Single-molecule analysis of thymine dimer-containing G-quadruplexes formed from the human telomere sequence

Biochemistry

Volumn 53, Issue 48, 2014, Pages 7484-7493

  Wolna, Anna H ^a   Fleming, Aaron M ^a   Burrows, Cynthia J ^a  

^a UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAINS; CIRCULAR DICHROISM SPECTROSCOPY; DICHROISM; DIMERS; ELECTROPHORETIC MOBILITY; EXPERIMENTS; MOLECULES; PROPELLERS; THERMODYNAMIC STABILITY;

BIOLOGICAL SIGNIFICANCE; CIRCULAR DICHROISM SPECTRA; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENOME STABILITY; HUMAN TELOMERE SEQUENCES; ION-CHANNEL RECORDING; SINGLE-MOLECULE ANALYSIS; STRUCTURAL DIFFERENCES;

CHROMOSOMES;

ALPHA HEMOLYSIN; GUANINE QUADRUPLEX; THYMINE; BACTERIAL TOXIN; HEMOLYSIN; PYRIMIDINE DIMER; STAPHYLOCOCCAL ALPHA-TOXIN;

ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; GEL MOBILITY SHIFT ASSAY; GENE SEQUENCE; MELTING POINT; MOLECULAR STABILITY; PROTEIN ANALYSIS; PROTEIN STRUCTURE; TELOMERE; THERMAL ANALYSIS; THERMODYNAMICS; THERMOSTABILITY; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; DNA DAMAGE; GENETICS; HUMAN; NANOPORE; NUCLEOTIDE SEQUENCE; RADIATION RESPONSE; ULTRAVIOLET RADIATION;

BACTERIAL TOXINS; BASE SEQUENCE; CIRCULAR DICHROISM; DNA DAMAGE; ELECTROPHORETIC MOBILITY SHIFT ASSAY; G-QUADRUPLEXES; HEMOLYSIN PROTEINS; HUMANS; MODELS, MOLECULAR; NANOPORES; NUCLEIC ACID CONFORMATION; PYRIMIDINE DIMERS; TELOMERE; ULTRAVIOLET RAYS;

EID: 84916634278     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi501072m     Document Type: Article

References (64)

