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Charge transfer dynamics in DNA revealed by time-
resolved spectroscopy
Mamoru Fujitsuka*and Tetsuro Majima*
In the past few decades, charge transfer in DNA has attracted considerable attention from researchers in
a wide variety of fields, including bioscience, physical chemistry, and nanotechnology. Charge transfer in
DNA has been investigated using various techniques. Among them, time-resolved spectroscopic
methods have yielded valuable information on charge transfer dynamics in DNA, providing an important
basis for numerical practical applications such as development of new therapy applications and
nanomaterials. In DNA, holes and excess electrons act as positive and negative charge carriers,
respectively. Although hole transfer dynamics have been investigated in detail, the dynamics of excess
electron transfer have only become clearer relatively recently. In the present paper, we summarize
studies on the dynamics of hole and excess electron transfer conducted by several groups including
our own.
1. Introduction
In the past few decades, charge transfer in DNA has attracted
considerable attention from researchers in diverse elds. Under
biological conditions, DNA is continuously attacked by envi-
ronmentally generated oxidants or reductants. Oxidation of
DNA promotes DNA damage,
1,2
and reduction of DNA is part of
the repair mechanism of DNA lesions by photolyase.
3–5
Charge
transfer in DNA is responsible for the remote oxidation or
reduction process, i.e., the oxidation or reduction of nucleo-
bases apart from the initially oxidized or reduced nucleobase. In
addition, the electrical conductivity of DNA has long been
a research focus, since DNA exhibits a highly stacked structure
of nucleobases in duplex, which is advantageous for electrical
conduction.
6
Thus, applications of DNA to nanowires have also
started to be explored. Charge transfer in DNA is an interesting
subject for physical chemists with respect to understanding
electron transfer processes in polymeric systems and other
related topics.
Charge transfer in DNA has been investigated using various
techniques. For example, the electrical conductivity measure-
ments have shown conductivities ranging from those of an
insulator to those of a superconductor.
7–10
Furthermore,
product analysis of the oxidative or reductive reactions of DNA
has provided valuable information on charge transfer mecha-
nisms. Such analyses have revealed that holes and excess
Mamoru Fujitsuka received B.S.,
M.S., and Doctor degrees from
Kyoto University. Aer two years
work as a postdoc, he became
a research associate of Institute
for Chemical Reaction Science,
Tohoku University. In 2003, he
moved to the Institute of Scien-
tic and Industrial Research
(SANKEN), Osaka University, as
an associate professor. His
research interest is photochem-
istry of various supramolecules.
Tetsuro Majima received B.S.,
M.S., and Doctor degrees from
Osaka University. Aer working
at the University of Texas at
Dallas (1980–1982) and at the
Institute of Physical and Chem-
ical Research (RIKEN, Japan)
(1982–1994), he became an
associate professor of the Insti-
tute of Scientic and Industrial
Research (SANKEN), Osaka
University, and a professor in
1997. His research interests
are radiation and photo
chemistries.
The Institute of Scientic and Industrial Research (SANKEN), Osaka University,
Mihogaoka 8-1, Ibaraki, Osaka 567-0047, Japan. E-mail: fuji@sanken.osaka-u.ac.jp;
majima@sanken.osaka-u.ac.jp
Cite this: Chem. Sci.,2017,8,1752
Received 2nd August 2016
Accepted 8th December 2016
DOI: 10.1039/c6sc03428d
www.rsc.org/chemicalscience
1752 |Chem. Sci.,2017,8,1752–1762 This journal is © The Royal Society of Chemistry 2017
Chemical
Science
PERSPECTIVE
electrons, which are positive and negative charge carriers in
DNA, respectively, can migrate rather long distances by means
of a multistep hopping process.
11,12
Furthermore, investigations
using time-resolved spectroscopic methods have provided
information on the charge transfer dynamics in DNA, including
the rate constants for single-step tunnelling and hopping
processes (Fig. 1a and b). Using these experimental techniques,
hole transfer (HT) dynamics have been investigated in detail for
decades, whereas the dynamics of excess electron transfer (EET)
have only started to become clear more recently. Our research
group has also carried out time-resolved spectroscopic studies
on charge transfer in DNA,
13
because the dynamics parameters
can provide quantitative and useful information for practical
applications. In the present paper, we summarize the time-
resolved spectroscopic studies on HT and EET in DNA con-
ducted by several research groups including our own.
2. Hole transfer in DNA
Using transient absorption spectroscopy during laser ash
photolysis of DNA conjugated with a photosensitizing electron
acceptor, Lewis et al. reported the distance and driving force
dependencies of the hole injection processes in DNA.
14–16
Based
on the charge separation rate between the singlet-excited stil-
bene dicarboxaminde and G through A : T base pairs, they
estimated the damping factor (b)ink
ET
fexp(br)tobe
0.7 ˚
A
1
, where k
ET
and rare the electron transfer rate and
distance required for single-step electron transfer, respectively.
This value is similar to those obtained by product analysis and
other time-resolved spectroscopic methods, including time-
resolved uorescence measurement and pulse radiolysis.
12,17
It
was shown that polyA or polyT between the photosensitizing
electron acceptor and G did not have a signicant effect on the
bvalue. However, the bvalue of the charge recombination
process was found to be larger, 0.9 ˚
A
1
, which was attributed
to its larger driving force. In addition, from the driving force
dependence of the charge separation and recombination
processes, Lewis et al. estimated a reorganization energy of 1.22
eV and electronic coupling of 347 cm
1
when the electron
acceptor and donor nucleobase were placed in close vicinity.
16
When the acceptor and donor were separated by two A : T base
pairs, these values changed to 1.30 eV and 25 cm
1
, respectively.
