Environmental Fluctuations Facilitate Electron‐Hole Transfer from Guanine to Adenine in DNA π Stacks

Voityuk, Alexander A.; Siriwong, Khatcharin; Rösch, Notker

doi:10.1002/anie.200352824

Cited by 126 publications

(190 citation statements)

References 36 publications

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“…The large amplitude of the computed fluctuations in the Hamiltonian makes it difficult to consider the electronic structure of DNA anyhow related to that of an idealized or 'averaged' structure. A similar observation was made also in other studies [14][15][16] and it is consistent with the variability of the intermolecular coupling computed using a set of crystallographic (static) structures. [11] The effect of these fluctuations on the electron dynamics depends on the charge transport mechanism, but there is not a consensus on the actual transport mechanism of positive charge in DNA and several contrasting hypotheses have been formulated.…”

Section: Dnasupporting

confidence: 91%

Charge dynamics through pi-stacked arrays of conjugated molecules: effect of dynamic disorder in different transport/transfer regimes

Troisi

2006

Molecular Simulation

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International audienceWe provide further computational evidence that the electronic coupling between pi-stacked molecules is strongly modulated by the thermal motions at room temperature, not only in supramolecular flexible systems (like DNA) but also in molecular crystals. The effect of this modulation on the charge dynamics is different for different transfer/transport mechanisms and depends on the modulation timescale. In the case of charge transfer between a donor and an acceptor, the effect of electronic coupling fluctuations introduces a corrective term in the expression of the rate constant (different for adiabatic and non-adiabatic charge transfer). For the transport in molecular crystals, this fluctuation can be the limiting factor for the charge mobility. Although the fluctuation of the electronic coupling is similar in magnitude for all systems containing molecular pi-stacking, its importance for the charge dynamics increases with the decrease of the reorganization energy

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Section: Dnasupporting

confidence: 91%

Charge dynamics through pi-stacked arrays of conjugated molecules: effect of dynamic disorder in different transport/transfer regimes

Troisi

2006

Molecular Simulation

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“…Hole density on the pyrimidines is found to be modulated by relative energies of bases on the same and opposite strand. Theoretical predictions have been made indicating the modulation of base ionization potentials in DNA by sequence-dependent structure (37) and dynamics (38). In this context, it is also interesting to consider the asymmetrical distribution of oxidative damage at the 5Ј-G of 5Ј-GG-3Ј doublets (39), observed after relatively slow secondary reactions leading to trapping of the G radical and ultimately DNA strand cleavage.…”

Section: Discussionmentioning

confidence: 99%

Long-range oxidative damage to cytosines in duplex DNA

Shao

O’Neill²,

Barton³

2004

Proc. Natl. Acad. Sci. U.S.A.

140

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Charge transport (CT) through DNA has been found to occur over long molecular distances in a reaction that is sensitive to intervening structure. The process has been described mechanistically as involving diffusive charge-hopping among low-energy guanine sites. Using a kinetically fast electron hole trap, N4-cyclopropylcytosine ( CP C), here we show that hole migration must involve also the higher-energy pyrimidine bases. In DNA assemblies containing either [Rh(phi)2(bpy )] 3؉ or an anthraquinone derivative, two highenergy photooxidants, appreciable oxidative damage at a distant CP C is observed. The damage yield is modulated by lower-energy guanine sites on the same or complementary strand. Significantly, the efficiency in trapping at CP C is equivalent to that at N2-cyclopropylguanosine ( CP G). Indeed, even when CP G and CP C are incorporated as neighboring bases on the same strand, their efficiency of photodecomposition is comparable. Thus, CT is not simply a function of the relative energies of the isolated bases but instead may require orbital mixing among the bases. We propose that charge migration through DNA involves occupation of all of the DNA bases with radical delocalization within transient structure-dependent domains. These delocalized domains may form and break up transiently, facilitating and limiting CT. This dynamic delocalized model for DNA CT accounts for the sensitivity of the process to sequence-dependent DNA structure and provides a basis to reconcile and exploit DNA CT chemistry and physics.charge transport ͉ delocalized domain ͉ radical trap ͉ base dynamics O xidative damage to DNA from a distance through longrange migration of charge has now been established in many DNA assemblies by using different pendant photooxidants through both biochemical and spectroscopic assays (1-8). The DNA base pair stack can mediate charge transport (CT) over at least 200 Å (2, 3), and the reaction is exquisitely sensitive to the dynamic structure and stacking within the DNA duplex (9, 10). This sensitivity to perturbations in base pair stacking has been advantageous in the development of DNA-based sensors for mutational analysis (11) and may provide a role for DNAmediated CT within the cell (12), but it has limited the application of physical techniques to explore CT mechanistically.Although not a robust molecular wire, the DNA duplex has in some experiments been characterized as a wide band gap semiconductor (13,14). More prevalent have been models of incoherent CT involving a mixture of localized charge-hopping among low-energy sites, guanines and sometimes adenines, and tunneling through higher-energy pyrimidine bases (15-18). These mechanisms do not provide a rationale, however, for the sensitivity of CT to DNA structure. We have observed that DNA CT is gated by the dynamical motions of the DNA bases (9, 19) and have described DNA CT as conformationally gated hopping through transient, well stacked DNA domains (20).Our experimental strategy to probe for hole density on pyrimidines exploits the rapid ...

