Generation of Singlet Oxygen by Photoexcited Au25(SR)18 Clusters

Article pubs.acs.org/cm

Generation of Singlet Oxygen by Photoexcited Au25(SR)18 Clusters Hideya Kawasaki,*,†,‡ Santosh Kumar,† Gao Li,† Chenjie Zeng,† Douglas R. Kauffman,§ Junya Yoshimoto,‡ Yasuhiko Iwasaki,‡ and Rongchao Jin*,† †

Department of Chemistry, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213, United States Department of Chemistry and Materials Engineering, Faculty of Chemistry, Materials and Bioengineering, Kansai University, 3-3-35 Yamate-cho, Suita-shi, Osaka 564-8680, Japan § National Energy Technology Laboratory (NETL), United States Department of Energy, Pittsburgh, Pennsylvania 15236, United States ‡

S Supporting Information *

ABSTRACT: The generation of highly reactive singlet oxygen (1O2) is of major importance for a variety of applications such as photodynamic therapy (PDT) for cancer treatment, water treatment, catalytic oxidation, and others. Herein, we demonstrate that 1O2 can be efficiently produced through the direct photosensitization by Au25(SR)18− clusters (H−SR = phenylethanethiol or captopril) without using conventional organic photosensitizers under visible/near-IR (532, 650, and 808 nm) irradiation. 1O2 was successfully detected by direct observation of the characteristic 1O2 emission around 1276 nm as well as three different 1 O 2 -selective probes. Water-soluble Au25(captopril)18− clusters were explored for cytocompatibility and photodynamic activity toward cancer cells. In addition, selective catalytic oxidation of organic sulfide to sulfoxide by 1O2 was demonstrated on the photoexcited Au25(SC2H4Ph)18− clusters. It is suggested that the optical gap of Au25(SR)18 clusters (∼1.3 eV) being larger than the energy of 1O2 (0.97 eV) allows for the efficient energy transfer to 3O2. In addition, the long lifetime of the electronic excited states of Au25(SR)18 and the well-defined O2 adsorption sites are the key factors that promote energy transfer from Au25(SR)18− to molecular oxygen, thus facilitating the formation of 1O2. Finally, neutral Au25(SR)180 can also produce 1O2 as efficiently as does the anionic Au25(SR)18−. superoxide and hydroxyl radicals. The type II pathway for 1O2 generation involves energy transfer during a collision between the excited photosensitizer and triplet oxygen. In addition to the traditional organic dyes that have been used as 1O2 photosensitizers, the potential role of nanomaterials has also been reported by several research groups. Such nanomaterials include semiconductor quantum dots (QDs),15−17 silicon nanocrystals,18 fullerene C60,19,20 metal nanoparticles,21−24 and QDs conjugated with aromatic photosensitizers.25,26 Some of the reported photosensitizers have several drawbacks, including poor water solubility, low selectivity, skin toxicity, and instability. The triplet structure of the excitons in photosensitizers is necessary for energy transfer from the exciton to molecular oxygen in order to generate 1O2. However, in direct band gap semiconductors, owing to a small singlet−triplet splitting energy, the lifetime of the exciton at room temperature is on the nanosecond time scale,27 whereas for effective 1O2 production, the exciton needs to have a lifetime of at least a microsecond.1−10

1. INTRODUCTION Reactive oxygen species (ROS) are chemically reactive molecules containing oxygen, such as singlet oxygen (1O2) or superoxide (O2−).1−13 The generation of highly reactive 1O2 is of major importance for a variety of applications such as photodynamic therapy (PDT) for cancer treatment, water treatment, catalytic oxidation, and others. The transition from oxygen in the ground state to one of the excited 1O2 states requires a change in the electron spin state (spin-flip process), but the direct conversion of spin states via absorption/emission of photons is spin-forbidden in the first approximation. To solve this problem and to facilitate direct photoexcitation, several assistant agents, termed photosensitizers, are commonly used for the photomediated production of 1O2.1−8,11−13 These photosensitizers are generally composed of strongly absorbing organic dye molecules such as porphyrin. The development of such photosensitizers for the production of highly reactive 1O2 is a key step in the advancement of PDT for effective cancer treatment, water treatment, and catalytic oxidation. There are two main photochemical reactions by which ROS are generated from photosensitizers, type I and type II,14 although care should be taken with their definitions.6 The type I pathway involves electron transfer between an excited sensitizer and a substrate, yielding a variety of oxygen free radicals, such as © 2014 American Chemical Society

