Next Article in Journal
Spectroscopic Studies of Amino Acid Ionic Liquid-Supported Schiff Bases
Next Article in Special Issue
Macrocyclic Drugs and Synthetic Methodologies toward Macrocycles
Previous Article in Journal
2'-Deoxythymidine Adducts from the Anti-HIV Drug Nevirapine
Previous Article in Special Issue
Evaluation of the Interaction between Long Telomeric DNA and Macrocyclic Hexaoxazole (6OTD) Dimer of a G-quadruplex Ligand
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

A Lead (II) 3D Coordination Polymer Based on a Marine Cyclic Peptide Motif

1
Department of Chemistry, National Dong-Hwa University, Hualien 974, Taiwan
2
Department of Chemistry, National Taiwan University, Taipei 106, Taiwan
*
Author to whom correspondence should be addressed.
Molecules 2013, 18(5), 4972-4985; https://doi.org/10.3390/molecules18054972
Submission received: 26 March 2013 / Revised: 16 April 2013 / Accepted: 24 April 2013 / Published: 26 April 2013
(This article belongs to the Special Issue Macrocyclic Chemistry)

Abstract

:
The crystal structure of a naturally occurring cyclic tetrapeptide cyclo(Gly-l-Ser-l-Pro-l-Glu) [cyclo(GSPE)] was obtained. The conformation of synthesized cyclo(GSPE) fixes the coordination to lead ion in a 1:1 ratio. This cyclo(GSPE)-Pb complex was constructed as an asymmetric 3D network in the crystalline state. The polymerization of a heavy metal ion with a rigid asymmetric cyclic tetrapeptide represents the first example of a new class of macrocyclic complexes.

Graphical Abstract

1. Introduction

In the area of biomedicinal chemistry much interest has been generated in the design of metal-organic frameworks (MOFs) [1,2]. Due to their chemical variety, biocompatibility and ability to assemble spontaneously, peptides can form excellent simple nanotubes [3,4,5]. Some metal-peptide frameworks (MPFs) [6] have been reported, but very few of them have been characterized by crystallography [6,7]. The size and conformation of cyclic peptides [8,9] and their metal binding side chains provide a novel tool for construction of discrete metal-assembled supermolecules with unique chemical and physical properties. Cyclic tetrapeptides (CTPs) [10,11,12,13,14,15] also possess a definite inner nanocavity of a constrained nature and hence, generated highly entropic advantages in molecular recognition with the potential to confer chirality and biological activity on these compounds [16,17,18]. Compared with the d- and f-block metals, Pb2+ ion has a larger radius, variable coordination numbers and unique prospects for the construction of novel polymeric or multi-dimensional supramolecular networks [19,20,21,22,23,24,25]. The chemistry of lead has drawn a lot of interest for its wide applications in fields such as fuel additives, batteries, oil refining and paint manufacturing, but also in biological systems, where Pb metal has been found to interact with many amino acids, peptides and proteins: these binding preferences of Pb(II) have provided the inspiration for the design of a selective chelating therapy agent [26,27,28,29,30,31].
Cyclo(Gly-l-Ser-l-Pro-l-Glu) [cyclo(GSPE), 1] has metal binding sites on the side chains (serine hydroxyl and glutamic carboxylate group) and the carbonyl groups. It was first isolated from the Ruegeria strain of marine bacteria [32] and was found to possess moderate antibacterial activity against Bacillus subtilis. Its structure was elucidated on the basis of 1D and 2D NMR data, followed by the determination of absolute configuration [33]. However, a crystal structure has not been reported. Due to strain of the twelve member ring, binding to metal ions by carbonyls is more difficult than by side chains. Keeping in mind the combination of hydroxyl and carboxylato groups and from a study of natural CTPs-metal complexes, cyclo(GSPE) 1 was selected as a linking ligand to investigate the coordination chemistry of Pb(II) ion. Here the crystal structure of cyclo(GSPE) and {[cyclo(Gly-l-Ser-l-Pro-l-Glu)Pb(NO3)]·2H2O}n 2 are reported for the first time. Further {[cyclo(Gly-l-Ser-l-Pro-l-Glu)Pb(NO3)]·2H2O}n 2 was constructed as an asymmetric 3D network in the crystalline state. Coordination relied on the prearranged conformation of synthesized cyclo(GSPE) 1. The polymerization of a heavy metal ion with a rigid asymmetric cyclic tetrapeptide represents the first example of a new class of complexes.

2. Results and Discussion

2.1. Synthesis of cyclo(GSPE) 1 and {[cyclo(Gly-l-Ser-l-Pro-l-Glu)Pb(NO3)]·2H2O}n 2

Cyclo(GSPE) 1 was synthesized by using standard solution-phase peptide coupling protocols. Its spectral data were identical with those of natural 1 [32,33]. Crystals were prepared for the first time by slow cooling to room temperature in water. The synthesized peptide 1 was subjected to complexation with Pb(II). By heating an aqueous solution of the peptide 1 and the lead(II) salt in a 1:1 ratio, the {[cyclo(Gly-l-Ser-l-Pro-l-Glu)Pb(NO3)]·2H2O}n 2 complex was obtained. Crystals were prepared by slow cooling to room temperature and resulted in a 3D coordination polymer. Several coordination polymers of lead with a variety of synthetic organic ligands have been reported earlier [34,35,36,37,38]. The structure of macrocyclic complex 2 is the first solved marine cyclo(GSPE) 1 lead complex.