1. Roderick, J. O. S. and Jan, K. (2010) Telomeres: Protecting chromosomes against genome instability Nat. Rev. Mol. Cell Biol. 11, 171-181
2. Osterhage, J. L. and Friedman, K. L. (2009) Chromosome end maintenance by telomerase J. Biol. Chem. 284, 16061-16065
3. n, present at the telomeres of human chromosomes Proc. Natl. Acad. Sci. U.S.A. 85, 6622-6626
4. Biffi, G., Tannahill, D., McCafferty, J., and Balasubramanian, S. (2013) Quantitative visualization of DNA G-quadruplex structures in human cells Nat. Chem. 5, 182-183
5. 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
6. Cahoon, L. A. and Seifert, H. S. (2009) An alternative DNA structure is necessary for pilin antigenic variation in Neisseria gonorrhoeae Science 325, 764-767
7. Rodriguez, R., Miller, K. M., Forment, J. V., Bradshaw, C. R., Nikan, M., Britton, S., Oelschlaegel, T., Xhemalce, B., Balasubramanian, S., and Jackson, S. P. (2012) Small-molecule-induced DNA damage identifies alternative DNA structures in human genes Nat. Chem. Biol. 8, 301-310
8. Cheung, I., Schertzer, M., Rose, A., and Lansdorp, P. M. (2002) Disruption of dog-1 in Caenorhabditis elegans triggers deletions upstream of guanine-rich DNA Nat. Genet. 31, 405-409
9. 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
10. Osterhage, J. L. and Friedman, K. L. (2009) Chromosome end maintenance by telomerase J. Biol. Chem. 284, 16061-16065
11. Xu, Y. (2011) Chemistry in human telomere biology: Structure, function and targeting of telomere DNA/RNA Chem. Soc. Rev. 40, 2719-2740
12. + solution Nucleic Acids Res. 35, 6517-6525
13. 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
14. + solution Bioorg. Med. Chem. 14, 5584-5591
15. 3] G-tetraplex Structure 1, 263-282
16. Parkinson, G. N., Lee, M. P. H., and Neidle, S. (2002) Crystal structure of parallel quadruplexes from human telomeric DNA Nature 417, 876-880
17. Heddi, B. and Phan, A. T. (2011) Structure of human telomeric DNA in crowded solution J. Am. Chem. Soc. 133, 9824-9833
18. Gray, R. D., Buscaglia, R., and Chaires, J. B. (2012) Populated intermediates in the thermal unfolding of the human telomeric quadruplex J. Am. Chem. Soc. 134, 16834-16844
19. 3 J. Am. Chem. Soc. 132, 17105-17107
20. 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
21. Yang, D. and Okamoto, K. (2010) Structural insights into G-quadruplexes: Towards new anticancer drugs Future Med. Chem. 2, 619-646
22. Lane, A. N., Chaires, J. B., Gray, R. D., and Trent, J. O. (2008) Stability and kinetics of G-quadruplex structures Nucleic Acids Res. 36, 5482-5515
23. Hänsel, R., Löhr, F., Foldynová-Trantírková, S., Bamberg, E., Trantírek, L., and Dötsch, V. (2011) The parallel G-quadruplex structure of vertebrate telomeric repeat sequences is not the preferred folding topology under physiological conditions Nucleic Acids Res. 39, 5768-5775
24. Ray, S., Bandaria, J. N., Qureshi, M. H., Yildiz, A., and Balci, H. (2014) G-quadruplex formation in telomeres enhances POT1/TPP1 protection against RPA binding Proc. Natl. Acad. Sci. U.S.A. 111, 2990-2995
25. He, Q., Zeng, P., Tan, J.-H., Ou, T.-M., Gu, L.-Q., Huang, Z.-S., and Li, D. (2014) G-quadruplex-mediated regulation of telomere binding protein POT1 gene expression Biochim. Biophys. Acta 1840, 2222-2233
26. Song, L., Hobaugh, M. R., Shustak, C., Cheley, S., Bayley, H., and Gouaux, J. E. (1996) Structure of Staphylococcal α-hemolysin, a heptameric transmembrane pore Science 274, 1859-1865
27. Rochette, P. J. and Brash, D. E. (2010) Human telomeres are hypersensitive to UV-induced DNA damage and refractory to repair PLoS Genet. 6, e1000926
28. 2+-mediated Fenton reactions has possible biological implications J. Biol. Chem. 274, 962-971
