Circular dichroism-active interactions between ... - ACS Publications

Subscriber access provided by UNIV OF DURHAM

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

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 26

Environmental Science & Technology Letters

1

Circular Dichroism-Active Interactions between Fipronil and Neuronal Cells

2 3

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

4 5

1

6

214122, People’s Republic of China

7

2

8

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

9

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,

12 13 14

*Corresponding author

15

Chuanlai Xu

16


17


18

Telephone: 86-0510-85329076

19

Email: [email protected], [email protected]

20

1 ACS Paragon Plus Environment


21

ABSTRACT

22

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

23

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

24

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

25

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

26

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

27

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

28

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

29

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

30

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

31

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

32

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

33

capacity of chemicals to induce intracellular oxidative DNA damage.

34


Page 2 of 26

Page 3 of 26

35


INTRODUCTION

36

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

37

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

38

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

39

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

40

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

41

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

42

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

43

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

44

in DNA by fipronil.

45

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

46

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

47

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

48

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

49

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

50

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

51

Both the experimental and theoretical aspects of chiral nanostructures have attracted

52

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

53

extracellular buffers and complex biological media is attributable to their uncomplicated

54

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

55

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

56

highly sensitive detection.31–34

57

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



58

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

59

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

60

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

61

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

62

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

63

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

64

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

65

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

66

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

67

environmental contaminants.

68 69

MATERIALS AND METHODS

70

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

71

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

72

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

73

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

74

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

75

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

76

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

77

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

78

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

79

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

80

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


Page 4 of 26

Page 5 of 26


81

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

82

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

83

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

84 85

RESULTS AND DISCUSSION

86

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

87

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

88

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

89

first

90

(5′-SH-TTTCTGTCCCACCCCCTGGCA-3′)

91

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

92

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

93

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

94

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

95

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

96

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

97

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

98

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

99

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

100

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

101

formed during DNA damage.

prepared

(Figure

S1)

and

modified

with

chemical and

attachment

of

DNA1 DNA2

102

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

103

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



Page 6 of 26

104

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

105

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

106

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

107

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

108

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

109

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

110

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

111

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

112

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

113

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

114

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

115

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

116 117

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

118

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

119

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

120

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

121

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

122

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

123

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

124

heterodimer NP make its intracellular application possible.

The

125

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

126

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


Page 7 of 26


127

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

128

dynamics indicate that the hybridized heterodimer NP showed highly efficient internalization

129

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

130

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

131

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

132

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

133

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



134


Page 8 of 26

Page 9 of 26


135

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

136

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

137

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

138

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

139

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

140

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

141

changes at 670 nm.

142 143

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

144

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

145

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

146

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

147

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

148

heterodimer NP probe.

149

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

150

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

151

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

152

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

153

the generation of 8-OHdG in NG108 cells.

154

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

155

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

156

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

157

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

158

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

159

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



160

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

161

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

162

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

163

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

164

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

165

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

166

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

167

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

168


Page 10 of 26

Page 11 of 26


169 170

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

171

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


172

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

173

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

174

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

175

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

176

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

177 178

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

179

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

180

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

181

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

182

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

183

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

184

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

185

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

186

demonstrating that this probe has excellent specificity in cells.

187

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

188

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

189

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

190

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

191

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

192

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

193

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

194

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

195

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


Page 12 of 26

Page 13 of 26


196

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

197

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

198

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

199

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

200

(Figure 3F).



201 14 ACS Paragon Plus Environment

Page 14 of 26

Page 15 of 26


202

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

203

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

204

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

205

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

206

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

207

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

208

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

209

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

210 211

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

212

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

213

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

214

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

215

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

216

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

217

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

218

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

219

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

220

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

221

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

222

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

223

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



224 225

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

226

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

227

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

228 229

ASSOCIATED CONTENT

230

Supporting Information Available


Page 16 of 26

Page 17 of 26


231

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

232

10.1021/*******.

233

Information as mentioned in the text. (PDF)

234

AUTHOR INFORMATION

235

Corresponding Author

236

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

237

ORCID

238

Chuanlai Xu: 0000-0002-5639-7102

239

Notes

240

The authors declare no competing financial interest.

241 242

ACKNOWLEDGMENTS

243

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

244

nos. 21471068 and 21371081).

