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Article Cite This: Inorg. Chem. 2017, 56, 13491-13499

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Singlet Oxygen Production and Biological Activity of Hexanuclear Chalcocyanide Rhenium Cluster Complexes [{Re6Q8}(CN)6]4− (Q = S, Se, Te)

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Anastasiya O. Solovieva,†,‡ Kaplan Kirakci,§ Anton A. Ivanov,†,∥ Pavel Kubát,⊥ Tatiana N. Pozmogova,‡,# Svetlana M. Miroshnichenko,‡ Elena V. Vorontsova,∇ Anton V. Chechushkov,† Kristina E. Trifonova,& Maria S. Fufaeva,† Evgeniy I. Kretov,$ Yuri V. Mironov,∥,# Alexander F. Poveshchenko,‡ Kamil Lang,*,§ and Michael A. Shestopalov*,†,‡,∥,# †

Research Institute of Experimental and Clinical Medicine, 2 Timakova st., 630117 Novosibirsk, Russian Federation Research Institute of Clinical and Experimental Lymphology−Branch of the ICG SB RAS, 2 Timakova st., 630060 Novosibirsk, Russian Federation § Institute of Inorganic Chemistry of the Czech Academy of Sciences, v.v.i., Husinec-Ř ež 1001, 250 68 Ř ež, Czech Republic ∥ Nikolaev Institute of Inorganic Chemistry SB RAS, 3, Acad. Lavrentiev Ave., Novosibirsk 630090, Russian Federation ⊥ J. Heyrovský Institute of Physical Chemistry of the Czech Academy of Sciences, v.v.i., Dolejškova 3, 182 23 Praha 8, Czech Republic # Novosibirsk State University, 2 Pirogova Str., Novosibirsk 630090, Russian Federation ∇ The Institute of Molecular Biology and Biophysics, 2/12 Timakova st., 630117 Novosibirsk, Russian Federation & The State Research Center of Virology and Biotechnology VECTOR, 630559 Koltsovo, Russian Federation $ Meshalkin Siberian Federal Biomedical Research Center, 15 Rechkunovskaya st., 630055 Novosibirsk, Russian Federation ‡

S Supporting Information *

ABSTRACT: Octahedral rhenium cluster complexes have recently emerged as relevant building blocks for the design of singlet oxygen photosensitizing materials toward biological applications such as blue-light photodynamic therapy. However, their singlet oxygen generation ability as well as biological properties have been studied only superficially. Herein we investigate in detail the singlet oxygen photogeneration, dark and photoinduced cytotoxicity, cellular uptake kinetics, cellular localization and in vitro photoinduced oxidative stress, and photodynamic cytotoxicity of the series of octahedral rhenium cluster complexes [{Re6Q8}(CN)6]4−, where Q = S, Se, Te. Our results demonstrate that the selenium-containing complex possesses optimal properties in terms of absorption and singlet oxygen productivity. These features coupled with the cellular internalization and low dark toxicity lead to the first photoinduced cytotoxic effect observed for a molecular [{M6Q8}L6] complex, making it a promising object for further study in terms of blue-light PDT.

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INTRODUCTION

The octahedral metal cluster complexes with general formula [{M6Q8}L6]n−, (M = Mo, W, Q = Cl, Br, I; M = Re, Q = S, Se, Te; L = apical organic or inorganic ligand) have recently emerged as relevant photosensitizers for blue-light PDT. Such clusters exhibit bright red luminescence that is efficiently quenched by oxygen to generate O2(1Δg) under UV/blue light irradiation (up to 500 nm).2−13 As opposed to commonly used organic photosensitizers such as porphyrins which lose their sensitizing activity upon aggregation, mostly due to π−π stacking interactions,14 the Mo6 complexes remain good O2(1Δg) sensitizers even in the solid state.15−17 Moreover, these complexes constitute versatile theranostic tools thanks to additional features such as high radiopacity,

The research of novel photosensitizers for generation of singlet oxygen, O2(1Δg), has attracted broad interest in the last decades for health-related applications, mainly the treatment of diseased tissue by photodynamic therapy. Indeed, this highly cytotoxic form of oxygen is generated by the interaction of molecular oxygen with the triplet states of a photosensitizer excited by visible light. Such a feature, coupled with the limited lifetime of O2(1Δg) in water, allow for a high selectivity in the killing of pathologic cells, as only the close vicinity of the zone containing the irradiated photosensitizer will be affected. In dermatology and cosmetology, blue-light photodynamic therapy (blue-light PDT) is a widely used method to treat actinic keratosis, basal cell carcinoma, squamous cell carcinoma, and acne using a photosensitizer activated by blue light.1 © 2017 American Chemical Society

