Synthesis of a new acetate bridged Cu(ii) building block generated 1D polymer and studies on structural, magnetic, antibacterial and anticancer properties

Article abstract of DOI:10.1039/C8NJ04937H

A new [Cu₃(Py)₆(μ-CH₃COO)₄(I₃)₂]_n (1) 1D polymer has been obtained from the mixture of Cu(NO₃)₂·3H₂O, Mn(CH₃COO)₂·4H₂O and solid I₂ in CH₃COOH/pyridine (py). The asymmetric unit 1 has the formula {[Cu_0.75(OAc)₁(pyridine)_1.5]·(I₃)_0.5}_n with Z = 2 and it has two Cu atoms, Cu1 on a mirror plane and Cu2 at a site with crystallographically imposed 2/m symmetry where the two acetate groups lie on a mirror plane; one pyridine ring in a general position is bonded to Cu1, while the other pyridine ring lies about a twofold axis and is bonded to Cu2. All C₅H₅N groups are involved in π-π stacking interactions with those on neighboring Cu₃ molecules to give a 1D polymeric supramolecular network resembling a metal-organic framework (MOF) with periodic voids resulting from a repeating unit consisting of [Cu₃]_n. Magnetic susceptibility studies in the 5.0-300 K temperature range in a 0.1 T (333 Hz) direct current (dc) magnetic field revealed the presence of weak antiferromagnetic intra-Cu₃ exchange couplings. The ground state spin (S) value calculated for 1 is S = 1/2. Alternating current magnetic susceptibility studies showed that the single-molecule magnet (SMM) behavior characteristic of 1 has been lost. The cluster 1 showed antimicrobial activity on different bacteria viz. Gram positive bacteria (Bacillus cereus MTCC1272, Staphylococcus epidermidis MTCC 3086 and Enterococcus faecalis MCC 2041(T)) and Gram negative bacteria (Salmonella enterica var Typhimurium MTCC 98 and E. coli MTCC 723). The highest significant growth inhibition zone (28.0 ± 1.34 mm) for the organisms was observed in E. faecalis MCC 2041(T) in the presence of 1 which was further confirmed by time kill assay and time kill endpoints activity. Cluster 1 was also found to induce apoptotic cell damage via generation of reactive oxygen species (ROS) when studied in human cervical cancer cells (HeLa) and human breast adenocarcinoma cells (MCF7), showing IC₅₀ values 18.54 ± 0.09 μM and 19.21 ± 0.15 μM, respectively.

Full text of DOI:10.1039/C8NJ04937H

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Synthesis of a new acetate bridged Cu(II) building
block generated 1D polymer and studies on
structural, magnetic, antibacterial and anticancer
properties†
Cite this:DOI: 10.1039/c8nj04937h
c
Sayantan Pathak,a Mithun K. Ghosh,b Manab Mandal,c Vivekananda Mandal,
ab
Arnab Bhattacharyya *d and Tanmay K. Ghorai
*
A new [Cu3(Py)6(m-CH3COO)4(I3)2]n (1) 1D polymer has been obtained from the mixture of Cu(NO3)2ꢀ
3H2O, Mn(CH3COO)2ꢀ4H2O and solid I2 in CH3COOH/pyridine (py). The asymmetric unit 1 has the
formula {[Cu0.75(OAc)1(pyridine)1.5]ꢀ(I3)0.5}n with Z = 2 and it has two Cu atoms, Cu1 on a mirror plane
and Cu2 at a site with crystallographically imposed 2/m symmetry where the two acetate groups lie on
a mirror plane; one pyridine ring in a general position is bonded to Cu1, while the other pyridine ring lies
about a twofold axis and is bonded to Cu2. All C5H5N groups are involved in p–p stacking interactions
with those on neighboring Cu3 molecules to give a 1D polymeric supramolecular network resembling a
metal–organic framework (MOF) with periodic voids resulting from a repeating unit consisting of [Cu3]n.
Magnetic susceptibility studies in the 5.0–300 K temperature range in a 0.1 T (333 Hz) direct current (dc)
magnetic field revealed the presence of weak antiferromagnetic intra-Cu3 exchange couplings. The
ground state spin (S) value calculated for 1 is S = 1/2. Alternating current magnetic susceptibility studies
showed that the single-molecule magnet (SMM) behavior characteristic of 1 has been lost. The cluster 1
showed antimicrobial activity on different bacteria viz. Gram positive bacteria (Bacillus cereus MTCC1272,
Staphylococcus epidermidis MTCC 3086 and Enterococcus faecalis MCC 2041(T)) and Gram negative
bacteria (Salmonella enterica var Typhimurium MTCC 98 and E. coli MTCC 723). The highest significant
growth inhibition zone (28.0 ꢁ 1.34 mm) for the organisms was observed in E. faecalis MCC 2041(T) in the
presence of 1 which was further confirmed by time kill assay and time kill endpoints activity. Cluster 1 was
also found to induce apoptotic cell damage via generation of reactive oxygen species (ROS) when studied
in human cervical cancer cells (HeLa) and human breast adenocarcinoma cells (MCF7), showing IC50
values 18.54 ꢁ 0.09 mM and 19.21 ꢁ 0.15 mM, respectively.
Received 28th September 2018,
Accepted 12th December 2018
DOI: 10.1039/c8nj04937h
rsc.li/njc
for the numerous applications they possess in various research
areas comprising chemistry,1 physics,2 biology,3 nanotechnology,4
Introduction
The design and synthesis of high nuclearity 3d transition metal materials science5 etc. In terms of the cluster chemistry, copper
clusters still continues to attract immense interest not only is unequivocally one of the most extensively studied first
because of the fascinating architectural point of view but also row transition elements, and over the past three decades,
researchers across the world have put forward immense efforts
to achieve high nuclearity copper clusters alongside exploring
their interesting magnetic properties. A. K. Powell et al. have
contributed significantly to this subject area and developed
a Department of Chemistry, University of GourBanga, Mokdumpur, Malda,
W.B.–732103, India
b Department of Chemistry, Indira Gandhi National Tribal University,
Cu27, Cu36 and Cu44 cage like clusters using o-vanillin-oxime and
Amarkantak, M. P.–484887, India. E-mail: tanmay.ghorai@igntu.ac.in,
nitrilopropionic acid based chelating ligands.6 These clusters
tanmayghorai66@gmail.com
c Department of Botany, University of GourBanga, Mokdumpur, Malda,
exhibited compelling structural properties and showed tempera-
ture dependent complex magnetic behaviour due to the presence
of nonzero spin ground state and low lying excited states. R. G.
