pH-Dependent ion permeability control of a modified amphotericin B channel through metal complexation

Article abstract of DOI:10.1039/d0cc08368b

Amphotericin B incorporating 2,2'-bipyridine (bpy-AmB) forms a membrane channel exhibiting pH-dependent Ca²⁺ion permeability with a selective response to Cu²⁺ions. The coordination structure at bpy sites depends on the pH and metal ions can control the association state of bpy-AmB in the membrane.

Full text of DOI:10.1039/d0cc08368b

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pH-Dependent ion permeability control of a
modified amphotericin B channel through
metal complexation†
Cite this: Chem. Commun., 2021,
57, 2895
Received 27th December 2020,
Accepted 4th February 2021
Tomomi Koshiyama, *a Yuki Inoue,b Sana Asada,b Koki Kawahara,b Shogo Ide,b
b
Kazuma Yasuharac and Masaaki Ohba
*
DOI: 10.1039/d0cc08368b
rsc.li/chemcomm
Amphotericin B incorporating 2,20-bipyridine (bpy-AmB) forms a forming effective channel assemblies. As another approach
membrane channel exhibiting pH-dependent Ca2+ ion permeability using metal complexes, many synthetic metal–organic polyhedral
with a selective response to Cu2+ ions. The coordination structure channels have been reported in recent years.10 These channels are
at bpy sites depends on the pH and metal ions can control the pre-organized and then embedded in the membrane, making
association state of bpy-AmB in the membrane.
them difficult to control. Thus, it remains challenging to control
the molecular association state of channel-forming building
Bioinspired synthetic ion channels and nanopores are important blocks within a membrane through metal coordination.
tools for investigating membrane transport processes and are In this paper, we describe a design for pH-dependent ion
expected to be applied in the development of sensing, drug permeability control triggered by metal complexation (Fig. 1).
release, and antibiotic agents.1,2 Various synthetic channels have We selected amphotericin B (AmB), an antifungal antibiotic,
been synthesized using linear and cyclic peptides and synthetic as a channel-forming compound. The self-assembly of 4–12
organic polymers as channel-forming building blocks.1–5 Once AmB molecules in lipid bilayers provides AmB channels with
these building blocks are inserted into a membrane, they can diameters of 3–10 Å, which provide permeability for cations,
self-assemble into ion channels as a result of weak intra- and anions and small molecules.11–15 The most widely known
intermolecular interactions including hydrogen bonding and p–p model of AmB channels are single- and double-length channels
stacking. Metal coordination is also expected to be useful for that span across the lipid bilayers.13,16,17 The elucidation of the
controlling self-assembly of channel-forming building blocks molecular association state of AmB within a membrane shows
because it can be strictly regulated by designing coordination two important features for forming AmB channels: (i) electro-
structures with appropriate metal ions and ligands. In nature, an static interactions of carboxyl and amino groups of AmB
antimicrobial peptide known as dermcidin utilizes the coordina- between neighboring AmB molecules and (ii) intermolecular
tion of zinc ions to amino acid side chains to drive formation of hydrogen bond and van der Waals interactions between AmB
its stable hexameric channel in lipid bilayers.6,7 A few examples of molecules and ergosterol.13,18 We modified AmB with a metal
artificial channels formed using metal coordination have been
reported.3,8,9 S. J. Webb et al. have described palladium(II)-gated
ion channels formed using assembly and disassembly of cholic
acid derivatives with an appended pyridyl group in bilayers
through the addition and removal of a palladium ion.8 Both in
nature and in artificial systems, metal coordination is useful for
a Department of Applied Chemistry, College of Life Sciences, Ritsumeikan University,
1-1-1, Noji-higashi, Kusatsu, Shiga 525-8577, Japan.
E-mail: koshi@fc.ritsumei.ac.jp
b Department of Chemistry, Faculty of Science, Kyushu University, 744 Motooka,
Nishi-ku, Fukuoka 819-0395, Japan. E-mail: ohba@chem.kyushu-univ.jp
c Division of Materials Science, Nara Institute of Science and Technology,
Fig. 1 (a) Structure of amphotericin
(bpy-AmB), and (b) schematic representation of ion permeability control
of bpy-AmB through metal complexation by a bpy site.
