Electronic coupling between photo-excited stacked bases in DNA and RNA strands with emphasis on the bright states initially populated

Photochemical and Photobiological Sciences

Volumn 12, Issue 8, 2013, Pages 1273-1285

  Nielsen, Lisbeth Munksgaard ^a   Hoffmann, Søren Vrønning ^a   Nielsen, Steen Brøndsted ^a  

^a AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; RNA;

ANIMAL; CHEMISTRY; CIRCULAR DICHROISM; CONFORMATION; HUMAN; PHOTOCHEMISTRY; RADIATION RESPONSE; RADIATION EXPOSURE; REVIEW;

ANIMALS; CIRCULAR DICHROISM; DNA; HUMANS; NUCLEIC ACID CONFORMATION; PHOTOCHEMICAL PROCESSES; RNA;

EID: 84881090106     PISSN: 1474905X     EISSN: 14749092     Source Type: Journal    
DOI: 10.1039/c3pp25438k     Document Type: Review

References (71)

1. C. E. Crespo-Hernandez B. Cohen P. M. Hare B. Kohler Ultrafast excited-state dynamics in nucleic acids Chem. Rev. 2004 104 1977 2019
2. C. T. Middleton K. de La Harpe C. Su Y. K. Law C. E. Crespo- Hernández B. Kohler DNA excited-state dynamics: from single bases to the double helix Annu. Rev. Phys. Chem. 2009 60 217 239
3. B. Kohler Nonradiative decay mechanisms in DNA model systems J. Phys. Chem. Lett. 2010 1 2047 2053
4. D. Markovitsi T. Gustavsson A. Banyasz Absorption of UV radiation by DNA: spatial and temporal features Mutat. Res., Rev. Mutat. Res. 2010 704 21 28
5. D. Markovitsi Interaction of UV radiation with DNA helices Pure Appl. Chem. 2009 81 1635 1644
6. D. Markovitsi T. Gustavsson I. Vayá Fluorescence of DNA duplexes: from model helices to natural DNA J. Phys. Chem. Lett. 2010 1 3271 3276
7. S. Brøndsted Nielsen J. U. Andersen J. S. Forster P. Hvelplund B. Liu U. V. Pedersen S. Tomita Photodestruction of adenosine 5′- monophosphate (AMP) nucleotide ions in vacuo: statistical versus nonstatistical processes Phys. Rev. Lett. 2003 91 048302
8. G. Aravind R. Antoine B. Klærke J. Lemoine A. Racaud D. B. Rahbek J. Rajput P. Dugourd L. H. Andersen Sub-microsecond photodissociation pathways of gas phase adenosine 5′-monophosphate nucleotide ions Phys. Chem. Chem. Phys. 2010 12 3486 3490
9. C. E. Crespo-Hernández B. Cohen B. Kohler Base stacking controls excited-state dynamics in A-T DNA Nature 2005 436 1141 1144
10. C. E. Crespo-Hernandez B. Cohen B. Kohler Molecular spectroscopy: complexity of excited-state dynamics in DNA-reply Nature 2006 441 E8
11. T. Takaya C. Su K. de La Harpe C. E. Crespo-Hernandez B. Kohler UV excitation of single DNA and RNA strands produces high yields of exciplex states between two stacked bases Proc. Natl. Acad. Sci. U. S. A. 2008 105 10285 10290
12. D. Markovitsi F. Talbot T. Gustavsson D. Onidas E. Lazzarotto S. Marguet Molecular spectroscopy: complexity of excited-state dynamics in DNA Nature 2006 441 E7
13. I. Vayá T. Gustavsson F.-A. Miannay T. Douki D. Markovitsi Fluorescence of Natural DNA: from the femtosecond to the nanosecond time scales J. Am. Chem. Soc. 2010 132 11834 11835
14. J. U. Andersen P. Hvelplund S. Brøndsted Nielsen S. Tomita H. Wahlgreen S. P. Møller U. V. Pedersen J. S. Forster T. J. D. Jørgensen The combination of an electrospray ion source and an electrostatic storage ring for lifetime and spectroscopy experiments on biomolecules Rev. Sci. Instrum. 2002 73 1284 1287