Raptis and co-workers have reported [{cis-CuII(m-OH)(m-pz)}n]
polymerization isomers [where n = 6, 8, 9, 12 and 14 and with
a pyrazolato (pz) group] and showed the potential application of
W.B.–732103, India
d Department of Inorganic & Physical Chemistry, Indian Institute of Science,
Bangalore–560012, India. E-mail: arnab.bhattacharyya1@gmail.com
† Electronic supplementary information (ESI) available: Fig. SI1–SI4. CCDC1517062(1).
For ESI and crystallographic data in CIF or other electronic format see DOI:
10.1039/c8nj04937h
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these metallacycles in anion encapsulation.7 Similarly S. Saha X-ray crystal structure of cluster 1 to explore its interesting
et al. have recently documented a copper(II)-azide 1D polymer of topological features. The significance of using manganous
general formula [Cu4(N3)8(en)2]n [en = ethelenediamine] showing acetate as acetate ion source in the synthesis of cluster 1 has
antiferromagnetic interactions.8 The origin of the intriguing been put forth. The magnetic properties of the acetate bridged
magnetic behavior of polynuclear copper clusters may be attri- copper cluster 1 are also investigated to find out the potential
buted to the presence of a large number of unpaired electrons application of this kind of novel coordination polymers (CP) as
giving rise to ground state spin (S) and significant negative promising magnetic material.23 To examine its application in
anisotropy (D) or zero field splitting (ZFS) values.9 These unique the subject area of bioinorganic chemistry, extensive studies on
features make them suitable candidates for visualizing biological both antimicrobial and anticancer activities have been carried
storage10 and in spintronics11 at the molecular level and also as out giving promising results.
quantum bits in quantum computation.12
However, the usefulness of copper clusters is not limited to
the domain of chemistry only. They are very much relevant in
Results and discussion
biology too as many of the naturally occurring enzymes and
proteins contain copper in their active site. Prof. E. Solomon
Different combinations of reagent and solvent ratios were
explored to synthesize 1. Finally, a reaction of Cu(NO3)2ꢀ3H2O,
et al. in their recent review article have highlighted different
Mn(CH3COO)2ꢀ4H2O and solid I2 in 2 : 1 : 1 ratio in CH3COOH/
types of biologically significant copper centers.13 Hemocyanin
pyridine (10/20, v/v) afforded a dark brownish-green solution
and tyrosinase are examples of binuclear copper containing
enzymes where Cu centers are coupled, whereas in dopamine
from which 1 was subsequently isolated in 55% yield. The
chemical reaction is given in eqn (1).
b-monooxygenase (DbM) decoupled binuclear Cu centers can
be seen.14 Similarly, trinuclear copper site is present in the
CH3COOH=C5H5N
nCuðNO3Þ2 þ MnðCH3COOÞ2 þ 3I2
ƒƒƒƒƒƒƒƒƒƒ!
particulate methane monooxygenase (pMMO) enzyme extracted
Â
Ã
CH3ðC5H5NÞ6ðm-O2CCH3Þ4ðI3Þ2 þ Mn3þ þ nNO3ꢂ þ nHþ
from Methylococcus capsulatus (Bath).15 Fet3p is another
multicopper-containing glycoprotein with four copper centers
that localizes in the yeast plasma membrane and catalyzes the
oxidation of Fe(II) to Fe(III).16 Interestingly, copper can exert both
cytoprotective and cytotoxic behavior. Cellular thiols like
n
(1)
Mn2+ + I2" Mn3+ + I3
(2)
ꢂ
glutathione can reduce Cu(II) to Cu(I), thus generating radicals From eqn (1) it is evident that the final product 1 is devoid of any
which can further initiate a Fenton type reaction to produce manganese ion although a heteronuclear Cu–Mn cluster could
different kinds of reactive oxygen species (ROS) like hydroxyl have also been formed. Interestingly, in the absence of Mn-acetate
and superoxide radicals.17 Thus, elevated levels of copper can or by replacing Mn-acetate with other acetate ion sources like
produce oxidative stress in living cells. This redox activity and ROS Na-acetate while keeping all other conditions constant, we could
producing ability of copper complexes can account for their not isolate cluster 1. Therefore it can be speculated that Mn-acetate
antibacterial and anticancer activities. Reports have shown that plays a significant role in the formation of cluster (1). The role of
copper can alter different three-dimensional protein structures Mn2+ as an additive to form cluster 1 might be explained by the
and activities by inappropriate binding leading to growth inhibi- redox type reaction shown in eqn (2). As depicted in eqn (2), Mn2+ is
tion and simultaneous inactivation of bacteria.18 In E. coli oxidized to Mn3+ in the presence of I2 as an oxidant. At the same
bacteria, copper can cause damage to the cellular membrane time, iodine also gets reduced to form triiodide (I3ꢂ) to provide the
integrity and to the respiratory system.19 D.S. Sigman et al. have anionic support needed for charge balance in the formation of 1
discovered that cationic copper complexes bearing the 1,10- which is further confirmed by X-ray analysis of cluster 1. To support
phenanthroline ligand can cleave DNA double strands efficiently the hypothesis, we have conducted a simple analytical experiment
in the presence of oxygen and hydrogen peroxide – a phenomenon to detect the presence of Mn2+ in the solution mixture using
known as ‘chemical nuclease’.20 This leads to the development of NaBiO3 under acidic conditions. No distinct pink colour was
copper based chemotherapeutics as an alternative of commercial observed however. We have also carried out UV-vis absorption
platinum drugs. Research groups like Reedjik et al. and Chakravarty measurements of reaction mixture and compared them with the
et al. have later reported several coordination complexes of copper spectral features of cluster 1, isolated Mn(II)-acetate and Mn(III)-
bearing a variety of nitrogen and oxygen donor chelating ligands acetate salts to further strengthen the claim [for details please see
with impressive anticancer potential.21,22
Fig. SI 1(A), ESI†]. The oxidation state of copper(II) remained
The current research thus stems from our interest to develop unchanged under reaction conditions, which also furnishes
copper containing polynuclear cluster compounds to explore an indirect but strong evidence of participation of Mn(II) in the
their application in the interface of chemistry and biology. From redox process. The unstable nature of manganese in the reaction
a chemical mixture of copper nitrate taken in acetic acid/ medium may also hindered the formation of Cu–Mn heteronuclear
pyridine in the presence of solid iodine and manganous acetate, cluster resulting in an acetate bridge between two copper atoms
we have been able to isolate a copper containing 1D coordination to produce the isolated 1D Cu polymer with different bonding
polymer of unique formula [Cu3(Py)6(m-CH3COO)4(I3)2]n (1). fashions around metal centers (one is syn, syn, anti, m3 and the
Herein, we report the detailed synthetic procedure along with other is syn, syn, anti, m as discussed later).
