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Environmental Aspects of Nanotechnology

Circular dichroism-active interactions between fipronil and neuronal cells xiuxiu wang, Liguang Xu, Changlong Hao, Chuanlai Xu, and Hua Kuang Environ. Sci. Technol. Lett., Just Accepted Manuscript • DOI: 10.1021/acs.estlett.8b00321 • Publication Date (Web): 18 Jul 2018 Downloaded from http://pubs.acs.org on July 19, 2018

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Environmental Science & Technology Letters

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Circular Dichroism-Active Interactions between Fipronil and Neuronal Cells

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Xiuxiu Wang1,2,3, Liguang Xu1,2,3, Changlong Hao1,2,3, Chuanlai Xu1,2,3* , Hua Kuang1,2,3*

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1

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214122, People’s Republic of China

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2

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Science and Technology, Jiangnan University, Wuxi, Jiangsu, 214122, People’s Republic of

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China

State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu,

International Joint Research Laboratory for Biointerface and Biodetection and School of Food

10

3

11

Jiangnan University, Wuxi, Jiangsu, 214122, People’s Republic of China

Collaborative Innovation center of Food Safety and Quality Control in Jiangsu Province,

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*Corresponding author

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Chuanlai Xu

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Telephone: 86-0510-85329076

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Email: [email protected], [email protected]

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1 ACS Paragon Plus Environment


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ABSTRACT

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Chemicals exert harmful effects on target species and cause DNA damage after

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exposure. Here, Au-Ag heterodimers have been fabricated with conjugated molecules such as

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DNA, cell-penetrating peptide and thiolated polyethylene glycol to investigate the intracellular

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interactions between fipronil and neuron cells. The hybridized heterodimer nanoparticles (NPs)

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show a strong plasmonic circular dichroism (CD) signal and were used for the intracellular

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detection of fipronil-induced 8-hydroxy-2′-deoxyguanosine (8-OHdG). And, the limit of

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detection for 8-OHdG was as low as 0.1 nM. More importantly, 8-OHdG could be visualized in

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cells with in situ cell imaging based on luminescence quenching via energy transfer. This method

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has been applied to measure the oxidative DNA damage caused by nonylphenol and alternariol in

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cells. All our results suggest that our chiroplasmonic platform is a promising and applicable

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method not only for detecting the 8-OHdG induced by fipronil in cells but also for assessing the

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capacity of chemicals to induce intracellular oxidative DNA damage.

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INTRODUCTION

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Fipronil, a phenylpyrazole insecticide, is widely used in agriculture, sanitation and

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combatting domestic pests. After entering the environment, fipronil exerts many harmful

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effects.1–3 It acts as a noncompetitive antagonist of the γ-aminobutyric acid receptor, blocking

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chloride channels, and is more toxic for insects than for mammals because of its target-site

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specificity.4,5 Because fipronil has broad applications, its persistence and transformation has

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drawn much attention.3,6,7 Notably, fipronil exerts harmful effects on nontarget species,8,9 and

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DNA damage has been observed after exposure to fipronil,10,11 which was banned to be used in

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agriculture by European Union12,13. However, little is known about the oxidative damage induced

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in DNA by fipronil.

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8-OHdG is an important biomarker of oxidative stress (such as DNA damage and

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carcinogenesis) and one of the predominant products of oxidative DNA lesions14,15 and has been

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considered a biomarker of many diseases, including hepatocellular carcinoma,16 cardiovascular

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disease,17 and major depression.18 A variety of methods have been established to quantify

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8-OHdG, including liquid chromatography–tandem mass spectrometry,19 enzyme-linked

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immunosorbent assay (ELISA),14 fluorescent aptasensors,20 and cyclic voltammetry21.

