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Electronic Excitations in Guanine Quadruplexes

  • Pascale Changenet-Barret
  • Ying Hua
  • Dimitra Markovitsi
Part of the Topics in Current Chemistry book series (TOPCURRCHEM, volume 356)

Abstract

Guanine rich DNA strands, such as those encountered at the extremities of human chromosomes, have the ability to form four-stranded structures (G-quadruplexes) whose building blocks are guanine tetrads. G-quadruplex structures are intensively studied in respect of their biological role, as targets for anticancer therapy and, more recently, of their potential applications in the field of molecular electronics. Here we focus on their electronic excited states which are compared to those of non-interacting mono-nucleotides and those of single and double stranded structures. Particular emphasis is given to excited state relaxation processes studied by time-resolved fluorescence spectroscopy from femtosecond to nanosecond time scales. They include ultrafast energy transfer and trapping of ππ* excitations by charge transfer states. The effect of various structural parameters, such as the nature of the metal cations located in the central cavity of G-quadruplexes, the number of tetrads or the conformation of the constitutive single strands, are examined.

Keywords

Charge transfer states DNA fluorescence Energy transfer Excitons Guanine quadruplexes Molecular electronics Multi-scale dynamics 

Notes

Acknowledgment

The French National Agency for Research (ANR-12-BS08-0001-01) is acknowledged for financial support.