Received: September 5, 2013 Revised: April 4, 2014 Published: April 22, 2014 2777

dx.doi.org/10.1021/cm500260z | Chem. Mater. 2014, 26, 2777−2788

Chemistry of Materials

Article

In this article, we demonstrate that 1O2 can be formed through direct sensitization under visible/near-IR (532, 650, and 808 nm) irradiation by organic-soluble Au25(PET)18− and water-soluble Au25(Capt)18− (Capt = captopril) without the presence of any organic photosensitizers. 1O2 was successfully detected by direct observation of 1O2 emission as well as using three different selective probes, and subsequent 1O2 quenching was demonstrated using an efficient scavenger (histidine). In particular, 1O2 production by water-soluble Au25 clusters under near-IR photoexcitation at 808 nm, within the biological optical window, is very attractive for PDT applications. Water-soluble Au25(Capt)18− is explored for cytocompatibility and photodynamic activity toward cancer cells, whereas organic-soluble Au25(PET)18− is demonstrated for use in the selective catalytic oxidation of sulfide to sulfoxide by 1O2 generation. The 1O2 production mechanism by Au25(SR)18− clusters is discussed on the basis of the electric structure of Au25(SR)18−, its long lifetime of the electronic excited states, and its well-defined O2 adsorption sites.

In recent years, atomically precise thiolate-protected gold clusters (denoted as Aun(SR)m, where SR refers to thiolate) have progressed considerably in solution-phase synthesis.28−30 A number of atomically precise Aun(SR)m clusters have been reported, such as Au20(SR)16,31 Au24(SR)20,32 Au25(SR)18,33−35 Au 3 6 (SR) 2 4 , 3 6 , 3 7 Au 3 8 (SR) 2 4 , 3 8 − 4 0 Au 4 0 (SR) 2 4 , 4 1 , 4 2 Au55(SR)31,43 Au67(SR)35,44 Au102(SR)44,45−47 Au130(SR)50,48 Au144(SR)60,36,49,50 and others. It is expected that they will be a promising new approach to the generation of 1O2. The atomically precise Aun(SR)m clusters have a precise atomic level composition, and their synthesis is relatively simple and inexpensive. Their surface can provide water solubility and good biocompatibility by the use of hydrophilic ligands such as peptides,51,52 and target specificity can be achieved via their surface modification. The Aun(SR)m clusters have the potential for their electronic structure to be optimized for efficient production of 1O2, as their size can be modified by varying the values of n and m.31−50 In spite of the promise of atomically precise Aun(SR)m clusters as 1O2 photosensitizers, little research has been carried out on exploitation of Aun(SR)m clusters for 1 O2 production. Apart from atomically precise Aun(SR)m, there are a few reports involving 1O2 production using bovine serum albumin (BSA)-stabilized Au clusters at a UV excitation of 330 nm53 and different-sized Au clusters embedded in a polymer film at a visible excitation of 532 nm.54 However, their 1O2 production efficiency was very low (e.g., quantum yield of 1O2 generation of ∼0.0154), and 1O2 generation at near-IR (NIR) excitation has not been achieved previously in metal cluster systems. The purpose of the present study is to examine the capability of Au25(SR)18− clusters to generate 1O2 by photoexcitation. The Au25(SR)18− cluster is the most thoroughly investigated cluster among various Aun(SR)m,28,29 and its crystal structure, 3 4 , 5 5 electronic properties, 3 4 catalytic properties,56,57magnetism,58 optical properties,34,51 and thermal stability52 have all been reported. Compared to other Aun(SR)m clusters, Au25(SR)18− seems to be an ideal candidate for use as an efficient photosensitizer for 1O2 production owing to its high stability,33,59 the presence of triplet excited states,60 and the long lifetime of the electronic excited states (on the order of a microsecond).60−62 The well-defined O2 adsorption sites should encourage energy transfer from Au25(SR)18− to molecular oxygen63 and thus facilitate the formation of 1O2. In addition, for bio-applications of clusters effective elimination from the body has been previously demonstrated for Au25(SG)18 (H−SG = glutathione), where 94% of the Au could be metabolized for renal clearance.64 Finally, Au25(SR)18− clusters show two regions of strong absorption: more energetic peaks at UV−vis wavelengths shorter than 500 nm and absorbance in the NIR region between 700 and 900 nm. The NIR absorbance is highly advantageous for optimal penetration of light deep into human tissue for PDT applications. More recently, we have reported the visible-light photocatalytic properties of a composite material consisting of Au25(PET)18 clusters (PET = phenylethanethiolate) and TiO2 nanocrystals,65 where the generated hydroxyl radicals (HO•) and 1O2 are proposed to be responsible for the decomposition of the dye. However, TiO2 nanoparticles were reported to be able to sensitize the formation of 1O2.66 Therefore, the 1O2 production of Au25(SR)18− clusters only (i.e., without TiO2) should be investigated. In addition, direct evidence of 1O2 production by 1O2 luminescence was not confirmed in the previous study.

