On the Long-Range Charge Transfer in DNA (original) (raw)

Sequence Dependent Long Range Hole Transport in DNA

Journal of the American Chemical Society, 1998

A guanine radical cation (G +• ) was site-selectively generated in double stranded DNA and the charge transfer in different oligonucleotide sequences was investigated. The method is based on the competition between a charge transfer from G +• through the DNA and its trapping reaction with H 2 O. We analyzed the hole transfer from this G +• to a GGG unit through one, two, three, and four AT base pairs and found that the rate decreases by about 1 order of magnitude with each intervening AT base pair. This strong distance dependence led to a -value of 0.7 ( 0.1 Å -1 . Within the time scale of this assay the charge transfer nearly vanished when the G +• was separated by four AT base pairs from the GGG unit. However, if the second or the third of the four intervening AT base pairs was exchanged by a GC base pair, the rate of the hole transfer from the G +• to the GGG unit increased by 2 orders of magnitude. In addition, a long-range charge transfer over 15 base pairs could be observed in a mixed strand that contained AT as well as GC base pairs. Because G +• can oxidize G but not A bases, the long-range charge transport can be explained by a hopping of the positive charge between the intervening G bases. Thus, the overall charge transport in a mixed strand is a multistep hopping process between G bases where the individual steps contribute to the overall rate. The distance dependence is no longer described by the value of the superexchange mechanism.

Absolute rates of hole transfer in DNA

Journal of The American Chemical Society, 2005

Absolute rates of hole transfer between guanine nucleobases separated by one or two A:T base pairs in stilbenedicarboxamide-linked DNA hairpins were obtained by improved kinetic analysis of experimental data. The charge-transfer rates in four different DNA sequences were calculated using a density-functional-based tight-binding model and a semiclassical superexchange model. Site energies and charge-transfer integrals were calculated directly as the diagonal and off-diagonal matrix elements of the Kohn-Sham Hamiltonian, respectively, for all possible combinations of nucleobases. Taking into account the Coulomb interaction between the negative charge on the stilbenedicarboxamide linker and the hole on the DNA strand as well as effects of base pair twisting, the relative order of the experimental rates for hole transfer in different hairpins could be reproduced by tight-binding calculations. To reproduce quantitatively the absolute values of the measured rate constants, the effect of the reorganization energy was taken into account within the semiclassical superexchange model for charge transfer. The experimental rates could be reproduced with reorganization energies near 1 eV. The quantum chemical data obtained were used to discuss charge carrier mobility and hole-transport equilibria in DNA.

Long-range and very long-range charge transport in DNA

Chemical Physics, 2002

We present a kinetic-quantum model for the mechanisms of hole transport in DNA duplexes, which involves a sequence of hole hopping processes between adjacent guanines (G) and/or hole hopping/trapping via GG or GGG, all of which are separated by thymine (T)-adenine (A) bridges. Individual hole hopping processes between G sites fall into two distinct parallel mechanisms, i.e., unistep superexchange mediated hopping via 'short' ðT-AÞ n bridges and thermally induced hopping (TIH) via 'long' ðT-AÞ n (n > 3-4) bridges. The bridge specificity for TIH via ðAÞ n chains pertains to the energetics, with the G þ A energy gap D ¼ 0:20 AE 0:05 eV being sufficiently low to warrant endothermic hole excitation from G þ to ðAÞ n , and to the electronic couplings, with the nearest-neighbor A-A couplings being unique in the sense that the intrastrand and interstrand couplings are close and large ðV ðA-AÞ ' 0:30-0:060 eVÞ. Accordingly, both effective intrastrand and interstrand (zigzagging) hole transport via ðAÞ n chains will prevail, being nearly invariant with respect to the nucleobases ordering within the ðT-AÞ n duplex. We treated the 'transition' between the superexchange and the TIH mechanism in 5 0 -G þ ðT-AÞ n G-3 0 duplexes to predict that the crossover occurs at n x ' 3-4, with n x exhibiting a moderate bridge specificity and energy gap dependence. n x is in accord with the experimental data of Giese et al. [Nature 412, 318, 2001]. We assert that the kinetic-quantum mechanical model for the chemical yields and elementary rates cannot be reconciled with the experimental TIH data, with respect to the very weak bridge size dependence of the relative chemical yields and the ratios of the rates. Configurational relaxation accompanying endothermic hole injection from G þ to ðAÞ n may result in the gating (switching-off) of the backrecombination, providing a reasonable description of TIH dynamics and very long-range hole transport in long ðAÞ n chains. Ó (J. Jortner). 0301-0104/02/$ -see front matter Ó 2002 Published by Elsevier Science B.V. PII: S 0 3 0 1 -0 1 0 4 ( 0 2 ) 0 0 4 9 5 -0

