Efficient synthetic supramolecular channels and their light-deactivated ion transport in bilayer lipid membranes

Article abstract of DOI:10.1039/c5nj00937e

Inspired by the critical role of ion channel proteins in the regulation of cellular activities, here we developed a new type of synthetic ion channel by simple benzocrown ether-based derivatives M1 and M2, where M1 had a dodecyl tail and M2 had a diethylene glycol-conjugated dodecyl tail. Being amphiphilic in nature, the two small molecules were assumed to form crown ether channels through supramolecular interactions in bilayer lipid membranes (BLMs). The efficient ion transport was investigated by both a fluorescence-based vesicle assay and a planar bilayer conductance measurement, and M2 with diethylene glycol substitution exhibited more efficient activity comparable to amphotericin B. Moreover, the presence of a photosensitive o-nitrobenzyl group provided the light-regulation to deactivate ion transport by destroying the channel assembly of the molecules in BLMs, which provides new opportunities for developing intelligent light-regulated systems for biomedical applications based on synthetic small molecules.

Full text of DOI:10.1039/c5nj00937e

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Efficient synthetic supramolecular channels and
their light-deactivated ion transport in bilayer
lipid membranes†
Cite this:DOI: 10.1039/c5nj00937e
Chunyan Bao,* Meixin Ma, Funa Meng, Qiuning Lin and Linyong Zhu*
Inspired by the critical role of ion channel proteins in the regulation of cellular activities, here we
developed a new type of synthetic ion channel by simple benzocrown ether-based derivatives M1
and M2, where M1 had a dodecyl tail and M2 had a diethylene glycol-conjugated dodecyl tail.
Being amphiphilic in nature, the two small molecules were assumed to form crown ether channels
through supramolecular interactions in bilayer lipid membranes (BLMs). The efficient ion transport was
investigated by both a fluorescence-based vesicle assay and a planar bilayer conductance measurement,
and M2 with diethylene glycol substitution exhibited more efficient activity comparable to amphotericin
B. Moreover, the presence of a photosensitive o-nitrobenzyl group provided the light-regulation to
deactivate ion transport by destroying the channel assembly of the molecules in BLMs, which provides
new opportunities for developing intelligent light-regulated systems for biomedical applications based
on synthetic small molecules.
Received (in Montpellier, France)
15th April 2015,
Accepted 3rd June 2015
DOI: 10.1039/c5nj00937e
www.rsc.org/njc
supramolecular self-assembly offers simple synthesis, structural
tunability and responsive functionalization to guide the for-
Introduction
Natural ion channels are a type of membrane protein that mation of channels in BLMs. However, the presence of excess
mediate ion flow across plasma membranes and play essential monomer and the participation competition of supramolecular
roles for the regulation of vital activities, including metabolism, aggregates between the solution and membrane phases greatly
signal transduction, cell proliferation and osmotic stress affect the transport efficiency, which increase the difficulty for
response.1–5 The unique transmembrane transport behavior scientists to develop diverse active supramolecular channels.24
of the channel proteins has overwhelmingly compelled chemists Thus, the creation of supramolecular channels with high activity
with great interests to develop various synthetic channels to attracts more and more scientific attention.
