Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Base stacking controls excited-state dynamics in A·T DNA

Nature volume 436, pages 1141–1144 (2005)Cite this article

Abstract

Solar ultraviolet light creates excited electronic states in DNA that can decay to mutagenic photoproducts. This vulnerability is compensated for in all organisms by enzymatic repair of photodamaged DNA. As repair is energetically costly, DNA is intrinsically photostable. Single bases eliminate electronic energy non-radiatively on a subpicosecond timescale1, but base stacking and base pairing mediate the decay of excess electronic energy in the double helix in poorly understood ways. In the past, considerable attention has been paid to excited base pairs2. Recent reports have suggested that light-triggered motion of a proton in one of the hydrogen bonds of an isolated base pair initiates non-radiative decay to the electronic ground state3,4. Here we show that vertical base stacking, and not base pairing, determines the fate of excited singlet electronic states in single- and double-stranded oligonucleotides composed of adenine (A) and thymine (T) bases. Intrastrand excimer states with lifetimes of 50–150 ps are formed in high yields whenever A is stacked with itself or with T. Excimers limit excitation energy to one strand at a time in the B-form double helix, enabling repair using the undamaged strand as a template.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: DNA photophysical pathways as a function of base pairing and base stacking interactions.
Figure 2: Femtosecond pump–probe transients for the single-stranded oligonucleotide (dA) 18 (filled circles) and the 5′-mononucleotide AMP (open circles).
Figure 3: Transient absorption versus time at several probe wavelengths for the single-stranded oligonucleotide d(T) 18 (filled circles) and its constituent 5′-mononucleotide, TMP (open circles).
Figure 4: Singlet excited-state dynamics in double-stranded oligonucleotides. a, Transient absorption at indicated probe wavelengths (top, 570 nm; bottom, 250 nm) following 266 nm excitation of (dA)18·(dT)18 (triangles).

References

  1. Crespo-Hernández, C. E., Cohen, B., Hare, P. M. & Kohler, B. Ultrafast excited-state dynamics in nucleic acids. Chem. Rev. 104, 1977–2019 (2004)

    Article  Google Scholar 

  2. Löwdin, P. O. Proton tunneling in DNA and its biological implications. Rev. Mod. Phys. 35, 724–732 (1963)

    Article  ADS  Google Scholar 

  3. Schultz, T. et al. Efficient deactivation of a model base pair via excited-state hydrogen transfer. Science 306, 1765–1768 (2004)

    Article  ADS  CAS  Google Scholar 

  4. Abo-Riziq, A. et al. Photochemical selectivity in guanine-cytosine base-pair structures. Proc. Natl Acad. Sci. USA 102, 20–23 (2005)

    Article  ADS  CAS  Google Scholar 

  5. Cadet, J. & Vigny, P. in The Photochemistry of Nucleic Acids (ed. Morrison, H.) 1–272 (Wiley, New York, 1990)

    Google Scholar 

  6. Lamola, A. A. & Eisinger, J. Mechanism of thymine photodimerization. Proc. Natl Acad. Sci. USA 59, 46–51 (1968)

    Article  ADS  CAS  Google Scholar 

  7. Rahn, R. O. Search for an adenine photoproduct in DNA. Nucleic Acids Res. 3, 879–890 (1976)

    Article  CAS  Google Scholar 

  8. Danilov, V. I., Slyusarchuk, O. N., Alderfer, J. L., Stewart, J. J. P. & Callis, P. R. A theoretical study of the cytosine excimer state: The role of geometry optimization. Photochem. Photobiol. 59, 125–129 (1994)

    Article  CAS  Google Scholar 

  9. Eisinger, J., Guéron, M., Schulman, R. G. & Yamane, T. Excimer fluorescence of dinucleotides, polynucleotides, and DNA. Proc. Natl Acad. Sci. USA 55, 1015–1020 (1966)

    Article  ADS  CAS  Google Scholar 

  10. Vigny, P. Fluorescence of polyadenylic acid at room temperature. C.R. Acad. Sci. D 277, 1941–1944 (1973)

    CAS  Google Scholar 

  11. Douhal, A., Kim, S. K. & Zewail, A. H. Femtosecond molecular dynamics of tautomerization in model base pairs. Nature 378, 260–263 (1995)

    Article  ADS  CAS  Google Scholar 

  12. Rahn, R. O., Yamane, T., Eisinger, J., Longworth, J. W. & Shulman, R. G. Luminescence and electron spin resonance studies of adenine in various polynucleotides. J. Chem. Phys. 45, 2947–2954 (1966)

    Article  ADS  CAS  Google Scholar 

  13. Crespo-Hernández, C. E. & Kohler, B. Influence of secondary structure on electronic energy relaxation in adenine homopolymers. J. Phys. Chem. B 108, 11182–11188 (2004)

    Article  Google Scholar 

  14. Pecourt, J.-M. L., Peon, J. & Kohler, B. DNA excited-state dynamics: Ultrafast internal conversion and vibrational cooling in a series of nucleosides. J. Am. Chem. Soc. 123, 10370–10378 (2001)

    Article  CAS  Google Scholar 

  15. Dewey, T. G. & Turner, D. H. Laser temperature-jump study of stacking in adenylic acid polymers. Biochemistry 18, 5757–5762 (1979)

    Article  CAS  Google Scholar 

  16. Marguet, S. & Markovitsi, D. Time-resolved study of thymine photodimer formation. J. Am. Chem. Soc. 127, 5780–5781 (2005)