These values are similar to those reported for various electron
transfer systems in non-adiabatic conditions.
Our research group measured the transient absorption
spectra during the laser ash photolysis of hairpin DNA con-
sisting of A : T base pairs, which were conjugated with naph-
thaldiimide (NDI) and phenothiazine (PTZ) as a photosensitizing
electron acceptor and donor, respectively.
18
Upon selective exci-
tation of NDI using a nanosecond laser pulse, generation of PTZ
radical cation was conrmed within the laser pulse duration.
Although the formation dynamics of PTZ radical cation were not
observed because of the fast hole-hopping among A's, the
distance dependence of the generation yield (Fig. 2) indicated
that PTZ radical cation was generated by multistep hopping of
the hole injected from the singlet excited NDI to DNA. This is in
accordance with the conclusions derived from product analysis.
12
In addition, the A-to-A hopping rate was estimated to be 2 10
10
s
1
. Recently, Lewis and co-workers estimated the A-to-A and G-
to-G hopping rates to be 1.2 10
9
and 4.3 10
9
s
1
,respectively,
based on the direct observation of HT dynamics in a photo-
sensitizing acceptor–DNA–donor system by transient absorption
spectroscopy.
19
Thus, it can be concluded that the single step
hole hopping time in A's or G's is on the order of several tens to
hundreds of picoseconds.
Insertion of other nucleobase(s) between A's or G's slows
down the hopping rate among them, because the inserted
nucleobase(s) act as a barrier for the hopping (Fig. 1). We esti-
mated the hopping rates between G's or G and C, separated by
various nucleobase(s), as summarized in Table 1.
20,21
The
hopping rate was found to depend on the type and number of
nucleobase(s) present. These ndings agree with the electron
transfer theory;
22,23
that is, the electron transfer rate depends to
a large extent on the barrier height and length between the
donor and acceptor. These studies revealed the detailed
mechanisms and rate constants of HT in DNA. It should be
emphasized that the rate constant of the charge transfer process
is also essential in certain applications such as the detection of
DNA sequences. For example, we showed that a single molec-
ular uorescence detection method can detect DNA sequences
on the basis of the HT rate in DNA.
24,25
Furthermore, we found
that titanium dioxide can be used as the photosensitizing
electron acceptor for the detection of a mismatch sequence.
26
Fig. 1 Mechanisms of HT and EET in DNA. (a) G-to-G consecutive
hole hopping, (b) G–X–G(X¼A, C, or T) hole tunnelling, (c) T-to-T
consecutive excess electron hopping, and (d) T–Y–T excess electron
tunnelling. E
ox
and E
red
are oxidation and reduction potentials,
respectively. Note: E
ox
(G) < E
ox
(X), while E
red
(T) > E
red
(Y).
Fig. 2 (Left) Schematic diagram for the HT in NDI- and PTZ-conju-
gated DNA and (Right) distance (N: step number) dependence of
generation yield of PTZ radical cation. Reprinted with permission from
literature.
18
Copyright (2004) American Chemical Society.
This journal is © The Royal Society of Chemistry 2017 Chem. Sci.,2017,8,1752–1762 | 1753
Perspective Chemical Science
3. Excess electron transfer in DNA
Studies on EET in DNA have been carried out by means of
several experimental methods such as product analysis and
laser ash photolysis. Compared to studies on the HT in DNA,
information on the kinetics such as EET rate is limited. The
small number of studies on EET in DNA is probably due to the
rather low reduction potentials of nucleobases,
27
which limit
the availability of the photosensitizing electron donor for such
analysis. In following section, the knowledge on EET obtained
to date is summarized.
3.1 Excess electron tunnelling in DNA in low temperature
glass
Sevilla and co-workers reported the results of an electron spin
resonance (ESR) study on the EET in DNA.
28
In their system,
DNA and a non-specically intercalated electron acceptor were
irradiated by g-rays in a glassy matrix at 77 K. The excess elec-
tron statistically generated on DNA nucleobases transfers to an
electron acceptor such as mitoxantrone (MX), ethidium
bromide, 1,10-phenanthroline, and 5-nitro-1,10-phenanthro-
line within a the time-scale of minutes to weeks. This EET
process can be tracked by monitoring the signal produced from
the radical anions of nucleobases using ESR. The distance for
the electron tunnelling (Fig. 1d) was estimated to be 4–10 base
pairs aer 1 min at 77 K. The estimated rate was on the order of
10
0
to 10
1
s
1
, from which they estimated the bvalues of each
intercalator to be 0.85–1.2 ˚
A
1
which is a similar range to the
bvalues estimated for the HT process.
Sevilla and colleagues further examined the effect of temper-
ature on EET using DNA with MX as the intercalator and D
2
Oas
the solvent, which was employed to distinguish T radical anion
and protonated reduced C.
29
They found that the excess electron
tunnelling from the nucleobase to MX was the dominant process
at a temperature of <77 K. The estimated bvalues of DNA at 4 and
77 K were conrmed to be the same. This lack of temperature
dependence can be attributed to the absence of the contribution
of higher vibronic states in this temperature range. Furthermore,
the deuteration of T radical anion at the C6position was found to
take place irreversibly above 130 K, which competes with the
excess electron tunnelling and acts as an irreversible sink for the
excess electrons. Furthermore, hybridization of G and C causes
the protonation of C radical anion at the N3 position in
a reversible manner to form a stable structure.
Furthermore, in 2002, Sevilla et al. estimated the bvalue and
ET distance for some base sequences according to ESR
measurements on duplexes of polydAdT and polydIdC, which
included MX as an intercalator.
