ZnO Core-shell Nanoparticles as Nano-photosensitizers

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Au Nanorod/ZnO Core-shell Nanoparticles as Nano-photosensitizers for Near-Infrared Light Induced Singlet Oxygen Generation Na Zhou, Hai Zhu, Shuang Li, Jing Yang, Taolin Zhao, Yanting Li, and Qing-Hua Xu J. Phys. Chem. C, Just Accepted Manuscript • DOI: 10.1021/acs.jpcc.7b12463 • Publication Date (Web): 20 Mar 2018 Downloaded from http://pubs.acs.org on March 21, 2018

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The Journal of Physical Chemistry

Au Nanorod/ZnO Core-shell Nanoparticles as Nano-photosensitizers for Near-Infrared Light Induced Singlet Oxygen Generation Na Zhou, †,‡ Hai Zhu, ‡ Shuang Li, ‡ Jing Yang, ∥ Taolin Zhao, † Yanting Li † and Qing-Hua Xu‡,§* †

School of Materials Science and Engineering, Hebei Provincial Key Laboratory of Traffic

Engineering Materials, Shijiazhuang Tiedao University, Shijiazhuang 050043, China ‡

Department of Chemistry, National University of Singapore, 3 Science Drive 3, Singapore

117543 ∥

Institute of Materials Research and Engineering, Agency for Science, Technology and

Research, Singapore 117602 §

National University of Singapore (Suzhou) Research Institute, Suzhou 215123, China

ABSTRACT

Photosensitizer is the key element for photodynamic therapy (PDT) to generate singlet oxygen to generate cytotoxic effects to cancerous or diseased tissues. Conventional organic photosensitizers generally suffer from poor photo-stability. Nano-photosensitizers generally display high resistance to photo-degradation. However, high toxicity of quantum dots and

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requirement of UV light activation for ZnO and TiO2 limit their practical applications. Here we developed AuNR/ZnO core-shell nanostructures that integrate Au nanorods (NRs) with ZnO to act as near-infrared light activated photosensitizers. The core-shell nanostructure helps to avoid direct contact of Au NRs with cells to reduce their cytotoxicity. These AuNR/ZnO core-shell NPs were found to display effective singlet oxygen generation under continuous wave nearinfrared light irradiation. AuNR/ZnO nanoparticles with thicker ZnO shell were found to display higher singlet oxygen generation efficiency. The mechanism of single oxygen generation by these AuNR/ZnO NPs was ascribed to injection of near-infrared light excited hot electrons of Au NRs into the conduction band of ZnO. The injected electrons were subsequently scavenged by oxygen molecules to form superoxide radicals O2-•, which can be further oxidized by the holes on Au NRs to form singlet oxygen. The proposed mechanism has been confirmed by ultrafast transient absorption and pump probe measurements. These AuNR/ZnO core-shell nanoparticles are promising nano-photosensitizers for near-infrared activated photodynamic therapy.

INTRODUCTION

Photodynamic therapy (PDT) is a non-invasive cancer therapy technique that combines photosensitizers, oxygen and light to generate cytotoxic effects to cancerous or diseased tissues.12

Photosensitizers can be activated by using light of appropriate wavelengths to produce reactive

oxygen species (ROS) such as singlet oxygen (1O2),3-5 which is highly oxidative and can react with many biological molecules.1, 6 Different types of photosensitizers such as rose bengal,7-8 porphyrins derivatives,2, 9-10 and transition metal complexes11-13 have been explored for singlet oxygen (1O2) generation.14 However, their practical applications in PDT have been hindered by their poor photo-stability.14


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Nanomaterials such as quantum dots (QDs),15-16 ZnO,17 Si,18 and TiO219-20 have been proposed to act as nano-photosensitizers due to their high resistance to photo-degradation. The singlet oxygen generation mechanism of semiconductor nanoparticles (NPs) have been previously studied by Nosaka et al.19, 21 Upon absorption of light, electrons are promoted onto the conduction band and holes are left on the valance band. Electrons on the conduction band interact with O2 to produce O2-• radicals, which are subsequently oxidized by the holes on the valance band to yield 1O2.22 However, some nano-photosensitizers display drawbacks such as high toxicity of QDs and requirement of UV light activation such as ZnO and TiO2, which are detrimental to healthy tissues. Practical PDT applications prefer the use of light in the nearInfrared (IR) region (700-1000 nm), which is coincident with the biological transparency window to render deep penetration into the tissues.2, 23-24 Near-IR light activated photosensitizers with high photo-stability and low toxicity are highly demanded for effective PDT. Metal NPs such as Au and Pt were recently combined with semiconductors for singlet oxygen generation, in which metal NPs absorb light in the visible range. So far a few published reports are limited to spherical metal-semiconductor nanostructures.25-26 To develop photo-stable and near-IR light activated nano-photosensitizers, Au nanorods (NRs) is a good candidate to combine with semiconductors due to their tunable longitudinal surface plasmon resonance (SPR) band from visible to near-IR range by controlling their aspect ratios.27 Although Au NRs alone have been reported to display singlet oxygen generation capability under two-photon excitation due to their large two-photon absorption cross sections,28 two-photon excitation requires expensive femtosecond laser system. The singlet oxygen generation efficiency of Au NRs under onephoton excitation using low-cost conventional continuous wave lasers is still quite low.


