Photoresponsive Molecular Switch for Regulating Transmembrane Proton-Transfer Kinetics

Article abstract of DOI:10.1021/jacs.5b10016

To control proton delivery across biological membranes, we synthesized a photoresponsive molecular switch and incorporated it in a lipid layer. This proton gate was reversibly activated with 390 nm light (Z-isomer) and then deactivated by 360 nm irradiation (E-isomer). In a lipid layer this stimuli responsive proton gate allowed the regulation of proton flux with irradiation to a lipid-buried O₂ reduction electrocatalyst. Thus, the catalyst was turned on and off with the E-to-Z interconversion. This light-induced membrane proton delivery system may be useful in developing any functional device that performs proton-coupled electron-transfer reactions.

Full text of DOI:10.1021/jacs.5b10016

Subscriber access provided by KUNGL TEKNISKA HOGSKOLAN
Communication
Photo-responsive Molecular Switch for Regulating
Trans-membrane Proton Transfer Kinetics
Ying Li, Edmund C. M. Tse, Christopher J. Barile, Andrew A. Gewirth, and Steven C. Zimmerman
J. Am. Chem. Soc., Just Accepted Manuscript • DOI: 10.1021/jacs.5b10016 • Publication Date (Web): 29 Oct 2015
Downloaded from http://pubs.acs.org on October 29, 2015
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.
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.

Page 1 of 5
Journal of the American Chemical Society
1
2
3
4
5
6
7
8
9
Photo-responsive Molecular Switch for Regulating Transmembrane
Proton Transfer Kinetics
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
Ying Li,† Edmund C. M. Tse,† Christopher J. Barile,† Andrew A. Gewirth,*,†,§ and
Steven C. Zimmerman*,†
† Department of Chemistry, University of Illinois at Urbana−Champaign, 600 South Mathews Avenue, Urbana,
Illinois 61801, United States
§ International Institute for Carbon Neutral Energy Research (WPI-I2CNER), Kyushu University, Fukuoka
812-8581, Japan
Supporting Information
of lipid-bound aliphatic acids function as a pH-sensitive
ABSTRACT: To control proton delivery across biological
switch turning on and off transmembrane proton delivery
membranes, we synthesized a photo-responsive molecu-
to the catalyst.15 The proton delivery via this flip-flop dif-
lar switch and incorporated it in a lipid layer. This proton
fusion of the proton carriers occurs spontaneously in the
gate was reversibly activated with 390 nm light (Z-isomer)
presence of a pH gradient.18,19 It can be advantageous to
and then deactivated by 360 nm irradiation (E-isomer). In
regulate the proton transfer kinetics more precisely with-
a lipid layer this stimuli responsive proton gate allowed
out the associated perturbation in proton thermodynam-
ics that arises with a pH change.
the regulation of proton flux with irradiation to a lipid-
buried O2 reduction electrocatalyst. Thus the catalyst was
turned on and off with the E- to Z-inter-conversion. This
light-induced membrane proton delivery system may be
Scheme 1. Preparation of the protected photoswitch
molecules: Z-1 and E-1.
useful in developing any functional device that performs
proton-coupled electron transfer (PCET) reactions.