30
The bvalue and ET distance
were estimated to be 0.75 ˚
A
1
and 9.4 base pairs, respectively,
for the polydAdT duplex, and were calculated to be 0.92 ˚
A
1
and
9.5 base pairs for the polydIdC duplex. They attributed these
results to the slow deuteron transfer from I to C radical anion
forming CD radical.
Therefore, from a series of ESR studies on g-ray irradiated
DNA with an intercalator, Sevilla et al. successfully obtained some
parameters of the excess electron tunnelling in DNA, which were
comparable to those of HT in DNA. In particular, the contribu-
tion of the protonated radical anion in EET is an important
nding, which can be clearly observed with ESR measurements
but is difficult to assess using other methods. In addition, it
should be noted that the radiation chemical method is advan-
tageous in the study of EET in DNA, because this method can
easily generate the reduced forms of various organic molecules.
31
Several groups have investigated charge transport in DNA using
another important radiation chemical technique, pulse radiol-
ysis. For example, Kobayashi et al. reported the transient
absorption spectra of reduced nucleobases, which revealed the
delocalization of the excess electron over several nucleobases.
32
However, oxidation or reduction via radiation chemical method
occurs in a random manner. In addition, oxidation or reduction
of the target molecules occurs from the reaction with an initially
generated oxidized orreduced solvent species, respectively. These
characteristics of radiation chemistry limit the time resolution
for kinetic research. Our research group attempted to apply pulse
radiolysis to the study of EET in DNA to determine the rate
constant of excess electron hopping (Fig. 1c), but the rate could
not be determined because of these limitations.
33
3.2 Excess electron hopping in DNA
Studies on excess electron hopping in DNA have been carried out
by means of product analysis of DNA with a tethered photo-
sensitizing electron donor, which injects excess electron to
a certain position of DNA. In 2002, Carell and co-workers inves-
tigated the distance dependence of EET in a DNA conjugated with
reduced avin and a T–T cyclobutane dimer as the electron donor
to DNA and acceptor, respectively.
34
UV irradiation to a sequence
of consecutive T's is known to generate a cyclobutane pyrimidine
dimer lesion in DNA, which can be repaired by DNA photolyase
enzymes through the electron transfer from reduced and
deprotonated FADH
cofactor to a cyclobutane dimer.
3
In this
sense, this system mimics the DNA repair process by DNA pho-
tolyase. In their system, the T dimer and avin were separated by
A : T base pairs. Photoirradiation to reduced and deprotonated
avin causes the excess electron injection to T's,which is trapped
by the T dimer aer the hopping process in DNA. The reduction
of the T dimer causes cycloreversion, which can be detected by
Table 1 The intra- and inter-strand hole hopping rates between two G
separated by A, T or C and activation energy
20,21
Sequence nk
ht
/s
1
E
a
/eV
G–A
n
–G 1 4.8 10
7
0.18
2 9.7 10
4
0.43
3 1.4 10
4
—
G–T
n
–G 1 4.6 10
5
0.35
2 3.6 10
4
0.50
3 9.1 10
3
—
G–A
n
–C
a
1 1.4 10
6
0.30
2 4.5 10
4
0.53
G–T
n
–C
a
1 1.6 10
6
0.25
2 3.1 10
4
0.50
G–C
n
–G
a
1 (3.6–4.0) 10
8
0.22–0.25
a
Interstrand hole hopping rate.
1754 |Chem. Sci.,2017,8,1752–1762 This journal is © The Royal Society of Chemistry 2017
Chemical Science Perspective
HPLC. From the yield of the cycloreversion of the T dimer, they
estimated the distance dependence of the electron transfer yield,
from which the bvalue was estimated to be 0.11 ˚
A
1
.They
attributed this small bvalue to hopping of excess electron in
DNA. The plot of ln Eagainst ln N,whereEand Nare the effi-
ciency of the charge transfer and the number of steps, respec-
tively, showed a linear relationship with a slope of approximately
2, which is in accordance with the one-dimensional random
walk model (EfN
2
). Furthermore, it was conrmed that the
excess electron induced to DNA could migrate over 24 ˚
A. They
also fabricated DNA hairpins with avin and T dimer as the
donor and acceptor, respectively, and showed a similar distance
dependence of EET.
35–37
Using this system of a avin donor and T dimer acceptor,
Carell and co-workers further investigated EET in a PNA : DNA
hybrid.
38
In this hybrid system, the avin donor and T dimer
acceptor were introduced to PNA and DNA chains, respectively.
They found that the distance dependence of EET efficiency was
similar to that of the DNA duplex system, indicating efficient
interstrand EET. Furthermore, their PNA : DNA hybrids did not
show a directional preference of EET (i.e.,5
0to 30or 30to 50).
39
Since the split rate of the T dimer is 10
6
s
1
, they suggested that
the rate-determining step of cycloreversion may be the splitting
rather than EET in DNA, indicating the fast EET in DNA. They
conrmed this speculation with experiments using BrU, BrA, and
BrG as the acceptor of the excess electron that was injected from
the avin donor to DNA.
40
They also investigated the effect of
G : C pair insertion in an A : T tract on EET yield. They found that
the DNA with the electron acceptor with higher electron accept-
ing ability (BrU) was more sensitive to the insertion of a G : C
pair, because the higher electron accepting ability results in
faster electron trapping than EET in DNA. From these results,
they suggested that the acceptor used in studies of the EET
process should possess high electron acceptor ability in order to
make the excess electron hopping a rate-determining step. More
recently, they suggested that the hopping rate through the (A : T)
4
pair is faster than 1.8 10
7
s
1
and slower than 1.4 10
8
s
1
based on the comparison of the EET rate through DNA with the
debromination rate of BrU or cleavage rate of the T dimer.
