Long - distance charge transport through DNA . An extended hopping model *

Long-distance transfer of a positive charge through DNA can be described by a hopping model. In double strands where the (A:T)n bridges between the guanines are short (n ≥ 3), the charge hops only between guanines, and each hopping step depends strongly upon the guanine to guanine distances. In strands where the (A:T)n sequences between the guanines are rather long (n ≥ 4), also the adenines act as charge carriers. To predict the yields of the H2O-trapping products one has to take into account not only the charge-transfer rates but also the rates of H2O-trapping reactions. In the 1990s, the question of long-distance electron transfer through DNA raised a controversial discussion [1]. We entered this area three years ago by studying radical-induced DNA strand cleavage reactions. Our experiments showed that photolysis of a 4'-acylated nucleoside in the DNA double strand 1 yields radical cation 2 that selectively oxidizes guanine (G) and forms a guanine radical cation (G) in 3 (Fig. 1) [2]. This reaction sequence led to an assay that made it possible to follow the charge migration through DNA by trapping of the positive charge at the heterocyclic base [3]. In order to understand the experimental results, we suggested in 1998 a hopping mechanism [3] for long-distance charge transport through DNA, which is based on the theoretical model of Jortner [4]. A similar hopping mechanism, which is slightly different in the details, was also suggested by Schuster [5], and today there is a con*Lecture presented at the XVIII IUPAC Symposium on Photochemistry, Dresden, Germany, 22–27 July 2000. Other presentations are published in this issue, pp. 395–548. †Corresponding author Fig. 1 Assay for the charge injection into a guanine (G). sensus that long-distance charge transport through DNA occurs by a multistep hopping process [6]. Out of the four natural heterocyclic bases guanine (G) has the lowest ionization potential [7], therefore G is the preferred carrier of the positive charge. Thus, in double strands 4–7 of Fig. 2 the positive charge hops between the guanines to the GGG unit, which has an even lower redox potential than a single G. Trapping of the guanosine radical cation (G) leads to products PG and PGGG that are separated and analyzed quantitatively by gel electrophoresis. This hopping model implies that the electron transfer from a G to a G is faster than the trapping reaction by H2O so that the charge should be partly distributed over the guanines before it is trapped [8]. Therefore, the yields of products PG decrease only slightly from PG1 to PG4, although the distance to the charge donor G1 •+ increases by 10 Å per each hopping step (Fig. 3). This slow decrease of the product yields must not be mixed up with a weak distance influence on the charge-transfer rate. It is the ratio between the charge transfer and the H2O-trapping rates that governs the product ratios (Fig. 4). We have quantitatively described this situation using the Curtin–Hammett principle [10]. The product ratio decreases only slightly as long as the H2O reaction is slower than the charge-transfer steps. Figure 5 shows how the charge migration from G1 via G2, G3, G4 to the GGG unit precedes the product formation. Despite this weak distance influence on the product formation, the influence of the distance on the charge-transfer rate kCT of each hopping step is large, and the β-value is about 0.7 Å –1 (Fig. 6) [3,9]. Thus, the electron-transfer rate between G and G over an (A:T)n bridge dramatically decreases with n until one reaches the situation in which the endothermic oxidation of the adjoining adenine (A) by G is as fast as the oxidation of a distant G [10]. Using a buffer at pH = 7, this seems to be the case if the number of A:T base pairs n of the (A:T)n bridge is larger than 3 where the charge-transfer rate between the guanines is smaller than 10 s. As shown in Fig. 7, in these strands also adenines (A) become charge carriers [10]. Once A is oxidized, the charge migrates in fast hopping steps between the B. GIESE et al. © 2001 IUPAC, Pure and Applied Chemistry 73, 449–453 450 Fig. 2 Yield of H2O-trapping products at the GGG sequence (PGGG) in long-distance charge transfer by a hopping between guanines (G).