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1 Electronic Supplementary Material (ESI) for Dalton Transactions. This journal is The Royal Society of Chemistry 2016 Electronic Supplementary Information (ESI) Cytotoxic and antimicrobial effects of indium(iii) complexes with 2-acetylpyridine-derived thiosemicarbazones Alexandre A. Oliveiraª, Gabriele M. C. Perdigão b, Luana E. Rodriguesª, Jeferson G. da Silva c, Elaine M. Souza-Fagundes b, Jacqueline A. Takahashi a, Willian R. Rocha a and Heloisa Beraldo a, * a Departamento de Química, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil. b Departamento de Fisiologia e Biofísica, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil. c Departamento de Farmácia, Universidade Federal de Juiz de Fora, Campus Governador Valadares, Governador Valadares, MG, Brazil. *Corresponding author. Tel.: +55 (31) address: hberaldo@ufmg.br heloisaberaldoufmg@gmail.com (H. Beraldo)
2 Table of contents Page Infrared spectra, 1 H and 13 C{ 1 H} NMR spectra of the complexes 2 [In(2Ac4oClPh)Cl 2 (MeOH)] (1), [In(2Ac4pFPh)Cl 2 (MeOH)] (2), [In(2Ac4pClPh)Cl 2 (MeOH)] (3) and [In(2Ac4pIPh)Cl 2 (MeOH)] (4) Stability in solution 15 X-ray crystallography 16 Albumin binding studies 18 DNA binding studies 22 Cartesian coordinates of the B3LYP/TZVP optimized structures of the 25 complexes Structure Activity Relationships results 50 References 56 1
3 Infrared spectra, 1 H and 13 C{ 1 H} NMR spectra of the complexes [In(2Ac4oClPh)Cl 2 (MeOH)] (1), [In(2Ac4pFPh)Cl 2 (MeOH)] (2), [In(2Ac4pClPh)Cl 2 (MeOH)] (3) and [In(2Ac4pIPh)Cl 2 (MeOH)] (4) N CH 3 N NH S 8 NH R MeOH, InCl 3 - HCl N 7 CH 3 1 Cl N In N Cl 8 S NH O H CH R Figure S1. Syntheses of the indium(iii) complexes with 2-acetylpyridine-derived thiosemicarbazones and carbon atom numbering. 2
4 Figure S2. 1 H NMR spectrum of [In(2Ac4oClPh)Cl 2 (MeOH)] (1) in DMSO-d 6 (400 MHz) at room temperature 3
5 Figure S3. 13 C{ 1 H} NMR spectrum of [In(2Ac4oClPh)Cl 2 (MeOH)] (1) in DMSO-d 6 (100 MHz) at room temperature 4
6 Figure S4. FT-IR spectrum of [In(2Ac4oClPh)Cl 2 (MeOH)] (1) (KBr pellet) 5
7 Figure S5. 1 H NMR spectrum of [In(2Ac4pFPh)Cl 2 (MeOH)] (2) in DMSO-d 6 (400 MHz) at room temperature 6
8 Figure S6. 13 C{ 1 H} NMR spectrum of [In(2Ac4pFPh)Cl 2 (MeOH)] (2) in DMSO-d 6 (100 MHz) at room temperature 7
9 Figure S7. FT-IR spectrum of of [In(2Ac4pFPh)Cl 2 (MeOH)] (2) (KBr pellet) 8
10 Figure S8. 1 H NMR spectrum of [In(2Ac4pClPh)Cl 2 (MeOH)] (3) in DMSO-d 6 (400 MHz) at room temperature 9
11 Figure S9. 13 C{ 1 H} NMR spectrum of [In(2Ac4pClPh)Cl 2 (MeOH)] (3) in DMSO-d 6 (100 MHz) at room temperature 10
12 Figure S10. FT-IR spectrum of [In(2Ac4pClPh)Cl 2 (MeOH)] (3) (KBr pellet) 11
13 Figure S11. 1 H NMR spectrum of [In(2Ac4pIPh)Cl 2 (MeOH)] (4) in DMSO-d 6 (400 MHz) at room temperature 12
14 Figure S C{ 1 H} NMR spectrum of [In(2Ac4pIPh)Cl 2 (MeOH)] (4) in DMSO-d 6 (100 MHz) at room temperature 13
15 Figure S13. FT-IR spectrum of [In(2Ac4pIPh)Cl 2 (MeOH)] (4) (KBr pellet) 14
16 Stability in solution Figure S14. Electronic spectra of complex (1) as a function of time at 7.5 µm in DMSO Figure S15. Electronic spectra of complex (1) as a function of time in DMSO 5%- Tris-HCl buffer ph 7.4 at 7.5 µm 15
17 X-ray crystallography Figure S16. Molecular plots of complexes [In(2Ac4pFPh)Cl 2 (DMSO)] 0.22DMSO 0.78C 3 H 6 O (2a) and [In(2Ac4pIPh)Cl 2 (DMSO)] 0.41DMSO 0.59C 3 H 6 O (4a) showing the labeling scheme of the non H atoms and their displacement ellipsoids at the 50 % probability level. 16
