Development of a metal-ion-mediated base pair for electron transfer in DNA

Article abstract of DOI:10.1002/chem.201300593

A new C-nucleoside structurally based on the hydroxyquinoline ligand was synthesized that is able to form stable pairs in DNA in both the absence and the presence of metal ions. The interactions between the metal centers in adjacent Cu^II-mediated base pairs in DNA were probed by electron paramagnetic resonance (EPR) spectroscopy. The metal-metal distance falls into the range of previously reported values. Fluorescence studies with a donor-DNA-acceptor system indicate that photoinduced charge-transfer processes across these metal-ion-mediated base pairs in DNA occur more efficiently than over natural base pairs. Ace of base: DNA duplex stability can be significantly increased by coordinating Cu^II ions to hydroxyquinoline base pairs (metal-mediated base pairing; see scheme). Fluorescence studies with a donor-DNA-acceptor system indicate that photoinduced charge-transfer processes across these metal-ion-mediated base pairs in DNA occur more efficiently than over natural base pairs. Copyright

Full text of DOI:10.1002/chem.201300593

FULL PAPER
Ace of base: DNA duplex stability can
be significantly increased by coordinat-
ing CuII ions to hydroxyquinoline base
pairs (metal-mediated base pairing;
see scheme). Fluorescence studies with
a donor–DNA–acceptor system indi-
cate that photoinduced charge-transfer
processes across these metal-ion-medi-
ated base pairs in DNA occur more
efficiently than over natural base pairs.
DNA
T. Ehrenschwender, W. Schmucker,
C. Wellner, T. Augenstein, P. Carl,
J. Harmer, F. Breher,*
H.-A. Wagenknecht* ......... &&&& — &&&&
Development of a Metal-Ion-Mediated
Base Pair for Electron Transfer in
DNA
Chem. Eur. J. 2013, 00, 0 – 0
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DOI: 10.1002/chem.201300593
Development of a Metal-Ion-Mediated Base Pair for Electron Transfer in
DNA
Thomas Ehrenschwender,[a] Wolfgang Schmucker,[a] Christian Wellner,[a]
Timo Augenstein,[b] Patrick Carl,[c] Jeffrey Harmer,[d] Frank Breher,*[b] and
Hans-Achim Wagenknecht*[a]
Abstract: A new C-nucleoside structur-
ally based on the hydroxyquinoline
ligand was synthesized that is able to
form stable pairs in DNA in both the
absence and the presence of metal
ions. The interactions between the
metal centers in adjacent CuII-mediat-
ed base pairs in DNA were probed by
electron
paramagnetic
resonance
ously reported values. Fluorescence
studies with a donor–DNA–acceptor
system indicate that photoinduced
charge-transfer processes across these
metal-ion-mediated base pairs in DNA
occur more efficiently than over natu-
ral base pairs.
(EPR) spectroscopy. The metal–metal
distance falls into the range of previ-
Keywords: copper · DNA · donor–
acceptor systems · electron transfer ·
nucleosides
Introduction
planarity and size of the corresponding metal complexes
ensure their proper intercalation within the DNA base
stack. Typically, the thermal stabilities of metal-mediated
DNA duplexes are strongly enhanced relative to duplexes
with normal hydrogen-bond interactions. By applying this
strategy, one-dimensional arrays of metal ions inside the
DNA helix were realized.[4–6] Moreover, correct replication
of a manganese–salen (salen=N,N’-bis(salicylidene)ethyle-
nediamine) complex as an artificial DNA base pair has been
achieved recently.[7]
Apart from the biological role of DNA as the carrier for ge-
netic information, the regular geometry of double-stranded
DNA can be regarded as a promising template for the gen-
eration of new functionalized molecular architectures.[1,2] In
particular, the specific and spontaneous self-assembly of two
oligonucleotides encoded by the canonical base pairing rep-
resents the most attractive aspect of DNA with respect to
new supramolecular structures with artificial functions. Over
the last decade, research on a new generation of such nu-
cleoside mimics was published that replaces the hydrogen-
bonding interface by metal-mediated base pairing.[3] The ad-
vantage of this modification strategy is that it allows one to
arrange metal ions in the interior of the DNA duplex. The
Herein we present the synthesis and evaluation of a new
metal-mediated base pair that is based on the hydroxyquino-
line ligand as part of C-nucleoside 1 (Hq, Scheme 1). A sim-
[a] Dr. T. Ehrenschwender, Dr. W. Schmucker, C. Wellner,
Prof. Dr. H.-A. Wagenknecht
Karlsruhe Institute of Technology (KIT)
Institute of Organic Chemistry
Fritz-Haber-Weg 6, 76131 Karlsruhe (Germany)
Fax : (+49)721-608-44825
E-mail: wagenknecht@kit.edu
Scheme 1. Nucleosides T, 1, and 2[8]
.
