Isotope Tracers To Study the Environmental Fate ... - ACS Publications

Feb 17, 2017 - Currently, the identification and tracking of MENPs in environmental and biological ...... (at picograms per cell level) in mouse fibro...
2 downloads 12 Views 10MB Size
This is an open access article published under an ACS AuthorChoice License, which permits copying and redistribution of the article or any adaptations for non-commercial purposes.

Review pubs.acs.org/CR

Isotope Tracers To Study the Environmental Fate and Bioaccumulation of Metal-Containing Engineered Nanoparticles: Techniques and Applications Yongguang Yin,†,‡ Zhiqiang Tan,† Ligang Hu,† Sujuan Yu,† Jingfu Liu,*,† and Guibin Jiang† †

State Key Laboratory of Environmental Chemistry and Ecotoxicology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China ‡ Institute of Environment and Health, Jianghan University, Wuhan 430056, China ABSTRACT: The rapidly growing applicability of metal-containing engineered nanoparticles (MENPs) has made their environmental fate, biouptake, and transformation important research topics. However, considering the relatively low concentration of MENPs and the high concentration of background metals in the environment and in organisms, tracking the fate of MENPs in environment-related scenarios remains a challenge. Intrinsic labeling of MENPs with radioactive or stable isotopes is a useful tool for the highly sensitive and selective detection of MENPs in the environment and organisms, thus enabling tracing of their transformation, uptake, distribution, and clearance. In this review, we focus on radioactive/stable isotope labeling of MENPs for their environmental and biological tracing. We summarize the advantages of intrinsic radioactive/stable isotopes for MENP labeling and discuss the considerations in labeling isotope selection and preparation of labeled MENPs, as well as exposure routes and detection of labeled MENPs. In addition, current practice in the use of radioactive/stable isotope labeling of MENPs to study their environmental fate and bioaccumulation is reviewed. Future perspectives and potential applications are also discussed, including imaging techniques for radioactive- and stable-isotope-labeled MENPs, hyphenated multistable isotope tracers with speciation analysis, and isotope fractionation as a MENP tracer. It is expected that this critical review could provide the necessary background information to further advance the applications of isotope tracers to study the environmental fate and bioaccumulation of MENPs.

CONTENTS 1. Introduction 2. Radioactive Isotopes as Tracers for Metal-Containing Engineered Nanoparticles 2.1. Need for Intrinsic Radioactive Isotopes for Metal-Containing Engineered Nanoparticle Labeling 2.2. Selection of Radioactive Isotopes for MetalContaining Engineered Nanoparticle Labeling 2.3. Preparation of Radioactive-Isotope-Labeled Metal-Containing Engineered Nanoparticles 2.4. Exposure of Radioactive-Isotope-Labeled Metal-Containing Engineered Nanoparticles for Various Evaluation Purposes 2.5. Detection of Radioactive-Isotope-Labeled Metal-Containing Engineered Nanoparticles 2.6. Applications of Radioactive-Isotope-Labeled Metal-Containing Engineered Nanoparticles 2.6.1. Uptake, Intracellular Dissolution, and Translocation of Metal-Containing Engineered Nanoparticles Revealed by Use of in Vitro Models

2.6.2. Uptake and Accumulation of MetalContaining Engineered Nanoparticles from Different Exposure Routes by Use of in Vivo Models 2.6.3. Environmental Transformation and Distribution of Metal-Containing Engineered Nanoparticles 3. Stable Isotopes as Tracers for Metal-Containing Engineered Nanoparticles 3.1. Advantages of Using Stable-Isotope-Labeled Metal-Containing Engineered Nanoparticles 3.2. Selection of Stable Isotopes for MetalContaining Engineered Nanoparticle Labeling 3.3. Synthesis of Stable-Isotope-Labeled MetalContaining Engineered Nanoparticles 3.4. Basis for Stable Isotope Tracing of MetalContaining Engineered Nanoparticles 3.5. Application of Stable-Isotope-Labeled MetalContaining Engineered Nanoparticles To Probe Their Environmental and Biological Behaviors

4463 4463

4463

4465 4468

4468 4468 4469

4469

4474 4474 4474

4474 4474 4474

4475

4469 Received: October 9, 2016 Published: February 17, 2017

© 2017 American Chemical Society

4462

DOI: 10.1021/acs.chemrev.6b00693 Chem. Rev. 2017, 117, 4462−4487

Chemical Reviews 3.5.1. Environmental Fate of Metal-Containing Engineered Nanoparticles 3.5.2. Uptake and Accumulation of MetalContaining Engineered Nanoparticles from Different Exposure Routes 4. Summary and Future Perspectives 4.1. Methods for Preparing Radioactive-IsotopeLabeled Metal-Containing Engineered Nanoparticles 4.2. Effect of Surface Modification and Functionalization of Metal-Containing Engineered Nanoparticles on Their Environmental Fate and Bioaccumulation 4.3. Long-Term Exposure of Metal-Containing Engineered Nanoparticles at Low Doses 4.4. Imaging Techniques for Radioactive- and Stable-Isotope-Labeled Metal-Containing Engineered Nanoparticles 4.5. High-Precision Stable Isotope Ratio Measurements To Enhance the Sensitivity of MetalContaining Engineered Nanoparticle Tracing 4.6. Microcosm and Mesocosm Combined with Isotope Tracers To Study the Behavior of Metal-Containing Engineered Nanoparticles in the Environment 4.7. Hyphenated Multistable Isotope Tracers with Speciation Analysis To Compare the Behaviors of Different Engineered Nanoparticles and Metal Species 4.8. Isotope Fractionation as a Tracer for MetalContaining Engineered Nanoparticles Author Information Corresponding Author ORCID Notes Biographies Acknowledgments Abbreviations References

Review

consequent effects is crucial prior to their clinical use14 and in the development of safer MENPs for both the environment and human health.15 Currently, the identification and tracking of MENPs in environmental and biological systems remain a great challenge. A major difficulty is the effective differentiation between MENPs and interference or artifacts from natural or background-level metallic components.16 For example, in studying the biodistribution of iron oxide NPs as magnetic resonance contrast agents, a distinction must be made between the iron in iron oxide NPs and nutritional iron in organisms. A possible solution is to label and track MENPs in the matrix according to their specific labeling information. Fluorescence (e.g., by organic dye fluorescein isothiocyanate)17 or exogenous radioactive labeling (e.g., by 125I, 188Re, 111In)18−20 can provide sensitive and specific signals. However, these modification methods could potentially change the surface properties of MENPs and subsequently alter their environmental or biological behavior. Additionally, the labels (organic dye or exogenous radioactive tracer) could possibly break away from the MENP core21 and would thus not be representative of the behavior of MENPs. Labeling of MENPs by use of intrinsic radioactive or stable isotopes has recently become a research focus. Isotopic tracers have several advantages when compared to exogenous fluorescence and radioactive labeling. First, they have much greater sensitivity compared to conventional fluorescence labeling due to the range of detection techniques that can be used, including γ spectrometry, scintillation counting, or inductively coupled plasma mass spectrometry (ICP-MS).16 In addition, the specific label signals can be easily distinguished from those of the matrix.22 Furthermore, and importantly, labeled MENPs have essentially the same chemical composition and surface chemistry as unlabeled MENPs and therefore reflect the behavior of MENPs much better than conventional fluorescence and exogenous radioactive labeling, which require additional surface modification of the MENPs.16 Comparably, radioactive isotope tracking is favorable for in situ imaging at individual, tissue, cell, and even subcellular levels, while tracking using multiple stable isotopes can be used to simultaneously monitor the differential behaviors of MENPs of varying morphology, size, and coatings. This review article focuses on the techniques and applications of radioactive and stable isotope tracers to study the environmental fate and biological uptake and distribution of MENPs. We summarize the advantages of intrinsic radioactive/stable isotopes for MENP labeling and discuss the considerations in isotope selection, preparation of labeled MENPs, and exposure routes and detection of labeled MENPs (Figure 1). In addition, the current and future applications of radioactive/stable-isotopelabeled MENPs to study their environmental fate and bioaccumulation are reviewed. Radioactive (14C) and stable isotope (13C) labeling to track carbon-based ENPs are excluded from this review, as they have been previously reported in other studies and reviews.22−24

4475

4476 4478

4478

4479 4479

4479

4479

4479

4479 4480 4480 4480 4480 4480 4480 4480 4481 4481

1. INTRODUCTION Engineered nanoparticles (ENPs), defined as anthropogenic particles less than 100 nm in size in at least one dimension, have been extensively produced and applied in many sectors such as consumer products, health care, transportation, energy, and agriculture.1 In particular, metal-containing engineered nanoparticles (MENPs), composed of noble metal (Au, Ag, Pt, Pd), metal oxide (ZnO, CuO, CeO2), or quantum dot (QD; CdS, ZnSe) nanoparticles (NPs), are widely used for catalysis,2 sensing,3,4 imaging,5 and disease diagnosis and therapy.6 Nevertheless, during the production, transport, use, disposal, and recycling of MENPs and their products, the release of MENPs into the environment is inevitable.7 Thus, as a class of emerging contaminants,8 MENPs have drawn considerable attention with regard to their environmental fate, their transformation, and their uptake by and toxicity to organisms in recent years.9,10 Of particular concern is their use as diagnostic and therapeutic tools, including as contrast-enhancement agents, nanocarriers, and phototherapy agents,11−13 when the intentional human contact or administration of MENPs for these applications is considered. Therefore, understanding their uptake, distribution, and clearance in the human body and

2. RADIOACTIVE ISOTOPES AS TRACERS FOR METAL-CONTAINING ENGINEERED NANOPARTICLES 2.1. Need for Intrinsic Radioactive Isotopes for Metal-Containing Engineered Nanoparticle Labeling

Although exogenous radioactive elements (e.g., 99mTc, 111In) have been widely used to label MENPs through physical or 4463

DOI: 10.1021/acs.chemrev.6b00693 Chem. Rev. 2017, 117, 4462−4487

Chemical Reviews

Review

Figure 1. Preparation, exposure, and detection of radioactive- or stable-isotope-labeled MENPs for environmental fate and bioaccumulation studies.

Figure 2. Sketch of double-radiolabeled nanoparticles. Au cores were composed of the radioactive isotope 198Au, and diethylenetriaminepentaacetic acid-chelated radioactive 111In was integrated into the polymer shell. Reprinted with permission from ref 21. Copyright 2015 Macmillan Publishers Limited.

quantitative analysis independent of 198Au and 111In showed significantly different biodistributions for the two elements. While 198Au accumulates mostly in the liver, 111In shows a nonparticulate biodistribution similar to that seen after intravenous injection of chelated 111In (diethylenetriaminepentaacetic acid-111In). This finding strongly supported the contention that in vivo removal of the polymer shell (or the labeled

chemical adsorption, recent studies have demonstrated that these exogenous radioactive tracers can be removed from the MENP core and are thus not adequate for in vivo studies.21,25 Doubleradiolabeled NPs have been recently synthesized by Kreyling et al.21 (Figure 2), using radioactively labeled Au nanoparticles (198Au NPs) as the core and 111In-labeled polymer as a shell around the Au core. After intravenous injection into rats, 4464

DOI: 10.1021/acs.chemrev.6b00693 Chem. Rev. 2017, 117, 4462−4487

Chemical Reviews

Review

Table 1. Summary of Metal-Containing Engineered Nanoparticles and Their Radioactive and Stable Metal Isotopes radioactive possible isotope 44

Ti 45 Ti

52

Fe Fe

59

60

Cu Cu 64 Cu 67 Cu 61

62

Zn Zn 65 Zn 63

69m

Zn Zn 72 Zn 71m

103

Ag 104 Ag 104m Ag 105 Ag 106 Ag 106m Ag 108m Ag 110m Ag 111

Ag 112 Ag 113 Ag 115 Ag 104

Cd 105 Cd

half-life

stable main decay modea

isotope

radioactive

natural relative abundance (%)

Titanium (TiO2 Nanoparticles) 46 60.4 years γ, ε Ti 47 3.08 h β+ Ti 48 Ti 49 Ti 50 Ti Iron (Iron Oxide Nanoparticles) 54 8.275 h β+ Fe − 56 44.495 β Fe days 57 Fe 58 Fe Copper (Cu, CuO, CuS Nanoparticles) 63 23.7 min β+ Cu + 65 3.333 h β Cu 12.70 h β+, β− 61.83 h β− Zinc (ZnO, ZnS, ZnSe, ZnTe Nanoparticles) 64 9.186 h β+ Zn + 66 38.47 min β Zn 67 244.06 β+ Zn days 68 55.6 min β− Zn − 70 3.97 days β Zn 46.5 h β− Silver (Ag, AgCl, Ag2S Nanoparticles) 107 65.7 min β+ Ag + 109 69.2 min β Ag 33.5 min β+ 41.29 days β+ 23.96 min β+ 8.28 days β+ 418 years β+ 249.78 β− days 7.45 days β− 3.13 h β− 5.37 h β− 20.0 min β− Cadmium (CdS, CdSe, CdTe Nanoparticles) 106 57.7 min β+ Cd 108 55.5 min β+ Cd

possible isotope 107

8.0 7.5 73.7 5.5 5.3

Cd 109 Cd 113m Cd 115 Cd 115m Cd 117 Cd 117m Cd 118 Cd

5.8 91.7 2.14 0.31

189

Au Au 191 Au 192 Au 193 Au 194 Au 195 Au

190

69 31

196

48.9 27.8 4.1

Au Au 199 Au 200 Au 200m Au 201 Au 198

18.6 0.62

130

Ce Ce 133 Ce 133m Ce 134 Ce 135 Ce 137 Ce 139 Ce

51.4 48.7

132

141

Ce

143

Ce Ce

144

a

half-life

stable main decay modea

isotope

natural relative abundance (%)

Cadmium (CdS, CdSe, CdTe Nanoparticles) 110 6.5 h β+ Cd 12.4 111 461.4 days EC Cd 12.8 112 14.1 years β− Cd 24.0 113 53.46 h β− Cd 12.3 114 44.56 h β− Cd 28.8 116 2.49 h β− Cd 7.6 3.36 h β− 50.3 min β− Gold (Au Nanoparticles) 197 28.7 min β+ Au 100 42.8 min β+ 3.18 h β+ 4.94 h β+ 17.65 h β+ 38.02 h β+ 186.10 EC days 6.17 days β+, β− 2.685 days β− 3.169 days β− 48.4 min β− 18.7 h β− 26 min β− Cerium (CeO2 Nanoparticles) 136 22.9 min β+ Ce 0.2 + 138 3.51 h β Ce 0.3 140 97 min β+ Ceb 88.5 142 4.9 days β+ Ce 11.0 3.16 days EC 17.7 days β+ 9.0 days β+ 137.640 EC days 32.501 β− days 33.04 days β− 284.893 β− days

EC, electron capture. bOnly

140

Ce is a stable isotope.