18 Table S1. Selected bond lengths (Å) and angles ( o ) for 1a, 2a, 3a and 4a in comparison with the parent free thiosemicarbazones Bond H2Ac4oClPh a 1 1a H2Ac4pFPh 2 2a H2Ac4pClPh 1 3a H2Ac4pIPh 2 4a S1 C (3)/1.654(3) (17) 1.672(2) (17) 1.671(2) (16) 1.670(3) 1.764(6) N2 C (3)/1.278(3) 1.287(2) 1.280(2) 1.294(2) 1.283(2) 1.290(2) 1.285(4) 1.287(7) N2 N (3)/1.361(3) (19) 1.377(2) (19) 1.374(2) (18) 1.376(3) 1.369(6) N3 C (3)/1.351(3) 1.308(2) 1.349(2) 1.316(2) 1.352(2) 1.312(2) 1.352(4) 1.315(7) In1 N (14) (14) (13) (5) In1 N (14) (13) (13) (4) In1 S (4) (5) (4) (17) In1 Cl (4) (5) (4) (14) In1 O (13) (12) (12) (4) Angle H2Ac4oClPh a 1a H2Ac4pFPh 2a H2Ac4pClPh 3a H2Ac4pIPh 4a C7 N2 N (2)/118.7(2) (14) (13) (13) (15) (13) 118.1(2) 118.5(4) N2 N3 C (2)/118.9(2) (14) (14) (13) (15) (13) 118.7(2) (4) N3 C8 S (2)/121.5(2) (13) (12) (13) (15) (12) 120.2(2) 128.7(4) N1 In1 N (5) (5) (5) (16) N1 In1 Cl (4) (4) (4) (12) N1 In1 Cl (4) (4) (3) (13) N1 In1 S (4) (4) (4) (13) N2 In1 Cl (7) (4) - 164,05(4) (12) N2 In1 Cl (4) (4) (4) (12) N2 In1 S (4) (4) (3) (12) Cl1 In1 S (15) (16) (14) (6) Cl2 In1 S (16) (17) (14) (6) O1 In1 S (4) (4) (3) (12) a The two bond distances and angles in H2Ac4oClPh refer to the two molecules per asymmetric unit. 17
19 Albumin binding studies Fluorescence quenching studies with HSA The emission spectra of HSA at 298 K in the absence and in the presence of various concentrations of complex (1) are shown in Figure S17. HSA displays strong emission at 340 nm (excitation at 295 nm). By increasing the concentration of 1, a decrease of the fluorescence maximum together with a hypsochromic shift (from 340 nm to 331 nm) were observed, indicating the presence of a more hydrophobic microenvironment around the Trp-214 residue upon formation of the HSA-1 system. 3 Similar changes occurred for complexes (2-4). Figure S17. Emission spectra of HSA (1.92 μm) at 298 K in the absence (- - -) and in the presence ( ) of increasing concentrations of 1 ( μm), λ ex = 295 nm. Arrows indicate the spectral changes. In order to determine the fluorescence quenching mechanism, HSA titration experiments were performed at three different temperatures (293, 298 and 308 K). Based on the fluorescence intensity at λ em = 340 nm for each different temperature, the Stern-Volmer quenching constant (K SV ) and the bimolecular quenching rate constant (K q ) were obtained using the classical Stern-Volmer Equation (S1): 4 18
20 F 0 /F = 1 + K SV [Q] = 1 + Kqτ 0 [Q] (S1) in which F 0 and F are the fluorescence intensities in the absence and in the presence of the quencher, respectively, [Q] is the quencher concentration and τ 0 is the average lifetime of the fluorophore (Trp-214) in the absence of quencher ( τ 0 = 10-8 s for most biomolecules). 5 K SV is graphically obtained as the slope of the linear fit from the plot of F 0 /F vs [Q] (Figure 3a, main article), and K q is calculated as the K SV / τ 0 ratio. Binding constants The fluorescence quenching was most probably preceded by complex formation between fluorophore (F) and quencher (Q). The binding constant (K b ) and the number of independent binding sites (n) on HSA were determined graphically using the Scatchard Equation (S2): 6 F + nq FQ log( F 0 F (S2) F ) = logk b + nlog[q] The plot of log[(f 0 -F)/F] vs log[complex] gives n and logk b as the slope and intercept, respectively (Table S2, Figure 3b, main article). Determination of thermodynamic parameters Figure 3c (main article) shows the Van't Hoff diagram (lnk vs 1 / T) for the interaction between HSA and complexes (1-4). The standard enthalpy change (ΔHº) and the standard entropy change (ΔS o ) were obtained from the Van't Hoff Equation (S3) by plotting lnk b vs 1/T, where -ΔHº / R is the angular coefficient and ΔS o / R is the linear coefficient. 19