B
modified with 2,20-bipyridine
8916-5 Takayama, Ikoma, Nara, 630-0192, Japan
† Electronic supplementary information (ESI) available. See DOI: 10.1039/
d0cc08368b
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binding site, 2,20-bipyridine ligand (bpy-AmB), to add metal-
binding ability. When bpy-AmB coordinates to a metal ion, a
metal–bpy-AmB complex is formed which has characteristics
that depend on the type of metal ion and pH. The coordination
leads to a change in the molecular association state of bpy-AmB
in a lipid membrane (Fig. 1). Here, we demonstrate that
bpy-AmB exhibits pH-dependent Ca2+ ion permeability in the
presence of Cu2+ ions. Spectral analyses suggest that the con-
version of bpy-AmB molecules from the monomer form to the
associated form is triggered by Cu2+ binding.
Fig. 2 Ca2+-influx assays of bpy-AmB and AmB in the presence of Cu2+
ions at pH 9.0 and 7.0.
2,20-bipyridine (bpy) can bind to various metal ions in
aqueous media, and its metal complexes adopt various coordi- metal complexation by bpy-AmB (Fig. S2b, ESI†). As a control
nation geometries depending on the type of metal ion and pH. experiment, both bpy-AmB and AmB showed no ion-channel
In particular, Cu(II)-bpy complexes in 1 : 1 Cu(II) : bpy solution activity in the absence of metal ions at pH 9.0 or pH 7.0
give a mononuclear complex [Cu(H2O)2(bpy)]2+ at pH o8, and a (Fig. S2d and e, ESI†). It was found that the addition of metal
hydroxo-bridged dinuclear complex [Cu2(m-OH)2(bpy)2]2+ at pH ions to bpy-AmB induces Ca2+ permeability, and only Cu2+ ions
8–12, as a result of coordination/dissociation of hydroxo ions showed pH dependence of the channel activity.
(Fig. 1).19–21 On the other hand, Ni(II) and Co(II)-bpy complexes
To evaluate the molecular association state of bpy-AmB and AmB
provide [M(bpy)]2+, [M(bpy)2]2+ and [M(bpy)3]2+, and do not in the POPC membrane before the addition of metal ions, UV-vis
form the [M2(m-OH)2(bpy)2]2+.21–23 The bpy moiety of bpy-AmB spectra of bpy-AmB or AmB in POPC liposome suspensions at pH
was conjugated to the amine group of the mycosamine sugar 9.0 or 7.0 were measured (Fig. S3, ESI†). UV-vis spectra of AmB and
moiety of AmB, which is oriented towards the extracellular bpy-AmB in MeOH have three strong peaks at 406 nm, 383 nm, and
space (Fig. 1a).11 The metal complexation by the bpy moiety of 364 nm and a smaller peak at 346 nm, which are characteristic of
bpy-AmB induces a change in the molecular association state of the monomeric form.13 It is seen that in the UV-vis spectra of AmB at
bpy-AmB in lipid bilayers, thereby altering ion permeability pH 9.0 and 7.0 (Fig. S3c and d, ESI†), the three peaks of the
(Fig. 1b). The UV-vis spectrum of bpy-AmB in MeOH has a monomeric form undergo a significant decrease in intensity
broad peak arising from the bpy ligand at about 290 nm, and with a short wavelength shift of the peak located in the range of
several peaks in the region between 330 nm and 400 nm that 330–350 nm. This hypsochromic shift is attributed to the close
are derived from the conjugated heptaene chromophore interaction between the heptaene chromophore of AmB and
of AmB (Fig. S1, ESI†).13 The longest wavelength peak of depends on the distances between neighboring heptaene
bpy-AmB observed at 413 nm in 1-palmitoyl-2-oleoyl-sn- chromophores.25,28,29 A shorter distance causes a larger hypsochro-
glycero-3-phosphocholine (POPC) liposomes is red-shifted from mic shift. In particular, the absorption near 330 nm is due to ‘‘dense
its position in MeOH (406 nm) (Fig. S1, ESI†). This red-shift is aggregates’’ that have an estimated interchromophore distance of
caused by increased hydrophobicity in the vicinity of the less than 6 Å.30,31 Dense aggregates are known to be largely phase-
heptaene moiety of AmB, suggesting that bpy-AmB can bind separated from the lipid bilayer, and do not induce membrane
efficiently to the POPC liposome bilayers.24,25
permeability.25,28 Thus, AmB molecules tend to form dense aggre-
To evaluate the ion-channel activity of bpy-AmB and AmB, gates at pH 9.0 and 7.0. This may be due to a lack of interactions
Ca2+-influx assays were performed using POPC liposomes with between ergosterol and AmB in the ergosterol-free POPC membrane.