1.2 0.9

lower-energy state can emit a γ photon. The emission of an α particle or an Auger electron (e−) in vivo results in tissue damage and could thus be used in radiotherapy. However, the short penetration distance of these particles in the body prevents their application in imaging. In contrast, radioactive isotopes emitting β+ or γ rays, which have good penetration, are widely used for MENP labeling, tracing, and imaging.27 The physical half-life is another important factor in radioactive isotope selection. A radioactive isotope with too short a half-life is not convenient for experimental operation, while a radioactive isotope with too long a half-life is not favorable for post-treatment of radioactive waste. Table 2 summarizes the recent applications of radioactiveisotope-labeled MENPs to trace their environmental and biological behaviors, including the preparation method, exposure

exogenous radioactive elements) from MENPs is inevitable. When this is considered, the use of intrinsic metal isotopes to label MENPs is appropriate and can essentially guarantee an accurate reflection of MENP behavior by the isotope tracer. 2.2. Selection of Radioactive Isotopes for Metal-Containing Engineered Nanoparticle Labeling

Table 1 provides a list of the possible radioactive isotopes that can be used as MENP tracers, along with their respective halflives. Suitable radioactive isotopes should be first selected according to their nuclear emission properties, physical half-life, cost, availability, and measurement method.26,27 Radioactive isotope decay can be mainly categorized as α, β [β−, β+, and electron capture (EC)], and γ decay. Following α and β decay, the nucleus is often at a high-energy state, and the transition to a 4465

DOI: 10.1021/acs.chemrev.6b00693 Chem. Rev. 2017, 117, 4462−4487

Chemical Reviews

Review

Table 2. Application of Radioactive-Isotope-Labeled Metal-Containing Engineered Nanoparticles in Tracing Their Environmental and Biological Behaviorsa In Vitro Exposureb radiolabeled MENPs or metal species 198g

Au NP 59 Fe NP, 60Co NP 192 Ir NP (18 nm)

NA of Au NP NA of Fe NP and Co NP synthesis from 192Ir metal precursor synthesis from 241AmO2 synthesis from 241AmO2 NA of CeO2 NP NA of CeO2 NP

241

AmO2 AmO2 141 CeO2 141 CeO2 (28.4 nm), 141CeO2 coated with SiO2 (28.4 nm), nm) 65 ZnO (28 nm), 65ZnO coated with SiO2 (27.6 nm) 57 Co3O4 (300, 700, 800, 1700 nm) 57 Co3O4 (500 nm) 241

exposure route

exposed cell, organism, or environmental matrix

radioactive labeling method

141

CeO2 (119

NA of ZnO NP synthesis from 57Co(NO3)2 synthesis from 57Co(NO3)2 In Vivo Exposurec

radiolabeled MENPs or metal species

ref

MDCK and HepG2 cells SKOV-3 and U87 cell lines isolated lung from male WKY rats

42 43 115

rat, dog, and monkey alveolar macrophages dog alveolar macrophages mouse fibroblast cell line Balb/3T3 human lung epithelial cells

46 45 44 48

human lung epithelial cells human and canine alveolar macrophages Fischer (F-344) rat alveolar macrophages

48 47 116

radioactive labeling method

exposed cell, organism, or environmental matrix

ref

d

iv iv

64

iv iv iv iv iv iv iv it

198

Au NP Au-incorporated Au nanostructure 198 Au nanocage 198 Au NP protein-coated 198Au NP [14C]CIT-[198Au]Au NP 198 Au NP gum arabic-coated 198Au NP

iv

(−) 198Au NP (1.4, 5, 18, 80, 200 nm); (+) 198Au NP (2.8 nm) sulfonated Ph3P-coated 198Au NP (1.4, 18, 80 nm)

iv

Cu nanocluster 64 Cu−Au alloy

198

Injection synthesis from 64CuCl2 precursor synthesis from 64CuCl2 precursor NA of Au NP synthesis from H198AuCl4 precursor synthesis from H198AuCl4 precursor NA of Au NP NA of Au NP NA of Au NP synthesis from

198

Au foil

NA of Au NP NA of Au NP

iv iv iv iv iv iv iv iv, ip iv iv iv iv iv iv iv iv iv iv, it

59

Fe3O4 Fe2O3 59 Fe2O3 59 Fe oxide 59 Fe oxide with different coatings 59 Fe oxide 59 Fe oxide with different sizes and surface charges 59 Fe oxide 59 Fe oxide 65 ZnO NP (10, 71 nm), 65Zn(NO3)2 65 ZnO NP, 69mZnO NP 141 CeO2 uncoated, silica-coated 141CeO2 141 CeO2, 141CeCl3 57 [ Co]CoO@SiO2 131 BaSO4 CIT- or PEG-coated [64Cu]CuS PEG-coated [64Cu]CuS

synthesis from 59FeCl3 precursor synthesis from 59FeCl3 precursor synthesis from 59FeCl3 precursor synthesis from 59FeCl3 precursor synthesis from 59FeCl3 precursor synthesis from 59FeCl3 precursor synthesis from 59FeCl3 precursor synthesis from 59FeCl3 precursor synthesis from 59FeCl3 precursor NA of ZnO NP NA of ZnO NP synthesis from 141CeCl3 precursor NA of CeO2 NP NA of CeO2 NPs and CeCl3 synthesis from 57CoCl2 precursor NA of BaSO4 NP synthesis from 64CuCl2 precursor synthesis from 64CuCl2 precursor

iv iv is it it it

CdSe/CdS/65ZnS CdSe/109CdZnS, CdTeSe/109CdZnSe, 109CdSe, 109CdTeSe 59 Fe2O3 198 Au0 composite nanodevice gum arabic-coated 198Au NP 198 Au NP with EGCg coating

synthesis from 65ZnCl2 precursor synthesis from 109Cd precursor synthesis from 59FeCl3 precursor NA of Au NP synthesis from 198Au foil synthesis from H198AuCl4 precursor

59

4466

lung tumor-bearing mice normal BALB/c mice and mouse breast cancer model female WKY rats EMT6 tumor-bearing BALB/c mice EMT-6 tumor- bearing mice female WKY rats female C57Bl/6 mice male Sprague-Dawley rats male ICR mice SCID mice bearing human prostate cancer xenografts female WKY rats pregnant rat model on day 18 of gestation mice mice mice wild-type FVB mice healthy adult male Wistar rats mice Swiss mice wild-type FVB mice wild-type FVB mice mice ICR mice female nude mice male Wistar Han rats Wistar Han rats nude mice male Wistar rats Harlan Sprague-Dawley mice male athymic nude mice with anaplastic thyroid carcinoma wild-type FVB/N mice female nude mice mice tumor-bearing male C57BL/6J mice prostate tumor-bearing dogs PC-3 tumor-bearing female SCID mice

77 57 21 73 63 54 74 58 36 117 62 70 50 51 59 25 56 61 72 75 68 71 69 60 64 53 65 55 52 118 67 66 51 119 120 76

DOI: 10.1021/acs.chemrev.6b00693 Chem. Rev. 2017, 117, 4462−4487

Chemical Reviews

Review

Table 2. continued In Vivo Exposurec exposure route it

inh inh inh endo inh endo

radiolabeled MENPs or metal species gum arabic glycoprotein- functionalized

192

Au NP

195

inh endo inh trp trp

57

Injectiond synthesis from H198AuCl4 precursor

Tracheal Perfusion or Inhalation Exposuree aerosol (15, 80 nm) synthesis from 192Ir metal precursor aerosol synthesis from 192Ir metal precursor aerosol (17−20 nm) synthesis from 192Ir metal precursor aerosol (primary particle size 2−4 nm) synthesis from 192Ir metal precursor aerosol (nominal particle diameter 10, 15, 35, 75 synthesis from 192Ir metal precursor

UF Ir UF 192Ir UF 192Ir UF 192Ir UF 192Ir nm) 195 Au NP (23 nm)

inh

trp trp

198

Au NP (20 nm)

Co3O4 (1100 nm) Co3O4 (800, 1700 nm) 131 BaSO4 198 Au NP (−) 198Au NP (1.4, 2.8, 5, 18, 80, 200 nm); (+) 198Au NP (2.8 nm) 59 Fe3O4 59 Fe2O3 57

SI generation of proton-activated gold electrodes SI generation of proton-activated gold electrodes synthesis from 57Co(NO3)2 synthesis from 57Co(NO3)2 NA of BaSO4 NP NA of Au NP NA of Au NP synthesis from 59FeCl3 precursor irradiation of Fe2O3 NP in heavy-water nuclear reactor synthesis from Fe(NO3)3 precursor NA of ZnO NP NA of CeO2 NP and CeCl3 synthesis from 141Ce(NO3)3 precursor NA of CeO2 NP NA of BaSO4 NP Oral Exposuref NA of Co core/Co3O4 shell NP NA of Fe NP NA of Ag NP NA of Au NP

trp trp trp trp trp trp

59

dietary gavage gavage gavage gavage

60

gavage gavage gavage gavage

NA of ZnO NP NA of CeO2 NP and CeCl3 NA of CeO2 NP NA of BaSO4 NP Implant 110m Ag NP-coated catheter synthesis from 110mAgNO3 precursor Waterborne Exposure for Aquatic Organismsg 110m 110m CIT- and PVP- Ag NP, AgNO3 synthesis from 110mAgNO3 precursor carbonate-coated 110mAg NP adsorption of 110mAg+ to Ag NP 110m Ag NP, 110mAgNO3 synthesis from 110mAgNO3 precursor 110m 110m Ag NP, AgNO3 synthesis from 110mAgNO3 precursor 110m Ag NP with different sizes (20, 50, 100 nm) and adsorption of 110mAg+ to Ag NP coatings (CIT, tannic acid) CIT-110mAg NP (80 nm), 110mAgNO3 adsorption of 110mAg+ to Ag NP 110m Ag NP (80%. The 65Cu-enriched snails were subsequently exposed to benthic algae mixed with natural Cubearing Fe−Al particles. The trace Cu bioavailability from the natural particles could therefore be calculated by measuring the 65 Cu/63Cu ratio in the tissues (Figure 10). Similar techniques could also be applied to study the biological uptake of MENPs, and the main advantage is that the synthesis of isotope-labeled MENPs is not needed.

efficiency of TiO2 NPs and high natural Ti background in organisms indicate a slow accumulation of TiO2 in internal organs and that long-term exposure is needed to evaluate the uptake and assimilation of TiO2 NPs by organisms. 3.5.2.2. Dermal Exposure. Skin is the largest organ, acting as a primary barrier protecting the body from external substances. However, hazardous substances on the dermal surface are potentially absorbed into the body through the stratum corneum and the epidermis toward the dermis and are subsequently transported to other organs through blood flow.159 The interaction of NPs with the skin can occur through unintentional occupational and environmental exposure (e.g., contact with MENP-containing textiles160) or intentional medical or daily application (e.g., photothermal and photodynamic therapy agents,161 sunscreen162). However, the present data on dermal absorption and skin penetration of MENPs remain controversial. Some studies suggest that MENPs cannot penetrate the skin,163,164 while other argue that MENPs are skin-penetrable, depending on the role of intrinsic characteristics of MENPs (e.g., size,165 charge, and surface properties166), solvent or dosage forms,167 and skin condition (damaged or intact).168,169 Therefore, a highly sensitive stable isotope tracing method is required to ensure the detection of very low levels (if any) of dermally absorbed MENPs and distinguish them from background metal signals.143 ZnO NPs are widely used as sunscreen due to their protection against sunburn.151 However, for a long time, the ability of these small-sized NPs to penetrate through human skin remained unknown. Gulson et al.143 were the first to assess this by synthesizing 68ZnO NPs (19 nm) and 68ZnO bulk particles (110 nm), incorporating them into an oil−water formulation of sunscreens, and testing whether the Zn from these particles was absorbed following sunscreen outdoor application on humans. As shown in Figure 9, small amounts of 68Zn from both ZnO NPs and bulk particles were observed in venous blood following sunscreen exposure; nevertheless, comparably higher levels of 68 Zn from ZnO NP exposure were observed in blood. In addition, the Δ68Zn (percent) and amounts of 68Zn tracer in blood following NP exposure were significantly higher than that following bulk exposure for females with the same treatment, but no difference were observed between the NP and bulk groups for males. However, generally, the amount of 68Zn detected in blood after the 5-day application period accounted for only approximately 0.1% of the total Zn in the blood compartment and less than 0.001% of the applied dose, which is minute when compared with the dietary intake of Zn. Nevertheless, as the 68Zn levels in blood continued to increase beyond the 5-day application, it is proposed that the absorbed 68Zn may be concentrated in particular tissues (e.g., epidermis and liver) and is released slowly into the blood. Further studies152,153 confirmed the above results and demonstrated the dermal absorption of Zn from different sunscreen formulations and differing UV exposure conditions.152 Recently, the uptake and distribution of 68Zn tracer in the internal organs of virgin or pregnant hairless mice were reported after application of nanosized and larger 68ZnO particles. 151 Similar to the result of human exposure, concentrations of 68Zn in organs of virgin mice treated with 68 ZnO NPs were significantly higher than in mice treated with larger 68ZnO particles. More importantly, increased concentrations 68Zn tracer was also observed in the fetal livers, demonstrating transplacental transfer of 68Zn. It is estimated that 0.0007−0.02% of bulk ZnO and 0.001−0.04% of ZnO NPs applied were absorbed in different organs, with liver having the

Figure 10. 65Cu/63Cu in soft tissue of freshwater snails (L. stagnalis) after pre-exposure to 65Cu and then dietary exposure to Cu-bearing Fe− Al particles with diatoms. Reprinted from ref 171. Copyright 2013 American Chemical Society.