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monoclinic space group C2/m with the molecules lying on
crystallographic inversion centers. The asymmetric unit of 1 is
of the formula {[Cu0.75(OAc)1(pyridine)1.5]ꢀ(I3)0.5}n with Z = 2. It
has two Cu atoms, Cu1 on a mirror plane and Cu2 at a site with
crystallographically imposed 2/m symmetry where the two acetate
groups lie on a mirror plane; one pyridine ring in a general
position is bonded to Cu1, while the other pyridꢂine ring lies about
a twofold axis and is bonded to Cu2. The I3 moiety has the
central iodine atom on a twofold axis (shown in Fig. 1(B)) and it
stabilizes the cationic complex to form the final 1D polymer of
formula [Cu3(Py)6(m-CH3COO)4(I3)2]n. The different binding modes
of Cu3(m-O2CMe)2 are presented in Fig. 1(C). The Cu atoms are six-
coordinated with Cu–O bonds in the 1.97–2.25 Å range. CuII
oxidation states and O2ꢂ protonation levels were again confirmed
by BVS calculations presented in Table 3.24 All CuII are nearly
octahedral and exhibit clear JT axial elongation of two trans bonds
and as expected, the JT axes avoid CuII(m-O) bonds. The bond
angles between the bridging pair O1–Cu1–O4, O3–Cu2–O2,
Cu1–O3–Cu2, C9–O1–Cu1 and C9–O2–Cu2 are found to be
172(2), 90.15(19), 109.93(5), 118.4(4) and 163.1(5), respectively.
The Cu1ꢀꢀ ꢀCu10 and Cu1ꢀꢀꢀCu2 bond distances are 3.428 and
3.814 Å, respectively, and interaction of Cu1ꢀꢀꢀCu1 is stronger
than that of the Cu1ꢀꢀꢀCu2 in cluster 1. The vacant coordination
site of the Cu metals in the molecule undergoes polymerization in
one direction and exists as a stable 1D polymeric chain which is
represented as [Cu3(Py)6(m-CH3COO)4(I3)2]n [Fig. 2(A)]. All C5H5N
groups are involved in p–p stacking interactions with those
on neighboring Cu3 molecules to give a 1D polymeric supra-
molecular network resembling a metal–organic framework (MOF)
with periodic voids resulting from a repeating unit comprising
[Cu3]n. The distance between two pyridine moieties or two
stacking layers in unit cell of 1 is found to be 3.83 Å [Fig. 2(B)].
Fig. 1 (A) Crystal structure of centrosymmetric 1. Color codes: CuII green,
O red, N blue, C gray, I violet, and H atoms have been eliminated for clarity.
The ellipsoids are drawn with 50% probability. Primed atoms are related by
symmetry ꢂx + 1, y, ꢂz. (B) Asymmetric unit of cluster 1. Color codes: CuII
green, O red, N blue, C gray, I violet, and H atoms have been eliminated for
clarity. The ellipsoids are drawn with 50% probability. (C) CH3CO2ꢂ binding
modes in cluster 1; syn, syn, anti, m for the asymmetric unit and syn, syn,
anti, m3 for the centrosymmetric unit.
X-ray crystallographic studies
The partially labelled structure of a 3D view of cluster 1 is presented
in Fig. 1(A); crystallographic data and selected inter-atomic dis-
tances and angles are listed in Tables 1 and 2, and ORTEP diagram
of 1 is provided in Fig. SI 2, ESI.† Cluster 1 crystallizes in the
Table 1 Crystallographic data for cluster 1
Parameters
Formula
1
C38H42Cu3I6N6O8
1662.79
Formula weight(g molꢂ1
)
Crystal system, space group
Monoclinic, C2/m
100
14.504 (4), 24.027 (6), 10.129 (3)
90
133.170 (2)
2574.2 (11)
Temperature (K)
a, b, c (Å)
a & g (1)
b (1)
V (Å3)
Z
2
Radiation type
Mo Ka
4.88
m (mmꢂ1
)
Crystal size (mm)
Data collection diffractometer
0.20 ꢃ 0.18 ꢃ 0.16
Bruker D8 Venture Duo Photon100 CMOS
Absorption correction
Tmin, Tmax
No. of measured, independent and observed [I 4 2s(I)] reflections
Multi-scan absorption correction
0.391, 0.458
19 903, 3338, 2353
0.063
Rint
(sin y/l)max (Åꢂ1
)
0.671
Refinement
R[F2 4 2s(F2)], wR(F2), S
No. of reflections
0.046, 0.159, 1.06
3338
No. of parameters
H-atom treatment
157
H-atom parameters constrained
0.87, ꢂ2.56
r
max, rmin(e Åꢂ3
)
Computer programs: Bruker APEX3, Bruker SAINT, SHELXL2014/7 (Sheldrick, 2014).
