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Full PaperReceived: 3 February 2010 Revised: 21 March 2010 Accepted: 23 March 2010 Published online in Wiley Interscience: 28 April 2010

(www.interscience.com) DOI 10.1002/aoc.1659

Synthesis, structure and DNA cleavageof mononuclear Fe(III) complexeswith 1,2,4-triazole-base ligandHui Liua,b, Ying-ying Koua, Li Fengc, Dong-dong Lia, Chun-Yan Gaoa,Jin-lei Tiana∗, Jing-yan Zhangb and Shi-ping Yana∗

Two new mononuclear iron(III) complexes, [Fe(HL)2](ClO4) · (H2O)1.75· CH3CN (1) and [Fe(HL)Cl2] · DMF (2) [H2L = 3-(2-phenol)-5-(pyridin-2-yl)-1,2,4-triazole] have been synthesized and characterized by X-ray single-crystal structure analysis. The singlecrystal X-ray crystallographic studies reveal that the central iron atom has a distorted octahedral environment for 1 and adistorted square pyramidal geometry for 2. The DNA cleavage activity of the iron(III) complexes was measured, indicatingthat the six-coordinated iron(III) (complex 1) was cleavage inactive and only five-coordinated complex 2 effectively promotedthe cleavage of plasmid DNA in the presence and/or absence of activating agents (peroxide oxygen) at physiological pH andtemperature. The mechanism of plasmid DNA cleavage was also studied by adding standard radical scavengers. Copyright c©2010 John Wiley & Sons, Ltd.

Supporting information may be found in the online version of this article.

Keywords: iron (III) complex; 1,2,4-triazole; crystal structure; DNA binding; DNA cleavage

Introduction

In recent years, interactions of transition metal complexes withnucleic acids have attracted considerable attention in nucleicacid chemistry. These complexes have been used in footprintingstudies, as sequence-specific DNA binding agents and as newstructural probes in diagnostic medicinal applications.[1,2] Owingto their inherently distinct structure and reactivity, these metalcomplexes are attractive reagents for potential nuclease activities.Stimulated by the growing interest in binding and cleavage ofnucleic acids, the past two decades have seen extensive researchdevoted to the study of small molecules of transition metalcomplexes as probes of nucleic acid structure,[3 – 17] especiallytheir copper complexes.[5 – 8]

The previous work of our research group mainly focused onthe nuclease activity of Cu(II) complexes.[9 – 13] However, it wasnecessary to generate more insight into the selectivity andefficiency of DNA recognized and cleaved by different metalcomplexes. Bleomycins (BLMs), in which iron(II) ions bind to itschelation unit, are glycopeptide antitumor antibiotics that cleaveDNA in an oxidative manner.[18] We decided to investigate thechemical nuclease activity of iron complexes. For this purpose,we successfully used the triazole ligand 3-(2-phenol)-5-(pyridin-2-yl)-1,2,4-triazole (Scheme 1) to form two new iron complexes. Asfar as we are aware, there are a few reports about the chemicalnuclease activity of iron complexes,[14 – 17] but no report on ironcomplexes based on 1,2,4-triazole. Our approach was to designactive complexes which could efficiently cleave DNA; however,only complex 2 shows chemical nuclease activity. In this article wepresent the synthesis and the single-crystal structures of two newiron complexes 1 and 2 based on 1,2,4-triazole, as well as the DNAbinding and cleavage activities of complex 2, which can efficientlycleave DNA in the presence of H2O2.

Experimental

Materials and Instruments

All the starting materials and solvents were obtained from com-mercial sources and used without further purification. LigandH2L [3-(2-phenol)-5-(pyridin-2-yl)-1,2,4-triazole] was prepared ac-cording to a published procedure.[19] Ethidium bromide (EB), calfthymus DNA (CT-DNA) and pBR322 plasmid DNA were purchasedfrom Sigma. Solvents used in this research were purified by stan-dard procedures. Tris–HCl buffer solution was prepared usingdeionized sonicated triple-distilled water. Solution of the iron (III)complex and other reagents used for strand scission were pre-pared freshly in triple-distilled water before use. Infrared spectrawere recorded as KBr pellets using a Bruker Tensor 27 spectropho-tometer in the 4000–400 cm−1 regions. Elemental analyses for C,H and N were obtained on a Perkin-Elmer analyzer model 240.Determination of Cl was by an Agilent 7500C ICP-MS instrument.Electronic spectra were measured on a Jasco V-570 spectropho-tometer. Fluorescence spectral data were obtained on an MPF-4fluorescence spectrophotometer at room temperature.