245 246



247

REFERENCES

248

(1)

Wang, X.; Martinez, M. A.; Wu, Q.; Ares, I.; Martínez-Larrañaga, M. R.; Anadon, A.;

249

Yuan, Z. Fipronil Insecticide Toxicology: Oxidative Stress and Metabolism. Crit. Rev.

250

Toxicol. 2016, 46, 876–899.

251

(2)

Simon-Delso, N.; Amaral-Rogers, V.; Belzunces, L. P.; Bonmatin, J. M.; Chagnon, M.;

252

Downs, C.; Furlan, L.; Gibbons, D. W.; Giorio, C.; Girolami, V. et al.; Systemic

253

Insecticides (Neonicotinoids and Fipronil): Trends, Uses, Mode of Action and

254

Metabolites. Environ. Sci. Pollut. Res. 2015, 22, 5–34.

255

(3)

Raveton, M.; Aajoud, A.; Willison, J. C.; Aouadi, H.; Tissut, M.; Ravanel, P.

256

Phototransformation of the Insecticide Fipronil: Identification of Novel Photoproducts

257

and Evidence for an Alternative Pathway of Photodegradation. Environ. Sci. Technol.

258

2006, 40, 4151–4157.

259

(4)

Chen, L.; Durkin, K. A.; Casida, J. E. Structural Model for γ-Aminobutyric Acid

260

Receptor Noncompetitive Antagonist Binding: Widely Diverse Structures Fit the Same

261

Site. Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 5185–5190.

262

(5)

Zhang, Y.; Meng, X.; Yang, Y.; Li, H.; Wang, X.; Yang, B.; Zhang, J.; Li, C.; Millar, N. S.;

263

Liu, Z. Synergistic and Compensatory Effects of Two Point Mutations Conferring

264

Target-Site Resistance to Fipronil in the Insect GABA Receptor RDL. Sci. Rep. 2016, 6,

265

32335.

266 267

(6)

Pisa, L. W.; Amaral-Rogers, V.; Belzunces, L. P.; Bonmatin, J. M.; Downs, C. A.; Goulson, D.; Kreutzweiser, D. P.; Krupke, C.; Liess, M.; McField, M. et al.; Effects of 18 ACS Paragon Plus Environment

Page 18 of 26

Page 19 of 26


268

Neonicotinoids and Fipronil on Non-Target Invertebrates. Environ. Sci. Pollut. Res. 2015,

269

22, 68–102.

270

(7)

Gan, J.; Bondarenko, S.; Oki, L.; Haver, D.; Li, J. X. Occurrence of Fipronil and its

271

Biologically Active Derivatives in Urban Residential Runoff. Environ. Sci. Technol. 2012,

272

46, 1489–1495.

273

(8)

McMahen, R. L.; Strynar, M. J.; Dagnino, S.; Herr, D. W.; Moser, V. C.; Garantziotis, S.;

274

Andersen, E. M.; Freeborn, D. L.; McMillan, L.; Lindstrom, A. B. Identification of

275

Fipronil Metabolites by Time-of-Flight Mass Spectrometry for Application in a Human

276

Exposure Study. Environ. Int. 2015, 78, 16–23.

277

(9)

Park, J. H.; Park, Y. S.; Lee, J. B.; Park, K. H.; Paik, M. k.; Jeong, M.; Koh, H. C.

278

Meloxicam Inhibits Fipronil-Induced Apoptosis via Modulation of the Oxidative Stress

279

and Inflammatory Response in SH-SY5Y Cells. J. Appl. Toxicol. 2016, 36, 10–23.

280

(10)

Wang, X.-Q.; Li, Y.-G.; Zhong, S.; Zhang, H.; Wang, X.-Y.; Qi, P.-P.; Xu, H. Oxidative

281

Injury is Involved in Fipronil-Induced G2/M Phase Arrest and Apoptosis in Spodoptera

282

Frugiperda (Sf9) Cell Line. Pestic. Biochem. Physiol. 2013, 105, 122–130.

283

(11)

Lopez-Antia, A.; Ortiz-Santaliestra, M. E.; Camarero, P. R.; Mougeot, F.; Mateo, R.

284

Assessing the Risk of Fipronil-Treated Seed Ingestion and Associated Adverse Effects in

285

the Red-Legged Partridge. Environ. Sci. Technol. 2015, 49, 13649–13657.

286

(12)

287 288

Comoretto, L.; Arfib, B.; Chiron, S. Pesticides in the Rhône River Delta (France): Basic Data for a Field-Based Exposure Assessment. Sci. Total Environ. 2007, 380, 124–132.