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Table 2 Selected bond distances (Å) and bond angles (1) for cluster 1
Atom
Bond length (Å) Atom
Bond angle (1)
I2–I1/I10
Cu1–O1
Cu1–O4
2.9236(7)
1.973(5)
1.989(5)
I1–I2–I10
O1–Cu1–O4
177.41(2)
172.0(2)
92.14(12)
87.92(12)
175.7(2)
180.0
90.0
180.0
90.15(19)
89.85(19)
O1–Cu1–N1/N10
O4–Cu1–N1/N10
N1–Cu1–N10
O3–Cu2–O30
O3–Cu2–N2/N20
N2–Cu2–N20
O3–Cu2–O2
Cu1–N1/N10 2.062(4)
Cu2–O3/O30 2.112 (5)
Cu2–O2/O20 2.246 (5)
Cu2–N2/N20 2.244(6)
O30–Cu2–O20
N2/N20–Cu2–O2/O20 90.0
O2–Cu2–O20
Cu1–O3–Cu2
C11–O4–Cu1
C9–O1–Cu1
C9–O2–Cu2
C11–O3–Cu2
C6/C60–N2–Cu2
C1–N1–Cu1
C5–N1–Cu1
180.0
109.93(5)
104.1(4)
118.4(4)
163.1(5)
171.2(5)
120.7(3)
123.4(4)
119.3(3)
Symmetry codes: primed atoms are related by symmetry ꢂx + 1, y, ꢂz
Table 3 Bond valence sumsb for cluster 1a
Atom
Cu(II)
Cu(I)
O2ꢂ
Cu1
Cu2
O1
2:033
1.73
1.19
ꢂꢂꢂꢂꢂ
1.41
ꢂ ꢂꢂ
1.89
ꢂ ꢂꢂ
O4
1.87
ꢂ ꢂꢂ
a
The oxidation state of a particular atom is the nearest integer to the
b
underlined value. The underlined value is the closest to the charge for
Fig. 2 (A) 1D polymeric structure of cluster 1. Color codes: CuII green,
O red, N blue, C gray, and H and I atoms have been eliminated for clarity.
(B) p–p stacking interactions of 1. Color codes: CuII green, O red, N blue,
C gray, and other groups have been eliminated for clarity.
which it was calculated.
Thermal and cyclic voltammetric studies
Thermal properties of coordination polymer 1 were evaluated by
thermogravimetric and differential thermal analysis under the
The cyclic voltammogram of 1 is presented in Fig. 3(B). In
the figure, one reduction hump can be seen which means one
N2 atmosphere from 50 to 600 1C at a heating rate of 10 1C minꢂ1
.
The TGA curve is presented in Fig. 3(A) and the TGA curve can be electron change is observed and copper is present in 2+ oxida-
divided mainly into two parts corresponding to the exothermic tion state in the complex. The upper portion of this voltammo-
peaks at 185.4 and 263.5 1C (DTA curve). From the TGA curve gram supports the reduction reaction of Cu2++ e - Cu+ and
it is worth noting that the structure of coordination polymer 1 potential value is ꢂ1.25 V, whereas the lower portion of the
is stable up to 125 1C and after 125 1C it begins to collapse. voltammogram supports the oxidation reaction of Cu+ - Cu2+ + e
From the TGA curve it was observed that at about 127–225 1C and the potential value is +1.0 V and it predicts the system
temperature range there is a drastic loss in the percentage of is Cu2+/Cu+ (E0 = ꢂ0.15 V).25 The electronic spectrum of 1 is
weight (from 9.20 mg to about 5.8 mg, i.e. almost 36.9% weight illustrated in Fig. SI 1(B), ESI.†
loss) which may be due to the fact that at about 1271–225 1C
temperature range, the complex loses its polymeric structure and
Magnetic studies
it decomposes because triiodide ion is present in the molecule
Direct current magnetic susceptibility study. Solid-state,
and on heating iodine vaporizes, so the molecule loses its variable-temperature magnetic susceptibility (wM) data were
identity. From the second part of the TGA curve it is very much collected on vacuum-dried microcrystalline sample of 1 in the
clear that as the temperature increases from 230 to 285 1C, there 1.5–300 K range in a 0.1 T (333 Hz and amplitude in 3 Oe) dc
is more loss in the weight of the molecule (from 5.8 mg to magnetic field. For 1, in wMT almost no change with decreasing
2.6 mg, i.e. 55.17% weight loss) which clearly indicates the T from 2.36 cm3 K molꢂ1 at 300 K to 2.34 cm3 K molꢂ1 at 20 K
elimination of all the ligands from the molecule and after has been seen and then a steep decrease has been observed to
300 1C the weight remains almost constant. So, from the thermal 1.59 cm3 K molꢂ1 at 3.0 K [Fig. 4(A)].
behavior of the molecule we can clearly say that the molecule is
very much thermodynamically stable up to B125 1C.
The value of wMT at 25 K is slightly less than the spin-only
(g = 2) value of 2.35 cm3 K molꢂ1 for CuII non-interacting atoms,
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Fig. 3 TGA curve (A) and cyclic voltammogram (B) of cluster 1.