4. SUMMARY AND FUTURE PERSPECTIVES Radioactive or stable isotope tracers, due to their advantage of intrinsic labeling, have proved helpful in the enhancement of detection of MENPs in the environment and organisms. An increase in their application in the tracing of MENP environmental fate, biouptake, and transformation is expected. Although isotope tracers provide great opportunities to further elucidate the behavior of MENPs in biological and environmental systems, there remain many unresolved issues and areas that require further exploration. The following advancements could enhance the significance of isotope tracer methods and contribute to understanding the distribution and fate of MENPs. 4.1. Methods for Preparing Radioactive-Isotope-Labeled Metal-Containing Engineered Nanoparticles

Currently, the reported radiolabeled MENPs are still very limited, possibly due to the lack of adequate preparation methods. There remain great challenges in the preparation of more radioactive-isotope-labeled MENPs with suitable half-lives and radioactivity to trace their behavior in biological and environmental systems. The synthesis of radiolabeled MENPs 4478

DOI: 10.1021/acs.chemrev.6b00693 Chem. Rev. 2017, 117, 4462−4487

Chemical Reviews

Review

multicollector (MC)-ICP-MS.139,141,142,153As the concentration of isotope-labeled MENPs is quantified by the variation of isotope ratio, the precision of stable isotope ratio measurements is very important for the sensitivity of MENP tracing. The use of high-resolution MC-ICP-MS could provide high-precision data with minimal levels of uncertainty and, thus, offer low detection limits and allow the detection of ENPs at environmentally or ecotoxicologically relevant concentrations against background levels.139,141 For example, by use of quadruple ICP-MS, 107 Ag/109Ag ratios can generally be measured with a precision no better than 1%. However, improved data with a precision of more than 0.02% can be obtained for 107Ag/109Ag by use of MCICP-MS coupled with an effective cleanup technique.142 Thus, the application of stable isotope labeling enhances the tracing sensitivity by at least 40-fold (for quadruple ICP-MS) and possibly by up to approximately 4000-fold (for MC-ICP-MS).142 Therefore, the application of high-precision MC-ICP-MS is highly promising to decrease the exposure concentration of MENPs to environmental or toxicologically realistic scenarios in further studies.

from their radioactive precursors or the direct radiolabeling of MENPs by use of ion-beam or neutron irradiation need to be optimized to produce MENPs of similar chemical composition, morphology, and surface modification to those we commonly used. 4.2. Effect of Surface Modification and Functionalization of Metal-Containing Engineered Nanoparticles on Their Environmental Fate and Bioaccumulation

Surface modification and functionalization of MENPs is an essential prerequisite for their successful applications,172 determining their interactions with environmental173 and biological interfaces.174 These interactions have a crucial impact not only on the colloidal stability (e.g., dissolution175 and aggregation176,177), transport,178 and environmental fate179 of MENPs but also on their uptake,180−182 blood circulation time,13,54,183 organ- or tumor-specific distribution,184,185 and toxicity186,187 in organisms. Intrinsic labeling with radioactive or stable isotopes provides a powerful tool for probing the fate of MENPs in environmental and biological systems. More importantly, coexposure of different coated/functionalized MENPs labeled with various stable isotopes (e.g., 107Ag for CIT-Ag NP and 109Ag for PVP-Ag NP) makes it possible to compare their environmental and biological behaviors simultaneously in one system.

4.6. Microcosm and Mesocosm Combined with Isotope Tracers To Study the Behavior of Metal-Containing Engineered Nanoparticles in the Environment

The fate and behavior of MENPs in the environment are highly sensitive to factors such as temperature, sunlight, natural organic matter, ionic strength, and the presence of plants, sediments, and bacteria.192 Therefore, the behavior of MENPs in highly controlled laboratory settings is unlikely to be reflective of their behavior under environmentally relevant conditions.192 Micro- or mesocosm studies could provide a more realistic approach by linking environmental scenarios with the behavior of MENPs. For example, a pond microcosm could include water, sediment, aquatic plants, and animals with varying trophic levels, which could simulate the distribution of MENPs in different compartments as well as food chain biouptake and possible bioaccumulation. Unfortunately, micro- or mesocosm experiments without the involvement of isotope tracers require high MENP concentration to distinguish their signal from that of the background. Consequently, the experimental settings do not accurately reflect the fate of environmental-level MENPs. However, the use of isotope tracers in micro- or mesocosm experiments could enhance the detection sensitivities for MENPs, and thus environmental levels of MENPs could be applied to better reflect a more realistic condition. In addition, the use of stable or radioactive isotopes with a suitable half-life allows the long-term monitoring of MENPs in environmental and biological systems, thus elucidating the long-term impacts of MENPs.

4.3. Long-Term Exposure of Metal-Containing Engineered Nanoparticles at Low Doses

The toxic effects of MENPs are usually observed under acute or subacute conditions at high doses. However, realistic exposure scenario studies of the effect of long-term (over 3 months) lowdose exposure are extremely important, but missing to a large extent, to elucidate the toxicity of MENPs.188,189 Long-term studies on the uptake, accumulation, distribution, and toxicity of MENPs are urgently needed to fully evaluate the toxicity of low MENP concentrations by using in vivo and in vitro models. Radioactive- and stable-isotope-labeled MENPs could play a critical role in tracing ultralow concentrations of MENPs in various organisms. 4.4. Imaging Techniques for Radioactive- and Stable-Isotope-Labeled Metal-Containing Engineered Nanoparticles

Imaging MENPs, in vivo or ex vivo, can provide direct information on their biodistribution and fate in organisms.190 Unfortunately, there are only a few reports on tissue imaging of radioactive-isotope-labeled MENPs in organisms by macroautoradiography and ECT techniques.32−36 High-resolution autoradiography (e.g., light microscope autoradiography37,38 and electron microscope autoradiography39,40) is suitable for cellular and subcellular localization of radioactive-isotope-labeled MENPs in biological organisms and should be further evaluated in future studies. Laser ablation−ICP-MS190 and secondary ion mass spectrometry191 could also potentially be used for 2D imaging of stable-isotope-labeled MENPs in organisms, although its spatial resolution needs to be further improved. Nevertheless, the utilization of imaging techniques will undoubtedly enrich our knowledge on the biological uptake, distribution, clearance, and possible effects of MENPs.

4.7. Hyphenated Multistable Isotope Tracers with Speciation Analysis To Compare the Behaviors of Different Engineered Nanoparticles and Metal Species

Multi-isotope tracing coupled with speciation analysis has been widely applied in species transformation and biological uptake studies of various toxic elements, especially Hg.193−195 However, to date, there are no reports on the transformation, uptake, and distribution of ENPs and metal species with multistable isotope tracers. Various speciation analytical methods have been developed to distinguish and quantify MENPs and metal ions (e.g., different-sized Ag NPs, AgCl, Ag2S, and Ag+) including ultrafiltration,196,197 cloud point extraction,198,199 size-exclusion chromatography,200 capillary electrophoresis,201 and field-flow fractionation.155,202 Multistable isotope tracers to label MENPs

4.5. High-Precision Stable Isotope Ratio Measurements To Enhance the Sensitivity of Metal-Containing Engineered Nanoparticle Tracing

The stable isotope ratio could be measured by conventional ICPMS (e.g., quadrupole ICP-MS)140,144,145 or high-resolution 4479

DOI: 10.1021/acs.chemrev.6b00693 Chem. Rev. 2017, 117, 4462−4487

Chemical Reviews

Review

and ions could be used to compare their behavior and study their intertransformation in the same system. For example: (1) through the synthesis of MENPs of varying size, morphology, or crystallinity (e.g., different-sized nano-ZnO labeled with 64Zn, 66 Zn, and 68Zn) and integration with speciation analytical techniques, their differential ion dissolution, uptake, and distribution can be compared in the same environmental or biological system. (2) In addition, different behaviors (e.g., adsorption from water to sediment, uptake by organisms) between MENPs and the corresponding metal ions can be compared by use of double stable isotope tracers (e.g., 107Ag NP and 109Ag+). (3) Last, but not least, double stable isotope tracers coupled with speciation analysis techniques could be used to measure the individual gross rates of two co-occurring transformation processes (e.g., dissolution and adsorption) simultaneously.

environmental fate and transformation of engineered nanomaterials/ toxic metals, especially by use of isotope tracing. Zhiqiang Tan was born in Shandong, China, in 1982. He obtained his B.S. in environmental sciences at Hebei University, China, in 2005 and then received his M.S. in environmental sciences under the supervision of Professor Xiandeng Hou from Sichuan University, China, in 2008. He obtained his Ph.D. in environmental sciences in 2011 under the supervision of Professor Jingfu Liu at RCEES, CAS, Beijing, China, and then became a postdoctoral researcher with Professor Guibin Jiang from 2011 to 2013. He is currently an associate professor at RCEES, CAS. His research focuses on analytical methods, environmental processes, and applications of micro/nanomaterials. Ligang Hu was born in Hubei, China, in 1976. He received his B.S. in chemistry at the University of Science and Technology, Beijing, China, in 1997 and obtained his Ph.D. in environmental sciences in 2006 from RCEES, CAS. He then continued his research at Florida International University and the University of Hong Kong as a postdoctoral fellow. He is now a professor of environmental chemistry at RCEES, CAS, with his current research focusing on environmental health and biogeochemical cycling of heavy metals.

4.8. Isotope Fractionation as a Tracer for Metal-Containing Engineered Nanoparticles

It has been reported that isotope fractionation can occur in the physical and chemical transformation of many elements, including Fe, Zn, Cu, and Cd. Isotope fractionation could be used as an intrinsic tracer to probe the source and transformation of these elements.203 Nevertheless, isotope fractionation in the transformation of MENPs is still not well understood, although studies have observed Fe isotope exchange between aqueous Fe2+ and nanoparticulate mackinawite,204,205 goethite,206 and magnetite,207 indicating possible isotope fractionation during the dissolution, adsorption, and redox transformation. Furthermore, a study found significant differences in Ag isotope ratios among a colloidal Ag dietary supplement, decanethiol-functionalized Ag NPs, and Ag in X-static socks.208 It was since demonstrated that the formation and dissolution of Ag NPs under natural conditions (e.g., under sunlight) caused significant variations in the ratio of natural Ag isotopes, with an isotopic enrichment factor of up to 0.86‰, and that engineered Ag NPs have distinctly different isotope fractionation effects than their naturally formed counterparts.209 These results suggest that the isotope ratio is a potential intrinsic tracer to differentiate between naturally occurring nanoparticles and synthetic MENPs, and to probe MENP sources as well as the transformation of MENPs in the environment.

Sujuan Yu received her Ph.D. in environmental sciences from University of Chinese Academy of Sciences in 2014 and then joined Professor Jingfu Liu’s research group. Her research focuses on the environmental behavior and effects of silver nanoparticles. Jingfu Liu is a professor of environmental chemistry at RCEES, CAS. He received his B.Sc. in 1986 from Jiangxi University and his Ph.D. in 2002 from CAS. In 2006, he finished his postdoctoral research in Lund University in Sweden and joined RCEES with the 100 Talents Project of Chinese Academy of Sciences. He was awarded the National Science Fund for Distinguished Young Scholars in 2010. He is the author and coauthor of over 200 peer-reviewed original research papers and invited reviews and coeditor of two books. His research interests involve environmental analytical chemistry, as well as environmental processes and effects of persistent toxic substances and emerging contaminants such as engineered nanomaterials. Guibin Jiang is a professor of environmental science at RCEES. He received his B.Sc. from Shandong University in 1981 and his Ph.D. from CAS in 1991. He completed his research work at the National Research Council of Canada (1989−1991) as a visiting scholar and at the University of Belgium (1994−1996) as a postdoctoral fellow. He has published more than 500 papers in peer-reviewed international scientific journals and has given more than 380 lectures, including plenary and keynote lectures at international and national meetings. Since 2006, he has been an associate editor of the journal Environmental Science & Technology, published by the American Chemical Society. He was honored with the prestigious Chang Jiang Scholars Achievement Award in 2007 and the Agilent Thought Leader Award in 2013. He was elected as a member of the Chinese Academy of Sciences in 2009 and as a fellow of the Third World Academy of Sciences in 2012. His research mainly focuses on environmental analytical chemistry and toxicology of persistent toxic substances.