References

  1. 1.
    Huppert JL (2008) Four-stranded nucleic acids: structure, function and targeting of G-quadruplexes. Chem Soc Rev 37:1375–1384CrossRefGoogle Scholar
  2. 2.
    Neidle S (2009) The structures of quadruplex nucleic acids and their drug complexes. Curr Opin Struct Biol 19:239–250CrossRefGoogle Scholar
  3. 3.
    Biffi G, Tannahill D, McCafferty J, Balasubramanian S (2013) Quantitative visualization of DNA G-quadruplex structures in human cells. Nat Chem 5:182–186CrossRefGoogle Scholar
  4. 4.
    De Cian A, Lacroix L, Douarre C, Temime-Smaali N, Trentesaux C, Riou JF, Mergny JL (2008) Targeting telomeres and telomerase. Biochimie 90:131–155CrossRefGoogle Scholar
  5. 5.
    Ruden M, Puri N (2013) Novel anticancer therapeutics targeting telomerase. Cancer Treat Rev 39:444–456CrossRefGoogle Scholar
  6. 6.
    Neidle S, Parkinson G (2002) Telomere maintenance as a target for anticancer drug discovery. Nat Rev Drug Discov 1:383–393CrossRefGoogle Scholar
  7. 7.
    Borovok N, Iram N, Zikich D, Ghabboun J, Livshits GI, Porath D, Kotlyar AB (2008) Assembling of G-strands into novel tetra-molecular parallel G4-DNA nanostructures using avidinbiotin recognition. Nucleic Acids Res 36:5050–5060CrossRefGoogle Scholar
  8. 8.
    Liu SP, Weisbrod SH, Tang Z, Marx A, Scheer E, Erbe A (2010) Direct measurement of electrical transport through G-quadruplex DNA with mechanically controllable break junction electrodes. Angew Chem Int Ed 49:3313–3316CrossRefGoogle Scholar
  9. 9.
    Lee JB, Campolongo MJ, Kahn JS, Roh YH, Hartman MR, Luo D (2010) DNA-based nanostructures for molecular sensing. Nanoscale 2:188–197CrossRefGoogle Scholar
  10. 10.
    Chaires BJ, Graves D (eds) (2013) Quadruplex nucleic acids, vol 330. Top Curr Chem SpringerGoogle Scholar
  11. 11.
    Markovitsi D, Gustavsson T, Sharonov A (2004) Cooperative effects in the photophysical properties of self-associated triguanosine diphosphates. Photochem Photobiol 79:526–530CrossRefGoogle Scholar
  12. 12.
    McGovern DA, Quinn S, Doorley GW, Whelan AM, Ronayne KL, Towrie M, Parker AW, Kelly JM (2007) Picosecond infrared probing of the vibrational spectra of transients formed upon UV excitation of stacked G-tetrad structures. Chem Commun 5158–5160Google Scholar
  13. 13.
    Gepshtein R, Huppert D, Lubitz I, Amdursky N, Kotlyar AB (2008) Radiationless transitions of G4 wires and dGMP. J Phys Chem C 112:12249–12258CrossRefGoogle Scholar
  14. 14.
    Miannay FA, Banyasz A, Gustavsson T, Markovitsi D (2009) Excited states and energy transfer in G-quadruplexes. J Phys Chem C 113:11760–11765CrossRefGoogle Scholar
  15. 15.
    Mendez MA, Szalai VA (2009) Fluorescence of unmodified oligonucleotides: a tool to probe G-quadruplex DNA structure. Biopolymers 91:841–850CrossRefGoogle Scholar
  16. 16.
    Changenet-Barret P, Emanuele E, Gustavsson T, Improta R, Kotlyar AB, Markovitsi D, Vaya I, Zakrzewska K, Zikich D (2010) Optical properties of guanine nanowires: experimental and theoretical study. J Phys Chem C 114:14339–14346CrossRefGoogle Scholar
  17. 17.
    Dumas A, Luedtke NW (2010) Cation-mediated energy transfer in G-quadruplexes revealed by an internal fluorescent probe. J Am Chem Soc 132:18004–18007CrossRefGoogle Scholar
  18. 18.
    Dao NT, Haselsberger R, Michel-Beyerle ME, Phan AT (2011) Following G-quadruplex formation by its intrinsic fluorescence. FEBS Lett 585:3969–3977CrossRefGoogle Scholar
  19. 19.
    Hua Y, Changenet-Barret P, Improta R, Vayá I, Gustavsson T, Kotlyar AB, Zikich D, Šket P, Plavec J, Markovitsi D (2012) Cation effect on the electronic excited states of guanine nanostructures studied by time-resolved fluorescence spectroscopy. J Phys Chem C 116:14682–14689CrossRefGoogle Scholar
  20. 20.
    Hua Y, Changenet-Barret P, Gustavsson T, Markovitsi D (2013) The effect of size on the optical properties of guanine nanostructures: a femtosecond to nanosecond study. Phys Chem Chem Phys 15:7396–7402CrossRefGoogle Scholar
  21. 21.
    Dao NT, Haselsberger R, Michel-Beyerle ME, Phan AT (2013) Excimer formation by stacking G-Quadruplex blocks. ChemBioChem 1–5Google Scholar