[b] Dipl.-Chem. T. Augenstein, Prof. Dr. F. Breher
Karlsruhe Institute of Technology (KIT)
Institute of Inorganic Chemistry
Engesserstrasse 15, 76131 Karlsruhe (Germany)
Fax : (+49)721-608-47021
E-mail: breher@kit.edu
ilar nucleoside (2) in which the sugar part was linked to the
6-position of hydroxyquinoline has been published by
Zhang and Meggers.[8] However, attachment to the 7-posi-
tion in nucleoside 1 provides more structural similarity with
natural pyridimine nucleosides. The hydrogen-bonding inter-
face of 1 in particular is placed in such a way (“ortho-like”),
that a hydrogen-bonded base pair can be expected if two of
the Hq nucleosides are placed opposite to each other in
DNA double strands. Another advantage of nucleoside 1
[c] Dr. P. Carl
Bruker BioSpin GmbH, Silberstreifen 4
76287 Rheinstetten (Germany)
[d] Dr. J. Harmer
Centre for Advanced Imaging, University of Queensland
St Lucia, QLD, 4072 (Australia)
Supporting information for this article is available on the WWW
under http://dx.doi.org/10.1002/chem.201300593.
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Electron Transfer in DNA
FULL PAPER
Table 1. Melting temperatures (Tm, [8C]) of Hq-modified DNA duplexes
relative to 2 is that the number of synthetic steps can be sig-
nificantly reduced, thus the whole procedure is facilitated.
in the absence and in the presence of CuII.
Sample
Tm (10 mm EDTA)
DTm without CuII
Tm with CuII
DNA1
DNA2
DNA3
DNA4
DNA5
DNA6
DNA7
DNA8
DNA9
58.0
57.6
59.3
49.0
45.7
59.2
60.9
59.4
58.3
ꢀ1.0[a]
ꢀ3.4[a]
ꢀ2.0[a]
n.d.[e]
80.0[b]
>90[c]
>90[d]
71.0[f]
Results and Discussion
The preparation starts with glycal 3 that possesses two tert-
butyldimethylsilyl (TBDMS) groups protecting the 3’- and
5’-hydroxy functions (Scheme 2).[9] The central step of the
n.d.[e]
79.0[g]
77.4[b]
>90[c]
73.5[b]
>90[c]
+0.2[h]
ꢀ0.1[h]
+0.4[h]
ꢀ2.7[h]
[a] With A–T base pairs instead of Hq–Hq pairs. [b] 1.5 equiv of CuCl2.
[c] 3.0 equiv of CuCl2. [d] 4.0 equiv of CuCl2. [e] Not determined. [f] 1.1
equiv of CuCl2. [g] 2.2 equiv of CuCl2. [h] With A–T base pairs instead of
Hq–Hq pairs and T instead of Dp–U and Ap–dU.
DNA1 exhibits a melting point (Tm) of 58.08C. Compared
to a completely unmodified duplex with an A–T base pair
instead of the Hq–Hq pair, the Tm of DNA1 is decreased by
only 1.08C. This is a remarkably low value relative to the
previously reported hydroquinoline base pair with the sugar
moiety attached to the 6-position.[8] In the latter case, the
exchange of an A–T pair by the Hq ligand pair results in a
significant destabilization of 5.28C.[8] The low destabilization
of our Hq–Hq pair in DNA1 indicates—according to its tail-
ored architecture—the formation of a (presumably hydro-
gen-bonded) base pair that perfectly stacks inside the DNA
double helix. Insertion of CuII ions into the Hq–Hq pair of
DNA1 furnishes an increase in the thermal stability by
228C, which is a typical value for metal-ion-mediated base
pairs. DNA1:Cu exhibits a Tm of 80.08C. DNA2 and DNA3
without CuII show Tm values of 57.6 and 59.38C, which are
very similar to the value observed for DNA1. Relative to
completely unmodified DNA double strands with A–T pairs
instead of the Hq–Hq pairs, DNA2 exhibits a destabilization
of 1.18C and DNA3 of only 0.78C per modified pair. In the
case of these duplexes, addition of CuII yields a significant
increase of Tm in such a way that Tm cannot be determined
in buffer solutions by heating up to 908C. UV/Vis absorp-
tion spectroscopy supports the formation of CuII-mediated
base pairs. The metal-to-ligand charge-transfer (MLCT)
band of the Hq–Hq pairs in DNA1, DNA2, and DNA3 at
approximately 400 nm gradually increases upon addition of
CuII ions to the sample solutions until all Hq–Hq pairs are
coordinated to copper (see the Supporting Information).