(13)

Vasylieva, N.; Ahn, K. C.; Barnych, B.; Gee, S. J.; Hammock, B. D. Development of an 19 ACS Paragon Plus Environment


289

Immunoassay for the Detection of the Phenylpyrazole Insecticide Fipronil. Environ. Sci.

290

Technol. 2015, 49, 10038–10047.

291

(14)

Wu, D.; Liu, B.; Yin, J.; Xu, T.; Zhao, S.; Xu, Q.; Chen, X.; Wang, H. Detection of

292

8-Hydroxydeoxyguanosine (8-OHdG) as a Biomarker of Oxidative Damage in Peripheral

293

Leukocyte DNA by UHPLC-MS/MS. J. Chromatogr. B: Anal. Technol. Biomed. Life Sci.

294

2017, 1064, 1–6.

295

(15)

Liu, Z.; Cai, Y.; He, J. High Serum Levels of 8-OHdG are an Independent Predictor of

296

Post-Stroke Depression in Chinese Stroke Survivors. Neuropsychiatr. Dis. Treat. 2018, 14,

297

587–596.

298

(16)

Li, S.; Wang, X.; Wu, Y.; Zhang, H.; Zhang, L.; Wang, C.; Zhang, R.; Guo, Z.

299

8-Hydroxy-2'-Deoxyguanosine Expression Predicts Hepatocellular Carcinoma Outcome.

300

Oncol. Lett. 2012, 3, 338–342.

301

(17)

Di Minno, A.; Turnu, L.; Porro, B.; Squellerio, I.; Cavalca, V.; Tremoli, E.; Di Minno, M.

302

N. 8-Hydroxy-2-Deoxyguanosine Levels and Cardiovascular Disease: a Systematic

303

Review and Meta-Analysis of the Literature. Antioxid. Redox Signaling 2016, 24, 548–

304

555.

305

(18)

Lopresti, A. L.; Maker, G. L.; Hood, S. D.; Drummond, P. D. A Review of Peripheral

306

Biomarkers in Major Depression: the Potential of Inflammatory and Oxidative Stress

307

Biomarkers. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 2014, 48, 102–111.

308 309

(19)

Jiang, D.; Malla, S.; Fu, Y. J.; Choudhary, D.; Rusling, J. F. Direct LC-MS/MS Detection of Guanine Oxidations in Exon 7 of the p53 Tumor Suppressor Gene. Anal. 20 ACS Paragon Plus Environment

Page 20 of 26

Page 21 of 26


310 311

Chem. 2017, 89, 12872–12879. (20)

Liu, H.; Wang, Y.; Tang, X.; Yang, H.; Chen, S.; Zhao, H.; Liu, S.; Zhu, Y.; Wang, X.;

312

Huang, Y. A Novel Fluorescence Aptasensor for 8-Hydroxy-2-Deoxyguanosine based on

313

the Conformational Switching of K+-Stabilized G-Quadruplex. J. Pharm. Biomed. Anal.

314

2016, 118, 177-182.

315

(21)

Jia, L.-P.; Liu, J.-F.; Wang, H.-S. Electrochemical Performance and Detection of

316

8-Hydroxy-2’-Deoxyguanosine at Single-Stranded DNA Functionalized Graphene

317

Modified Glassy Carbon Electrode. Biosens. Bioelectron. 2015, 67, 139–145.

318

(22)

319 320

Ma, W.; Xu, L.; De Moura, A. F.; Wu, X.; Kuang, H.; Xu, C.; Kotov, N. A. Chiral Inorganic Nanostructures. Chem. Rev. 2017, 117, 8041–8093.

(23)

Yan, W.; Xu, L.; Xu, C.; Ma, W.; Kuang, H.; Wang, L.; Kotov, N. A. Self-Assembly of

321

Chiral Nanoparticle Pyramids with Strong R/S Optical Activity. J. Am. Chem. Soc. 2012,

322

134, 15114–15121.

323

(24)

Wu, X.; Xu, L.; Liu, L.; Ma, W.; Yin, H.; Kuang, H.; Wang, L.; Xu, C.; Kotov, N. A.

324

Unexpected Chirality of Nanoparticle Dimers and Ultrasensitive Chiroplasmonic

325

Bioanalysis. J. Am. Chem. Soc. 2013, 135, 18629–18636.

