T.R. (2004) Beginning to understand the end of the chromosome. Cell, 116, 273-279.
14. Huang,C., Lin,Y., Huang,S. and Chen,C.W. (1998) The telomeres of Streptomyces chromosomes contain conserved palindromic sequences with potential to form complex secondary structures. Mol. Microbiol., 28, 905-916.
15. Jing,N., Zhu,Q., Yuan,P., Li,Y., Mao,L. and Tweardy,D.J. (2006) Targeting signal transducer and activator of transcription 3 with G-tetrad oligonucleotides: A potential novel therapy for head and neck cancer. Mol. Cancer Ther., 5, 279-286.
16. McMicken,H.W., Bates,P.J. and Chen,Y. (2003) Antiproliferative activity of G-tetrad-containing oligonucleotides generated by a novel single-stranded DNA expression system. Cancer Gene Ther., 10, 867-869.
17. Kelly,J.A., Feigon,J. and Yeates,T.O. (1996) Reconciliation of the X-ray and NMR structures of the thrombin-binding aptamer d(GGTTGGTGTGGTTGG). J. Mol. Biol., 256, 417-422.
18. Todd,A.K., Johnston,M. and Neidle,S. (2005) Highly prevalent putative quadruplex sequence motifs in human DNA. Nucleic Acids Res., 33, 2901-2907.
19. Huppert,J.L. and Balasubramanian,S. (2005) Prevalence of quadruplexes in the human genome. Nucleic Acids Res., 33, 2901-2907.
20. Simonsson,T., Pecinka,P. and Kubista,M. (1998) DNA tetraplex formation in the control region of c-myc. Nucleic Acids Res., 26, 1167-1172.
21. Rawal,P., Kummarasetti,V.B., Ravindran,J., Kumar,N., Halder,K., Sharma,R., Mukerji,M., Das,S.K. and Chowdhury,S. (2006) Genome-wide prediction of G4 DNA as regulatory motifs: Role in Escherichia coli global regulation. Genome Res., 16, 644-655.
22. Parkinson,G.N., Lee,M.P.H. and Neidle,S. (2002) Crystal structure of parallel quadruplexes from human telomeric DNA. Nature, 417, 876-880.
23. Phan,A.T. and Patel,D.J. (2003) 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., 125, 15021-15027.
24. Phan,A.T., Modi,Y.S. and Patel,D.J. (2004) Two-repeat Tetrahymena telomeric d(TGGGGTTGGGGT) sequence interconverts between asymmetric dimeric G-quadruplexes in solution. J. Mol. Biol., 338, 93-102.
25. Kettani,A., Bouaziz,S., Gorin,A., Zhao,H., Jones,R.A. and Patel,D.J. (1998) Solution structure of a Na cation stabilized DNA quadruplex containing G.G.G.G and G.C.G.C tetrads formed by G-G-G-C repeats observed in adeno-associated viral DNA. J. Mol. Biol., 282, 619-636.
26. Hazel,P., Parkinson,G.N. and Neidle,S. (2006) Topology variation and loop structural homology in crystal and simulated structures of a bimolecular DNA quadruplex. J. Amer. Chem. Soc., 128, 5480-5487.
27. 205Tl MNR methods for the characterisation of monovalent cation binding to nucleic acids. J. Amer. Chem. Soc., 127, 16723-16732.
28. Haider,S., Parkinson,G.N. and Neidle,S. (2002) Crystal structure of the potassium form of an Oxytricha nova G-quadruplex. J. Mol. Biol., 320, 189-200.
29. Smith,F.W. and Feigon,J. (1992) Quadruplex structure of Oxytricha telomeric DNA oligonucleotides. Nature, 356, 164-168.
30. 4). Nucleic Acids Res., 27, 3018-3028.
31. Schultze,P., Smith,F.W. and Feigon,J. (1994) Refined solution structure of the dimeric quadruplex formed from the Oxytricha telomeric oligonucleotide d(GGGGTTTTGGGG). Structure, 2, 221-233.
32. Clay,E.H. and Gould,I.R. (2005) A combined QM and MM investigation into guanine quadruplexes. J. Mol. Graphics Modelling, 24, 138-146.
