Synthesis, crystal structure, magnetic property and nuclease activity of a new binuclear cobat(II) complex

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Inorganic Biochemistry Journal of Inorganic Biochemistry 101 (2007) 196–202 www.elsevier.com/locate/jinorgbio

Synthesis, crystal structure, magnetic property and nuclease activity of a new binuclear cobat(II) complex Jin-Lei Tian a, Li Feng a,b, Wen Gu a, Guang-Jun Xu a, Shi-Ping Yan Dai-Zheng Liao a, Zong-Hui Jiang a, Peng Cheng a b

a,*

,

a Department of Chemistry, Nankai University, Tianjin 300071, PR China Tianjin University of Traditional Chinese Medicine, Tianjin 300193, PR China

Received 28 March 2006; received in revised form 7 August 2006; accepted 12 August 2006 Available online 30 August 2006

Abstract One new binuclear Co(II) complex of N,N,N 0 ,N 0 -tetrakis(2-benzimidazolylmethyl)-2-hydroxyl-1,3-diaminopropane (HL), [Co2L(l2Cl)](ClO4)2 Æ 3CH3CN Æ C2H5OC2H5 (1), has been synthesized and its crystal structure and magnetic properties are shown. In 1, each Co(II) atom has a distorted trigonal bipyramidal geometry with a N3OCl donor set. The central two Co(II) atoms are bridged by ˚ . Susceptibility data of 1 indicate strong intramolecular one alkoxo-O atom and one Cl atom with the Co1–Co2 separation of 3.239 A antiferromagnetic coupling of the high-spin Co(II) atoms. In this paper, the interaction with calf thymus DNA was investigated by UV absorption and fluorescent spectroscopy. Results show the complex binds to ct-DNA with a intercalative mode. The interaction between complex 1 and pBR322 DNA has also been investigated by submarine gel electrophoresis, noticeably, the complex exhibits effective DNA cleavage activity in the absence of any external agents.  2006 Published by Elsevier Inc. Keywords: Binuclear Co(II) complex; DNA cleavage; Crystal structure; Magnetic property

1. Introduction Transition metal complexes capable of cleaving DNA and RNA under physiological conditions via oxidative and hydrolytic mechanisms are of importance for their potential use as new structural probes in nucleic acids chemistry and as therapeutic agents [1]. Among these active transition metal species, the nuclearity of metal complexes is of importance and dinuclear complexes generally give higher cleavage rates provided that the ligand holds the metal centers in an appropriate geometry [2–9]. At present, there are at least 15 confirmed examples of metallohydrolases that contain and require a dinuclear metal ion site, and there is evidence that certain nucleases and ribozymes

*

Corresponding author. Tel.: +86 022 23509957; fax: +86 022 23502779/4853. E-mail address: [email protected] (S.-P. Yan). 0162-0134/$ - see front matter  2006 Published by Elsevier Inc. doi:10.1016/j.jinorgbio.2006.08.009

have two or more metal ions which are required for hydrolysis of DNA and RNA [10]. In these native enzymes, the ˚. average separation between the metal ions is about 3.5 A Currently, dinuclear and polynuclear hydroxo-, alkoxoand phenoxo-bridged complexes are of interest in chemistry and in biochemistry, some of which have been proven to be effective chemical nucleases [11–17]. For example, Karlin have discovered a dicopper complex [Cu2(PD 0 O)(H2O)2](ClO4)3 Æ 2H2O that predominantly effects DNA base (rather than ribose) oxidation on G residues in single-stranded regions of DNA [11]. Nishida reported that the binuclear iron(III) complex with HPTP does not cleave DNA in the absence of hydrogen peroxide, but the binuclear cobalt(II) complex has induced the cleavage of Form I DNA in the absence of hydrogen peroxide, because formation of Form II DNA was observed [12]. In attempt to obtain more insight into the selectivity and efficiency of DNA recognized and cleaved by different binuclear complexes, we have synthesized and characterized one

