Table of Contents Author Guidelines Submit a Manuscript
Journal of Nucleic Acids
Volume 2017, Article ID 9170371, 14 pages
https://doi.org/10.1155/2017/9170371
Research Article

Telomeric G-Quadruplexes: From Human to Tetrahymena Repeats

1Department of Biochemistry, Institute of Chemistry, Faculty of Sciences, P. J. Šafárik University, 04001 Kosice, Slovakia
2Department of Biological Sciences/RNA Institute, University at Albany, SUNY, Albany, NY 12222, USA
3Institute of Experimental Physics, Slovak Academy of Sciences, Watsonova 47, 040 01 Košice, Slovakia

Correspondence should be addressed to Viktor Víglaský; ks.sjpu@yksalgiv.rotkiv

Received 30 July 2017; Revised 11 November 2017; Accepted 5 December 2017; Published 28 December 2017

Academic Editor: Shozeb Haider

Copyright © 2017 Erika Demkovičová et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. W. Lim, V. C. M. Ng, N. Martín-Pintado, B. Heddi, and A. T. Phan, “Structure of the human telomere in Na+ solution: An antiparallel (2+2) G-quadruplex scaffold reveals additional diversity,” Nucleic Acids Research, vol. 41, no. 22, pp. 10556–10562, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. V. Víglaský, K. Tlučková, and Ľ. Bauer, “The first derivative of a function of circular dichroism spectra: Biophysical study of human telomeric G-quadruplex,” European Biophysics Journal, vol. 40, no. 1, pp. 29–37, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. G. N. Parkinson, M. P. H. Lee, and S. Neidle, “Crystal structure of parallel quadruplexes from human telomeric DNA,” Nature, vol. 417, no. 6891, pp. 876–880, 2002. View at Publisher · View at Google Scholar · View at Scopus
  4. Y. Wang and D. J. Patel, “Solution structure of the human telomeric repeat d[AG3(T2AG3)3] G-tetraplex,” Structure, vol. 1, no. 4, pp. 263–282, 1993. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Ambrus, D. Chen, J. Dai, T. Bialis, R. A. Jones, and D. Yang, “Human telomeric sequence forms a hybrid-type intramolecular G-quadruplex structure with mixed parallel/antiparallel strands in potassium solution,” Nucleic Acids Research, vol. 34, no. 9, pp. 2723–2735, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. K. N. Luu, A. T. Phan, V. Kuryavyi, L. Lacroix, and D. J. Patel, “Structure of the human telomere in K+ solution: An intramolecular (3 + 1) G-quadruplex scaffold,” Journal of the American Chemical Society, vol. 128, no. 30, pp. 9963–9970, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. A. T. Phan, V. Kuryavyi, K. N. Luu, and D. J. Patel, “Structure of two intramolecular G-quadruplexes formed by natural human telomere sequences in K+ solution,” Nucleic Acids Research, vol. 35, no. 19, pp. 6517–6525, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Marušič, P. Šket, L. Bauer, V. Viglasky, and J. Plavec, “Solution-state structure of an intramolecular G-quadruplex with propeller, diagonal and edgewise loops,” Nucleic Acids Research, vol. 40, no. 14, pp. 6946–6956, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. P. Tóthová, P. Krafčíková, and V. Víglaský, “Formation of highly ordered multimers in G-quadruplexes,” Biochemistry, vol. 53, no. 45, pp. 7013–7027, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. N. Smargiasso, F. Rosu, W. Hsia et al., “G-quadruplex DNA assemblies: Loop length, cation identity, and multimer formation,” Journal of the American Chemical Society, vol. 130, no. 31, pp. 10208–10216, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. B. Heddi and A. T. Phan, “Structure of human telomeric DNA in crowded solution,” Journal of the American Chemical Society, vol. 133, no. 25, pp. 9824–9833, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. M. C. Miller, R. Buscaglia, J. B. Chaires, A. N. Lane, and J. O. Trent, “Hydration is a major determinant of the G-quadruplex stability and conformation of the human telomere 3 sequence of d(AG 3(TTAG3)3),” Journal of the American Chemical Society, vol. 132, no. 48, pp. 17105–17107, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. D. Miyoshi, A. Nakao, and N. Sugimoto, “Molecular crowding regulates the structural switch of the DNA G-quadruplex,” Biochemistry, vol. 41, no. 50, pp. 15017–15024, 2002. View at Publisher · View at Google Scholar · View at Scopus