2.2. Characterization of {[cyclo(Gly-l-Ser-l-Pro-l-Glu)Pb(NO3)]·2H2O}n 2

NMR Spectra. Interaction between cyclo(GSPE) 1 with Pb2+ was first examined by 1H-NMR after reaction with Pb(NO3)2 (1.0 equiv) in water at pH 5.0 and 70 °C for 4 days. The NMR spectrum of the complex 2 showed the appearance of new multiplet (δ = 4.19–4.26) and triplet (δ = 4.76) peaks for glutamic acid and the serine α-protons in place of the doublet (δ = 4.08–4.10) and multiplet (δ = 4.81–4.85) peaks of the free peptide, respectively (Figure S3). These NMR signal changes only in the side chain protons clearly indicated their binding with Pb2+ ions outside of the cyclic peptide ring.
Mass Spectra. MALDI-TOF mass spectrometry on the reaction product with 1.0 equivalents of Pb2+ ions showed interaction with the peptide, with peaks at m/z 577.69, 595.71 and 719.69 corresponding to [M+Pb–H]+, [M+Pb+H2O–H]+ and [M+Pb+2NO3+H2O–H]+, respectively. This was further confirmed by HR-ESI mass spectrometry (Figure S4, Figure S5, Figure S6 and Figure S7). All the assignments showed good agreement between the observed and calculated isotopic distributions.
IR Spectra. The IR spectrum of macrocycle 1 showed a characteristic ν(C=O) absorption band for the –COOH group at 1,718 cm−1, which vanishes in the case of metal complex 2. For the free peptide the νas(COO) and νs(COO) stretching vibrations of the carboxylate group appear at 1,545 and 1,444 cm−1 respectively, while for the lead complex 2, the first absorption region became broad and the second was obscured by the nitrate ion absorption, which displays a quite intense band at 1,384 cm−1 (Figure S8 and Figure S9).

2.3. Crystal Structures

2.3.1. Crystal Structure of CTP 1

X-ray crystallographic studies showed a crystal structure of macrocycle 1 with a cis-trans-cis-trans (two transoid amide bonds between Gly-Ser, Pro-Glu and two cisoid amide bonds between Ser-Pro, and Glu-Gly) peptide bond, a sequence closely associated with biological activity. A summary of the crystal data and refinement results is listed in Table 1.
Table 1. Selected crystallographic data of 1 and 2.
Table 1. Selected crystallographic data of 1 and 2.
12
Empirical formulaC15H22N4O7C15H25N5O12Pb
Formula weight370.37674.59
Temperature296(2) K296(2) K
Wavelength0.710730.71073
Crystal system, space groupMonoclinic, P2(1)Monoclinic, P2(1)
Unit cell dimensions
a (Å)4.9855(7) 5.0532(3)
b (Å)17.257(3)17.7774(11)
c (Å)9.7830(14)11.8317(5)
α (°)90.0090.00
β (°)104.064(3)94.550(3)
γ (°)90.0090.00
Volume (Å3)816.4(2)1059.52(10)
Z, Calculated density (Mg/m3)2, 1.5072, 2.115
Absorption coef. (mm−1)0.1218.037
F(000)392656
Crystal size (mm)0.13 × 0.08 × 0.050.44 × 0.09 × 0.05
θ range for data collection (°)2.15-28.101.73-27.5
Limiting indices−5≤ h ≤6, −22 ≤ k ≤ 22, −12 ≤ l ≤ 12−6≤ h ≤ 6, −23 ≤ k ≤11, −14 ≤ l ≤ 15
Reflection collected/unique7693/3848 [R(int) = 0.0395]6993/3657 [R(int) = 0.0363]
Absorption correctionMulti-scanMulti-scan
Max. and min. transmission0.7456 and 0.63920.6990 and 0.1278
Refinement methodFull-matrix least-squares on F2Full-matrix least-squares on F2
Data/restraints/parameter3848/1/2373657/1/298
Goodness-of-fit on F21.0630.949
Final R indices [I > 2sigma(I)]R1 = 0.0471, wR2 = 0.1071 R1 = 0.0278, wR2 = 0.0618
R indices (all data)R1 = 0.0739, wR2 = 0.1292 R1 = 0.0317, wR2 = 0.0636
Larg. diff. peak and hole (e.Å−3)0.214 and −0.222 e.Å−31.336 and −1.127 e.Å−3
The backbone of the cyclic peptide adopts a two-fold symmetric conformation which is very common for cyclic tetrapeptides containing alternate ‘cis’ and ‘trans’ peptide units and the two side chains (glutamic and serine) are away from the ring. The glutamic residue assumes the gauche conformation to the main-chain amino group (χ1 = −54.6°). In the prolyl residue, Cα, Cβ, Cδ and N form an approximate plane with Cγ deviating from the plane by 0.56 Å towards the side of the carbonyl group. The torsion angles that define the conformation of the molecule are listed in Table 2.
Table 2. Backbone and side-chain torsion angles (°) of 1.
Table 2. Backbone and side-chain torsion angles (°) of 1.
AngleGlyl-Serl-Prol-Glu
Φ−98.2−134.5−84.355.1
ψ−13.649.7153.947.0
ω−176.072.91177.2613.45
χ1 32.15−54.65
χ2 −39.57151.99
χ3 32.21
χ4 −11.30
χ5 −13.08
The conformation of the cyclic tetrapeptide 1 is illustrated in the Figure 1 (top, left). The overall shape of the backbone is a distorted boat with the cis amide bonds at the two ends which could facilitate ion binding.
Each discrete molecule of cyclo(GSPE) 1 is strongly hydrogen bonded to a neighboring molecule through the amide N-H of glutamic acid moiety to a carboxyl O-atom of proline (dN-H···O 2.066 Å and θN-H···O 176.6°) moiety and amide N-H of serine to a carboxyl O-atom of a glycine moiety (dN-H···O 1.997 Å and θN-H···O 145.3°), to form a 1D-chain along the a-axis. An oriented CTP nanotube (yellow) is thus assembled. The structure of this nanotube is expanded into a three-dimensional network (5.4 × 2.8 Å2), which is devoid of water molecules (Figure 1, top and right).
The carboxylic acid group of glutamic acid and the hydroxyl group of serine are flanked in opposite directions and are hydrogen bonded to a neighboring 1D-chain to form an overall 3D-network. Each cyclo(GSPE) 1 molecule is surrounded by four neighboring molecules and two molecules are hydrogen bonded (between amide N-H of glycine moiety of neighboring molecule to carboxyl O-atom of glutamic acid moiety of the core molecule (dN-H···O 2.162 Å and θN-H···O 154.1°), and hydroxyl H-atom of serine from neighboring molecule to O-atom of the amide group of the glutamic acid moiety (dO-H···O 1.999 Å and θO-H···O 169.0°) of the core molecule. The remaining two neighboring molecules are linked to the core molecule through O···O interactions between the amide O-atom of the serine moiety to the O-atom of carboxylic acid group of glutamic acid (dC-O···O 2.605 Å and θC-O···O 169.1°) moiety (Figure 1, bottom).
Figure 1. Thermal ellipsoid plot of cyclo(Gly-l-Ser-l-Pro-l-Glu) 1. Color code: light gray, C; blue, N; red, O; dark gray, H.
Figure 1. Thermal ellipsoid plot of cyclo(Gly-l-Ser-l-Pro-l-Glu) 1. Color code: light gray, C; blue, N; red, O; dark gray, H.
Molecules 18 04972 g001