  22. 22.
    Kwok CK, Sherlock ME, Bevilacqua PC (2013) Effect of loop sequence and loop length on the intrinsic fluorescence of G-quadruplexes. Biochemistry 52:3019–3021CrossRefGoogle Scholar
  23. 23.
    Kotlyar AB, Borovok N, Molotsky T, Cohen H, Shapir E, Porath D (2005) Long, monomolecular guanine-based nanowires. Adv Mater 17:1901–1905CrossRefGoogle Scholar
  24. 24.
    Burge S, Parkinson GN, Hazel P, Todd AK, Neidle S (2006) Quadruplex DNA: sequence, topology and structure. Nucleic Acids Res 34:5402–5415CrossRefGoogle Scholar
  25. 25.
    Mergny JL, Gros J, De Cian A, Bourdoncle A, Rosu F, Sacca B, Guitatat L, Amrane S, Mills M, Alberti P, Takasugi M, Lacroix L (2006) Energetics, kinetics and dynamics of quadruplex folding. In: Neidle S, Balasubramanian S (eds) Quadruplex nucleic acids. RSC Publishing, CambridgeGoogle Scholar
  26. 26.
    Qin Y, Hurley LH (2008) Structures, folding patterns, and functions of intramolecular DNA G-quadruplexes found in eukaryotic promoter regions. Biochimie 90:1149–1171CrossRefGoogle Scholar
  27. 27.
    Starikov EB (2004) Importance of charge transfer excitations in DNA electron spectrum: a ZINDO semiempirical quantum-chemical study. Mod Phys Lett B 18:825–831CrossRefGoogle Scholar
  28. 28.
    Varsano D, Di Felice R, Marques MAL, Rubio A (2006) A TDDFT study of the excited states of DNA bases and their assemblies. J Phys Chem B 110:7129–7138CrossRefGoogle Scholar
  29. 29.
    Santoro F, Barone V, Improta R (2009) Excited states decay of the A-T DNA: a PCM/TD-DFT study in aqueous solution of the (9-methyl-adenine) 2 (1-methyl-thymine) 2 stacked tetramer. J Am Chem Soc 131:15232–15245CrossRefGoogle Scholar
  30. 30.
    Lange AW, Herbert JM (2009) Both intra- and interstrand charge-transfer excited states in aqueous B-DNA are present at energies comparable to, or just above, the 1ππ* excitonic bright states. J Am Chem Soc 131:3913–3922CrossRefGoogle Scholar
  31. 31.
    Plasser F, Aquino AJA, Hase WL, Lischka H (2012) UV absorption spectrum of alternating DNA duplexes. Analysis of excitonic and charge transfer interactions. J Phys Chem A 116:11151–11160CrossRefGoogle Scholar
  32. 32.
    Mergny JL, Phan AT, Lacroix L (1998) Following G-quartet formation by UV-spectroscopy. FEBS Lett 435:74–78CrossRefGoogle Scholar
  33. 33.
    Bouvier B, Dognon JP, Lavery R, Markovitsi D, Millié P, Onidas D, Zakrzewska K (2003) Influence of conformational dynamics on the exciton states of DNA oligomers. J Phys Chem B 107:13512–13522CrossRefGoogle Scholar
  34. 34.
    Emanuele E, Zakrzewska K, Markovitsi D, Lavery R, Millie P (2005) Exciton states of dynamic DNA double helices: alternating dCdG sequences. J Phys Chem B 109:16109–16118CrossRefGoogle Scholar
  35. 35.
    Masiero S, Trotta R, Pieraccini S, De Tito S, Perone R, Randazzo A, Spada GP (2010) A non-empirical chromophoric interpretation of CD spectra of DNA G-quadruplex structures. Org Biomol Chem 8:2683–2692CrossRefGoogle Scholar
  36. 36.
    Randazzo A, Spada GP, Webba da Silva M (2013) Circular dichroism of quadruplex structures. Top Curr Chem 330:67–86CrossRefGoogle Scholar
  37. 37.
    Markovitsi D, Onidas D, Gustavsson T, Talbot F, Lazzarotto E (2005) Collective behavior of Franck–Condon excited states and energy transfer in DNA double helices. J Am Chem Soc 127:17130–17131CrossRefGoogle Scholar
  38. 38.
    Miannay FA, Banyasz A, Gustavsson T, Markovitsi D (2007) Ultrafast excited state deactivation and energy transfer in guanine-cytosine DNA double helices. J Am Chem Soc 129:14574–14575CrossRefGoogle Scholar
  39. 39.
    Onidas D, Gustavsson T, Lazzarotto E, Markovitsi D (2007) Fluorescence of the DNA double helices (dAdT)n. (dAdT)n studied by femtosecond spectroscopy. Phys Chem Chem Phys 9:5143–5148CrossRefGoogle Scholar
  40. 40.
    Vayá I, Gustavsson T, Douki T, Berlin Y, Markovitsi D (2012) Electronic excitation energy transfer between nucleobases of natural DNA. J Am Chem Soc 134:11366–11368CrossRefGoogle Scholar
  41. 41.