Precisely regulated proton transfer is essential to many
biological reactions and alternative energy schemes that
involve redox reactions with one or more proton-coupled
electron transfer (PCET) steps.1-4 As one example, the ox-
ygen reduction reaction to form water (ORR: O2 + 4e– +
4H+ → 2H2O) is critical to sustaining life on earth.5,6 Cy-
tochrome c oxidase (CcO) and laccase are two enzymes
that evolved to develop intricate proton transport chains
which provide exquisite control over the kinetics of pro-
ton delivery to the ORR active site.7-11
The mechanisms associated with multi-step PCET reac-
tions are difficult to decipher because of the intricate in-
terplay between the thermodynamics and kinetics of elec-
tron and proton transfer.2-4,12 The use of a self-assembled
monolayer (SAM) can decouple the kinetics and thermo-
dynamics of electron transfer, the latter dictated by the
electrode potential.13,14 We recently developed a new ex-
perimental framework using a hybrid bilayer membrane
To avoid concomitant changes in proton thermody-
(HBM) to delineate the relative importance of the kinetics
namics while modulating the proton kinetics, natural
and thermodynamics of proton transfer to a system that
systems utilize light to execute an additional level of con-
catalyzes PCET reactions.15,16 A HBM consists of a SAM
trol over proton and electron transfer steps by having
with a monolayer of lipid appended on top.17 In one em-
specific functional groups that adopt precise photo-
bodiment,
a dinuclear Cu molecular ORR catalyst
induced conformational changes. For example, a 5 Å
movement of an ubiquinone moiety accompanied by a
180° propeller twist of an isoprene chain upon illumina-
tion in the photosynthetic reaction center of Rhodobacter
(CuBTT: Cu complex of 6-((3-(benzylamino)-1,2,4-triazol-
5-yl)amino)hexane-1-thiol) forms the SAM.16 We previous-
ly demonstrated that the spontaneous flip-flop diffusion
ACS Paragon Plus Environment

Journal of the American Chemical Society
Page 2 of 5
sphaeroides is a necessary prerequisite to proton uptake derivatization, lack of thermal relaxation at room temper-
for photosynthesis that involves PCET steps.20 The intri-
cate photo-regulation of proton transport in nature has
inspired a tremendous amount of effort towards mimick-
ing these natural systems on the macromolecular level.21
Although artificial photosynthetic reaction centers have
been developed in the past decades,22,23 the photo-
regulation of transmembrane proton kinetics without
involving electron transfer or proton thermodynamics
fluctuation to our best knowledge has not been achieved
with a single-component small molecular system.
ature, high quantum yield (50%) for E to Z photoisomeri-
zation, and quantitative Z to E reversion.27-32 The stiff stil-
bene moiety has been applied as a light driven internal
molecular force probe.31,32 Nevertheless, the proton gating
ability of functional materials based on stiff stilbene re-
mains largely unexplored.
1
2
3
4
5
6
7
8
We first prepared both the Z- and E-forms of the pro-
tected photo-responsive switch, the synthesis beginning
from the photoreactive core, followed by the sequential
installation of the alkyl tail and the protected acid head-
group (see Scheme 1 and SI for details). The trivalent N-
methyliminodiacetic acid (MIDA) ligand, developed by
Burke and coworkers,33,34 was used to avoid decomposi-
tion of the boronic acid group during the synthesis. In-
deed, the MIDA boronate ester was simply prepared from
commercially available starting materials, survived the
harsh reaction conditions, and allowed purification by
chromatography. The deprotection of Z-1 and E-1 was
easily achieved at room temperature with concentrated
aqueous NaOH solution to afford the two isomers Z-BA
and E-BA, respectively.
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 1. a) Structures of E-BA and Z-BA with the protons of
interest labeled; b) stacked truncated NMR spectra of BA (Z-
and E-isomers) in CD2Cl2, indicating the corresponding pro-
*
1
ton signal shifts according to the irradiation cycles. = H
resonance of the methyl group from MIDA after the depro-
tection step; c) repeated cycles of E-BA to Z-BA conversion.
See SI for additional information (e.g., irradiation times).
Figure 2. (a) Schematic of the HBMs studied: (i) DMPC only,
(ii) DMPC with Z-BA incorporated, and (iii) DMPC with E-
BA incorporated. (b) Linear sweep voltammograms (LSVs) of
O2 reduction catalyzed by CuBTT covered by a monolayer of
DMPC (black) with Z-BA (blue) or E-BA (red) incorporated
in the lipid layer in O2-saturated pH 7 buffer at 10 mV/s.
A HBM with a photo-responsive proton carrier could
mimic the light-induced conformational gating found in
nature and afford a new approach to tune transmembrane
proton transfer kinetics with temporal and spatial control.
Further, such a system could eliminate the need for
chemical inputs that invariably generates waste products.