21 lnk b = H o RT + S o R (S3) Furthermore, the Gibbs free energy (ΔG) of the binding processes, at a given temperature, is calculated from Equation (S4): G = RTlnK b (S4) As shown in Table S2, the variation in standard enthalpy (ΔHº) and standard entropy (ΔSº) are negative, suggesting that Van der Waals forces and / or hydrogen bonds play a major role in the interactions. The negative values for ΔG show that the binding processes are spontaneous. 20
22 Table S2. Fluorescence suppression constants (K SV ), binding constants logarithm (logk b ), number of binding sites (n) and thermodynamic parameters for the interaction between HSA and indium(iii) complexes (1-4) at different temperatures Compound T (K) K SV (10 5 M -1 ) logk b n ΔG (kj mol -1 ) ΔHº (kj mol -1 ) ΔSº (J mol -1 K -1 ) 293 (5.20 ± 0.09) (5.86 ± 0.12) (1.03 ± 0.02) [In(2Ac4oClPh)Cl 2 (MeOH)] (3.32 ± 0.07) (5.32 ± 0.09) (0.94 ± 0.02) (2.40 ± 0.05) (4.69 ± 0.16) (0.86 ± 0.03) (4.88 ± 0.09) (5.37 ± 0.09) (0.95 ± 0.02) [In(2Ac4pFPh)Cl 2 (MeOH)] (3.65 ± 0.07) (5.30 ± 0.13) (0.95 ± 0.02) (2.61 ± 0.07) (4.88 ± 0.10) (0.90 ± 0.02) (4.69 ± 0.07) (5.66 ± 0.14) (0.98 ± 0.02) [In(2Ac4pClPh)Cl 2 (MeOH)] (3.13 ± 0.07) (5.04 ± 0.12) (0.91 ± 0.03) (2.68 ± 0.05) (4.41 ± 0.07) (0.87 ± 0.01) (3.84 ± 0.08) (5.38 ± 0.10) (0.96 ± 0.02) [In(2Ac4pIPh)Cl 2 (MeOH)] (3.42 ± 0.05) (5.22 ± 0.10) (0.95 ± 0.02) (2.67 ± 0.04) (5.02 ± 0.09) (0.93 ± 0.01)
23 DNA binding studies Electronic spectral studies The absorption spectra of 1-4 in the absence and in the presence of increasing concentrations of CT-DNA are given in Figure S18. Upon addition of DNA, a significant hypochromism accompanied by a small bathochromic shift were observed at the wavelength of maximum absorption, in accordance with an intercalative binding mode, as in the case of classical intercalators such as ethidium bromide (EB). 7 Figure S18. Electronic absorption spectra of 1 (initial concentration of 33 μm) in the absence (- - -) and in the presence ( ) of increasing concentrations of CT-DNA (complex:dna molar ratios ranging from 10:1 to 1:1). Arrows indicate the spectral changes. In order to quantitatively compare the non-covalent binding strength, the intrinsic binding constants (K b ) of 1-4 with CT-DNA were obtained using Equation (S5): 6 [DNA] (ε a ε f ) = [DNA] (ε b ε f ) + 1 K b (ε b ε f ) (S5) 22
24 where [DNA] is the concentration of DNA base pairs, ε a is the molar absorption coefficient of the complex at a given DNA concentration, ε f and ε b are the molar absorption coefficients of the complex unbound and fully bound to DNA, respectively. As shown in Figure 4a (main article), the plot of [DNA] / [ε a - ε f ] vs [DNA] gives 1 / [ε b - ε f ] as slope and 1 / (K b [ε b - ε f ]) as the intercept. The intrinsic binding constant K b is calculated as the ratio between slope and intercept. The determined K b values are shown in Table 6 (main article). Competitive binding between ethidium bromide (EB) and complexes (1-4) for CT-DNA Figure S19 shows the emission spectra of EB bound to DNA in the absence