Structure of the human telomere in Na+ solution: An antiparallel (2+2) G-quadruplex scaffold reveals additional diversity

Nucleic Acids Research

Volumn 41, Issue 22, 2013, Pages 10556-10562

  Lim, Kah Wai ^a,b   Ng, Veronica Chinn Min ^a   Martín Pintado, Nerea ^a,c   Heddi, Brahim ^a   Phan, Anh Tuân ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^c INSTITUTO DE QUÍMICA FÍSICA ROCASOLANO   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

8 BROMOGUANOSINE; GUANINE QUADRUPLEX; POTASSIUM ION; SODIUM ION;

ARTICLE; CHROMOSOME POLYMORPHISM; DNA CONFORMATION; DNA FLANKING REGION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEIC ACID BASE SUBSTITUTION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TELOMERE;

DNA; G-QUADRUPLEXES; HUMANS; MODELS, MOLECULAR; REPETITIVE SEQUENCES, NUCLEIC ACID; SODIUM; TELOMERE;

EID: 84890418685     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt771     Document Type: Article

References (58)

1. Blackburn, E.H. (1991) Structure and function of telomeres. Nature, 350, 569-573.
2. Moyzis, R.K., Buckingham, J.M., Cram, L.S., Dani, M., Deaven, L.L., Jones, M.D., Meyne, J., Ratliff, R.L. and Wu, J.R. (1988) A highly conserved repetitive DNA sequence, (TTAGGG)n, present at the telomeres of human chromosomes. Proc. Natl Acad. Sci. USA, 85, 6622-6626.
3. Allshire, R.C., Dempster, M. and Hastie, N.D. (1989) Human telomeres contain at least three types of G-rich repeat distributed non-randomly. Nucleic Acids Res., 17, 4611-4627.
4. Makarov, V.L., Hirose, Y. and Langmore, J.P. (1997) Long G tails at both ends of human chromosomes suggest a C strand degradation mechanism for telomere shortening. Cell, 88, 657-666.
5. Simonsson, T. (2001) G-quadruplex DNA structures-Variations on a theme. Biol. Chem., 382, 621-628.
6. Davis, J.T. (2004) G-quartets 40 years later: From 50-GMP to molecular biology and supramolecular chemistry. Angew. Chem. Int. Ed., 43, 668-698.
7. 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.
8. Patel, D.J., Phan, A.T. and Kuryavyi, V. (2007) Human telomere, oncogenic promoter and 50-UTR G-quadruplexes: Diverse higher order DNA and RNA targets for cancer therapeutics. Nucleic Acids Res., 35, 7429-7455.
9. Zahler, A.M., Williamson, J.R., Cech, T.R. and Prescott, D.M. (1991) Inhibition of telomerase by G-quartet DNA structures. Nature, 350, 718-720.
10. Counter, C.M., Avilion, A.A., Lefeuvre, C.E., Stewart, N.G., Greider, C.W., Harley, C.B. and Bacchetti, S. (1992) Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J., 11, 1921-1929.
11. Kim, N.W., Piatyszek, M.A., Prowse, K.R., Harley, C.B., West, M.D., Ho, P.L.C., Coviello, G.M., Wright, W.E., Weinrich, S.L. and Shay, J.W. (1994) Specific association of human telomerase activity with immortal cells and cancer. Science, 266, 2011-2015.
12. Neidle, S. and Parkinson, G. (2002) Telomere maintenance as a target for anticancer drug discovery. Nat. Rev. Drug Discov., 1, 383-393.
13. De Cian, A., Lacroix, L., Douarre, C., Temime-Smaali, N., Trentesaux, C., Riou, J.F. and Mergny, J.L. (2008) Targeting telomeres and telomerase. Biochimie, 90, 131-155.
14. Phan, A.T. (2010) Human telomeric G-quadruplex: structures of DNA and RNA sequences. FEBS J., 277, 1107-1117.
15. 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.
16. Dai, J.X., Punchihewa, C., Ambrus, A., Chen, D., Jones, R.A. and Yang, D.Z. (2007) Structure of the intramolecular human telomeric G-quadruplex in potassium solution: A novel adenine triple formation. Nucleic Acids Res., 35, 2440-2450.
17. Matsugami, A., Xu, Y., Noguchi, Y., Sugiyama, H. and Katahira, M. (2007) Structure of a human telomeric DNA sequence stabilized by 8-bromoguanosine substitutions, as determined by NMR in a K+ solution. FEBS J., 274, 3545-3556.
18. 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.
19. Dai, J.X., Carver, M., Punchihewa, C., Jones, R.A. and Yang, D.Z. (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.
20. Lim, K.W., Amrane, S., Bouaziz, S., Xu, W.X., Mu, Y.G., 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.
21. Parkinson, G.N., Lee, M.P.H. and Neidle, S. (2002) Crystal structure of parallel quadruplexes from human telomeric DNA. Nature, 417, 876-880.
22. Heddi, B. and Phan, A.T. (2011) Structure of human telomeric DNA in crowded solution. J. Am. Chem. Soc., 133, 9824-9833.
23. Wang, Y. and Patel, D.J. (1993) Solution structure of the human telomeric repeat d[AG3(T2AG3)3] G-tetraplex. Structure, 1, 263-282.
24. Xue, Y., Kan, Z.Y., Wang, Q., Yao, Y., Liu, J., Hao, Y.H. and Tan, Z. (2007) Human telomeric DNA forms parallel-stranded intramolecular G-quadruplex in K+ solution under molecular crowding condition. J. Am. Chem. Soc., 129, 11185-11191.
25. Lannan, F.M., Mamajanov, I. and Hud, N.V. (2012) Human telomere sequence DNA in water-free and high-viscosity solvents: G-quadruplex folding governed by Kramers rate theory. J. Am. Chem. Soc., 134, 15324-15330.
26. Yu, H.Q., Gu, X.B., Nakano, S., Miyoshi, D. and Sugimoto, N. (2012) Beads-on-a-string structure of long telomeric DNAs under molecular crowding conditions. J. Am. Chem. Soc., 134, 20060-20069.
27. Tran, P.L.T., Mergny, J.L. and Alberti, P. (2011) Stability of telomeric G-quadruplexes. Nucleic Acids Res., 39, 3282-3294.
28. Renciuk, D., Kejnovska, I., S kolaova, P., Bednarova, K., Motlova, J. and VorlkovaM. (2009) Arrangements of human telomere DNA quadruplex in physiologically relevant K+ solutions. Nucleic Acids Res., 37, 6625-6634.
29. 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.
30. Mendez, M.A. and Szalai, V.A. (2009) Fluorescence of unmodified oligonucleotides: A tool to probe G-quadruplex DNA structure. Biopolymers, 91, 841-850.
31. Dao, N.T., Haselsberger, R., Michel-Beyerle, M.E. and Phan, A.T. (2011) Following G-quadruplex formation by its intrinsic fluorescence. FEBS Lett., 585, 3969-3977.
32. Palacky, J., Vorlkova, M., Kejnovska, I. and Mojzes, P. (2013) Polymorphism of human telomeric quadruplex structure controlled by DNA concentration: A Raman study. Nucleic Acids Res., 41, 1005-1016.
33. Singh, V., Azarkh, M., Exner, T.E., Hartig, J.S. and Drescher, M. (2009) Human telomeric quadruplex conformations studied by pulsed EPR. Angew. Chem. Int. Ed., 48, 9728-9730.
34. Adrian, M., Heddi, B. and Phan, A.T. (2012) NMR spectroscopy of G-quadruplexes. Methods, 57, 11-24.
35. Smargiasso, N., Rosu, F., Hsia, W., Colson, P., Baker, E.S., Bowers, M.T., De Pauw, E. and Gabelica, V. (2008) G-quadruplex DNA assemblies: Loop length, cation identity, and multimer formation. J. Am. Chem. Soc., 130, 10208-10216.
36. Gaynutdinov, T.I., Neumann, R.D. and Panyutin, I.G. (2008) Structural polymorphism of intramolecular quadruplex of human telomeric DNA: Effect of cations, quadruplex-binding drugs and flanking sequences. Nucleic Acids Res., 36, 4079-4087.
37. Ying, L.M., Green, J.J., Li, H.T., 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.
