Structure of long human telomeric RNA (TERRA): G-quadruplexes formed by four and eight UUAGGG repeats are stable building blocks

Biochemistry

Volumn 50, Issue 29, 2011, Pages 6455-6461

  Martadinata, Herry ^a,b   Heddi, Brahim ^a   Lim, Kah Wai ^a,b   Phan, Anh Tuân ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

BUILDING BLOCKES; G-QUADRUPLEXES; MOLECULAR DYNAMICS SIMULATIONS; PROTECTION ASSAY; STACKING CONFORMATIONS;

MOLECULAR DYNAMICS; RNA;

DNA SEQUENCES;

ADENINE; GUANINE; GUANINE QUADRUPLEX; RIBONUCLEASE T1; RNA; URACIL;

ARTICLE; CHROMOSOME STRUCTURE; CONTROLLED STUDY; ENZYME ASSAY; HUMAN; MOLECULAR DYNAMICS; NUCLEOTIDE REPEAT; PRIORITY JOURNAL; PROTEIN DEGRADATION; RNA CONFORMATION; RNA STABILITY; RNA STRUCTURE; SIMULATION; TELOMERE;

BASE SEQUENCE; CIRCULAR DICHROISM; G-QUADRUPLEXES; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; POTASSIUM; REPETITIVE SEQUENCES, NUCLEIC ACID; RIBONUCLEASE T1; RNA; SOLUTIONS; TELOMERE;

EID: 79960516726     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200569f     Document Type: Article

References (47)

