13754 Phys. Chem. Chem. Phys., 2012, 14, 13754–13771 This journal is c the Owner Societies 2012 Cite this: Phys. Chem. Chem. Phys., 2012, 14, 13754–13771 Solution, surface, and single molecule platforms for the study of DNA-mediated charge transport Natalie B. Muren, Eric D. Olmon and Jacqueline K. Barton* Received 17th May 2012, Accepted 18th July 2012 DOI: 10.1039/c2cp41602f The structural core of DNA, a continuous stack of aromatic heterocycles, the base pairs, which extends down the helical axis, gives rise to the fascinating electronic properties of this molecule that is so critical for life. Our laboratory and others have developed diverse experimental platforms to investigate the capacity of DNA to conduct charge, termed DNA-mediated charge transport (DNA CT). Here, we present an overview of DNA CT experiments in solution, on surfaces, and with single molecules that collectively provide a broad and consistent perspective on the essential characteristics of this chemistry. DNA CT can proceed over long molecular distances but is remarkably sensitive to perturbations in base pair stacking. We discuss how this foundation, built with data from diverse platforms, can be used both to inform a mechanistic description of DNA CT and to inspire the next platforms for its study: living organisms and molecular electronics. 1. Introduction DNA holds great promise as a medium for charge transport (CT) in nanoscale electronic and biomedical devices due to its stability and structural programmability. 1,2 Conductive properties of DNA were forecast in 1962 by Eley and Spivey when they observed similarities between stacked DNA base pairs and stacked graphene sheets: both are composed of planar, aromatic molecules, and both exhibit an inter-plane stacking distance of 3.4 A ˚ . 3 Evidence of DNA-mediated CT was presented in a 1993 experiment involving oxidative quenching of a DNA-bound metal complex through the DNA base stack. 4 Since then, the ability of DNA to mediate CT reactions has been verified in many experimental systems, and the factors that affect the rate and efficiency of the reaction are for the most part well understood. Despite our knowledge of the fundamental characteristics of DNA CT, these systems remain quite challenging to model. Indeed, the nature of the CT bridge must be considered, and variations in the base sequence, the introduction of perturbations such as base mismatches between the donor and the acceptor, and dynamic motions of the bases, among other factors, can alter the rate of the reaction and the yield of CT products. It is clear that a mechanistic description must be informed by and consistent with the characteristics of DNA CT that have been observed and validated across diverse experimental platforms (Fig. 1). Division of Chemistry and Chemical Engineering, California Institute of Technology, Pasadena CA 91125, USA. E-mail: [email protected]Natalie B. Muren Natalie B. Muren received her B.A. in chemistry from Willamette University in 2006, where she studied aminoglyco- side antibiotics in the laboratory of Professor Sarah R. Kirk. Natalie’s graduate work in Professor Jacqueline K. Barton’s group involves both fundamental studies of DNA charge transport and the use of this sensitive chemistry for the electrochemical detection of clinically relevant DNA-binding proteins. Eric D. Olmon Eric D. Olmon grew up in Troy, Ohio and earned his B.S. in chemistry from The Ohio State University, where he studied the effect of DNA conformation on the efficiency of thymine dimer formation in the laboratory of Bern Kohler. Eric recently earned his PhD in chemistry from Caltech for his work involving the study of DNA-mediated charge transport by time-resolved spectroscopy. PCCP Dynamic Article Links www.rsc.org/pccp PERSPECTIVE Downloaded by California Institute of Technology on 15 January 2013 Published on 31 July 2012 on http://pubs.rsc.org | doi:10.1039/C2CP41602F View Article Online / Journal Homepage / Table of Contents for this issue
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13754 Phys. Chem. Chem. Phys., 2012, 14, 13754–13771 This journal is c the Owner Societies 2012
Solution, surface, and single molecule platforms for the
study of DNA-mediated charge transport
Natalie B. Muren, Eric D. Olmon and Jacqueline K. Barton*
Received 17th May 2012, Accepted 18th July 2012
DOI: 10.1039/c2cp41602f
The structural core of DNA, a continuous stack of aromatic heterocycles, the base pairs, which
extends down the helical axis, gives rise to the fascinating electronic properties of this molecule
that is so critical for life. Our laboratory and others have developed diverse experimental
platforms to investigate the capacity of DNA to conduct charge, termed DNA-mediated charge
transport (DNA CT). Here, we present an overview of DNA CT experiments in solution, on
surfaces, and with single molecules that collectively provide a broad and consistent perspective on
the essential characteristics of this chemistry. DNA CT can proceed over long molecular distances
but is remarkably sensitive to perturbations in base pair stacking. We discuss how this
foundation, built with data from diverse platforms, can be used both to inform a mechanistic
description of DNA CT and to inspire the next platforms for its study: living organisms and
molecular electronics.