entrapped ArsenazoIII (ArsIII@Lipo).26 We selected sterol-free In the spectrum of bpy-AmB at pH 9.0 (Fig. S3a, ESI†), the peak
POPC liposomes because AmB molecules do not easily form intensity ratio was found to be nearly identical to the same ratio
channels in this medium due to a lack of interactions between measured in MeOH, indicating that bpy-AmB molecules exist in the
AmB and sterol molecules.27 The ion-channel activity was monomeric form (Fig. 4). It is believed that the bulky structure of the
examined under several conditions, to examine (i) pH depen- bpy-AmB molecule suppresses aggregation.32,33 The UV-vis spectrum
dence (pH 9.0 or 7.0) in the presence of Cu2+ ions, (ii) concen- of bpy-AmB at pH 7.0 showed a slight increase in the absorbance
tration dependence of Cu2+ ions, and (iii) metal-ion intensity below 350 nm (Fig. S3b, ESI†), suggesting co-existence of
dependence (Co2+ or Ni2+ ion). The results of Ca2+ influx assays the monomeric form with a minor ‘‘associated form’’, in which the
of bpy-AmB and AmB in the presence of Cu2+ ions at pH 9.0 or distances between neighboring heptaene chromophores is longer
7.0 are shown in Fig. 2. The ion-channel activity of bpy-AmB in than the distances between dense aggregates (Fig. 4). CD spectra of
the presence of Cu2+ ions at pH 9.0 was found to be signifi- bpy-AmB or AmB in the POPC liposome suspension at pH 9.0 or 7.0
cantly increased over that at pH 7.0, whereas AmB at both pH supporting the molecular association states predicted by the UV-vis
9.0 and 7.0 showed almost no activity. The channel activity spectra. The CD spectra of AmB at pH 9.0 and 7.0 show an
of bpy-AmB at pH 9.0 depends on the equivalence ratio of asymmetric couplet in the 300–400 nm range (Fig. S4, ESI†), which
bpy-AmB to Cu2+ ions (Fig. S2a, ESI†). The addition of a is caused by very close interactions between the heptaene moieties
stronger chelating reagent, EDTA, to the mixture of bpy-AmB of AmB.34,35 On the other hand, a weak couplet was observed in the
and ArsIII@Lipo (pH 9.0) in the presence of Cu2+ ions was CD spectra of bpy-AmB at pH 9.0 and 7.0 (Fig. 3c and d), suggesting
found to reduce Ca2+ permeability as a result of inhibition of the presence of monomers which are CD silent.34,35
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Fig. 4 Schematic representation of the changes in the molecular asso-
ciation state of bpy-AmB triggered by Cu2+ coordination.
Fig. 3 UV-vis spectra of bpy-AmB in POPC liposomes before and after
the addition of Cu2+ ions at (a) pH 9.0 and (b) pH 7.0. UV-vis spectra of
[Cu2(m-OH)2(bpy)2]2+ in 20 mM Tris/HCl buffer (pH 9.0) and
[Cu(H2O)2(bpy)]2+ in 20 mM Tris/HCl buffer (pH 7.0) are also shown in
(a) and (b), respectively. CD spectra of bpy-AmB in POPC liposomes before
and after the addition of metal ions at (c) pH 9.0 and (d) pH 7.0.