Received: August 28, 2017 Published: October 9, 2017 13491

DOI: 10.1021/acs.inorgchem.7b02212 Inorg. Chem. 2017, 56, 13491−13499

Article

Inorganic Chemistry

laser. Bimolecular quenching rate constants, kO2, were evaluated using the Stern−Volmer equation, i.e., 1/τT = 1/τT0 + kO2[O2], and oxygen solubility in air-saturated water (0.28 mM), where τT and τT0 are triplet state lifetimes at the specific oxygen concentration [O2] and under oxygen-free conditions, respectively. The kinetics of O2(1Δg) luminescence was recorded at 1270 nm at the right angle to 425 nm laser pulses (FL3002 dye laser, pulse width ∼28 ns) using a homemade Ge detector. Decay traces recorded at 1270 nm were averaged (1000−5000 traces) to improve the signal to noise ratio. The initial parts of the signals were omitted to eliminate light scattering and luminescence of cluster complexes. In addition, all measurements were carried out in oxygen-saturated D2O, where the luminescence lifetimes of cluster complexes are quite short ( K4-3 indicate that cluster complexes quench O2(1Δg) themselves and that the effectiveness of this process increases in the series K4-1 < K4-2 < K4-3. On the basis of these data, K4-3 exhibits the most effective self-quenching effect. Using data presented in Table 1, we can qualitatively analyze ΦΔ values in physiological fluids such as the cell cytoplasm, not accessible by the direct measurements. The quantum yield of O2(1Δg) formation is given by the equation ΦΔ = ΦTFTSΔ, where ΦT is the quantum yield of triplet state formation, FT is the fraction of the triplet states quenched by oxygen under experimental conditions, i.e, oxygen trapping efficiency, and SΔ is the efficiency of O2(1Δg) formation during oxygen quenching of triplet states, which is not affected in solvents of very similar polarity.37 Thus, efficient solvent-mediated deactivation of the triplet states (low FT values) in air-saturated H2O in comparison to D2O indicates that the title cluster complexes have lower ΦΔ values in cells in comparison to those measured in D2O. Cell Viability, Proliferation, and Cellular Uptake. Two of the main requirements for photosensitizers are low toxicity and high phototoxicity. Thus, the cytotoxicity of the cluster complexes on three different cell linesnamely the two cancer cell lines human larynx carcinoma (Hep-2) and human epithelioid cervix carcinoma (HeLa) and the normal cell line fetal lung fibroblasts (MRC-5)was evaluated using the MTT colorimetric assay (Figure 2). In order to eliminate toxic effects of K+ ions and in order to minimize cation effect on the radiopacity of the compounds in CT-scan experiments the sodium salts of the cluster complexes were used. The cells were incubated with Na4-1 and Na4-2 within a wide concentration range from 3.9 to 1000 μM. The results show some variations in the half-maximal inhibitory concentration (IC50) depending on the cell lines (Table 2). The reported IC50

Figure 2. Effects of Na4[{Re6Q8}(CN)6] (Q = S, Se) on the viability of Hep-2, HeLa, and MRC-5 cells (determined using the MTT assay). Data are presented as mean ± SEM.

values for Na4-3 on Hep-2 and MRC-5 cells30 are presented for comparison. According to the results, the cytotoxicity depends on the chalcogen atoms in the cluster compounds and 13494


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dependent on the cluster core composition and increases in the order S < Se < Te. The study of the cellular internalization of the investigated cluster complexes was carried out using CLSM and TEM. According to CLSM imaging (Figure 4) of treated Hep-2 cells, we observed the red luminescence, and the Z-stack analysis (from 0 to 16 μm) (Figure S8 in the Supporting Information) revealed that this luminescence comes from inside the cells: namely, from the cell cytoplasm in a punctate manner. It should be noted that the luminescent intensity of the cells treated with Na4-2 is significantly higher than the intensity after the treatment with Na4-1 because of better uptake and higher brightness of emission of Na4-2 (Figure 4 and Figure S8). For a detailed definition of the subcellular localization within Hep-2 cells, the sample preparation for TEM images was carried out under conditions identical with those for the CLSM assay. TEM images of the cells incubated with Na4-2 show more contrast than the images of the cells incubated with Na4-1. This difference is in agreement with the better uptake of Na4-2 and with the fact that Na4-2 with heavier elements in the cluster core has higher electron density (Figures 5 and 6) and, as a consequence, higher electron beam attenuation. As shown in Figures 5 and 6, the mitochondria and heterochromatin of the cells treated with Na4-2 display significantly higher electron beam attenuation. The elemental analysis showed a homogeneous distribution of Na4-2 within these intracellular structures (Figure 5). These data indicate that Na4-2 has tropism to these structures. The cluster concentration in the nucleus is the highest near the nuclear membrane, suggesting the penetration of the cluster from the endoplasmic reticulum into the nuclear pores. Such localization