2.3.2. Crystal Structure of Complex 2

A single-crystal X-ray diffraction study reveals that complex 2 is a 3D-coordinated polymer, crystallized in the monoclinic system with P 2(1) space group. Crystallographic data of 2 are listed in Table 1. As shown in Figure 2, the asymmetric unit of 2 is composed of one Pb(II) center, one deprotonated cyclo(GSPE) ligand, one nitrate molecule and two lattice water molecules.
Figure 2. Crystal structure of 2. Perspective view showing binding mode of cyclo(Gly-l-Ser-l-Pro-l-Glu) 1 to Pb(II) ion. Only hydroxyl O-H and amide N-H group hydrogen atoms are shown.
Figure 2. Crystal structure of 2. Perspective view showing binding mode of cyclo(Gly-l-Ser-l-Pro-l-Glu) 1 to Pb(II) ion. Only hydroxyl O-H and amide N-H group hydrogen atoms are shown.
Molecules 18 04972 g002
The Pb(II) center is in a seven coordination environment (Figure 2) with five oxygen atoms [O1(proline carbonyl), O3(glutamic carbonyl), O5(serine hydroxyl) O6 and O7(glutamic carboxylate)] of three distinct cyclo(GSPE) 1 ligands and two μ1,1- oxygen atoms (O8) of nitrate molecules from two EO bridges (joining it to a neighboring Pb atom). The torsion angles that define the conformation of the complex 2 are listed in Table 3.
Table 3. Selected bond lengths (Å) and angles (°) of 2.
Table 3. Selected bond lengths (Å) and angles (°) of 2.
Pb-O12.489(4)Pb-O32.833(5)
Pb-O52.475(5)Pb-O62.463(6)
Pb-O72.644(6)Pb-O82.571(5)
Pb-O82.755(5)
O6-Pb-O573.42(19)O6-Pb-O180.12(17)
O5-Pb-O169.53(16)O6-Pb-O871.78(19)
O5-Pb-O8135.80(18)O1-Pb-O878.36(16)
O6-Pb-O750.55(17)O5-Pb-O778.39(19)
O1-Pb-O7127.25(17)O8-Pb-O799.17(19)
O6-Pb-O8145.03(18)O5-Pb-O875.99(18)
O1-Pb-O8104.61(16)O8-Pb-O8143.1(3)
O7-Pb-O8106.82(18)O6-Pb-O3129.40(16)
O5-Pb-O3143.21(16)O1-Pb-O3134.98(17)
O8-Pb-O380.86(17)O7-Pb-O395.17(17)
O8-Pb-O371.33(15)
The geometry around the Pb center appears holodirected [39]. The bidentate carboxylate oxygen atoms (O6 and O7) provided the asymmetric chelation (Pb-O 2.463(6) and 2.643 (6) Å). The Pb-O bond distances (Table 3) are in the range of 2.463(6)–2.833(5) Å and the O-Pb-O bond angles vary from 50.55(17)–145.03(18)° and are comparable to those reported earlier for lead-oxygen donor complexes [24,40,41,42]. 1D linear chain around the Pb center is formed via carbonyl and hydroxyl oxygen atoms of two distinct cyclo(GSPE) ligands along [001] direction (Figure 3).
Figure 3. View of the 1D linear chain of 2 along [001] direction. Color code: green, Pb; gray, C; blue, N; red, O.
Figure 3. View of the 1D linear chain of 2 along [001] direction. Color code: green, Pb; gray, C; blue, N; red, O.
Molecules 18 04972 g003
Three molecules of cyclo(GSPE) 1 binds with three Pb(II) ions to form one cyclic ring and the same unit repeats along b-axis to form a 2D layer structure (Figure 4a,b). When viewed along the [100] direction, these sheets are further cross-linked by NO3 molecules giving rise to a three-dimensional structure. The size and the shape of the CTP nanotube remains unchanged (Figure 5).
Figure 4. (a) Perspective view of 2D-network along a-axis. Color code: yellow, Pb; cyan, C; blue, N; red, O. (b) 2D sheet of 2 in the bc plane. Color code: green, Pb; gray, C; blue, N; red, O.
Figure 4. (a) Perspective view of 2D-network along a-axis. Color code: yellow, Pb; cyan, C; blue, N; red, O. (b) 2D sheet of 2 in the bc plane. Color code: green, Pb; gray, C; blue, N; red, O.
Molecules 18 04972 g004
Figure 5. Polyhedral view in three-dimensional structure of 2. Color code: green, Pb; gray, C; blue, N; red, O.
Figure 5. Polyhedral view in three-dimensional structure of 2. Color code: green, Pb; gray, C; blue, N; red, O.
Molecules 18 04972 g005
Two adjacent Pb(II) ions in 2 are bridged by one oxygen atom from μ1,1-bridging NO3 molecule (Figure 6) to build a dinuclear unit with a Pb···Pb distance of 5.053(0) Å. Of three coordinated nitrates to Pb(II), one nitrate faces the cavity of the cage (Figure 6, left) and the remaining two nitrate anion lie in neighboring cavities. The coordinated nitrate facing the cavity of the cage interact with one (out of two) water molecule inside cage (dO11-H11···O10 2.207 Å, θO11-H11···O10 155.7(53)°).
Figure 6. Perspective view of hydrogen bonded (between amide N-H and carbonyl O-atom) cage (left) of two layer and each cyclic layer formed by three cyclo(Gly-l-Ser-l-Pro-l-Glu) 1 molecule coordinated to three Pb(II) ions. Between two layers, nitrate anions are weakly coordinated to two Pb(II) ions of each layer (right). Out of three nitrate anion, one nitrate anion lying inside the cage is further coordinated to a water molecule and the remaining two nitrate anions lying inside two neighboring cages. For clarity, each layer is differentiated from neighboring layer by different color.
Figure 6. Perspective view of hydrogen bonded (between amide N-H and carbonyl O-atom) cage (left) of two layer and each cyclic layer formed by three cyclo(Gly-l-Ser-l-Pro-l-Glu) 1 molecule coordinated to three Pb(II) ions. Between two layers, nitrate anions are weakly coordinated to two Pb(II) ions of each layer (right). Out of three nitrate anion, one nitrate anion lying inside the cage is further coordinated to a water molecule and the remaining two nitrate anions lying inside two neighboring cages. For clarity, each layer is differentiated from neighboring layer by different color.
Molecules 18 04972 g006