2. MATERIALS AND METHODS 2.1. Chemicals. All of the chemicals were used as received without further purification. Tetrachloroauric(III) acid (HAuCl4·3H2O, 99.99%), 2-phenylethanethiol (PET, 99%), sodium borohydride (NaBH4, 99.99%), 3,3′-diaminobenzidine (DAB, >99%), 1,3-diphenylisobenzofuran (DPBF, 97%), L-ascorbic acid (>98%), glutathione (HSG, 98%), L-histidine (>99%), methylphenyl sulfide (99%), toluene (HPLC grade, 99.9%), ethanol (HPLC grade), tetrahydrofuran (THF, HPLC grade), carbon tetrachloride (99.9%), acetone (>99.5%), acetonitrile (ACN, HPLC grade, 99%), dichlorom ethane (HPLC grade, 99.9%), chloroform (CCl3, HPLC grade, 99%, containing amylenes), dimethylformamide (DMF; 99.8%), and human serum (sera human) were purchased from Sigma-Aldrich. Tetraoctylammonium bromide (TOAB, >98%) was obtained from Fluka. 9,10Dimethylanthracene was purchased from TCI Japan, Inc. New methylene blue (NMB) was purchased from TCI America, Inc. Nanopure water (resistivity 18.2 MΩ cm) was obtained using a Barnstead NANOpure DI water system. Heavy water (D2O, 99.9%) was purchased from Cambridge Isotope Laboratories Inc. 2.2. Synthesis of Aun(SR)m. 2.2.1. Au25(PET)18−. Au25(PET)18− clusters were synthesized according to a literature procedure.33,67 Briefly, HAuCl4·3H2O (80 mg, 0.203 mmol), TOAB (129 mg, 0.235 mmol), and THF (15 mL) were mixed in a 50 mL three-necked flask. After vigorous stirring for 15 min, PET (140 μL, 1.02 mmol, Au/S = 1:5) was injected into the solution using a syringe. Over a period of 90 min, the color of the solution changed from orange to transparent. Subsequently, NaBH4 (77 mg, 2.03 mmol, Au/NaBH4 = 1:10) was freshly dissolved in cold water (5 mL) and then rapidly poured into the reaction solution under vigorous stirring. The mixture was stirred for a further 8 h. The final product was dried in a rotary vacuum evaporator at room temperature. The dried black oil-like clusters were precipitated by adding methanol (∼15 mL) and were then washed with fresh methanol and collected by centrifugation. Acetonitrile (15 mL) was then added to extract the pure Au25(PET)18−TOA+ clusters from the black precipitate. Hereafter, the Au25(PET)18−TOA+ clusters are designated Au25(PET)18−. 2.2.2. Au38(PET)240. Au38(PET)240 clusters were synthesized according to the acetone-mediated synthesis previously described in the literature.40 Briefly, the Aun(SG)m starting material was prepared in acetone followed by conversion of the size mixed Aun(SG)m clusters into monodisperse Au38(PET)240 via thermal etching. Au38(PET)240 clusters were separated from the black precipitate by extraction with dichloromethane/methanol (1:1 v/v). 2.2.3. Au25(Capt)18−. The synthesis of Au25(Capt)18− was done at room temperature in air according to the synthesis previously described in the literature.52 The synthetic scheme is shown in Supporting Information Figure S1. Typically, HAuCl4·3H2O (0.20 2778



