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COMMENTS Exciting DNA Torsten Fiebig Boston College, 2609 Beacon Street, Chestnut Hill, Massachusetts 02467 ReceiVed: NoVember 19, 2008; ReVised Manuscript ReceiVed: April 20, 2009 Overexposure to sunlight causes DNA damage in sunburnt skin cells and may lead to irreparable genetic mutations. A cascade of gene mutation has recently been found to induce melanoma skin cancer.1 Most genetic mutations have been associated with free radicals as reactive intermediates, generated by the UV spectral component of sunlight. While the chemistry of DNA damage (and repair) has long been the target of research,2 details about the physical nature of excited states in DNA have only recently been discovered.3-6 Progress in the latter area has been achieved through continuous advancements in ultrafast laser spectroscopy, particularly through the development of broadband (from the UV to the near IR) probing techniques.7 More than a decade ago, the controversy surrounding the electric conduction properties of DNA8-10 stimulated many scientists to study DNA charge transfer reactions.11,12 At first, it seemed that this new field had not much in common with the pioneering studies on DNA photophysics in the 1950s and 1960s.13 Here, the central question was whether electronic excitation is localized on a single base pair or “spread out” over several base pairs, as a result of interbase excitonic coupling. The latest experimental and theoretical results4,5,14,15 have finally provided an answer to this longstanding question. Why are these results related to the DNA charge transfer field? Recently, Kohler et al. reported that charge transfer (or charge separation, to be exact!) occurs in the majority of natural DNA sequences without the addition of photosensitizers and artificial donor/ acceptor chromophores.6 Buchvarov et al. have demonstrated that electronic excitation in A-tracts leads instantaneously to delocalized exciton states.4 However, these exciton states are relatively short-lived (several picoseconds) compared to the overall excited state lifetime (several hundred picoseconds) observed in transient absorption experiments. The picture that emerges from these different studies is the following. The absorption of a UV photon leads to an exciton state that is delocalized along the base stack. The exact extent of this delocalization is dependent upon the local structure and sequence of the DNA. After a few picoseconds, the exciton states “collapse” into excited (hetero) dimeric base states (see Figure 1). Such exciplexes can vary in their electronic composition from highly polar contact ion pairs (CIP) to predominantly excitonic resonance states with relatively small dipole moments.16 The dipole moment (i.e., the degree of charge separation) is mainly dictated by the difference in redox potentials between the 16 possible adjacent base-base combinations. The recognition that charge separation may occur naturally in DNA as a pathway for excess energy dissipation raises a number of new and exciting questions, many of which have
Figure 1. Schematic representation of the early photophysical events in duplex DNA: The absorption of a photon leads to the collective excitation of several adjacent bases and populates a delocalized exciton state. After a few picoseconds, the exciton “collapses” into a localized exciplex with charge transfer character.
been addressed in the 1960s for organic crystals.17 For example, how fast can exciplexes migrate through the base stack? What are the fundamental differences between the transport of a single charge versus the transport of a pair of charge carriers? The decisive new elements in this discussion which distinguishes and separates DNA from organic crystals are the structural dynamics, i.e., the motions of the base pairs, the backbone, the surrounding solvent, and the counterions. Theorists have made substantial progress by including molecular dynamics in electronic structure calculations.18 However, most of the theoretical work until today has been focused on the transfer of single charge carriers. The description of delocalized base states, or even binary excited DNA base states, is immensely more difficult and requires electronic structure methods with expansive inclusion of electron correlation. One of the most important questions concerns the biological implication of exciplexes in DNA. It has often been speculated that the four natural bases (adenine, thymine, cytosine, and guanine), with their extreme