2.4. Discussion

There is no report on the solid state structure of a natural (12-membered) cyclic tetrapeptide with a metal ion. The molecular structure of the cyclo(GSPE)-Pb complex 2 is unique as all the complexes reported to date are with higher cyclic peptides or β-cyclic tetrapeptides and are sandwich complexes [43,44,45]. Structure 2 showed that conformation of 1 remains cis-trans-cis-trans and only the side chains and ring carbonyls are pointing towards the Pb metal for binding and, hence, represent an example of a metal complex bound with both a cyclic skeleton and functional groups in side chains. Unlike linear peptides, the retention of conformation of 1 is attributed to the highly constrained nature of CTPs. The rigidity of cyclopeptide backbones ensures the formation of nanotubes [46]. The inability to adjust their conformation makes CTP-metal complexes rare. However, once it formed, the resulting CTP-metal complexes 2 will preserve the nanotubes.

3. Experimental

3.1. Materials and Physical Measurements

All reagents were commercially available (Aldrich, Saint Louis, MO, USA or Merck, Darmstadt, Germany) and used as supplied. Solvents were dried by standard procedures. The NMR spectra were recorded on a Bruker DRX 400 (1H at 400.13 MHz, 13C at 100.03 MHz) spectrometer (Bruker Daltonik, Bremen, Germany). MALDI TOF was performed on a Bruker Autoflex MALDI-TOF mass spectrometer (Bruker Daltonik, Bremen, Germany). High-resolution electrospray ionization mass spectrometry (ESI-MS) was performed on a Shimadzu-LCMS-IT-TOF mass spectrometer (Shimadzu, Kyoto, Japan). Elemental analysis for C, H, N was performed on VarioEL-III elementar analyzer (Elementar, Hanau, Germany). Infrared spectra were recorded on a PerkinElmer Spectrum one FT-IR spectrometer (PerkinElmer, Shelton, CT, USA) using KBr pellets (4,000–400 cm−1).