33. van Mourik,T. and Dingley,A.J. (2005) Characterization of the monovalent ion position and hydrogen-bond network in guanine tetrads by DFT calculations of NMR parameters. Chemistry, 7, 6064-6079.
34. Dingley,A.J., Peterson,R.D., Grzesiek,S. and Feigon,J. (2005) Characterization of the cation and temperature dependence of DNA quadruplex hydrogen bond properties using high-resolution NMR. J. Amer. Chem. Soc., 127, 14466-14472.
35. 4T). Nature, 360, 280-282.
36. Phillips,K., Dauter,Z., Murchie,A.I., Lilley,D.M. and Luisi,B. (1997) The crystal structure of a parallel-stranded guanine tetraplex at 0.95 Å resolution. J. Mol. Biol., 273, 171-182.
37. Rueda,M., Luque,F.J. and Orozco,M. (2006) G-quadruplexes can maintain their structure in the gas phase. J Amer. Chem. Soc., 128, 3608-3619.
38. 2+) ions at subatomic resolution (0.61 Å). Proc. Natl Acad. Sci. USA, 98, 13665-13670.
39. Krishnan-Ghosh,Y., Liu,D. and Balasubramanian,S. (2004) Formation of an interlocked quadruplex dimer by d(GGGT). J. Amer. Chem. Soc., 126, 11009-11016.
40. Mergny,J.-L., De Cian,A., Amrane,S. and Webba de Silva,M. (2006) Kinetics of double-chain reversals bridging contiguous tetrads in tetramolecular quadruplexes. Nucleic Acids Res., 34, 2386-2397.
41. Cmugelj,M., Sket,P. and Plavec,J. (2003) Small change in a G-rich sequence, a dramatic change in topology: New dimeric G-quadruplex folding motif with unique loop orientations. J. Am. Chem. Soc., 125, 7866-7871.
42. + ions. Bioorg. Med. Chem., 12, 5735-5744.
43. Sket,P., Crnugelj,M. and Plavec,J. (2005) Identification of mixed di-cation forms of G-quadruplex in solution. Nucleic Acids Res., 33, 3691-3697.
44. 3)2: A bimolecular G-quadruplex with a novel fold. J. Mol. Biol., 320, 911-924.
45. 3) forms an asymmetric diagonally looped dimeric G-quadruplex with guanosine 5′-syn-syn-anti and 5′-syn-anti-anti N-glycosidic conformations. Proc. Natl Acad. Sci. USA, 91, 10546-10550.
46. 2 quadruplex via particle mesh Ewald molecular dynamics simulations. Biophys. J., 75, 968-981.
47. Cevec,M. and Plavec,J. (2005) Role of loop residues and cations on the formation and stability of dimeric DNA G-quadruplexes. Biochemistry, 44, 15238-15246.
48. Risitano,A. and Fox,K.R. (2004) Influence of loop size on the stability of intramolecular DNA quadruplexes. Nucleic Acids Res., 32, 2598-2606.
49. Spackova,N., Berger,I. and Sponer,J. (1999) Nanosecond molecular dynamics simulations of parallel and antiparallel guanine quadruplex DNA molecules. J. Amer. Chem. Soc., 121, 5519-5534.
50. Spackova,N., Berger,I. and Sponer,J. (2001) Structural dynamics and cation interactions of DNA quadruplex molecules containing mixed guanine/ cytosine tetrads revealed by large-scale MD simulations. J. Amer. Chem. Soc., 123, 3295-3307.
51. Stefl,R., Cheatham,T.E., III, Spackova,N., Fadrna,E., Berger,I., Koca,J. and Sponer,J. (2003) Formation pathways of a guanine-quadruplex DNA revealed by molecular dynamics and thermodynamic analysis of substates. Biophys. J., 85, 1787-1804.
52. Fadrna,E., Spackova,N., Stefl,R., Koca,J., Cheatham,T.E., III and Sponer,J. (2004) Molecular dynamics simulations of guanine quadruplex loops: Advances and force field limitations. Biophys. J., 87, 227-242.
53. Hazel,P., Parkinson,G.N. and Neidle,S. (2006) Predictive modelling of topology and loop variations in dimeric DNA quadruplex structures. Nucleic Acids Res., 34, 2117-2127.
