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New Generation Cadmium-Free Quantum Dots for Biophotonics and Nanomedicine † ⊥ ∇ ‡ ⊥ ∇ ‡ § ‡ Gaixia Xu, , , Shuwen Zeng, , , Butian Zhang, Mark T

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New Generation Cadmium-Free Quantum Dots for Biophotonics and Nanomedicine † ⊥ ∇ ‡ ⊥ ∇ ‡ § ‡ Gaixia Xu, , , Shuwen Zeng, , , Butian Zhang, Mark T Review pubs.acs.org/CR New Generation Cadmium-Free Quantum Dots for Biophotonics and Nanomedicine † ⊥ ∇ ‡ ⊥ ∇ ‡ § ‡ Gaixia Xu, , , Shuwen Zeng, , , Butian Zhang, Mark T. Swihart,*, Ken-Tye Yong,*, ∥ and Paras N. Prasad*, † Key Laboratory of Optoelectronics Devices and Systems of Ministry of Education/Guangdong Province, College of Optoelectronic Engineering, Shenzhen University, Shenzhen 518060, People’s Republic of China ‡ School of Electrical and Electronic Engineering, Nanyang Technological University, Singapore 639798, Singapore § ∥ Department of Chemical and Biological Engineering and Institute for Lasers, Photonics, and Biophotonics and Department of Chemistry, University at Buffalo, The State University of New York, Buffalo, New York 14260, United States ⊥ CINTRA CNRS/NTU/THALES, UMI 3288, Research Techno Plaza, 50 Nanyang Drive, Border X Block, Singapore 637553, Singapore ABSTRACT: This review summarizes recent progress in the design and applications of cadmium-free quantum dots (Cd-free QDs), with an emphasis on their role in biophotonics and nanomedicine. We first present the features of Cd-free QDs and describe the physics and emergent optical properties of various types of Cd-free QDs whose applications are discussed in subsequent sections. Selected specific QD systems are introduced, followed by the preparation of these Cd-free QDs in a form useful for biological applications, including recent advances in achieving high photoluminescence quantum yield (PL QY) and tunability of emission color. Next, we summarize biophotonic applications of Cd-free QDs in optical imaging, photoacoustic imaging, sensing, optical tracking, and photothermal therapy. Research advances in the use of Cd- free QDs for nanomedicine applications are discussed, including drug/gene delivery, protein/peptide delivery, image-guided surgery, diagnostics, and medical devices. The review then considers the pharmacokinetics and biodistribution of Cd-free QDs and summarizes current studies on the in vitro and in vivo toxicity of Cd-free QDs. Finally, we provide perspectives on the overall current status, challenges, and future directions in this field. CONTENTS 3.2. CuInS2 and CuInS2/ZnS Quantum Dots 12246 3.3. Ag2S and Ag2Se Quantum Dots 12247 1. Introduction and Background 12235 − 3.4. ZnS AgInS2 (ZAIS) Quantum Dots 12248 1.1. Introduction to Quantum Dots 12235 3.5. Silicon Quantum Dots 12249 1.2. Biophotonics Applications 12236 3.6. Graphene Quantum Dots 12249 1.3. Applications in Nanomedicine 12236 3.7. Doped ZnS/ZnSe Quantum Dots 12250 1.4. Pharmacokinetics and Biodistribution 12237 Downloaded via NANYANG TECHNOLOGICAL UNIV on March 26, 2019 at 15:36:26 (UTC). 3.8. Plasmonic Copper Chalcogenide Quantum See https://pubs.acs.org/sharingguidelines for options on how to legitimately share published articles. 1.5. In Vitro and in Vivo Toxicity 12237 Dots 12251 1.6. Review Outline 12238 4. Preparation of Biocompatible Cadmium-Free 2. Features of Cadmium-Free Quantum Dots 12238 fi ff Quantum Dots 12253 2.1. Quantum Con nement E ects 12238 4.1. InP and InP/ZnS Quantum Dots 12253 2.2. Core/Shell Architectures 12239 4.2. CuInS2, CuInS2/ZnS, and CuInZnS/ZnS Quan- 2.3. Tunability in the Biological Transparency tum Dots 12254 Window 12240 4.3. Ag2S and Ag2Se Quantum Dots 12255 2.4. Opportunity To Introduce Tunable Plas- − 4.4. ZnS AgInS2 (ZAIS) Quantum Dots 12257 monic Features 12241 4.5. ZnSe/InP/ZnS Quantum Dots 12258 2.5. Doping To Achieve Enhanced Emission from 4.6. InAs/InP/ZnSe Quantum Dots 12258 Dopant States 12241 4.7. Silicon Quantum Dots 12259 2.6. Magnetic Doping To Introduce Magnetic 4.8. ZnO Quantum Dots 12260 Imaging Capability 12242 4.9. WS Quantum Dots 12260 2.7. Relationship of Quantum Dot Physics, 2 Properties, and Applications 12243 3. Selected Quantum Dot Systems 12244 3.1. InP and InP/ZnS Quantum Dots 12244 Received: May 6, 2016 Published: September 22, 2016 © 2016 American Chemical Society 12234 DOI: 10.1021/acs.chemrev.6b00290 Chem. Rev. 2016, 116, 12234−12327 Chemical Reviews Review 4.10. Graphene Quantum Dots 12261 excited by a single light source, to produce separate emission 4.11. Doped ZnS/ZnSe Quantum Dots 12262 colors over a wide spectral range with minimal spectral overlap, 4.12. Plasmonic Copper Chalcogenide Quantum making them particularly attractive for multiplex imaging.4 Also, Dots 12263 unlike organic dyes, most QDs are highly resistant to 5. Biophotonic Applications 12264 photobleaching, which allows them to be used for long-term − 5.1. Optical Imaging 12265 in vitro and in vivo imaging.5 7 More importantly, these 5.2. Photoacoustic Imaging 12271 nanocrystals can be engineered to emit at wavelengths ranging 5.3. Biosensing 12272 from 450 to 1500 nm by tailoring their size, shape, and − 5.4. Optical Tracking 12275 composition.8 11 QDs can be prepared as dispersions in either 5.5. Photothermal Therapy 12278 organic or aqueous media, depending on their intended 5.6. Multimodal Imaging 12280 application. The basic features of QDs are described in greater 6. Nanomedicine Applications 12282 detail in section 2. 