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new binuclear cobalt(II) complex [Co2L(l2-Cl)](ClO4)2 Æ 3CH3CN Æ C2H5OC2H5 (1) containing symmetric heptadentate ligand HL (HL = N,N,N 0 ,N 0 -tetrakis(2-benzimidazolylmethyl)-2-hydroxyl-1,3-diaminopropane). Some crystal structures of Fe, Ni, Cu complexes containing ligand HL are known at present [18–22], but as far as we know, no crystal structures of cobalt complexes were reported. In this paper, the interaction with calf thymus DNA was investigated by UV absorption and fluorescent spectroscopy, as well as the DNA cleavage experiments induced by 1 are also demonstrated. 2. Experimental 2.1. Materials All chemicals and reagents purchased were of reagent grade and used without further purification unless otherwise noted. Ligand HL was synthesized by the methods of the literature [20]. Calf thymus DNA, pBR322 DNA, agarose (molecular biology grade) and ethidium bromide (EB) were all purchased from the sino-American Biotechnol Biotechnology Company. Tris–HCl buffer solution was prepared using deionised, sonicated triple distilled water.

197

4.52; N, 15.71. IR (KBr, cm1): 3200–3600br, 1619m, 1595w, 1539s, 1490m, 1459s, 1443s, 1385m, 1342m, 1275s, 1220w, 1090br, 900w, 748s (w, weak; m, medium; s, strong; br, broad). 2.4. X-ray structure determination Suitable single crystals with approximate dimensions of 0.32 · 0.26 · 0.20 mm3 was used for X-ray diffraction analyses by mounting on the tip of a glass fiber in air. Data were collected on a Bruker Smart-1000 CCD diffractometer ˚ ) at 293(2) K. The structure with Mo Ka (k = 0.71073 A was solved by direct method using the program SHELXS-97 [23] and subsequent Fourier difference techniques, and refined anisotropically by fullmatrix leastsquares on F2 using SHELXL-97 [24]. All the nonhydrogen atoms were refined anisotropically and all the hydrogen atoms were located in the Fourier difference maps. Molecular graphics were drawn with the program package XP. Further crystallographic data and experimental details for structural analyses of complexes are summarized in Table 1. Crystallographic data for the structure reported in this paper have been deposited with the Cambridge Crystallographic Data Centre as supplementary publication No. CCDC-211155.

2.2. Physical measurements Elemental analyses for C, H, and N were obtained on a Perkin–Elmer analyzer model 240. Infrared spectroscopy on KBr pellets was performed on a Bruker Vector 22 FTIR spectrophotometer in the 4000–400 cm1 regions. The electronic spectra were measured on a JASCO V-570 spectrophotometer. Emission spectra were measured on a Varian Cary Eclipse fluorescence spectrophotometer at room temperature. Magnetic susceptibilities on crystal samples were measured with a Quantum Design MPMS SQUID magnetometer in the temperature 5–300 K. The applied magnetic field was 0.5 T. Diamagnetic correction was made with Pascal’s constant for all the constituent atoms. 2.3. Synthesis of [Co2L(l2-Cl)] (ClO4)2 Æ 3CH3CN Æ C2H5OC2H5 (1) A 5 mL aqueous solution of Co(ClO4)2 Æ 6H2O (0.146 g, 0.4 mmol) and NaCl (0.033 g, 0.4 mmol) was added dropwise to a 10 mL methanol solution of HL (0.122 g, 0.2 mmol) and N(Et)3 (0.2 mmol). (Caution! Perchlorate salts of metal complexes with organic ligands are potentially explosive). After 24 h stirring, the purple precipitate formed was filtered and dissolved in 10 mL acetonitrile. Diethyl ether was slowly diffused into the solution. About two days later, purple well-shaped prismatic crystals were obtained, and many of them were suitable for X-ray diffraction studies. Element analysis (%): Found: C, 46.31; H, 4.20; N, 15.92; Calc. for C45H52Cl3Co2N13O10 (1): C, 46.63; H,

Table 1 Crystal data and structure refinement for 1 1 Empirical formula Fw Temperature/K ˚ Wavelength/A Crystal system Space group