326

(25)

327 328

Lan, X.; Wang, Q. Self-Assembly of Chiral Plasmonic Nanostructures. Adv. Mater. 2016, 28, 10499–10507.

(26)

Lan, X.; Chen, Z.; Dai, G.; Lu, X.; Ni, W.; Wang, Q. Bifacial DNA Origami-Directed

329

Discrete, Three-Dimensional, Anisotropic Plasmonic Nanoarchitectures with Tailored

330

Optical Chirality. J. Am. Chem. Soc. 2013, 135, 11441–11444. 21 ACS Paragon Plus Environment


331

(27)

Page 22 of 26

Shen, X.; Asenjo-Garcia, A.; Liu, Q.; Jiang, Q.; De Abajo, F. J. G.; Liu, N.; Ding, B.

332

Three-Dimensional Plasmonic Chiral Tetramers Assembled by DNA Origami. Nano Lett.

333

2013, 13, 2128–2133.

334

(28)

Shen, C.; Lan, X.; Zhu, C.; Zhang, W.; Wang, L.; Wang, Q. Spiral Patterning of Au

335

Nanoparticles on Au Nanorod Surface to Form Chiral AuNR@AuNP Helical

336

Superstructures Templated by DNA Origami. Adv. Mater. 2017, 29, 1606533.

337

(29)

Shen, C.; Lan, X.; Lu, X.; Meyer, T. A.; Ni, W.; Ke, Y.; Wang, Q. Site-Specific Surface

338

Functionalization of Gold Nanorods Using DNA Origami Clamps. J. Am. Chem. Soc.

339

2016, 138, 1764–1767.

340

(30)

341 342

Lan, X.; Lu, X.; Shen, C.; Ke, Y.; Ni, W.; Wang, Q. Au Nanorod Helical Superstructures with Designed Chirality. J. Am. Chem. Soc. 2015, 137, 457–462.

(31)

Ma,

W.;

Sun,

M.;

Fu,

P.;

Li,

S.;

Kuang,

Xu,

344

Glycoprotein and MicroRNA in Living Cells. Adv. Mater. 2017, 29, 1703410.

346 347

Simultaneously

H.;

Chiral-Nanoassemblies-Enabled

(32)

for

L.;

343

345

Strategy

Xu,

Profiling

C.

A

Surface

Fu, P.; Sun, M.; Xu, L.; Wu, X.; Liu, L.; Kuang, H.; Song, S.; Xu, C. A Self-Assembled Chiral-Aptasensor for ATP Activity Detection. Nanoscale 2016, 8, 15008–150015.

(33)

Sun, M.; Xu, L.; Fu, P.; Wu, X.; Kuang, H.; Liu, L.; Xu, C. Scissor-Like Chiral

348

Metamolecules for Probing Intracellular Telomerase Activity. Adv. Funct. Mater. 2016, 26,

349

7352–7358.

350 351

(34)

Li, S.; Xu, L.; Sun, M.; Wu, X.; Liu, L.; Kuang, H.; Xu, C. Hybrid Nanoparticle Pyramids for Intracellular Dual MicroRNAs Biosensing and Bioimaging. Adv. Mater. 22 ACS Paragon Plus Environment

Page 23 of 26


352 353

2017, 29, 1606086. (35)

Sun, M.; Xu, L.; Ma, W.; Wu, X.; Kuang, H.; Wang, L.; Xu, C. Hierarchical Plasmonic

354

Nanorods and Upconversion Core-Satellite Nanoassemblies for Multimodal Imaging-

355

Guided Combination Phototherapy. Adv. Mater. 2016, 28, 898–904.

356

(36)

357 358

Xu, Z.; Xu, L.; Zhu, Y.; Ma, W.; Kuang, H.; Wang, L.; Xu, C. Chirality based Sensor for Bisphenol A Detection. Chem. Commun. 2012, 48, 5760–5762.

(37)

Hao, T.; Wu, X.; Xu, L.; Liu, L.; Ma, W.; Kuang, H.; Xu, C. Ultrasensitive Detection of

359

Prostate-Specific Antigen and Thrombin based on Gold-Upconversion Nanoparticle

360

Assembled Pyramids. Small 2017, 13, 1603944.

361

(38)

Liu, Y.; Wei, M.; Zhang, L.; Zhang, Y.; Wei, W.; Yin, L.; Pu, Y.; Liu, S. Chiroplasmonic

362

Assemblies

363

8-Hydroxy-2’-Deoxyguanosine in Human Serum Sample. Anal. Chem. 2016, 88, 6509–

364

6514.