To use the CuII-mediated Hq–Hq base pair for electron
transfer through DNA, it is important to know more about
the metal–metal interaction inside the DNA base stack. To
this end, DNA4 and DNA5 were synthesized. They contain
a sequence identical to the literature (Scheme 3) to allow
full comparison of the results.[12] The Tm behavior of DNA4
and DNA5 is similar to that observed for DNA1 and DNA2
(Table 1). In contrast to the salen base pair known from the
literature,[12] the Hq pair investigated in this work forms
more stable duplexes in the absence of CuII ions.
Scheme 2. Synthesis of 1 and sequences DNA1–DNA3: a) Pivaloyl chlor-
ide, DMAP in pyridine, 16 h, RT, 57%; b) Pd
CH3CN, 20 h, 608C, 43%; c) NEt3·3HF, THF, 15 min at 08C, 16 h, RT,
86%; d) Na[BH(OAc)3] in AcOH/CH3CN, 08C, 20 min, 76%.
ACHTUGNTRENN(NUG OAc)2, AsPh3, NEt3 in
ACHTUNGTRENNUNG
C-nucleoside synthesis is the Pd-catalyzed cross-coupling
(Heck-type) of glycal 3 with the isobutyroyl-protected hy-
droxyquinoline 5[10] that is available from 4 by a standard
protecting step. This synthetic route has the advantage that
a separation of an anomeric mixture is not necessary. The
bulky TBDMS group in the 3’-position of 3 directs the
cross-coupling in such a way that the b-anomer of 6 is
formed exclusively. Subsequently, the TBDMS groups of 6
are cleaved and nucleoside 7 is reduced stereoselectively[11]
to the hydroxyquinoline C-nucleoside 1. The preparation of
the corresponding phosphoramidite as a DNA building
block for solid-phase oligonucleotide synthesis follows
standard procedures (see the Supporting Information).
In the first step, DNA1 to DNA3 were prepared to inves-
tigate the melting temperatures (Tm) of DNA double strands
that contain the Hq ligand as C-nucleoside 1 (Scheme 2,
Table 1). DNA1 contains just one Hq–Hq pair in the middle
of the sequence, whereas DNA2 and DNA3 bear two and
three Hq–Hq pairs in a row.
To shed light on the nature of the metal–metal interac-
tion, we performed electron paramagnetic resonance (EPR)
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F. Breher, H.-A. Wagenknecht et al.
1
= spin, and its experimentally derived spin Hamiltonian pa-
2
rameters are very similar to those reported for bis(8-quin
AHCTUNGTRENNUNG
ACHTUNGTRENNUNGo-
linolato)copper(II) complexes (Table 2).[13] A close inspec-
tion of the EPR spectrum in Figure 2 reveals that it com-
prises two components: the broad signal of the dinuclear
Scheme 3. Sequences of DNA4 and DNA5 for EPR measurements.
Table 2. Principal g values, hyperfine couplings A [MHz], and the elec-
tron–electron coupling D [MHz] for mononuclear DNA4:Cu, DNA5:Cu,
and dinuclear DNA5:Cu2.
measurements. We focused in particular on both the internu-
clear distance and the interaction between the two CuII ions
in DNA5:Cu2. To achieve this goal, the continuous-wave
(CW) X-band EPR spectra of frozen aqueous solutions of
the mononuclear (DNA4:Cu) and the dinuclear
(DNA5:Cu2) compounds were recorded at low temperatures
(Figures 1 and 2).
[b]
DNA4:Cu[a]
DNA5:Cu2
DNA5:Cu[c]
g?
gj j
A?(Cu)
Aj j(Cu)
A?