54. 3] G-tetraplex. Structure, 1, 263-282.
55. Phan,A.T., Kuryavyi,V., Ma,J.B., Faure,A., Andreola,M.L. and Patel,D.J. (2005) An interlocked dimeric parallel-stranded DNA quadruplex: A potent inhibitor of HIV-1 integrase. Proc. Natl Acad. Sci. USA, 102, 634-639.
56. 4 G-tetraplex. Structure, 2, 1141-1156.
57. Kuryavyi,V., Majumdar,A., Shallop,A., Chernichenko,N., Skripkin,E., Jones,R. and Patel,D.J. (2001) A double chain reversal loop and two diagonal loops define the architecture of a unimolecular DNA quadruplex containing a pair of stacked G(syn)-G(syn)-G(anti)-G(anti) tetrads flanked by a G-(T-T) Triad and a T-T-T triple. J. Mol. Biol., 310, 181-194.
58. Petraccone,L., Erra,E., Esposito,V., Randazzo,A., Mayol,L., Nasti,L., Barone,G. and Giancola,C. (2004) Stability and structure of telomeric DNA sequences forming quadruplexes containing four G-tetrads with different topological arrangements. Biochemistry, 43, 4877-4884.
59. Hazel,P., Huppert,J., Balasubramanian,S. and Neidle,S. (2004) Loop-length-dependent folding of G-quadruplexes. J. Amer. Chem. Soc., 1286, 16405-16415.
60. Olsen,C.M., Gmeiner,W.H. and Marky,L.A. (2006) Unfolding of G-quadruplexes: Energetic, and ion and water contributions of G-tetrad stacking. J. Phys. Chem. B, 110, 6962-6969.
61. Tang,C.F. and Shafer,R.H. (2006) Engineering the quadruplex fold: nucleoside conformation determines both folding topology and molecularity in guanine quadruplexes. J. Amer. Chem. Soc., 128, 5966-5973.
62. de Lange,T. (2005) Shelterin: The protein complex that shapes and safeguards human telomeres. Genes Dev., 19, 2100-2110.
63. Phan,A.T. and Mergny,J.L (2002) Human telomeric DNA: G-quadruplex, i-motif and Watson-Crick double helix. Nucleic Acids Res., 30, 4618-4625.
64. Marathias,V.M. and Bolton,P.H. (1999) Determinants of DNA quadruplex structural type: Sequence and potassium binding. Biochemistry, 38, 4355-4364.
65. Risitano,A. and Fox,K.R. (2005) Inosine substitutions demonstrate that intramolecular DNA quadruplexes adopt different conformations in the presence of sodium and potassium. Bioorg. Med. Chem. Lett., 15, 2047-2050.
66. Rujan,I.N., Meleney,J.C. and Bolton,P.H. (2005) Vertebrate telomere repeat DNAs favor external loop propeller quadruplex structures in the presence of high concentrations of potassium. Nucleic Acids Res., 33, 2022-2031.
67. Ying,L., Green,J.J., Li,H., Klenerman,D. and Balasubramanian,S. (2003) Studies on the structure and dynamics of the human telomeric G quadruplex by single-molecule fluorescence resonance energy transfer. Proc. Natl Acad. Sci. USA, 100, 14629-14634.
68. Lee,J.Y., Okumus,B., Kim,D.S. and Ha,T. (2005) Extreme conformational diversity in human telomeric DNA. Proc. Natl Acad. Sci. USA, 102, 18934-18943.
69. Zhan,N, Phan,A.T. and Patel,D.J. (2005) (3+1) assembly of three human telomeric repeats into an asymmetric dimeric G-quadruplex. J. Amer. Chem. Soc., 127, 17277-17285.
70. Balagurumoorthy,P. and Brahmachari,S.K. (1994) Structure and stability of human telomeric sequence. J. Biol. Chem., 269, 21858-21869.
71. Li,J., Correia,J.J., Wang,L., Trent,J.O. and Chaires,J.B. (2005) Not so crystal clear: The structure of the human telomere G-quadruplex in solution differs from that present in a crystal. Nucleic Acids Res., 33, 4649-4659.