Fig. 4 (A) Top – wMT vs. T plot for 1 in a 333 Hz and amplitude in 3 Oe dc
field. The solid line is the fit of the data using the 3-ꢂJ1model shown in the
figure. (B) Bottom –temperature dependence of wM versus T curves.
indicating the presence of weak antiferromagnetic intra-
molecular exchange interactions.8 The plot appears to be heading
towards 1.6 at 0 K, indicating an overall ground state of (S = 1/2) for
the system. 1/wM versus T plot [Fig. 4(B)] gives a straight line along
the zero point which indicates the paramagnetic nature of cluster 1,
and the value of Curie constant (C) is 2.387 cm3 K molꢂ1 and y = 0
was fitted according to Curie–Weiss law.26 The temperature depen-
dent magnetization studies (from 2 to 300 K) carried out on cluster
1 at 100 Oe in zero field cooled (ZFC) and field cooled (FC)
condition are shown in Fig. SI 3, ESI.†
zone of inhibition 22.5 ꢁ 1.05 mm. From this study it can be
inferred that the synthesized cluster has antibacterial potenti-
ality comparable to the standard antibiotic.
Minimum inhibitory concentration (MIC), minimum bacter-
icidal concentration (MBC) and effect on cellular integrity. The
MIC of the test sample was in the range of 10.00–1.25 mg mLꢂ1
as shown in Table 4, while the MBC value was in the range of
10.00–2.5 mg mLꢂ1 as shown in Table 5. It was observed that
the strains S. epidermidis MTCC 3086, E. faecalis MCC 2041(T)
and S. enterica var Typhimurium were the most resistant to the
Biological studies
Antimicrobial efficacy of cluster 1. Antimicrobial efficacy of parental compound than the other strains while all these strains
the test sample was determined against a number of human showed sensitivity to all the doses (i.e. up to 1.25 mg mLꢂ1
)
pathogenic bacteria. It significantly inhibited the growth of of the synthesized compound. Therefore, it can be inferred
the organisms, viz. B. cereus MTCC 1272, S. epidermidis MTCC that the synthesized compound is more potent than parental
3086, S. enterica var Typhimurium MTCC 98, E. faecalis MCC compound due to its antimicrobial efficacy. The amount of
2041(T) and E. coli MTCC 723 with 18.5 ꢁ 0.913, 21.0 ꢁ 1.14, LDH released after treatment of the synthesized active com-
21.5 ꢁ 1.064, 28.0 ꢁ 1.34 and 15.0 ꢁ 0.61 mm inhibition zone pound is shown in Fig. 5. The elevated LDH content in treated
diameters, respectively. The values are comparable to the samples indicates that the compound has the cellulolytic mode
standard antibiotic streptomycin (200 mg mLꢂ1) with an average of action.
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Table 4 MIC of parental and synthesized compound 1
B. cereus
S. epidermidis
E. faecalis
E. coli
S. typhimurium
MIC concentration Parental
Parental
compound Cluster 1
Parental
compound Cluster1
Parental
compound Cluster 1
Parental
compound Cluster 1
grade (mg mLꢂ1
)
compound Cluster 1
20
10
05
2.5
1.25
0.625
16.5 ꢁ 2.64 21.5 ꢁ 2.64 15.5 ꢁ 2.64 21.0 ꢁ 2.64 15.5 ꢁ 2.64 15.8 ꢁ 2.64 18.5 ꢁ 2.4 20.5 ꢁ 2.64 15.3 ꢁ 2.64 15.7 ꢁ 2.64
14.0 ꢁ 2.64 18.0 ꢁ 2.64 13.0 ꢁ 2.64 20.0 ꢁ 2.64 14.0 ꢁ 2.64 15.0 ꢁ 2.64 16.0 ꢁ 2.61 18.0 ꢁ 2.64 14.0 ꢁ 2.64 15.0 ꢁ 2.64
12.5 ꢁ 2.64 16 ꢁ 2.64 —
16.5 ꢁ 2.64 —
13.0 ꢁ 2.64 —
11.5 ꢁ 2.64 —
12.5 ꢁ 2.64 10.5 ꢁ 1.64 15 ꢁ 2.64 —
17.5 ꢁ 2.64
15.0 ꢁ 2.64
13.0 ꢁ 2.64
—
—
—
—
13 ꢁ 2.64 —
12 ꢁ 2.64 —
10 ꢁ 2.64 —
15.5 ꢁ 2.64 —
13.0 ꢁ 2.64 —
13 ꢁ 2.54 —
11 ꢁ 2.34 —
9 ꢁ 2.74 —
—
—
—
—
Here, figures in the parental and synthetic compound 1 are the diameters of inhibition zones (mm).
Table 5 MBC of the synthesized compound 1. Here, the ‘+’ symbol
was performed in human cervical carcinoma (HeLa) and
human breast adenocarcinoma (MCF-7) cells. In the presence
of cellular NADPH dependent oxidoreductase enzymes, in
viable cells 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium
bromide or MTT gets reduced to insoluble formazan and
provides a method to determine the half maximal inhibitory
concentration (IC50) of cytotoxic substances. Compound 1 was
found to be moderately cytotoxic in nature and exhibited IC50
values of 18.54 ꢁ 0.09 mM and 19.21 ꢁ 0.15 mM, respectively, in
HeLa and MCF-7 cell lines (Fig. 7). From the results, it can be
postulated that the presence of a redox active metal centre
along with the contribution from pyridine moieties is primarily
responsible for anticancer activity.
Annexin V-FITC/PI assay for cellular apoptosis. To investi-
gate the nature of cell death in the presence of 1, Annexin
V-FITC/PI assay was performed. Annexin V is a protein which
binds to phosphatidylserine of phospholipid bilayer. In healthy
cells, phosphatidylserine resides in the inner leaflet of lipid
bilayer, but at the early stage of apoptosis, phospholipid
asymmetry is reverted resulting in a flipping in cell membrane
with a simultaneous release of phosphatidylserine to the outer
leaflet. This specific morphological change can then be mon-
itored by flow cytometric analysis using Annexin V coupled with
a green fluorescent marker FITC. In this assay, red emissive and
cell membrane impermeable dye propidium iodide (PI) is also
required as a second marker which can intercalate with nuclear
DNA. Thus, cells undergoing early apoptosis where cell
membrane remained intact were quantified by FITC marker
and necrotic cells were stained only by PI, while the double
positive population showed cells undergoing late apoptosis
where cell membrane was compromised. In this study, the
ability of copper cluster 1 to activate cellular death machinery
was evaluated. HeLa cells were incubated with 1 (conc. = 20 mM)
for 4 h in the dark, and after 20 h post-incubation, the assay was
performed using flow cytometry. The plots are shown in Fig. 8
and cluster 1 was found to induce early and late apoptosis in
35.92% and 33.57% cells, respectively, while 25.35% of cells
remained healthy. The necrotic cell population was found to be
insignificant in the study, further proving the usefulness of
cluster 1 as a potential antitumour agent.
indicates no visible colony counts and ‘ꢂ’ indicates the presence of visible
colony growth
MIC concentration B.