with the spectrum of [Cu(H2O)2(bpy)]2+ in 20 mM Tris/HCl
buffer at pH 7.0 (Fig. 3b). A slight decrease in the peak
intensities at 413 nm and 386 nm, and a slight increase in
the absorbance intensity below 365 nm indicate a change in the
Fig. 3a and b show the UV-vis spectra of bpy-AmB in the molecular association state of bpy-AmB (Fig. 3b). The aggrega-
POPC liposome before and after the addition of Cu2+ ions at pH tion level of bpy-AmB, as estimated by the intensity ratio at
9.0 and pH 7.0 ([bpy-AmB] = [Cu2+] = 10 mM). Immediately after 330 nm (dense aggregates) and 413 nm (monomeric form) at
the addition of Cu2+ ions at pH 9.0, (i) the three peaks at pH 7.0 is greater than at pH 9.0 (Fig. 3). The CD spectrum of
413 nm, 388 nm, and 367 nm (monomeric form) were found to bpy-AmB in the POPC liposome after the addition of Cu2+ ions
be reduced in intensity significantly, and (ii) the absorbance at pH 7.0 generates an asymmetric couplet in the 300–400 nm
below 350 nm (associated form) was found to be relatively range derived from aggregates (Fig. 3d). This spectrum is quite
increased (Fig. 3a). The absorption near 290 nm is derived from different from that of bpy-AmB in the POPC liposome after the
the p–p* band of the bpy moiety, which is shifted to a longer addition of Cu2+ ions at pH 9.0. In addition, a shift of the three
wavelength. Since the spectral change of the p–p* band is peaks from the monomeric form to shorter wavelengths was
consistent with the spectrum of [Cu2(m-OH)2(bpy)2]2+ in observed (Fig. S7, ESI†), indicating the coexistence of bpy-AmB
20 mM Tris/HCl buffer at pH 9.0 (Fig. 3a), it appears that a in the membrane and in the water phase.25 Thus, the formation
dinuclear Cu2(m-OH)2(bpy-AmB)2 complex is formed. The addi- of the Cu(H2O)2(bpy-AmB) complex at pH 7.0 induces aggrega-
tion of EDTA to bpy-AmB in the associated form at pH 9.0 leads tion and transfer of bpy-AmB into the water phase (Fig. 4).
to rapid conversion to the original monomeric form in the
The reported crystal structure of [Cu2(bpy)2(H2O)(OH)2
membrane due to dissociation of Cu2+ ions from the bpy site (SO4)]4H2O has a hydroxo-bridged planar structure (Fig. S8, ESI†).37
(Fig. S5, ESI†). The 2nd addition of Cu2+ ions induces associa- The distances between C2 and C19 and between C9 and C12 of
tion of bpy-AmB. These results indicate that rapid coordination [Cu2(bpy)2(H2O)(OH)2(SO4)]4H2O are 7.78 Å and 8.02 Å, respectively
of Cu2+ to the bpy moiety of bpy-AmB at pH 9.0 induces the (Fig. S8, ESI†). Based on this coordination structure, it is possible
formation of the dinuclear Cu2(m-OH)2(bpy-AmB)2 complex, that Cu2(m-OH)2(bpy-AmB)2 dimers have a parallel (head-to-head)
resulting in conversion from the monomeric form to the orientation, and their intra-chromophore distance is about 8 Å.
associated form in the channel assembly (Fig. 4). The CD Several groups have reported that a head-to-head dimerization
spectrum of bpy-AmB in POPC liposomes measured after the process of AmB molecules may be an early step in channel
addition of Cu2+ ions at pH 9.0 is similar to the reported spectra formation and the reported intra-chromophore distance in the
of AmB in ergosterol-containing liposomes with membrane- channel assembly has been estimated as greater than 8 Å based on
permeability activity (Fig. 3c).34,36 This indicates the formation simulations.11,38–41 Matsumori and Murata et al. have reported on
of the channel assembly. Time course UV-vis spectra of several AmB covalent dimers and described their channel
bpy-AmB after the addition of Cu2+ ions show that the aggrega- activity.42,43 The aminoalkyl-linked AmB dimer channels described
tion level of bpy-AmB estimated by the intensity ratio at 330 nm herein have higher channel activity than the channel assembly
(dense aggregates) and 413 nm (monomeric form) is gradually formed by AmB monomers. These results indicate that the
increased over 60 min (Fig. S6, ESI†).