short excited state lifetimes of several hundred femtoseconds, are the result of evolutionary selection (and amplification) because they rid the genome of harmful electronic excitations which are the precursors for chemical damage and mutations in DNA. However, as clearly established now through both time-resolved fluorescence and absorption experiments, the lifetimes of excited DNA base stacks have components that are seVeral thousand times longer than those of the individual bases. In other words, the deactivation channel for electronically excited DNA is determined by interchromophore coupling in the base stack and not by the intrinsic photophysical properties of its constituents. Does the presence of long-lived exciplexes exhibit an increased risk for cell damage? Can exciplexes function as precursor states for thymine dimerization?19 While these questions cannot be finally answered at this point, one may refer to the expansive body of work on exciplexes as photophysical intermediates, both in biomimetic and in artificial chromophore systems.20 A large number of exciplexes deactivate by radiative and/or radiationless recombination without irreversible chemical transformations. Since the fluorescence quantum yields of DNA are very small (e10-4), radiationless charge recombination clearly dominates
10.1021/jp8101783 CCC: $40.75 2009 American Chemical Society Published on Web 06/17/2009
Comments in base stacks. As the Kohler group has shown, the exciplex lifetimes depend largely on the individual base-base complex, ranging from 10 to 100 ps.6 Mataga et al. showed that the charge recombination rate of CIP is determined by the energy gap between the CIP and the ground state of the complex, as well as by specific vibrational modes of the complex.20 In general, the exciplex structure (tightly vs loosely bound) and the exciplex deactivation paths and rates depend strongly on the surrounding dielectrics and thus on the molecular environment. So far, most of the spectroscopic measurements on DNA have been carried out in aqueous solutions. The question of exciplex lifetimes and deactivation pathways must be readdressed in biologically more relevant systems, e.g., in DNA-wrapped histones. It is very possible that DNA displays new and unexpected abilities to rid itself of excess electronic energy in its “natural” environment. Acknowledgment. This work was supported by the National Science Foundation, Grant CHE 0628119. References and Notes (1) Martin, M. J.; et al. Cancer Cell 2009, 15, 123. (2) Friedberg, E. C. Nature 2003, 421, 436. (3) Crespo-Herna´ndez, C. E.; Cohen, B.; Kohler, B. Nature 2005, 436, 1141. (4) Buchvarov, I.; Wang, Q.; Raytchev, M.; Trifonov, A.; Fiebig, T. Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 4794.
J. Phys. Chem. B, Vol. 113, No. 27, 2009 9349 (5) Onidas, D.; Gustavsson, T.; Lazzarotto, E.; Markovitsi, D. J. Phys. Chem. B 2007, 111, 9644. (6) Takaya, T.; Su, C.; de La Harpe, K.; Crespo-Hernandez, C. E.; Kohler, B. Proc. Natl. Acad. Sci U.S.A. 2008, 105, 10285. (7) Raytchev, M.; Pandurski, E.; Buchvarov, I.; Modrakowski, C.; Fiebig, T. J. Phys. Chem. A 2003, 107, 4592. (8) Murphy, C. J.; Arkin, M. R.; Jenkins, Y.; Ghatlia, N. D.; Bossmann, S. H.; Turro, N. J.; Barton, J. K. Science 1993, 262, 1025. (9) Lewis, F. D.; Wu, T. F.; Zhang, Y. F.; Letsinger, R. L.; Greenfield, S. R.; Wasielewski, M. R. Science 1997, 277, 673. (10) Wan, C. Z.; Fiebig, T.; Kelley, S. O.; Treadway, C. R.; Barton, J. K.; Zewail, A. H. Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 6014. (11) Schuster, G. B., Ed. Long-Range Charge Transfer in DNA; Springer: Berlin, 2004; Vol. I & II. (12) Chakraborty, T., Ed. Charge Migration in DNA; Springer: Berlin, 2007. (13) Eisinger, J.; Shulman, R. G. Science 1968, 161, 1311. (14) Conwell, E. M.; McLaughlin, P. M.; Bloch, S. M. J. Phys. Chem. B 2008, 112, 2268. (15) Tonzani, S.; Schatz, G. C. J. Am. Chem. Soc. 2008, 130, 7607. (16) Weller A. In The Exciplex; Gordon, M., Ware, W. R., Eds.; Academic Press: New York, 1975; pp 23-38. (17) Sinanoglu, O., Ed. Modern Quantum Chemistry Part III: Action of Light and Organic Crystals; Academic Press: New York, 1965. (18) Barnett, R. N.; Cleveland, C. L.; Joy, A.; Landman, U.; Schuster, G. B. Science 2001, 294, 567. (19) Schreier, W. J.; Schrader, T. E.; Koller, F. O.; Gilch, P.; CrespoHernandez, C. E.; Swaminathan, V. N.; Carell, T.; Zinth, W.; Kohler, B. Science 2007, 315, 625. (20) Mataga, N.; Miyasaka, H. AdV. Chem. Phys. 1999, 107, 431.
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