C45H52Cl3Co2N13O10 1159.2 293(2) 0.71073 Triclinic Pı

˚ , deg) Unit cell dimensions (A

a = 13.127(6) b = 14.050(7) c = 15.599(7) a = 105.698(10) b = 102.358(10) c = 94.462(10)

˚3 Volume/A Z Density (calc.)/g cm3 l/mm1 F(0 0 0) Crystal size/mm h range/deg Limiting indices

2677(2) 2 1.438 0.835 1196 0.32 · 0.26 · 0.20 1.40–25.00 15 6 h 6 15, 13 6 k 6 16, 18 6 l 6 14 13,894 9388 [Rint = 0.0613] 1.0000 and 0.8419 9388/7/662 0.971 R1 = 0.0755, wR2 = 0.1624 R1 = 0.1884, wR2 = 0.2223 0.956 and 0.393

Reflection collected Independent reflection Max. and Min. Trans. Data/restraints/parameters S Final R indices [I > 2r(I)] R indices (all data) ˚ 3 Largest diff. peak and hole/e A

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2.5. DNA-binding and cleavage experiments The DNA-binding and cleavage experiments were performed at room temperature. All studies on the interaction of complex 1 with calf thymus (ct) DNA were carried out in doubly distilled water buffer containing 10 mM Tris and 1 mM Na2EDTA and adjusted to pH 7.5 with hydrochloride acid. Relative binding of complex 1 to ct-DNA was studied by UV–visible absorption and fluorescence spectral method. The solutions of ct-DNA gave a ratio of UV absorbance at 260 and 280 nm of 1.8–1.9:1, indicating that the DNA was sufficiently free of protein [25]. The DNA concentration per nucleotide was determined by absorption spectroscopy using the known molar extinction coefficient value of 6600 M1 cm1 at 260 nm [26]. UV–visible absorption spectroscopy experiments were conducted by adding ct-DNA solution to the sample of complex 1 (2.7 lM) at different concentrations (0–40 lM). Fluorescence quenching experiments were conducted by adding the solution of complex 1 to the samples containing 2.5 lM EB and 1 mM DNA at different concentrations (0–63 lM). All the samples were excited at 305 nm, and emission was recorded at 550–800 nm. For the gel electrophoresis experiments, supercoiled pBR322 DNA (0.4 lg) was treated with complex 1 in a total volume of 10 ll Tris-EDTA/1 mM Na2EDTA buffer (pH 7.5), and the solution was then incubated at 37 C, 2 ll of a quench buffer solution consisting of 0.25% bromophenol blue and 40% sucrose was added. The samples were immediately loaded on 0.7% agarose gel. Electrophoresis was carried out at 75 V for 3 h in TAE buffer (40 mM Tris base, 40 mM acetic acid, 1 mM EDTA). The gel was stained with 1 mg/ml ethidium bromide and photographed under UV light. 3. Results and discussion 3.1. Description of the crystal structure of 1 The structure of 1 consists of a two-charged, binuclear cobalt(II) cation, two perchlorate anions, three acetonitrile and one diethyl ether molecules. The ORTEP drawing of the cation is shown in Fig. 1 and the selected bond lengths and angles are listed in Table 2. In 1, both Co atoms are five-coordinated with N3OCl donor sets derived from a bridging Cl atom, a bridging alkoxo-O atom, two benzimidazolic-N atoms and a tertiary amiono-N atom. The coordination geometry is distorted trigonal bipyramidal (tbp) and this is reflected in the index of trigonality, s (Co1, 0.75; Co2, 0.72) (s = 0 for a perfect square pyramidal and 1 for a perfect trigonal bipyramidal geometry according to the Addison/Reedijk geometric criterion [27]). In each Cobalt atom, the bridging Cl atom and a tertiary amiono-N atom serve as the axial donors with two benzimidazolic-N atoms and the alkoxo-O atom providing the equatorial donor sets. The deviation of the metals from ˚ (Co1) and 0.3914 A ˚ the equatorial planes is 0.3941 A

Fig. 1. An ORTEP drawing of the cation and the atom numbering.