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Both the experimental and theoretical aspects of chiral nanostructures have attracted

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increasing attention in recent years.22–26 The wide use of chiral nanostructures in both

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extracellular buffers and complex biological media is attributable to their uncomplicated

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preparation, wide range of components, and intense chiroplasmonic responses.24,27-30 Recently,

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our group has developed various chiral nanostructures and evaluated them with cell imaging and

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highly sensitive detection.31–34

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Chiral assemblies can be constructed based on DNA hybridization33,35 and



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antibody-antigen recognition.24,36,37 Here, a chiral Au–Ag heterodimer was constructed with a

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conjugated DNA-driven assembly. After the dimer structure formation with conjugated

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Au-DNA1 and Ag-DNA2 NPs linked by DNA3, a strong plasmonic circular dichroism (CD)

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signal at~526 and 405 nm was observed, and the fluorescent signal from Cy5 was quenched by

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the metallic nanoparticles (Figure S5C). The plasmonic CD response allowed the Au–Ag

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heterodimer to be used as a chiral biosensor of fipronil-induced 8-OHdG. The intracellular

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bioimaging of 8-OHdG was also achieved with recovery of Cy5 fluorescence that occurred in the

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presence of 8-OHdG. Thus, we not only detected extracellular 8-OHdG but also established a

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platform with which to evaluate the intracellular oxidative DNA damage caused by other

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environmental contaminants.

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MATERIALS AND METHODS

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Measurement of 8-OHdG Induced by Fipronil in Cells. NG108 cells were cultured for

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12 h in six-well culture plates with (initially) 1.0 × 105 cells well-1 before they were exposed to

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0.05, 0.2, 2, 10, or 50 µM fipronil or to 0.1% methyl alcohol (MeOH) for 24 h. The culture

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medium was then removed, and the cells were incubated with new culture medium containing

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the heterodimer (8 nM) for another 8 h. The cells were washed twice with ice-cold

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phosphate-buffered saline (PBS), harvested and re-suspended in 200 µL of ice-cold PBS. The

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CD and fluorescence spectra of the dimer were measured in the cells.

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Confocal Fluorescence Microscopic Imaging of Fipronil-Induced 8-OHdG in Cells.

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All cellular fluorescent images were obtained with a confocal microscope with laser excitation.

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The heterodimer modified with Cy5 was excited at 638 nm. NG108 cells were seeded in 35-mm

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glass-bottomed culture dishes with 200 µL of culture medium containing fipronil (0.05, 0.2, 2,


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10, or 50 µM) or 0.1% MeOH and incubated for 24, 48, or 72 h. New culture medium (200 µL)

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containing 8 nM dimer was then added to the cells, which were then incubated for another 8 h.

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The cells were washed twice with ice-cold PBS (0.1 M, pH 7.4) to remove any residual probe.

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RESULTS AND DISCUSSION

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Characterization of Chiral Heterodimers. The principle underlying the strategy in this

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study is illustrated in Figure 1A and 1B. The Au–Ag heterodimer was constructed with DNA

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hybridization. To prepare the Au–Ag dimer, AuNPs (20 ± 5 nm) and AgNPs (15 ± 5 nm) were

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first

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(5′-SH-TTTCTGTCCCACCCCCTGGCA-3′)

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(5′-CAGAGCGCACGCACCCCTTT-SH-3′), respectively. The Au–Ag dimer then formed after

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the addition of DNA3, an aptamer of 8-OHdG38. The heterodimer produced displayed strong

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chiroptical activity (Figure S5B), which was attributed to the formation of a dihedral angle in the

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nanostructure.24 In the presence of 8-OHdG, the Au-DNA1+DNA3+DNA2-Ag was

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disassembled into individual Au-DNA1 NPs and Ag-DNA2 NPs in response to the affinity

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between the aptamer and 8-OHdG being stronger than that between the aptamer and the

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complementary sequences.39 DNA3 modified with the fluorochrome Cy5 was simultaneously

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released into the solution, restoring the fluorescent signal. Thus, we could quantify the level of

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8-OHdG using the CD signal and fluorescence intensity. This sensing platform is suitable for the

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intracellular detection of 8-OHdG and was used to assess a potentially harmful compound

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formed during DNA damage.

prepared

(Figure

S1)

and

modified

with

chemical and

attachment

of

DNA1 DNA2

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The transmission electron microscopy (TEM), ultraviolet–visible (UV–vis) spectra

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(Figure S2A), and DLS (Figure S3) results indicated good uniformity and dispersity of the NPs.