72. Chang,C.C., Chu,J.F., Kao,F.J., Chiu,Y.C., Lou,P.J., Chen,H.C. and Chang,T.C. (2006) Verification of antiparallel G-quadruplex structure in human telomeres by using two-photon excitation fluorescence lifetime imaging microscopy of the 3,6-Bis(1-methyl-4-vinylpyridinium)carbazole diiodide molecule. Anal. Chem., 78, 2810-2815.
73. + solution. Bioorg. Med. Chem., 14, 5584-5591.
74. Dapic,V., Abdomericovic,V., Marrington,R., Peberdy,J., Rodger,A., Trent,J.O. and Bates,P.J. (2003) Biophysical and biological properties of quadruplex oligodeoxyribonucleotides. Nucleic Acids Res., 31, 2097-2107.
75. 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.
76. Simonsson,T. (2001) G-quadruplex DNA structures - variations on a theme. Biol. Chem., 382, 621-628.
77. Paces,J., Pavlicek,A. and Paces,V. (2002) HERVd: Database of human endogenous retroviruses. Nucleic Acids Res., 30, 205-206.
78. Kostadinov,R., Malhotra,N., Viotti,M., Shine,R., D'Antonio,L. and Bagga,P. (2006) GRSDB: A database of quadruplex forming G-rich sequences in alternatively processed mammalian pre-mRNA sequences. Nucleic Acids Res., 34, D119-D1124.
79. Zanotti,K.J., Lackey,P.E., Evans,G.L. and Mihaela-Rita,M. (2006) Thermodynamics of the fragile X mental retardation protein RGG box interactions with G tetrad forming RNA. Biochemistry, 45, 8319-8330.
80. Eddy,J. and Maizels,N. (2006) Gene function correlates with potential for G4 DNA formation in the human genome. Nucleic Acids Res., 34, 3887-3896.
81. Raghavan,S.C., Swanson,P.C., Wu,X., Hsieh,C.-L. and Lieber,M.R. (2004) A non-B-DNA structure at the bcl-2 major breakpoint region is cleaved by the RAG complex. Nature, 428, 88-93.
82. Bonaglia,M.C., Giorda,R., Mani,E., Aceti,G., Anderlid,B.M., Baroncini,A., Pramparo,T. and Zuffardi,O. (2005) Identification of a recurrent breakpoint within the SHANK3 gene in the 22q13.3 deletion syndrome. J. Med. Genetics, doi:10.1136/jmg.2005.038604.
83. 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.
84. Liu,W., Sun,D. and Hurley,L.H. (2005) Binding of G-quadruplex-interactive agents to distinct G-quadruplexes induces different biological effects in MiaPaCa cells. Nucleosides Nucleotides Nucleic Acids, 24, 1801-1815.
85. Shafer,R.H. and Smirnov,I. (2000) Biological aspects of DNA/RNA quadruplexes. Biopolymers, 56, 209-227.
86. Simonsson,T. and Sjoback,R. (1999) DNA tetraplex formation studied with fluorescence resonance energy transfer. J. Biol. Chem., 274, 17379-17383.
87. Phan,AT., Modi,Y.S. and Patel,D.J. (2004) Propeller-type parallel-stranded G-quadruplexes in the human c-myc promoter. J. Amer. Chem. Soc., 126, 8710-8716.
88. Ambrus,A., Chen,D., Dai,J., Jones,R.A. and Yang,D. (2005) Solution structure of the biologically relevant G-quadruplex element in the human c-myc promoter. Implications for G-quadruplex stabilization. Biochemistry, 44, 2048-2058.
89. Phan,A.T., Kuryavyi,V., Gaw,H.Y. and Patel,D.J. (2005) Small-molecule interaction with a five-guanine-tract G-quadruplex structure from the human MYC promoter. Nature Chem. Biol., 1, 167-173.
90. 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. Amer. Chem. Soc., 127, 10584-10589.
91. Fernando,H., Reszka,A.P., Huppert,J., Ladame,S., Rankin,S., Venkitaraman,A.R., Neidle,S. and Balasubramanian,S. (2006) A conserved quadruplex motif located in a transcription activation site of the human c-kit oncogene. Biochemistry, 45, 7854-7860.