  14. V. Víglaský, L. Bauer, and K. Tlučková, “Structural features of intra- and intermolecular G-quadruplexes derived from telomeric repeats,” Biochemistry, vol. 49, no. 10, pp. 2110–2120, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. J. L. Huppert and S. Balasubramanian, “Prevalence of quadruplexes in the human genome,” Nucleic Acids Research, vol. 33, no. 9, pp. 2908–2916, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. A. K. Todd, M. Johnston, and S. Neidle, “Highly prevalent putative quadruplex sequence motifs in human DNA,” Nucleic Acids Research, vol. 33, no. 9, pp. 2901–2907, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Eddy and N. Maizels, “Gene function correlates with potential for G4 DNA formation in the human genome,” Nucleic Acids Research, vol. 34, no. 14, pp. 3887–3896, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Henderson, Y. Wu, Y. C. Huang et al., “Detection of G-quadruplex DNA in mammalian cells,” Nucleic Acids Research, vol. 42, no. 2, pp. 860–869, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. R. F. Hoffmann, Y. M. Moshkin, S. Mouton et al., “Guanine quadruplex structures localize to heterochromatin,” Nucleic Acids Research, vol. 44, no. 1, pp. 152–163, 2016. View at Publisher · View at Google Scholar · View at Scopus
  20. V. S. Chambers, G. Marsico, J. M. Boutell, M. Di Antonio, G. P. Smith, and S. Balasubramanian, “High-throughput sequencing of DNA G-quadruplex structures in the human genome,” Nature Biotechnology, vol. 33, no. 8, pp. 877–881, 2015. View at Publisher · View at Google Scholar · View at Scopus
  21. E. H. Blackburn, “Telomere states and cell fates,” Nature, vol. 408, no. 6808, pp. 53–56, 2000. View at Publisher · View at Google Scholar · View at Scopus
  22. M. J. McEachern, A. Krauskopf, and E. H. Blackburn, “Telomeres and their control,” Annual Review of Genetics, vol. 34, pp. 331–358, 2000. View at Publisher · View at Google Scholar · View at Scopus
  23. N. Grandin and M. Charbonneau, “Protection against chromosome degradation at the telomeres,” Biochimie, vol. 90, no. 1, pp. 41–59, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. W. E. Wright, V. M. Tesmer, K. E. Huffman, S. D. Levene, and J. W. Shay, “Normal human chromosomes have long G-rich telomeric overhangs at one end,” Genes & Development, vol. 11, no. 21, pp. 2801–2809, 1997. View at Publisher · View at Google Scholar · View at Scopus
  25. J. A. Londoño-Vallejo, “Telomere instability and cancer,” Biochimie, vol. 90, no. 1, pp. 73–82, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. C. B. Harley, “Telomere loss: mitotic clock or genetic time bomb?” Mutation Research DNAging, vol. 256, no. 2–6, pp. 271–282, 1991. View at Publisher · View at Google Scholar · View at Scopus
  27. A. J. Sfeir, W. Chai, J. W. Shay, and W. E. Wright, “Telomere-end processing: The terminal nucleotidesof human chromosomes,” Molecular Cell, vol. 18, no. 1, pp. 131–138, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. L. M. Colgin and R. R. Reddel, “Telomere maintenance mechanisms and cellular immortalization,” Current Opinion in Genetics & Development, vol. 9, no. 1, pp. 97–103, 1999. View at Publisher · View at Google Scholar · View at Scopus