S.
E.
E.
S. enterica var
grade (mg mLꢂ1
)
cereus epidermidis faecalis coli Typhimurium
20
10
05
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
2.5
1.25
MBC MBC
MBC
—
MBC MBC
—
—
—
—
Time kill assay and time kill endpoints. In the time kill assay
and time kill endpoints studies it was observed that a dose of
10 mg mLꢂ1 of the test sample had a complete bactericidal activity
within 8 h of treatment against both E. faecalis MCC 2041(T) and
S. enterica var Typhimurium MTCC 98, while it had a time kill
endpoint of 10 h at a dose of 10 mg mLꢂ1 against both strains
tested (Fig. 6). From this key experiment, it can be concluded that
the synthesized compound is a very promising antimicrobial agent
that is useful against some highly pathogenic human bacteria, like
E. faecalis MCC 2041(T) and S. enterica var Typhimurium MTCC98
and similar pathogenic microbes.
In vitro cellular studies
Cell viability assay (MTT assay). To determine the in vitro
anti-proliferative and cytotoxic potential of cluster 1, MTT assay
DCFDA assay for ROS generation. Overproduction of ROS
(reactive oxygen species) inside cells often plays a key role in
inducing cell death via apoptosis. As cluster 1 was found
to induce apoptosis, we further investigated its potential to
Fig. 5 LDH assay of cluster 1.
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Fig. 6 Time kill assay of the synthesized compound 1 on human pathogenic bacteria. E. faecalis MCC 2041(T(A)) and S. enterica var Typhimurium
MTCC98(B).
dye which in the presence of cellular esterases cleaves initially,
followed by simultaneous oxidation by reactive oxygen species
present to produce DCF (dichlorofluorescein) inside cells. The
cell membrane impermeable and fluorescent nature of DCF
(lem = 525 nm) can then be used to quantify the level of
intracellular ROS by flow cytometric analysis. HeLa cells were
treated with 1 (conc. = 20 mM) for 4 h in the dark followed by
FACS analysis. Histogram revealed a significant positive shift of
DCF fluorescence intensity in the presence of cluster 1, while
untreated cells and control (1% DMSO) could only produce
insignificant amount of ROS under similar conditions (Fig. 9).
The presence of redox active CuII centers in the cluster, which
are vulnerable to glutathione (GSH) attack inside cancer cells,
can account for this ROS generation. Thus, the results of
Annexin V-FITC/PI assay and DCFDA assay could lead to a
Fig. 7 MTT assay in HeLa (red) and MCF-7 cells (blue) treated with cluster
primary conclusion that the overproduction of ROS inside
cancer cells in the presence of cluster 1 activates the apoptotic
pathways leading to cell death. The results also strengthen
the claim of anticancer potential of the corresponding 1D
polymeric copper cluster.
1 for 4 h.
generate ROS using DCFDA assay. 2,7-Dichlorofuorescein dia-
cetate (DCFDA) is a non-fluorescent, cell membrane permeable
Fig. 8 Annexin V-FITC/PI coupled flow cytometric analysis showing cluster 1 (20 mM) induced apoptosis.
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and the mixture was then stirred for another 45 minutes.
Finally the resulting solution was filtered and the filtrate was
kept for slow evaporation. After 10 days, greenish-black high
X-ray quality crystals (1) were obtained and were washed with
Et2O (2–3 times) and dried under vacuum.
Yield: 55% (0.78 g). Anal. calcd for cluster 1 (C38H42Cu3I6N6O8):
C, 27.45; H, 2.55; N, 5.05%. Found: C, 27.31; H, 2.57; N, 5.13%.
Selected IR data in cmꢂ1: 689 (s), 754 (m), 1218 (m), 1387 (s), 1445 (s),
1559 (s), 1644 (b) [s = strong, m = medium, b = broad]. Detailed
discussion of IR spectrum (Fig. SI 4) of 1 is provided in ESI.†
Fig. 9 Flow cytometry to detect ROS using DCFDA assay for cluster 1
(20 mM): Colour codes: cells alone, black; cells + DCFDA, blue; cells +
DCFDA + DMSO, green; and cells + DCFDA + 1, red. The greater shift in
fluorescence intensity implies a higher amount of ROS.
X-ray crystallography
Single crystal X-ray data were collected for complex 1 at 100 K on
a Bruker SMART APEX CCD diffractometer using the SMART/
SAINT software.27 Intensity data were collected using graphite-
monochromatized Mo Ka radiation (0.71073 Å) at 100 K. The
structures were solved by direct methods using the SHELXL-
201428 program incorporated into WinGX.29 Empirical absorp-
tion corrections were applied with SADABS.30 All non-hydrogen
atoms were refined with anisotropic displacement coefficients.
The hydrogen atoms bonded to carbon were included in geo-
metric positions and given thermal parameters equivalent to
1.2 times those of the atom to which they were attached.
An initial search for reciprocal space revealed a monoclinic
cell with space group C2/m for 1 and was confirmed by the
subsequent solution and refinement of the structures. In the
final cycle of refinement, 3338 reflections (of which 2358 are
observed with I 4 2s(I)) were used to refine 392 parameters and
the resulting R1, wR2 and S (goodness of fit) were 4.60%,
15.92% and 1.057, respectively. Refinement was carried out
by minimizing the wR2 function using F2 rather than F values.