Aj j
D
2.052
2.225
66
555
35
2.05
2.22
<70
555
–
2.00, 2.07
2.33
<50
330
–
–
–
(14N)
ACHTUNGTRENNUNG
(14N)
29
–
–
A
The spectrum of DNA4:Cu (Figure 1) shows the charac-
[a] Line widths: x, y=18.7 MHz, z=30.2 MHz. [b] Line widths: x, y=
350 MHz, z=450 MHz and at half-field x, y=175 MHz, z=255. [c] Line
widths: x, y=180 MHz, z=250 MHz. [d] An axial electron–electron in-
teraction was used with the unique axis tilted from the gj j axis by (30ꢁ
10)8. The model employs collinear g and Cu hyperfine axes in and be-
tween the two spins with the assumption that the gj j axes point perpen-
dicular to the base pairs (see Figure S23 of the Supporting Information).
teristic features of a square-planar CuII system with an S=
DNA5:Cu2 (modeled by two interacting S=1= spins, see
2
below) and a second signal that shows the typical character-
istics of a mononuclear CuII complex. It is reasonable to
assume that this signal arises from the partially copper-
loaded compound DNA5:Cu. Several attempts to synthesize
and isolate pure DNA5:Cu2 were not successful (also see
the Supporting Information).
Figure 1. X-band CW EPR spectrum of DNA4:Cu at 100 K (30 mm
As expected for the dinuclear system DNA5:Cu2, we
were able to detect the half-field signal around B=1550 G,
which stems from the forbidden Dms = ꢁ2 transition be-
tween the ms = +1 and ms =ꢀ1 levels within the triplet state
(see inset in Figure 2). Note that this signal is not affected
by the mononuclear impurities DNA5:Cu (but see below;
this signal is affected by trace amounts of Fe3+ impurities).
The experimental spectrum of DNA5:Cu2 shown in Figure 2
contains significant amounts of mononuclear DNA5:Cu. We
were able to simulate the data using a two-component
model with 50% DNA5:Cu2 and 50% DNA5:Cu (see
Table 2 and the Supporting Information). Note that the g
values for mononuclear DNA5:Cu deviate from axial sym-
metry, which might be attributed to a different chemical en-
vironment than DNA4:Cu (the exact reason of this effect
was not investigated further).
frozen aqueous solution) overlaid with the simulation (gray).
The dinuclear species DNA5:Cu2 was modeled as a dimer
with a spin Hamiltonian that comprises two interacting S=
Figure 2. X-band CW EPR spectrum of DNA5:Cu2/DNA5:Cu at 39 K
(30 mm frozen aqueous solution). Experimental is black. Gray indicates
the simulated spectrum using fractions of 50% DNA5:Cu and 50%
DNA5:Cu2 and the parameters in Table 2; see the Supporting Informa-
tion for plots of the individual spectra (Figures S20 and S21). The inset
shows the half-field signal from the dimer, which exhibits clear splittings
as a result of the large hyperfine coupling of Aj j(Cu)=555 MHz. The
signal at g=4.3, which is assigned to Fe3+ impurities, is marked with an
arrow.
1
= spins with an axial electron–electron dipolar interaction
2
D and with each spin exhibiting a large CuII hyperfine cou-
pling (the 14N hyperfine structure is not resolved). By apply-
ing Equation (1)—in which m0 =permeability constant, mB =
Bohr magneton, and h=Planck constant—the dipolar cou-
ꢀ
pling constant of D=(790ꢁ40) MHz translates into a Cu
Cu distance of r=(4.2ꢁ0.1) ꢁ. Similar values have been re-
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Electron Transfer in DNA
FULL PAPER
ported previously by Shionoya et al. as well as Schiemann
et al.[4,14]
rffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
rffiffiffiffiffiffiffiffiffiffiffiffi
3 m0m2Bg2avg
3
57557
D
ð1Þ
r ¼
¼
4phD
Equation (1) uses the average dimer g value of gavg =2.107
and is based on the point-dipole approximation. It is noted
that this approximation might break down at such short dis-
tances as a result of, for example, spin delocalization or ani-
sotropic exchange coupling contributions.[14] As stated
before by Schiemann et al. for a very similar system,[14]
a
contribution of anisotropic exchange coupling contributions
cannot be excluded. However, the effect of spin delocaliza-
tion in such systems is generally assumed to be small owing
to the stacked arrangement of the two CuII-mediated base
pairs. The simulations furnished an angle of (30ꢁ10)8 be-
tween the unique axis of D and the two g|| axes of the two
spins, which implies an offset of this size between the two
CuII centers (and the corresponding metal-mediated base
pairs). The natural twist angle between two base pairs
within the DNA molecule is known from the literature to be
368.[15]
To gain further insight into the interaction of the two CuII
ions in DNA5:Cu2, specifically, whether it is ferro- or anti-
ferromagnetic in nature, we measured CW EPR spectra at
various temperatures to determine a value for the exchange
coupling constant J from the half-field signal (Bleaney–
Bowers-type plot; Figure S22 of the Supporting Informa-
tion). The magnitude of the J value was found to be very
small, and the interaction between the two CuII should thus
be weak and antiferromagnetic in nature (J estimate
ꢀ1.0ꢁ0.2 cm-1; see the Supporting Information for further
details).[16] However, owing to trace amounts of Fe3+ impuri-
ties that give rise to the signal at g=4.3 (see Figure 2), we
refrain from drawing any strong conclusions from this data
and analysis.