mimic the ionic transport processes and thus enhance the
In addition to the efficient ion transport, natural ion channels
understanding of how ion channels work and provide tools for are sensitive to external stimulus, including ligand,25 potential,26
many applications in the life sciences and materials science.6–10 pH27 and light28 stimulation. Although light-sensitive ion trans-
To date, typical architectures of synthetic channels can be location is limited in naturally occurring organisms, a light-regulated
classified into two types, namely, unimolecular and supra- ion channel can enable the direct manipulation of cellular excit-
molecular channels. Cyclodextrins,11 pillararene,12,13 and helical ability in genetically modified cells, because cell activation can be
oligomers14,15 have been greatly used in the former models as directly linked to the diffusion of ions across the cell membrane.29,30
single molecules for efficient channel transport in BLMs, Over the last few decades, many light-regulated channel proteins
while crown ethers,16 cyclic peptides,17 aromatic macrocycles,18 have been reported using either a reversible photo-switch31–33 or
and other supramolecular aggregates19–23 have been applied to irreversible photo-cage methodologies.34–36 In contrast to the
construct supramolecular channels. Compared to the channels photo-switch modified channels with the function of reversible-
constructed by unimolecular macromolecules, the utilization of gated ion transfer, photo-caged channels are irreversible but also
exhibit significant utility in biomedical areas. Koçer et al. reported
Key Laboratory for Advanced Materials, Institute of Fine Chemicals,
East China University of Science and Technology, 130# Meilong Road, Shanghai,
200237, P. R. China. E-mail: baochunyan@ecust.edu.cn, linyongzhu@ecust.edu.cn;
Fax: +86-21-64253742
an o-nitrobenzyl modified protein to show irreversible photo-
activated channel activity,34 while England et al. devised a variant
by preparing a photo-deactivated protein channel to explore the
structure and function of the channel protein.35 By opening ion
channels to activate and restore cell functions, the persistent
partial activation of ion channels is not necessarily a good thing.37
† Electronic supplementary information (ESI) available: The detailed synthesis
and characterizations of compounds, self-assembled properties, some HPTS
assays, doping and solubility measurements. See DOI: 10.1039/c5nj00937e
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chloroform to the hydrophobic phase of membrane, the self-
assembly of the molecules in chloroform and HEPES solution was
characterized by both NMR and TEM to evaluate the morphology.
The downfield shifted signal of the NH protons with increasing
concentration in the concentrated NMR spectra indicated the
formation of self-assembly through intermolecular H-bonding
(Fig. 1a, Fig. S2, ESI†). The micelle-like aggregates in chloroform
(Fig. 1b and c) and the necklace-like fibrous aggregates in the
buffer solution (Fig. 1d and e) further indicated the self-
assembled morphologies through intermolecular supramolecular
interactions. Although no more stacking information was
obtained due to the weakly self-assembled interaction and soft
backbone of the compounds, it was reasonable to speculate
that compounds M1 and M2 would also adopt columnar
stacking, in which the crown ether moieties arrayed into
channel-like stacking.16,39,40
Channel current studies in planar lipid bilayers
Scheme 1 Schematic of (a) the molecular structures, (b) the proposed
channel-like self-assembly of M1 and M2 in the BLMs, (c) the photolysis
mechanism of M1, and (d) the proposed light-deactivated ion transport
mechanism of M1 and M2.
A patch-clamp technique in the planar membrane was first
applied to characterize ion transport of the synthetic ion channels,
For example, an overload of Ca2+ from persistent influx can
induce myocardial necrosis and cell apoptosis.38 Therefore, by
following the efficient activation of ion transport, producing a
light-induced loss of channel ability is also very important.
In this study, we designed two model molecules M1 and M2
(Scheme 1a) to construct efficient supramolecular ion channels
in BLMs and achieve light-regulated loss of channel activity by
intramolecular photocleavage. In the two channel molecules,
18-benzocrown-6 ether, a common cation-recognition moiety,
was selected for potential channel stacking, and an o-nitrobenzyl
phototrigger was introduced as the photocleavage group to deacti-
vate ion transport upon light illumination. We expected that the
amphiphilic character of these molecules could provide a face-to-
face assembly, which helped the formation of a crown ether
channel for transporting ions across BLMs efficiently (Scheme 1b).
The photo-induced cleavage in the amphiphilic building blocks
would trigger disassembly of the channel molecules and disable
ion transport (Scheme 1c and d). We envision that these unique
optical deactivated ion channels, which are quite different from the
reported optical activated protein channels, would possess great
biomedical properties for use in sterilization, anticancer therapy
and treatment of diseases.