29. Oikawa, S., Tada-Oikawa, S., and Kawanishi, S. (2001) Site-specific DNA damage at the GGG sequence by UVA involves acceleration of telomere shortening Biochemistry 40, 4763-4768
30. Verdun, R. E. and Karlseder, J. (2007) Replication and protection of telomeres Nature 447, 924-931
31. Samassekou, O., Gadji, M., Drouin, R., and Yan, J. (2010) Sizing the ends: Normal length of human telomeres Ann. Anat. 192, 284-291
32. Wolkowitz, O. M., Mellon, S. H., Epel, E. S., Lin, J., Dhabhar, F. S., Su, Y., Reus, V. I., Rosser, R., Burke, H. M., Kupferman, E., Compagnone, M., Nelson, J. C., and Blackburn, E. H. (2011) Leukocyte telomere length in major depression: Correlations with chronicity, inflammation and oxidative stress - preliminary findings PLoS One 6, e17837
33. Steenken, S. and Jovanovic, S. (1997) How easily oxidizable is DNA? One-electron reduction potentials of adenosine and guanosine radicals in aqueous solution J. Am. Chem. Soc. 119, 617-618
34. Burrows, C. J. and Muller, J. G. (1998) Oxidative nucleobase modifications leading to strand scission Chem. Rev. 98, 1109-1152
35. Fleming, A. M. and Burrows, C. J. (2013) G-quadruplex folds of the human telomere sequence alter the site reactivity and reaction pathway of guanine oxidation compared to duplex DNA Chem. Res. Toxicol. 26, 593-607
36. Zhou, J., Liu, M., Fleming, A. M., Burrows, C. J., and Wallace, S. S. (2013) Neil3 and NEIL1 DNA glycosylases remove oxidative damages from quadruplex DNA and exhibit preferences for lesions in the telomeric sequence context J. Biol. Chem. 288, 27263-27272
37. Fleming, A. M., Orendt, A. M., He, Y., Zhu, J., Dukor, R. K., and Burrows, C. J. (2013) Reconciliation of chemical, enzymatic, spectroscopic and computational data to assign the absolute configuration of the DNA base lesion spiroiminodihydantoin J. Am. Chem. Soc. 135, 18191-18204
38. Aggrawal, M., Joo, H., Liu, W., Tsai, J., and Xue, L. (2012) 8-Oxo-7,8-dihydrodeoxyadenosine: The first example of a native DNA lesion that stabilizes human telomeric G-quadruplex DNA Biochem. Biophys. Res. Commun. 421, 671-677
39. Sinha, R. P. and Hader, D. P. (2002) UV-induced DNA damage and repair: A review Photochem. Photobiol. Sci. 1, 225-236
40. Norval, M., Lucas, R. M., Cullen, A. P., de Gruijl, F. R., Longstreth, J., Takizawa, Y., and van der Leun, J. C. (2011) The human health effects of ozone depletion and interactions with climate change Photochem. Photobiol. Sci. 10, 199-225
41. Su, D. G. T., Fang, H., Gross, M. L., and Taylor, J.-S. A. (2009) Photocrosslinking of human telomeric G-quadruplex loops by anti cyclobutane thymine dimer formation Proc. Natl. Acad. Sci. U.S.A. 106, 12861-12866
42. Smith, J. E., Lu, C., and Taylor, J.-S. (2014) Effect of sequence and metal ions on UVB-induced anti cyclobutane pyrimidine dimer formation in human telomeric DNA sequences Nucleic Acids Res. 42, 5007-5019
43. An, N., Fleming, A. M., and Burrows, C. J. (2013) Interactions of the human telomere sequence with the nanocavity of the α-hemolysin ion channel reveal structure-dependent electrical signatures for hybrid folds J. Am. Chem. Soc. 135, 8562-8570
44. An, N., Fleming, A. M., Middleton, E. G., and Burrows, C. J. (2014) Size-selective property of α-hemolysin provides signatures for DNA nanostructures formed by the human telomere sequence Proc. Natl. Acad. Sci. U.S.A. 111, 14325-14331
45. Nguyen, K. V. and Burrows, C. J. (2011) A prebiotic role for 8-oxoguanosine as a flavin mimic in pyrimidine dimer photorepair J. Am. Chem. Soc. 133, 14586-14589
