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Applications of Magnetic Nanomaterials in Biosensors and Diagnostics
Purpose – Based on DNase I and reduced graphene oxide (rGO)-magnetic silicon microspheres (MNPS), a highly sensitive and selective fluorescent probe for the detection of PD-L1 was developed. Design/methodology/approach – Here °C we present a feasibility of biosensor to detection of PD-L1 in lung tumors plasma. In the absence of PD- L1°C the PD-L1 aptamer is absorbed on the surface of graphene oxide modified magnetic nanoparticles °8rGO-MNPS°9 and leading to effective fluorescence quenching. Upon adding PD-L1°C the aptamer sequences could be specifically recognized by PD-L1 and the aptamer/PD-L1 complex is formed°C resulting in the recovery of quenched fluorescence. 1 1 1 Findings – This sensor can detect PD-L1 with a linear range from 100 pg mL to 100 ng mL , and a detection limit of 10 pgm was achieved. Originality/value – This method provides an easy and sensitive method for the detection of PD-L1 and will be beneficial to the early diagnosis and prognosis of tumors. Keywords Biosensors, Sensor networks, Programmed death-ligand 1, Cancer diagnosis, Fluorescence Biosensor Paper type Research paper 1. Introduction Cancer has a major impact on society across the world; it is the © Xudong He, GuangYi Yang, E. Yang, Moli Zhang, Dan Luo, leading cause of death in the worldwide. In 2012, there were Jingjian Liu, Chongnan Zhao, Qinhua Chen and Fengying Ran. Published 14.1 million new cases of cancer and 8.2 million cancer-related by Emerald Publishing Limited. This article is published under the Creative Commons Attribution (CC BY 4.0) licence. Anyone may reproduce, deaths in the worldwide; the number of new cases of cancer per distribute, translate and create derivative works of this article (for both year is expected to rise to 23.6 million by 2030 (www.cancer. commercial and non-commercial purposes), subject to full attribution to the gov/about-cancer/understanding/statistics). At present, the original publication and authors. The full terms of this licence may be seen at main early detection techniques of cancer are low-dose http://creativecommons.org/licences/by/4.0/legalcode computed tomography, mammography and magnetic These works were supported by the National Natural Science Foundation of China (81872509), the Hubei Provincial Technology Innovation Project resonance imaging, colonoscopy and tissue biopsy, etc. (2017ACA176), the Shennongjia National Park, Hubei Provincial Key However, its often high cost, low sensitivity, high false positive Laboratory for Conservation Biology of Snub-nosed Monkeys, open Project rate and have invasive procedure (Oeffinger et al., 2015; Patz Fund of Shennongjia Golden Monkey Conservation Biology Hubei et al., 2014; Chudgar et al., 2015; Aberle et al.,2013). Provincial Key Laboratory (201801), the Free Exploration Project of Hubei Therefore, it is urgent to develop a rapid and accurate method University of Medicine (FDFR201804), the Open Project of Hubei Key for detecting cancer biomarkers. Laboratory of Wudang Local Chinese Medicine Research (Hubei University of Medicine) (Grant No. WDCM2018004), the Research Project of Traditional Chinese Medicine of the Foundation of Health Commission of The current issue and full text archive of this journal is available on Emerald Hubei Province (ZY2019M034), the Key Discipline Project of Hubei Insight at: https://www.emerald.com/insight/0260-2288.htm University of Medicine and Hubei Province health, family planning scientific research project (WJ2019M054), the Science and Technology Key Program of Shiyan (19Y93). Sensor Review Received 20 April 2020 41/3 (2021) 229–234 Revised 6 August 2020 Emerald Publishing Limited [ISSN 0260-2288] [DOI 10.1108/SR-04-2020-0087] Accepted 30 September 2020 229 Human plasma Sensor Review Xudong He et al. Volume 41 · Number 3 · 2021 · 229–234 PD-L1 is an important immunosuppressive molecule (Lieping interaction with double-stranded DNA-RNA hybrids (Joon Soo and Flies, 2013; Okazaki et al.,2013); it has important significance et al.,2014), more importantly, nano-materials will have inner in antitumor, anti-infection, anti-autoimmune diseases and organ filter effect in solution, the magnetic nanoparticles modified GO transplantation survival (Zhang et al., 2016). Studies have shown can be separated from solution by magnetic field to avoid inner that PD-L1 is a protein biomarker over expression in many lung filter effect, thus reduce its interference on the sample tumors (Dholaria et al., 2016; D’Incecco et al., 2015). It plays an fluorescence, because the presence of particles in the solution will important