Table 2. Half-Maximal Inhibitory Concentration (IC50) of Cluster Complexes for Different Cell Linesa IC50, μM

a

cluster complex

Hep-2

HeLa

MRC-5

Na4-1 Na4-2 Na4-3b

417 ± 4 478 ± 8 721 ± 36

401 ± 7 410 ± 5

471 ± 13 551 ± 21 815 ± 41

Data are presented as mean ± SEM. bReference 30.

decreases in the series S > Se ≫ Te. Summing up, the cancer HeLa and Hep-2 cell lines appear less resistant to the cluster complexes than normal cells MRC-5. However, the differences are small and do not allow any discussion about selective toxicity between tumor and normal cells. In addition to the cytotoxicity evaluation, a quantitative analysis of the cellular uptake kinetic for Na4-1 and Na4-2 on Hep-2 cells was carried out using flow cytometry (FACS). Figure 3 displays the results as the proportion of luminescent events versus incubation time. The results document that the proportion of luminescent cells is negligible for Na4-1 after incubation for 15 min (5 ± 3%) whereas it reaches 30 ± 12% for Na4-2. After 30 min of incubation, the proportion of luminescent cells increased to 21 ± 9% (Na4-1) and 45 ± 10% (Na4-2). The maximum of accumulation was reached after 24 h and reached 61 ± 10 and 90 ± 10% for Na4-1 and Na4-2, respectively. Note that these parameters are 57 ± 7 (15 min), 79 ± 5 (30 min), and 97 ± 3% (24 h) for Na4-3.30 Thus, the analysis of cellular uptake kinetics for Hep-2 cells documents that the accumulation rate in cells is

Figure 3. Kinetics of Na4-1 and Na4-2 uptake by Hep-2 cells. Percentage of cells positive (top) and flow cytometry histogram (bottom) for Na4-1 and Na4-2 after 0.25, 0.5, 2, 8, and 24 h incubation. Error bars represent the standard error of the mean percentage of fluorescent positive cells. 13495


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Figure 4. Laser confocal microscopy images of Hep-2 cells incubated with Na4-1 and Na4-2 for 24 h (magnification ×100, λex = 405 nm).

Na4-3 are approximately 1.4 and 2.3 times more radiopaque than the sulfur derivate, Na4-1, respectively. Photodynamic Treatment on Hep-2 Cells. Since the title hexarhenium cluster complexes produce O2(1Δg) and are internalized by the cells, the evaluation of the photoinduced cytotoxicity of sodium salts Na4-1, Na4-2 ,and Na4-3 on Hep-2 cells was performed. First, we quantified the level of intracellular oxidative stress induced by cluster complexes in Hep-2 cells after photoirradiation using cell-permeable 5,6carboxy-2′,7′-dichlorofluorescein diacetate (DCFH-DA). This fluorescence probe is sensitive to oxidation by ROS, including O2(1Δg). The cells incubated in free media and with H2O2, i.e., an irradiation-independent ROS, as negative and positive controls, respectively, were investigated. In the presence of H2O2, the fluorescence intensity of DCFH-DA indicates a high ROS level, whereas the ROS level in the cells incubated in the free media is negligible both before and after irradiation (Figure 7). The cells incubated with Na4-1 and Na4-2 demonstrated bright green fluorescence after irradiation that is a clear indication of the ROS photoproduction. Comparison of mean fluorescence intensities shows that Na4-2 generates an approximately 3 times higher ROS level than Na4-1, whereas the photoproduction of ROS by Na4-3 is within the level of negative control (Figure 7). Such a difference between Na4-1 and Na4-2 can be related to more effective light absorption in the visible region (Figure 1) and more efficient accumulation of Na4-2 in the cells (Figure 6). The negligible generation of ROS by Na4-3, while having by far the best absorption properties in Na4-2 can be related to more effective light absorption in the visible region, can be correlated with the lowest ΦΔ and the most effective self-quenching of O2(1Δg) from the series.

Figure 5. TEM images of Hep-2 cells incubated with Na4-1 (left) and Na4-2 (right): white arrows, mitochondria; red arrows, heterochromatin (nucleus) (magnification ×8000).

indicates that Na4-2 (and presumably Na4-1) accumulates in the area with highest protein density. The same localization was proved for Na4-330 and other hexarhenium clusters.9,38,39 Because these cluster complexes are attractive contrast agents thanks to the heavy cluster core and the low dark toxicity, we assessed the effect of the composition on the radiopacity, by performing CT and angiography studies of H2O solutions of Na4-1−Na4-3 (Figure S9 and Table S1 in the Supporting Information). Figure S10 in the Supporting Information demonstrates the dependence of radiopacity in the Hounsfield unit scale vs concentration. The graphs evidence that, for all of the clusters studied, the radiopacity has a linear dependence on the concentration. The slope of the plot is a characteristic of the molar radiopacity and can be used to compare X-ray attenuations of different compounds. Evidently, Na4-2 and 13496


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Figure 6. TEM images of Hep-2 cells incubated with Na4-1 (A) and Na4-2 (B): asterisk, mitochondria; arrows, heterochromatin (nucleus) (magnification ×12000). Elemental analysis indicates the subcellular localization of Re atoms.