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ZnO is a widely used semiconductor with band gap of 3.2 eV. It has been recently reported to display singlet oxygen generation under UV light irradiation.29 Spherical metal NPs such as Au, Ag and Pd have been combined with ZnO to form hybrid nanostructures to significantly improve their singlet oxygen generation efficiency.30-32 In these studies, enhanced singlet oxygen generation capability was mainly ascribed to deposition of Au onto ZnO to increases charge separation and transport efficiency upon UV light excitation of ZnO NPs. Combination of Au NRs and ZnO can extend the excitation wavelength to near-IR range to allow deep penetration and even in vivo applications. To develop highly efficient one-photon excitation near-IR light activated photosensitizers, AuNR/ZnO core-shell nanostructures were designed to study their singlet oxygen generation capabilities. The core-shell structure helps to avoid the direct contact of Au NRs and cell to reduce their cytotoxicity. Ultrafast spectroscopy studies have been further performed to understand their singlet oxygen generation mechanisms. EXPERIMENTAL METHODS Chemicals and Materials. Hexadecyltrimethylammoniumbromide (CTAB, 98%), sodium borohydride (NaBH4, 99%), 9, 10-anthracenediyl-bis(methylene) dimalonic acid (ABDA), zinc nitrate (Zn(NO3)2•6H2O), hexamethylenetetramine (HMT), gold(III) chloride trihydrate (HAuCl4•3H2O, 99.9%), and polyethylene glycol sorbitan monolaurate (Tween20) were purchased from Sigma-Aldrich. Silver nitrate (AgNO3) and L- (+) -ascorbic acid (AA) were purchased from Alfa Aesar. De-ionized water was used in all the experiments. Preparation of AuNR/ZnO. Au NRs were prepared by using a seed-mediated growth method.27 The detailed procedures were described in the supporting information. AuNR/ZnO core-shell NPs were prepared by hydrolysis the Zn2+ precursor in basic environment.33 Briefly,


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24 mM of CTAB, 12 mM of AA, 24 mM of freshly prepared Zn(NO3)2 and 24 mM of HMT were gently mixed by the volume ratio of 1:1:1:1, which acted as the growth solution. 4.0 mL of CTAB stabilized Au NRs were washed twice with deionized water by centrifuge before adding 12.0 mL of growth solution into different amounts of Au NRs in a glass bottle. The pH value of the obtained mixture was adjusted to 9.0 using NaOH (0.1 M). The mixture was then placed in an 80 oC oven and kept undisturbed for 6 h. Finally, the prepared AuNR/ZnO NPs were washed with deionised water and re-dispersed in 4.0 mL of ethanol. AuNR/ZnO NPs with different ZnO shell thickness (28.7±1.6 nm, 38.4±3.3 nm, 45.5±3.5 nm, 54.5±2.3 nm and 63.1±3.7 nm) were prepared by adjusting the relative amount of Au NRs (from 6 to 2 mL) and growth solution (12 mL). The volumes of obtained AuNR/ZnO NPs were adjusted to the same volumes as that of Au NRs used in the original synthesis, so as to maintain the same number of AuNR/ZnO NPs per millilitre for each sample. Detection of singlet oxygen generation. Singlet oxygen generation was evaluated by monitoring chemical oxidation of ABDA. ABDA can react irreversibly with singlet oxygen and result in a decrease in ABDA absorption.34 0.2 mL of AuNR/ZnO NPs in ethanol was centrifuged and re-dispersed in 0.2 mL of Tween20 (0.1 wt%). Tween20 helps to disperse AuNR/ZnO NPs in water without affecting their singlet oxygen generation capability.35 0.2 mL of AuNR/ZnO NPs and 1.8 mL of ABDA solution with absorbance of ~0.2 were mixed in a quartz cuvette. The mixture was purged with O2 for 2 min before the cuvette was sealed. The mixture was then irradiated by the output of a Ti:sapphire oscillator in the continuous wave (CW) mode. The laser wavelength with the power density of 0.1 W/cm2 (beam diameter of 8 mm) was tuned to match the longitudinal SPR band maximum of the AuNR/ZnO NPs. AuNR/ZnO