1. Introduction
DNA holds great promise as a medium for charge transport (CT)
in nanoscale electronic and biomedical devices due to its stability
and structural programmability.1,2 Conductive properties
of DNA were forecast in 1962 by Eley and Spivey when
they observed similarities between stacked DNA base pairs
and stacked graphene sheets: both are composed of planar,
aromatic molecules, and both exhibit an inter-plane stacking
distance of 3.4 A.3 Evidence of DNA-mediated CT was
presented in a 1993 experiment involving oxidative quenching
of a DNA-bound metal complex through the DNA base
stack.4 Since then, the ability of DNA to mediate CT reactions
has been verified in many experimental systems, and the
factors that affect the rate and efficiency of the reaction are
for the most part well understood. Despite our knowledge of
the fundamental characteristics of DNA CT, these systems
remain quite challenging to model. Indeed, the nature of the
CT bridge must be considered, and variations in the base
sequence, the introduction of perturbations such as base
mismatches between the donor and the acceptor, and dynamic
motions of the bases, among other factors, can alter the rate of
the reaction and the yield of CT products. It is clear that a
mechanistic description must be informed by and consistent
with the characteristics of DNA CT that have been observed
and validated across diverse experimental platforms (Fig. 1).
Division of Chemistry and Chemical Engineering, California Instituteof Technology, Pasadena CA 91125, USA.E-mail: [email protected]
Natalie B. Muren
Natalie B. Muren received herB.A. in chemistry fromWillamette University in 2006,where she studied aminoglyco-side antibiotics in the laboratoryof Professor Sarah R. Kirk.Natalie’s graduate work inProfessor Jacqueline K. Barton’sgroup involves both fundamentalstudies of DNA charge transportand the use of this sensitivechemistry for the electrochemicaldetection of clinically relevantDNA-binding proteins.
Eric D. Olmon
Eric D. Olmon grew up inTroy, Ohio and earned hisB.S. in chemistry from TheOhio State University, wherehe studied the effect of DNAconformation on the efficiencyof thymine dimer formation inthe laboratory of Bern Kohler.Eric recently earned his PhDin chemistry from Caltechfor his work involving the studyof DNA-mediated chargetransport by time-resolvedspectroscopy.
PCCP Dynamic Article Links
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This journal is c the Owner Societies 2012 Phys. Chem. Chem. Phys., 2012, 14, 13754–13771 13755
Here, we present an overview of DNACT experiments conducted
in solution, on surfaces, and with single molecules, focusing on
studies in our laboratory but also highlighting others. We show
that several characteristics of DNA CT appear to be general,
irrespective of the experimental platform used to observe this
process. We then discuss how these conserved characteristics can
inform a mechanistic description of DNA CT.
2. DNA CT in solution
The majority of experiments that examine the nature of DNACT
have been conducted in solution. In general, solution-phase DNA
CT systems involve a photoexcited charge donor separated from
a charge acceptor by a DNA bridge (Fig. 1). By positioning the
donor and acceptor at opposite ends of the duplex, it is possible to
survey the base sequence between them in a systematic manner in
order to gain information about the CT characteristics of the
medium itself. A wide variety of donors and acceptors have been
utilized in solution measurements of DNA CT, and some are
illustrated in Scheme 1. In contrast to other experimental
platforms that will be discussed in later sections, almost all
solution studies involve CT from the excited state, so the
values obtained depend on the photophysical characteristics
of the charge donor. The measurements are also ensemble
measurements, so the reaction parameters obtained in solution
experiments represent average values. The solution state
provides many measurement techniques, including steady-
state and time-resolved luminescence and transient absorption
spectroscopies, as well as biochemical DNA oxidation assays.
In addition, any conclusions drawn from observations of DNA
CT in aqueous, solution-phase experiments are immediately
applicable to biological systems.
2.1 Interactions between probes and DNA
Primary among the requirements for efficient DNA CT is the
necessity for intimate electronic interaction between the donor–
acceptor pair and the DNA base stack. The effect of varying the
strength of DNA association is nicely illustrated in an experiment
involving naphthalimide (NI) derivatives bearing substituents that
render them positively-charged, negatively-charged, or neutral
without greatly modifying the structure of the probe.5 The
cationic and neutral derivatives bind, as evidenced by hypo-
chromicity in their absorbance spectra upon the addition of
DNA and by luminescence quenching, while the anionic
derivative does not. The lack of binding by the anionic
derivative is attributed to electrostatic repulsion by the
negatively-charged DNA phosphate backbone. Importantly,
the electrostatic association between NI and DNA is not the
only interaction that allows for the observed spectroscopic
changes upon binding; the planar, aromatic character of the
probe lends itself to intercalative binding as well. Indeed, for the
NI derivatives, the changes in the absorption and luminescence
intensities are comparable for the neutral and cationic species,
despite their difference in charge. It is the intimacy of the inter-
calative binding mode, rather than the promiscuity of the electro-
static one, that influences the photophysics of these molecules.
Fig. 1 Platforms for the study of DNA CT. In solution (top), donor
and acceptor molecules are covalently tethered or otherwise incorporated
into opposite ends of a DNA duplex. DNA CT is initiated by photo-
excitation of the donor and measured by spectroscopic or biochemical
methods. On electrode surfaces (center), DNA is covalently tethered to
the surface by one end and modified with a redox-active probe moiety on
the distal end. An applied potential to the electrode results in DNA CT
to the distal probe and produces a characteristic DNA-mediated redox
signal. With single molecules (bottom), one DNA duplex is covalently
attached by amide bonds across a gap that has been cut in a carbon
nanotube within an electrical circuit. Current flow through the
CNT–DNA device is a reflection of DNA CT through the single DNA
duplex that bridges the gap and can be used to make fundamental
measurements of DNA conductivity.
Jacqueline K. Barton
Jacqueline K. Barton is theArthur and Marion HanischMemorial Professor of Chem-istry. She also currently servesas the Chair of the Division ofChemistry and ChemicalEngineering at Caltech.Barton obtained her PhD inInorganic Chemistry atColumbia University andserved as a member of thefaculty at Hunter College andColumbia University beforejoining Caltech in 1989. Herwork is focused on the chem-istry of double helical DNA.
She has received many awards for this research including mostrecently the National Medal of Science (2011).
This journal is c the Owner Societies 2012 Phys. Chem. Chem. Phys., 2012, 14, 13754–13771 13769
6. Conclusions and the next platforms for DNA CT
Studies of DNA CT with photooxidation, spectroscopy, and
electrochemistry, in solution, on surfaces, and with single molecule
techniques, and using a variety of donors and acceptors have
established a solid, experimentally-based foundation to understand
this process. These complementary vantage points are collectively
valuable as they serve to validate shared characteristics and cast
light on pieces of the DNA CT puzzle that are only visible from a
particular experimental platform. Despite the diversity of platforms
that we have explored, we consistently observe a common set of
characteristics for CT processes that are mediated by DNA.
Namely, the electronic coupling of the donor and acceptor to the
p-stack of DNA is required to access DNA CT. The CT itself is
highly sensitive to the structural integrity of the stack of bases
between the donor and acceptor pair. For donors and acceptors
that are well coupled to structurally undisturbed, undamaged
DNA duplexes, the DNA can mediate CT that is rapid and has
an extremely shallow distance dependence which allows this
process to efficiently occur over very long distances. Additionally,
this rapid rate is gated by the dynamic motions of the bases, donor,
and acceptor as they move in and out of CT-active conformations.
Despite these consistent observables, a mechanism for DNA
CT is still not well defined. DNA CT clearly does not fit within
the bounds of either superexchange or hopping models. Our
experiments suggest that transient delocalization of charge
across multi-base domains must necessarily play an important
role. Given the dynamic and structural complexity of the DNA
molecule and the variability introduced by different sequences,
donors, and acceptors, it is likely overly restrictive to confine
this process to a single mechanistic description. Instead, as we
continue to shed light on DNA CT from diverse experimental
viewpoints it will be important to validate known characteristics
and integrate new observations into a mechanistic understanding
that is consistent with the complexity of this process.
Standing upon the strong foundation that was built by these
solution, surface, and single molecule platforms in the pursuit
of a mechanistic understanding, we are now well equipped to
study and utilize DNA CT in two exciting new platforms:
living organisms and molecular electronics. Indeed, our efforts
to answer the question ‘‘How does DNA CT work?’’ has not
only yielded a multifaceted understanding of this complex
process but also inspired the fascinating questions that propel
us toward these bigger platforms: How does biology utilize
DNA CT to coordinate proteins in their efforts to meet complex
cellular challenges? How can we utilize the unique conductive
properties of DNA CT in the development of nanoelectronic
devices? Although more work is clearly still needed to
construct a fuller mechanistic understanding, what we already
know about DNA CT indicates that these new platforms
are promising investments in elucidating and applying this
chemistry.
Acknowledgements
We are grateful to the NIH (GM49216 and GM61077) for
their support of this work. We thank also our coworkers
for their great efforts, sometimes against the tide, in carrying
out their experiments.
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