< 0.01). These are the first molecular complexes of the general formula [{M6Q8}L6]n− with photocytotoxic effects that make them promising for further study in terms of blue-light PDT.

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CONCLUSIONS

In the context of blue-light PDT, we investigated the singlet oxygen production and biological activity of the hexarhenium cluster complexes [{Re6Q8}(CN)6]4−, where Q = S, Se, Te. Even when they have low luminescence quantum yields, the studied complexes exhibit singlet oxygen productivity comparable to that of commonly used photosensitizers (0.22 < ΦΔ < 0.59 in D2O). The complex with tellurium as inner ligands displays the most advantageous light absorption in the visible region; however, a low fraction of the triplet states quenched by oxygen leading to a lower ΦΔ value and efficient self-quenching of O2(1Δg) seem to be detrimental to the overall photosensitizing activity of this cluster complex. On the other hand, the complex with selenium inner ligands appears to have optimal properties in terms of absorption and O2(1Δg) productivity. These findings are reflected in the oxidative stress and photocytotoxic effects on Hep-2 cells, which are the most preeminent for the complex with selenium inner ligands, while the complex with sulfur showed a somewhat lower activity and the complex with tellurium did not provide any measurable effect. It worth noting that the last two complexes are unique among other M6 cluster-based molecular photosensitizers due to the phototoxic effect on tumor cells. These results make these complexes relevant objects for further studies on their use for blue-light PDT.

Figure 7. Detection and quantification of ROS levels induced by Na41, Na4-2, and Na4-3 on Hep-2 cells before (black columns) and after (blue columns) photoirradiation, respectively. Data represent the mean DCF fluorescence intensity ± SD.

Second, we evaluated the in vitro photodynamic toxicity of cluster complexes toward Hep-2 cells. Hep-2 cells were treated with Na4-1, Na4-2, and Na4-3 in the concentration range 12.5− 100 μM: i.e., using concentrations with negligible dark cellular toxicity (Figure 2). Both treated cells and untreated control cells were then irradiated with a 500 W halogen lamp (λ ≥400 nm) (Figure 8). According to our data, Na4-1 and Na4-2 are moderately phototoxic toward Hep-2 cells, whereas Na4-3 did not show any phototoxicity (Figure 8). Note that Na4-2 is more phototoxic than Na4-1. Thus, the cell viability after the treatment with 50 μM Na4-1 and irradiation was 87 ± 9% (94 ± 9.7% without irradiation, p ≥ 0.01), but Na4-2 reduced the cell viability up to 77 ± 6.3% (95 ± 7.5% without irradiation, p < 0.01). A much more significant effect can be achieved after the treatment with 100 μM Na4-2 (63 ± 1.5% vs. 90 ± 0.4% without irradiation, p 13497


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Inorganic Chemistry ORCID

Kaplan Kirakci: 0000-0002-1068-5133 Anton A. Ivanov: 0000-0003-2026-8568 Pavel Kubát: 0000-0002-7861-9212 Yuri V. Mironov: 0000-0002-8559-3313 Kamil Lang: 0000-0002-4151-8805 Michael A. Shestopalov: 0000-0001-9833-6060 Funding

This work was supported by the Russian Science Foundation (Grant Number 15-15-10006) and by the Czech Science Foundation (No. 16-15020S). Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work involved the use of equipment from the MultiAccess Center “Proteomics” of the Institute of Molecular Biology and Biophysics (Novosibirsk, Russia) and Multi-Access Center “Modern optical systems” of the Institute of Clinical and Experimental Medicine (Novosibirsk, Russia).

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Figure 8. In vitro photodynamic toxicity of Na4-1−Na4-3.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.inorgchem.7b02212. Luminescence decay curves, transient absorption decay curves, Stern−Volmer analysis of the triplet state quenching, Z-stacked image of Hep-2 cells incubated with Na4[{Re6Q8}(CN)6] (Q = S, Se) by confocal fluorescence microscopy, X-ray computed tomography and angiography images, and radiopacity of aqueous solutions (PDF)

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REFERENCES

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AUTHOR INFORMATION

Corresponding Authors

*E-mail for K.L.: [email protected]. *E-mail for M.A.S.: [email protected]. 13498


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