15. K. Støchkel U. Kadhane J. U. Andersen A. I. S. Holm P. Hvelplund M.-B. S. Kirketerp M. K. Larsen M. K. Lykkegaard S. Brøndsted Nielsen S. Panja H. Zettergren A new technique for time-resolved daughter ion mass spectrometry on the microsecond to millisecond time scale using an electrostatic ion storage ring Rev. Sci. Instrum. 2008 79 023107
16. A. J. Miles S. V. Hoffmann Y. Tao R. W. Janes B. A. Wallace Synchrotron radiation circular dichroism (SRCD) spectroscopy: new beamlines and new applications in biology Spectroscopy 2007 21 245 255
17. A. J. Miles R. W. Janes A. Brown D. T. Clarke J. C. Sutherland Y. Tao B. A. Wallace S. V. Hoffmann Light flux density threshold at which protein denaturation is induced by synchrotron radiation circular dichroism beamlines J. Synchrotron Radiat. 2008 15 420 422
18. I. Tinocor Jr. Physical chemistry of nucleic acids Annu. Rev. Phys. Chem. 2002 53 1 15
19. W. C. Johnson Jr. Circular-dichroism spectroscopy and vacuum ultraviolet region Annu. Rev. Phys. Chem. 1978 29 93 114
20. D. M. Gray S. H. Hung K. H. Johnson Absorption and circular dichroism spectroscopy of nucleic acid duplexes and triplexes Methods Enzymol. 1995 246 19 34
21. J. C. Sutherland K. P. Griffin P. C. Keck P. Z. Takacs Z-DNA-Vacuum ultraviolet circular-dichroism Proc. Natl. Acad. Sci. U. S. A. 1981 78 4801 4804
22. K. E. van Holde J. Brahms A. M. Michelson Base interactions of nucleotide polymers in aqueous solution J. Mol. Biol. 1965 12 726 739
23. C. R. Cantor I. Tinoco Jr. Absorption and optical rotatory dispersion of 7 trinucleoside diphosphates J. Mol. Biol. 1965 13 65 77
24. B. H. Johnston Generation and detection of Z-DNA Methods Enzymol. 1992 211 127 158
25. K. H. Johnson R. H. Durland M. E. Hogan The vacuum UV CD spectra of GGC triplexes Nucleic Acids Res. 1992 20 3859 3864
26. C. R. Cantor and P. R. Schimmel, Biophysical Chemistry part II, W. H. Freeman and Company, USA, 1980
27. J. Frenkel On the transformation of light into heat in solids. I Phys. Rev. 1931 37 17 44
28. S. Patwardhan S. Tonzani F. D. Lewis L. D. A. Siebbeles G. C. Schatz F. C. Grozema Effect of structural dynamics and base pair sequence on the nature of excited states in DNA hairpins J. Phys. Chem. B 2012 116 11447 11458
29. A. Czader E. R. Bittner Calculations of the exciton coupling elements between the DNA bases using the transition density cube methods J. Chem. Phys. 2008 128 035101
30. B. Bouvier T. Gustavsson D. Markovitsi P. Millié Dipolar coupling between electronic transitions of the DNA bases and its relevance to exciton states in double helices Chem. Phys. 2002 275 75 92
31. Y. C. Cheng G. R. Fleming Dynamics of light harvesting in photosynthesis Annu. Rev. Phys. Chem. 2009 60 241 262
32. B. Dick Circular dichroism of a finite number of identical chromophores in a helical arrangement ChemPhysChem 2011 12 1578 1587
33. C. Su C. T. Middleton B. Kohler Base-stacking disorder and excited-state dynamics in single-stranded adenine homo-oligonucleotides J. Phys. Chem. B 2012 116 10266 10274
34. J. Applequist V. Damle Thermodynamics of one-stranded helix-coil equilibrium in polyadenylic acid J. Am. Chem. Soc. 1966 88 3895 3900
35. M. Leng G. Felsenfeld A study of polyadenylic acid at neutral pH J. Mol. Biol. 1966 15 455 466
36. R. M. Epand H. A. Scheraga Enthalpy of stacking in single-stranded polyriboadenylic acid J. Am. Chem. Soc. 1967 89 3888 3892