Results and discussion
Self-assembly of compounds M1 and M2 in solutions
Amphiphilic compounds M1 and M2 were synthesized easily in
several steps with high yields (Fig. S1, ESI†). Because com-
pounds M1 and M2 have backbones similar to our previous
amphiphilic channel molecules,39,40 we expected them to display
similar channel transport mechanisms via supramolecular self-
assembly of the amphiphiles. Based on the similar property of
Fig. 1 (a) Partial 1H NMR spectra for compound M1 at different concen-
trations in CDCl3 at 25 1C. Direct TEM observation for morphologies of M1
and M2: (b) M1 in chloroform, (c) M2 in chloroform, (d) M1 in 10 mM HEPES
solution and (e) M2 in 10 mM HEPES solution. The samples of d and e were
prepared by dropping the chloroform solution into 10 mM HEPES solution.
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since planar bilayer conductance measurements provided diag- (alkali hydroxide), and then the addition of channel molecules
nostic evidence for a channel mechanism.1,24 After a short duration to these vesicles led to the antiport of H+/K+ or the synport of
of membrane disruption with spikes of highly variable amplitude K+/OHÀ and thus induced the changes in HPTS emission. For
(not shown), both M1 and M2 at 2.5 mM exhibited current signals each set of experiments, the final concentration of the lipids in
during dozens of separated experiments and the predominant the experiments was a constant at 33 mM (assuming 100% of
signals are shown in Fig. 2 (Fig. S3, ESI†). Both of them exhibited lipids were incorporated into liposomes). As shown in Fig. 3a, a
single channel-like character with square-topped current signals variation in the concentration of M1 induced a corresponding
(Fig. 2a). M1 generated a predominant signal of 12.5 pA at 50 mV change in the transmembrane activity, suggesting successful
and the ohmic I–U profiles had a conductance of 0.25 Æ 0.1 nS permeability to ions. Compound M2 exhibited similar but more
(nanosiemens), while M2 had an open current signal of 20 pA at efficient transmembrane activity (Fig. 3b), arriving at a value
50 mV with a specific conductance at 0.40 Æ 0.1 nS (in 1 M KCl). for the normalized fluorescence of 1.0 at a concentration of
The obtained conductance value was consistent with our previous 9.0 mol% (18.0 mol% for M1). To quantitatively compare the
results39,40 and the pore size calculated from the Hille equation transmembrane activities of the amphiphiles, the transport
was about 3.2 Å for M2, matching with the diameter of a single activity EC50 (concentration of transport required to achieve
benzocrown ether (2.8–3.2 Å) (see ESI†).
50% activity) and Hill coefficient n value were determined from
the dose response curves (Fig. S4, ESI†). M2 had an EC50 value
at 3.38 mol%, while M1 had an EC50 value of 10.26 mol%
(B3 times more active than M1). Meanwhile, the nonlinear
relationship between transmembrane activities and concentra-
tions further suggested the channel-like ion transport of
amphiphilic molecules M1 and M2 in lipid bilayers. Since
18-benzocrown-6 ether has selective recognition with K+, the
transmembrane activity with different cations was explored. As
shown in Fig. 4, M1 exhibited a slight preference for transporting
Ion transporting activity studies by vesicle assays
A
8-hydroxy-1,3,6-pyrenetrisulfonate (HPTS) labelled LUV
fluorescence assay was carried out to explore the transport
activity of the channels.24,39 In this assay, the ion transport
through the membranes was accessed by the change in the ratio
of fluorescence intensity at 510 nm (I450/I405) of the pH-sensitive
HPTS dye entrapped inside the vesicles. A pH gradient across
the vesicle membrane was introduced by the addition of base
Fig. 2 Bilayer planar membrane activity of compounds at 2.5 mM in a
DPhPc membrane with 1 M KCl (10.0 mM HEPES, pH 7.0). (a) Selected
single-current signals for M1 and M2; (b) the corresponding current
statistic histograms and Gaussian fitting of the current signal in (a); and
(c) the I–V plot using a voltage ramp from À100 mV to 100 mV.
Fig. 3 HPTS assays for (a) M1 and (b) M2 for K+ transport with increasing
M1 and M2 concentrations (final concentrations, mol% relative to lipids).
Conditions: internal and external buffer (1 mM HPTS, 10 mM HEPES,
100 mM KCl, pH 7.0); external buffer (10 mM HEPES, 100 mM KCl, pH 7.0).