R1 is calculated to provide a reference to the conventional
R value but its function is not minimized. Unit cell data and
structure refinement details are listed in Table 1.
Conclusions
In conclusion, we have successfully synthesized a new acetate
bridged Cu(II) building block generated 1D polymer of formula
[Cu3(Py)6(m-CH3COO)4(I3)2]n(1) which is thermodynamically
stable up to 125 1C. Asymmetric unit of 1 contains {[Cu0.75(OAc)1-
(pyridine)1.5]ꢀ(I3)0.5}n, and the presence of vacant coordination
sites on the copper atoms in the molecule allows polymerization
in one direction to produce supramolecular coordination poly-
mers (CP). Magnetic study reveals that the molecule is para-
magnetic with S = 1/2 and weak antiferromagnetic interactions
between the Cu(II) ions exist in the molecule. Antimicrobial
studies with the cluster 1 show that it can significantly inhibit
the growth of different bacteria with the maximum effect against
E. faecalis MCC 2041(T) (28.0 ꢁ 1.34 mm), and it can act as a
promising biocide that could be useful against several highly
pathogenic human bacteria. The MIC and MBC values of the test
sample are in the range of 10 mg mLꢂ1 to 1.25 mg mLꢂ1 and
10.00 to 2.5 mg mLꢂ1, respectively. On the other hand, cluster 1
is also found to be cytotoxic when studied in HeLa and MCF-7
cancer cells (IC50 B18–19 mM) and can initiate cell death
machinery via inducing apoptosis through overproduction
of reactive oxygen species (ROS) which makes this novel Cu
polymer a potential anticancer agent. Thus, the synthesized
copper based 1D polymer can significantly contribute to the
research area of dual action copper based therapeutics.
Physical measurements
Infrared spectrum was recorded in the solid state (KBr pellets) on
a PerkinElmer FTIR spectrometer in the 400–4000 cmꢂ1 range.
Elemental analyses (C, H, and N) and X-ray crystallography were
performed by the Central facilities of IISER Pune. Variable-
temperature direct current (dc) and alternating current (ac) magnetic
susceptibility data were collected on vacuum dried solids using a
Quantum Design MPMS-XL SQUID magnetometer equipped with a
7 T magnet and operating in the 1.8–300 K range recorded from
UGC-DAE Indore. Samples were embedded in solid eicosane in a gel
capsule to prevent torquing. Diamagnetic and background contribu-
tions from the eicosane and gel capsule were measured as a blank
and subtracted from susceptibility. Magnetization versus field and
temperature data was fitted using the program MAGNET.31 Pascal’s
constants32 were used to estimate the diamagnetic correction, which
was subtracted from experimental susceptibility to give molar para-
Experimental section
Materials and methods
All chemicals were of reagent grade and were used without
further purification and were purchased from Sigma-Aldrich,
India. Solvents were used as received.
Synthesis of [Cu3(Py)6(l-CH3COO)4(I3)2]n(1)
A
mixture of Cu(NO3)2ꢀ3H2O (1.41 g,
6
mmol) and magnetic susceptibility (wM). Cyclic voltammogram of the compound
Mn(CH3COO)2ꢀ4H2O (0.735 g, 3 mmol) was dissolved in a was recorded using SYNSIL (Model No. PH660) and electronic
mixture of CH3COOH/pyridine (10/20, v/v) in a round bottom spectrum of the compound was analyzed using UV-vis spectro-
flask. Then solid I2 (0.762 g, 3 mmol) was added to the reaction photometer PerkinElmer LAMBDA 35 from Department of Chem-
mixture. Immediately the solution became dark brownish-green istry, West Bengal State University, Barasat, Kolkata-700126.
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Assay for antimicrobial activity by the agar diffusion method
NADH (L mmolꢂ1 cmꢂ1), d = light path length (1 cm),
v = volume of enzyme sample (0.02 mL).
The antibacterial activity was measured by the agar well diffu-
sion method33 against Gram positive bacteria (Bacillus cereus
MTCC 1272, Staphylococcus epidermidis MTCC 3086 and E. faecalis
MCC 2041(T)) and Gram negative bacteria (Salmonella enterica var
Typhimurium MTCC 98). Briefly, the assay was done by using
overnight grown culture of each strain overlaid on Mueller–Hinton
agar plates (comprising meat infusion from 300.0 g Lꢂ1, casein
acid hydrolysate 17.50, starch 1.5 g Lꢂ1, agar 17.0 g Lꢂ1, final pH
(at 25 1C) 7.3 ꢁ 0.1) using a spreader. Agar cups were cut using
sterile cork-borer (7 mm diameter) and 30 mL of the test samples,
viz. synthesized and parental compounds (20 mg mLꢂ1 and
100 mg mLꢂ1, respectively) were loaded into the well and
incubated for 24 h at 37 1C and observed for zone of growth
inhibition. The assay was compared with the respective solvent
as negative control and the standard antibiotic streptomycin
(200 mg mLꢂ1) as positive control.
Determining time kill assay and time kill endpoints
Bactericidal kinetic assay was performed in Muller–Hinton agar
plates. Test samples, i.e. synthesized compound, at different
concentrations greater than MBC were used. The actively grown
bacterial strains (log phase growth) were treated with the test
sample and incubated at 37 1C for 24 h. At different time points
of incubation (i.e. 30 min, 240 min and 480 min), 100 mL of the
treated culture was taken out and spread on nutrient agar
plates in triplicate trials. The plates were incubated at 37 1C
for 24 h and observed for viable colony development. The viable
counts were calculated as CFU per mL, and time kill curve was
plotted with time against the viable count. The time required to
produce zero cell count is defined as the time kill endpoint with
100% efficiency. A decrease in CFU over time indicates the
bactericidal nature of the antimicrobial compounds.
Determination of MIC, MBC and effect on cellular integrity.