41
In their series of studies on EET using a avin donor, Carrell
et al. also revealed that the formation of the duplex structure is
essential for EET. In addition, they conrmed that N
2
O,
a solvated electron scavenger, has no effect on the EET. From
this nding, they excluded a contribution of the solvated elec-
tron, which can be generated by electron ejection from the
photoexcited donor to the solvent mediating the negative
charge to the acceptor.
42
Thus, the EET should be mediated by
nucleobases in DNA. These are also important conclusions of
their studies.
Rokita and Ito studied the EET using product analysis of the
photolysis of DNA conjugated with N,N,N0,N0-tetramethyl-1,5-
diaminonaphthalene (TMDN) and BrU, as the photosensitizing
electron donor and electron acceptor, respectively (Fig. 3).
43,44
Photoirradiation to TMDN causes the injection of the excess
electron to DNA. The arrival of the excess electron to BrU aer
hopping through DNA generates a radical anion of BrU, which
results in decomposition of the 50neighbour by generation of
the U radical, H abstraction, and hydrolysis. The yield of the
electron transfer to BrU was evaluated by electrophoresis. In
2003, they reported the small distance dependence of the
generation yield of reduced BrU, which is in accordance with
the results obtained by Carell et al., indicating that the excess
electron transfer occurred via a hopping mechanism. Further-
more, in 2004, Rokita and Ito further claried that T transfers
the excess electron more efficiently than C for the same
distance. Analysis of the isotope effect of the solvent showed
that the contribution of the C radical anion to the excess charge
transfer is limited due to the protonation of the C radical anion.
Thus, T is a primary carrier of the excess electron. Furthermore,
it was indicated that the interstrand EET is slower than the
intrastrand EET, and the electron transfer in the 30to 50direc-
tion is faster than that of the reverse direction. This trend is
opposite to that observed for the HT in DNA. They pointed out
the importance of the contribution of MO to the charge carrier;
i.e. HOMO for the HT and LUMO for the EET. These ndings
were not observed by Carell et al. because the slower splitting
step of the reduced T dimer acted as the rate-determining step.
In summary, important information on the EET in DNA has
also been obtained through studies based on product analysis.
According to these results, DNA, especially T acts as the major
carrier of the excess electron, whereas C has a minor contri-
bution because of the protonation by G, which forms a pair with
C, and surrounding water. The distance dependence of the EET
yield associated with a bvalue of 0.1–0.3 ˚
A
1
, indicating that the
multistep hopping of the excess electron is important in the
long-range EET as in the case of the HT. This issue was
conrmed by Carell et al. who showed that the EET yield obeys
a one-dimensional random walk model. The tendencies
observed by Rokita are quite interesting issues to be claried
through more detailed investigations. However, in contrast to
the HT the rate constant of the EET has not been determined.
For determination of the rate constant, kinetic information
based on the time-resolved measurements is essential. In the
next section, an overview of time-resolved spectroscopic studies
for the EET is provided.
3.3 Excess electron injection to DNA
The kinetic properties of excess electron injection have been
studied by means of ultrafast spectroscopic methods. In 1999,
Fig. 3 DNA conjugated with TMDN and BrU as the electron donor to
DNA and acceptor, respectively. Reprinted with permission from
literature.
43
Copyright (2003) American Chemical Society.
This journal is © The Royal Society of Chemistry 2017 Chem. Sci.,2017,8,1752–1762 | 1755
Perspective Chemical Science
the research groups of Lewis and Wasielewski reported the
results of a femtosecond transient absorption study on the
electron injection from photoexcited stilbenediether (Sd) at the
loop position of DNA hairpin.
45,46
They found that the excess
electron injection to T occurs within 0.2 ps when T is located
next to Sd. They also conrmed that the electron injection to C
occurred with a rate constant of 3.3 10
11
s
1
, which is slower
than that to T (>2 10
12
s
1
) due to the smaller driving force of
the excess electron injection. In addition, they determined that
the electron transfer rate from excited Sd to the I : C pair was 1.4
10
12
s
1
, which is much faster than that of the G : C pair,
because of the enhanced electron accepting ability of C due to
base pairing. They also studied the distance dependence of the
excess electron injection using DNA hairpins with noncanonical
G : G base pairs between Sd and A : T pairs (Fig. 4) to ensure
that G acts as a barrier for the excess electron injection process
without a contribution of C, which is a possible electron
acceptor for photoexcited Sd. The electron injection rate
decreased to 5.7 10
9
and 4.4 10
8
s
1
when one and two
G : G pairs, respectively, were inserted between Sd and T. They
indicated that these rates are slower than the hole injection
from the singlet excited stilbenedicarboxamide (Sa) by a factor
of approximately 25, in spite of a similar driving force for the
charge separation. They attributed the observed difference in
the charge injection rates to the longer donor–acceptor distance
or weak donor–bridge–acceptor electronic coupling.
In 2009, the research groups of Lewis and Fiebig reported the
charge injection process in DNA conjugated with aminopyrene
(APy) as an end-capping group and BrU.
47
The charge separation
time from photoexcited APy to T was 0.55 ps, which decreased to
0.27 ps when BrU was located at the rst or second neighbour of
APy. The efficiency of the formation of reduced BrU, which is
formed by accepting the excess electron aer EET in DNA, was
evaluated by HPLC or MALDI TOF mass spectroscopy. The
distance dependence of the generation yield of the reduced
product was obtained as shown in Fig. 5, in which the HT yield
in Sa–A
n
–Sd is also plotted. The plots were almost parallel to
each other, supporting the hopping mechanism of the excess
electron along DNA. These results are in accordance with those
by Carell et al. and Rokita and Ito described in the former
section.
Wagenknecht and co-workers also investigated the excess
electron injection process in DNA.
48
In 2004, they reported the
photoinduced process of pyrene-conjugated U and C (PydU and
PydC, respectively).