3.2. Sythesis

Cyclo(Gly-l-Ser-l-Pro-l-Glu) (1). Linear peptide Boc-GS(OBn)PE(OBn)2 was synthesized by using standard solution-phase peptide coupling protocols starting from Fmoc-L-proline. Subsequently, regioselective enzymatic hydrolysis of the α-benzyl ester on glutamate was achieved [47]. The linear precursor was then activated with pentafluorophenol and cyclized with pyridine to form dibenzyl protected CTP [48]. Deprotection of the benzyl group finished the synthesis of 1. The overall yield was 19%. IR (KBr, cm−1): 3459 ν(NH), 3236 ν(OH vs –CH2OH), 3066 ν(CH), 2990 2961 ν(CH2), 1718 ν(C=O vs -COOH), 1663 1646 1615 ν(C=O vs amide), 1545 νas(COO), 1444 νs(COO). 1H-NMR: (D2O) δ 1.60–1.89 (m, 3H), 1.93–2.17 (m, 3H), 2.20–2.38 (m, 2H), 3.36–3.54 (m, 2H), 3.57–3.65 (m, 1H), 3.77–3.82 (m, 1H), 3.86–3.97 (m, 2H), 4.08–4.10 (d, 1H, J = 8 Hz), 4.35–4.37 (d, 1H, J = 8 Hz), 4.80–4.82 (m, 1H). MALDI-TOF: m/z 371.35 [M+H]+, ESI-MS: [M−H] calculated m/z 369.1488, obtained m/z 369.1426.
{[cyclo(Gly-l-Ser-l-Pro-l-Glu)Pb(NO3)]·2H2O}n (2). Pb(NO3)2 (4.5 mg, 13.5 μmol) was dissolved in water (1 mL). cyclo(GSPE) 1 (5.0 mg, 13.5 μmol) was dissolved in water (1 mL) and added to the metal solution. The pH of solution was adjuted to 5 with diluted HNO3 solution. The reaction mixture was stirred at RT for 10 minutes and then at 70 °C for 4 days. Crystals suitable for X-ray diffraction were obtained from saturated solution by slow cooling. Anal. Calc. for C15H25N5O12Pb (674.6): C 26.70, H 3.73, N 10.38, O 28.46. Found: C 26.23, H 2.94, N 10.64, O 28.17. IR (KBr, cm−1): 3433, ν(NH); 1645, ν(C=O vs amide); 1384, ν(NO3). 1H-NMR: (D2O) 1.86–1.99 (m, 3H); 2.04–2.31 (m, 3H); 2.35–2.53 (m, 2H); 3.45–3.55 (m, 1H); 3.59 (s, 1H); 3.65–3.71 (m, 1H); 3.73–3.81 (m, 1H); 3.82 (s, 1H); 3.87–4.00 (m, 1H); 4.19–4.26 (m, 1H); 4.38–4.45 (m, 1H); 4.76 (t, 1H, J = 5.88 Hz). MALDI-TOF: m/z 577.69 [M+Pb–H]+ , 595.71 [M+Pb+H2O–H]+ and 719.69 [M+Pb+2NO3+H2O–H]+. ESI-MS: [M+Pb–H]+ calculated m/z 577.1177, obtained m/z 577.1183; [M+Pb+NO3–H]+ calculated m/z 639.1055, obtained m/z 639.1049; [M+Pb+2NO3–H]+ calculated m/z 701.0933, obtained m/z 701.0973; [M+Pb+2NO3+2H2O+H]+ calculated m/z 739.1301, obtained m/z 739.2925.

3.3. X-ray Crystallography

Colorless prism-like crystals of 1 and rod-like crystals of 2 were obtained by slow solvent evaporation at room temperature, respectively. Crystals suitable for X-ray diffraction analysis were selected with size of 0.13 × 0.08 × 0.05 mm for 1 and 0.44 × 0.09 × 0.05 mm for 2. Crystals were mounted on a glass fiber and used for data collection. For both compounds 1 and 2 diffraction data were preliminarily collected with a Bruker APEX-II CCD diffractometer using graphite monochromated MoKα radiation (λ = 0.71073 Å). Absorption corrections for the area detector were performed with the program SADABS. Structures were solved by direct methods and were refined against the least-squares methods on F2 with the SHELXL-97 package, incorporated in SHELXTL/PC V5. Anisotropic thermal factors were used only for all non-hydrogen atoms.
CCDC 831318 and 831319 contains the supplementary crystallographic data for this paper. These data can be obtained free of charge via www.ccdc.cam.ac.uk/conts/retrieving.html (or from the CCDC, 12 Union Road, Cambridge CB2 1EZ, UK; fax: +44 1223 336033; e-mail: [email protected]).

4. Conclusions

We have developed the synthesis of a CTP cyclo(GSPE) 1. The synthetic building blocks were coupled through hydroxyl, carboxylate and two amide bonds to lead ion and thus created water-soluble, coordination polymers (tris-CTPs) with well-defined three-dimensional structures. This is the first report of a naturally occurring CTP as the host for metal complexation. The CTP retains its conformation through the binding process with metals. The unique crystal structure of this rigid molecule suggests the formation of a designated complex with nanotube properties.

Supplementary Materials

Supplementary materials can be accessed at: https://www.mdpi.com/1420-3049/18/5/4972/s1.