Table 2 ˚ ) and angles (deg) for 1 Selected bond lengths (A ˚ Bond distances (A) Co(1)–O(1) Co(1)–N(1) Co(1)–N(3) Co(1)–N(5) Co(1)–Cl(1) Bond angles (deg) O(1)–Co(1)–N(1) O(1)–Co(1)–N(3) N(1)–Co(1)–N(3) O(1)–Co(1)–N(5) N(1)–Co(1)–N(5) N(3)–Co(1)–N(5) O(1)–Co(1)–Cl(1) N(1)–Co(1)–Cl(1) N(3)–Co(1)–Cl(1) N(5)–Co(1)–Cl(1) Co(1)–O(1)–Co(2)

1.912(5) 2.018(6) 2.023(6) 2.296(6) 2.449(2) 116.1(2) 116.2(2) 116.2(2) 78.3(2) 78.2(2) 79.1(2) 82.70(15) 111.91(18) 108.54(18) 160.95(15) 112.6(2)

Co(2)–O(1) Co(2)–N(8) Co(2)–N(6) Co(2)–N(10) Co(2)–Cl(1) O(1)–Co(2)–N(8) O(1)–Co(2)–N(6) N(8)–Co(2)–N(6) O(1)–Co(2)–N(10) N(8)–Co(2)–N(10) N(6)–Co(2)–N(10) O(1)–Co(2)–Cl(1) N(8)–Co(2)–Cl(1) N(6)–Co(2)–Cl(1) N(10)–Co(2)–Cl(1) Co(1)–Cl(1)–Co(2)

1.916(5) 2.014(6) 2.026(6) 2.297(6) 2.458(2) 117.3(2) 113.6(2) 117.7(3) 78.6(2) 78.1(2) 79.2(2) 82.38(15) 109.57(18) 110.48(19) 160.87(17) 80.90(7)

(Co2). The Co–O and Co–Cl distances indicate that these bridges are close to symmetric (Co1–O1, 1.912; Co1–O2, ˚ ). The Co1–Co2 1.916; Co1–Cl, 2.449; Co1–Cl2, 2.458 A ˚ separation is 3.239 A, which is comparable to a reported binuclear Co complex containing phenoxo-O and Cl ˚ ) [28]. bridges (3.236, 3.241 A 3.2. Magnetic properties Complex 1 was studied by magnetic susceptibility measurements in the 5–300 K regions. The effective magnetic moment (leff) and the molar magnetic susceptibilities

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199

6

0.03

2.0

0.01

2

0.00

0

Absorbtance

μeff / B.M.

χ /cm3mol-1 M

1.5

4

0.02

1.0

0.5

0.0 0

50

100

150

200

250

200

300

T(K) Fig. 2. Plots of vM and leff vs. T of 1; solid lines represent the best theoretical fits.

(vM) vs. T are plotted in Fig. 2. The leff value per binuclear in 1 varies gradually from 5.58 B.M. at 300 K, which is lower than the spin-only value of two Co(II) atoms (5.78 B.M.), down to 0.4 B.M. at 5 K. The behaviour indicates strong intramolecular antiferromagnetic coupling of the high-spin cobalt irons, tending to a diamagnetic (S = 0) ground state. In this case, the molar paramagnetic susceptibility data are fit an expression [29], which is based on the b ¼ 2J b general isotropic exchange Hamiltonian, H S1  b S 2, with J = magnetic exchange coupling constant and S1 = S2 = 3/2: 2Ng2 b2 vM ¼  kT

14 þ 5 expð6 J=kTÞ þ expð10 J=kTÞ 7 þ 5 expð6 J=kTÞ þ 3 expð10 J=kTÞ þ expð12 J=kTÞ