49,50
They showed that the excess electron
injection in PydC was weak pH dependent (pH ¼5 or 11), while
the injection process in PydU was completely inhibited at
higher pH. The weak pH dependence of PydC can be explained
on the basis of the protonation of the C radical anion in the
picosecond time-scale, even under a basic aqueous condition.
The degree of the proton association to the C radical anion
affected the charge recombination rate. By contrast, in the case
of PydU, the relatively higher energy of Pyc
+
dUc
than the pyrene
excited state inhibited the formation of Pyc
+
dUc
, and excited
PydU then undergoes proton coupled electron transfer to form
Pyc
+
dU(H)c. The authors pointed out that the observed pH
dependence is important to the EET in DNA, because the
protonated C radical anion, which should be generated by its
complement base G or surrounding water, will limit or termi-
nate the EET in DNA. That is, the C radical anion cannot act as
a charge carrier.
In a subsequent study in 2005, Wagenknecht and co-workers
reported the EET in DNA using PTZ as the electron donor and
BrU as the acceptor.
51
The efficiency of the EET was evaluated
according to the strand cleavage yield. They conrmed that the
A : T base pairs transport the excess electron more efficiently
Fig. 4 DNA hairpins conjugated with Sd at the loop position and
schematic energy diagram for the excess electron injection from the
photoexcited Sd. Reprinted with permission from literature.
46
Copy-
right (2002) American Chemical Society.
Fig. 5 The distance dependence of the generation yield of the
reduced product. The hole transport yield in Sa–A
n
–Sd was also
plotted. Reprinted with permission from literature.
47
Copyright (2009)
American Chemical Society.
1756 |Chem. Sci.,2017,8,1752–1762 This journal is © The Royal Society of Chemistry 2017
Chemical Science Perspective
than do G : C pairs due to protonation of the C radical anion.
This result is consistent with that reported by Rokita and Ito
described above.
Our group has employed oligothiophenes as the photo-
sensitizing electron donor for nucleobases, because the electron
donor ability can be controlled by changing the substituents and
number of repeating units. In addition, strong absorption bands
in the radical cation state in the visible regions are good spectral
markers for a transient absorption study. We investigated the
charge-injection ability of oligothiophenes toward nucleobases
using dyad systems, as indicated in Fig. 6.
52,53
An ethylenedioxy-
substituent was introduced to some oligothiophenes, because it
has been reported that the oligomers of ethylenedioxythiophene
(EDOT) showed higher electron donor-ability than those of non-
substituted oligothiophenes.
54
Charge injection from the singlet
excited oligothiophenes to the nucleobases was indicated by the
uorescence quenching, and conrmed by the transient
absorption measurements during femtosecond laser ash
photolysis. The observed charge separation (CS) and recombi-
nation (CR) rates and corresponding driving forces (DG
CS
and
DG
CR
) are summarized in Table 2. The results indicated that the
CS rate becomes faster with an increase in the driving force, while
the CR rate becomes slower, indicating that the CS and CR
processes are in the normal and inverted regions of Marcus
theory, respectively, as shown in eqn (1).
22,23
kET ¼ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
p
ħ2lokBT
rjVj2X
meSðSm=m!Þ
exp ðloþDGþmħhuiÞ2
4lokBT!(1)
lo¼e21
2rD
þ1
2rA
1
r1
n21
3S(2)
S¼li
ħhui:(3)
In eqn (1), l
o
is the outer sphere reorganization energy given
by eqn (2), Vis the electronic coupling, Sis the electron-vibra-
tion coupling constant given by eqn (3), and huiis the averaged
angular frequency. In eqn (2), nis the refractive index. In eqn
(3), l
i
is the inner sphere reorganization energy. By applying the
Marcus theory to the observed driving force dependence of rate
constants, parameters such as V,l
o
, and l
i
were estimated to be
0.050, 0.20, and 1.10 eV, respectively (Fig. 7). Notably, for the
hole injection process, these values have been reported to be
0.043, 0.23, and 0.99 eV, respectively.
16
Thus, a similar total
reorganization energy was conrmed for hole and excess elec-
tron injection. The slightly faster excess electron injection rate
can be mainly attributed to the larger Vvalue. These results
conrm that the nucleobases act as electron acceptor when the
appropriate photosensitizing electron donor is employed,
although lots of chemists have paid attention to the oxidation
process of nucleobases in relation to DNA damage, as discussed
in the Introduction part.
3.4 Direct evaluation of excess electron transfer dynamics in
DNA
As summarized in the former sections, the excess electron
injection process has been investigated by both product anal-
ysis and transient absorption spectroscopy. However, the EET
process in DNA has mainly been studied using product analysis.
As observed in studies of the HT process in DNA, a donor–DNA–
acceptor system, of which the acceptor radical anion is detect-
able with transient absorption spectroscopy, will be useful for
the detailed analysis of the EET process in DNA. From this
perspective, our research group investigated the EET in DNA
hairpin conjugated with N-methyl-N-aminoglycine (
A
Py) and
diphenylacetylene (DPA), as the photosensitizing electron
donor and electron acceptor at the loop position, respectively.
55
To enhance the generation yield of the DPA radical anion,
Fig. 6 Structures of (a) 2E,3T, and 3E, and (b) dyads 1–15. Reprinted
with permission from literature.
52
Copyright (2014) American Chemical
Society.
Table 2 Driving forces (DG
CS
and DG
CR
) and rate constants (k
CS
and
k
CR
) of CS and CR in dyads 1–15. Reprinted with permission from
literature.