6.1. Drug Delivery 12283 For biological applications, QDs must be water-dispersible. 6.2. Gene Delivery 12287 When QDs are initially synthesized as colloidal dispersions in 6.3. Protein and Peptide Delivery 12288 nonpolar organic media, surface modification is required to 6.4. Cancer Nanotechnology 12288 render them dispersible in aqueous biological media. Ligand 6.5. Imaging Guided Surgery 12290 exchange and encapsulation of QDs using hydrophilic/ 6.6. In Vitro Diagnostics 12291 amphiphilic molecules or polymers are common strategies for − 6.7. Infectious Diseases 12293 preparing water-dispersible QDs from hydrophobic QDs.12 15 7. Pharmacokinetics and Biodistribution of Cadmi- The QDs can then be functionalized with a variety of um-Free Quantum Dots 12295 biomolecules (e.g., proteins, antibodies, peptides, DNA, and 7.1. Biodistribution of Nontargeted Cadmium- vitamins) through established conjugation techniques. The Free Quantum Dots 12297 large surface area of each QD, relative to organic dyes and other 7.2. Biodistribution of Targeted Cadmium-Free small molecules, provides many surface attachment sites for − Quantum Dots 12299 conjugation.16 18 This opens up possibilities for multivalent 8. In Vitro and in Vivo Toxicity of Cadmium-Free binding via multiple targeting moieties. Flexibility in surface Quantum Dots 12301 chemistry as well as in emission wavelength of bioconjugated 8.1. In Vitro Toxicity 12302 QDs enables their use as nanoprobes or traceable nanocarriers 8.2. In Vivo Toxicity 12307 for broad applications in biophotonics and nanomedicine, 8.3. Mechanisms of Toxicity 12307 including near-IR deep tissue imaging (e.g., 700−900 nm),19,20 9. Concluding Remarks and Perspectives 12309 PL imaging in the second near-IR window (e.g., 1000−1400 9.1. Quantum Dot Synthesis and Functionaliza- nm),21,22 single cell detection,23 and controlled release of − tion 12310 drugs.24 26 However, to date, the majority of QD-related 9.2. Understanding of Quantum Dot Behavior in research in biology and medicine has employed Cd-based QDs Living Systems 12311 including CdSe, CdTe, CdS, and CdTe/CdSe core/shell QDs, 9.3. New Applications and Technologies 12311 often with additional protective shells of ZnS and/or ZnSe.27,28 Author Information 12311 The popularity of these Cd-based QDs is primarily due to their Corresponding Authors 12311 ease of synthesis using readily available precursors and Author Contributions 12311 straightforward solution phase synthesis methods. Protocols Notes 12311 for preparing and using these QDs have been somewhat Biographies 12311 standardized. They are also readily available commercially in Acknowledgments 12312 formats optimized for specific biological assays and applications. References 12312 With the rapidly developing biological applications of Cd- based QDs, their potential toxicity has become a subject of serious discussion and debate. Some studies have demonstrated 1. INTRODUCTION AND BACKGROUND that Cd-based QDs can degrade in a biological environment, releasing highly cytotoxic Cd2+ ions.29,30 Other studies suggest 1.1. Introduction to Quantum Dots that the observed degradation results from the poor quality Quantum dots (QDs) are semiconductor nanocrystals (i.e., insufficient stability or encapsulation) of the QDs (typically 2−10 nm in diameter) that exhibit size-dependent employed.31,32 Researchers ranging from biomedical engineers optical properties, including absorbance and photolumines- to clinicians have raised doubts about the possible use of Cd- cence (PL). They have proven useful in many biophotonic and based QDs for clinical applications such as in vivo diagnostics nanomedical applications including imaging and sensing.1 A and surgery, due to toxicity concerns associated with their Cd single QD typically contains hundreds to thousands of atoms of content. At present, two approaches are being pursued to group II−VI elements (e.g., CdTe, CdSe, CdS, ZnS, ZnSe, or address these concerns. The first approach involves the use of ZnTe), group III−V elements (e.g., InP or InAs), group I−III− one or more biocompatible and long-lasting polymeric layers to − 33−35 VI2 elements (e.g., CuInS2 or AgInS2), group IV VI elements encapsulate the QDs and prevent their breakdown in vivo. (e.g., PbSe, PbS, or PbTe), or group IV elements (e.g., Si, C, or The second approach, which is arguably more challenging and Ge). QDs are large in comparison to conventional organic dyes, time-consuming as it requires advances in material science and but can be comparable in size to fluorescent proteins and other nanochemistry, is to create Cd-free QDs with performance − large biomolecules. QDs have unique advantages relative to comparable to or even better than existing Cd-based QDs.36 38 organic dyes as luminescent labels for biological applications.2,3 Currently, many research groups are developing and applying Specifically, QDs of different sizes or compositions can all be nanochemistry methods to design and fabricate Cd-free QDs 12235 DOI: 10.1021/acs.chemrev.6b00290 Chem. Rev. 2016, 116, 12234−12327 Chemical Reviews Review with tunable emission color, and are testing them in improve diagnosis and treatment of human diseases.
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