Scheme 4. Sequences of DNA6–DNA9 and structures of the charge
donor (Dp–U) and charge acceptor (Ap–dU). The inset shows the main
indicated charge-transfer pathway between Dp (hole donor) and Ap
(hole acceptor).
gives a tremendous driving force of ꢀ1.9 eV for the photoin-
duced charge-transfer process between Dp and Ap–dU (see
inset in Scheme 4).
To elucidate the potential role of the Hq–Hq pair as
charge carrier for photoinduced charge transfer, we prelimi-
narily synthesized DNA6 and DNA7 with sequences similar
to DNA1 and DNA2 but equipped with 2,7-diazapyrenium
(Dp) as charge donor on one side of the Hq pairs
(Scheme 4). Dp is amenable for photoexcitation at l=
339 nm to induce a hole transfer into DNA. Owing to the
low chemical stability of Dp under the conditions of solid-
phase oligonucleotide synthesis and workup,[17] the chromo-
phore had to be ligated post-synthetically to the propargyl
group and thereby attached to the 2’-position of uridine ac-
cording to our published protocol.[18] 6-N,N-Dimethyl ami-
nopyrene (Ap) represents the additional complementary
electron–hole acceptor in DNA8 and DNA9 and is attached
through its 2-position to the 5-position of 2’-deoxyuridine
(dU).[19] The oxidation potential of this nucleoside conjugate
Ap–dU was investigated by cyclic voltammetry (E01 (ox)=
DG ¼ EoxꢀEredꢀE0,0
ð2Þ
On the basis of these findings, it appeared both reasonable
and promising to combine these chromophores to follow the
charge-transfer efficiency over Hq–Hq base pairs prelimi-
narily by steady-state fluorescence spectroscopy. It is impor-
tant to mention here that excitation at l=339 nm exhibits
high selectivity for Dp since the MLCT band of the Hq
complexes contribute only slightly to the absorption in this
area. Indeed, the spectra of DNA8 and DNA9 excited at
339 nm (Figure 3) reveal decreased Dp fluorescence intensi-
ty at 425 nm but does not show Ap fluorescence at all. The
Fq (fluorescence quenching) values describe the relative
amount of Dp fluorescence intensity that is quenched in a
DNA double strand with acceptor Ap relative to a compara-
ble DNA double strand without acceptor (e.g., DNA8
versus DNA6, DNA9 versus DNA7). The amount of
quenching of Dp fluorescence that is caused by the presence
of the electron-hole acceptor Ap in DNA8 and DNA9 is
similar to those observed in DNA samples with G–C base
=
2
0.88 V versus the normal hydrogen electrode (NHE)). Com-
bined with E01
(red)=ꢀ0.21 V[20] and E0,0 =3.0 eV for Dp,
2
the Rehm–Weller equation [Eq. (2) without Coulomb term]
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F. Breher, H.-A. Wagenknecht et al.