52
Copyright (2014) American Chemical Society
DG
CSa
(eV) k
CSb
(s
1
)DG
CRa
(eV) k
CRc
(s
1
)
10.01 6.4 10
11
3.63 1.1 10
11
20.32 1.0 10
12
3.32 6.7 10
10
30.54 7.7 10
11
3.10 2.9 10
11
40.63 1.0 10
12
3.01 3.8 10
11
50.73 2.5 10
12
2.91 3.4 10
11
60.75 —
d
3.93 —
d
70.44 —
d
3.62 —
d
80.22 3.5 10
10
3.40 6.5 10
9
90.13 5.8 10
10
3.31 6.5 10
9
10 0.03 8.7 10
10
3.21 7.3 10
9
11 0.27 —
d
3.39 —
d
12 0.04 1.1 10
11
3.08 8.3 10
10e
13 0.26 1.1 10
12
2.86 2.8 10
11e
14 0.35 1.8 10
12
2.77 3.7 10
11e
15 0.45 2.0 10
12
2.67 3.7 10
11e
a
DG
CS
and DG
CR
were calculated as indicated in literature.
52
b
Estimated error is less than 20%.
c
Estimated error is less than 10%.
d
Not observed.
e
Rate constant of the fast component.
This journal is © The Royal Society of Chemistry 2017 Chem. Sci.,2017,8,1752–1762 | 1757
Perspective Chemical Science
dihydrothymine (
D
T), which acts as a barrier for rapid charge
recombination,
56
was inserted between
A
Py and T. The genera-
tion of DPA radical anion was conrmed with nanosecond laser
ash photolysis, indicating that the EET time should be shorter
than 10 ns. It was conrmed that insertion of C in T's decreased
the generation of DPA radical anion. Thus, discussion based on
product analysis can also be assessed on the basis of the yield of
DPA radical anion. Furthermore, it was conrmed that the
excess electron could migrate even when
A
Py and DPA were
separated by 10 base pairs, i.e. 34 ˚
A.
In 2011, we investigated a series of donor–DNA–acceptor
conjugates, in which thiophene tetramer (4T) was employed as
a photosensitizing electron donor, for evaluation of the rate of
single-step excess electron hopping among nucleobases.
57
4T
has certain advantages such as sufficient excited state oxidation
potentials to reduce nucleobases and strong absorption bands
upon oxidation, which can be distinguished from the excited
state and radical anion of the electron acceptor, i.e., DPA.
53
Furthermore, for the observation of the excess electron hopping
process within the time window possible with our current
instrument, rather short DNA dumbbells including a few
nucleobases were examined (Fig. 8a). The formation of duplex
structure was conrmed by means of the CD spectra and
melting temperature measurements, and supported by molec-
ular modelling.
The transient absorption spectra of the dumbbell DNA T
3
,
obtained by selective excitation of 4T with a 400 nm femto-
second laser pulse, are indicated in Fig. 8. Immediately aer the
laser pulse, the singlet excited 4T was observed. With the decay
of the singlet excited 4T, the generation of the radical cation of
4T was conrmed, indicating the excess electron injection from
the singlet excited 4T within 10 ps. However, the generation of
the DPA radical anion exhibited a two-step rising prole. The
rising rate of the faster component was the same as decay rate of
the singlet excited 4T, while the slow component reached
maximal absorbance about 200 ps aer the laser pulse excita-
tion. The fast component can be attributed to the single-step
charge separation between singlet excited 4T and DPA, whereas
the slow component can be attributed to the formation of DPA
radical anion by the excess electron aer hopping through the T
tract (Fig. 8b). Moreover, the generation rate of DPA radical
anion by the EET process became slower with increasing
number of T's between 4T and DPA, supporting the generation
of DPA radical anion by excess electron hopping in DNA. By
applying a one-dimensional random walk model, the T-to-T
hopping rate in consecutive T's was determined to be 4.4 10
10
s
1
. As described above, Lewis et al. reported that the single-step
hopping rate of HT was 4.3 10
9
and 1.2 10
9
s
1
for G-to-G
and A-to-A, respectively.
19
Our research group found that the A-
to-A hopping rate was 2 10
10
s
1
.
58
Therefore, it became clear
that the hopping rate of the excess electron among consecutive
T's is faster than the hole hopping rate among A's and G's.
In addition to the nicked-dumbbell DNA, we conrmed the
EET in DNA hairpin, in which DPA was placed at the
loop position and N,N0-dimethylaminopyrene (
A
Py0),
Fig. 7 DG(DG
CS
and DG
CR
) dependence of k
ET
(k
CS
Cand k
CR
B).
Numbers close to the marks indicate compounds. The solid and
hollow black squares are the 2T dyads. The solid and hollow red circles
are the dyads 1–5. The solid and hollow green circles are corre-
sponded to the dyads 8–10. The solid and hollow orange circles are
corresponded to the dyads 12–15. The solid blue line was calculated
by eqn (1), (2), and (3) using l
S
,l
V
,V, and ħhuiof 0.20, 1.10, 0.050, and
0.19 eV, respectively. The solid pink line was calculated using l
S
,l
V
,V,
and ħhuiof 0.23, 0.99, 0.043, and 0.19 eV, respectively. Reprinted with
permission from literature.
52
Copyright (2014) American Chemical
Society.
Fig. 8 (a) Structures of dumbbell DNAs conjugated with 4T and DPA.
(b) Expected energy diagram. (c) Transient absorption spectra of T
3
during the laser flash photolysis using 400 nm femtosecond laser
pulse. Reprinted with permission from literature.
57
Copyright (2011)
American Chemical Society.
1758 |Chem. Sci.,2017,8,1752–1762 This journal is © The Royal Society of Chemistry 2017
Chemical Science Perspective
a photosensitizing electron donor, was attached at the 50end.