AUTHOR INFORMATION Corresponding Author

*Telephone +86-10-62849192; fax +86-10-62849192; e-mail jfl[email protected]. ORCID

Jingfu Liu: 0000-0001-7134-7026 Notes

The authors declare no competing financial interest. Biographies

ACKNOWLEDGMENTS We thank the National Key Research and Development Program of China (2016YFA0203102), the National Natural Science Foundation of China (21337004, 21522705, 21377156), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB14020101), and Key Projects for Frontier Sciences of the Chinese Academy of Sciences (QYZDB-SSWDQC018) for their support. Y.Y. acknowledges support from the Youth Innovation Promotion Association of the Chinese

Yongguang Yin was born in Hebei, China, in 1981. He received his B.S. in chemistry at Chongqing University, China, in 2002 and then received his M.S. in analytical chemistry under the supervision of Professor Zhining Xia from Chongqing University in 2005. He obtained his Ph.D. in environmental sciences in 2008 with the guidance of Professor Guibin Jiang at Research Center for Eco-Environmental Sciences (RCEES), Chinese Academy of Sciences (CAS), Beijing, China. Currently, he is an associate professor at RCEES, CAS. His research focuses on 4480

DOI: 10.1021/acs.chemrev.6b00693 Chem. Rev. 2017, 117, 4462−4487

Chemical Reviews

Review

(12) Zhang, L.; Gu, F. X.; Chan, J. M.; Wang, A. Z.; Langer, R. S.; Farokhzad, O. C. Nanoparticles in Medicine: Therapeutic Applications and Developments. Clin. Pharmacol. Ther. 2008, 83, 761−769. (13) Moghimi, S. M.; Hunter, A. C.; Murray, J. C. Nanomedicine: Current Status and Future Prospects. FASEB J. 2005, 19, 311−330. (14) Lewinski, N.; Colvin, V.; Drezek, R. Cytotoxicity of Nanoparticles. Small 2008, 4, 26−49. (15) Nel, A. E.; Parak, W. J.; Chan, W. C. W.; Xia, T.; Hersam, M. C.; Brinker, C. J.; Zink, J. I.; Pinkerton, K. E.; Baer, D. R.; Weiss, P. S. Where Are We Heading in Nanotechnology Environmental Health and Safety and Materials Characterization? ACS Nano 2015, 9, 5627−5630. (16) Gibson, N.; Holzwarth, U.; Abbas, K.; Simonelli, F.; Kozempel, J.; Cydzik, I.; Cotogno, G.; Bulgheroni, A.; Gilliland, D.; Ponti, J.; et al. Radiolabelling of Engineered Nanoparticles for in Vitro and in Vivo Tracing Applications Using Cyclotron Accelerators. Arch. Toxicol. 2011, 85, 751−773. (17) Liong, M.; Lu, J.; Kovochich, M.; Xia, T.; Ruehm, S. G.; Nel, A. E.; Tamanoi, F.; Zink, J. I. Multifunctional Inorganic Nanoparticles for Imaging, Targeting, and Drug Delivery. ACS Nano 2008, 2, 889−896. (18) Shao, X.; Zhang, H. A.; Rajian, J. R.; Chamberland, D. L.; Sherman, P. S.; Quesada, C. A.; Koch, A. E.; Kotov, N. A.; Wang, X. D. I125-Labeled Gold Nanorods for Targeted Imaging of Inflammation. ACS Nano 2011, 5, 8967−8973. (19) Sun, H. W.; Zhang, L. Y.; Zhang, X. L.; Zhang, C. L.; Wei, Z. L.; Yao, S. D. Re-188-Labeled MPEG-Modified Superparamagnetic Nanogels: Preparation and Targeting Application in Rabbits. Biomed. Microdevices 2008, 10, 281−287. (20) Melancon, M. P.; Lu, W.; Yang, Z.; Zhang, R.; Cheng, Z.; Elliot, A. M.; Stafford, J.; Olson, T.; Zhang, J. Z.; Li, C. In Vitro and in Vivo Targeting of Hollow Gold Nanoshells Directed at Epidermal Growth Factor Receptor for Photothermal Ablation Therapy. Mol. Cancer Ther. 2008, 7, 1730−1739. (21) Kreyling, W. G.; Abdelmonem, A. M.; Ali, Z.; Alves, F.; Geiser, M.; Haberl, N.; Hartmann, R.; Hirn, S.; de Aberasturi, D. J.; Kantner, K.; et al. In Vivo Integrity of Polymer-Coated Gold Nanoparticles. Nat. Nanotechnol. 2015, 10, 619−623. (22) Zhang, Z. Y.; Zhao, Y. L.; Chai, Z. F. Applications of Radiotracer Techniques for the Pharmacology and Toxicology Studies of Nanomaterials. Chin. Sci. Bull. 2009, 54, 173−182. (23) Simon, F.; Kramberger, C.; Pfeiffer, R.; Kuzmany, H.; Zolyomi, V.; Kurti, J.; Singer, P. M.; Alloul, H. Isotope Engineering of Carbon Nanotube Systems. Phys. Rev. Lett. 2005, 95, No. 017401. (24) Ruan, L. F.; Chang, X. L.; Sun, B. Y.; Guo, C. B.; Dong, J. Q.; Yang, S. T.; Gao, X. F.; Zhao, Y. L.; Yang, M. Preparation and spectra of 13Cenriched fullerene. Kexue Tongbao (Chin. Ed.) 2014, 59, 905−912. (25) Freund, B.; Tromsdorf, U. I.; Bruns, O. T.; Heine, M.; Giemsa, A.; Bartelt, A.; Salmen, S. C.; Raabe, N.; Heeren, J.; Ittrich, H.; et al. A Simple and Widely Applicable Method to Fe-59-Radiolabel Monodisperse Superparamagnetic Iron Oxide Nanoparticles for In Vivo Quantification Studies. ACS Nano 2012, 6, 7318−7325. (26) Volkert, W. A.; Hoffman, T. J. Therapeutic Radiopharmaceuticals. Chem. Rev. 1999, 99, 2269−2292. (27) Cutler, C. S.; Hennkens, H. M.; Sisay, N.; Huclier-Markai, S.; Jurisson, S. S. Radiometals for Combined Imaging and Therapy. Chem. Rev. 2013, 113, 858−883. (28) Holzwarth, U.; Bulgheroni, A.; Gibson, N.; Kozempel, J.; Cotogno, G.; Abbas, K.; Simonelli, F.; Cydzik, I. Radiolabelling of Nanoparticles by Proton Irradiation: Temperature Control in Nanoparticulate Powder Targets. J. Nanopart. Res. 2012, 14, No. 880. (29) Hildebrand, H.; Franke, K. A New Radiolabeling Method for Commercial Ag0 Nanopowder with Ag-110m for Sensitive Nanoparticle Detection in Complex Media. J. Nanopart. Res. 2012, 14, No. 1142. (30) Zhao, C. M.; Wang, W. X. Biokinetic Uptake and Efflux of Silver Nanoparticles in Daphnia magna. Environ. Sci. Technol. 2010, 44, 7699− 7704. (31) Zhao, C. M.; Wang, W. X. Size-Dependent Uptake of Silver Nanoparticles in Daphnia magna. Environ. Sci. Technol. 2012, 46, 11345−11351.

Academy of Sciences. We also express our sincere thanks to the anonymous reviewers for their valuable comments and suggestions on this paper.

ABBREVIATIONS Ag NP silver nanoparticle Au NP gold nanoparticle BSA bovine serum albumin CIT citrate Co@Co3O4 Co core/Co3O4 shell Cu NC copper nanocluster EC electron capture ECT emission computed tomography EGCg epigallocatechin−gallate ENP engineered nanoparticle ICP-MS inductively coupled plasma mass spectrometry LHRH luteinizing hormone-releasing hormone MC-ICP-MS multicollector inductively coupled plasma mass spectrometry MENP metal-containing engineered nanoparticle NP nanoparticle nZVI zerovalent iron nanoparticle PEG poly(ethylene glycol) PET positron emission tomography PVP poly(vinylpyrrolidone) QD quantum dot SPECT single-photon emission computed tomography TEM transmission electron microscope REFERENCES (1) Morris, J.; Willis, J.; Gallagher, K. Nanotechnology White Paper, EPA 100/B-07/001; U.S. Environmental Protection Agency, Washington, DC, 2007; https://www.epa.gov/sites/production/files/2015-01/ documents/nanotechnology_whitepaper.pdf. (2) Crooks, R. M.; Zhao, M. Q.; Sun, L.; Chechik, V.; Yeung, L. K. Dendrimer-Encapsulated Metal Nanoparticles: Synthesis, Characterization, and Applications to Catalysis. Acc. Chem. Res. 2001, 34, 181− 190. (3) Anker, J. N.; Hall, W. P.; Lyandres, O.; Shah, N. C.; Zhao, J.; Van Duyne, R. P. Biosensing with Plasmonic Nanosensors. Nat. Mater. 2008, 7, 442−453. (4) Willets, K. A.; Van Duyne, R. P. Localized Surface Plasmon Resonance Spectroscopy and Sensing. Annu. Rev. Phys. Chem. 2007, 58, 267−297. (5) Jain, P. K.; Huang, X. H.; El-Sayed, I. H.; El-Sayed, M. A. Noble Metals on the Nanoscale: Optical and Photothermal Properties and Some Applications in Imaging, Sensing, Biology, and Medicine. Acc. Chem. Res. 2008, 41, 1578−1586. (6) Loo, C.; Lin, A.; Hirsch, L.; Lee, M. H.; Barton, J.; Halas, N. J.; West, J.; Drezek, R. Nanoshell-Enabled Photonics-Based Imaging and Therapy of Cancer. Technol. Cancer Res. Treat. 2004, 3, 33−40. (7) Nowack, B.; Bucheli, T. D. Occurrence, Behavior and Effects of Nanoparticles in the Environment. Environ. Pollut. 2007, 150, 5−22. (8) Richardson, S. D. Environmental Mass Spectrometry: Emerging Contaminants and Current Issues. Anal. Chem. 2012, 84, 747−778. (9) Lowry, G. V.; Gregory, K. B.; Apte, S. C.; Lead, J. R. Transformations of Nanomaterials in the Environment. Environ. Sci. Technol. 2012, 46, 6893−6899. (10) Wiesner, M. R.; Lowry, G. V.; Alvarez, P.; Dionysiou, D.; Biswas, P. Assessing the Risks of Manufactured Nanomaterials. Environ. Sci. Technol. 2006, 40, 4336−4345. (11) Petros, R. A.; DeSimone, J. M. Strategies in the Design of Nanoparticles for Therapeutic Applications. Nat. Rev. Drug Discovery 2010, 9, 615−627. 4481

DOI: 10.1021/acs.chemrev.6b00693 Chem. Rev. 2017, 117, 4462−4487

Chemical Reviews

Review

CJFDTOTAL-TWSZ200101009.htm; abstract in English, paper in Chinese). (51) Yin, Q. H.; Liu, L.; Gu, N.; Huang, Y.; Liu, L.; Song, J. H.; Cui, Y. Determining the biodistribution of nano-Fe2O3-Glu in mice by 59Fe tracer and preparation. J. Med. Postgrad. 2005, 18, 312−317 (in Chinese). (52) Zhou, M.; Zhang, R.; Huang, M. A.; Lu, W.; Song, S. L.; Melancon, M. P.; Tian, M.; Liang, D.; Li, C. A Chelator-Free Multifunctional [Cu-64]CuS Nanoparticle Platform for Simultaneous Micro-PET/CT Imaging and Photothermal Ablation Therapy. J. Am. Chem. Soc. 2010, 132, 15351−15358. (53) Molina, R. M.; Konduru, N. V.; Jimenez, R. J.; Pyrgiotakis, G.; Demokritou, P.; Wohlleben, W.; Brain, J. D. Bioavailability, Distribution and Clearance of Tracheally Instilled, Gavaged or Injected Cerium Dioxide Nanoparticles and Ionic Cerium. Environ. Sci.: Nano 2014, 1, 561−573. (54) Lipka, J.; Semmler-Behnke, M.; Sperling, R. A.; Wenk, A.; Takenaka, S.; Schleh, C.; Kissel, T.; Parak, W. J.; Kreyling, W. G. Biodistribution of PEG-Modified Gold Nanoparticles Following Intratracheal Instillation and Intravenous Injection. Biomaterials 2010, 31, 6574−6581. (55) Konduru, N.; Keller, J.; Ma-Hock, L.; Groters, S.; Landsiedel, R.; Donaghey, T. C.; Brain, J. D.; Wohlleben, W.; Molina, R. M. Biokinetics and Effects of Barium Sulfate Nanoparticles. Part. Fibre Toxicol. 2014, 11, No. 55. (56) Portet, D.; Denizot, B.; Rump, E.; Hindre, F.; Le Jeune, J. J.; Jallet, P. Comparative Biodistribution of Thin-Coated Iron Oxide Nanoparticles TCION: Effect of Different Bisphosphonate Coatings. Drug Dev. Res. 2001, 54, 173−181. (57) Zhao, Y. F.; Sultan, D.; Detering, L.; Cho, S. H.; Sun, G. R.; Pierce, R.; Wooley, K. L.; Liu, Y. J. Copper-64-Alloyed Gold Nanoparticles for Cancer Imaging: Improved Radiolabel Stability and Diagnostic Accuracy. Angew. Chem., Int. Ed. 2014, 53, 156−159. (58) Rambanapasi, C.; Barnard, N.; Grobler, A.; Buntting, H.; Sonopo, M.; Jansen, D.; Jordaan, A.; Steyn, H.; Zeevaart, J. R. Dual Radiolabeling as a Technique to Track Nanocarriers: The Case of Gold Nanoparticles. Molecules 2015, 20, 12863−12879. (59) Liu, L.; Tang, M.; Liu, L.; Yin, Q. H.; Wang, B.; Xiong, L. L.; Gu, N.; Ma, M.; Zhang, Y. The Pharmacokinetics Study of Nanoparticles of Fe2O3 Coated with Glutamic Acid. J. Environ. Occup. Med. 2006, 23, 1−3 (in Chinese). (60) Yang, L. K.; Sundaresan, G.; Sun, M. H.; Jose, P.; Hoffman, D.; McDonagh, P. R.; Lamichhane, N.; Cutler, C. S.; Perez, J. M.; Zweit, J. Intrinsically Radiolabeled Multifunctional Cerium Oxide Nanoparticles for in Vivo Studies. J. Mater. Chem. B 2013, 1, 1421−1431. (61) Pouliquen, D.; Lejeune, J. J.; Perdrisot, R.; Ermias, A.; Jallet, P. Iron-Oxide Nanoparticles for Use as an Mri Contrast Agent Pharmacokinetics and Metabolism. Magn. Reson. Imaging 1991, 9, 275−283. (62) Hirn, S.; Semmler-Behnke, M.; Schleh, C.; Wenk, A.; Lipka, J.; Schaffler, M.; Takenaka, S.; Möller, W.; Schmid, G.; Simon, U.; Kreyling, W. G. Particle Size-Dependent and Surface Charge-Dependent Biodistribution of Gold Nanoparticles after Intravenous Administration. Eur. J. Pharm. Biopharm. 2011, 77, 407−416. (63) Wang, Y. C.; Liu, Y. J.; Luehmann, H.; Xia, X. H.; Wan, D. H.; Cutler, C.; Xia, Y. N. Radioluminescent Gold Nanocages with Controlled Radioactivity for Real-Time in Vivo Imaging. Nano Lett. 2013, 13, 581−585. (64) Konduru, N. V.; Jimenez, R. J.; Swami, A.; Friend, S.; Castranova, V.; Demokritou, P.; Brain, J. D.; Molina, R. M. Silica Coating Influences the Corona and Biokinetics of Cerium Oxide Nanoparticles. Part. Fibre Toxicol. 2015, 12, No. 31. (65) Kwon, M.; Park, J. H.; Jang, B. S.; Jung, H. Synthesis and Biodistribution of Cat’s Eye-shaped [Co-57]CoO@SiO2 Nanoshell Aqueous Colloids for Single Photon Emission Computed Tomography (SPECT) Imaging Agent. Bull. Korean Chem. Soc. 2014, 35, 2367−2370. (66) Sun, M. H.; Hoffman, D.; Sundaresan, G.; Yang, L. K.; Lamichhane, N.; Zweit, J. Synthesis and Characterization of Intrinsically Radiolabeled Quantum Dots for Bimodal Detection. Am. J. Nucl. Med.