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Fig. 5 Evolution of the UV-vis absorption spectra of M1 (6.0 mM in DMSO
Fig. 4 Assays of cation selectivity of M1 (final concentration, 18.0 mol%).
Conditions: internal buffer (1 mM HPTS, 10 mM HEPES, 100 mM KCl,
pH 7.0); external buffer (10 mM HEPES, 100 mM MCl, pH 7.0).
with microcuvette) as a function of the irradiation with a 365 nm LED lamp
at 30 mW cmÀ2
.
carbon dioxide, and the corresponding nitroso ketone derivative
(Scheme 1c). Accompanying the successful photolysis, the self-
assembly of the molecules was also disrupted as confirmed by
the collapsed TEM morphologies (Fig. S11, ESI†). Knowing that
efficient ion transport of the amphiphiles was triggered by a
supramolecular channel mechanism, the light-induced destruction
of the assembly in both solution and BLMs would deactivate the
ion transport, as illustrated in Scheme 1d.
The photo-deactivated ion transport of the molecules in
BLMs was investigated by HPTS assays. A 365 nm LED lamp
with an intensity of 30 mW cmÀ2 was used to irradiate the
DMSO stock solutions containing the compounds. Aliquots
that were irradiated for certain time intervals were used for
the assay. To optimize the photo-regulation of transmembrane
activity, 18.0 mol% M1 and 9.0 mol% M2 were applied based on
their maximum transport ability at these concentrations. As
shown in Fig. 6, the transmembrane activity for both com-
pounds decreased rapidly upon irradiation of 365 nm UV light
and reached a minimum after ten minutes. Upon irradiation,
M1 displayed a significant decrease in transmembrane activity,
decreasing from 0.97 to 0.09 (subtracting the DMSO back-
ground, Fig. 6a), while M2 displayed an even more rapid
decrease from 1.00 to 0.05 (subtracting the DMSO background,
Fig. 6b). The activity variation before and after 365 nm irradia-
tion at different concentrations was also measured (Fig. S12,
ESI†). This suggested that the photo-irradiation significantly
decreased the transport activities of the compounds.
K+ over Rb+, Cs+, Na+ and Li+. All of this suggests that the ion
transport of the compounds could be due to the channel for-
mation by crown ether stacking and not through undefined
perturbation or pores created by the other constituents of the
molecules (as illustrated in Scheme 1b).
To illustrate efficient ion transport of M1 and M2, ampho-
tericin B, a commercial channel antibiotic, was analyzed using
HTPS transmembrane activity assay under the same conditions
(Fig. S5, ESI†). Similarly, the transmembrane activity of ampho-
tericin B increased as a function of concentrations and reached
a maximum activity of B0.8 at 181.8 mol% with EC50
=
3.0 mol%. The comparable transmembrane activity to ampho-
tericin B suggested that both M1 and M2 possessed excellent
ion transport activity across BLMs, and M2 was especially
effective due to its diethylene glycol substitution. To clarify
the improved transmembrane activity of M2 compared to M1,
the solubility of the compounds in buffer solution and their
doping amounts in the BLMs were determined.39 Unexpectedly,
the compounds exhibited similar solubility (480 mM, Fig. S6,
ESI†) and doping amount within the BLMs (B70%, Fig. S7,
ESI†). Combining with the similar association constants with
K+ ions of M1 and M2 (Table S1, ESI†), the improved trans-
membrane activity of M2 could be attributed to the different
ion–dipole interactions by way of the diethylene glycol substi-
tution (Fig. S8, ESI†).41,42
Photo-deactivated ion transport
To quantitatively compare the regulated ion transport before
The photolysis process of M1 was detected by the evolution of and after light irradiation, the transmembrane activity of the
the UV-vis absorption signal. As shown in Fig. 5, with an main photolysis products, 4-amino-18-benzocrown-6 ether, was
increase in irradiation time, the absorption band at 358 nm detected (Fig. S13, ESI†). There was a linear relationship
decreases, which is accompanied by the appearance of a band between activity and concentrations, with an EC50 4 2.2 Â
at 380 nm, indicating the photo-cleavage of M1 into its products.43 103 mol%, which was considerably higher than the EC50 of M1
The generation of isosbestic points at 288, 303, and 346 nm and M2 by a factor of 103, suggesting the carrier transport of the
indicate a relatively clean photochemical reaction for M1 upon photolysis product with significantly lower activity and providing
irradiation. The photolysis products of M1 and M2 were verified the determinate reason for the significantly decreased transport
1
by the H NMR spectroscopy and HPLC (Fig. S9 and S10, ESI†), activity of photo-irradiated M1 and M2. The photo-deactivated
including one molecule of parent 4-amino-benzocrown ether, ion transport was also confirmed by in situ photo-regulation of
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products with three orders of magnitude lower transport activity,
producing the light-regulated deactivation of ion transport. These
readily available small molecules can be used to easily regulate
ion transport via light illumination.