37. J. A. Holbrook M. W. Capp R. M. Saecker M. T. Record Enthalpy and heat capacity changes for formation of an oligomeric DNA duplex: interpretation in terms of coupled processes of formation and association of single-stranded helices Biochemistry 1999 38 8409 8422
38. B. Bouvier J.-P. Dognon R. Lavery D. Markovitsi P. Millié D. Onidas K. Zakrzewska Influence of conformational dynamics on the exciton states of DNA oligomers J. Phys. Chem. B 2003 107 13512 13522
39. 1ππ* excitonic bright states J. Am. Chem. Soc. 2009 131 3913 3922
40. L. M. Nielsen S. Ø. Pedersen M.-B. S. Kirketerp S. Brøndsted Nielsen Absorption by DNA single strands of adenine isolated in vacuo: the role of multiple chromophores J. Chem. Phys. 2012 136 064302
41. V. Gabelica T. Tabarin R. Antoine F. Rosu I. Compagnon M. Broyer E. de Pauw P. Dugourd Electron photodetachment dissociation of DNA polyanions in a quadrupole ion trap mass spectrometer Anal. Chem. 2006 78 6564 6572
42. F. Rosu V. Gabelica E. de Pauw R. Antoine M. Broyer P. Dugourd UV spectroscopy of DNA duplex and quadruplex structures in the gas phase J. Phys. Chem. A 2012 116 5383 5391
43. J. C. Marcum A. Halevi J. M. Weber Photodamage to isolated mononucleotides-photodissociation spectra and fragment channels Phys. Chem. Chem. Phys. 2009 11 1740 1751
44. L. Li D. M. Lubman Ultraviolet visible absorption-spectra of biological molecules in the gas-phase using pulsed laser-induced volatilization enhancement in a diode-array spectrophotometer Anal. Chem. 1987 59 2538 2541
45. C. A. Sprecher W. C. Johnson Jr. Circular-dichroism of nucleic-acid monomers Biopolymers 1977 16 2243 2264
46. W. C. Johnson Jr. I. Tinoco Jr. Circular dichroism of polynucleotides-a simple theory Biopolymers 1969 7 727 749
47. U. Kadhane A. I. S. Holm S. V. Hoffmann S. Brøndsted Nielsen Strong coupling between adenine nucleobases in DNA single strands revealed by circular dichroism using synchrotron radiation Phys. Rev. E 2008 77 021901
48. A. I. S. Holm L. M. Nielsen S. V. Hoffmann S. Brøndsted Nielsen On the formation of the double helix between adenine single strands at acidic pH from synchrotron radiation circular dichroism experiments Biopolymers 2012 97 550 557
49. N. Ogasawara Y. Inoue Titration properties of homodinucleoside monophosphates-Determination of overlapping ionization-constants and intramolecular stacking equilibrium quotients of ApA, CpC, CpG, and UpU J. Am. Chem. Soc. 1976 98 7048 7053
50. L. M. Nielsen S. V. Hoffmann S. Brøndsted Nielsen Probing electronic coupling between adenine bases in RNA strands from synchrotron radiation circular dichroism experiments Chem. Commun. 2012 48 10425 10427
51. B. Jolles A. Laigle L. Chinsky P. Y. Turpin The poly dA strand of poly dA poly dT adopts an A-form in solution-a UV resonance Raman-study Nucleic Acids Res. 1985 13 2075 2085
52. D. Poerschke Analysis of a specific photoreaction in oligo- and polydeoxyadenylic acids J. Am. Chem. Soc. 1973 95 8440 8446
53. D. Poerschke A specific photoreaction in polydeoxyadenylic acid Proc. Natl. Acad. Sci. U. S. A. 1973 70 2683 2686
54. S. Kumar N. D. Sharma R. J. H. Davies D. W. Phillipson J. A. McCloskey The isolation and characterization of a new type of dimeric adenine photoproduct in UV-irradiated deoxyadenylates Nucleic Acids Res. 1987 15 1199 1216