At pH 7.0, after the addition of Cu2+ ions, the bpy-AmB the channel, resulting in higher channel activity (Fig. 2).
spectrum indicates that the absorption of the p–p* band of the
The coordination structure of the Cu–bpy complex differs
Cu2(m-OH)2(bpy-AmB)2 complex at pH 9.0 is responsible for forming
bpy moiety shifts from 306 nm to 320 nm (Fig. 3b). It appears greatly between pH 9.0 and pH 7.0, but the main species of Co-
that a mononuclear Cu(H2O)2(bpy-AmB) complex is formed bpy or Ni-bpy complexes at both pH 9.0 and 7.0 are [M(bpy)2]
because the spectral change of the p–p* band is consistent and [M(bpy)] according to the speciation diagram for the 1 : 1
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M : bpy solution (M = Co2+ or Ni2+).21,22 The ion-channel activity
of bpy-AmB in the presence of Co2+ or Ni2+ ions exhibits lower
permeability than Cu2+ ions at pH 9.0 (Fig. S2c, ESI†). The
activities of these complexes were found to be nearly identical
at pH 9.0 and pH 7.0 (Fig. S2c, ESI†). Fig. S9 (ESI†) shows the
bpy-AmB spectrum changes in the POPC liposome at pH
9.0 and 7.0 after the addition of Co2+or Ni2+ ions. From the
comparison with the reported coefficient and absorption wave-
length of [M(bpy)n] (Table S1, ESI†),21,22 it appears that the
M(bpy-AmB) complex and the M(bpy-AmB)2 complex (M = Co2+
or Ni2+) are formed at both pH 9.0 and 7.0 (Fig. S10, ESI†).
These complexes lead to changes in the molecular association
state of bpy-AmB, resulting in higher aggregation levels
(estimated by the intensity ratio at 330 nm and 413 nm) than
generated by the Cu2+ ion (Fig. 3a and b and Fig. S9, ESI†). In
addition, the CD spectra of bpy-AmB in the POPC liposome
after the addition of metal ions at pH 9.0 and 7.0 suggest that
the intensity of the negative peaks in the range of 360–420 nm
tends to increase as channel activity decreases caused by higher
aggregation level (Fig. 3c and d, ESI†). The reported calculated
structure of [Ni(bpy)2]2+ and the crystal structure of [CoCl2
(bpy)2]3H2O show that the two bpy molecules are not on the
same plane and the distance between the bpy molecules is relatively
short.23 Based on this coordination structure, Ni(bpy-AmB)2 and
Co(bpy-AmB)2 complexes are not suitable for forming the parallel
dimers which are required for channel formation. As a result, it
appears that bpy-AmB in the presence of Co2+ or Ni2+ ions exhibits
low channel activities with no pH dependency.
In summary, we succeeded in providing pH-dependent ion
permeability control to a membrane using Cu2+ coordination to
the bpy moiety of bpy-AmB as the control mechanism. We
propose that a dinuclear Cu2(m-OH)2(bpy-AmB)2 complex at pH
9.0 provides parallel orientation of two bpy-AmB molecules
with a distance between chromophores of about 8 Å, which is
suitable for formation of an ion channel. This molecular
association process triggered by metal coordination differs
from the original AmB process which requires intermolecular
hydrogen bonding and van der Waals interactions between
AmB and ergosterol molecules. We believe that our approach
will lead to modification of a variety of natural channel mole-
cules and construction of stimulus-responsive channels.
This work was supported by a Grant-in-Aid for Scientific Research
on Innovative Areas ‘‘Chemistry for Multimolecular Crowding
Biosystems’’ (JSPS KAKENHI Grant No. 20H04718) to T. K., and
‘‘Coordination Asymmetry’’ (JSPS KAKENHI Grant No. 16H06519)
to M. O.
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