In this report, we develop a simple, artificial, membrane-
bound, photo-responsive proton carrier that regulates
proton kinetics across a lipid membrane. The new proton
carrier (BA) features a boronic acid head-group for proton
transfer, a stiff stilbene body for photo-responsiveness,
and an alkyl tail for lipid incorporation. Boronic acids
typically exhibit pKa values of ca. 9,24 a feature that en-
sures the proton carrier to be mostly in the neutral form
in pH 7 solution. The ability of BA to cycle between two
photo-distinguishable states allows us to construct a
proof-of-concept, light-addressable transmembrane pro-
ton kinetics regulator in a HBM platform without per-
turbing the proton thermodynamics in the bulk solution.
The light-induced E-Z isomerization of BA was first
1
demonstrated in solution and followed by H NMR spec-
troscopy. Figure 1a displays the structures of E-BA and Z-
BA, and highlights the protons whose resonances were
followed in the 1H NMR study. Figure 1b shows an overlay
1
of truncated H NMR spectra: Z-BA, E-BA and one cycle
of the E-Z-E conversion. The protons Ha and Hb in Z-BA
(Figure 1b, black line) appeared at 2.88 and 2.79 ppm,
respectively. Their equivalent protons Ha’ and Hb’ in E-BA
(red line) shifted downfield to 3.15 ppm (Δδ [Ha] = 0.27
ppm) and 3.05 ppm (Δδ [Hb] = 0.26 ppm), corresponding-
ly. Upon UV irradiation at 360 nm, about 40% of E-BA
1
was converted into Z-BA according to the H NMR inte-
gration (green line). The mixture was exposed to UV irra-
diation at 390 nm and the Z-isomer was almost quantita-
tively converted back to the E-isomer (blue line). The
complete Z- to E- and partial E- to Z-stilbene photo-
isomerization is consistent with reported systems.27,28 The
full isomerization cycle was repeated two more times, and
similar results were obtained. Figure 1c shows the per-
centage of E-BA versus the total BA plotted across se-
Like many other photo-responsive chromophores,25,26
a
stiff stilbene moiety (1,1′-biindane) has either a Z or E con-
figuration with respect to its central double bond upon
photoisomerization.27-29 This chromophore has garnered
increasing attention because of its scalable synthesis, easy
ACS Paragon Plus Environment

Page 3 of 5
Journal of the American Chemical Society
quential photo-irradiation events. Despite these observa-
O2 reduction current density at -450 mV drops by about
ble changes in the 1H NMR spectra, no significant changes
60% and 95%, respectively (Figure 3a, red and blue lines).
As the irradiation time increases, the O2 reduction cur-
rent decreases until it reaches nearly the same value as
the lipid-only case or the case with E-BA added to the
DMPC layer. These findings indicate that as more of the
proton carrier is converted to its inactive form (E-BA),
fewer protons are delivered across the lipid membrane,
thus resulting in less catalytic O2 reduction current.
1
2
3
4
5
6
7
8
11
are notable in the B NMR spectra (Figure S1), suggesting
that the boronic-acid group remains intact.
Having demonstrated in solution the reversible photo-
responsiveness of E-BA and Z-BA, we probed their ability
to act as proton carriers in a HBM. Figure 2a displays the
architecture of the three HBMs with and without BA in-
corporated in the lipid layer. Figure 2b shows linear sweep
voltammograms (LSVs) of O2 reduction by a SAM of
CuBTT covered by a DMPC monolayer with and without
the proton carriers added. In the absence of the proton
carriers, the lipid layer blocks access of protons in bulk
solution to CuBTT inside a HBM, resulting in a back-
ground O2 reduction current density of about 40 µA cm-2
at -450 mV vs. Ag/AgCl (Figure 2b, black line).
9
Figure 3b shows O2 reduction LSVs by CuBTT covered
by a DMPC monolayer with E-BA added to the lipid layer
with various irradiation periods. Upon irradiation with
360 nm for 10 s, the O2 reduction current density increas-
es by about 65% (Figure 3b, red line). The O2 reduction
current reaches a value similar to the case with Z-BA add-
ed to the DMPC layer by irradiating for 1 min (blue line).