46. Zhang, B., Galusha, J., Shiozawa, P. G., Wang, G., Bergren, A. J., Jones, R. M., White, R. J., Ervin, E. N., Cauley, C. C., and White, H. S. (2007) Bench-top method for fabricating glass-sealed nanodisk electrodes, glass nanopore electrodes, and glass nanopore membranes of controlled size Anal. Chem. 79, 4778-4787
47. White, R. J., Ervin, E. N., Yang, T., Chen, X., Daniel, S., Cremer, P. S., and White, H. S. (2007) Single ion-channel recordings using glass nanopore membranes J. Am. Chem. Soc. 129, 11766-11775
48. Karsisiotis, A. I., Hessari, N. M. A., Novellino, E., Spada, G. P., Randazzo, A., and Webba da Silva, M. (2011) Topological characterization of nucleic acid G-quadruplexes by UV absorption and circular dichroism Angew. Chem., Int. Ed. 50, 10645-10648
49. Koirala, D., Mashimo, T., Sannohe, Y., Yu, Z., Mao, H., and Sugiyama, H. (2012) Intramolecular folding in three tandem guanine repeats of human telomeric DNA Chem. Commun. 48, 2006-2008
50. Rajendran, A., Endo, M., Hidaka, K., and Sugiyama, H. (2014) Direct and single-molecule visualization of the solution-state structures of G-hairpin and G-triplex intermediates Angew. Chem., Int. Ed. 53, 4107-4112
51. + solution: A stable basket-type G-quadruplex with only two G-tetrad layers J. Am. Chem. Soc. 131, 4301-4309
52. Vercoutere, W. A., Winters-Hilt, S., DeGuzman, V. S., Deamer, D., Ridino, S. E., Rodgers, J. T., Olsen, H. E., Marziali, A., and Akeson, M. (2003) Discrimination among individual Watson-Crick base pairs at the termini of single DNA hairpin molecules Nucleic Acids Res. 31, 1311-1318
53. 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
54. Stadlbauer, P., Trantirek, L., Cheatham, T. E., III, Koca, J., and Sponer, J. (2014) Triplex intermediates in folding of human telomeric quadruplexes probed by microsecond-scale molecular dynamics simulations Biochimie 105, 22-35
55. Branton, D., Deamer, D. W., Marziali, A., Bayley, H., Benner, S. A., Butler, T., Di Ventra, M., Garaj, S., Hibbs, A., Huang, X., Jovanovich, S. B., Krstic, P. S., Lindsay, S., Ling, X. S., Mastrangelo, C. H., Meller, A., Oliver, J. S., Pershin, Y. V., Ramsey, J. M., Riehn, R., Soni, G. V., Tabard-Cossa, V., Wanunu, M., Wiggin, M., and Schloss, J. A. (2008) The potential and challenges of nanopore sequencing Nat. Biotechnol. 26, 1146-1158
56. Cherf, G. M., Lieberman, K. R., Rashid, H., Lam, C. E., Karplus, K., and Akeson, M. (2012) Automated forward and reverse ratcheting of DNA in a nanopore at 5-Å precision Nat. Biotechnol. 30, 344-348
57. Kasianowicz, J. J., Brandin, E., Branton, D., and Deamer, D. W. (1996) Characterization of individual polynucleotide molecules using a membrane channel Proc. Natl. Acad. Sci. U.S.A. 93, 13770-13773
58. Shim, J. and Gu, L.-Q. (2012) Single-molecule investigation of G-quadruplex using a nanopore sensor Methods 57, 40-46
59. Shim, J. W., Tan, Q., and Gu, L.-Q. (2009) Single-molecule detection of folding and unfolding of the G-quadruplex aptamer in a nanopore nanocavity Nucleic Acids Res. 37, 972-982
60. Rotem, D., Jayasinghe, L., Salichou, M., and Bayley, H. (2012) Protein detection by nanopores equipped with aptamers J. Am. Chem. Soc. 134, 2781-2787
61. Renner, S., Geltinger, S., and Simmel, F. C. (2010) Nanopore translocation and force spectroscopy experiments in microemulsion droplets Small 6, 190-194
62. Gu, L.-Q. and Shim, J. W. (2010) Single molecule sensing by nanopores and nanopore devices Analyst 135, 441-451
63. Jin, Q., Fleming, A. M., Johnson, R. P., Ding, Y., Burrows, C. J., and White, H. S. (2013) Base-excision repair activity of uracil-DNA glycosylase monitored using the latch zone of α-hemolysin J. Am. Chem. Soc. 135, 19347-19353
64. Blasco, M. A. (2007) Telomere length, stem cells and aging Nat. Chem. Biol. 3, 640-649