Experimental section
Materials
All starting materials were obtained from commercial suppliers
and were used without further purification unless otherwise
stated. All air- or moisture-sensitive reactions were performed
using oven-dried or flame-dried glassware under an inert atmo-
sphere of dry argon. Air- or moisture-sensitive liquids and
solutions were transferred via syringe. Egg yolk phosphatidyl-
choline (EYPC) was obtained from Avanti Polar lipids as a
solution in chloroform (25 mg mLÀ1). 8-Hydroxy-1,3,6-pyrene-
trisulfonate (HPTS) and trixon-100 were obtained from Sigma-
Aldrich and used without further purification.
Characterizations
Proton and carbon nuclear magnetic resonance spectra (1H, 13
C
NMR) were recorded using a Bruker Avance 500 (400 MHz)
spectrometer. Chemical shifts were reported in parts per
million (ppm) downfield from the Me4Si resonance which was
used as the internal standard when recording 1H NMR spectra.
Mass spectra were recorded using a Micromass GCTTM and a
Micromass LCTTM. Fluorescence measurements were per-
formed using a Varian Cary Eclipses fluorescence spectrometer
equipped with a stirrer and a temperature controller (kept
at 25 1C unless otherwise noted). Absorption spectra were
recorded using a Shimadzu UV-2550 UV-vis spectrometer. A
Mini-Extruder used for the preparation of large unilamellar
vesicles (LUVs) was purchased from Avanti Polar lipids. The size
of EYPC vesicles was determined using a Delsat Nano Submicron
Particle Size and Zeta Potential Particle Analyzer (Beckman Coulter
Inc., USA). A 365 nm LED lamp (30 mW cmÀ2) was used for the
photolysis of compounds and photo-controlled experiments.
Detailed synthesis methods and partial experimental data
are described in the ESI.†
Fig. 6 Observed change in transmembrane activity when (a) M1 (18.0 mol%,
final concentration) and (b) M2 (9.0 mol%, final concentration) were photo-
cleaved by irradiation at 365 nm UV light (30 mW cmÀ2).
Fig. 7 In situ photo-regulation of the current signal of M1 for the ion
transport on the planar BLMs at 50 mV.
compound M1 on planar BLMs (Fig. 7). Upon irradiation at
365 nm, the frequency of the open current signal was signifi-
cantly reduced and even disappeared after several minutes.
Acknowledgements
This work was supported by NSFC (51273064, 21472044),
Innovation Program of Shanghai Municipal Education Com-
mission and Fundamental Research Funds for the Central
University.
Conclusions
In conclusion, we developed a new class of supramolecular
synthetic ion channels based on the structurally simple amphi-
philic molecules M1 and M2. The 8-hydroxy-1,3,6-pyrenetri-
sulfonate (HPTS) fluorescence assay and the patch-clamp current
experiment revealed that both the amphiphiles possessed effi-
cient ion channel transmembrane activity across bilayer lipid
membranes, and M2 was particularly active with comparable
activity to amphotericin B because of its diethylene glycol
substitution. Upon light irradiation, there was a deformation
of the self-assembled channel and generation of photolysis
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