Acknowledgments

The present work is supported by a Grant from the National Science Council of Taiwan.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Horcajada, P.; Gref, R.; Baati, T.; Allan, P.K.; Maurin, G.; Couvreur, P.; Ferey, G.; Morris, R.E.; Serre, C. Metalorganic frameworks in biomedicine. Chem. Rev. 2012, 112, 1232–1268. [Google Scholar]
  2. Keskin, S.; Kızılel, S. Biomedical applications of metal organic frameworks. Ind. Eng. Chem. Res. 2011, 50, 1799–1812. [Google Scholar] [CrossRef]
  3. Ulijn, R.V.; Smith, A.M. Designing peptide based nanomaterials. Chem. Soc. Rev. 2008, 37, 664–675. [Google Scholar] [CrossRef]
  4. Scanlon, S.; Aggeli, A. Self-assembling peptide nanotubes. Nanotoday 2008, 3, 22–30. [Google Scholar] [CrossRef]
  5. Valery, C.; Franck Artzner, F.; Paternostre, M. Peptide nanotubes: Molecular organisations, self-assembly mechanisms andapplications. Soft Matter 2011, 7, 9583–9594. [Google Scholar]
  6. Lee, H.-Y.; Kampf, J.W.; Park, K.S.; Marsh, E.N.G. Covalent metal-peptide framework compounds that extend in one and two dimensions. Cryst. Growth Des. 2008, 8, 296–303. [Google Scholar] [CrossRef]
  7. Mantion, A.; Massuger, L.; Rabu, P.; Palivan, C.; McCusker, L.B.; Taubert, A. Design, Synthesis, Biological evaluation, and structural characterization of potent histone deacetylase inhibitors based on cyclic α/β- tetrapeptide architectures. J. Am. Chem. Soc. 2008, 130, 2517–2526. [Google Scholar] [CrossRef]
  8. Ghadiri, M.R.; Granja, J.R.; Milligan, R.A.; McRee, D.E.; Khazanovich, N. Self-assembling organic nanotubes based on a cyclic peptide architecture. Nature 1993, 366, 324–327. [Google Scholar] [CrossRef]
  9. Ghadiri, M.R.; Granja, J.R.; Buehler, L.K. Artificial transmembrane ion channels from self-assembling peptide nanotubes. Nature 1994, 369, 301–304. [Google Scholar]
  10. Yang, L.; Tan, R.-X.; Wang, Q.; Huang, W.-Y.; Yin, Y.-X. Antifungal cyclopeptides from halobacillus litoralis YS3106 of marine origin. Tetrahedron Lett. 2002, 43, 6545–6548. [Google Scholar] [CrossRef]
  11. Mitova, M.; Tommonaro, G.; De Rosa, S. A novel cyclopeptide from a bacterium associated with the marine sponge Ircinia muscarum. Z. Naturforsch 2003, 58c, 740–745. [Google Scholar]
  12. Shin, J.; Seo, Y.; Lee, H.-S.; Rho, J.-R.; Mo, S.J. A new cyclic peptide from a marine-derived bacterium of the Genus Nocardiopsis. J. Nat. Proc. 2003, 66, 883–884. [Google Scholar] [CrossRef]
  13. Rungprom, W.; Siwu, E.R.O.; Lambert, L.K.; Dechsakulwatana, C.; Barden, M.C.; Kokpol, U.; Blanchfield, J.T.; Kita, M.; Garson, M.J. Cyclic tetrapeptides from marine bacteria associated with the seaweed diginea sp. and the sponge halisarca ectofibrosa. Tetrahedron 2008, 64, 3147–3152. [Google Scholar] [CrossRef]
  14. Gu, W.; Cueto, M.; Jensen, P.R.; Fenical, W.; Silverman, R.B. Microsporins A and B: New histone deacetylase inhibitors from the marine-derived fungus microsporum cf. gypseum and the solid-phase synthesis of microsporin A. Tetrahedron 2007, 63, 6535–6541. [Google Scholar]
  15. Thomas, D.; Walter, G.; Hans, B. Natural cyclopeptaibiotics and related cyclic tetrapeptides: Structural diversity and future prospects. Chem. Biodiv. 2008, 5, 693–706. [Google Scholar]
  16. Nakao, Y.; Yoshida, S.; Matsunaga, S.; Shindoh, N.; Terada, Y.; Nagai, K.; Yamashita, J.K.; Ganesan, A.; Van Soes, R.W.M.; Fusetani, N. Azumamides A–E: Histone deacetylase inhibitory cyclic tetrapeptides from the marine sponge Mycale izuensis. Angew. Chem. Int. Ed. 2006, 45, 7553–7557. [Google Scholar] [CrossRef]
  17. Montero, A.; Beierle, J.M.; Olsen, C.A.; Ghadiri, M.R. Design, Synthesis, Biological evaluation, and structural characterization of potent histone deacetylase inhibitors based on cyclic alpha/beta-tetrapeptide architectures. J. Am. Chem. Soc. 2009, 131, 3033–3041. [Google Scholar] [CrossRef]
  18. Kawagishi, H.; Somoto, A.; Kuranari, J.; Kimura, A.; Chiba, S. A novel cyclotetrapeptide produced by Lactobacillus helveticus as a tyrosinase inhibitor. Tetrahedron Lett. 1993, 34, 3439–3440. [Google Scholar] [CrossRef]