∗ Correspondence to: Jin-lei Tian and Shi-ping Yan, Department of Chemistry,Nankai University, Tianjin 300071, People’s Republic of China.E-mail: yansp@nankai.edu.cn

a Department of Chenistry, Nankai University, Tianjin, 300071, People’s Republicof China

b School of Pharmacy, East China University of Science and Technology, Shanghai200237, People’s Republic of China

c Tianjin University of Traditional Chinese Medicine, Tianjin 300193, People’sRepublic of China

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N N

HN

N

HO

Scheme 1. structure of the ligand.

Synthesis of [Fe(HL)2](ClO4) · (H2O)1.75· CH3CN (1)

Complex 1 was prepared by a general synthetic method in whichan aqueous solution of Fe(ClO4)3·6H2O (46.2 mg, 0.1 mmol in 10 mlH2O) was initially reacted with an acetonitrile solution of ligand(47.6 mg, 0.2 mmol resolved in 10 ml CH3CN) treated with 1 equiv.of Et3N. The reaction mixture was stirred at room temperaturefor 4 h, the formed dark purple solution was filtered. The filtrategave dark purple single crystals suitable for X-ray diffraction onslow evaporation for several days. The crystals were isolated andwashed with cold aqueous acetonitrile (1 : 1 v/v) then dried overP4O10 (yield ca 51%). Anal. calcd for C28H24.50ClFeN9O7.75: C, 47.88;H, 3.52; N, 17.95; Cl, 5.05. Found: C, 47.82; H, 3.59; N, 17.91; Cl, 4.67%.Selected IR data (KBr, cm−1): 3400(vs), 1624(vs), 1260(s), 1517(s),1090(s), 923(s), 751(m). Conductivimetry: 89 �−1 mol−1 cm2 (inacetonitrile).

Synthesis of [Fe(HL)Cl2] · DMF (2)

Complex 2 was synthesized by the similar procedure using FeCl3instead of Fe(ClO4)3 · 6H2O. The formed purple solid productswere resolved in DMF, then filtered and the filtrate was kept inair; after 2 weeks, the single crystals suitable for X-ray diffraction

were isolated by filtration and were air-dried. Yield ca 65%. Anal.calcd for C16H16Cl2FeN5O2: C, 43.97; H, 3.69; N, 16.02; Cl, 16.22.Found: C, 43.93; H, 3.75; N, 16.11; Cl, 15.03%. Selected IR data (KBr,cm−1): 1630(vs), 1265(s), 1518(s), 924(s), 748 (m). Conductivimetry:56 �−1 mol−1 cm2 (in DMF).

X-ray crystallography

The determination of the unit cells and the intensity datacollections for 1 and 2 were performed on a Bruker Smart 1000diffractometer equipped with Mo-Kα radiation (λ = 0.71070 Å)and graphite-monochromated byω−2θ scan technique at 293(2) Kfor 1 and 113(2) K for 2. Semi-empirical absorption correctionswere applied using the SADABS program. The structure ofcomplexes were solved by direct methods and successive Fourierdifference syntheses (SHELX-97) and refined by full-matrix least-squares procedure on F2 with anisotropic thermal parametersfor all non-hydrogen atoms (SHELXL-97).[20,21] Hydrogen atomswere generated geometrically and refined isotropically. Thecrystallographic data and the refinement results are listed inTable 1.