365

(39)

of

Gold

Nanoparticles

for

Ultrasensitive

Detection

of

Ma, W.; Yin, H.; Xu, L.; Wu, X.; Kuang, H.; Wang, L.; Xu, C. Ultrasensitive

366

Aptamer-based SERS Detection of PSAs by Heterogeneous Satellite Nanoassemblies.

367

Chem. Commun. 2014, 50, 9737–9740.

368

(40)

Zhang, T. T.; Zhao, H. M.; Fan, X. F.; Chen, S.; Quan, X. Electrochemiluminescence

369

Immunosensor for Highly Sensitive Detection of 8-Hydroxy-2'-Deoxyguanosine based

370

on Carbon Quantum Dot Coated Au/SiO2 Core-Shell Nanoparticles. Talanta 2015, 131,

371

379–385.

372

(41)

Wang, J.-C.; Wang, Y.-S.; Rang, W.-Q.; Xue, J.-H.; Zhou, B.; Liu, L.; Qian, Q.-M.; Wang, 23 ACS Paragon Plus Environment


373

Y.-S.; Yin, J.-C. Colorimetric Determination of 8-Hydroxy-2’-Deoxyguanosine using

374

Label-Free Aptamer and Unmodified Gold Nanoparticles. Microchim. Acta 2014, 181,

375

903–910.

376

(42)

Zhang, Q.; Wang, Y.; Meng, X.; Dhar, R.; Huang, H. Triple-Stranded DNA Containing

377

8-Oxo-7,8-Dihydro-2'-Deoxyguanosine: Implication in the Design of Selective Aptamer

378

Sensors for 8-Oxo-7,8-Dihydroguanine. Anal. Chem. 2013, 85, 201–207.

379

(43)

Krpetic, Z.; Saleemi, S.; Prior, I. A.; See, V.; Qureshi, R.; Brust, M. Negotiation of

380

Intracellular Membrane Barriers by TAT-Modified Gold Nanoparticles. ACS Nano 2011,

381

5, 5195–5201.

382

(44)

Todorova, N.; Chiappini, C.; Mager, M.; Simona, B.; Patel, I. I.; Stevens, M. M.;

383

Yarovsky, I. Surface Presentation of Functional Peptides in Solution Determines Cell

384

Internalization Efficiency of TAT Conjugated Nanoparticles. Nano Lett. 2014, 14, 5229–

385

5237.

386

(45)

Zhang, B.; Xu, Z.; Zhang, Y.; Shao, X.; Xu, X.; Cheng, J.; Li, Z. Fipronil Induces

387

Apoptosis through Caspase-Dependent Mitochondrial Pathways in Drosophila S2 Cells.

388

Pestic. Biochem. Physiol. 2015, 119, 81–89.

389

(46)

Kong, D.; Liu, L.; Song, S.; Suryoprabowo, S.; Li, A.; Kuang, H.; Wang, L.; Xu, C. A

390

Gold Nanoparticle-based Semi-Quantitative and Quantitative Ultrasensitive Paper Sensor

391

for the Detection of Twenty Mycotoxins. Nanoscale 2016, 8, 5245–5253.

392 393

(47)

Huang, Y. F.; Wang, P. W.; Huang, L. W.; Lai, C. H.; Yang, W.; Wu, K. Y.; Lu, C. A.; Chen, H. C.; Chen, M. L. Prenatal Nonylphenol and Bisphenol a Exposures and 24 ACS Paragon Plus Environment

Page 24 of 26

Page 25 of 26


394

Inflammation are Determinants of Oxidative/Nitrative Stress: a Taiwanese Cohort Study.

395

Environ. Sci. Technol. 2017, 51, 6422–6429.

396

(48)

Kong, D.; Xie, Z.; Liu, L.; Song, S.; Zheng, Q.; Kuang, H. Development of an

397

Immunochromatographic Assay for the Detection of Alternariol in Cereal and Fruit juice

398

samples. Food Agric. Immunol. 2017, 28, 1082–1093.

399 400 401



402

For Table of Contents Use Only

403

Circular Dichroism-Active Interactions between Fipronil and Neuron Cells

404 405

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

406 407

1

408


409

2

410

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

411

China

412

3

413

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

414

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,

415

416


Page 26 of 26

Circular dichroism-active interactions between ... - ACS Publications

Recommend Documents