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mmol, 78.7 mg) and TOAB (0.23 mmol, 126.8 mg) were first dissolved in 10 mL of methanol and vigorously stirred for 20 min. The solution color changed from yellow−orange to deep red. After 20 min, captopril (1 mmol, 217.2 mg) was dissolved in 5 mL of methanol and rapidly injected in the reaction mixture, which was further stirred for 30 min. The solution color quickly changed to white. After 30 min, NaBH4 (2 mmol, 75.6 mg) was dissolved in 5 mL of ice-cold water and rapidly added under vigorous stirring of the reaction mixture. The solution color immediately changed to brown−black. The reaction was further run for 8 h, and then the reaction mixture was centrifuged to remove insoluble Au(I) polymer. The supernatant was collected and further concentrated by rotary evaporation and then precipitated by adding ethanol. The precipitate was extracted several times with minimum amounts of methanol, and then the extracted clusters were finally precipitated by ethanol and dried in vacuum. 2.3. UV−Vis Absorption and Fluorescence Spectroscopy. UV−vis spectra were acquired using a Hewlett-Packard (HP) Agilent 8453 diode array spectrophotometer at room temperature. Fluorescence spectra (99.5 >99.5 87

trace trace trace 13

a Reaction conditions: 50 μmol of phenyl methyl sulfide, 2 mL of CHCl3, 0.2 μmol of Au25(PET)18 cluster catalyst (0.4 mol %). bThe conversion of sulfide and selectivity for sulfoxide was determined by NMR (Supporting Information Figure S12). NMR data have a quantification error of about 3% of the values of the conversion and selectivity. cIt is difficult to determine the selectivity by NMR, as the conversion was too low. dThe data (solvent: dichloromethane, 40 °C, 12 h) was cited from ref 98. PhIO = iodosylbenzene.