DNA-binding and cleavage experiments

The UV absorbance at 260 and 280 nm of the CT-DNA solutionin 18 mM NaCl–50 mM Tris–HCl buffer (pH = 7.2) gives a ratio of1.8–1.9, indicating that the DNA was sufficiently free of protein.[21]

The stock solution of CT-DNA was prepared in Tris–HCl/NaClbuffer, pH = 7.2 (stored at 4 ◦C and used within 4 days). Theconcentration of CT-DNA was determined from its absorption

Table 1. Crystal data and structure refinement for 1 and 2

Complex 1 2

Empirical formula C28 H24.50 Cl Fe N9 O7.75 C16 H16 Cl2 Fe N5 O2

Formula weight 702.37 437.09

Temperature (K) 293(2) 113(2)

Crystal system Triclinic Triclinic

Space group P1 P1

a (Å) 9.7815(18) 7.162(4)

b (Å) 12.943(2) 9.195(6)

c (Å) 13.575(2) 14.590(10)

α (deg) 102.400(3) 107.376(9)

β (deg) 110.358(3) 98.540(12)

γ (deg) 93.410(4) 91.114(3)

V (Å3) 1556.7(5) 904.7(10)

Z 2 2

ρ (g cm−3) 1.498 1.605

µ (mm−1) 0.634 1.150

F (000) 721 446

Crystal size (mm3) 0.22 × 0.14 × 0.12 0.20 × 0.18 × 0.16

θ range for data collection 1.63–25.02 2.33–25.01

Limiting indices −7 ≤ h ≤ 11, −15 ≤ k ≤ 12, −16 ≤ l ≤ 16 −8 ≤ h ≤ 8, −10 ≤ k ≤ 10, −17 ≤ l ≤ 17

Reflections collected/unique 8000/5459 [R(int) = 0.0332] 6751/3123 [R(int) = 0.0427]

Max. and min. transmission 1.000000 and 0.760997 0.8374 and 0.8026

Data/restraints/parameters 5459/113/468 3123/0/238

Goodness-of-fit on F2 1.026 1.062

Final R indices [I > 2σ (I)] R1 = 0.0552, wR2 = 0.1285 R1 = 0.0442, wR2 = 0.1233

R indices (all data) R1 = 0.1105, wR2 = 0.1626 R1 = 0.0520, wR2 = 0.1260

Largest difference peak and hole (e Å−3) 0.498 and −0.336 0.914 and −0.681

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intensity at 260 nm using the molar absorption coefficient as 6600M−1 cm−1.[22] The binding constant was determined using thefollowing equation (1):[23]

[DNA]/(εA − εF) = [DNA]/(εB − εF) + 1/Kb(εB − εF) (1)

Here εA, εF, and εB correspond to Aabsd/[complex], the extinctioncoefficient for the free complex, and the extinction coefficient forthe complex in the fully bound form, respectively.

The fluorescence quenching experiments were studied byadding the solution of complex 2 into the EB-bound CT-DNAsolution (containing 4.0 × 10−6 M EB and 80 × 10−6 M of DNA) in5 mM Tris–HCl/NaCl buffer (pH = 7.2) at different concentrations.The fluorescence spectra were recorded at room temperature withexcitation at 510 nm and emission at 602 nm.

The DNA cleavage experiments were carried out by agarose gelelectrophoresis, which was performed as described previously.[10]

After being electrophoresed for 4 h at 80 V on 0.8% agarose gelusing Tris–boric acid–EDTA buffer, bands were visualized by UVlight and photographed. For cleavage mechanistic investigation ofpBR322 DNA, the experiments were done using different reagentssuch as DMSO, SOD, NaN3 and EDTA, which are added to PBR322DNA prior to the addition of complex.