þ Na

The parameters obtained on fitting of the data were g = 2.22,P J = 13.0 cm1 and P the agreement factor defined by R ¼ ðvobsd  vcalcd Þ2 = v2obsd is equal to 2.10 · 103. The value of J demonstrates strong intramolecular antiferromagnetic coupling of the high-spin Co(II) atoms. 3.3. DNA-binding and cleavage activity 3.3.1. UV–visible absorption spectroscopy Electronic absorption spectroscopy is one of the most useful techniques for DNA-binding studies of metal complexes. The absorption spectra of complex 1 in the absence and presence of ct-DNA at different concentrations (0– 40 lM) are given in Fig. 3. The UV spectroscopy of 1 in DMSO show one very strong absorption at ca. 223 nm, which can be assigned to charge-transfer transitions of ligand L. An intercalative binding of a complex to DNA generally results in hypochromism along with a red shift (bathochromic shift) of the electronic spectral band [30–32]. With increasing DNA concentrations, the hypochromisms increased up to 35.1% at 223 nm. The hypochromisms observed for the bands of complex 1 is

220

240 260 Wavelength (nm)

280

300

Fig. 3. Absorption spectra of complex 1 in the absence (dash line) and presence (solid line) of ct-DNA. [CoL] = 2.7 lM, [DNA] = (0–40) lM. Arrow shows the absorbance change upon increasing DNA concentrations.

accompanied by a small red shift by less than 4 nm. The hypochromisms and red-shifts observed above which are even though not enough evidences, may suggest an intercalative mode. Analysis of the changes in ligand-based band resulted in a scattered Scatchard plot, which rendered it difficult to obtain reliable DNA binding constants. 3.3.2. Luminescence studies The binding of complex 1 to the ct-DNA has been studied by fluorescence spectral method. Measurements have been carried out using emission intensity of EB bound to DNA as a probe. EB is a weak fluorescent, but its emission intensity in the presence of DNA can be greatly enhanced because of its strong intercalation between the adjacent DNA base pairs [33]. Competitive binding to DNA of the complex with EB could provide rich information regarding DNA binding nature and relative DNA binding affinity. It was previously reported that this enhanced fluorescence could be quenched, at least partly by the addition of a second molecule [34,35]. The emission spectra of EB bound to DNA in the absence and the presence of complex 1 are given in Fig. 4. The addition of complex 1 to the DNA bound EB solutions, caused obvious reduction in emission intensities, indicating that complex 1 competitively bound to DNA with EB. The extent of reduction of the emission intensity gives a measure of the binding propensity of the complex to DNA. According to the classical Stern–Volmer equation [36]: I0/I = 1 + K[Q]; I0 and I are the fluorescence intensities in the absence and presence of complex 1, respectively. K is a linear Stern–Volmer quenching constant. [Q] is the concentration of the quencher complex 1. The fluorescence quenching curve of EB bound to DNA by complex 1 is shown in Fig. 5. The quenching plot illustrate that the quenching of EB bound to DNA by complex 1 is in agreement with the linear Stern–Volmer equation, which also indicates that the complex bind to DNA. In the plot of

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80 a Intensity (a.u.)

60 f 40

20

0 500

600

700

800

Fig. 6. Cleavage of pBR322 DNA (0.4 lg) by complex 1 at different concentrations in the absence of any reducing agents with an incubation time of 3 h in a buffer containing 10 mM Tris-EDTA/1 mM Na2EDTA (pH 7.5) at 37 C. Lane 1: DNA control; lines 2–9: 2.7, 5.4, 13.5, 27, 54, 81, 135, 270 lM.

Wavelength (nm) Fig. 4. Emission spectra of EB bound to DNA in the absence (dash line) and presence (solid line) of complex 1. [EB] = 2.5 lM, [DNA] = 100 lM, [CoL]a–f = 0, 9, 18, 27, 36, 45, 54, 63 lM, respectively; kex = 305 nm. The arrow shows the intensity changes on increasing the complex concentration.

2.4

Io/I

2.0

1.6

1.2

0

2

4

6

105 X [CoL] (M) Fig. 5. The fluorescence quenching curve of EB bound to DNA by complex 1. [EB] = 2.5 lM, [DNA] = 100 lM, [CoL] = 0 to 63 lM, respectively; kex = 305 nm.