(32) Al-Sid-Cheikh, M.; Pelletier, E.; Rouleau, C. Synthesis and Characterization of [Ag-110m]-Nanoparticles with Application to Whole-Body Autoradiography of Aquatic Organisms. Appl. Radiat. Isot. 2011, 69, 1415−1421. (33) Zhang, Z. Y.; He, X.; Zhang, H. F.; Ma, Y. H.; Zhang, P.; Ding, Y. Y.; Zhao, Y. L. Uptake and Distribution of Ceria Nanoparticles in Cucumber Plants. Metallomics 2011, 3, 816−822. (34) Zuykov, M.; Pelletier, E.; Demers, S. Colloidal Complexed Silver and Silver Nanoparticles in Extrapallial Fluid of Mytilus edulis. Mar. Environ. Res. 2011, 71, 17−21. (35) Al-Sid-Cheikh, M.; Rouleau, C.; Pelletier, E. Tissue Distribution and Kinetics of Dissolved and Nanoparticulate Silver in Iceland Scallop (Chlamys islandica). Mar. Environ. Res. 2013, 86, 21−28. (36) Chen, C. H.; Lin, F. S.; Liao, W. N.; Liang, S. C. L.; Chen, M. H.; Chen, Y. W.; Lin, W. Y.; Hsu, M. H.; Wang, M. Y.; Peir, J. J.; et al. Establishment of a Trimodality Analytical Platform for Tracing, Imaging and Quantification of Gold Nanoparticles in Animals by Radiotracer Techniques. Anal. Chem. 2015, 87, 601−608. (37) Mize, R. R. Quantitative Image-Analysis for Immunocytochemistry and in-Situ Hybridization. J. Neurosci. Methods 1994, 54, 219−237. (38) Bertherat, J.; Slama, A.; Kordon, C.; Videau, C.; Epelbaum, J. Characterization of Pericellular [I-125i]Tyr0 Dtrp8 Somatostatin Binding-Sites in the Rat Arcuate Nucleus by a Newly Developed Method - Quantitative High-Resolution Light Microscopic Autoradiography. Neuroscience 1991, 41, 571−579. (39) Caro, L. G.; van Tubergen, R. P. High-Resolution Autoradiography.1. Methods. J. Cell Biol. 1962, 15, 173−188. (40) Salpeter, M. M.; Bachmann, L.; Salpeter, E. E. Resolution in Electron Microscope Radioautography. J. Cell Biol. 1969, 41, 1−20. (41) Pang, B.; Zhao, Y. F.; Luehmann, H.; Yang, X.; Detering, L.; You, M.; Zhang, C.; Zhang, L.; Li, Z. Y.; Ren, Q. S.; et al. Cu-64-Doped PdCu@Au Tripods: A Multifunctional Nanomaterial for Positron Emission Tomography and Image-Guided Photothermal Cancer Treatment. ACS Nano 2016, 10, 3121−3131. (42) Ponti, J.; Colognato, R.; Franchini, F.; Gioria, S.; Simonelli, F.; Abbas, K.; Uboldi, C.; Kirkpatrick, C. J.; Holzwarth, U.; Rossi, F. A Quantitative in Vitro Approach to Study the Intracellular Fate of Gold Nanoparticles: from Synthesis to Cytotoxicity. Nanotoxicology 2009, 3, 296−306. (43) Gornati, R.; Pedretti, E.; Rossi, F.; Cappellini, F.; Zanella, M.; Olivato, I.; Sabbioni, E.; Bernardini, G. Zerovalent Fe, Co and Ni Nanoparticle Toxicity Evaluated on SKOV-3 and U87 Cell Lines. J. Appl. Toxicol. 2016, 36, 385−393. (44) Simonelli, F.; Marmorato, P.; Abbas, K.; Ponti, J.; Kozempel, J.; Holzwarth, U.; Franchini, F.; Rossi, F. Cyclotron Production of Radioactive CeO2 Nanoparticles and Their Application for In Vitro Uptake Studies. IEEE Trans. Nanobiosci. 2011, 10, 44−50. (45) Taya, A.; Mewhinney, J. A. Cytotoxicity, Uptake and Dissolution of (AmO2)-Am-214 Particles in Dog Alveolar Macrophages in Vitro. Int. J. Radiat. Biol. 1992, 62, 81−88. (46) Taya, A.; Carmack, D. B.; Muggenburg, B. A.; Mewhinney, J. A. An Interspecies Comparison of the Phagocytosis and Dissolution of (AmO2)-Am-241 Particles by Rat, Dog and Monkey Alveolar Macrophages in Vitro. Int. J. Radiat. Biol. 1992, 62, 89−95. (47) Kreyling, W. G.; Godleski, J. J.; Kariya, S. T.; Rose, R. M.; Brain, J. D. In Vitro Dissolution of Uniform Cobalt Oxide Particles by Human and Canine Alveolar Macrophages. Am. J. Respir. Cell Mol. Biol. 1990, 2, 413−422. (48) Cohen, J. M.; Derk, R.; Wang, L. Y.; Godleski, J.; Kobzik, L.; Brain, J.; Demokritou, P. Tracking Translocation of Industrially Relevant Engineered Nanomaterials (ENMs) across Alveolar Epithelial Monolayers. Nanotoxicology 2014, 8, 216−225. (49) Sharifi, S.; Behzadi, S.; Laurent, S.; Forrest, M. L.; Stroeve, P.; Mahmoudi, M. Toxicity of Nanomaterials. Chem. Soc. Rev. 2012, 41, 2323−2343. (50) Fan, W.; Yang, K.; Qian, J. H.; Zhu, R.; Zhu, B. X. Determining the Distribution of Nano-particles Magnetic Iron Oxide in Mice by 59Fe Tracer. J. Isot. 2001, 14, 31−35 ( http://en.cnki.com.cn/Article_en/ 4482

DOI: 10.1021/acs.chemrev.6b00693 Chem. Rev. 2017, 117, 4462−4487

Chemical Reviews

Review

Mol. Imaging 2012, 2, 122−135 ( https://www.ncbi.nlm.nih.gov/pmc/ articles/PMC3477726/). (67) Bargheer, D.; Giemsa, A.; Freund, B.; Heine, M.; Waurisch, C.; Stachowski, G. M.; Hickey, S. G.; Eychmuller, A.; Heeren, J.; Nielsen, P. The Distribution and Degradation of Radiolabeled Superparamagnetic Iron Oxide Nanoparticles and Quantum Dots in Mice. Beilstein J. Nanotechnol. 2015, 6, 111−123. (68) Bargheer, D.; Nielsen, J.; Gebel, G.; Heine, M.; Salmen, S. C.; Stauber, R.; Weller, H.; Heeren, J.; Nielsen, P. The Fate of a Designed Protein Corona on Nanoparticles in Vitro and in Vivo. Beilstein J. Nanotechnol. 2015, 6, 36−46. (69) Chen, J. K.; Shih, M. H.; Peir, J. J.; Liu, C. H.; Chou, F. I.; Lai, W. H.; Chang, L. W.; Lin, P. P.; Wang, M. Y.; Yang, M. H.; et al. The Use of Radioactive Zinc Oxide Nanoparticles in Determination of Their Tissue Concentrations Following Intravenous Administration in Mice. Analyst 2010, 135, 1742−1746. (70) Semmler-Behnke, M.; Lipka, J.; Wenk, A.; Hirn, S.; Schaffler, M.; Tian, F. R.; Schmid, G.; Oberdorster, G.; Kreyling, W. G. Size Dependent Translocation and Fetal Accumulation of Gold Nanoparticles from Maternal Blood in the Rat. Part. Fibre Toxicol. 2014, 11, No. 33. (71) Yeh, T. K.; Chen, J. K.; Lin, C. H.; Yang, M. H.; Yang, C. S.; Chou, F. I.; Peir, J. J.; Wang, M. Y.; Chang, W. H.; Tsai, M. H.; et al. Kinetics and Tissue Distribution of Neutron-Activated Zinc Oxide Nanoparticles and Zinc Nitrate in Mice: Effects of Size and Particulate Nature. Nanotechnology 2012, 23, 085102. (72) Chouly, C.; Pouliquen, D.; Lucet, I.; Jeune, J. J.; Jallet, P. Development of Superparamagnetic Nanoparticles for MRI: Effect of Particle Size, Charge and Surface Nature on Biodistribution. J. Microencapsulation 1996, 13, 245−255. (73) Black, K. C. L.; Wang, Y. C.; Luehmann, H. P.; Cai, X.; Xing, W. X.; Pang, B.; Zhao, Y. F.; Cutler, C. S.; Wang, L. H. V.; Liu, Y. J.; et al. Radioactive Au-198-Doped Nanostructures with Different Shapes for In Vivo Analyses of Their Biodistribution, Tumor Uptake, and Intratumoral Distribution. ACS Nano 2014, 8, 4385−4394. (74) Schaffler, M.; Sousa, F.; Wenk, A.; Sitia, L.; Hirn, S.; Schleh, C.; Haberl, N.; Violatto, M.; Canovi, M.; Andreozzi, P.; et al. Blood Protein Coating of Gold Nanoparticles as Potential Tool for Organ Targeting. Biomaterials 2014, 35, 3455−3466. (75) Jung, C. S. L.; Heine, M.; Freund, B.; Reimer, R.; Koziolek, E. J.; Kaul, M. G.; Kording, F.; Schumacher, U.; Weller, H.; Nielsen, P.; et al. Quantitative Activity Measurements of Brown Adipose Tissue at 7 T Magnetic Resonance Imaging After Application of Triglyceride-Rich Lipoprotein 59Fe-Superparamagnetic Iron Oxide Nanoparticle Intravenous Versus Intraperitoneal Approach. Invest. Radiol. 2016, 51, 194− 202. (76) Shukla, R.; Chanda, N.; Zambre, A.; Upendran, A.; Katti, K.; Kulkarni, R. R.; Nune, S. K.; Casteel, S. W.; Smith, C. J.; Vimal, J.; et al. Laminin Receptor Specific Therapeutic Gold Nanoparticles ((AuNP)Au-198-EGCg) Show Efficacy in Treating Prostate Cancer. Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 12426−12431. (77) Gao, F. P.; Cai, P. J.; Yang, W. J.; Xue, J. Q.; Gao, L.; Liu, R.; Wang, Y. L.; Zhao, Y. W.; He, X.; Zhao, L. N.; et al. Ultrasmall [Cu-64] Cu Nanoclusters for Targeting Orthotopic Lung Tumors Using Accurate Positron Emission Tomography Imaging. ACS Nano 2015, 9, 4976− 4986. (78) Schleh, C.; Holzwarth, U.; Hirn, S.; Wenk, A.; Simonelli, F.; Schaffler, M.; Möller, W.; Gibson, N.; Kreyling, W. G. Biodistribution of Inhaled Gold Nanoparticles in Mice and the Influence of Surfactant Protein D. J. Aerosol Med. Pulm. Drug Delivery 2013, 26, 24−30. (79) Kreyling, W. G.; Semmler-Behnke, M.; Seitz, J.; Scymczak, W.; Wenk, A.; Mayer, P.; Takenaka, S.; Oberdorster, G. Size Dependence of the Translocation of Inhaled Iridium and Carbon Nanoparticle Aggregates from the Lung of Rats to the Blood and Secondary Target Organs. Inhalation Toxicol. 2009, 21, 55−60. (80) Zhu, M. T.; Feng, W. Y.; Wang, Y.; Wang, B.; Wang, M.; Ouyang, H.; Zhao, Y. L.; Chai, Z. F. Particokinetics and Extrapulmonary Translocation of Intratracheally Instilled Ferric Oxide Nanoparticles in