  29. A. M. Zahler, J. R. Williamson, T. R. Cech, and D. M. Prescott, “Inhibition of telomerase by G-quartet DNA structures,” Nature, vol. 350, no. 6320, pp. 718–720, 1991. View at Publisher · View at Google Scholar · View at Scopus
  30. S. Neidle and G. Parkinson, “Telomere maintenance as a target for anticancer drug discovery,” Nature Reviews Drug Discovery, vol. 1, no. 5, pp. 383–393, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. K. W. Lim, S. Amrane, S. Bouaziz et al., “Structure of the human telomere in K + solution: A stable basket-type G-quadruplex with only two G-tetrad layers,” Journal of the American Chemical Society, vol. 131, no. 12, pp. 4301–4309, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. R. Buscaglia, M. C. Miller, W. L. Dean et al., “Polyethylene glycol binding alters human telomere G-quadruplex structure by conformational selection,” Nucleic Acids Research, vol. 41, no. 16, pp. 7934–7946, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. L. Petraccone, A. Malafronte, J. Amato, and C. Giancola, “G-quadruplexes from human telomeric DNA: How many conformations in PEG containing solutions?” The Journal of Physical Chemistry B, vol. 116, no. 7, pp. 2294–2305, 2012. View at Publisher · View at Google Scholar · View at Scopus
  34. V. Viglasky, L. Bauer, K. Tluckova, and P. Javorsky, “Evaluation of human telomeric G-quadruplexes: The influence of overhanging sequences on quadruplex stability and folding,” Journal of Nucleic Acids, vol. 2010, Article ID 820356, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Vorlícková, M. Tomasko, A. J. Sagi, K. Bednarova, and J. Sagi, “8-Oxoguanine in a quadruplex of the human telomere DNA sequence,” FEBS Journal, vol. 279, no. 1, pp. 29–39, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. D. Renčiuk, I. Kejnovská, P. Školáková, K. Bednářová, J. Motlová, and M. Vorlíčková, “Arrangements of human telomere DNA quadruplex in physiologically relevant K+ solutions,” Nucleic Acids Research, vol. 37, no. 19, pp. 6625–6634, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Tomaško, M. Vorlíčková, and J. Sagi, “Substitution of adenine for guanine in the quadruplex-forming human telomere DNA sequence G3(T2AG3)3,” Biochimie, vol. 91, no. 2, pp. 171–179, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Vorlíčková, J. Chládková, I. Kejnovská, M. Fialová, and J. Kypr, “Guanine tetraplex topology of human telomere DNA is governed by the number of (TTAGGG) repeats,” Nucleic Acids Research, vol. 33, no. 18, pp. 5851–5860, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. I. Kejnovská, K. Bednářová, D. Renčiuk et al., “Clustered abasic lesions profoundly change the structure and stability of human telomeric G-quadruplexes,” Nucleic Acids Research, vol. 45, no. 8, pp. 4294–4305, 2017. View at Publisher · View at Google Scholar
  40. H. Konvalinová, Z. Dvořáková, D. Renčiuk et al., “Diverse effects of naturally occurring base lesions on the structure and stability of the human telomere DNA quadruplex,” Biochimie, vol. 118, article no. 4773, pp. 15–25, 2015. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Babinský, R. Fiala, I. Kejnovská et al., “Loss of loop adenines alters human telomere d(AG(3)(TTAG(3))(3)) quadruplex folding,” Nucleic Acids Research, vol. 42, no. 22, pp. 14031–14041, 2014. View at Publisher · View at Google Scholar · View at Scopus
  42. C. W. Greider and E. H. Blackburn, “A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis,” Nature, vol. 337, no. 6205, pp. 331–337, 1989. View at Publisher · View at Google Scholar · View at Scopus
  43. I. Lubitz, D. Zikich, and A. Kotlyar, “Specific high-affinity binding of thiazole orange to triplex and g-quadruplex DNA,” Biochemistry, vol. 49, no. 17, pp. 3567–3574, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. P. Krafčíková, E. Demkovičová, and V. Víglaský, “Ebola virus derived G-quadruplexes: Thiazole orange interaction,” Biochimica et Biophysica Acta (BBA) - General Subjects, vol. 1861, no. 5, pp. 1321–1328, 2016. View at Publisher · View at Google Scholar · View at Scopus