55. P. H. Clingen R. J. H. Davies Quantum yields of adenine photodimerization in poly(deoxyadenylic acid) and DNA J. Photochem. Photobiol., B 1997 38 81 87
56. Y. Wang J.-S. Taylor M. L. Gross Isolation and mass spectrometric characterization of dimeric adenine photoproducts in oligodeoxynucleotides Chem. Res. Toxicol. 2001 14 738 745
57. S. Tonzani G. C. Schatz Electronic excitations and spectra in single-stranded DNA J. Am. Chem. Soc. 2008 130 7607 7612
58. A. I. S. Holm L. M. Nielsen S. V. Hoffmann S. Brøndsted Nielsen Vacuum-ultraviolet circular dichroism spectroscopy of DNA: a valuable tool to elucidate topology and electronic coupling in DNA Phys. Chem. Chem. Phys. 2010 12 9581 9596
59. A. I. S. Holm L. M. Nielsen B. Kohler S. V. Hoffmann S. Brøndsted Nielsen Electronic coupling between cytosine bases in DNA single strands and i-motifs revealed from synchrotron radiation circular dichroism experiments Phys. Chem. Chem. Phys. 2010 12 3426 3430
60. K. Gehring J. L. Leroy M. Gueron A tetrameric DNA-structure with protonated cytosine cytosine base-pairs Nature 1993 363 561 565
61. A. I. S. Holm B. Kohler S. V. Hoffmann S. Brøndsted Nielsen Synchrotron radiation circular dichroism of various G-quadruplex structures Biopolymers 2010 93 429 433
62. D. Nachtigallová P. Hobza H.-H. Ritze Electronic splitting in the excited states of DNA base homodimers and -trimers: an evaluation of short-range and Coulombic interactions Phys. Chem. Chem. Phys. 2008 10 5689 5697
63. H.-H. Ritze P. Hobza D. Nachtigallová Electronic coupling in the excited state of stacked DNA base homodimers Phys. Chem. Chem. Phys. 2007 9 1672 1675
64. R. Improta F. Santoro V. Barone A. Lami Vibronic model for the quantum dynamical study of the competition between bright and charge-transfer excited states in single-strand polynucleotides: the adenine dimer case J. Phys. Chem. A 2009 113 15346 15354
65. F. Santoro V. Barone R. Improta Influence of base stacking on excited-state behavior of polyadenine in water, based on time-dependent density functional calculations Proc. Natl. Acad. Sci. U. S. A. 2007 104 9931 9936
66. L. M. Nielsen A. I. S. Holm S. V. Hoffmann S. Brøndsted Nielsen Effect of introducing thymine spacers into an adenine strand: electronic decoupling? J. Photochem. Photobiol., A 2011 220 1 3
67. U. Kadhane A. I. S. Holm S. V. Hoffmann S. Brøndsted Nielsen Effect of the electronic coupling in dinucleotides and oligonucleotides of adenine and thymine from synchrotron radiation absorption and circular dichroism J. Photochem. Photobiol., A 2008 197 110 114
68. F. Plasser A. J. A. Aquino W. L. Hase H. Lischka UV absorption spectrum of alternating DNA duplexes. Analysis of excitonic and charge transfer interactions J. Phys. Chem. A 2012 116 11151 11160
69. I. Buchvarov Q. Wang M. Raytchev A. Trifonov T. Fiebig Electronic energy delocalization and dissipation in single- and double-stranded DNA Proc. Natl. Acad. Sci. U. S. A. 2007 104 4794 4797
70. D. Markovitsi T. Gustavsson F. Talbot Excited states and energy transfer among DNA bases in double helices Photochem. Photobiol. Sci. 2007 6 717 724
71. S. R. Mercier O. V. Boyarkin A. Kamariotis M. Guglielmi I. Tavernelli M. Cascella U. Rothlisberger T. R. Rizzo Microsolvation effects on the excited-state dynamics of protonated tryptophan J. Am. Chem. Soc. 2006 128 16938 16943