Elementary steps for charge transport in DNA: thermal activation vs. tunneling

Chemical Physics, 2002

Using stacks of Watson-Crick base pairs as an important example of multichromophoric molecular assemblies, we studied charge migration in DNA with special emphasis on the mechanism of hole hopping between neighboring guanines (G) connected by the adenine-thymine (AT) bridge. The tight-binding model proposed for this elementary step shows that for short AT bridges, hole transfer between two G bases proceeds via quantum mechanical tunneling. By contrast, hopping over long bridges requires thermal activation. The condition for crossover between tunneling and thermal activation near room temperature is specified and applies to the analysis of experimental data. We show that thermal activation dominates, if the bridge between two G bases contains more than three AT pairs. Our theoretical findings predict that the replacement of AT base pairs by GC pairs increases the efficiency of hole transport only in the case of short base pair sequences. For long sequences, however, the opposite effect is expected. Ó

The Dynamics of Hole Transfer in DNA

Molecules

High-energy radiation and oxidizing agents can ionize DNA. One electron oxidation gives rise to a radical cation whose charge (hole) can migrate through DNA covering several hundreds of Å, eventually leading to irreversible oxidative damage and consequent disease. Understanding the thermodynamic, kinetic and chemical aspects of the hole transport in DNA is important not only for its biological consequences, but also for assessing the properties of DNA in redox sensing or labeling. Furthermore, due to hole migration, DNA could potentially play an important role in nanoelectronics, by acting as both a template and active component. Herein, we review our work on the dynamics of hole transfer in DNA carried out in the last decade. After retrieving the thermodynamic parameters needed to address the dynamics of hole transfer by voltammetric and spectroscopic experiments and quantum chemical computations, we develop a theoretical methodology which allows for a faithful interpretation of th...

Charge Transport in DNA Via Thermally Induced Hopping

Journal of the American Chemical Society, 2001

In this contribution we advance and explore the thermally induced hopping (TIH) mechanism for long-range charge transport (CT) in DNA and in large-scale chemical systems. TIH occurs in donor-bridgeacceptor systems, which are characterized by off-resonance donor-bridge interactions (energy gap ∆E > 0), involving thermally activated donor-bridge charge injection followed by intrabridge charge hopping. We observe a "transition" from superexchange to TIH with increasing the bridge length (i.e., the number N of the bridge constituents), which is manifested by crossing from the exponential N-dependent donor-acceptor CT rate at low N (< N X) to a weakly (algebraic) N-dependent CT rate at high N (>N X). The "critical" bridge size N X is determined by the energy gap, the nearest-neighbor electronic couplings, and the temperature. Experimental evidence for the TIH mechanism was inferred from our analysis of the chemical yields for the distal/proximal guanine (G) triplets in the (GGG) + TTXTT(GGG) duplex (X) G, azadine (z A), and adenine (A)) studied by Nakatani, Dohno and Saito [J. Am. Chem. Soc. 2000, 122, 5893]. The TIH sequential model, which involves hole hopping between (GGG) and X, is analyzed in terms of a sequential process in conjunction with parallel reactions of (GGG) + with water, and provides a scale of (free) energy gaps (relative to (GGG) +) of ∆) 0.21-0.24 eV for X) A, ∆) 0.10-0.14 eV for X) z A, and ∆) 0.05-0.10 eV for X) G. We further investigated the chemical yields for long-range TIH in (G) l + X n (G) l (l) 1-3) duplexes, establishing the energetic constraints (i.e., the donor (G) l +bridge base (X) energy gap ∆), the bridge structural constraints (i.e., the intrabridge X-X hopping rates k m), and the kinetic constraints (i.e., the rate k d for the reaction of (G) l + with water). Effective TIH is expected to prevail for ∆ j 0.20 eV with a "fast" water reaction (k d /k m = 10-3) and for ∆ < 0.30 eV with a "slow" water reaction (k d /k m = 10-5). We conclude that (T) n bridges (for which ∆ = 0.6 eV) cannot act in TIH of holes. From an analysis based on the energetics of the electronic coupling matrix elements in G + (T-A) n (GGG) duplexes we conclude that the superexchange mechanism is expected to dominate for n) 1-4. For long (A) n bridges (n J 4) the TIH prevails, provided that the water side reaction is slow, raising the issue of chemical control of TIH through long (A) n bridges in DNA attained by changing the solution composition. I. Prologue Apart from the fundamental interest in the electronic properties of DNA in the context of radiation damage and repair, 1,2 novel research areas of the dynamics, response, and function of nanostructures and biosensors are emerging. 3 DNA-based molecular electronic devices are expected to utilize the unique features of recognition, assembly, and specific binding properties of the nucleobases. The DNA duplexes may serve as conducting building blocks or as insulating (or conducting) templates for the assembly of other electrically active nanoelements, for example, semiconducting or metal clusters. While presently nanoelectronic DNA-based systems still constitute "theoreticians' dreams", the elucidation of the mechanism and dynamics of charge transport/transfer in DNA is of central importance. The majority of the experimental information on charge transport in DNA pertains to the positive charge (hole) migration, that is, the propagation of the radical cation along the duplex. 4-13 In view of the hierarchy of the oxidation potentials of single nucleobases in solution 14 and of the ionization

