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Immunoengineered Magnetic-Quantum Dot Nanobead Zhang et al. J Nanobiotechnol (2021) 19:116 https://doi.org/10.1186/s12951-021-00860-1 Journal of Nanobiotechnology RESEARCH Open Access Immunoengineered magnetic-quantum dot nanobead system for the isolation and detection of circulating tumor cells Pengfei Zhang1,2† , Mohamed S. Draz3,4,5†, Anwen Xiong6†, Wannian Yan2, Huanxing Han1,7* and Wansheng Chen1,8* Abstract Background: Highly efcient capture and detection of circulating tumor cells (CTCs) remain elusive mainly because of their extremely low concentration in patients’ peripheral blood. Methods: We present an approach for the simultaneous capturing, isolation, and detection of CTCs using an immuno-fuorescent magnetic nanobead system (iFMNS) coated with a monoclonal anti-EpCAM antibody. Results: The developed antibody nanobead system allows magnetic isolation and fuorescent-based quantifcation of CTCs. The expression of EpCAM on the surface of captured CTCs could be directly visualized without additional immune-fuorescent labeling. Our approach is shown to result in a 70–95% capture efciency of CTCs, and 95% of the captured cells remain viable. Using our approach, the isolated cells could be directly used for culture, reverse transcription-polymerase chain reaction (RT-PCR), and immunocytochemistry (ICC) identifcation. We applied iFMNS for testing CTCs in peripheral blood samples from a lung cancer patient. Conclusions: It is suggested that our iFMNS approach would be a promising tool for CTCs enrichment and detection in one step. Keywords: Magnetic nanoparticle, Quantum dots, Fluorescent magnetic nanobeads, Circulating tumor cells, Simultaneous capture and detection Introduction 5]. Compared with other early cancer diagnostic tools, Circulating tumor cells (CTCs) are free tumor cells shed such as genetic or metabolite omics analysis [6–8], cap- from original or metastatic tumors into the peripheral tured CTCs could provide more information for further blood [1–3]. CTCs play critical roles in cancer metasta- analysis. However, the limited sensitivity of commer- sis, resulting in 90% of cancer-related deaths. Capturing, cially available approaches combined with the disease’s characterization, and enumeration of CTCs were con- complexity and heterogeneity had restricted the broad sidered as prognostic biomarkers in tumor metastasis acceptance and dissemination of CTC-based diagnostics. and a promising method for early cancer diagnostics [4, Tus, highly efcient isolation and analysis of CTCs from the whole blood is an urgent clinical need. Immunomagnetic separation represents a promising *Correspondence: [email protected]; [email protected] †Pengfei Zhang, Mohamed S. Draz and Anwen Xiong contributed equally approach for cell isolation because of its capability to rap- to this manuscript idly process a large volume of samples and easy operation 1 Department of Pharmacy, Changzheng Hospital, Second Military and facile cell recovery by the end users [9, 10]. Te Cell Medical University, Shanghai 200003, China Full list of author information is available at the end of the article © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Zhang et al. J Nanobiotechnol (2021) 19:116 Page 2 of 12 Search System [11, 12], a U. S. Food and Drug Admin- immunofuorescent labeling procedures. Tese biocom- istration approved platform for clinical CTC enrich- patible small nanobeads have no signifcant change on ment, provides low capture purities (< 1%) with high the viability and propagation of captured tumor cells, background of white blood cells. Recently, some analyti- which is of signifcant importance for testing the isolated cal methods with diferent signaling modes have been cells using cellular and molecular analysis techniques. explored to detect CTCs [13–16], including electrochem- Furthermore, this method was successfully validated on a istry [17–19], inductively coupled plasma-mass spec- lung cancer patient peripheral blood sample and showed trometry [20], Raman imaging [21, 22], colorimetry [23, potential for clinical application. 