  19. Lacouture, F.; Francois, M.; Didierjean, C.; Rivera, J.P.; Rocca, E.; Steinmetz, J. Anhydrous lead(II) heptanoate. Acta Crystallogra C 2001, 57, 530–531. [Google Scholar] [CrossRef]
  20. Ferrari, R.; Bernes, S.; Barbarin, C.R.D.; Mendoza-Diaz, G.; Gasque, L. Interaction between glyglu and Ca2+, Pb2+, Cd2+ and Zn2+ in solid state and aqueous solution.: Crystal structures of poly[aqua-1,2-κ-O-di[lead(gly-gluH)]bis(perchlorate)] and poly[bisglycylglutamic-cadmium(II) tetrahydrate]. Inorg. Chim. Acta 2002, 339, 193–201. [Google Scholar] [CrossRef]
  21. Lei, Z.-H.; Li, X.; Dong, L.-N. Synthesis, Structure, and luminescence of a novel lead(II) coordination polymer with 1,2- phenylenediacetic acid. Inorg. Chem. Commun. 2010, 13, 1383–1386. [Google Scholar] [CrossRef]
  22. Zhang, X.; Cheng, J.-K.; Yin, P.-X.; Yao, Y.-G. Synthesis and characterization of a novel coordination polymer with isolated tetranuclear lead(II) clusters as building subunits. J. Mol. Struc. 2011, 990, 1–5. [Google Scholar] [CrossRef]
  23. Chen, S.-C.; Zhang, Z.-H.; Zhou, Y.-S.; Zhou, W.-Y.; Li, Y.-Z.; He, M.-Y.; Chen, Q.; Du, M. Alkali-metal-templated assemblies of new 3D lead(II)tetrachloroterephthalate coordination frameworks. Cryst. Growth Des. 2011, 11, 4190–4197. [Google Scholar] [CrossRef]
  24. Peedikakkal, A.M.P.; Vittal, J.J. Structural transformations of Pb(II)-trans-1,2-bis(4'-pyridyl)ethane coordination polymers in solution. Cryst. Growth Des. 2011, 11, 4697–4703. [Google Scholar] [CrossRef]
  25. Zhao, Y.-H.; Xu, H.-B.; Shao, K.-Z.; Xing, Y.; Su, Z.-M.; Ma, J.-F. Syntheses, Characterization, and luminescent properties of three 3D lead-organic frameworks with 1D Channels. Cryst. Growth Des. 2007, 7, 513–520. [Google Scholar] [CrossRef]
  26. Farrer, B.T.; Pecoraro, V.L. Heavy-metal complexation by de novo peptide design. Curr. Opin. Drug Discov. Dev. 2002, 5, 937–943. [Google Scholar]
  27. Claudio, E.S.; Godwin, H.A.; Magyar, J.S. Fundamental coordination chemistry, environmental chemistry, and biochemistry of lead(II). Progr. Inorg. Chem. 2003, 51, 1–144. [Google Scholar]
  28. Saxena, G.; Flora, S.J.S. Lead-induced oxidative stress and hematological alterations and their response to combined administration of calcium disodium EDTA with a thiol chelator in rats. J. Biochem. Mol. Toxicol. 2004, 18, 221–233. [Google Scholar] [CrossRef]
  29. Magyar, J.S.; Weng, T.C.; Stern, C.M.; Dye, D.F.; Rous, B.W.; Payne, J.C.; Bridgewater, B.M.; Mijovilovich, A.; Parkin, G.; Zaleski, J.M.; et al. Reexamination of lead(II) coordination preferences in sulfur-rich sites: implications for a critical mechanism of lead poisoning. J. Am. Chem. Soc. 2005, 127, 9495–9505. [Google Scholar] [CrossRef]
  30. Gracia, R.C.; Snodgrass, W.R. Lead toxicity and chelation therapy. Am. J. Health Syst. Pharm. 2007, 64, 45–53. [Google Scholar] [CrossRef]
  31. Chakraborty, S.; Kravitz, J.Y.; Thulstrup, P.W.; Hemmingsen, L.; DeGrado, W.F.; Pecoraro, V.L. Design of a three-helix bundle capable of binding heavy metals in a triscysteine environment. Angew. Chem. Int. Ed. 2011, 50, 2049–2053. [Google Scholar] [CrossRef]
  32. Mitova, M.; Popov, S.; De Rosa, S. Cyclic peptides from a Ruegeria strain of bacteria associated with the sponge Suberites domuncula. J. Nat. Prod. 2004, 67, 1178–1181. [Google Scholar] [CrossRef]
  33. Lim, H.A.; Kang, C.; Chia, C.S.B. Solid-phase synthesis and NMR structural studies of the marine antibacterial cyclic tetrapeptide: cyclo[GSPE]. Int. J. Pept. Res. Ther. 2010, 16, 145–152. [Google Scholar] [CrossRef]
  34. Davidovich, R.L.; Stavila, V.; Marinin, D.V.; Voit, E.I.; Whitmire, K.H. Stereochemistry of lead(II) complexes with oxygen donor ligands. Coord. Chem. Rev. 2009, 253, 1316–1352. [Google Scholar] [CrossRef]
  35. Pan, Q.-H.; Chen, Q.; Chang, Z.; Nhao, Y.-C.; Wang, Y.-C.; He, T.-L. A 3D lead(II) coordination polymer containing helical chains with rare ecl topology. Chin. J. Inorg. Chem. 2010, 26, 2299–2302. [Google Scholar]
