Electronic excitations in guanine quadruplexes

Topics in Current Chemistry

Volumn 356, Issue , 2015, Pages 183-202

  Changenet Barret, Pascale ^a   Hua, Ying ^a   Markovitsi, Dimitra ^a  

^a CNRS   (France)

Author keywords

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

Indexed keywords

CYTOSINE; GUANINE; GUANINE QUADRUPLEX;

CHEMICAL STRUCTURE; CHEMISTRY; ENERGY TRANSFER; PHOTOCHEMISTRY; RADIATION RESPONSE; SPECTROFLUOROMETRY; ULTRAVIOLET RADIATION;

CYTOSINE; ENERGY TRANSFER; G-QUADRUPLEXES; GUANINE; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PHOTOCHEMICAL PROCESSES; SPECTROMETRY, FLUORESCENCE; ULTRAVIOLET RAYS;

EID: 84924040596     PISSN: 03401022     EISSN: None     Source Type: Book Series    
DOI: 10.1007/128_2013_511     Document Type: Article

References (77)

1. Huppert JL (2008) Four-stranded nucleic acids: structure, function and targeting of G-quadruplexes. Chem Soc Rev 37:1375–1384.
2. Neidle S (2009) The structures of quadruplex nucleic acids and their drug complexes. Curr Opin Struct Biol 19:239–250.
3. Biffi G, Tannahill D, McCafferty J, Balasubramanian S (2013) Quantitative visualization of DNA G-quadruplex structures in human cells. Nat Chem 5:182–186.
4. De Cian A, Lacroix L, Douarre C, Temime-Smaali N, Trentesaux C, Riou JF, Mergny JL (2008) Targeting telomeres and telomerase. Biochimie 90:131–155.
5. Ruden M, Puri N (2013) Novel anticancer therapeutics targeting telomerase. Cancer Treat Rev 39:444–456.
6. Neidle S, Parkinson G (2002) Telomere maintenance as a target for anticancer drug discovery. Nat Rev Drug Discov 1:383–393.
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 36:5050–5060.
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 49:3313–3316.
9. Lee JB, Campolongo MJ, Kahn JS, Roh YH, Hartman MR, Luo D (2010) DNA-based nanostructures for molecular sensing. Nanoscale 2:188–197.
10. Chaires BJ, Graves D (eds) (2013) Quadruplex nucleic acids, vol 330. Top Curr Chem Springer
11. Markovitsi D, Gustavsson T, Sharonov A (2004) Cooperative effects in the photophysical properties of self-associated triguanosine diphosphates. Photochem Photobiol 79:526–530.
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 5158–5160.
13. Gepshtein R, Huppert D, Lubitz I, Amdursky N, Kotlyar AB (2008) Radiationless transitions of G4 wires and dGMP. J Phys Chem C 112:12249–12258.
14. Miannay FA, Banyasz A, Gustavsson T, Markovitsi D (2009) Excited states and energy transfer in G-quadruplexes. J Phys Chem C 113:11760–11765.
15. Mendez MA, Szalai VA (2009) Fluorescence of unmodified oligonucleotides: a tool to probe G-quadruplex DNA structure. Biopolymers 91:841–850.
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 114:14339–14346.
17. Dumas A, Luedtke NW (2010) Cation-mediated energy transfer in G-quadruplexes revealed by an internal fluorescent probe. J Am Chem Soc 132:18004–18007.
18. Dao NT, Haselsberger R, Michel-Beyerle ME, Phan AT (2011) Following G-quadruplex formation by its intrinsic fluorescence. FEBS Lett 585:3969–3977.
19. Hua Y, Changenet-Barret P, Improta R, Vaya´ 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 116:14682–14689.
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 15:7396–7402.
21. Dao NT, Haselsberger R, Michel-Beyerle ME, Phan AT (2013) Excimer formation by stacking G-Quadruplex blocks. ChemBioChem 1–5.
22. Kwok CK, Sherlock ME, Bevilacqua PC (2013) Effect of loop sequence and loop length on the intrinsic fluorescence of G-quadruplexes. Biochemistry 52:3019–3021.
23. Kotlyar AB, Borovok N, Molotsky T, Cohen H, Shapir E, Porath D (2005) Long, monomolecular guanine-based nanowires. Adv Mater 17:1901–1905.
24. Burge S, Parkinson GN, Hazel P, Todd AK, Neidle S (2006) Quadruplex DNA: sequence, topology and structure. Nucleic Acids Res 34:5402–5415.
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, Cambridge
26. Qin Y, Hurley LH (2008) Structures, folding patterns, and functions of intramolecular DNA G-quadruplexes found in eukaryotic promoter regions. Biochimie 90:1149–1171.
27. Starikov EB (2004) Importance of charge transfer excitations in DNA electron spectrum: a ZINDO semiempirical quantum-chemical study. Mod Phys Lett B 18:825–831.
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 110:7129–7138.
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 131:15232–15245.
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 131:3913–3922.
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 116:11151–11160.
32. Mergny JL, Phan AT, Lacroix L (1998) Following G-quartet formation by UV-spectroscopy. FEBS Lett 435:74–78.