Rats and the Potential Health Risk Assessment. Toxicol. Sci. 2008, 107, 342−351. (81) Konduru, N. V.; Murdaugh, K. M.; Sotiriou, G. A.; Donaghey, T. C.; Demokritou, P.; Brain, J. D.; Molina, R. M. Bioavailability, Distribution and Clearance of Tracheally-Instilled and Gavaged Uncoated or Silica-Coated Zinc Oxide Nanoparticles. Part. Fibre Toxicol. 2014, 11, No. 44. (82) Kreyling, W. G.; Andre, S.; Collier, C. G.; Ferron, G. A.; Metivier, H.; Schumann, G. Interspecies Comparison of Lung Clearance after Inhalation of Monodisperse, Solid Cobalt Oxide Aerosol-Particles. J. Aerosol Sci. 1991, 22, 509−535. (83) Kreyling, W. G.; Semmler, M.; Erbe, F.; Mayer, P.; Takenaka, S.; Schulz, H.; Oberdorster, G.; Ziesenis, A. Translocation of Ultrafine Insoluble Iridium Particles from Lung Epithelium to Extrapulmonary Organs is Size Dependent but Very Low. J. Toxicol. Environ. Health, Part A 2002, 65, 1513−1530. (84) Kreyling, W. G.; Hirn, S.; Möller, W.; Schleh, C.; Wenk, A.; Celik, G.; Lipka, J.; Schaffler, M.; Haberl, N.; Johnston, B. D.; et al. Air-Blood Barrier Translocation of Tracheally Instilled Gold Nanoparticles Inversely Depends on Particle Size. ACS Nano 2014, 8, 222−233. (85) Semmler, M.; Seitz, J.; Erbe, F.; Mayer, P.; Heyder, J.; Oberdorster, G.; Kreyling, W. G. Long-Term Clearance Kinetics of Inhaled Ultrafine Insoluble Iridium Particles from the Rat Lung, including Transient Translocation into Secondary Organs. Inhalation Toxicol. 2004, 16, 453−459. (86) He, X. A.; Zhang, H. F.; Ma, Y. H.; Bai, W.; Zhang, Z. Y.; Lu, K.; Ding, Y. Y.; Zhao, Y. L.; Chai, Z. F. Lung Deposition and Extrapulmonary Translocation of Nano-ceria after Intratracheal Instillation. Nanotechnology 2010, 21, 285103. (87) Liang, F.; Li, C.; Jiang, R. F.; Lin, J.; Liu, W.; Jin, C.; Song, W. M.; Fan, W.; Zhang, G. L.; Li, Y. Permeating Process of Nanoparticles Labeled by 59Fe in Rat Lung. Nuclear Technol. 2007, 30, 763−767 (in Chinese). (88) Latunde-Dada, G. O.; Pereira, D. I. A.; Tempest, B.; Ilyas, H.; Flynn, A. C.; Aslam, M. F.; Simpson, R. J.; Powell, J. J. A Nanoparticulate Ferritin-Core Mimetic Is Well Taken Up by HuTu 80 Duodenal Cells and Its Absorption in Mice Is Regulated by Body Iron. J. Nutr. 2014, 144, 1896−1902. (89) Hughes, M. F.; Long, T. C.; Boyes, W. K.; Ramabhadran, R. Whole-Body Retention and Distribution of Orally Administered Radiolabelled Zerovalent Iron Nanoparticles in Mice. Nanotoxicology 2012, 7, 1064−1069. (90) Schleh, C.; Semmler-Behnke, M.; Lipka, J.; Wenk, A.; Hirn, S.; Schaffler, M.; Schmid, G.; Simon, U.; Kreyling, W. G. Size and Surface Charge of Gold Nanoparticles Determine Absorption Across Intestinal Barriers and Accumulation in Secondary Target Organs after Oral Administration. Nanotoxicology 2012, 6, 36−46. (91) Oughton, D. H.; Hertel-Aas, T.; Pellicer, E.; Mendoza, E.; Joner, E. J. Neutron Activation of Engineered Nanoparticles as a Tool for Tracing Their Environmental Fate and Uptake in Organisms. Environ. Toxicol. Chem. 2008, 27, 1883−1887. (92) Melnik, E. A.; Buzulukov, Y. P.; Demin, V. F.; Demin, V. A.; Gmoshinski, I. V.; Tyshko, N. V.; Tutelyan, V. A. Transfer of Silver Nanoparticles through the Placenta and Breast Milk during in vivo Experiments on Rats. ActaNaturae 2013, 5, 107−115 ( https://www. ncbi.nlm.nih.gov/pmc/articles/PMC3848846/). (93) Ates, M.; Arslan, Z.; Demir, V.; Daniels, J.; Farah, I. O. Accumulation and Toxicity of CuO and ZnO Nanoparticles Through Waterborne and Dietary Exposure of Goldfish (Carassius auratus). Environ. Toxicol. 2015, 30, 119−128. (94) Buffet, P. E.; Poirier, L.; Zalouk-Vergnoux, A.; Lopes, C.; Amiard, J. C.; Gaudin, P.; Risso-de Faverney, C.; Guibbolini, M.; Gilliland, D.; Perrein-Ettajani, H.; Valsami-Jones, E.; et al. Biochemical and Behavioural Responses of the Marine Polychaete Hediste diversicolor to Cadmium Sulfide Quantum Dots (CdS QDs): Waterborne and Dietary Exposure. Chemosphere 2014, 100, 63−70. (95) Li, W. M.; Wang, W. X. Distinct Biokinetic Behavior of ZnO Nanoparticles in Daphnia magna Quantified by Synthesizing Zn-65 Tracer. Water Res. 2013, 47, 895−902. 4483

DOI: 10.1021/acs.chemrev.6b00693 Chem. Rev. 2017, 117, 4462−4487

Chemical Reviews

Review

(96) Asztemborska, M.; Jakubiak, M.; Ksiazyk, M.; Steborowski, R.; Polkowska-Motrenko, H.; Bystrzejewska-Piotrowska, G. Silver Nanoparticle Accumulation by Aquatic Organisms - Neutron Activation as a Tool for the Environmental Fate of Nanoparticles Tracing. Nukleonika 2014, 59, 169−173. (97) Jung, Y. J.; Kim, K. T.; Kim, J. Y.; Yang, S. Y.; Lee, B. G.; Kim, S. D. Bioconcentration and Distribution of Silver Nanoparticles in Japanese Medaka (Oryzias latipes). J. Hazard. Mater. 2014, 267, 206−213. (98) Wang, J.; Wang, W. X. Salinity Influences on the Uptake of Silver Nanoparticles and Silver Nitrate by Marine Medaka (Oryzias melastigma). Environ. Toxicol. Chem. 2014, 33, 632−640. (99) Lu, K.; Zhang, Z. Y.; He, X. A.; Ma, Y. H.; Zhou, K. B.; Zhang, H. F.; Bai, W.; Ding, Y. Y.; Wu, Z. Q.; Zhao, Y. L.; et al. Bioavailability and Distribution and of Ceria Nanoparticles in Simulated Aquatic Ecosystems, Quantification with a Radiotracer Technique. J. Nanosci. Nanotechnol. 2010, 10, 8658−8662. (100) Zhang, P.; He, X.; Ma, Y. H.; Lu, K.; Zhao, Y. L.; Zhang, Z. Y. Distribution and Bioavailability of Ceria Nanoparticles in an Aquatic Ecosystem Model. Chemosphere 2012, 89, 530−535. (101) Lin, D. H.; Xing, B. S. Root Uptake and Phytotoxicity of ZnO Nanoparticles. Environ. Sci. Technol. 2008, 42, 5580−5585. (102) Stampoulis, D.; Sinha, S. K.; White, J. C. Assay-Dependent Phytotoxicity of Nanoparticles to Plants. Environ. Sci. Technol. 2009, 43, 9473−9479. (103) Dimkpa, C. O.; McLean, J. E.; Latta, D. E.; Manangon, E.; Britt, D. W.; Johnson, W. P.; Boyanov, M. I.; Anderson, A. J. CuO and ZnO Nanoparticles: Phytotoxicity, Metal speciation, and Induction of Oxidative Stress in Sand-Grown Wheat. J. Nanopart. Res. 2012, 14, No. 1125. (104) Dimkpa, C. O.; McLean, J. E.; Martineau, N.; Britt, D. W.; Haverkamp, R.; Anderson, A. J. Silver Nanoparticles Disrupt Wheat (Triticum aestivum L.) Growth in a Sand Matrix. Environ. Sci. Technol. 2013, 47, 1082−1090. (105) Dimkpa, C. O.; Latta, D. E.; McLean, J. E.; Britt, D. W.; Boyanov, M. I.; Anderson, A. J. Fate of CuO and ZnO Nano- and Microparticles in the Plant Environment. Environ. Sci. Technol. 2013, 47, 4734−4742. (106) Hernandez-Viezcas, J. A.; Castillo-Michel, H.; Andrews, J. C.; Cotte, M.; Rico, C.; Peralta-Videa, J. R.; Ge, Y.; Priester, J. H.; Holden, P. A.; Gardea-Torresdey, J. L. In Situ Synchrotron X-ray Fluorescence Mapping and Speciation of CeO2 and ZnO Nanoparticles in Soil Cultivated Soybean (Glycine max). ACS Nano 2013, 7, 1415−1423. (107) Servin, A. D.; Morales, M. I.; Castillo-Michel, H.; HernandezViezcas, J. A.; Munoz, B.; Zhao, L. J.; Nunez, J. E.; Peralta-Videa, J. R.; Gardea-Torresdey, J. L. Synchrotron Verification of TiO2 Accumulation in Cucumber Fruit: A Possible Pathway of TiO2 Nanoparticle Transfer from Soil into the Food Chain. Environ. Sci. Technol. 2013, 47, 11592− 11598. (108) Larue, C.; Castillo-Michel, H.; Sobanska, S.; Cecillon, L.; Bureau, S.; Barthes, V.; Ouerdane, L.; Carriere, M.; Sarret, G. Foliar Exposure of the Crop Lactuca sativa to Silver Nanoparticles: Evidence for Internalization and Changes in Ag Speciation. J. Hazard. Mater. 2014, 264, 98−106. (109) Larue, C.; Castillo-Michel, H.; Sobanska, S.; Trcera, N.; Sorieul, S.; Cecillon, L.; Ouerdane, L.; Legros, S.; Sarret, G. Fate of Pristine TiO2 Nanoparticles and Aged Paint-Containing TiO2 Nanoparticles in Lettuce Crop after Foliar Exposure. J. Hazard. Mater. 2014, 273, 17−26. (110) Hong, J.; Peralta-Videa, J. R.; Rico, C.; Sahi, S.; Viveros, M. N.; Bartonjo, J.; Zhao, L. J.; Gardea-Torresdey, J. L. Evidence of Translocation and Physiological Impacts of Foliar Applied CeO2 Nanoparticles on Cucumber (Cucumis sativus) Plants. Environ. Sci. Technol. 2014, 48, 4376−4385. (111) Ma, X. M.; Geiser-Lee, J.; Deng, Y.; Kolmakov, A. Interactions between Engineered Nanoparticles (ENPs) and Plants: Phytotoxicity, Uptake and Accumulation. Sci. Total Environ. 2010, 408, 3053−3061. (112) Gardea-Torresdey, J. L.; Rico, C. M.; White, J. C. Trophic Transfer, Transformation, and Impact of Engineered Nanomaterials in Terrestrial Environments. Environ. Sci. Technol. 2014, 48, 2526−2540. (113) Bystrzejewska-Piotrowska, G.; Asztemborska, M.; Steborowski, R.; Polkowska-Motrenko, H.; Danko, B.; Ryniewicz, J. Application of