    Onidas D, Markovitsi D, Marguet S, Sharonov A, Gustavsson T (2002) Fluorescence properties of DNA nucleosides and nucleotides: a refined steady-state and femtosecond investigation. J Phys Chem B 106:11367–11374CrossRefGoogle Scholar
  42. 42.
    Sundstrom V, Pullerits T, van Grondelle R (1999) Photosynthetic light-harvesting: reconciling dynamics and structure of purple bacterial LH2 reveals function of photosynthetic unit. J Phys Chem B 103:2327–2346CrossRefGoogle Scholar
  43. 43.
    Kennis JTM, Gobets B, van Stokkum IHM, Dekker JP, van Grondelle R, Fleming GR (2001) Light harvesting by chlorophylls and carotenoids in the photosystem I core complex of Synechococcus elongatus: a fluorescence upconversion study. J Phys Chem B 105:4485–4494CrossRefGoogle Scholar
  44. 44.
    Zigmantas D, Read EL, Mancal T, Brixner T, Gardiner AT, Cogdell RJ, Fleming GR (2006) Two-dimensional electronic spectroscopy of the B800-B820 light-harvesting complex. Proc Natl Acad Sci U S A 103:12672–12677CrossRefGoogle Scholar
  45. 45.
    Albrecht AC (1961) Polarizations and assignments of transitions – method of photoselection. J Mol Spectrosc 6:84–108CrossRefGoogle Scholar
  46. 46.
    Vayá I, Gustavsson T, Miannay FA, Douki T, Markovitsi D (2010) Fluorescence of natural DNA: from the femtosecond to the nanosecond time-scales. J Am Chem Soc 132:11834–11835CrossRefGoogle Scholar
  47. 47.
    Schwalb N, Temps F (2007) Ultrafast electronic excitation in guanosine is promoted by hydrogen bonding with cytidine. J Am Chem Soc 129:9272–9273CrossRefGoogle Scholar
  48. 48.
    Vayá I, Miannay FA, Gustavsson T, Markovitsi D (2010) High energy long-lived excited states in DNA double strands. ChemPhysChem 11:987–989CrossRefGoogle Scholar
  49. 49.
    Vayá I, Changenet-Barret P, Gustavsson T, Zikich D, Kotlyar A, Markovitsi D (2010) Long-lived fluorescence of homopolymeric guanine-cytosine DNA duplexes. Photochem Photobiol Sci 9:1193–1195CrossRefGoogle Scholar
  50. 50.
    Brazard J, Thazhathveetil A, Vayá I, Lewis F, Gustavsson T, Markovitsi D (2013) Electronic excited states of guanine-cytosine hairpins and duplexes studied by fluorescence spectroscopy. Photochem Photobiol Sci 12:1453–1459CrossRefGoogle Scholar
  51. 51.
    Sobolewski AL, Domcke W, Hattig C (2005) Tautomeric selectivity of the excited-state lifetime of guanine/cytosine base pairs: the role of electron-driven proton-transfer processes. Proc Natl Acad Sci U S A 102:17903–17906CrossRefGoogle Scholar
  52. 52.
    Groenhof G, Schäfer LV, Boggio-Pasqua M, Goette M, Grubmüller H, Robb MA (2007) Ultrafast decactivation of an excited cytosine guanine base pair in DNA. J Am Chem Soc 129:6812–6819CrossRefGoogle Scholar
  53. 53.
    Biemann L, Kovalenko SA, Kleinermanns K, Mahrwald R, Markert M, Improta R (2011) Excited state proton transfer is not involved in the ultrafast deactivation of guanine-cytosine pair in solution. J Am Chem Soc 133:19664–19667CrossRefGoogle Scholar
  54. 54.
    Onidas D, Gustavsson T, Lazzarotto E, Markovitsi D (2007) Fluorescence of the DNA double helix (dA)20. (dT)20 studied by femtosecond spectroscopy – effect of the duplex size on the properties of the excited states. J Phys Chem B 111:9644–9650CrossRefGoogle Scholar
  55. 55.
    Markovitsi D, Gustavsson T, Talbot F (2007) Excited states and energy transfer among DNA bases in double helices. Photochem Photobiol Sci 6:717–724CrossRefGoogle Scholar
  56. 56.
    Gustavsson T, Improta R, Markovitsi D (2010) DNA/RNA: building blocks of life under UV irradiation. J Phys Chem Lett 1:2025–2030CrossRefGoogle Scholar
  57. 57.
    Kleinermanns K, Nachtigallová D, de Vries MS (2013) Excited state dynamics of DNA bases. Int Rev Phys Chem. doi: 10.1080/0144235X.0142012.0760884 Google Scholar
  58. 58.
    Karunakaran V, Kleinermanns K, Improta R, Kovalenko SA (2009) Photoinduced dynamics of guanosine monophosphate in water from broad-band transient absorption spectroscopy and quantum-chemical calculations. J Am Chem Soc 131:5839–5850CrossRefGoogle Scholar
  59. 59.