Results and Discussion

Description of the Structure

Complexes 1 and 2 have been structurally characterized by X-raycrystallography. Selected bond lengths and bond angles for 1 and2 are summarized in Tables 2 and 3, respectively. The structure of1 consists of mononuclear [Fe(HL)2]+ cations (Fig. 1), perchlorateanions and some solvate molecules. The central Fe(III) atom iscoordinated to two HL− , giving a distorted octahedral geometrywith an O2N4 donor set. The phenolic hydroxyl group in H2Lis active and easily deprotoned, thus each HL− servers as atridentate monoanion coordinated to one Fe(III) atom. The basalplane is formed by the N2O2 set of donors, including two pyridinenitrogen atoms (N1, N5), and two phenolate oxygen atoms (O1,O2). Two triazole nitrogen atoms (N2, N6) occupy the other twoaxial positions in the octahedron. The Fe (III) center is lifted0.167 Å above this least-squares plane. For 2, it is a neutralmononuclear Fe(III) complex (Fig. 2) and the iron atom has afive-coordinated geometry with two nitrogen atoms and onephenolate oxygen atom from the ligand and two chloride ions.The trigonality τ value is calculated to be 0.41 according to theAddison–Reedijk geometric criterion,[24] which reveals that thegeometry of 2 is closer to the square-pyramidal configuration.O1, N1, N4 and Cl1 atoms form the basal plane with Fe1–N12.290(3) Å, Fe1–N4 2.019(3) Å, Fe1–O1 1.8903 Å and Fe1–Cl12.246 (1) Å, respectively. The deviations of the four donor atomsfrom their mean plane are −0.296, 0.368, −0.291 and 0.218 Å,respectively. The apical position is occupied by Cl2 with Fe1–Cl2distance of 2.235 (2) Å and the iron atom is out of the basal planeby 0.435 Å.

DNA-binding and cleavage activity

DNA binding properties

DNA binding is the critical step for DNA activity; therefore thebinding ability of complex 2 with calf thymus (CT- DNA) was

Table 2. Selected bond lengths (Å) and bond angles (deg) forcomplex 1

Bond lengths

Fe(1)–O(1) 1.891(3) Fe(1)–O(2) 1.931(3)

Fe(1)–N(1) 2.270(4) Fe(1)–N(5) 2.305(4)

Fe(1)–N(2) 2.031(4) Fe(1)–N(6) 2.024(3)

Bond angles

O(1)–Fe(1)–O(2) 98.32(15) O(1)–Fe(1)–N(6) 107.61(14)

O(2)–Fe(1)–N(6) 84.52(14) O(1)–Fe(1)–N(2) 84.51(14)

O(2)–Fe(1)–N(2) 111.18(14) N(6)–Fe(1)–N(2) 159.02(16)

O(1)–Fe(1)–N(1) 157.51(13) O(2)–Fe(1)–N(1) 88.80(15)

N(6)–Fe(1)–N(1) 94.25(14) N(2)–Fe(1)–N(1) 73.03(14)

O(1)–Fe(1)–N(5) 91.65(15) O(2)–Fe(1)–N(5) 157.33(13)

N(6)–Fe(1)–N(5) 73.03(14) N(2)–Fe(1)–N(5) 89.92(14)

N(1)–Fe(1)–N(5) 89.65(14)

Table 3. Selected bond lengths (Å) and bond angles (deg) forcomplex 2

Bond lengths

Fe(1)–O(1) 1.890(3) Fe(1)–N(1) 2.290(3)

Fe(1)–Cl(1) 2.2460(14) Fe(1)–Cl(2) 2.2353(15)

Fe(1)–N(4) 2.019(3)

Bond angles

O(1)–Fe(1)–N(4) 84.19(12) O(1)–Fe(1)–Cl(2) 103.75(9)

N(4)–Fe(1)–Cl(2) 115.97(9) O(1)–Fe(1)–Cl(1) 101.98(9)

N(4)–Fe(1)–Cl(1) 132.12(9) Cl(2)–Fe(1)–Cl(1) 108.56(6)

O(1)–Fe(1)–N(1) 156.75(11) N(4)–Fe(1)–N(1) 72.84(11)

Cl(2)–Fe(1)–N(1) 89.81(8) Cl(1)–Fe(1)–N(1) 91.15(8)

Figure 1. A drawing of [Fe(HL)2]+ in 1; hydrogen atoms are omitted forclarity.

Figure 2. A drawing of [Fe(HL)Cl2] in 2; hydrogen atoms are omitted forclarity.

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200 250 300 350

0.5

1.0

1.5

2.0

2.5

217nm

203nm

Abs

.