Conclusion
A new DNA nucleoside based on the hydroxyquinoline
ligand was synthesized on the basis of a Pd-catalyzed cross-
coupling methodology. The artificial Hq–Hq base pair in the
absence of metal ions has a stability that is similar to natural
A–T pairs. The duplex stability can be significantly in-
creased by coordinating CuII ions to the Hq–Hq pairs
(metal-mediated base pairing). EPR spectroscopic investiga-
tions revealed that the two CuII ions in DNA5:Cu2 are
within the natural offset between two base pairs within ex-
perimental uncertainty. The metal–metal distance within the
CuII-mediated Hq–Hq base pair obtained from the dipolar
coupling constant D and a point dipole approximation of r
falls into the range of previously reported CuII-mediated
DNA fragments. Further evidence for either ferro- or anti-
ferromagnetic interactions between the two CuII ions in
DNA5:Cu2 could not be estimated without doubt. Indica-
tions for charge-transfer processes across both the nonmeta-
lated and the metal-ion-mediated Hq–Hq pairs in DNA
could be observed by fluorescence measurements. However,
it has to be emphasized that measurement and comparison
of fluorescence intensities is not sufficient to undoubtedly
prove photoinduced charge transfer. Time-resolved meas-
urements have to follow. Nevertheless, on the basis of the
careful analysis of changes in fluorescence intensities and
melting temperatures presented in this work, it can be as-
sumed that charge transfer over nonmetalated Hq–Hq base
pairs occurs with similar efficiency to that over natural G–C
pairs. The charge transfer becomes more efficient in the
presence of CuII ions. Overall, this work further supports the
idea of utilizing intraduplex metal complexes as artificial
charge carriers for the application of DNA-based architec-
tures for molecular electronics.[21]
Figure 3. Fluorescence of the reference duplexes DNA6/DNA7 and the
charge-transfer duplexes DNA8/DNA9 in the absence (EDTA) and in
the presence of CuII ions (lexc =339 nm).
pairs between donor and acceptor (Table 3). This is remark-
able and fits nicely with the tailored structural characteris-
tics of nucleoside 1. On the basis of the previously discussed
Table 3. Quenching of Dp fluorescence (Fq) due to the presence of the
charge acceptor Ap–dU in the absence and in the presence of CuII.
Samples
Fq [%]
(10 mm EDTA)
Fq [%]
Fq [%] over
G–C[a]
with CuII
DNA8 versus DNA6
DNA9 versus DNA7
58[b]
26[c]
75[b]
33[c]
50
19
[a] DNA duplexes with G–C pairs instead of Hq–Hq pairs. [b] Fq=
1ꢀIDNA8/IDNA6. [c] Fq=1ꢀIDNA9/IDNA7
.
melting temperatures it can be assumed that the artificial
DNA base Hq forms—very similar to natural base pairs—
stable Hq–Hq pairs also in the absence of metal ions, most
likely due to the complementarity of the hydrogen-bonding
interface. Clearly, Hq–Hq pairs stack inside the DNA
double helix and thereby provide a charge-transfer efficien-
cy that is as good as that of natural G–C pairs. Moreover,
the quenching of Dp fluorescence increases by approximate-
ly 30% upon addition of CuII ions to the DNA samples that
bear the Hq–Hq base pairs (Figure 3, Table 3). This fluores-
cence quenching in DNA8 and DNA9 has to be attributed
solely to the presence of the charge acceptor Ap since both
Fq values are referenced to fluorescence intensities of
DNA6 and DNA7, both in the presence of CuII. This obser-
vation indicates that CuII-mediated Hq–Hq pairs increase
not only the efficiency of charge injection (e.g., DNA6 with-
out CuII versus DNA6 with CuII) but also charge transfer to
the acceptor (DNA8 with CuII versus DNA6 with CuII). It is
clear that the comparison of fluorescence intensities will not
undoubtedly prove photoinduced charge transfer. Neverthe-
less, careful comparison of fluorescence intensities as pre-
sented herein support the proposition that charge-transfer
efficiency over Hq–Hq pairs without CuII is similar to G–C
pairs and enhanced in the presence of CuII.
Experimental Section
See the Supporting Information for experimental details. It includes a
synthetic description for 1 and modified oligonucleotide preparation, fig-
ures depicting the NMR spectra, MS data of modified oligonucleotides,
and details on the EPR measurements.
Acknowledgements
F.B. acknowledges financial support by the DFG-funded transregional
collaborative research center SFB/TRR 88 “Cooperative effects in homo-
and heterometallic complexes (3MET)”. H.A.W. is grateful for financial
support by the Deutsche Forschungsgemeinschaft (DFG Wa 1386/12-2),
the University of Regensburg, and Karlsruhe Institute of Technology.
J.H. acknowledges financial support from the ARC/FT120100421 and in-
formative discussions with Prof. Hanson.
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Electron Transfer in DNA
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Received: June 4, 2013
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