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NPs with different ZnO shell thickness. The absorption spectra of the solution were recorded every 15 min using a Hitachi UH5300 UV-Vis spectrometer. Instruments. UV-vis extinction spectra were measured using a Hitachi UH5300 UV-vis spectrometer. Transmission electron microscopy (TEM) images were taken on a JEOL 1220 electron microscope. Time-resolved transient absorption and pump-probe measurements were performed using the output laser pulses of a Ti:sapphire oscillator seeded regenerative amplifier system (Spectra Physics Spitfire Pro).36 The output of a Ti:sapphire oscillator operating in the continuous wave (CW) mode (Avesta Ti-Saphire TiF-100M) was utilized as the illumination light source for singlet oxygen generation. RESULTS AND DISCUSSION TEM images and extinction spectra of Au NRs and AuNR/ZnO core-shell NPs with different shell thicknesses are shown in Figure 1. Au NRs have averaged length and diameter of 69.9±4.5 nm and 19.7±2.1 nm with an aspect ratio of 3.55. The extinction spectrum of Au NRs in H2O solution displayed two bands at 512 and 792 nm, corresponding to their transverse and longitudinal SPR modes, respectively.37 AuNR/ZnO NPs with different ZnO shell thickness were prepared by using different amounts of Zinc precursor during the coating process. TEM images confirmed the successful formation of uniform ZnO coating with averaged shell thicknesses of 28.7±1.6 nm, 38.4±3.3 nm, 45.5±3.5 nm, 54.5±2.3 nm and 63.1±3.7 nm, respectively (Figure 1b-f). The samples were later referred as AuNR/ZnO-n, where n is the ZnO average shell thickness. The obtained sample was named AuNR/ZnO-29, AuNR/ZnO-38, AuNR/ZnO-46, AuNR/ZnO-55 and AuNR/ZnO-63, respectively. UV-vis extinction spectra of AuNR/ZnO NPs displayed redshifted longitudinal SPR bands with respect to that of Au NRs (Figure 1g). The


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extent of redshift steadily increased with the increasing shell thickness. The observed redshift can be ascribed to an overall increase in the refractive index of the dielectric environment surrounding the Au NRs upon ZnO coating.38 In addition, the intensity ratios between the transverse and longitudinal SPR modes increased with the increasing ZnO shell thickness. This is primarily due to increased absorption in the short wavelength range upon formation of ZnO shell, partially due to more dramatic rise in the scattering intensity for the transverse mode than for the longitudinal mode.39 X-ray diffraction (XRD) pattern of AuNR/ZnO-63 NPs (Figure S1) shows only the peaks of Au, indicating amorphous nature of the ZnO shell. The amorphous structure of the ZnO shells allows exposure of the metal cores to their surrounding environments.

Figure 1. TEM images (a-f) and extinction spectra (g) of Au NRs (a) and AuNR/ZnO core-shell NPs with different ZnO shell thicknesses: 28.7±1.6 nm (b), 38.4±3.3 nm (c), 45.5±3.5 nm (d), 54.5±2.3 nm (e) and 63.1±3.7 nm (f). Singlet oxygen generation capability of AuNR/ZnO NPs under CW laser irradiation was evaluated by a chemical method using 9, 10-anthracenediyl-bis(methylene) dimalonic acid (ABDA) as the singlet oxygen probe. ABDA can react irreversibly with singlet oxygen to yield an endoperoxide, causing decreased ABDA absorption at 380 nm. The change in absorbance of


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ABDA at 380 nm in the presence of photosensitizers could be utilized to evaluate the capability of singlet oxygen generation. For direct comparison, singlet oxygen generation efficiencies of different AuNR/ZnO NPs were evaluated by using the same number of nanoparticles by adjusting their concentrations to be identical to that of the original Au NRs used for ZnO shell coating. The irradiation laser wavelength was tuned to the corresponding absorption maximum: 805, 825, 835, 848 and 860 nm for AuNR/ZnO-29, AuNR/ZnO-38, AuNR/ZnO-46, AuNR/ZnO55 and AuNR/ZnO-63 NPs, respectively. Effective singlet oxygen generation in the presence of different nano-photosensitizers was manifested by the steady decrease of ABDA absorption under CW laser illumination (Figure 2). Figure 2a shows the evolution of absorption spectra of ABDA in presence of AuNR/ZnO-29 NPs under CW laser illumination at 805 nm (0.1 W/cm2) for 75 min. Figure 2a inset shows the change in the absorbance of ABDA with different irradiation time, which was obtained by subtracting the extinction at 380 nm of AuNR/ZnO-29 NPs from that of the mixture solution (ABDA + AuNR/ZnO-29 NPs). It needs to be noted that a slight blueshift (100 ps), which persisted for a long time before decaying back with a long time scale beyond our measurement window. The observation of this long-lived transient species is a direct evidence of hot electron injection from the excited Au NRs to ZnO shell. Electron transfer from Au NRs to ZnO shell can also be confirmed by faster decay of the single wavelength dynamics probed at 770 nm of AuNR/ZnO-63 NPs compared to that in Au NRs. The corresponding electron transfer rate (τET) can be estimated to be 10.7 ps by comparing the single wavelength dynamics of Au NRs and AuNR/ZnO-63 NPs according to ଵ ఛಲೠಿೃ/ೋ೙ೀ

−ఛ

ଵ ಲೠಿೃ

ଵ ఛಶ೅

=

, where τAuNR/ZnO and τAuNR is the fast decay component obtained from fitting of

the curves in Figure 3c. The obtained electron transfer time constants (Table S1) are consistent with other reports on Au NR interacting with other molecules or materials.28. The influence of ZnO shell thickness on electron transfer rate was investigated by comparing the single wavelength decay dynamics (pump 800 nm/probe 770 nm) of AuNR/ZnO-29 and AuNR/ZnO63 NPs (Figure S10 and Table S2). The bleaching recovery dynamics of both ZnO coated Au NRs samples displayed faster decay than that of uncoated Au NRs due to hot electron injection, which gives electron transfer time of ~17.5 ps and ~10.7 ps for sample AuNR/ZnO-29 NPs and AuNR/ZnO-63 NPs, respectively. The samples with thicker ZnO shell (AuNR/ZnO-63 NPs) displayed faster electron transfer dynamics and consequently larger charge separation efficiency than the samples with thinner ZnO shell (AuNR/ZnO-29 NPs), which contribute partially to the results that AuNR/ZnO NPs with thickest ZnO shell give most efficient singlet oxygen generation.


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CONCLUSIONS AuNR/ZnO core-shell nanostructures with varied thickness of ZnO shell have been prepared by controlling the ratio of growth solution and Au NRs. These core-shell NPs have been further utilized as nano-photosensitizers for singlet oxygen generation. It was found that AuNR/ZnO NPs displayed much higher singlet oxygen generation efficiency than Au NRs or ZnO NPs alone under CW laser irradiation in the near-IR range. AuNR/ZnO NPs with thicker ZnO shell were found to display higher singlet oxygen generation efficiency. The mechanism of single oxygen generation by AuNR/ZnO NPs is believed due to injection of near-IR light excited hot electrons of Au NRs into the conduction band of ZnO. The injected electrons are further scavenged by oxygen molecules to form superoxide radicals O2-•, which can be further oxidized by hole on Au NRs to form singlet oxygen. The proposed mechanism has been further confirmed by ultrafast transient absorption and pump probe measurements. These AuNR/ZnO core-shell NPs are promising candidate as nano-photosensitizers for near-IR activated photodynamic therapy.

ASSOCIATED CONTENT Supporting Information The following files are available free of charge. Preparation of Gold Nanorods (Au NRs), XRD data and TEM images of some samples, photodegradation of ABDA in the presence of AuNR/ZnO-46 NPs under different purge environment, plots of ln(C0/C) as the function of time, irradiation laser wavelength dependent photodegradation of ABDA in the presence of AuNR/ZnO-29 NPs, computational details, band


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structure of Au-ZnO contact, surface density normalized rate coefficient, schematic illustration of hot electron injection from Au NR to ZnO, single wavelength dynamics and fitting results of Au NRs, AuNR/ZnO-29 and AuNR/ZnO-63 NPs. AUTHOR INFORMATION Corresponding Author *Email: [email protected]. ORCID Qing-Hua Xu: 0000-0002-4153-0767

ACKNOWLEDGMENT This work was supported by NUS AcRF Tier 1 grant (grant number R-143-000-607-112) and the National Natural Science Foundation of China (21673155 and 21603151), Natural Science Foundation of Hebei Province (B2016210111 and B2018210090) and Natural Science Foundation of Hebei Education Department (QN2016118 and ZD2015082). REFERENCES 1.

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ZnO Core-shell Nanoparticles as Nano-photosensitizers

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