59
In this case, the EET dynamics indicated that
A
Py0did not
behave as an end-capping group but rather seems to be inter-
calated between two terminal base pairs; Lewis et al. conrmed
a similar structure with 50-pyrenecarboxamide tethered DNA.
60
The T-to-T hopping rate was estimated to be 6.1 10
10
s
1
,
which is slightly larger than the value estimated with the above
mentioned nicked-dumbbell DNA, but the hopping rate on the
order of 10
10
s
1
was conrmed.
3.5 T-to-T hopping rate depends on the driving force for
charge injection
As introduced in the former section, we have claried the T-to-T
hopping rate by studying donor–DNA–acceptor systems. As
a photosensitizing electron donor, we employed 4T and
A
Py0as
discussed in the previous section, which provided T-to-T
hopping rates of 4.4 10
10
and 6.1 10
10
s
1
, respectively. Our
further studies using a trimer and dimer of EDOT (3E and 2E,
respectively) as the photosensitizing electron donor yielded
T-to-T hopping rates of 2.2 10
11
and 2.6 10
11
s
1
, respec-
tively.
61
Thus, the reported EET rate constants for consecutive
T's are in the range of 10
10
to 10
11
s
1
depending on the pho-
tosensitizing electron donors (Table 3), which provided various
driving forces for excess-electron injection to DNA. It was
conrmed that a larger driving force for excess electron injec-
tion results in a faster T-to-T hopping rate. In fact, a nearly
linear relationship was conrmed between the T-to-T hopping
rate and driving force for excess electron injection (Fig. 9). The
intercept of the linear t ((3.8 1.5) 10
10
s
1
) should corre-
spond to the hopping rate for a non-energy assisted (DG
CS
¼0)
EET in DNA, i.e., the intrinsic hopping rate. Interestingly, the
intrinsic hopping rate agrees with the reported value for the
DNA sugar backbone and base motions, which occur with
periods as short as 30 ps at 303 K,
62,63
suggesting that the excess-
electron hopping is likely dominated by the structural dynamics
of DNA.
3.6 T-to-T hopping rate in an alternating A–T sequence
Excess electrons should migrate through the LUMOs of C or T in
DNA due to their relatively high reduction potentials in DNA.
According to the results of product analysis, EET has been
conrmed to be a sequence-dependent process. Furthermore, it
was conrmed that the protonated C radical anion will limit or
terminate EET, as discussed in the next section in more detail.
Thus, T should contribute to EET signicantly. Several groups,
including our own, have reported the dynamics of intrastrand
EET in DNA through A : T sequences; however, investigations
on interstrand EET in alternating A : T sequences in DNA, in
which the interaction between the LUMOs of T's does not exist,
are still limited. For example, Carell and co-workers reported an
interstrand EET in PNA : DNA double strands based on product
analysis.
38
Their qualitative results showed that an interstrand
EET can efficiently proceed in PNA : DNA double strands,
indicating that the EET in PNA : DNA is somewhat inuenced
by the specic stacking situation. By contrast, for interstrand
HT in DNA, Lewis's group reported that the efficiency of inter-
strand HT in DNA is lower than that of intrastrand HT by
a factor of 4, due to the lack of interaction between the HOMOs
of A's, based on femtosecond laser ash photolysis studies.
66
We obtained similar results using nanosecond laser ash
photolysis in our previous report.
18
Thus, direct measurement
of the dynamics of EET in DNA by laser ash photolysis is
essential to achieve a quantitative understanding of interstrand
EET. Here, two series of functionalized DNA oligomers, Tn and
ATn, were synthesized with a strong electron-donating photo-
sensitizer (3E) and an electron acceptor (DPA) (Fig. 10).
64
Table 3 Excess electron hopping rates
57,59,61,64,65
Sequence Donor k
hop
/s
1
Note
T–T 4T 4.4 10
10
Intrastrand T-to-T
A
Py06.1 10
10
Intrastrand T-to-T
3E 2.2 10
11
Intrastrand T-to-T
2E 2.6 10
11
Intrastrand T-to-T
T–A–T3E 1.1 10
11
Interstrand T-to-T
T–C–T3E 110
11
Assuming C as an excess electron carrier
3E 4.9 10
10
Assuming intrastrand T-to-T tunneling
Fig. 9 Dependence of ln k
hop
on DG
CS
. A, B, C, and 2-Tn were
estimated from DNA conjugated with 4T,
A
Py0,3E, and 2E, respectively,
as a photosensitizing electron donor. Reprinted with permission from
literature.
61
Copyright (2016) American Chemical Society.
This journal is © The Royal Society of Chemistry 2017 Chem. Sci.,2017,8,1752–1762 | 1759
Perspective Chemical Science
Transient absorption measurements during femtosecond laser
ash photolysis of ATn showed the generation of DPAc
for AT3,
whereas AT4 and AT5 did not result in the generation of DPAc
.
The absence of DPAc
can be attributed to the fast CR between
3Ec
+
and DNAc
. For AT3 and T3, the generation of 3Ec
+
–DNA–
DPAc
was conrmed, indicating that the inter- and intrastrand
EET is strongly limited by the CR rate. By applying the random
walk model, the inter- and intrastrand excess electron hopping
rates were determined. It was conrmed that the EET rate
constant of AT3 (1.1 10
11
s
1
) is 2-times lower than that of T3
(2.2 10
11
s
1
). The slower EET rate for intrastrand EET can be
attributed to the lack of p-stacking of T's in AT3. Thus, these
results indicated that excess electron hopping is affected by the
interaction between the LUMOs of nucleotides.
3.7 Effect of G and C
It has also been noted that pH affects the dynamics of EET in
DNA. This is because the protonated C radical anion, which can
be generated by proton transfer from the complementary base,
G, or from surrounding water molecules, will limit or terminate
EET.