Hole Trapping, Detrapping, and Hopping in DNA †

The Journal of Physical Chemistry A, 2001

In this paper we present a self-consistent kinetic-quantum mechanical analysis of chemical yield data for hole trapping/detrapping in G + (T-A) m GGG duplexes (with free energy gaps ∆ t ) and for hole hopping/trapping/ detrapping in G + [(T) m G] n (T) m GGG duplexes of DNA. Bridge specificity of hole trapping/detrapping by GGG traps was specified by superexchange electronic contributions, inferred from electronic coupling matrix elements between nearest-neighbor nucleobases and semiempirical energy gaps, and energetic contributions, which determine the nuclear Franck-Condon factors. Unistep hole-trapping yields are accounted for by a weak bridge length dependence for short (N ) 1, 2) bridges, due to detrapping. Marked bridge specificity is manifested for short (N ) 1, 2) bridges, being distinct for (T) N and for [(A) m+1 (T) m′ ] n (m, m′ g 0 and N ) n(m + m′ + 1)) bridges. For long (N > 2) bridges an exponential bridge size dependence of the trapping yields prevails. Multistep hole transport results in different reaction rates of G + (rate k d ) and of (GGG) + (rate k dt ) with water, i.e., k d /k dt ) 1.6, which, in conjunction with the unistep trapping/detrapping data, results in the free energy gaps for hole trapping of ∆ t ) 0.096 eV in the G + (T) N GGG duplexes and of ∆ t ) 0.062 eV in the G + [(A) m+1 (T) m′ ] n GGG duplexes.

Superexchange Mediated Charge Hopping in DNA †

The Journal of Physical Chemistry A, 2002

We explore the relationship between the electronic-nuclear level structure, the electronic couplings, and the dynamics of hole hopping transport in DNA. We utilized the electronic coupling matrix elements for hole transfer between nearest-neighbor nucleobases in DNA Rösch, N. J. Chem. Phys. 2001, 114, 5614] to evaluate intrastrand and interstrand superexchange electronic couplings, which determine hole hopping rates within the framework of a semiempirical quantum mechanical-kinetic model. Calculations of the exponential distance (R) dependence of the superexchange mediated intrastrand electronic couplings |V super | 2 ∝ exp(-R) between guanines (G) in "short" G + (T-A) n G (n j 3) duplexes result in ) 0.8-0.9 Å -1 . We interpret the experimental data on time-resolved hole transport in the presence of a site-specifically bound methyl transferase mutant in DNA [Wagenknecht, H.-A.; Rajski, S. R.; Pascally, M.; Stemp, E. D. A.; Barton, J. K. J. Am. Chem. Soc. 2001, 123, 4400] in terms of composite sequential, interstrand and intrastrand superexchange mediated, and direct interstrand hole hopping. This mechanism accounts for the rate determining step, for the weak duplex size dependence of the rate, and for the longrange charge transport induced by interstrand superexchange via short (T-A) bridges, containing a single mediating nucleobase. For hole transfer via longer (T-A) n (n J 3) bridges, the superexchange mechanism is replaced by the parallel mechanism of thermally induced hole hopping (TIH) via long (A) n chains. A kinetic analysis of the experimental data for hole transport through seven GG pairs separated by (T-A) n (n ) 2-5) bridges across the 3′-5′ strand of the DNA duplex Schuster, G. B. J. Phys. Chem. B, 2001, 105, 11057] reveals that the superexchange-TIH crossover occurs at n ) n x ) 3. The explorations of the range of applicability and the breakdown of the superexchange mechanism in DNA lay the foundations for the scrutiny of the universality and system specificity of this mechanism in large-scale chemical and biophysical systems.