Au25(PET)18− is presented as a reference in Supporting Information Figures S6, showing no changes in DPBF absorbance under light irradiation at 532 nm for 1 h. Substantially smaller DPBF optical changes were observed in the absence of O2 (Supporting Information Figures S7), further indicating that optical changes were caused by 1O2 production in the presence of Au25(PET)18−. It was also found that the spectrum of DPBF in a DMF solution of Au25(PET)18− after 60 min of irradiation is almost consistent with that of Au25(PET)18− in the absence of DPBF before light irradiation (red line in Figure 5a). This indicates that Au25(PET)18− clusters are stable during 1O2 generation. It should be noted that a lower irradiation power (∼0.2 mW/ cm2, 1 mW) was used to slow the 1O2 production process for the convenience of UV−vis monitoring for 30 min in Figure 5a, in contrast with the 50 mW green light (34 mW/cm2) used in Figures 1 and 2. Actually, the disappearance of DPBF absorbance using the 50 mW green light was very fast: nearly 5 min (Figure S8). There is a possibility that DPBF is undergoing thermal degradation resulting from the photothermal effect of Au25(PET)18− during light irradiation because of the thermal instability of DPBF.87 However, it is unlikely that DPBF degradation is attributed only to the photothermal effect because using ascorbic acid as the 1O2 scavenger suppressed the oxidation of DPBF (Figure S9),88 supporting the conclusion that the 1O2 species generated by Au25(PET)18− contributed to the oxidation of DPBF. In addition, we also confirmed spectroscopic 1O2 detection for Au25(PET)18− in DMF using another specific 1O2 dye, 9,10-dimethylanthracene (DMA), which is thermally stable (Figure S10).89 3.4. Detection of 1 O 2 Phosphorescence for Au25(PET)18−. During the relaxation, the electronic excitation energy of 1O2 is converted into the vibrational energy of the ground state of O2 and the surrounding solvent molecules. Solvents composed of low-energy oscillators such as C−F and C−Cl act as poor quenchers in terms of energy transfer, whereas those with high-energy oscillators such as O−H and C−H are strong quenchers. As a result, the 1O2 phosphorescence should be stronger in a solvent that provides 1O2 with a longer lifetime.74,75 Carbon tetrachloride is a molecule that fulfills these conditions. The 1O2 lifetime in CCl4 is about 900−

26 000 μs,90,91 which is about 4 orders of magnitude longer than its lifetime in water. Figure 6 shows the photoluminescence of Au25(PET)18− in N2-purged (black curve) and O2-saturated (red curve) CCl4. 1 O2 photoluminescence (PL) was detected in O2-saturated solutions of Au25(PET)18− dissolved in CCl4 (Figure 6a). The PL difference spectrum (ΔPL) indicates a peak from 1O2 PL at ∼1276 nm. The photoluminescence was not detected in airsaturated solutions because the 1O2 concentration and/or photoluminescence intensity was too low. The presence of the 1 O2 signal was reversible and reproducible, as tested by repeated N2-purging and O2-saturation cycles (Figure 6b and Supporting Information Figure S11). The spectroscopic detection of 1276 nm PL in the presence of O2 provides strong, direct evidence for 1O2 production by Au25(PET)18−. 3.5. Catalytic Oxidation of Sulfide to Sulfoxide by 1O2 over Photoexcited Au25(PET)18−. Selective oxidation of sulfides to sulfoxides is an important organic transformation because the resulting sulfoxides are versatile intermediates for the preparation of biologically and medicinally important products.92 The main side reaction of sulfoxidation is the formation of sulfone. Therefore, synthetic methods for mild and selective oxidation of sulfides to sulfoxides that minimize the production of sulfones and side reactions are highly desirable from both synthetic and mechanistic points of view. Many methods have been developed to achieve selective sulfoxidation in the use of oxidants.93 However, the oxidants used are toxic, resulting in the production of toxic waste as well as the need to separate the oxidants. Thus, a sulfoxidation process using molecular oxygen as the oxidant would be more advantageous over methods using other oxidants. Herein, we utilize the singlet oxygen from photoexcited Au25(PET)18− and demonstrate a highly selective, green sulfoxidation process. The results are shown in Table 1. In the first round of catalyst evaluation, a solution of thioanisole was added into the Au25(PET)18− catalyst solution. The reactions were carried out in open vessels in the dark with O2 bubbling, where almost no sulfoxidation of sulfides was observed at 25 and 55 °C (Table 1, entries 1 and 2). With the assistance of photoexcited Au25(PET)18− at 532 nm, Au25(PET)18− exhibited selective catalytic oxidation of sulfides to sulfoxides even with a small amount of catalyst (0.4 mol%) (Table 1, entry 5). The 2784