    Article  CAS  Google Scholar 

  17. Hosszu, J. L. & Rahn, R. O. Thymine dimer formation in DNA between 25 °C and 100 °C. Biochem. Biophys. Res. Commun. 29, 327–330 (1967)

    Article  CAS  Google Scholar 

  18. Ostrowski, T., Maurizot, J.-C., Adeline, M.-T., Fourrey, J.-L. & Clivio, P. Sugar conformational effects on the photochemistry of thymidylyl(3′–5′)thymidine. J. Org. Chem. 68, 6502–6510 (2003)

    Article  CAS  Google Scholar 

  19. Samoylova, E. et al. Dynamics of photoinduced processes in adenine and thymine base pairs. J. Am. Chem. Soc. 127, 1782–1786 (2005)

    Article  CAS  Google Scholar 

  20. Plützer, C., Hunig, I. & Kleinermanns, K. Pairing of the nucleobase adenine studied by IR-UV double-resonance spectroscopy and ab initio calculations. Phys. Chem. Chem. Phys. 5, 1158–1163 (2003)

    Article  Google Scholar 

  21. Cukier, R. I. & Nocera, D. G. Proton-coupled electron transfer. Annu. Rev. Phys. Chem. 49, 337–369 (1998)

    Article  ADS  CAS  Google Scholar 

  22. Azumi, T., Armstrong, A. T. & McGlynn, S. P. Energy of excimer luminescence. II. Configuration interaction between molecular exciton states and charge resonance states. J. Chem. Phys. 41, 3839–3852 (1964)

    Article  ADS  CAS  Google Scholar 

  23. Markovitsi, D., Sharonov, A., Onidas, D. & Gustavsson, T. The effect of molecular organization in DNA oligomers studied by femtosecond fluorescence spectroscopy. ChemPhysChem 4, 303–305 (2003)

    Article  CAS  Google Scholar 

  24. Kelley, S. O. & Barton, J. K. Electron transfer between bases in double helical DNA. Science 283, 375–381 (1999)

    Article  ADS  CAS  Google Scholar 

  25. Lewis, F. D., Zuo, X. B., Liu, J. Q., Hayes, R. T. & Wasielewski, M. R. Dynamics of inter- and intrastrand hole transport in DNA hairpins. J. Am. Chem. Soc. 124, 4568–4569 (2002)

    Article  CAS  Google Scholar 

  26. Glisin, V. & Doty, P. The cross-linking of DNA by ultraviolet radiation. Biochim. Biophys. Acta 142, 314–321 (1967)

    Article  CAS  Google Scholar 

  27. Kypr, J., Penazova, H., Sagi, J., Pospisilova, S. & Vorlickova, M. UV light-induced crosslinking of the strands of poly(dA-dT) and related alternating purine-pyrimidine DNAs. J. Biomol. Struct. Dyn. 11, 1225–1236 (1994)

    Article  CAS  Google Scholar 

  28. Douki, T., Laporte, G. & Cadet, J. Inter-strand photoproducts are produced in high yield within A-DNA exposed to UVC radiation. Nucleic Acids Res. 31, 3134–3142 (2003)

    Article  CAS  Google Scholar 

  29. Cantor, C. R., Warshaw, M. M. & Shapiro, H. Oligonucleotide interactions. 3. Circular dichroism studies of the conformation of deoxyoligonucleotides. Biopolymers 9, 1059–1077 (1970)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the NIH and performed using laser instrumentation in Ohio State's Center for Chemical and Biophysical Dynamics funded by the NSF. B.K. acknowledges support from the Alexander von Humboldt Foundation.

Author information

Authors and Affiliations

  1. Department of Chemistry, The Ohio State University, 100 W. 18th Avenue, Ohio, 43210, Columbus, USA

    Carlos E. Crespo-Hernández, Boiko Cohen & Bern Kohler

Authors
  1. Carlos E. Crespo-Hernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Boiko Cohen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bern Kohler
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bern Kohler.

Ethics declarations

Competing interests

Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Figures S1–S4

These 4 figures show the kinetic data from Figures 2 through 4 on conventional, linear time axes. (DOC 160 kb)

Supplementary Figure S5

This figure depicts the steady-state UV absorption spectra of the investigated compounds before and after 30 min of irradiation at the excitation pump wavelength of 266 nm. (DOC 42 kb)

Supplementary Figure S6

This figure shows the UV-melting profiles for the double-stranded oligonucleotides at 260 nm. This confirms that both (dA)18·(dT)18, and the alternating oligonucleotide, d(AT)9·d(AT)9 are double stranded at room temperature. (DOC 31 kb)

Supplementary Figure S7

This figure shows the room-temperature circular dichroism spectra for the double-stranded oligonucleotides. (DOC 28 kb)

Supplementary Tables S1–S4

These tables list the parameters obtained by global fitting to the kinetic traces presented in Figures 1 through 4 and Supplementary Figures 1 through 4. (DOC 74 kb)

Supplementary Discussion

This file contains discussion regarding the two photon absorption signal seen in the UV probe measurements. (DOC 20 kb)

Supplementary Methods

This file contains the methods used to measure circular dichroism spectra and melting profiles. (DOC 19 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Crespo-Hernández, C., Cohen, B. & Kohler, B. Base stacking controls excited-state dynamics in A·T DNA. Nature 436, 1141–1144 (2005). https://doi.org/10.1038/nature03933

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature03933

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing