Subscriber access provided by Caltech Library Services
Journal of the American Chemical Society is published by the American Chemical
Society. 1155 Sixteenth Street N.W., Washington, DC 20036
Published by American Chemical Society. Copyright © American Chemical Society.
However, no copyright claim is made to original U.S. Government works, or works
produced by employees of any Commonwealth realm Crown government in the course
of their duties.
Communication
Helix-dependent Spin Filtering through the DNA Duplex
Theodore J. Zwang, Sylvia Hürlimann, Michael G. Hill, and Jacqueline K. Barton
J. Am. Chem. Soc.
,
Just Accepted Manuscript
• DOI: 10.1021/jacs.6b10538
• Publication Date (Web): 15 Nov 2016
Downloaded from http://pubs.acs.org on November 16, 2016
Just Accepted
“Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted
online prior to technical editing, formatting for publication and author proofing. The American Chemical
Society provides “Just Accepted” as a free service to the research community to expedite the
dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts
appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been
fully peer reviewed, but should not be considered the official version of record. They are accessible to all
readers and citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered
to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published
in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just
Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor
changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers
and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors
or consequences arising from the use of information contained in these “Just Accepted” manuscripts.
Helix-dependent Spin Filtering through the DNA Dupl
ex
Theodore J. Zwang,
1
Sylvia Hürlimann,
1
Michael G. Hill,
2
Jacqueline K. Barton
1,
*
1
Division of Chemistry and Chemical Engineering, Cal
ifornia Institute of Technology, Pasadena, CA 91125
2
Division of Chemistry, Occidental College, Los Ange
les, CA, 90041
Supporting Information Placeholder
ABSTRACT:
Recent work suggests that electrons can travel
through DNA and other chiral molecules in a spin-se
lective man-
ner, but little is known about the origin of this s
pin selectivity.
Here we describe experiments on magnetized DNA-modi
fied
electrodes to explore spin-selective electron trans
port through
hydrated duplex DNA. Our results show that the two
spins mi-
grate through duplex DNA with different yield, and
that spin
selectivity requires charge transport
through
the DNA duplex.
Significantly, shifting the same duplex DNA between
right-
handed B- and left-handed Z-forms leads to a diode-
like switch in
spin-selectivity; which spin moves more efficiently
through the
duplex depends upon the DNA helicity. With DNA, the
supramo-
lecular organization of chiral moieties, rather tha
n the chirality of
the individual monomers, determines the selectivity
in spin, and
thus a conformational change can switch the spin se
lectivity.
DNA-mediated charge transport (DNA CT) is well esta
blished in
both ground and excited state systems
(
1
). Although theoretical
models are still being developed, it is clear that
the integrity of
the extended π-stack of the aromatic heterocycles,
the nucleic
acid bases, plays a critical role (
2-4
): electron donors and accep-
tors must be electronically well coupled into the π
-stack, typically
via
intercalation, and perturbations that distort the
π-stack, such
as single-base mismatches, abasic sites, base lesio
ns, protein-
binding that kinks the double helix
,
attenuate DNA CT dramati-
cally. This latter characteristic has found practi
cal use in elec-
tronic devices and biosensors (
5-7
).
Recent experimental work in the field of spintronic
s has raised
the intriguing possibility that DNA CT is affected
by the inherent
spin of the electrons passing through it. The first
experiments to
show that double stranded DNA (dsDNA) could functio
n as a spin
filter were conducted under vacuum, where photoelec
trons
ejected from a gold surface became spin-polarized a
fter passing
through an adsorbed dsDNA monolayer (
8
). Subsequent conduc-
tive AFM measurements showed that the resistance of
spin-
polarized currents traveling through a thin film of
air-dry dsDNA
depended on the ratio of spin up versus spin down e
lectrons
injected into the film (
9
).
These observations mirror similar ex-
periments that feature other chiral organic molecul
es within a
thin film (
10
). Because organic molecules display small spin-orb
it
coupling that would otherwise preclude them from ex
hibiting
spin-selective transport properties, this work has
spawned much
interest in chirality-induced spin selectivity (CIS
S) (
11-13
). Several
theories have been offered to account for this effe
ct (
14-17
). One
question of particular interest is whether CISS dep
ends more on
the isolated molecular chiral centers or the large-
scale macromo-
lecular structures within the films (
15
).
Owing to its ability to undergo macromolecular conf
ormation-
al changes that affect the helical structure but no
t the local chi-
rality of the sugar backbone, dsDNA in its native,
hydrated state
presents a unique opportunity to differentiate betw
een the
monomeric and macromolecular parameters of CISS. Of
particu-
lar interest is the conformational switching betwee
n right-
handed B-DNA and left-handed Z-DNA.
At high salt concentra-
tions, CG-repeat sequences in the right-handed B-fo
rm can flip
into a left-handed zigzag Z-form helix (
18
). Notably, both B-DNA
and Z-DNA support efficient DNA CT (
19
).
Figure 1. Cyclic voltammetry on electrodes modified
with 16 bp
dsDNA. A.
Illustration of the dsDNA modified electrodes with
1
μM methylene blue (MB) (left) or 10 μM Ru(NH
3
)
6
3+
(right).
B.
For
intercalated MB (above) and electrostatically bound
Ru(NH
3
)
6
3+
(below) reduction yield upon switching the magnetic
field
direction. Data were normalized to the first scan w
ith the
magnetic field pointing up.
C.
Representative cyclic
voltammograms with the magnet up (red, solid) and m
agnet
down (blue, dotted).
D.
Difference plot showing the current
when the magnetic field is pointing up minus the cu
rrent when
the magnetic field pointing down. The Ru(NH
3
)
6
3+
experiments
were typically done following MB experiments on the
same sur-
face.
We have developed an electrochemical assay to inves
tigate
dsDNA-promoted CISS under fluid conditions. Follow
ing work by
others, (
20
) our study employs a nickel working electrode capp
ed
with a thin (~ 10 nm) layer of gold (Figure 1) (
21).
Thiol-modified
DNA duplexes are then self assembled onto these ele
ctrodes,
Page 1 of 5
ACS Paragon Plus Environment
Journal of the American Chemical Society
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
and DNA-binding redox-active probes are added to th
e electro-
lyte solution. Magnetizing the nickel surface with
a permanent
neodymium magnet (0.66 T) generates a spin-polarize
d current
when the potential is poised negative of the formal
reduction
potential of the DNA-bound probe molecules.
The sign of the
polarization can be switched by changing the direct
ion of the
magnetic field, but its magnitude remains the same.
Integrating
the Faradaic response of probe-molecule reduction u
sing cyclic
voltammetry gives the total number of redox probes
reduced,
which can be used to quantify the yield of DNA CT u
nder differ-
ent experimental conditions. Importantly, the redo
x potentials
of all of the probes lie well negative of the poten
tial of zero
charge of the working electrode (
22
). As a result, duplexes with-
in the DNA film line up approximately normal to the
gold surface
with the magnetic field lines essentially collinear
with the helical
axes.
Figure 1 shows the results obtained at a densely pa
cked dsD-
NA film (16 bp duplexes, ~ 40 pmol/cm
2
) using methylene blue
(MB) as the redox probe. We have previously shown t
hat MB
binds reversibly to DNA monolayers and undergoes a
proton-
coupled, DNA-mediated 2e
-
reduction to leucomethylene blue
(LB) at -300 mV versus AgCl/Ag (
23
). As can be seen in Figure 1,
the yield of MB undergoing electrochemical reduction
varies
regularly with the orientation of the underlying ma
gnetic field,
“up” versus “down”. The change in yield measured by
cyclic volt-
ammetry is not large but it is highly reproducible.
This effect is
fully reversible and can be switched repeatedly by
simply flipping
over the permanent magnet beneath the nickel surfac
e. The
ratio of the integrated reduction peaks of MB varies
by 10.9% ±
0.6% upon switching the magnetic field direction (u
p/down).
Increasing the length of the individual DNA helices
in these films
to 30 bp consistently results in a larger ratio, 15
±1%. Importantly,
the difference in reduction yield is observed regar
dless of which
direction the nickel is magnetized initially, and t
he difference
persists even when taking multiple scans. There is
also no dis-
cernable change in the magnetic field effect upon v
arying the
scan rate between 10mV/s to 20 V/s (
21
).
The magnetic field dependence of DNA CT was also ex
amined
using Nile blue (NB) as a redox probe. NB is coval
ently bound to
DNA, conjugated through a DNA base, and has been us
ed exten-
sively as a covalent redox reporter (Figure 2) (
24-26
). Self-
assembled monolayers of 17 bp thiolated dsDNA with
tethered
NB (~ 40 pmol/cm
2
) show a change in the integrated reduction
peaks of 7±1% upon switching the magnetic field dir
ection. The
magnitude of this effect increases with increasing
length of dsD-
NA to 12±2% for 29bp, 16±4% for 43bp, and 29±6% for
60bp
oligomers (Fig. S1). There is no measurable effect
on the charge-
transfer rates with a change in magnetic field dire
ction (
27
). The-
se data with NB, however, reveal a clear dependence
of the yield
of DNA CT on magnetic field orientation.
Given the range of possible etiologies for the obse
rved mag-
netic field effect on the electrochemistry of MB and
NB, we car-
ried out a series of control experiments (Figure 2)
. Monolayers in
which MB is adsorbed directly onto the gold-capped n
ickel elec-
trodes in the absence of DNA show no differences in
the reduc-
tion yield of MB upon switching the orientation of t
he magnetic
field. Similarly, there is no magnetic field effect
on the reduction
of MB bound electrostatically to surfaces coated wit
h single
stranded DNA. Moreover, capping the nickel electrode
s with a
thicker (35-nm) gold layer eliminates the magnetic
field effects,
even for electrodes modified with dsDNA.
Non-intercalative redox probes were also examined f
or com-
parison. Ru(NH
3
)
6
3+
binds electrostatically to the phosphate
backbone of DNA and undergoes rapid electrochemical
reduction
to Ru(NH
3
)
6
2+
at dsDNA-modified electrodes (
28
). Significantly,
we find no magnetic field dependence of the Ru(NH
3
)
6
3+/2+
cou-
ple, despite its proximity to the chiral macromolec
ule and likely
helical path (Figure 1). We also prepared dsDNA wit
h a covalently
bound diazobenzene probe (dabcyl) tethered to the 3
’-
phosphate near the electrode surface. This arrange
ment allowed
us to monitor simultaneously the direct electrode r
eduction of
dabcyl, which contacts the electrode surface, and t
he DNA-
mediated reduction of MB. There is a significant dif
ference in the
up/down yield of MB reduction, but no measurable dif
ference
for the dabcyl signal (Fig. S3).
Page 2 of 5
ACS Paragon Plus Environment
Journal of the American Chemical Society
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
Figure 2.
Representative cyclic voltammetry data for various
assemblies of DNA-modified electrodes.
29 bp dsDNA or ssDNA
was tethered to a gold-capped nickel surface with a
n alkanethiol
linker. Insets display the full cyclic voltammogram
, while the
larger plot displayed is centered around the reduct
ion peak of
the redox probe.
We examined the effect of an intervening single bas
e mis-
match in the film (Fig. S4). A mismatch incorpora
ted into dsDNA
between the surface and the redox probe decreases t
he yield of
CT to either MB or NB, which shows that the DNA dupl
ex medi-
ates the CT (
24
); charge migrates
through
the DNA base pair
stack. Interestingly, the spin selectivity measured
through a mis-
match mirrors the magnitude of the effect seen in w
ell-matched
duplexes of similar length. This result suggests th
at when charge
is successfully transported through dsDNA with a mi
smatch, it
travels through the entire dsDNA to the probe; the
attenuation in
CT yield with a mismatch leads to an interruption o
f some of that
CT, but no effect on spin selectivity.
Combined, these results indicate that: (i) spin pol
arized cur-
rents induced by the underlying magnetic field are
needed for
spin selectivity in the DNA electrochemistry; (ii)
spin selectivity
requires double stranded; and (iii) the magnetic fi
eld effects are
observed only with probes that undergo CT reactions
mediated
by the DNA duplex.
If the helical structure of dsDNA is responsible fo
r the appar-
ent CISS behavior in these films, it follows that r
eversing the chi-
rality of the helices would switch the sense of the
magnetic field
effect. Indeed, this is precisely what we find. Bo
th methylated
and unmethylated monolayers of 16bp duplexes featur
ing d(CG)
8
repeats were self-assembled onto gold-capped nickel
. Circular
dichroism confirms that DNA oligomers containing 5-
methylcytosine, d(
m
CG)
8
undergo a B-to-Z transition in the pres-
ence of 10 mM MgCl
2
, while the unmethylated analog, d(CG)
8
remains B-form (Fig. S5); methylated Z-DNA reverts
back to B-
DNA upon rinsing away the MgCl
2
(
18,29,30)
. Previous work has
shown that MB intercalates into both B- and Z-DNA an
d under-
goes DNA-mediated reduction in the presence of 10 m
M MgCl
2
(
19
).
We carried out the electrochemistry to examine B- a
nd Z-form
helices on a multiplexed chip (
24
) consisting of 16 separate gold-
capped nickel regions that allowed for the simultan
eous compar-
ison of four distinct monolayers under the identica
l magnetic
field (Figure 3). In the absence of MgCl
2,
both methylated and
unmethylated DNA films show the same favored magnet
ization
direction for a higher yield of MB reduction (up/dow
n ratio =
18±3%). Upon addition of 10 mM MgCl
2
, the unmethylated films
show no change in behavior, but the methylated film
s switch
which magnetic field direction promotes the higher
yield of MB
reduction (up/down ratio = -9±2%). Replacing the bu
ffer with
one that lacks MgCl
2
reverts the structure from Z- to B-form and
restores the original characteristics, yielding aga
in an up/down
ratio of 18±2% for both films.
In addition to functioning as a magnetic field diod
e, switching
between B- and Z-form dsDNA gives a difference in t
he magni-
tude of DNA CISS; normalized to the yield of electr
ochemically
active MB and with the assumption that 10 mM MgCl
2
results in
complete conversion of surface-bound DNA to Z-form,
B-DNA
appears to have an approximately 50% larger spin se
lectivity
than Z-DNA. This change in magnitude of spin select
ivity corre-
lates well with the change in pitch between B-DNA a
nd Z-DNA
(3.32 nm and 4.56 nm respectively) but may result f
rom other
differences between the two forms (such as the grea
ter
π
-
stacking in the B- versus Z-form) (
18,29,30
). These data suggest
that the charge is moving through the duplex along
a helical
path, because a charge moving in a fully delocalize
d π-stacked
column would not be able to interact with the hande
dness of the
Page 3 of 5
ACS Paragon Plus Environment
Journal of the American Chemical Society
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
macromolecule; helical transport among delocalized
domains of
a few base pairs is possible.
The CISS measured in these experiments is significa
ntly larger
than expected for molecules that lack large spin-or
bit coupling.
Calculating the energy difference between the two e
lectron spins
at the surface of fully magnetized nickel (~0.6 T)
yields a gap
(
B
gB
≈
1 cm
-1
) far lower than k
b
T at ambient temperature. Sev-
eral theoretical models have been proffered to rati
onalize the
large CISS exhibited by chiral organic films (
16,17,
31-35
). Aspects
of each of these models can be used to
Figure 3. Switching of methylated and unmethylated
dsDNA
measured on a single multiplexed chip. A.
A multiplexed chip
was prepared with 4 distinct monolayers.
B.
Summary of cyclic
voltammetry data for the two magnetizations were co
llected for
all four quadrants with no MgCl
2
, then with 10 mM MgCl
2
, then
once washing away the MgCl
2
. Each bar represents a minimum of
4 separate electrode surfaces.
C.
Representative example of 30
bp (top) methylated d(
m
CG)
15
and (bottom) unmethylated
d(CG)
15
Data are plotted as the difference in current for
a
reductive sweep when the magnetic field is pointing
up minus
the current when the magnetic field pointing down.
understand our data. In addition, it is worthwhile
to consider
other factors not currently included in these model
s that are
important in the context of DNA CT, such as the lar
ge polarizabil-
ity of the π-stack in dsDNA (
36
) or the delocalization of domains
across multiple adjacent nucleotides (
37,38
).
Our experiments thus demonstrate that magnetic fiel
ds can af-
fect the flow of electrons through native, hydrated
dsDNA. Sig-
nificantly, our data show that electrochemically ge
nerated DNA
CISS is observed only at films containing duplex DN
A and with
redox probes intercalated into the π-stack that und
ergo DNA-
mediated CT. Magnetic field effects are not observed
with redox
reporters bound electrostatically to the DNA duplex
nor with
tethered reporters that contact the surface directl
y. It is not
simply the electrostatic helical field that is resp
onsible for the
spin-selectivity. Nor is it simply the chiral cente
rs on the DNA;
redox reporters bound to single stranded DNA do not
show mag-
netic field effects. As with DNA CT, the extended π
-stack appears
to play the crucial role: reversing the handedness
of the helix in
the films generates a diode-like spin-filtering res
ponse. It is inter-
esting to consider how conformational changes such
as that be-
tween B- and Z-DNA might be utilized as a diode in
organic
spintronics, indeed, how this spin filtering might
be applied in
practical devices. Finally, it is intriguing to con
sider whether Na-
ture exploits this helix-dependent spin selectivity
of DNA in some
context.
ASSOCIATED CONTENT
Supporting Information includes materials and metho
ds, sup-
plementary text, Figs. S1 to S5, Table S1. This mat
erial is available
free of charge via the Internet at http://pubs.acs.
org.
AUTHOR INFORMATION
Corresponding Author
*jkbarton@caltech.edu
Notes
The authors declare no competing financial interest
s.
ACKNOWLEDGMENT
We are grateful to the NIH (GM61077) and the Moore F
ounda-
tion for their financial support. TJZ is also an NS
F GRFP fellow
(DGE-1144469). We thank Dr. Natalie Muren for discus
sions. We
thank John Abendroth, Professor Paul Weiss, Elizabe
th O’Brien,
and Philip Bartels for providing gold-capped nickel
surfaces.
REFERENCES
(1) Genereux, J.C.; Barton, J.K.
Chem. Rev
.
2010
,
110
, 1642-1662.
(2) Guo, X.; Gorodetsky, A.A.; Hone, J.; Barton, J.
K.; Nuckolls, C.
Nat.
Nanotech
.
2008
,
3
, 163-167.
(3) Muren, N.B.; Olmon, E.D.; Barton, J.K.
Phys. Chem. Chem. Phys
.
2012
,
14
, 13754-13771.
(4) Berlin, Y.A.; Voityuk, A.A.; Ratner, M.A.
ACS Nano
.
2012,
6
, 8216.
(5) Porath, D.; Cuniberti, G.; Felice, R.D.
Top. Curr. Chem
.
2004
,
237
, 183.
(6) Drummond, T.G.; Hill, M.G.; Barton, J.K.
Nature Biotech
.
2003
21
,
6475.
(7) Barton, J.K.; Furst, A.L.; Grodick, M.A.
DNA in Supramolecular Chemis-
try and Nanotechnology
, E. Stulz; G.H Clever, ed. Wiley, West Sussex, UK,
2015.
(8) Gohler, B.; Hamelbeck, V.; Markus, T.Z.; Kettne
r, M.; Hanne, G.F.;
Vager, Z.; Naaman, R.; Zacharias, H.
Science
2011,
331
, 894.
(9) Xie, Z.; Markus, T.Z.; Cohen, S.R.; Vager, Z.;
Gutierrez, R.; Naaman, R.
Nano
Lett
.
2011
,
11
, 4652-5644.
(10) Sun, D.; Ehrenfreund, E.; Varedny, Z.V.
Chem
.
Commun
.
2014,
50
1781-1793.
(11) Michaeli, K.; Kantor-Uriel, N.; Naaman, R.; Wa
ldeck, D.H.
Chem. Soc.
Rev.
2016
,
in press
DOI: 10.1039/C6CS00369A.
(12) Mondal, P.C.; Kantor-Uriel, N.; Mathew, S.P.;
Tassinary, F.; Fontanesi,
C.; Naaman, R.
Adv
.
Material
.
2015
,
27
, 1924-1927.
(13) Dor, O.B.; Yochelis, S.; Mathew, S.P.; Naaman,
R.; Paltiel, Y.
Nat
.
Comm
.
2013
,
4
, 2256.
(14) Gutierrez, R.; Diaz, E.; Naaman, R.; Cuniberti
, G.
Phys
.
Rev
.
B
2012
,
85
, 081404.
(15) Naaman, R.; Waldeck, D.H.
Ann. Rev. Phys. Chem
.
2015,
66
, 263
(16) Guo, A.-M; Sun, Q.-F.
Phys
.
Rev
.
Lett
.
2012
,
108
, 218102.
(17) Medina, E.; Lopez, F.; Ratner, M.A.; Mujica, V
.
Eur
.
Phys
.
Lett
.
2012
,
99
, 17006.
(18) Saenger, W.
Principles of nucleic acid structure
; Springer-Verlag, New
York, 1984.
(19) Boon, E. M.; Barton, J. K.
Bioconjugate
Chem
.
2003
,
14
, 1140-1147.
(20) Mondal, P.C.; Fontanesi, C.; Waldeck, D.H.; Na
aman, R.
ACS
Nano
2015
, 9
, 3377-3384.
(21) See Supplementary Materials for additional Fig
ures.
(22) Kelley, S.O.; Barton, J.K.; Jackson, N.M.; McP
herson, L.D.; Potter,
A.B.; Spain, E.M.; Allen, M.J.; Hill, M.G.
Langmuir
1998
,
14
, 6781
Page 4 of 5
ACS Paragon Plus Environment
Journal of the American Chemical Society
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
(23) Kelley, S.O.; Barton, J.K.; Jackson, N.; Hill,
M.G.
Bioconjugate
Chem
.
1997
, 8
, 31-37.
(24) Slinker, J.D.; Muren, N.B.; Renfrew, S.E.; Bar
ton, J.K.
Nat
.
Chem
.
2011
,
3
, 228-233.
(25) Gorodetsky, A.A.; Hammond, W.J.; Hill, M.G.;
Slowinski, K.; Barton,
J.K.
Langmuir
2008
,
24
, 14282-14288.
(26) Muren, N.B.; Barton, J.K.
J. Am. Chem. Soc
.
2013
,
135
, 16632-40.
(27) To test for effects of magnetic field on the C
T rate, we varied the
scan rate from 50 mV/s to 20 V/s (Fig. S2); we see
no difference in the
cathodic/anodic peak splittings when the magnetic f
ield direction is
switched, suggesting that there is no measurable ef
fect on the charge-
transfer rates with a change in magnetic field dire
ction. We stress how-
ever that previous work has shown that in these ele
ctrochemical experi-
ments the DNA CT rates are limited by tunneling thr
ough the alkanethiol
linker, (Drummond, T.G.; Hill, M.G.; Barton, J.K.
J. Am. Chem. Soc
.
2004
,
126
, 15010) not transport through the DNA, so small ch
anges in the in-
herent tunneling efficiencies of oppositely polariz
ed currents through the
π-stack would not be accessible electrochemically.
(28) Yu, H.-Z.; Luo, C.-Y.; Sankar, C.G.; Sen, D.
Anal
.
Chem
.
2003
,
75
, 3902.
(29) Hartmann, B.; Lavery, R.
Q. Rev. Biophys
.
1996
,
29
, 309-368.
(30) Wang, A. H.-J.; Quigley, G.J.; Kolpak, F.J.; C
rawford, J.L.; Van Boom,
J.H.; Van Der Marel, G.A.; Rich, A.
Nature
1979
,
282
, 680-686.
(31) Gutierrez, R.; Diaz, E.; Naaman, R.; Cuniberti
, G.
Phys. Rev. B
2012
,
85
, 081404.
(32) Gutierrez, R.; Diaz, E.; Gaul, C.; Brumme, T.;
Dominguez-Adame, F.;
Cuniberti, G.
J. Phys. Chem. C
2013
,
117
, 22276-22284.
(33) Guo, A.M.; Sun, Q.F.
Proc. Natl. Acad. Sci
.
2014
,
111
, 11658-11662.
(34) Gersten, J.; Kaasbjerg, K.; Nitzan, A
. J. Chem. Phys
.
2013
,
139
,
114111.
(35) Michaeli, K.; Naaman, R.
arXiv,
2016
, 1512.03435v2
(36) Williams, T.T.; Barton, J.K
. J. Am. Chem. Soc
.
2002,
6
, 1840-1841.
(37) O’Neil, M.A.; Barton, J.K.
J. Am. Chem. Soc
.
2004
,
126
, 11471.
(38) Xiang, L.; Palma, J.L.; Bruot, C.; Mujhica, V.
; Ratner, M.A.; Tao, N.
Nature Chem.
2015
,
7
, 221-226.
Authors are required to submit a graphic entry for
the Table of Contents (TOC) that, in conjunction wi
th the manuscript
title, should give the reader a representative idea
of one of the following: A key structure, reaction
, equation, concept, or
theorem, etc., that is discussed in the manuscript.
Consult the journal’s Instructions for Authors for
TOC graphic specifica-
tions.
Insert Table of Contents artwork here
Page 5 of 5
ACS Paragon Plus Environment
Journal of the American Chemical Society
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60