38. Lee, J.Y., Okumus, B., Kim, D.S. and Ha, T.J. (2005) Extreme conformational diversity in human telomeric DNA. Proc. Natl Acad. Sci. USA, 102, 18938-18943.
39. Koirala, D., Ghimire, C., Bohrer, C., Sannohe, Y., Sugiyama, H. and Mao, H.B. (2013) Long-loop G-quadruplexes are misfolded population minorities with fast transition kinetics in human telomeric sequences. J. Am. Chem. Soc., 135, 2235-2241.
40. Petraccone, L., Spink, C., Trent, J.O., Garbett, N.C., Mekmaysy, C.S., Giancola, C. and Chaires, J.B. (2011) Structure and stability of higher-order human telomeric quadruplexes. J. Am. Chem. Soc., 133, 20951-20961.
41. Cang, X.H., S poner, J. and Cheatham, 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.
42. Cantor, C.R., Warshaw, M.M. and Shapiro, H. (1970) Oligonucleotide interactions. III. Circular dichroism studies of conformation of deoxyoligonucleotides. Biopolymers, 9, 1059-1077.
43. Mergny, J.L., Phan, A.T. and Lacroix, L. (1998) Following G-quartet formation by UV-spectroscopy. FEBS Lett., 435, 74-78.
44. Phan, A.T. and Patel, D.J. (2002) A site-specific low-enrichment 15N, 13C isotope-labeling approach to unambiguous NMR spectral assignments in nucleic acids. J. Am. Chem. Soc., 124, 1160-1161.
45. Huang, X.N., Yu, P.L., LeProust, E. and Gao, X.L. (1997) An efficient and economic site-specific deuteration strategy for NMR studies of homologous oligonucleotide repeat sequences. Nucleic Acids Res., 25, 4758-4763.
46. Phan, A.T. (2000) Long-range imino proton-13C J-couplings and the through-bond correlation of imino and nonexchangeable protons in unlabeled DNA.J. Biomol. NMR, 16, 175-178.
47. Phan, A.T., Gueon, M. and Leroy, J.L. (2002) Investigation of unusual DNA motifs. Methods Enzymol., 338, 341-371.
48. Schwieters, C.D., Kuszewski, J.J., Tjandra, N. and Clore, G.M. (2003) The Xplor-NIH NMR molecular structure determination package. J. Magn. Reson., 160, 65-73.
49. DeLano, W.L. and Bromberg, S. (2004) PyMOL User's Guide. DeLano Scientific LLC, San Carlos, California, USA.
50. Gray, D.M., Wen, J.D., Gray, C.W., Repges, R., Repges, C., Raabe, G. and Fleischhauer, J. (2008) Measured and calculated CD spectra of G-quartets stacked with the same or opposite polarities. Chirality, 20, 431-440.
51. Xu, Y., Noguchi, Y. and Sugiyama, H. (2006) The new models of the human telomere d[AGGG(TTAGGG)3] in K+ solution. Bioorgan Med Chem, 14, 5584-5591.
52. Smith, F.W., Lau, F.W. and Feigon, J. (1994) d(G3T4G3) forms an asymmetric diagonally looped dimeric quadruplex with guanosine 50-syn-syn-anti and 50-syn-anti-anti N-glycosidic conformations. Proc. Natl Acad. Sci. USA, 91, 10546-10550.
53. Strahan, G.D., Shafer, R.H. and Keniry, M.A. (1994) Structural properties of the [d(G3T4G3)]2 quadruplex: Evidence for sequential syn-syn deoxyguanosines. Nucleic Acids Res., 22, 5447-5455.
54. C rnugelj, M., Hud, N.V. and Plavec, J. (2002) The solution structure of d(G4T4G3)2: A bimolecular G-quadruplex with a novel fold. J. Mol. Biol., 320, 911-924.
55. C rnugelj, 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.
56. da Silva, M.W., Trajkovski, M., Sannohe, Y., Hessari, N.M., Sugiyama, H. and Plavec, J. (2009) Design of a G-quadruplex topology through glycosidic bond angles. Angew. Chem. Int. Ed., 48, 9167-9170.
57. Marusic, M., S ket, P., Bauer, L., Viglasky, V. and Plavec, J. (2012) Solution-state structure of an intramolecular G-quadruplex with propeller, diagonal and edgewise loops. Nucleic Acids Res., 40, 6946-6956.
58. 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.