Wav.(nm)

Figure 3. Absorption spectra of complex 2 (1.1 × 10−5 M) in theabsence (dashed line) and presence (solid line) of increasingamounts of CT-DNA (0–1.6 × 10−4 M) at room temperature in 5 mMTris–HCl/NaCl buffer (pH = 7.2). The dashed lines indicate the freecomplex.

studied using UV–vis absorption and fluorescence spectra. Beforeadding CT-DNA to 2, its behavior in CH3CN and/or Tris buffersolution (pH 7.2) at room temperature was monitored by UV–visspectroscopy for 24 h; two absorption bands at 203 and 298 nmwere observed from start to finish, indicating that 2 is stableunder the experiment condition. The absorption spectra of 2 inthe absence and presence of CT-DNA at different concentrationsare given in Fig. 3. As shown in Fig. 3, the absorption spectra of 2in CH3CN show one very strong absorption at ca 203 nm, whichcan be assigned to intraligand π − π∗ transition and a weakerabsorption band at 298 nm in the CT region of 2. Upon addition ofdifferent concentrations of calf thymus DNA (0–1.6 × 10−4 M) to 2(1.1 × 10−5 M), the band at 203 nm showed a 31% hypochromismalong with a 14 nm red shift, which suggests moderate bindingof the complex 2 with DNA, whereas the band at 298 nm didnot show any significant change. From the observed spectralchange, the value of the intrinsic binding constant Kb (1.89 × 104

M−1) was determined by regression analysis using eqn (1). ThisKb value is smaller than those reported for typical classicalintercalators (EB-DNA, 3.3 × 105 M−1 in 50 mM Tris–HCl/1.0 NaClbuffer, pH 7.5).[25]

Moreover, the fluorescence study of 2 was made in the samebuffer solution at room temperature to further clarify the bindinginteraction of 2 with CT-DNA. No luminescence emission canbe observed for 2, so the binding of the complex cannot bedirectly presented in the emission spectra. The relative bindingof complex 2 to CT-DNA was studied with an EB-bound CT-DNA solution. EB emits intense fluorescent light in the presenceof DNA due to its strong intercalation between the adjacentDNA base pairs. The addition of a second DNA-binding moleculecan quench the DNA-EB adduct emission. As depict in Fig. 4,addition of complex 2 to the DNA-bound EB solutions causes anappreciable reduction in emission intensity. The quenching plots(Fig. 5) are in agreement with the linear Stern–Volmer equation:[26]

I0/I = 1 + K[complex]. In the plot of I0/I vs the concentrationsof complex, K is given by the ratio of the slope to intercept.According to the equation KEB[EB] = Kapp[complex], where thecomplex concentration is the value for a 50% reduction of thefluorescence intensity of EB (KEB = 1.0 × 107 M−1, [EB] = 4.0 µM),the Kapp values are calculated to be 4.48 × 106 M−1 for complex2, less than the binding constant of the classical intercalatorsand metallointercalators (107 M−1),[27] which suggests that theinteractions of the complex 2 with DNA is moderate intercalativemodes.

550 600 650 700 750 8000

1

2

3

4

5

6

7

8

Inte

nsity

Wav.(nm)

Figure 4. Emission spectra of complex 2 (1.1 × 10−5 M) in the absence(dashed line) and presence (solid line) of increasing amounts of CT-DNA(0–1.6×10−4 M) at room temperature in 5 mM Tris–HCl/NaCl buffer (pH =7.2). The arrow shows the changes in intensity at increasing concentrationsof the complex.

0 1 2 3 4 5

1.0

1.1

1.2

1.3

1.4

1.5

1.6

I 0/I

[complex]/ µM

Figure 5. The plot of I0/I vs [complex]: I0 is the emission intensity of EB-DNAin the absence of complex and I is the emission intensity of EB-DNA in thepresence of complex.

DNA cleavage properties

The ability of 2 to cleavage supercoiled (SC) pBR322 DNA has beenstudied using agarose gel electrophoresis in Tris–HCl/NaCl buffer(pH = 7.2) medium, in the absence and/or presence of additivessuch as H2O2. Complex 2 showed pronounced nuclease activityon SC DNA in absence of any external agents, in a concentration-dependent manner (Fig. 6, lanes 1–8). As shown in Fig. 6, withthe increase of the concentrations of 2, form I plasmid DNA isgradually converted into form II (lanes 1–8). In the absence ofH2O2, complex 2 cleaved SC form (form I) is only about 40%,producing 40% nicked circular form (NC, form II) and no linearform (form III, 0%) at 0.8 mM concentration (lane 8 in Fig. 6).However, in the presence of hydrogen peroxide, the most strikingfeature is a higher nuclease activity of complex 2 (Fig. 7, lane 8,0.8 mM 2: form I, 0%; form II, 85%; form III, 15%, even at 0.05 mM