33. Bouvier B, Dognon JP, Lavery R, Markovitsi D, Millie´ P, Onidas D, Zakrzewska K (2003) Influence of conformational dynamics on the exciton states of DNA oligomers. J Phys Chem B 107:13512–13522.
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 109:16109–16118.
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 8:2683–2692.
36. Randazzo A, Spada GP, Webba da Silva M (2013) Circular dichroism of quadruplex structures. Top Curr Chem 330:67–86.
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 127:17130–17131.
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 129:14574–14575.
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 9:5143–5148.
40. Vaya´ I, Gustavsson T, Douki T, Berlin Y, Markovitsi D (2012) Electronic excitation energy transfer between nucleobases of natural DNA. J Am Chem Soc 134:11366–11368.
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 106:11367–11374.
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 103:2327–2346.
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 105:4485–4494.
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 103:12672–12677.
45. Albrecht AC (1961) Polarizations and assignments of transitions – method of photoselection. J Mol Spectrosc 6:84–108.
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 132:11834–11835.
47. Schwalb N, Temps F (2007) Ultrafast electronic excitation in guanosine is promoted by hydrogen bonding with cytidine. J Am Chem Soc 129:9272–9273.
48. Vaya´ I, Miannay FA, Gustavsson T, Markovitsi D (2010) High energy long-lived excited states in DNA double strands. ChemPhysChem 11:987–989.
49. Vaya´ I, Changenet-Barret P, Gustavsson T, Zikich D, Kotlyar A, Markovitsi D (2010) Longlived fluorescence of homopolymeric guanine-cytosine DNA duplexes. Photochem Photobiol Sci 9:1193–1195.
50. Brazard J, Thazhathveetil A, Vaya´ I, Lewis F, Gustavsson T, Markovitsi D (2013) Electronic excited states of guanine-cytosine hairpins and duplexes studied by fluorescence spectroscopy. Photochem Photobiol Sci 12:1453–1459.
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 102:17903–17906.
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 129:6812–6819.
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 133:19664–19667.
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 111:9644–9650.
55. Markovitsi D, Gustavsson T, Talbot F (2007) Excited states and energy transfer among DNA bases in double helices. Photochem Photobiol Sci 6:717–724.
56. Gustavsson T, Improta R, Markovitsi D (2010) DNA/RNA: building blocks of life under UV irradiation. J Phys Chem Lett 1:2025–2030.
57. Kleinermanns K, Nachtigallova´ D, de Vries MS (2013) Excited state dynamics of DNA bases. Int Rev Phys Chem. doi:10.1080/0144235X.0142012.0760884.
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 131:5839–5850.
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 114:3256–3263.
60. Kasha M, Rawls HR, El-Bayoumi MA (1965) The exciton model in molecular spectroscopy. Pure Appl Chem 11:371–392.
61. Spano FC (2010) The spectral signatures of Frenkel polarons in H- and J-aggregates. Acc Chem Res 43:429–439.
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 50:10645–10648.
63. Hua Y (2013) Self-associated gunanine structures studied by time-resolved optical spectroscopy. Université de Paris Sud, Orsay
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 40:29–37.
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 13:540–551.
66. Wang Y, Patel DJ (1993) Solution structure of the human telomeric repeat d[AG3(T2AG3)3] G-tetratraplex. Structure 1:263–282.
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 128:9963–9970.
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 35:6517–6525.
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 48:9167–9170.
70. Barnett RN, Cleveland CL, Joy A, Landman U, Schuster GB (2001) Charge migration in DNA: ion-gated transport. Science 294:567–571.
71. Sket P, Plavec J (2010) Tetramolecular DNA quadruplexes in solution: insights into structural diversity and cation movement. J Am Chem Soc 132:12724–12732.
72. Banyasz A, Vaya´ 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 133:5163–5165.
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.
74. Rochette P, Brash D (2010) Human telomers are hypersensitive to UV-induced DNA damage and refractory to repair. PLoS Genet 6:e1000926.
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 106:12861–12866.
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 67:627–645.
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 113:10051–10055