Neutron Activation for Investigation of Fe3O4 Nanoparticles Accumulation by Plants. Nukleonika 2012, 57, 427−430 ( http://www. nukleonika.pl/www/back/full/vol57_2012/v57n3p427f.pdf). (114) Coutris, C.; Joner, E. J.; Oughton, D. H. Aging and Soil Organic Matter Content Affect the Fate of Silver Nanoparticles in Soil. Sci. Total Environ. 2012, 420, 327−333. (115) Meiring, J. J.; Borm, P. J.; Bagate, K.; Semmler, M.; Seitz, J.; Takenaka, S.; Kreyling, W. G. The Influence of Hydrogen Peroxide and Histamine on Lung Permeability and Translocation of Iridium Nanoparticles in the Isolated Perfused Rat Lung. Part. Fibre Toxicol. 2005, 2, No. 3. (116) Harper, R. A.; Stirling, C.; Townsend, K. M. S.; Kreyling, W. G.; Patrick, G. Intracellular Particle Dissolution in Macrophages Isolated from the Lung of the Fischer (F-344) Rat. Exp. Lung Res. 1994, 20, 143− 156. (117) Kannan, R.; Zambre, A.; Chanda, N.; Kulkarni, R.; Shukla, R.; Katti, K.; Upendran, A.; Cutler, C.; Boote, E.; Katti, K. V. Functionalized Radioactive Gold Nanoparticles in Tumor Therapy. Wiley Interdis. Rev. Nanomed. Nanobiotech. 2012, 4, 42−51. (118) Zhou, M.; Chen, Y. Y.; Adachi, M.; Wen, X. X.; Erwin, B.; Mawlawi, O.; Lai, S. Y.; Li, C. Single Agent Nanoparticle for Radiotherapy and Radio-photothermal Therapy in Anaplastic Thyroid Cancer. Biomaterials 2015, 57, 41−49. (119) Khan, M. K.; Minc, L. D.; Nigavekar, S. S.; Kariapper, M. S. T.; Nair, B. M.; Schipper, M.; Cook, A. C.; Lesniak, W. G.; Balogh, L. P. Fabrication of {Au-198(0)} Radioactive Composite Nanodevices and Their Use for Nanobrachytherapy. Nanomedicine 2008, 4, 57−69. (120) Axiak-Bechtel, A. M.; Upendran, A.; Lattimer, J. C.; Kelsey, J.; Cutler, C. S.; Selting, K. A.; Bryan, J. N.; Henry, C. J.; Boote, E.; Tate, D. J.; et al. Gum Arabic-Coated Radioactive Gold Nanoparticles Cause No Short-Term Local or Systemic Toxicity in the Clinically Relevant Canine Model of Prostate Cancer. Int. J. Nanomed. 2014, 9, 5001−5011. (121) Chanda, N.; Kan, P.; Watkinson, L. D.; Shukla, R.; Zambre, A.; Carmack, T. L.; Engelbrecht, H.; Lever, J. R.; Katti, K.; Fent, G. M.; et al. Radioactive Gold Nanoparticles in Cancer Therapy: Therapeutic Efficacy Studies of GA-(AuNP)-Au-198 Nanoconstruct in Prostate Tumor-Bearing Mice. Nanomedicine 2010, 6, 201−209. (122) Semmler-Behnke, M.; Takenaka, S.; Fertsch, S.; Wenk, A.; Seitz, J.; Mayer, P.; Oberdorster, G.; Kreyling, W. G. Efficient Elimination of Inhaled Nanoparticles from the Alveolar Region: Evidence for Interstitial Uptake and Subsequent Reentrainment onto Airway Epithelium. Environ. Health. Persp. 2007, 115, 728−733. (123) Buckley, A.; Hodgson, A.; Warren, J.; Guo, C.; Smith, R. SizeDependent Deposition of Inhaled Nanoparticles in the Rat Respiratory Tract Using a New Nose-Only Exposure System. Aerosol Sci. Technol. 2016, 50, 1−10. (124) Möller, W.; Gibson, N.; Geiser, M.; Pokhrel, S.; Wenk, A.; Takenaka, S.; Schmid, O.; Bulgheroni, A.; Simonelli, F.; Kozempel, J.; et al. Gold Nanoparticle Aerosols for Rodent Inhalation and Translocation Studies. J. Nanopart. Res. 2013, 15, No. 1574. (125) Ferron, G. A.; Erbe, F.; Furst, G.; Haider, B.; Haller, J.; Kohl, B.; Kreyling, W. G.; Schumann, G.; Stocker, M.; Heyder, J. A ScintillationCounter for Measuring Removal of Radioactive Particles from Dog Lungs. J. Aerosol Sci. 1989, 20, 1297−1300. (126) Kreyling, W. G.; Cox, C.; Ferron, G. A.; Oberdorster, G. Lung Clearance in Long-Evans Rats after Inhalation of Porous, Monodisperse Cobalt Oxide Particles. Exp. Lung Res. 1993, 19, 445−467. (127) Beck-Speier, I.; Kreyling, W. G.; Maier, K. L.; Dayal, N.; Schladweiler, M. C.; Mayer, P.; Semmler-Behnke, M.; Kodavanti, U. P. Soluble Iron Modulates Iron Oxide Particle-Induced Inflammatory Responses via Prostaglandin E-2 Synthesis: In Vitro and In Vivo Studies. Part. Fibre Toxicol. 2009, 6, 34. (128) Roe, D.; Karandikar, B.; Bonn-Savage, N.; Gibbins, B.; Roullet, J. B. Antimicrobial Surface Functionalization of Plastic Catheters by Silver Nanoparticles. J. Antimicrob. Chemother. 2008, 61, 869−876. (129) Zuykov, M.; Pelletier, E.; Belzile, C.; Demers, S. Alteration of Shell Nacre Micromorphology in Blue Mussel Mytilus edulis after Exposure to Free-Ionic Silver and Silver Nanoparticles. Chemosphere 2011, 84, 701−706. 4484

DOI: 10.1021/acs.chemrev.6b00693 Chem. Rev. 2017, 117, 4462−4487

Chemical Reviews

Review

(130) Liu, J. S.; He, X.; Ma, Y. H.; Zhang, Z. Y.; Wu, Z. Q. The Translocation of Ceria Nanoparticles to Olfactory Bulb after Intranasal Instillation. J. Toxicol. 2012, 26, 157−159 ( http://en.cnki.com.cn/ Article_en/CJFDTotal-WSDL201203002.htm; abstract in English, paper in Chinese). (131) Ichedef, C.; Simonelli, F.; Holzwarth, U.; Bagaria, J. P.; Puntes, V. F.; Cotogno, G.; Gilliland, D.; Gibson, N. Radiochemical Synthesis of Ag-105g-labelled Silver Nanoparticles. J. Nanopart. Res. 2013, 15, No. 2073. (132) Jung, J. H.; Jung, S. H.; Kim, S. H.; Choi, S. H. Synthesis and Characterization of Radioisotope Nanospheres Containing Two Gamma Emitters. Appl. Radiat. Isot. 2012, 70, 2677−2681. (133) Mandal, S. Synthesis of Radioactive Gold Nanoparticle in Surfactant Medium. J. Radioanal. Nucl. Chem. 2014, 299, 1209−1212. (134) Roy, K.; Lahiri, S. A Green Method for Synthesis of Radioactive Gold Nanoparticles. Green Chem. 2006, 8, 1063−1066. (135) Hildebrand, H.; Schymura, S.; Holzwarth, U.; Gibson, N.; Dalmiglio, M.; Franke, K. Strategies for Radiolabeling of Commercial TiO2 Nanopowder as a Tool for Sensitive Nanoparticle Detection in Complex Matrices. J. Nanopart. Res. 2015, 17, No. 278. (136) Bakht, M. K.; Sadeghi, M.; Tenreiro, C. A Novel Technique for Simultaneous Diagnosis and Radioprotection by Radioactive Cerium Oxide Nanoparticles: Study of Cyclotron Production of Ce-137m. J. Radioanal. Nucl. Chem. 2012, 292, 53−59. (137) Soltani, F.; Samani, A. B.; Sadeghi, M.; Arani, S. S.; Yavari, K. Production of Cerium-141 Using Ceria and Nanoceria Powder: A Potential Radioisotope for Simultaneous Therapeutic and Diagnostic Applications. J. Radioanal. Nucl. Chem. 2015, 303, 385−391. (138) Kharisov, B. I.; Kharissova, O. V.; Berdonosov, S. S. Radioactive Nanoparticles and their Main Applications: Recent Advances. Recent Pat. Nanotechnol. 2014, 8, 79−96. (139) Larner, F.; Rehkamper, M. Evaluation of Stable Isotope Tracing for ZnO Nanomaterials-New Constraints from High Precision Isotope Analyses and Modeling. Environ. Sci. Technol. 2012, 46, 4149−4158. (140) Bourgeault, A.; Cousin, C.; Geertsen, V.; Cassier-Chauvat, C.; Chauvat, F.; Durupthy, O.; Chaneac, C.; Spalla, O. The Challenge of Studying TiO2 Nanoparticle Bioaccumulation at Environmental Concentrations: Crucial Use of a Stable Isotope Tracer. Environ. Sci. Technol. 2015, 49, 2451−2459. (141) Khan, F. R.; Laycock, A.; Dybowska, A.; Larner, F.; Smith, B. D.; Rainbow, P. S.; Luoma, S. N.; Rehkamper, M.; Valsami-Jones, E. Stable Isotope Tracer To Determine Uptake and Efflux Dynamics of ZnO Nano- and Bulk Particles and Dissolved Zn to an Estuarine Snail. Environ. Sci. Technol. 2013, 47, 8532−8539. (142) Laycock, A.; Stolpe, B.; Roemer, I.; Dybowska, A.; ValsamiJones, E.; Lead, J. R.; Rehkamper, M. Synthesis and Characterization of Isotopically Labeled Silver Nanoparticles for Tracing Studies. Environ. Sci.: Nano 2014, 1, 271−283. (143) Gulson, B.; McCall, M.; Korsch, M.; Gomez, L.; Casey, P.; Oytam, Y.; Taylor, A.; McCulloch, M.; Trotter, J.; Kinsley, L.; et al. Small Amounts of Zinc from Zinc Oxide Particles in Sunscreens Applied Outdoors Are Absorbed through Human Skin. Toxicol. Sci. 2010, 118, 140−149. (144) Croteau, M. N.; Misra, S. K.; Luoma, S. N.; Valsami-Jones, E. Bioaccumulation and Toxicity of CuO Nanoparticles by a Freshwater Invertebrate after Waterborne and Dietborne Exposures. Environ. Sci. Technol. 2014, 48, 10929−10937. (145) Croteau, M. N.; Dybowska, A. D.; Luoma, S. N.; Misra, S. K.; Valsami-Jones, E. Isotopically Modified Silver Nanoparticles to Assess Nanosilver Bioavailability and Toxicity at Environmentally Relevant Exposures. Environ. Chem. 2014, 11, 247−256. (146) Misra, S. K.; Dybowska, A.; Berhanu, D.; Croteau, M. N.; Luoma, S. N.; Boccaccini, A. R.; Valsami-Jones, E. Isotopically Modified Nanoparticles for Enhanced Detection in Bioaccumulation Studies. Environ. Sci. Technol. 2012, 46, 1216−1222. (147) Lee, P. L.; Chen, B. C.; Gollavelli, G.; Shen, S. Y.; Yin, Y. S.; Lei, S. L.; Jhang, C. L.; Lee, W. R.; Ling, Y. C. Development and Validation of TOF-SIMS and CLSM Imaging Method for Cytotoxicity Study of ZnO Nanoparticles in HaCaT Cells. J. Hazard. Mater. 2014, 277, 3−12.

(148) Dybowska, A. D.; Croteau, M. N.; Misra, S. K.; Berhanu, D.; Luoma, S. N.; Christian, P.; O’Brien, P.; Valsami-Jones, E. Synthesis of Isotopically Modified ZnO Nanoparticles and Their Potential as Nanotoxicity Tracers. Environ. Pollut. 2011, 159, 266−273. (149) Buffet, P. E.; Amiard-Triquet, C.; Dybowska, A.; Risso-de Faverney, C.; Guibbolini, M.; Valsami-Jones, E.; Mouneyrac, C. Fate of Isotopically Labeled Zinc Oxide Nanoparticles in Sediment and Effects on Two Endobenthic Species, the Clam Scrobicularia plana and the Ragworm Hediste diversicolor. Ecotoxicol. Environ. Saf. 2012, 84, 191− 198. (150) Larner, F.; Dogra, Y.; Dybowska, A.; Fabrega, J.; Stolpe, B.; Bridgestock, L. J.; Goodhead, R.; Weiss, D. J.; Moger, J.; Lead, J. R.; et al. Tracing Bioavailability of ZnO Nanoparticles Using Stable Isotope Labeling. Environ. Sci. Technol. 2012, 46, 12137−12145. (151) Osmond-McLeod, M. J.; Oytam, Y.; Kirby, J. K.; GomezFernandez, L.; Baxter, B.; McCall, M. J. Dermal Absorption and Shortterm Biological Impact in Hairless Mice from Sunscreens Containing Zinc Oxide Nano- or Larger Particles. Nanotoxicology 2014, 8, 72−84. (152) Gulson, B.; Wong, H.; Korsch, M.; Gomez, L.; Casey, P.; McCall, M.; McCulloch, M.; Trotter, J.; Stauber, J.; Greenoak, G. Comparison of Dermal Absorption of Zinc from Different Sunscreen Formulations and Differing UV Exposure Based on Stable Isotope Tracing. Sci. Total Environ. 2012, 420, 313−318. (153) Larner, F.; Gulson, B.; McCall, M.; Oytam, Y.; Rehkamper, M. An Inter-Laboratory Comparison of High Precision Stable Isotope Ratio Measurements for Nanoparticle Tracing in Biological Samples. J. Anal. At. Spectrom. 2014, 29, 471−477. (154) Meermann, B.; Wichmann, K.; Lauer, F.; Vanhaecke, F.; Ternes, T. A. Application of Stable Isotopes and AF4/ICP-SFMS for Simultaneous Tracing and Quantification of Iron Oxide Nanoparticles in a Sediment-Slurry Matrix. J. Anal. At. Spectrom. 2016, 31, 890−901. (155) Gigault, J.; Hackley, V. A. Differentiation and Characterization of Isotopically Modified Silver Nanoparticles in Aqueous Media Using Asymmetric-Flow Field Flow Fractionation Coupled to Optical Detection and Mass Spectrometry. Anal. Chim. Acta 2013, 763, 57−66. (156) Yu, S. J.; Yin, Y. G.; Zhou, X. X.; Dong, L. J.; Liu, J. F. Transformation Kinetics of Silver Nanoparticles and Silver Ions in Aquatic Environments Revealed by Double Stable Isotope Labeling. Environ. Sci.: Nano 2016, 3, 883−893. (157) Yin, Y. G.; Liu, J. F.; Jiang, G. B. Sunlight-Induced Reduction of Ionic Ag and Au to Metallic Nanoparticles by Dissolved Organic Matter. ACS Nano 2012, 6, 7910−7919. (158) Yu, S. J.; Yin, Y. G.; Chao, J. B.; Shen, M. H.; Liu, J. F. Highly Dynamic PVP-Coated Silver Nanoparticles in Aquatic Environments: Chemical and Morphology Change Induced by Oxidation of Ag0 and Reduction of Ag+. Environ. Sci. Technol. 2014, 48, 403−411. (159) Schneider, T.; Vermeulen, R.; Brouwer, D. H.; Cherrie, J. W.; Kromhout, H.; Fogh, C. L. Conceptual Model for Assessment of Dermal Exposure. Occup. Environ. Med. 1999, 56, 765−773. (160) von Goetz, N.; Lorenz, C.; Windler, L.; Nowack, B.; Heuberger, M.; Hungerbuhler, K. Migration of Ag- and TiO2-(Nano)particles from Textiles into Artificial Sweat under Physical Stress: Experiments and Exposure Modeling. Environ. Sci. Technol. 2013, 47, 9979−9987. (161) Papakostas, D.; Rancan, F.; Sterry, W.; Blume-Peytavi, U.; Vogt, A. Nanoparticles in Dermatology. Arch. Dermatol. Res. 2011, 303, 533− 550. (162) Nohynek, G. J.; Lademann, J.; Ribaud, C.; Roberts, M. S. Grey Goo on the Skin? Nanotechnology, Cosmetic and Sunscreen Safety. Crit. Rev. Toxicol. 2007, 37, 251−277. (163) Watkinson, A. C.; Bunge, A. L.; Hadgraft, J.; Lane, M. E. Nanoparticles Do Not Penetrate Human SkinA Theoretical Perspective. Pharm. Res. 2013, 30, 1943−1946. (164) Zvyagin, A. V.; Zhao, X.; Gierden, A.; Sanchez, W.; Ross, J. A.; Roberts, M. S. Imaging of Zinc Oxide Nanoparticle Penetration in Human Skin In Vitro and In Vivo. J. Biomed. Opt. 2008, 13, 064031. (165) Filon, F. L.; Mauro, M.; Adami, G.; Bovenzi, M.; Crosera, M. Nanoparticles Skin Absorption: New Aspects for A Safety Profile Evaluation. Regul. Toxicol. Pharmacol. 2015, 72, 310−322. 4485