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sulfoxides would be enhanced on the surface of Au25(PET)18− because the sulfide is likely adsorbed onto the pocket sites of Au25(SR)18,98 leading to a greater probability of interaction among 1O2, the intermediate of sulfide, and another sulfide molecule. The detailed mechanism of sulfoxidation by 1O2 in the presence of photoexcited Au25(PET)18− is the topic of further study. 3.6. Comparison of Au25(PET)18− and Au38(PET)240 for 1 O2 Production. Aun(SR)m clusters have a size-dependent electronic structure,29 which may affect the efficiency of 1O2 production. In this study, we examined the efficiency of 1O2 production by Au38(PET)240 in comparison to Au25(PET)18−. Au38(PET)240 clusters have a core diameter of 1.4 nm and a HOMO−LUMO gap energy of 0.9 eV.38−40,99 Au25(PET)18− clusters have a core diameter of 1.27 nm and a HOMO− LUMO gap energy of 1.3 eV. Figure 7 shows the absorption spectra of a DAB-containing solution of Au38(PET)240 in DMF. Interestingly, the change in absorbance was extremely small, indicating that this Au38 species was much less effective for the generation of 1O2 (Figure 7b). An effective photosensitizer for 1O2 production requires a high triplet-state yield with a triplet-state energy (ΔEt) larger than the energy of 1O2 (0.97 eV) for efficient energy transfer to 3 O2.8 From this viewpoint, the HOMO−LUMO optical gap of Au25(SR)18 is ∼1.3 eV, and it has a high triplet-state efficiency (86.6%). As a result, photoexcited Au25(SR)18 can donate enough energy to convert 3O2 into 1O2. Conversely, the optical gap of Au38(PET)240 is only ∼0.9 eV and therefore it cannot donate enough energy to form 1O2. In addition, the long lifetime of the electronic excited states (on the order of a microsecond)60,61 and the well-defined O2 adsorption sites63 can be key factors to promote energy transfer from Au25(SR)18− to molecular oxygen, thus facilitating the formation of 1O2. Of note, the 532 nm photoexcitation pumps the electron from the HOMO to LUMO + n in both the Au25(PET)18− and Au38(PET)240 clusters, but those higher excited states (i.e., LUMO + n) have very short lifetimes (on the order of picoseconds) and are not good at enabling energy transfer to oxygen, whereas the LUMO level has a relatively long lifetime (e.g., on the order of a microsecond) and can thus contribute to 1 O2 production. Taken together, our results highlight how discrete, quantized energy levels influence the chemistry of atomically precise Au clusters.

conversion increased with higher reaction temperatures or longer reaction times (Table 1, entries 3−5). The most striking result is that ∼100% selectivity was achieved in the sulfoxidation of sulfides, in contrast to the use of other oxidants such as PhIO (87%, Table 1, entry 6). To evaluate the catalytic oxidation efficiency at different wavelengths of photoexcitation, we also examined the catalytic oxidation of sulfides to sulfoxides by 1O2 in the presence of Au25(PET)18− upon 532, 650, and 808 nm photoexcitation, as shown in Table 2. Nearly 100% selectivity was achieved in the sulfoxidation of Table 2. Oxidation of Sulfides Using Photoexcited Au25(PET)18− Catalyst at Different Wavelengths of Photoexcitationa selectivity (%)b entry oxidant 1 2 3

1

O2 1 O2 1 O2

catalyst

conversion (%)b

sulfoxide

sulfone

Au25(SR)18 (532 nm) Au25(SR)18 (650 nm) Au25(SR)18 (808 nm)

4 12 10

>99.5 >99.5 >99.5

trace trace trace

a Reaction conditions: 50 μmol of phenyl methyl sulfide, 2 mL of CHCl3, 0.2 μmol of Au25(PET)18 cluster catalyst (0.4 mol %), 25 °C, 3 h. bThe conversion and selectivity were determined by NMR. NMR data have a quantification error of about 3% of the values.