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Representative TEM images showed the progress of self-assembly at different times, from 0 to

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48 h (Figure S5A); during this time, the yield of heterodimer increased from 1% to 82%

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(Figures S5B and S6). The dimer displayed distinct CD signals at 405 nm and 526 nm, which

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corresponded to the plasmon resonance of the AgNPs and AuNPs, respectively (Figure S2). The

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CD response increased with the assembly time and remained stable at 24 h (Figure S7). As

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expected, the individual NPs displayed no CD signal (Figure S2B and S2C). Conversely, the

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fluorescence intensity at 670 nm decreased as the assembly process progressed (Figures S5C

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and S8) because the fluorescence of Cy5 was quenched by the formation of the heterodimer.22

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However, the corresponding UV–vis spectrum (Figure S9) could not display the significant

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change. Note that limit of detection (LOD) (3σ/slope) for 8-OHdG detection was 0.032 and

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0.064 nM using CD and fluorescence signals, respectively, which displayed much more

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sensitivity than most reported technologies. 2,38,40–43 (Figures S10-S15)

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Cellular Uptake of the Heterodimer. To investigate the fipronil cytotoxicity to neurons,

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neuroblastomaxglioma hybrid cell line (NG108 cells), as a common neuronal model, was chosen

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for further study. As results shown in CD, fluorescence and UV–vis spectra and TEM images

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(Figure S16-S19), the probe showed good structural stability in culture medium.

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cytotoxicity of the hybridized heterodimer NP was estimated with the Cell Counting Kit-8. After

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NG108 cells were treated with 8 nM hybridized heterodimer NP for 12 h, they showed 95.36%

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viability (Figures S20 and S21). The high stability and low cytotoxicity of the hybridized

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heterodimer NP make its intracellular application possible.

The

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To monitor the dynamics of the chiral hybridized heterodimer NP in cells, both the CD

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and fluorescent spectra were recorded after different time incubation. The intracellular CD signal


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was time-dependent and reached a plateau after 8 h incubation (Figure 1C and 1D). These

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dynamics indicate that the hybridized heterodimer NP showed highly efficient internalization

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with the assistance of TAT43,44 and reached saturation after 8 h. The fluorescent response showed

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no significant change during the entire incubation period but remained stable for 8 h (Figure 1E

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and 1F), demonstrating the high specificity and excellent stability of the probe in cells. All these

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results indicate that 8 h is the optimal time for the cellular uptake of the hybridized heterodimer

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NP and that this probe displayed high dispersion and excellent stability.



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Figure 1. (A) Hybridized heterodimer NP for 8-OHdG detection. (B) Schematic representation

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of intracellular detection of 8-OHdG with interactions with fipronil. (C-F) Time course of

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spectrum of NG108 cells incubated with culture medium containing hybridized heterodimer NP.

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(C, E) Intracellular CD and fluorescence signals during a series of culture times (0, 2, 4, 6, 8, 12

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and 24 h). (D) Statistics of the absolute value of the CD intensity at wavelengths of 526 nm and

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405 nm and of the ∆CD (∆CD = CD526nm-CD405nm). (F) Corresponding fluorescence intensity

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changes at 670 nm.

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Fipronil Induced 8-OHdG in NG108 Cells. To establish a method for evaluating the

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oxidative DNA damage induced by fipronil, the effect of time on cell viability was first

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investigated. As expected, NG108 cells incubated with increasing concentrations of fipronil

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always exhibited remarkably higher cellular activity at 24 h than at 48 h or 72 h (Figure 2A).

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Normal cellular activity may be an essential factor for the subsequent use of the hybridized

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heterodimer NP probe.