Although the solution studies (Figure 1) indicated that E-
Z isomerization is non-quantitative, the results shown
here suggest that a sufficient amount of Z-isomer is gen-
erated in the lipid layer to achieve saturation in the
transmembrane proton flux. We note that the E-to-Z
switching time is shorter than the Z-to-E switching time,
an observation consistent with the isomerization kinetics
of other stiff stilbenes.37 Control experiments demonstrate
that the integrity of the CuBTT SAM and the lipid layer is
not compromised by irradiating with light at 360 and 390
nm (Figure S3a-c). For example, the possibility of pore
formation or another defect is ruled out using K3Fe(CN)6
as a probe (Figure S3d). Furthermore, we interrogate the
content of the lipid layer using ESI-MS, which confirms
the presence of proton carrier in the lipid layer (Figure
S4). Taken together, these results represent the first ex-
ample of using a molecular switch and light to gate pro-
ton delivery across a phospholipid membrane.
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 3. (a) O2 reduction LSVs in O2-saturated pH 7 phos-
phate buffer at a scan rate of 10 mV/s by CuBTT covered by a
monolayer of DMPC with Z-BA incorporated in the lipid
layer irradiated with 390 nm light for 0 min (black), 1 min
(red), and 5 min (blue), and (b) E-BA incorporated in the
lipid layer irradiated with 360 nm light for 0 s (black), 10 s
(red), and 60 s (blue).
Upon incorporating Z-BA, the O2 reduction current
density at -450 mV increases by about 60% (blue line),
indicating that Z-BA delivers protons from bulk solution
across the lipid layer to the CuBTT catalyst for O2 reduc-
tion as has been demonstrated previously for other pro-
ton carriers in HBM systems.15,16 However, the O2 reduc-
tion current density with E-BA added to the lipid layer
(red line) is the same as the lipid-only case, signifying that
E-BA is unable to transport protons across the hydropho-
bic lipid layer. The different behavior of E-BA and Z-BA is
likely not a result from a change in pKa, because analo-
gous carboxylic acids exhibit similar pKa values (Figure
S2). We propose that the effect originates from the differ-
ent lengths of the two isomers in the phospholipid. When
the proton carrier isomerizes from E to Z, it decreases in
length by ~10 Å and reduces the van der Waals interac-
tions between the proton carrier and the phospholip-
ids.35,36 Thus, we suggest that, relative to the E-isomer the
Z-isomer has a lower energy barrier for transmembrane
flip-flop diffusion and thus induces proton delivery.
Figure 4. O2 reduction LSVs in O2-saturated pH 7 phosphate
buffer at a scan rate of 10 mV/s by CuBTT covered by a mon-
olayer of DMPC with Z-BA incorporated in the lipid layer
(black) irradiated with 390 nm light for 5 min (red) followed
by 360 nm light for 1 min (blue).
We further examined light-induced proton delivery in a
HBM after a complete on-off-on cycle. Figure 4 displays
LSVs of O2 reduction by CuBTT covered by a DMPC
monolayer with Z-BA incorporated after sequential irra-
diation. Upon irradiation at 390 nm for 5 min and then at
360 nm for 1 min, the O2 reduction current density is re-
vived to within 10% of the current density of the initial
on-state (Figure 4, blue line), showing the reversibility of
We next explore the photo-switching behavior of E-BA
and Z-BA in a HBM. Figure 3a displays a set of LSVs of O2
reduction by CuBTT covered by a DMPC monolayer with
Z-BA added to the lipid layer with various irradiation pe-
riods. Upon irradiation with 390 nm for 1 and 5 min, the
1
the system. H NMR spectra demonstrate that the slight
ACS Paragon Plus Environment

Journal of the American Chemical Society
Page 4 of 5
(6) Hüttemann, M.; Pecina, P.; Rainbolt, M.; Sanderson, T. H.;
Kagan, V. E.; Samavati, L.; Doan, J. W.; Lee, I. Mitochondrion
2011, 11, 369-381.
decrease in O2 reduction current density stems from
leaching of the proton carrier from the lipid layer of the
HBM into bulk solution (Figure S5).