30,44,50,51,67
Steenken and co-workers proposed a proton-
transfer reaction pathway for the G : C base pair radical anion
(G : Cc
base pair) as shown in Fig. 11,
68,69
which is a thermo-
dynamically favourable process and has been supported by
various experimental
70,71
and theoretical studies.
72–74
Although
the rate constant of proton transfer in G : Cc
base pairs (k
PT
)
was theoretically calculated to be 10
11
s
1
,
75
it has not been
determined directly. Furthermore, limited information is
available for the effect of G : C base pairs on EET dynamics. To
clarify the dynamics of EET in DNA, a femtosecond laser ash
photolysis study of a donor–DNA–acceptor system was carried
out (Fig. 12).
65
In the transient absorption spectra of C4, the
transient absorption band at 580 nm, which can be attributed to
G(H)
: C(H)c, the product of the proton-transfer reaction of
G:Cc
base pairs, was observed as well as 3Ec
+
. From the global
analysis, the proton transfer rate was estimated to be 2.6 10
10
s
1
, which agreed with the theoretical estimation.
76
In addition,
generation of DPA was not conrmed with C3 and C4, indi-
cating that multiple C's completely terminated the EET in DNA.
Notably, the generation of DPAc
was conrmed from anal-
ysis of the transient absorption spectra of CTT, TCT, and TTC,
indicating that the single G : C pair in T's cannot completely
terminate the EET. The intervening G : C base pair in the
consecutive T's reduced the k
ET
value to 50%, regardless of the
position of the G : C base pair in the DNA oligomers. In addi-
tion, the yield of the formation of DPAc
with respect to the
initial 3Ec
+
generation showed a decrease of 30% in CTT, TCT,
and TTC. As a role of C in EET, two possibilities are pointed out:
(1) C acts as excess electron carrier and (2) C acts as a barrier for
excess electron (Table 3).
3.8 Detection of long range EET by electrochemical method
Because of the rapid CR, long-range EET through DNA has been
difficult to conrm with laser ash photolysis study of donor–
DNA–acceptor systems. Therefore, to observe long-range EET
through DNA we employed electrophotochemical systems using
donor–DNA–Au gold systems.
77
In this system, photoexcitation
of 3E yielded a charge separated state, i.e., excess-electron
injection from the singlet excited 3E,
1
3E*, to T. The injected
excess-electron migrated through T and was then trapped by the
Au electrode to yield a photocurrent. 3Ec
+
was reduced by
ascorbic acid, AA, as an electron-donating sacrice, to regen-
erate 3E. The redox levels of the components are presented in
Fig. 13. The signicant sequence dependence of photocurrent
generation suggests that T-to-T hopping is a dominant mecha-
nism for EET in DNA. Using this system, we conrmed EET
through DNA up to 40.8 ˚
A. We further conrmed the sequence
dependence of the process, as shown in Fig. 14. From the
experiments on DNAs with an alternating A : T sequence and
consecutive G : C sequence, the hopping models described in
the sections above were supported.
Fig. 10 Structures of DNA oligomers. The gap between the 50and 30
indicates a missing phosphate linker between two nucleotides in
nicked dumbbell structure. Reprinted with permission from litera-
ture.
64
Copyright (2015) John Wiley and Sons.
Fig. 11 Proposed proton-transfer reaction pathway for G : Cc
base
pair. Reprinted with permission from literature.
65
Copyright (2015)
American Chemical Society.
Fig. 12 Structures of 3E, DPA, and DNA oligomers (C3, C4, T3, CTT,
TCT, and TTC). The gap between the 50and 30indicates a missing
phosphate linker between two nucleobases in nicked dumbbell
structure. Reprinted with permission from literature.
65
Copyright
(2015) American Chemical Society.
1760 |Chem. Sci.,2017,8,1752–1762 This journal is © The Royal Society of Chemistry 2017
Chemical Science Perspective
4. Conclusions and remarks
In this perspective article, the EET in DNA were summarized
and a brief summary of the HT process was provided. Compared
to HT in DNA, our understanding of the EET process is still
limited, although the results of recent detailed investigations
have claried various aspects of EET. The following questions
point out examples of unknown issues about EET in DNA: (1)
how do multiple nucleobase insertions (i.e., G's between T's)
alter the EET hopping rate? We have already pointed out that
single C between T's does not terminate EET, but multiple C's
can terminate. How about G? (2) How far can the excess electron
migrate? In laser ash photolysis experiment, fast CR limits the
EET distance. But as indicated by the photoelectrochemical
method, excess electron potentially migrates over several tens
angstrom. Is EET over hundred angstrom possible? (3) To what
extent do mismatches change the EET hopping rate? Is the
mismatch effect similar to that for HT? (4) What effect does
DNA conformation, such as, A, B, C, and Z, have on the EET
rate? (5) What effect does protein association have on EET in
DNA? For example, would the EET rate in the chromosomes in
cellular nucleus be faster or not? This point should be essential
in DNA damage and repair in cell as indicated by the electro-
chemical studies.
78,79
These questions are fundamental for EET
in DNA. We hope that the detailed processes of EET in DNA will
be claried in the near future.
Note added after first publication
This article replaces the version published on 23rd December
2016, in which incorrect contact details for the rst author were
presented through editorial error.
Acknowledgements
We are grateful to a number of collaborators, especially Prof.
Kiyohiko Kawai, Prof. Takashi Tachikawa, Dr Man Jae Park and
Dr Shih-Hsun Lin, SANKEN, Osaka University. This work has
been partly supported by a Grant-in-Aid for Scientic Research
(Projects 25220806, 25288035, and others) from the Ministry of
Education, Culture, Sports, Science and Technology (MEXT) of
Japanese Government.
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