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After incubation for 24 h, even with only 0.05 µM fipronil, the 8-OHdG concentration in

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the cells differed significantly from that in the MeOH-treated cells (Figure 2B and S22). The

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concentration of 8-OHdG was also significantly higher in these cells than in the control group

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after exposure for 48 and 72 h. These results demonstrate that fipronil dose-dependently induces

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the generation of 8-OHdG in NG108 cells.

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Because fipronil induces the production of 8-OHdG in cells, the corresponding CD and

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fluorescent signals from the hybridized heterodimer NP were observed in cells. First, NG108

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cells were exposed to 10 µM fipronil for different times (0, 2, 4, 8, 12, 24, or 48 h), and the

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hybridized heterodimer NP was then added to the culture medium, which was incubated for

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another 8 h. The UV–vis spectra of the cells showed that the amount of hybridized heterodimer

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NP entering each cell was almost constant (Figure S23). Confocal images of the NG 108 cells



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showed visible differences after incubation with 10 µM fipronil for 8 h (Figure 2C). Moreover,

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the corresponding CD (Figure 2D) and fluorescence spectra (Figure 2E) were in good

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agreement with the confocal results, both showing distinct changes in the signal after 8 h of

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incubation. These results confirm that fipronil-induced intracellular 8-OHdG triggered the

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dissociation of the hybridized heterodimer NP probe and that the corresponding optical response

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was the same as that in the extracellular model. Therefore, the feasibility of our scheme was

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verified. The relative cell viability and corresponding optical signal at 24 h resulted in this

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duration being selected as the best incubation period for NG108 cells and fipronil.

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Figure 2. Fipronil induced 8-OHdG in NG108 cells. (A) NG108 cell viability when cultured

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with different concentrations of added fipronil (0.05, 0.2, 2, 10 and 50 µM) at 24, 48 and 72 h; 11 ACS Paragon Plus Environment


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cell viability was measured by CCK-8 at 24-h intervals. For nucleus staining, 200 µL of 50

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µg/mL DAPI was added into 2 mL cells for incubating 10 min. (B) Dose and time effects of

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fipronil on DNA oxidative damage in NG108 cells; an asterisk (*) indicates significance at the p

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≤0.05 level. (C) Confocal images, CD spectra (D) and fluorescence intensity (E) of NG108 cells

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exposed to 10 µM fipronil for 0, 2, 4, 8, 12, 24, and 48 h. The scale bar indicates 50 µm.

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Intracellular Detection of 8-OHdG. To develop an intracellular 8-OHdG detection

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strategy, NG108 cells were exposed to different concentrations of fipronil (0.05, 0.2, 2, 10, or 50

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µM) for 24 h and then incubated with the hybridized heterodimer NP for another 8 h. As

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expected, confocal images (Figure 3A) showed that the intensity of the red fluorescence (Cy5)

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increased as the concentration of fipronil increased, which is consistent with the results shown in

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Figure 2B, displaying that fipronil dose-dependently induced 8-OHdG in NG108 cells. To

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evaluate of specificity of this probe, NG108 cells were incubated with the heterodimer (linked to

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DNA4) after their exposure to fipronil (Figure S24). There was no fluorescent signal,

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demonstrating that this probe has excellent specificity in cells.

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The changes in the CD and fluorescence signals were consistent with the confocal images

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(Figure 3B and 3D). The CD and fluorescence intensities showed a linear relationship with the

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8-OHdG concentration in a detection range of 0.532–5.061 nM (Figure 3C and 3E). The LOD

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was calculated to be 0.1 nM for the CD signal and 0.3 nM for the fluorescent signal, indicating

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that the CD signal is the more sensitive tool for detecting 8-OHdG. We also estimated the

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fluorescence intensity from confocal images (Figure S25-S26).

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These results demonstrate that we have successfully established, for the first time, a

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probe for the intracellular detection and bioimaging of fipronil-induced 8-OHdG. How does

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fipronil induce 8-OHdG formation in cells? Based on previous research in Sf9, S2 (insect cell


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line), and human neuroblastoma cells (SH-SY5Y),9,10,45 we hypothesize that the induction of

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8-OHdG by fipronil in NG108 cells is associated with cell apoptosis. Therefore, NG108 cells

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incubated with different concentrations of fipronil were stained with annexin V-FITC/PI and

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analyzed with flow cytometry. Cell apoptosis increased as the concentration of fipronil increased

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(Figure 3F).



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Figure 3. Effect of fipronil concentration on NG108 cells in the presence of hybridized

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heterodimer NPs. (A) Confocal images of NG108 cells after exposure to various concentrations

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of fipronil (0.05-50 µM) or 0.1% MeOH for 48 h. The scale bar indicates 50 µm. (B, D) CD and

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fluorescence spectra of NG108 cells treated with 50, 10, 2, 0.2, or 0.05 µM fipronil or 0.1%

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MeOH. (C, E) Calibration curve for intracellular 8-OHdG detection based on the CD signal and

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the fluorescence intensity at 670 nm. (F) NG108 cells incubated with (a) 0, (b) 0.05, (c) 2, or (d)

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50 µM fipronil were stained with recombinant fluorescein isothiocyanate-conjugated annexin V

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and propidium iodide (Annexin V-FITC/PI) and analyzed by ﬂow cytometry.

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Effects of Nonylphenol and Alternariol on NG108 Cells. Many poisonous and harmful

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substances are present in the environment.46 Therefore, we verified that our system is suitable for

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the analysis of other compounds. Nonylphenol is a widespread toxic endocrine disrupter,47 and

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alternariol is an important contaminant of food.48 We incubated NG108 cells with nonylphenol or

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alternariol and observed their harmful effects. As shown in Figure 4A, cells treated with 10 µM

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nonylphenol or alternariol showed brighter fluorescence than the control cells, suggesting that

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both compounds induced intracellular 8-OHdG. The CD and fluorescent signals supported the

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results in the confocal images (Figure 4B and 4C). The 8-OHdG concentration was measured

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with a calibration curve (Figure 3C), and the concentrations of 8-OHdG induced by nonylphenol

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and alternariol were 4.72 ± 0.19 and 3.87 ± 0.21 nM, respectively. This assessment is the first of

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the induction of 8-OHdG by nonylphenol and alternariol in NG108 cells. These results indicate

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that the strategy proposed in this study, based on the use of a chiral assembly, has wide utility in

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the evaluation of intracellular 8-OHdG induced by exogenous compounds.



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Figure 4. Effect of nonylphenol and alternariol (AOH) in NG108 cells. (A) Confocal images, (B)

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CD absorption and (C) fluorescence intensity of NG108 cells after incubation with 10 µM

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alternariol or nonylphenol or with 0.1% DMSO. The scale bar indicates 50 µm.

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ASSOCIATED CONTENT

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Supporting Information Available


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The Supporting Information is available free of charge on the ACS Publications website at DOI:

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10.1021/*******.

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Information as mentioned in the text. (PDF)

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AUTHOR INFORMATION

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Corresponding Author

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*E-mail: [email protected], [email protected]

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ORCID

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Chuanlai Xu: 0000-0002-5639-7102

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Notes

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The authors declare no competing financial interest.

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ACKNOWLEDGMENTS

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This work is financially supported by the National Natural Science Foundation of China (grant

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nos. 21471068 and 21371081).

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For Table of Contents Use Only

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Circular Dichroism-Active Interactions between Fipronil and Neuron Cells

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Xiuxiu Wang1,2,3, Liguang Xu1,2,3, Changlong Hao1,2,3, Chuanlai Xu1,2,3*, Hua Kuang1,2,3*

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Science and Technology, Jiangnan University, Wuxi, Jiangsu, 214122, People’s Republic of

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China

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3

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Jiangnan University, Wuxi, Jiangsu, 214122, People’s Republic of China

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Email: [email protected], [email protected]


International Joint Research Laboratory for Biointerface and Biodetection and School of Food

Collaborative Innovation center of Food Safety and Quality Control in Jiangsu Province,

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1 Circular Dichroism-Active Interactions between ... - ACS Publications

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