concentration, lane 2, form I, 5%; form II, 85%; form III 10%). Theresults indicated that complex 2 can efficiently promote DNAcleavage in the presence of hydrogen peroxide. The cleavagemediated by complex 2 produces double-strand cleavage on theDNA. This is evidenced in Fig. 7, where the linear form appearsbefore the supercoiled form (SC) is completely converted to thenick form (NC). The double-stranded DNA cleaving ability of thecomplex 2 is quite novel, and a synthetic model for the bleomycins.

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Figure 6. Agarose gel electrophoresis of pBR322 plasmid DNA treated withcomplex 2 at different concentrations in a medium of 50 mM Tris–HCl/NaClbuffer (pH = 7.2) and in the absence of any external agents. Lane 0,supercoiled DNA (control); lanes 1–8, DNA + complex 2 (0.1, 0.2, 0.3, 0.4,0.5, 0.6, 0.7, 0.8 mM).

Figure 7. Agarose gel electrophoresis of pBR322 plasmid DNA treated withcomplexes with addition of hydrogen peroxide (25 mM) + complex 2 indifferent concentrations. Lane 0, supercoiled DNA (control); lane 1, H2O2(25 mM); lanes 2–8, DNA + H2O2 (25 mM) + complex 2 (0.05, 0.1, 0.2, 0.4,0.6, 0.7, 0.8 mM).

Figure 8. Agarose gel electrophoresis of pBR322 plasmid DNA treatedwith 0.8 mM complex 2 in the presence of potential inhibitor agents. Theincubation time is 3 h (37 ◦C). Lane 0, supercoiled DNA (control); lane 1,DNA + 2; lane 2, DNA + 2 + DMSO (1 M); lane 3, DNA + 2 + NaN3 (100 mM);lane 4, DNA + 2 + SOD (15 units); lane 5, DNA + 2 + EDTA (1 mM).

To understand the DNA cleavage mechanism by complex 2,the experiment was carried out in the presence of a hydroxylradical scavenger (DMSO), a singlet oxygen quencher (NaN3),a superoxide scavenger (SOD) and a chelating agent (EDTA)[28]

under our experimental conditions (Fig. 8, lanes 1–5). As shownin Fig. 8, all of the radical scavengers used can more or less inhibitthe DNA cleavage in the cleavage reactions, which indicatesthat reactive oxygen species (including hydroxyl radical, singletoxygen, superoxide anion radical) are involved in the course ofthe DNA cleavage reaction. It is noteworthy that addition of EDTAto the reaction system can efficiently catalyze DNA cleavage (seeFig 8, lane 5); this is due to Fenton reaction.[29] On the basis of theresults mentioned above, we propose that the iron(III) complex2 can promote DNA cleavage through an oxidative DNA damagepathway.

Conclusion

In summary, we have synthesized and characterized two mononu-clear iron (III) complexes based on 1,2,4-triazole. The interaction ofcomplex 2 with calf thymus DNA (CT-DNA) has been investigatedby UV absorption and fluorescence spectroscopy, showing thatcomplex 2 can bind to CT-DNA, and the chemical nuclease activityof complex 2 was also studied by agarose gel electrophoreses.Complex 2 can effectively cleave plasmid DNA without addi-tion of external agents. However, in the presence of hydrogen

peroxide at pH = 7.2 and 37 ◦C, the DNA cleavage reaction with 2is significantly promoted. Comparative reactions have been carriedout in the presence of various radical inhibitors and/or trapperssuch as NaN3, SOD and DMSO. These results are indicative of anoxidative-type cleavage of DNA for 2.

Acknowledgments

This work was supported by the National Natural ScienceFoundation of China (no. 20771063).

Supporting information

Supporting information may be found in the online version of thisarticle.

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www.interscience.wiley.com/journal/aoc Copyright c© 2010 John Wiley & Sons, Ltd. Appl. Organometal. Chem. 2010, 24, 636–640