DOI: 10.1021/acs.chemrev.6b00693 Chem. Rev. 2017, 117, 4462−4487

Chemical Reviews

Review

Chemical Characterisation and Ecotoxicological Risk Assessment. J. Biomed. Nanotechnol. 2012, 8, 991−999. (185) Ferro-Flores, G.; Ocampo-Garcia, B. E.; Santos-Cuevas, C. L.; Morales-Avila, E.; Azorin-Vega, E. Multifunctional Radiolabeled Nanoparticles for Targeted Therapy. Curr. Med. Chem. 2014, 21, 124−138. (186) Kim, S. T.; Saha, K.; Kim, C.; Rotello, V. M. The Role of Surface Functionality in Determining Nanoparticle Cytotoxicity. Acc. Chem. Res. 2013, 46, 681−691. (187) Albanese, A.; Tang, P. S.; Chan, W. C. W. The Effect of Nanoparticle Size, Shape, and Surface Chemistry on Biological Systems. Annu. Rev. Biomed. Eng. 2012, 14, 1−16. (188) Simko, M.; Mattsson, M. O. Risks from Accidental Exposures to Engineered Nanoparticles and Neurological Health Effects: A Critical Review. Part. Fibre Toxicol. 2010, 7, 42. (189) Teow, Y.; Asharani, P. V.; Hande, M. P.; Valiyaveettil, S. Health Impact and Safety of Engineered Nanomaterials. Chem. Commun. 2011, 47, 7025−7038. (190) He, X.; Ma, Y. H.; Li, M.; Zhang, P.; Li, Y. Y.; Zhang, Z. Y. Quantifying and Imaging Engineered Nanomaterials In Vivo: Challenges and Techniques. Small 2013, 9, 1482−1491. (191) Georgantzopoulou, A.; Balachandran, Y. L.; Rosenkranz, P.; Dusinska, M.; Lankoff, A.; Wojewodzka, M.; Kruszewski, M.; Guignard, C.; Audinot, J.-N.; Girija, S.; et al. Ag Nanoparticles: Size- and SurfaceDependent Effects on Model Aquatic Organisms and Uptake Evaluation with NanoSIMS. Nanotoxicology 2012, 7, 1168−1178. (192) Bone, A. J.; Matson, C. W.; Colman, B. P.; Yang, X. Y.; Meyer, J. N.; Di Giulio, R. T. Silver Nanoparticle Toxicity to Atlantic Killifish (Fundulus Heteroclitus) and Caenorhabditis Elegans: A Comparison of Mesocosm, Microcosm, and Conventional Laboratory Studies. Environ. Toxicol. Chem. 2015, 34, 275−282. (193) Wang, R.; Feng, X. B.; Wang, W. X. In Vivo Mercury Methylation and Demethylation in Freshwater Tilapia Quantified by Mercury Stable Isotopes. Environ. Sci. Technol. 2013, 47, 7949−7957. (194) Yin, Y. G.; Li, Y. B.; Tai, C.; Cai, Y.; Jiang, G. B. Fumigant Methyl Iodide Can Methylate Inorganic Mercury Species in Natural Waters. Nat. Commun. 2014, 5, 4633. (195) Wang, Y. M.; Li, Y. B.; Liu, G. L.; Wang, D. Y.; Jiang, G. B.; Cai, Y. Elemental Mercury in Natural Waters: Occurrence and Determination of Particulate Hg(0). Environ. Sci. Technol. 2015, 49, 9742−9749. (196) Liu, J. Y.; Sonshine, D. A.; Shervani, S.; Hurt, R. H. Controlled Release of Biologically Active Silver from Nanosilver Surfaces. ACS Nano 2010, 4, 6903−6913. (197) Liu, J. Y.; Hurt, R. H. Ion Release Kinetics and Particle Persistence in Aqueous Nano-Silver Colloids. Environ. Sci. Technol. 2010, 44, 2169−2175. (198) Liu, J. F.; Chao, J. B.; Liu, R.; Tan, Z. Q.; Yin, Y. G.; Wu, Y.; Jiang, G. B. Cloud Point Extraction as an Advantageous Preconcentration Approach for Analysis of Trace Silver Nanoparticles in Environmental Waters. Anal. Chem. 2009, 81, 6496−6502. (199) Chao, J. B.; Liu, J. F.; Yu, S. J.; Feng, Y. D.; Tan, Z. Q.; Liu, R.; Yin, Y. G. Speciation Analysis of Silver Nanoparticles and Silver Ions in Antibacterial Products and Environmental Waters via Cloud Point Extraction-Based Separation. Anal. Chem. 2011, 83, 6875−6882. (200) Zhou, X. X.; Liu, R.; Liu, J. F. Rapid Chromatographic Separation of Dissoluble Ag(I) and Silver-Containing Nanoparticles of 1−100 Nanometer in Antibacterial Products and Environmental Waters. Environ. Sci. Technol. 2014, 48, 14516−14524. (201) Liu, L. H.; He, B.; Liu, Q.; Yun, Z. J.; Yan, X. T.; Long, Y. M.; Jiang, G. B. Identification and Accurate Size Characterization of Nanoparticles in Complex Media. Angew. Chem., Int. Ed. 2014, 53, 14476−14479. (202) Tan, Z. Q.; Liu, J. F.; Guo, X. R.; Yin, Y. G.; Byeon, S. K.; Moon, M. H.; Jiang, G. B. Toward Full Spectrum Speciation of Silver Nanoparticles and Ionic Silver by On-Line Coupling of Hollow Fiber Flow Field-Flow Fractionation and Minicolumn Concentration with Multiple Detectors. Anal. Chem. 2015, 87, 8441−8447.

(166) Ryman-Rasmussen, J. P.; Riviere, J. E.; Monteiro-Riviere, N. A. Penetration of Intact Skin by Quantum Dots with Diverse Physicochemical Properties. Toxicol. Sci. 2006, 91, 159−165. (167) van der Merwe, D.; Tawde, S.; Pickrell, J. A.; Erickson, L. E. Nanocrystalline Titanium Dioxide and Magnesium Oxide In Vitro Dermal Absorption in Human Skin. Cutaneous Ocul. Toxicol. 2009, 28, 78−82. (168) Crosera, M.; Adami, G.; Mauro, M.; Bovenzi, M.; Baracchini, E.; Filon, F. L. In Vitro Dermal Penetration of Nickel Nanoparticles. Chemosphere 2016, 145, 301−306. (169) Gopee, N. V.; Roberts, D. W.; Webb, P.; Cozart, C. R.; Siitonen, P. H.; Latendresse, J. R.; Warbitton, A. R.; Yu, W. W.; Colvin, V. L.; Walker, N. J.; et al. Quantitative Determination of Skin Penetration of PEG-Coated CdSe Quantum Dots in Dermabraded but not Intact SKH1 Hairless Mouse Skin. Toxicol. Sci. 2009, 111, 37−48. (170) Gulson, B.; McCall, M. J.; Bowman, D. M.; Pinheiro, T. A Review of Critical Factors for Assessing the Dermal Absorption of Metal Oxide Nanoparticles from Sunscreens Applied to Humans, and A Research Strategy to Address Current Deficiencies. Arch. Toxicol. 2015, 89, 1909−1930. (171) Croteau, M. N.; Cain, D. J.; Fuller, C. C. Novel and Nontraditional Use of Stable Isotope Tracers to Study Metal Bioavailability from Natural Particles. Environ. Sci. Technol. 2013, 47, 3424−3431. (172) Sperling, R. A.; Parak, W. J. Surface Modification, Functionalization and Bioconjugation of Colloidal Inorganic Nanoparticles. Philos. Philos. Trans. R. Soc., A 2010, 368, 1333−1383. (173) Batley, G. E.; Kirby, J. K.; McLaughlin, M. J. Fate and Risks of Nanomaterials in Aquatic and Terrestrial Environments. Acc. Chem. Res. 2013, 46, 854−862. (174) Nel, A. E.; Madler, L.; Velegol, D.; Xia, T.; Hoek, E. M. V.; Somasundaran, P.; Klaessig, F.; Castranova, V.; Thompson, M. Understanding Biophysicochemical Interactions at the Nano-bio Interface. Nat. Mater. 2009, 8, 543−557. (175) Li, X.; Lenhart, J. J.; Walker, H. W. Aggregation Kinetics and Dissolution of Coated Silver Nanoparticles. Langmuir 2012, 28, 1095− 1104. (176) Huynh, K. A.; Chen, K. L. Aggregation Kinetics of Citrate and Polyvinylpyrrolidone Coated Silver Nanoparticles in Monovalent and Divalent Electrolyte Solutions. Environ. Sci. Technol. 2011, 45, 5564− 5571. (177) Yin, Y. G.; Shen, M. H.; Tan, Z. Q.; Yu, S. J.; Liu, J. F.; Jiang, G. B. Particle Coating-Dependent Interaction of Molecular Weight Fractionated Natural Organic Matter: Impacts on the Aggregation of Silver Nanoparticles. Environ. Sci. Technol. 2015, 49, 6581−6589. (178) El Badawy, A. M.; Hassan, A. A.; Scheckel, K. G.; Suidan, M. T.; Tolaymat, T. M. Key Factors Controlling the Transport of Silver Nanoparticles in Porous Media. Environ. Sci. Technol. 2013, 47, 4039− 4045. (179) Unrine, J. M.; Colman, B. P.; Bone, A. J.; Gondikas, A. P.; Matson, C. W. Biotic and Abiotic Interactions in Aquatic Microcosms Determine Fate and Toxicity of Ag Nanoparticles. Part 1. Aggregation and Dissolution. Environ. Sci. Technol. 2012, 46, 6915−6924. (180) Kirchner, C.; Liedl, T.; Kudera, S.; Pellegrino, T.; Javier, A. M.; Gaub, H. E.; Stolzle, S.; Fertig, N.; Parak, W. J. Cytotoxicity of Colloidal CdSe and CdSe/ZnS Nanoparticles. Nano Lett. 2005, 5, 331−338. (181) Alkilany, A. M.; Nagaria, P. K.; Hexel, C. R.; Shaw, T. J.; Murphy, C. J.; Wyatt, M. D. Cellular Uptake and Cytotoxicity of Gold Nanorods: Molecular Origin of Cytotoxicity and Surface Effects. Small 2009, 5, 701−708. (182) Storm, G.; Belliot, S. O.; Daemen, T.; Lasic, D. D. Surface Modification of Nanoparticles to Oppose Uptake by the Mononuclear Phagocyte System. Adv. Drug Delivery Rev. 1995, 17, 31−48. (183) Mornet, S.; Vasseur, S.; Grasset, F.; Duguet, E. Magnetic Nanoparticle Design for Medical Diagnosis and Therapy. J. Mater. Chem. 2004, 14, 2161−2175. (184) Morales-Avila, E.; Ferro-Flores, G.; Ocampo-Garcia, B. E.; Gomez-Olivan, L. M. Engineered Multifunctional RGD-Gold Nanoparticles for the Detection of Tumour-Specific α(ν) β(3) Expression: 4486

DOI: 10.1021/acs.chemrev.6b00693 Chem. Rev. 2017, 117, 4462−4487

Chemical Reviews

Review

(203) Wiederhold, J. G. Metal Stable Isotope Signatures as Tracers in Environmental Geochemistry. Environ. Sci. Technol. 2015, 49, 2606− 2624. (204) Guilbaud, R.; Butler, I. B.; Ellam, R. M.; Rickard, D. Fe Isotope Exchange Between Fe(II) (aq) and Nanoparticulate Mackinawite (FeSm) during Nanoparticle Growth. Earth Planet. Sci. Lett. 2010, 300, 174−183. (205) Wu, L. L.; Druschel, G.; Findlay, A.; Beard, B. L.; Johnson, C. M. Experimental Determination of Iron Isotope Fractionations among Feaq2+-FeSaq-Mackinawite at Low Temperatures: Implications for the Rock Record. Geochim. Cosmochim. Acta 2012, 89, 46−61. (206) Beard, B. L.; Handler, R. M.; Scherer, M. M.; Wu, L. L.; Czaja, A. D.; Heimann, A.; Johnson, C. M. Iron Isotope Fractionation between Aqueous Ferrous Iron and Goethite. Earth Planet. Sci. Lett. 2010, 295, 241−250. (207) Frierdich, A. J.; Beard, B. L.; Scherer, M. M.; Johnson, C. M. Determination of the Fe(II) (aq)-Magnetite Equilibrium Iron Isotope Fractionation Factor Using the Three-Isotope Method and a MultiDirection Approach to Equilibrium. Earth Planet. Sci. Lett. 2014, 391, 77−86. (208) Yang, L.; Dabek-Zlotorzynska, E.; Celo, V. High Precision Determination of Silver Isotope Ratios in Commercial Products by MCICP-MS. J. Anal. At. Spectrom. 2009, 24, 1564−1569. (209) Lu, D. W.; Liu, Q.; Zhang, T. Y.; Cai, Y.; Yin, Y. G.; Jiang, G. B. Stable Silver Isotope Fractionation in the Natural Transformation Process of Silver Nanoparticles. Nat. Nanotechnol. 2016, 11, 682−686.

4487

DOI: 10.1021/acs.chemrev.6b00693 Chem. Rev. 2017, 117, 4462−4487