I0/I vs. [CoL], K is given by the ratio of the slope to intercept. The value of K is 1.90 · 104, corresponding to the complex concentration [Q] = 53.1 lM when effecting 50% quenching of initial EB fluorescence, which suggests that the interaction of the complex with DNA is a weak intercalative mode. 3.3.3. DNA-cleavage activity The ability of complex 1 to perform pBR322 DNA cleavage has been studied by agarose gel electrophoresis. When circular plasmid DNA is conducted by electrophoresis, the fastest migration will be observed for the supercoiled form (Form I). If one strand is cleaved, the supercoils will relax to produce a slower-moving nicked circular form (Form II). If both strands are cleaved, a linear form (Form III) will be generated that migrates in between. Interestingly, we have found that complex 1 can cleave the

supercoiled DNA to nicked circular DNA in aerobic condition. Figs. 6 and 7 illustrate the gel electrophoretic separations showing the cleavage of plasmid pBR322 DNA induced by complex 1 at different concentrations and different time, respectively. As shown in Fig. 6, with the increase of the complex concentration, the intensity of the circular supercoiled DNA (Form I) band was found decrease, while that of nicked (Form II) bands increase apparently (lane 2–9). When the complex concentration was up to 135 lM (lane 8), the circular supercoiled DNA (Form I) was disappeared and cleaved to nicked circular DNA completely. As shown in Fig. 7, Form I can be efficiently transformed to Form II within 120 min (line 6). Although the cleavage reaction through 1 does not require additional external agents, we carefully investigated the possibility that diffusible OH radical, singlet 1O2 or superoxide anion radical O 2 were involved in this reaction. As shown in Fig. 8, the cleavage efficiency does not change in the presence of ethanol (lane 3) or DMSO (lane 4) as potential OH scavengers, NaN3 (lane 5) or histidine (lane 6) as potential singlet 1O2 inhibitors, or SOD (lane 7) as a superoxide anion radical O 2 inhibitor [37–39]. In conclusion, the results presented here rule out the involvement of any oxidation inhibitors in the strand cleavage, and this

Fig. 7. Cleavage of pBR322 DNA (0.4 lg) by complex 1 with different time. Cleavage conditions: [complex 1] = 135 lM. Lane 1: DNA control, 120 min; lines 2–6: 5, 15, 30, 60, 120 min. The other conditions see Fig. 6.

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References

Fig. 8. Cleavage of pBR322 DNA by complex 1 (135 lM) with different oxidation inhibitors, incubation time 2 h. Lane 1, DNA control; Lane 2, DNA + 1; lane 3, DNA + 1 + ethanol (1 mM); lane 4, DNA + 1 + DMSO(1 mM); lane 5, DNA + 1 + NaN3 (25 mM); lane 6, DNA + 1 + histidine (25 mM), lane 7, DNA + 1 + SOD (10 units).

reaction most probably occurs through a hydrolytic mechanism. 4. Conclusions To obtain more insight into the selectivity and efficiency of DNA recognized and cleaved by binuclear complexes, we selected one heptadentate ligand and obtained a new binuclear cobalt(II) complex (1). Crystal structure of 1 shows each Co(II) atom has a distorted trigonal bipyramidal geometry. The DNA binding behaviors of complex 1 has been investigated by UV–vis absorption and fluorescence spectroscopy. Results suggest that the complex binds to ct-DNA with a intercalative mode. The interaction between complex 1 and pBR322 DNA has also been investigated by submarine gel electrophoresis, noticeably, the complex exhibits effective DNA cleavage activity in the absence of any external agents. 5. Abbreviations HL PD 0 OH HPTP UV–vis ct-DNA Tris EB EDTA TAE DMSO

N,N,N 0 ,N 0 -tetrakis(2-benzimidazolylmethyl)2-hydroxyl-1,3-diaminopropane 4-tert-butyl-2,6-bis[bis(2-pyridylethyl)amino]phenol) N,N,N 0 ,N 0 -tetra-(2-methylpyridyl)2-hydroxypropanediamine UV–visible calf thymus DNA tris(hydroxymethyl) aminomethane ethidium bromide ethylenediamine tetraacetic acid Tris-acetate-EDTA dimethyl sulfoxide

Acknowledgement This work was supported financially by the National Science Foundation of China (Grant No. 20331020).

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