24], and fuorescence [25]. Among these detection tech- niques, fuorescence-based assays have attracted much Materials and methods interest due to the quick response, high sensitivity, non- Materials destructivity, and real-time monitoring. Many organic fuorescent dyes and fuorescent nanoprobes, such as Oil-soluble CdSe/ZnS QDs were obtained from Suzhou upconversion nanoparticles [26], quantum dots [27–29] Xingshuo Nanotech. Oleic acid capped magnetic nano- and gold nanoclusters with visible light emission [30, 31], particles (MNPs) with a diameter of 10 ± 5 nm were have been applied for the detection of biological targets purchased from Nanjing Nanoeast Biotech. Poly(styrene- circulating in blood including CTCs [32–34]. co-maleic anhydride) (PSMA) copolymer, streptavidin, An ideal probe for CTCs measurement would allow bovine serum albumin (BSA), N-(3-(dimethylamino) magnetic isolation and fuorescent-based detection of propyl)-Nʹ-ethylcarbodiimide hydrochloride (EDC), were the cells. Such probes require a compact structure with obtained from Sigma-Aldrich. Te biotinylated anti- a rapid magnetic response, high specifcity and minimal EpCAM antibody was obtained from R&D Systems. Red nonspecifc binding, and strong fuorescent signals for blood cell (RBC) lysis bufer was bought from Sangon CTCs detection and quantifcation. Quantum dots (QDs) Biotech. FITC anti-mouse/human CD45 antibody (FITC- with unique optical properties, including tunable wave- CD45) was purchased from BioLegend. Blood samples length, high quantum yields, and photobleaching resist- were obtained from Shanghai Changzheng Hospital. ance, are ideal for the preparation of fuorescent magnetic Human cell lines of gastric cancer cells (SGC-7901), nanoprobes. QDs based fuorescent magnetic nanobeads pancreas cancer cells (PANC1), lymphoma cells (Raji), (FMN) prepared by swelling with polymer nanospheres EGFR-mutated (HCC827), and non-EGFR-mutated [35–37], layer-by-layer self-assembly [38–40], DNA (A549) lung cancer cells were obtained from the Cell templated hybridization [27, 41], silica shell coating, or Bank of the Chinese Academy of Sciences. All the cell polymer assembly [42, 43], have been reported for CTCs lines were cultured in Dulbecco’s modifed Eagle’s isolation and identifcation. However, these probes still medium (DMEM) medium except Raji cells in RPMI- sufer from complicated preparation steps, low fuores- 1640 medium, containing 10% fetal bovine serum at cent signals, and weak magnetic response. 37 °C in a humidifed 5% CO2 atmosphere. Here, a fuorescent magnetic nanobeads system (iFMNS) with a highly bright fuorescent intensity that Fabrication of FMN allows immunomagnetic separation of CTCs was pre- Fluorescent magnetic nanobeads (FMN) were prepared pared via a simple emulsion/evaporation method. Te according to our previously reported method with a slight prepared FMN has a diameter of 114 nm with considera- modifcation. Typically, one milliliter of a chloroform solu- ble colloidal stability (i.e., did not aggregate or precipitate tion containing PSMA (10 mg), QDs (10 mg), and MNPs in the bufer during incubation or centrifugation,) and (10 mg) was added into a 4 mL aqueous solution contain- ultrabright fuorescence (encapsulated with many QDs) ing sodium dodecyl sulfate (11.5 mg). After magnetic stir- can improve the fuorescent immunoassay sensitivity ring for 3 min at 8 rcf, the miniemulsion was prepared compared with single QDs immunoprobe. Together with through ultrasonication for 100 s (10 s pulse, 10 s pause) these unique properties, the anti-EpCAM antibody was at 50% amplitude with a sonicator (Fisher Sonic Dismem- conjugated with FMN via streptavidin–biotin bridges. brator Model 500, USA) under ice-bath cooling to prevent Te obtained anti-EpCAM antibody-modifed FMN the evaporation of chloroform. Afterward, the prepared nanoprobes were successfully used for cancer cell isola- miniemulsion was magnetically stirred at 8 rcf overnight in tion with efciency in a range of 70–95% of the tested an open container to evaporate chloroform. Te resulting cells within 10 min using an external magnetic feld. Te nanobeads with PSMA as matrix polymer were pelleted at cells isolated by this method are directly identifed by 13,523 rcf for 10 min, and the supernatant was discarded. the fuorescent signals generated from iFMNS that exist Te pellet of nanobeads was washed with deionized water on the surface of isolated CTCs without any additional three times. After that,
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