and presence of complex (1). The EB-DNA system shows a strong emission at 595 nm when the excitation wavelength is 546 nm. In all cases a remarkable reduction in the emission intensity was observed in the presence of the indium(iii) complex, presumably due to the reduction in the number of binding sites on DNA available for EB. Figure S19. Emission spectra of EB-DNA system ([EB] = 1.26 μm; [DNA] = 2.00 μm) in the absence (- - -) and presence ( ) of increasing concentrations of complex (1) (0 to 29 μm). Arrow indicates the spectral changes by increasing the concentration of 1 and the vertical line represents λ em = 595 nm. 23
25 The apparent binding constants (K app ) for complexes (1-4) were calculated from Equation (S6): K app = K EB x [EB] C 50 (S6) where K EB is the binding constant between ethidium bromide and DNA (9.5 x 10 6 M -1 per base pair), [EB] is the ethidium bromide concentration ([EB] = 1.26 μm) and C 50 is the required concentration of the compound to reduce 50% of fluorescence of the EB-DNA system. As shown in Figure 4b (main article), the C 50 values were obtained from the plot of fluorescence intensity vs [complex] when fluorescence is 50% of the initial fluorescence. The C 50 values (μm) and K app (10 5 M -1 ) are shown in Table 6 (main article). 24
26 Cartesian coordinates of the B3LYP/TZVP optimized structures of the complexes 1-MeOH (MeOH Coordinated) C C H C H C H C H C C C C C H C H C H C H C H H H N N N N S
27 Cl Cl Cl In H C H H H O H MeOH (MeOH intermolecular) C C H C H C H C H C C C C C H C H C H C H C
28 H H H N N N N S Cl Cl Cl In H C H H H O H Compound 1a (in DMSO) C C H C H C H C H C C C C C
29 H C H C H C H C H H H C H H H C H H H N N N N O S S Cl Cl Cl In H Compound 2a (in DMSO) C C H
30 C H C H C H C C C C H C H C C H C H C H H H C H H H C H H H N N N N O
31 F S S Cl Cl In H Compound 3a (in DMSO) C C H C H C H C H C C C C H C H C C H C H C H H H C
32 H H H C H H H N N N N O S S Cl Cl Cl In H Compound 4a (in DMSO) C C H C H C H C H C C C C H
33 C H C C H C H C H H H C H H H C H H H N N N N H O S S Cl Cl I In Compound 1a (in H 2 O) C C
34 H C H C H C H C C C C C H C H C H C H C H H H C H H H C H H H N N N N
35 O S S Cl Cl Cl In H Compound 2a (in H 2 O) C C H C H C H C H C C C C H C H C C H C H C H H H
36 C H H H C H H H N N N N O F S S Cl Cl In H Compound 3a (in water) C C H C H C H C H C C C C
37 H C H C C H C H C H H H C H H H C H H H N N N N O S S Cl Cl Cl In H Compound 4a (in H 2 O) C
38 C H C H C H C H C C C C H C H C C H C H C H H H C H H H C H H H N N N
39 N H O S S Cl Cl I In Compound 1a-(H 2 O) (in H 2 O) C C H C H C H C H C C C C C H C H C H C H C H H
40 H C H H H C H H H N N N N O S S Cl Cl In H O H H Compound 1a-(H 2 O) 2 (in H 2 O) C C H C H C H C H C
41 C C C C H C H C H C H C H H H C H H H C H H H N N N N O S S Cl In H O H
42 H O H H Compound 2a-(H 2 O) (in H 2 O) C C H C H C H C H C C C C H C H C C H C H C H H H C H H H
43 C H H H N N N N O F S S Cl In H O H H Compound 2a-(H 2 O) 2 (in H 2 O) C C H C H C H C H C C C C H C
44 H C C H C H C H H H C H H H C H H H N N N N O F S S In H O H H O H H
45 Compound 3a-(H 2 O) (in H 2 O) C C H C H C H C H C C C C H C H C C H C H C H H H C H H H C H H H N
46 N N N O S S Cl Cl In H O H H Compound 3a-(H 2 O) 2 (in H 2 O) C C H C H C H C H C C C C H C H C C H C
47 H C H H H C H H H C H H H N N N N O S S Cl In H O H H O H H Compound 4a-(H 2 O) (in H 2 O) C C H C
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