1
2
3
4
5
6
7
8
(7) Brändén, G.; Gennis, R. B.; Brzezinski, P. BBA-Bioenergetics
2006, 1757, 1052-1063.
In summary, we have developed the first photo-
responsive proton gate in a HBM and demonstrated its
application by successively turning off and back on pro-
ton transfer for use in a PCET reaction without concomi-
tant changes in solution pH. The photo-switch uses the
interconversion of the Z- or E-isomer, which allows a flip-
ping mechanism that, in turn, facilitates transmembrane
proton delivery. This matching of molecular to lipid
structure by modulating proton flux directly leads to the
on- and off-switching of the lipid-covered O2 reduction
catalyst. We envision that by delineating the effects of
proton transfer thermodynamics and kinetics, we can
further elucidate the reaction mechanism of PCET pro-
cesses. Further spatial regulation of this photo-responsive
proton gate in the bio-inspired HBM platform could per-
mit the development of more complex hybrid models for
future biophotonics, optoelectronics, molecular switches,
and memory elements.
(8) Hofacker, I.; Schulten, K. Proteins 1998, 30, 100-107.
(9) Kirchberg, K.; Michel, H.; Alexiev, U. BBA-Bioenergetics 2013,
1827, 276-284.
(10) Bento, I.; Silva, C.; Chen, Z.; Martins, L.; Lindley, P.; Soares, C.
BMC Struct. Biol. 2010, 10, 28.
9
(11) Silva, C. S.; Damas, J. M.; Chen, Z.; Brissos, V.; Martins, L. O.;
Soares, C. M.; Lindley, P. F.; Bento, I. Acta Crystallogr. D 2012,
68, 186-193.
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
(12) Mayer, J. M. Annu. Rev. Phys. Chem. 2004, 55, 363-390.
(13) Chidsey, C. E. D. Science 1991, 251, 919-922.
(14) Bard, A. J.; Faulkner, L. R. Electrochemical Methods: Fundamen-
tals and Applications; Wiley: New York, 2000.
(15) Barile, C. J.; Tse, E. C. M.; Li, Y.; Sobyra, T. B.; Zimmerman, S.
C.; Hosseini, A.; Gewirth, A. A. Nat. Mater. 2014, 13, 619-623.
(16) Hosseini, A.; Barile, C. J.; Devadoss, A.; Eberspacher, T. A.;
Decreau, R. A.; Collman, J. P. J. Am. Chem. Soc. 2011, 133, 11100-
11102.
(17) Hosseini, A.; Collman, J. P.; Devadoss, A.; Williams, G. Y.; Ba-
rile, C. J.; Eberspacher, T. A. Langmuir 2010, 26, 17674-17678.
ASSOCIATED CONTENT
Supporting Information
(18) Schönfeld, P.; Schild, L.; Kunz, W. BBA-Bioenergetics 1989, 977,
266-272.
Experimental procedures, NMR spectra, and electro-
chemical data. The Supporting Information is available
free of charge on the ACS Publications website at
http://pubs.acs.org.
(19) McConnell, H. M.; Kornberg, R. D. Biochemistry 1971, 10, 1111-
1120.
(20) Stowell, M. H. B.; McPhillips, T. M.; Rees, D. C.; Soltis, S. M.;
Abresch, E.; Feher, G. Science 1997, 276, 812-816.
(21) Koçer, A.; Walko, M.; Meijberg, W.; Feringa, B. L. Science 2005,
309, 755-758.
AUTHOR INFORMATION
Corresponding Author
(22) Steinberg-Yfrach, G.; Liddell, P. A.; Hung, S.-C.; Moore, A. L.;
Gust, D.; Moore, T. A. Nature 1997, 385, 239-241.