  45. J. Mohanty, N. Barooah, V. Dhamodharan, S. Harikrishna, P. I. Pradeepkumar, and A. C. Bhasikuttan, “Thioflavin T as an efficient inducer and selective fluorescent sensor for the human telomeric G-quadruplex DNA,” Journal of the American Chemical Society, vol. 135, no. 1, pp. 367–376, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. J. B. Chaires, “Human telomeric G-quadruplex: Thermodynamic and kinetic studies of telomeric quadruplex stability,” FEBS Journal, vol. 277, no. 5, pp. 1098–1106, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. Y. Wang and D. J. Patel, “Solution Structure of a Parallel-stranded G-Quadruplex DNA,” Journal of Molecular Biology, vol. 234, no. 4, pp. 1171–1183, 1993. View at Publisher · View at Google Scholar · View at Scopus
  48. Y. Wang and D. J. Patel, “Solution structure of the Tetrahymena telomeric repeat d(T2G4)4 G-tetraplex,” Structure, vol. 2, no. 12, pp. 1141–1156, 1994. View at Publisher · View at Google Scholar · View at Scopus
  49. J. Dai, C. Punchihewa, A. Ambrus, D. Chen, R. A. Jones, and D. Yang, “Structure of the intramolecular human telomeric G-quadruplex in potassium solution: A novel adenine triple formation,” Nucleic Acids Research, vol. 35, no. 7, pp. 2440–2450, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. J. Dai, M. Carver, C. Punchihewa, R. A. Jones, and D. Yang, “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 Research, vol. 35, no. 15, pp. 4927–4940, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. Y. Wang and D. J. Patel, “Solution Structure of theOxytrichaTelomeric Repeat d[G4(T4G4)3] G-tetraplex,” Journal of Molecular Biology, vol. 251, no. 1, pp. 76–94, 1995. View at Publisher · View at Google Scholar · View at Scopus
  52. F. W. Smith, P. Schultze, and J. Feigon, “Solution structures of unimolecular quadruplexes formed by oligonucleotides containing Oxytricha telomere repeats,” Structure, vol. 3, no. 10, pp. 997–1008, 1995. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Brčić and J. Plavec, “Solution structure of a DNA quadruplex containing ALS and FTD related GGGGCC repeat stabilized by 8-bromodeoxyguanosine substitution,” Nucleic Acids Research, vol. 43, no. 17, pp. 8590–8600, 2015. View at Publisher · View at Google Scholar · View at Scopus
  54. J. Kypr, I. Kejnovská, D. Renčiuk, and M. Vorlíčková, “Circular dichroism and conformational polymorphism of DNA,” Nucleic Acids Research, vol. 37, no. 6, pp. 1713–1725, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. A. I. Karsisiotis, N. M. Hessari, E. Novellino, G. P. Spada, A. Randazzo, and M. Webba Da Silva, “Topological characterization of nucleic acid G-quadruplexes by UV absorption and circular dichroism,” Angewandte Chemie International Edition, vol. 50, no. 45, pp. 10645–10648, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. D. Miyoshi, T. Fujimoto, and N. Sugimoto, “Molecular crowding and hydration regulating of G-quadruplex formation,” Topics in Current Chemistry, vol. 330, pp. 87–110, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. D. M. Gray, J.-D. Wen, C. W. Gray et al., “Measured and calculated CD spectra of G-quartets stacked with the same or opposite polarities,” Chirality, vol. 20, no. 3-4, pp. 431–440, 2008. View at Publisher · View at Google Scholar · View at Scopus
  58. C. Allain, D. Monchaud, and M.-P. Teulade-Fichou, “FRET templated by G-quadruplex DNA: A specific ternary interaction using an original pair of donor/acceptor partners,” Journal of the American Chemical Society, vol. 128, no. 36, pp. 11890–11893, 2006. View at Publisher · View at Google Scholar · View at Scopus