  36. Kong, Z.G.; Ma, X.Y.; Xu, Z.L.; Wang, X.Y. Synthesis and crystal structure of a new lead coordination polymer: [Pb(L)(1,4-ndc)]. Chin. J. Struc. Chem. 2010, 29, 1749–1752. [Google Scholar]
  37. Zhang, Y.Y.; Liu, S.X.; Du, K.K.; Xue, M.X. A 3D-diamond-like coordination network of lead(II) complex: Synthesis, Structure and luminescent property. Inorg. Chem. Commun. 2010, 13, 641–644. [Google Scholar] [CrossRef]
  38. Shaabani, B.; Mirtamizdoust, B.; Viterbo, D.; Croce, G.; Hammud, H.; Hojati-Lalemi, P.; Khandar, A.; Anorg, Z. Sonochemical synthesis of a novel nanoscale lead(II) coordination polymer: Synthesis, Crystal structure, Thermal properties, and DFT calculations of [Pb(dmp)(μ-N3)(μ-NO3)]n with the novel Pb2(μ-N3)2(μ- NO3)2 unit. Allg. Chem. 2011, 637, 713–719. [Google Scholar] [CrossRef]
  39. Shimoni-Livny, L.; Glusker, J.P.; Bock, C.W. Lone pair functionality in divalent lead compounds. Inorg. Chem. 1998, 37, 1853–1867. [Google Scholar] [CrossRef]
  40. Saunders, C.D.L.; Longobardi, L.E.; Burford, N.; Lumsden, M.D.; Zwanziger, U.W.; Chena, B.; McDonald, R. Comprehensive chemical characterization of complexes involving lead-amino acid interactions. Inorg. Chem. 2011, 50, 2799–2810. [Google Scholar] [CrossRef]
  41. Sun, J.-Y.; Wang, W.; Wang, L.; Zhang, D.-J.; Chen, Y.-L.; Ji, X.-D.; Fan, Y.; Song, T.-Y. Novel lead-organic framework based on 2,2'-bipyridine-3,3'-dicarboxylate ligand: Synthesis, structure and luminescence. J. Mol. Stru. 2011, 990, 204–208. [Google Scholar] [CrossRef]
  42. Chen, Z.; Yan, J.; Xing, H.; Zhang, Z.; Liang, F. Two lead(II) 2,4-dioxo-1,2,3,4-tetrahydropyrimidine-5-carboxylate complexes exhibiting different topologies and fluorescent properties. J. Solid State Chem. 2011, 184, 1063–1069. [Google Scholar] [CrossRef]
  43. Kartha, G.; Varughese, K.I.; Aimoto, S. Conformationof cyclo(-L-Pro-Gly-)3 and its Ca2+ and Mg2+ complexes. Proc. Natl. Acad. Sci. USA 1982, 79, 4519–4522. [Google Scholar] [CrossRef]
  44. Doi, M.; Asano, A.; Ishida, T.; Katsuya, Y.; Mezaki, Y.; Sasaki, M.; Terashima, A.; Taniguchi, T.; Hasegawa, H.; Shionod, M. Caged and clustered structures of endothelin inhibitor BQ123, cyclo(-D-Trp-D-Asp-Pro-D-Val- Leu-).Na+, forming five and six coordination bonds between sodium ions and peptides. Acta Cryst. D 2001, 57, 628–634. [Google Scholar]
  45. Okada, T.; Tanaka, K.; Shiro, M.; Shionoya, M. Heterogeneous assembly of silver (I) and calcium(II) ions accompanyinga dimer formation of cyclo(L-Ala–L-Met)3 isolation. Chem. Commum. 2005, 1484–1486. [Google Scholar]
  46. Li, L.; Zhan, H.; Duan, P.; Liao, J.; Quan, J.; Hu, Y.; Chen, Z.; Zhu, J.; Liu, M.; Wu, Y.-D.; et al. Self-assembling nanotubes consisting of rigid cyclicγ–peptides. Adv. Funct. Mater. 2012, 22, 3051–3056. [Google Scholar] [CrossRef]
  47. Miyazawa, T.; Ogura, M.; Nakajo, S.; Yamada, T. Synthesis of monoesters of N-protected α-aminocarboxylic acids via the microbial protease-catalyzed regioselective hydrolysis of their diesters. Biotechnol. Tech. 1998, 12, 431–434. [Google Scholar] [CrossRef]
  48. Cheng, C.-T.; Lo, V.; Chen, J.; Chen, W.-C.; Lin, C.-Y.; Lin, H.-C.; Yang, C.-H.; Sheh, L. Synthesis and DNA nicking studies of a novel cyclic peptide: cyclo[Lys-Trp-Lys-Ahx-]. Bioorg. Med. Chem. 2001, 9, 1493–1498. [Google Scholar] [CrossRef]
  • Sample Availability: Samples of the compounds 1 and 2 are available from the authors.

Share and Cite

MDPI and ACS Style

Chakraborty, S.; Tyagi, P.; Tai, D.-F.; Lee, G.-H.; Peng, S.-M. A Lead (II) 3D Coordination Polymer Based on a Marine Cyclic Peptide Motif. Molecules 2013, 18, 4972-4985. https://doi.org/10.3390/molecules18054972

AMA Style

Chakraborty S, Tyagi P, Tai D-F, Lee G-H, Peng S-M. A Lead (II) 3D Coordination Polymer Based on a Marine Cyclic Peptide Motif. Molecules. 2013; 18(5):4972-4985. https://doi.org/10.3390/molecules18054972

Chicago/Turabian Style

Chakraborty, Subrata, Pooja Tyagi, Dar-Fu Tai, Gene-Hsiang Lee, and Shie-Ming Peng. 2013. "A Lead (II) 3D Coordination Polymer Based on a Marine Cyclic Peptide Motif" Molecules 18, no. 5: 4972-4985. https://doi.org/10.3390/molecules18054972

Article Metrics

Back to TopTop