The strains sensitive to test samples were used for minimum
inhibitory concentration (MIC) determination following the
protocol of Mandal et al., 2016.34 For this purpose, the following
concentration grades of the samples, viz. parental and synthe-
sized, were prepared by serial two-fold dilution using methanol
as the diluents: 10, 05, 2.5, 1.25, and 0.625 mg mLꢂ1. MIC is the
concentration of antimicrobial compound where no zone of
inhibition is observed, while the minimum bactericidal concen-
tration (MBC) is the concentration where no viable cells are
found. The bacterial lawn and agar cups were prepared following
the method described above. 20 mL of the test samples of
different concentrations was loaded into the well and incubated
for 24 h at 37 1C and observed for zone of growth inhibition. The
concentration at which no zone of growth inhibition was found
was treated as MIC. For the determination of MBC, only the
synthesized compound with greater MIC values were used
against the actively grown bacterial strains (log phase growth)
and incubated for 1 h. The treated culture was then plated on a
nutrient agar plate at a dilution of 10ꢂ1 to 10ꢂ3 in triplicate and
incubated for 24 h at 37 1C and observed for any viable colony
formation. The concentration at which no viable cells were
observed was determined as MBC. The effect of the antimicro-
bial compound on cellular integrity was assessed by the amount
of lactate dehydrogenase content in the treated and untreated
samples, following the protocol of Mandal et al. 2016 using the
bacterial strains, viz. E. faecalis MCC 2041(T) and Salmonella
enterica var Typhimurium MTCC 98. The amount of LDH
released was calculated using the following formula:
In vitro cellular studies
Cell culture. HeLa (human cervical carcinoma) and MCF-7
(human breast adenocarcinoma) cells were cultured in
DMEM supplemented with 10% FBS, 100 IU mLꢂ1 of penicillin,
100 mg mLꢂ1 of streptomycin and 2.0 mM of Glutamax at 37 1C
in a humidified incubator maintaining a constant level of
5% CO2. The adherent cultures were grown as monolayer and
were passaged once in 4–5 days by trypsinizing with 0.25%
trypsin–EDTA.
Cell viability (MTT) assay. Approximately 1 ꢃ 104 HeLa and
MCF-7 cells were plated in each well of a 96-well culture plate
using DMEM supplemented with 10% fetal bovine serum (FBS)
and cultured overnight. MTT (3-(4,5-dimethylthiazol-2-yl)-2,5
diphenyl tetrazolium bromide) assay was then performed using
standard protocols previously reported.35 Cluster 1 was then
dissolved in 10% FBS-DMEM containing 1% DMSO and was
added to the cells at varying concentrations following the
method of successive dilution in a triplicate manner keeping
a constant volume of 250 mL in each well. Incubation was then
allowed to continue for 4 h in the dark and post-incubation was
then allowed for 20 h for the plates using DMEM containing
10% FBS. 25 mL of MTT dissolved in PBS (conc. = 4.0 mg mLꢂ1
)
was then added to each plate and kept for 4 h in the dark. The
culture media was removed and 100 mL of HPLC grade DMSO
was added to each well to dissolve the formazan thus formed.
The intensity of formazan was then measured by recording its
absorbance at 540 nm using an ELISA microplate reader
(BioRad, Hercules, CA, USA). Cytotoxicity of each sample was
found as a percentage ratio of the absorbance of the treated cells
over the untreated controls. The IC50 values were calculated
following a nonlinear regression analysis method by plotting
‘‘log(inhibitor) vs. normalised response (variable slope)’’ using
GraphPad Prism version 6.36 The errors were calculated by
taking the average of the deviation obtained by repeating the
Calculation
DA
min
6:3 ꢀ d ꢀ v
ꢀ V ꢀ D
¼ 1 U mLꢂ1
where, DA/min = the change in absorbance at 340 nm per experiment three times.
minute, V = total volume of reaction mixture (3.17 mL),
D = enzyme dilution factor, 6.3 = mM extinction coefficient of were treated with complex 1 (20 mM) dissolved in 10% FBS-DMEM
Annexin-V/FITC-PI assay. HeLa (B4 ꢃ 105 cells per mL) cells
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and V. Marvaud, Dalton Trans., 2016, 45, 9412–9418; (e) H. Chen,
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containing 1% DMSO and kept in the dark for 4 h. The cells
were then cultured for 20 h in complete medium, harvested and
washed twice with refrigerated PBS at 4 1C. The cells were
re-suspended in 100 mL Annexin V binding buffer (100 mM
HEPES/NaOH, pH 7.4 containing 140 mM NaCl and 2.5 mM
CaCl2), stained with Annexin V-FITC and propidium iodide (PI),
and incubated for 15 min at 25 1C in the dark. Binding buffer
(400 mL) was added to the cells after incubation and analysed
immediately using flow cytometry.37
DCFDA assay for the detection of ROS. HeLa cells were
incubated with complex 1 (20 mM) for 4 h. Cells were then
harvested by trypsinization and single cell suspension of
1 ꢃ 106 cells per mL was prepared. The suspension was then
treated with 10 mM DCFDA solution in DMSO and kept in the dark
for 5 min at 25 1C. Flow cytometric analysis was then performed
for distribution of the HeLa cells stained with DCFDA to find out
the amount of intracellular ROS generated.38
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Conflicts of interest
The authors declare no conflict of interest.
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Acknowledgements
This work is fully supported by Department of Science &
Technology (SR/FT/CS-021/2010), Govt. of India, New Delhi;
Indira Gandhi National Tribal University, Amarkantak; and
University of Gour Banga, Malda, West Bengal, India. Authors
also thank West Bengal State University, Barasat, Kolkata,
IISER-Pune and UGC-DAE Indore for the cyclic voltammetric
study (CV), FTIR, single crystal crystallography and magnetic
measurements, respectively. The FACS facility from the division
of Biological Sciences, Indian Institute of Science Bangalore
(IISc), which is supported by Department of Biotechnology
(DBT), Government of India, is acknowledged.
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