1. Davis, J. T. (2004) G-quartets 40 years later: from 5′-GMP to molecular biology and supramolecular chemistry Angew. Chem., Int. Ed. 43, 668-698 (Pubitemid 38197045)
2. Patel, D. J., Phan, A. T., and Kuryavyi, V. (2007) Human telomere, oncogenic promoter and 5′-UTR G-quadruplexes: diverse higher order DNA and RNA targets for cancer therapeutics Nucleic Acids Res. 35, 7429-7455
3. Neidle, S. (2009) The structures of quadruplex nucleic acids and their drug complexes Curr. Opin. Struct. Biol. 19, 239-250
4. Maizels, N. (2006) Dynamic roles for G4 DNA in the biology of eukaryotic cells Nat. Struct. Mol. Biol. 13, 1055-1059 (Pubitemid 44885914)
5. De Cian, A., Lacroix, L., Douarre, C., Temimesmaali, N., Trentesaux, C., Riou, J., and Mergny, J. (2008) Targeting telomeres and telomerase Biochimie 90, 131-155 (Pubitemid 350245369)
6. Simonsson, T., Pecinka, P., and Kubista, M. (1998) DNA tetraplex formation in the control region of c-myc Nucleic Acids Res. 26, 1167-1172 (Pubitemid 28291685)
7. 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. U.S.A. 99, 11593-11598 (Pubitemid 34994444)
8. 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 Nat. Chem. Biol. 3, 218-221 (Pubitemid 46440536)
9. Azzalin, C., Reichenbach, P., Khoriauli, L., Giulotto, E., and Lingner, J. (2007) Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends Science 318, 798-801 (Pubitemid 351411771)
10. Schoeftner, S. and Blasco, M. A. (2008) Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II Nat. Cell Biol. 10, 228-236 (Pubitemid 351194053)
11. Luke, B., Panza, A., Redon, S., Iglesias, N., Li, Z., and Lingner, J. (2008) The Rat1p 5′ to 3′ exonuclease degrades telomeric repeat-containing RNA and promotes telomere elongation in Saccharomyces cerevisiae Mol. Cell 32, 465-477
12. Caslini, C., Connelly, J. A., Serna, A., Broccoli, D., and Hess, J. L. (2009) MLL associates with telomeres and regulates telomeric repeat-containing RNA transcription Mol. Cell. Biol. 29, 4519-4526
13. Redon, S., Reichenbach, P., and Lingner, J. (2010) The non-coding RNA TERRA is a natural ligand and direct inhibitor of human telomerase Nucleic Acids Res. 38, 5797-5806
14. Deng, Z., Norseen, J., Wiedmer, A., Riethman, H., and Lieberman, P. M. (2009) TERRA RNA binding to TRF2 facilitates heterochromatin formation and ORC recruitment at telomeres Mol. Cell 35, 403-413
15. Deng, Z., Campbell, A., and Lieberman, P. (2010) TERRA, CpG methylation and telomere heterochromatin: lessons from ICF syndrome cells Cell Cycle 9, 69-74
16. Horard, B. and Gilson, E. (2008) Telomeric RNA enters the game Nat. Cell Biol. 10, 113-115 (Pubitemid 351194036)
17. Luke, B. and Lingner, J. (2009) TERRA: telomeric repeat-containing RNA EMBO J. 28, 2503-2510
18. Feuerhahn, S., Iglesias, N., Panza, A., Porro, A., and Lingner, J. (2010) TERRA biogenesis, turnover and implications for function FEBS Lett. 584, 3812-3818
19. Qi, J. and Shafer, R. (2007) Human telomere quadruplex: refolding and selection of individual conformers via RNA/DNA chimeric editing Biochemistry 46, 7599-7606 (Pubitemid 46986384)
20. + solution J. Am. Chem. Soc. 130, 11179-11184
21. + solution J. Am. Chem. Soc. 131, 2570-2578
22. Randall, A. and Griffith, J. D. (2009) Structure of long telomeric RNA transcripts: The G-rich RNA forms a compact repeating structure containing G-quartets J. Biol. Chem. 284, 13980-13986
23. Arora, A. and Maiti, S. (2009) Differential biophysical behavior of human telomeric RNA and DNA quadruplex J. Phys. Chem. B 113, 10515-10520
24. Joachimi, A., Benz, A., and Hartig, J. S. (2009) A comparison of DNA and RNA quadruplex structures and stabilities Bioorg. Med. Chem. 17, 6811-6815
25. Collie, G. W., Haider, S. M., Neidle, S., and Parkinson, G. N. (2010) A crystallographic and modelling study of a human telomeric RNA (TERRA) quadruplex Nucleic Acids Res. 38, 5569-5580
26. Collie, G. W., Parkinson, G. N., Neidle, S., Rosu, F., De Pauw, E., and Gabelica, V. (2010) Electrospray mass spectrometry of telomeric RNA (TERRA) reveals the formation of stable multimeric G-quadruplex structures J. Am. Chem. Soc. 132, 9328-9334
27. Zhang, D.-H., Fujimoto, T., Saxena, S., Yu, H.-Q., Miyoshi, D., and Sugimoto, N. (2010) Monomorphic RNA G-quadruplex and polymorphic DNA G-quadruplex structures responding to cellular environmental factors Biochemistry 49, 4554-4563
28. Xu, Y., Suzuki, Y., Ito, K., and Komiyama, M. (2010) Telomeric repeat-containing RNA structure in living cells Proc. Nat. Acad. Sci. U.S.A. 107, 14579-14584
29. Phan, A. T. (2010) Human telomeric G-quadruplex: structures of DNA and RNA sequences FEBS J. 277, 1107-1117
30. Xu, Y., Ishizuka, T., Kurabayashi, K., and Komiyama, M. (2009) Consecutive formation of G-quadruplexes in human telomeric-overhang DNA: a protective capping structure for telomere ends Angew. Chem., Int. Ed. 48, 7833-7836
31. Parkinson, G., Lee, M., and Neidle, S. (2002) Crystal structure of parallel quadruplexes from human telomeric DNA Nature 417, 876-880 (Pubitemid 34670337)
32. Vorlícková, M., Chládková, J., Kejnovská, I., Fialová, M., and Kypr, J. (2005) Guanine tetraplex topology of human telomere DNA is governed by the number of (TTAGGG) repeats Nucleic Acids Res. 33, 5851-5860 (Pubitemid 41742604)
33. Yu, H., Miyoshi, D., and Sugimoto, N. (2006) Characterization of structure and stability of long telomeric DNA G-quadruplexes J. Am. Chem. Soc. 128, 15461-15468 (Pubitemid 44876022)
34. Pomerantz, A. K., Moerner, W. E., and Kool, E. T. (2008) Visualization of long human telomere mimics by single-molecule fluorescence imaging J. Phys. Chem. B 112, 13184-13187
35. Stansel, R. M., de Lange, T., and Griffith, J. D. (2001) T-loop assembly in vitro involves binding of TRF2 near the 3′ telomeric overhang EMBO J. 20, 5532-5540 (Pubitemid 32959473)
36. Plateau, P. and Gueron, M. (1982) Exchangeable proton NMR without base-line distortion using new strong pulse sequences J. Am. Chem. Soc. 104, 7310-7311
37. Phan, A. T., Gueron, M., and Leroy, J. L. (2001) Investigation of unusual DNA motifs Methods Enzymol. 338, 341-371 (Pubitemid 32666587)
38. Case, D. A., Cheatham, T. E., III, Darden, T., Gohlke, H., Luo, R., Merz, K. M., Jr., Onufriev, A., Simmerling, C., Wang, B., and Woods, R. J. (2005) The Amber biomolecular simulation programs J. Comput. Chem. 26, 1668-1688 (Pubitemid 43076180)
39. Perez, A., Marchan, I., Svozil, D., Sponer, J., Cheatham, T. E., III, Laughton, C. A., and Orozco, M. (2007) Refinement of the AMBER force field for nucleic acids: improving the description of alpha/gamma conformers Biophys. J. 92, 3817-3829 (Pubitemid 46910569)
40. DeLano, W. L. (2002) The PyMOL Users Manual, DeLano Scientific, Palo Alto, CA.
41. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79, 926-935
42. Berendsen, H. J. C., Postma, J. P. M., Vangunsteren, W. F., Dinola, A., and Haak, J. R. (1984) Molecular-Dynamics with coupling to an external bath J. Chem. Phys. 81, 3684-3690
43. Vangunsteren, W. F. and Berendsen, H. J. C. (1977) Algorithms for macromolecular dynamics and constraint dynamics Mol. Phys. 34, 1311-1327
44. Darden, T., York, D., and Pedersen, L. (1993) Particle Mesh Ewald-an N.Log(N) Method for Ewald sums in large systems J. Chem. Phys. 98, 10089-10092
45. Balagurumoorthy, P., Brahmachari, S. K., Mohanty, D., Bansal, M., and Sasisekharan, V. (1992) Hairpin and parallel quartet structures for telomeric sequences Nucleic Acids Res. 20, 4061-4067
46. Kuryavyi, V., Phan, A. T., and Patel, D. J. (2010) Solution structures of all parallel-stranded monomeric and dimeric G-quadruplex scaffolds of the human c-kit2 promoter Nucleic Acids Res. 38, 6757-6773
47. Shinohara, K., Sannohe, Y., Kaieda, S., Tanaka, K., Osuga, H., Tahara, H., Xu, Y., Kawase, T., Bando, T., and Sugiyama, H. (2010) A chiral wedge molecule inhibits telomerase activity J. Am. Chem. Soc. 132, 3778-3782