92. Sun,D., Guo,K., Rusche,J.J. and Hurley,L.H. (2005) Facilitation of a structural transition in the polypurine/polypyrimidine tract within the proximal promoter region of the human VEGF gene by the presence of potassium and G-quadruplex-interactive agents. Nucleic Acids Res., 33, 6070-6080.
93. De Armond,R., Wood,S., Sun,D., Hurley,L.H. and Ebbinghaus,S.W. (2005) Evidence for the presence of a guanine quadruplex forming region within a polypurine tract of the hypoxia inducible factor 1alpha promoter. Biochemistry, 44, 16341-16350.
94. Dai,J., Dexheimer,T.S., Chen,D., Carver,M., Ambrus,A., Jones,R.A. and Yang,D. (2006) An intramolecular G-quadruplex structure with mixed parallel/antiparallel G-strands formed in the human BCL-2 promoter region in solution. J. Amer. Chem. Soc., 128, 1096-1098.
95. Dexheimer,T.S., Sun,D. and Hurley,L.H. (2006) Deconvoluting the structural and drug-recognition complexity of the G-quadruplex-forming region upstream of the bcl-2 P1 promoter. J. Amer. Chem. Soc., 128, 5404-5415.
96. + solution: An intramolecular (3 + 1) G-quadruplex scaffold. J. Amer. Chem. Soc., 128, 9963-9970.
97. Cogio,S. and Xodo,L.E. (2006) G-quadruplex formation within the promoter of the KRAS proto-oncogene and its effect on transcription. Nucleic Acids Res., 34, 2536-2549.
98. Xu,Y. and Sugiyama,H. (2006) Formation of the G-quadruplex and i-motif structures in retinoblastoma susceptibility genes (Rb). Nucleic Acids Res., 34, 949-954.
99. Krishnan-Ghosh,Y., Stephens,E. and Balasubramanian,S. (2004) A PNA4 quadraplex. J. Amer. Chem. Soc., 126, 5944-5945.
100. Datta,B., Bier,M.E., Roy,S. and Armitage,B.A. (2005) Quadruplex formation by a guanine-rich PNA oligomer. J. Amer. Chem. Soc., 127, 4199-4207.
101. Randazzo,A., Esposito,V., Ohlenschlager,O., Ramachandran,R and Mayola,L. (2004) NMR solution structure of a parallel LNA quadruplex. Nucleic Acids Res., 32, 3083-3092.
102. Nielsen,J.T., Arar,K. and Petersen,M. (2006) NMR solution structures of LNA (locked nucleic acid) modified quadruplexes. Nucleic Acids Res., 34, 2006-2014.
103. Matsugami,A., Okuizumi,T., Uesugi,S. and Katahira,M. (2003) Intramolecular higher order packing of parallel quadruplexes comprising a G:G:G:G tetrad and a G(:A):G(:A):G(:A):G heptad of GGA triplet repeat DNA. J. Biol. Chem., 278, 28147-28153.
104. Khateb,S., Weisman-Shomer,P., Hershco,L., Loeb,L.A. and Fry,M. (2004) Destabilization of tetraplex structures of the fragile X repeat sequence (CGG)n is mediated by homolog-conserved domains in three members of the hnRNP family. Nucleic Acids Res., 32, 4145-4154.
105. Duquette,M.L., Handa,P., Vincent,J.A., Taylor,A.F. and Maizels,N. (2004) Intracellular transcription of G-rich DNAs induces formation of G-loops, novel structures containing G4 DNA. Genes Dev., 18, 1618-1629.
106. Ju,B.G., Lunyak,V.V., Perissi,V., Garcia-Bassets,I., Rose,D.W., Glass,C.K. and Rosenfeld,M.G. (2006) A topoisomerase IIβ-mediated dsDNA break required for regulated transcription. Science, 312, 1798-1802.
107. Rangan,A., Fedoroff,O.Y. and Hurley,L.H. (2001) Induction of duplex to G-quadruplex transition in the c-myc promoter region by a small molecule. J. Biol. Chem. 276, 4640-4646.