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“…Standard deviations (σ E , SD) for DNA base energies estimated from quantum mechanical (QM) analysis of molecular dynamics (MD) sampled structures indicate σ E ≈ 0.2 eV without solvent (21-23); inclusion of solvent interactions increases these values to ∼0.3-0.5 eV (24,25). Fig.…”

Section: The Multisite Matching Probabilitymentioning

confidence: 99%

Biological charge transfer via flickering resonance

Zhang¹,

Liu²,

Balaeff³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

164

263

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Biological electron-transfer (ET) reactions are typically described in the framework of coherent two-state electron tunneling or multistep hopping. However, these ET reactions may involve multiple redox cofactors in van der Waals contact with each other and with vibronic broadenings on the same scale as the energy gaps among the species. In this regime, fluctuations of the molecular structures and of the medium can produce transient energy level matching among multiple electronic states. This transient degeneracy, or flickering electronic resonance among states, is found to support coherent (ballistic) charge transfer. Importantly, ET rates arising from a flickering resonance (FR) mechanism will decay exponentially with distance because the probability of energy matching multiple states is multiplicative. The distance dependence of FR transport thus mimics the exponential decay that is usually associated with electron tunneling, although FR transport involves real carrier population on the bridge and is not a tunneling phenomenon. Likely candidates for FR transport are macromolecules with ET groups in van der Waals contact: DNA, bacterial nanowires, multiheme proteins, strongly coupled porphyrin arrays, and proteins with closely packed redox-active residues. The theory developed here is used to analyze DNA charge-transfer kinetics, and we find that charge-transfer distances up to three to four bases may be accounted for with this mechanism. Thus, the observed rapid (exponential) distance dependence of DNA ET rates over distances of K K K K15 Å does not necessarily prove a tunneling mechanism.vibronic coupling | resonant tunneling pathways | superexchange | coherence | gated transport C hemical structure and, importantly, structural fluctuations determine the mechanism and kinetics of charge transfer. Redox energy fluctuations are of particular significance when transport barrier heights and the energy fluctuations are of similar magnitude. Indeed, the sensitivity of biological electrontransfer (ET) rates to conformational fluctuations and consequent (transient) delocalization is the topic of intense interest (1-3). Resonant enhancement of biological ET rates is consistent with a growing body of physical and structural data found in DNA ET through stacked nucleobases (4), extended delocalized structures of bacterial photosynthesis (including the special pair, bridging chlorophyll and pheophytin) (5), the polaronic states of oxidized porphyrin arrays up to seven porphyrin diameters in spatial extent (6), micrometer-scale bacterial nanowires (7, 8), multiheme oxidoreductases (9, 10), amino acid side chains in ribonucleotide reductase (11), engineered protein-based hopping-chains (12), and centimeter-scale charge-transport chains in filamentous bacteria (13). Here, we describe a transient or flickering resonance (FR) mechanism for ET. The FR mechanism arises when thermal fluctuations produce geometries that enable charge delocalization across the entire structure by bringing the donor (D), bridge (B), and acceptor (...

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Environmental Fluctuations Facilitate Electron‐Hole Transfer from Guanine to Adenine in DNA π Stacks

Cited by 126 publications

References 36 publications

Charge dynamics through pi-stacked arrays of conjugated molecules: effect of dynamic disorder in different transport/transfer regimes

Charge dynamics through pi-stacked arrays of conjugated molecules: effect of dynamic disorder in different transport/transfer regimes

Long-range oxidative damage to cytosines in duplex DNA

Biological charge transfer via flickering resonance

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