sulfide irrespective of the excitation wavelength, and the conversion was the largest for photoexcited Au25(PET)18− upon 650 nm photoexcitation, which is very close to the absorbance at the HOMO−LUMO peak of Au25(PET)18−. This indicates the excellent photocatalytic performance of Au25(PET)18− for a highly selective sulfoxidation process, which is likely due to the 1O2 production over photoexcited Au25(PET)18−. Photosensitized sulfoxidation is generally accepted to occur via two main mechanisms in aprotic solvents: (i) singlet oxygen oxidation through an energy transfer and (ii) a radical pathway through electron transfer.94−97 In the former case (i.e., 1O2 photosulfoxidation), the oxidation pathway of sulfides to sulfoxides involves the reaction of an intermediate (S-hydroperoxysulfonium) with another sulfide molecule, but there is a possibility that the intermediate can be rearranged to a sulfone, forming fragmentation products. According to this mechanism, the reaction of the intermediate with another sulfide molecule is the key for the selective oxidation of sulfides to sulfoxides. Such an oxidation pathway of sulfides to

Figure 7. (a) Absorption spectra of a DAB-containing solution of Au38(PET)240 in DMF after light irradiation at 532 nm (50 mW) for 30 min. [Au38] = 30 μM, [DAB] = 500 μM. (b) Change in absorbance at 445 nm of a DAB-containing DMF solution of Au25(PET)18− (black) and Au38(PET)240 (red) after light irradiation at 532 nm (50 mW) for 30 min. [Au38]= [Au25] = 30 μM, [DAB] = 500 μM. 2785



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production efficiency for Au25(Capt)18− clusters compared to that of NMB was observed. Water-soluble Au25(Capt)18− clusters were explored to evaluate the cytocompatibility and photodynamic activity of Au25(Capt)18− toward cancer cells. It was also found that Au25(PET)18− clusters exhibited a highly selective 1O2 sulfoxidation process mediated by photoexcited Au25(PET)18−. The quantity of 1O2 generated was dependent on the size of clusters; Au38(PET)240 clusters were found to be less effective for the generation of 1O2 in comparison to Au25(PET)18−. It is suggested that the optical gap of Au25(SR)18 clusters (∼1.3 eV), which is larger than the energy of 1O2 (0.97 eV), allows for efficient energy transfer to 3O2. In addition, the long lifetime of the electronic excitations and the well-defined O2 adsorption sites are the key factors to promote energy transfer from Au25(SR)18− to molecular oxygen, thus facilitating the formation of 1 O 2 . In future work, water-soluble Au25(Capt)18− clusters conjugated with biomolecules will be investigated for their potential use in targeting, imaging, and PDT applications, whereas the organic-soluble Au25(PET)18− clusters show promise for use as heterogeneous 1O2 catalysts for chemical processes.