(23) Xie, X.; Crespo, G. A.; Mistlberger, G.; Bakker, E. Nat. Chem.
2014, 6, 202-207.
* sczimmer@illinois.edu
* agewirth@illinois.edu
(24) Hall, D. G. In Boronic Acids; Wiley-VCH Verlag GmbH & Co.
KGaA: Weinheim, Germany, 2006, p 1-99.
Notes
(25) Beharry, A. A.; Woolley, G. A. Chem. Soc. Rev. 2011, 40, 4422-
4437.
The authors declare no competing financial interest.
(26) Klajn, R. Chem. Soc. Rev. 2014, 43, 148-184.
ACKNOWLEDGMENT
(27) Xu, J.-F.; Chen, Y.-Z.; Wu, D.; Wu, L.-Z.; Tung, C.-H.; Yang, Q.-
Z. Angew. Chem. Int. Ed. 2013, 52, 9738-9742.
S.C.Z. acknowledges support of the National Science
Foundation (NSF CHE-1307404). E.C.M.T. acknowledg-
es a Croucher Foundation Scholarship. C.J.B. acknowl-
edges a National Science Foundation Graduate Re-
search Fellowship (NSF DGE-1144245) and a Springborn
Fellowship. We thank the US Department of Energy
(DEFG02-95ER46260) for support of this research.
(28) Yan, X.; Xu, J.-F.; Cook, T. R.; Huang, F.; Yang, Q.-Z.; Tung, C.-
H.; Stang, P. J. Proc. Natl. Acad. Sci. USA 2014, 111, 8717-8722.
(29) Wang, J.; Feringa, B. L. Science 2011, 331, 1429-1432.
(30) Kucharski, T. J.; Boulatov, R. J. Mater. Chem. 2011, 21, 8237-8255.
(31) Yang, Q.-Z.; Huang, Z.; Kucharski, T. J.; Khvostichenko, D.;
Chen, J.; Boulatov, R. Nat. Nano. 2009, 4, 302-306.
(32) Akbulatov, S.; Tian, Y.; Boulatov, R. J. Am. Chem. Soc. 2012, 134,
7620-7623.
REFERENCES
(33) Uno, B. E.; Gillis, E. P.; Burke, M. D. Tetrahedron 2009, 65, 3130-
3138.
(1) Chang, C. J.; Chang, M. C. Y.; Damrauer, N. H.; Nocera, D. G.
BBA-Bioenergetics 2004, 1655, 13-28.
(34) Gillis, E. P.; Burke, M. D. J. Am. Chem. Soc. 2007, 129, 6716-6717.
(2) Weinberg, D. R.; Gagliardi, C. J.; Hull, J. F.; Murphy, C. F.; Kent,
C. A.; Westlake, B. C.; Paul, A.; Ess, D. H.; McCafferty, D. G.;
Meyer, T. J. Chem. Rev. 2012, 112, 4016-4093.
(35) Disalvo, E. A.; Simon, S. A. Permeability and Stability of Lipid
Bilayers; Taylor & Francis: Boca Raton, FL, 1995.
(36) Kampf, J. P.; Cupp, D.; Kleinfeld, A. M. J. Biol. Chem. 2006, 281,
21566-21574.
(3) Mayer, J. M.; Rhile, I. J. BBA-Bioenergetics 2004, 1655, 51-58.
(4) Hammes-Schiffer, S. Acc. Chem. Res. 2009, 42, 1881-1889.
(5) Arnold, S. Mitochondrion 2012, 12, 46-56.
(37) Quick, M.; Berndt, F.; Dobryakov, A. L.; Ioffe, I. N.; Granovsky,
A. A.; Knie, C.; Mahrwald, R.; Lenoir, D.; Ernsting, N. P.; Ko-
valenko, S. A. J. Phys. Chem. B 2014, 118, 1389-1402.
ACS Paragon Plus Environment

Page 5 of 5
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
5
ACS Paragon Plus Environment