    Miannay FA, Gustavsson T, Banyasz A, Markovitsi D (2010) Excited state dynamics of deoxy-guanosine monophosphate dGMP measured by steady-state and femtosecond fluorescence spectroscopy. J Phys Chem A 114:3256–3263CrossRefGoogle Scholar
  60. 60.
    Kasha M, Rawls HR, El-Bayoumi MA (1965) The exciton model in molecular spectroscopy. Pure Appl Chem 11:371–392CrossRefGoogle Scholar
  61. 61.
    Spano FC (2010) The spectral signatures of Frenkel polarons in H- and J-aggregates. Acc Chem Res 43:429–439CrossRefGoogle Scholar
  62. 62.
    Karsisiotis AI, Hessari NM, Novellino E, Spada GP, Randazzo A, da Silva MW (2011) Topological characterization of nucleic acid G-quadruplexes by UV absorption and circular dichroism. Angew Chem Int Ed 50:10645–10648CrossRefGoogle Scholar
  63. 63.
    Hua Y (2013) Self-associated gunanine structures studied by time-resolved optical spectroscopy. Université de Paris Sud, OrsayGoogle Scholar
  64. 64.
    Viglasky V, Tluckova K, Bauer L (2011) The first derivative of a function of circular dichroism spectra: biophysical study of human telomeric G-quadruplex. Eur Biophys J 40:29–37CrossRefGoogle Scholar
  65. 65.
    Manet I, Manoli F, Zambelli B, Andreano G, Masi A, Cellai L, Monti S (2011) Affinity of the anthracycline antitumor drugs Doxorubicin and Sabarubicin for human telomeric G-quadruplex structures. Phys Chem Chem Phys 13:540–551CrossRefGoogle Scholar
  66. 66.
    Wang Y, Patel DJ (1993) Solution structure of the human telomeric repeat d[AG3(T2AG3)3] G-tetratraplex. Structure 1:263–282CrossRefGoogle Scholar
  67. 67.
    Luu KN, Phan AT, Kuryavyi V, Lacroix L, Patel DJ (2006) Structure of the human telomere in K+ solution: an intramolecular (3+1) G-quadruplex scaffold. J Am Chem Soc 128:9963–9970CrossRefGoogle Scholar
  68. 68.
    Phan AT, Kuryavyi V, Luu KN, Patel DJ (2007) Structure of two intramolecular G-quadruplexes formed by natural human telomere sequences in K+ solution. Nucleic Acids Res 35:6517–6525CrossRefGoogle Scholar
  69. 69.
    da Silva MW, Trajkovski M, Sannohe Y, Hessari NM, Sugiyama H, Plavec J (2009) Design of a G-quadruplex topology through glycosidic bond angles. Angew Chem Int Ed 48:9167–9170CrossRefGoogle Scholar
  70. 70.
    Barnett RN, Cleveland CL, Joy A, Landman U, Schuster GB (2001) Charge migration in DNA: ion-gated transport. Science 294:567–571CrossRefGoogle Scholar
  71. 71.
    Sket P, Plavec J (2010) Tetramolecular DNA quadruplexes in solution: insights into structural diversity and cation movement. J Am Chem Soc 132:12724–12732CrossRefGoogle Scholar
  72. 72.
    Banyasz A, Vayá I, Changenet-Barret P, Gustavsson T, Douki T, Markovitsi D (2011) Base-pairing enhances fluorescence and favors cyclobutane dimer formation induced upon absorption of UVA radiation by DNA. J Am Chem Soc 133:5163–5165CrossRefGoogle Scholar
  73. 73.
    Banyasz A, Gustavsson T, Onidas D, Changenet-Barret P, Markovitsi D, Importa R (2013) Multi-pathway excited state relaxation of adenine oligomers in aqueous solution: a joint theoretical and experimental study. Chem Eur J. doi: 10.1002/chem.201202741 Google Scholar
  74. 74.
    Rochette P, Brash D (2010) Human telomers are hypersensitive to UV-induced DNA damage and refractory to repair. PLoS Genet 6:e1000926CrossRefGoogle Scholar
  75. 75.
    Su DGT, Fang HF, Gross ML, Taylor JSA (2009) Photocrosslinking of human telomeric G-quadruplex loops by anti cyclobutane thymine dimer formation. Proc Natl Acad Sci U S A 106:12861–12866CrossRefGoogle Scholar
  76. 76.
    Colson AO, Sevilla MD (1995) Elucidation of primary radiation damage in DNA through Application of ab initio molecular orbital theory. Int J Radiat Biol 67:627–645CrossRefGoogle Scholar
  77. 77.
    Kim NJ, Jeong G, Sung J, Kim YS, Park YD (2000) Resonant two-photon ionization and laser induced fluorescence spectroscopy of jet cooled adenine. J Chem Phys 113:10051–10055CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Pascale Changenet-Barret
    • 1
  • Ying Hua
    • 1
  • Dimitra Markovitsi
    • 1
  1. 1.CNRS, IRAMIS, LIDYL, Laboratoire Francis Perrin, URA 2453Gif-sur-YvetteFrance

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