It has been reported that Au clusters can display a high photoluminescence yield of up to 0.7, for example, polyamidoamine−Au clusters.100 Au clusters with a high photoluminescence yield could show a low 1O2 generation yield because less energy from the excited Au clusters is available for transfer to triplet oxygen. In the case of the Au25(SR)18 clusters, it has been reported that Au25(SR)18 clusters show a relatively low photoluminescence yield of 0.0001−0.002.61 Furthermore, it has also been reported that the high quantum efficiency of triplet formation was 86.6% at 690 nm for Au25 clusters.101 The relatively low photoluminescence yield and the high quantum efficiency of triplet formation for Au25 clusters can result in enhanced 1O2 production. In a previous report by Russell and co-workers, they prepared phthalocyanine(photosensitizer)-stabilized gold nanoparticles with particle sizes between 2 and 4 nm.102 TOAB, which was used during the synthesis of these gold nanoparticles, was adsorbed on the surface and made the nanoparticles soluble in polar solvents. The three-component (photosensitizer/gold/ TOAB) nanoparticles were shown to generate 1O2 with enhanced quantum yields of ∼50% compared to free phthalocyanine. It was suggested that the enhanced quantum yield was attributed to the TOAB reagent, which affects the excited singlet state of phthalocyanine as well as the triplet energy transfer to molecular oxygen to form 1O2. In the present study, both the anionic Au25 clusters (protected by PET or Capt) have the TOA+ cation stabilizing the anionic clusters. However, it is unlikely that the presence of the TOA+ cation affects the 1O2-generation process in this case because nonionic Au25(PET)180 clusters without the TOA+ cation showed comparable 1O2 production as that by Au25(Capt)18− TOA+, as shown in Supporting Information Figures S13. Finally, we comment on the relationship between our present result and the previously reported oxidation of Au25(PET)18− to Au25(PET)180.63 In the present experiments for 1O2 formation (i.e., photoirradiation at 532 nm for 1 h under an air atmosphere), we did not observe the oxidation of Au25(SR)18− to Au25(SR)180 (where SR = PET, Capt), which was evidenced by the UV−vis spectra of the clusters being identical to that of the initial anionic Au25(SR)18− state. However, using a pure O2 saturation of the cluster solution may result in the oxidation of Au25(SR)18− to Au25(SR)180. It should also be noted that the photoluminescence intensity of the O2saturated Au25(Capt)18− solution was reduced to approximately 30% of the N2-purged solution and that the Au25(Capt)18− became oxidized under light illumination in the presence of pure O2 (Supporting Information Figure S2a). These results are similar to our previous findings for Au25(PET)18− in DMF.63 However, the quenching of Au25(Capt)18− photoluminescence in the presence of O2 was not attributed to the oxidation of Au25 (Capt) 18 − to Au 25(Capt)180 because the oxidation increased the photoluminescence intensity.63 The origins of the O2-dependent quenching of Au25(Capt)18− photoluminescence may be ascribed to a mechanism involving transient nonradiative energy transfer from the photoexcited Au25(Capt)18− to the adsorbed O2 molecule, resulting 1O2 formation.

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ASSOCIATED CONTENT

S Supporting Information *

Synthetic scheme of Au25(Capt)18−; NIR photoluminescence and absorbance spectra of Au25(Capt)18− in a D2O solution; absorption spectra of a DAB-containing solution of Au25(Capt)18− in D2O under a N2 gas atmosphere before and after irradiation; absorption spectra of Au25(Capt)18− in human serum containing DAB before and after irradiation; absorption spectra of DPBF in a DMF solution before and after irradiation; fluorescence spectra of a DPBF-containing solution of Au25(PET)18− in DMF under a N2 atmosphere before and after irradiation; photographs of a DPBF-containing DMF solution in the absence of Au25(PET)18−; fluorescence spectra of a DMA-containing solution of Au25(PET)18− in DMF under an air atmosphere before and after irradiation; photoluminescence spectra of Au25(PET)18− in CCl4 after several N2-purging and O2-saturation cycles; 1H NMR of sulfide, sulfoxide, and sulfone; absorption spectra of Au25(PET) 18−TOA+ and Au25(PET)180; and normalized fluorescence intensity of DPBF in a DMF solution containing Au25(PET)18−TOA+ and Au25(PET)180 after irradiation. This material is available free of charge via the Internet at http:// pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Authors

*(H.K.) E-mail: [email protected]. *(R.J.) E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This research was partly supported by Kansai University’s Overseas Research Program for 2012 and by Grants-in-Aid for Scientific Research (nos. 23360361, 23655074, and 22350040) from the Japan Society for the Promotion of Science (JSPS) (to H.K.). R.J. thanks support from the U.S. Department of Energy, Office of Basic Energy Sciences, grant no. DE-FG0212ER16354. Y.I. thanks MEXT, Japan for a Grant-in-Aid for

4. CONCLUSIONS We have shown that organic-soluble Au25(PET)18− and watersoluble Au25(Capt)18− clusters efficiently generate 1O2 under visible/NIR (532, 650, and 808 nm) irradiation in the absence of organic photosensitizers. In human serum, a superior 1O2 2786



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Scientific Research on Innovative Areas “Nanomedicine Molecular Science” (no. 24107524).

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