role in lung tumors diagnosis, screening, evaluation of reduce the fluorescence intensity (Altintas,,2017). Based on the therapeutic efficacy and prognosis. Currently, the technique for above advantages, in the absence of PD-L1, PD-L1 aptamer determining the level of PD-L1 are mainly including western blot, (Apt) could be absorbed by rGO-MNPs, so that the effective enzyme-linked immunosorbent assay, immunobeads-based flow fluorescence quenching. Correspondingly, in the presence of cytometry, SELDI-MS or MALDI-MS (Grasso et al., 2015; PD-L1, because of double-stranded DNA-RNA hybrids, the Muhammad et al.,2014; Lewis et al.,2018)and biosensors Apt/PD-L1 complex was away from rGO-MNPS and resulting techniques (including immunofluorescence, colorimetric, surface- in the recovery of quenched fluorescence. When DNase I is enhanced Raman scattering, electrochemical, nuclear magnetic added, it can cleave phosphodiester as well as enzyme-aided resonance and surface plasmon resonance biosensor) (He et al., signal amplification, leading to the release of PD-L1 and FAM 2014; Zhang et al.,2016; Xia et al., 2017; Zong et al., 2016; fluorophores, so that the accumulation of free FAM fluorophores Doldan et al., 2016; Zhou et al., 2016). Among these techniques, and the quantities of PD-L1 can be achieved by fluorescence biosensors have been introduced as alternative technologies to increment. With the detection range from 100 pg·mL to 1 1 overcome other methods disadvantages; such as the kit is 100 ng·mL , the detection limit was low at 10 pg·mL .More expensive, time-consuming and has the complex operation steps. importantly, the method has been successfully applied to the Biosensor is rapid, highly sensitive and throughput and real-time detection of PD-L1 in various spiked biological samples optical detection of PD-L1. According to the relevant data, it has (including human urine, saliva, serum, lung cancer patients and been proved that many biosensors have great application prospects normal controls plasma). We believe that this biosensor may be in cancer diagnosis and testing; in particular, fluorescence-based used as a clinical therapeutic and diagnosis tool for lung tumors. methods biosensor have attracted special attention because of their low sample volume, easy operation, sensitivity and high specificity. 2. Experimental section In recent years, there are some reports of immunofluorescence 2.1 Reagents and materials biosensor based on aptamers and deoxyribonuclease I (DNase I); The ExoQuick Plasma prep and Exosome precipitation kit (from aptamer is a single-stranded oligonucleotides, generated by a System Biosciences, PM-EXOQ5TM-1). DNase I was obtained SELEX process, and can specifically bind to small molecules, from solarbio (Beijing, China; www.solarbio.com). The rGO- cells and proteins (Jin et al., 2017; Jun et al.,2018). Aptamers are MNPS was purchased from Nanjing Xianfeng, as a reduced high stability, low cost and easy chemical synthesis; thus, it has graphene oxide modified magnetic nanoparticles. The PD-L1, been widely used for biomarker discovery and biosensing fields CA125, CD63, EPCAM and VEGF were purchased from Cusabio (Yuan et al., 2017; Lan et al.,2013). DNase I is an enzyme-aided Biotech Co.Ltd. (www.cusabio.cn/). The PD-L1 aptamer (5’-ACG signal amplification, which can cleave phosphodiester bonds to GGC CAC ATC AAC TCA TTG ATA GAC AAT GCG TCC product many polynucleotides with 5-phosphate and 3’-OH ACT GCC CGT-3’-FAM) was synthesizedby SangonBiological groups but cannot digest RNA sequences (Lagardère et al., 2017; Engineering Technology Co., Ltd. (Shanghai, China; www.sangon. Li et al.,2017). Thus, it has been developed to achieve the com), and purified using high performance liquid chromatography. sensitive detection of biomolecules recently. In addition, the All reagents were diluted to the required concentration with working application of nanomaterials in fluorescent biosensors has buffer (10mM Tris, 100mM NaNO pH 7.4) before usage. The become an advancing field, such as organic dyes, quantum dots, 3 ultrapure water obtained from a millipore water purification system noble metal nanoclusters, carbon dots and graphene oxide (GO) (18.2 MX·cm resistivity, Milli-Q Direct 8). (Zhang et al., 2012; Xu et al., 2015; Yin et al., 2015; Rizwan et al., 2018). GO is a one-atom-thick two-dimensional carbon 2.2 Human samples nanomaterial with a honeycomb structure (Liu et al.,2016), In this study, human plasma samples were collected from non- which has attracted remarkable attention due its unique small cell lung cancer patients prior to treatment and healthy quenching fluorescence ability as well as adsorption capacity for donors. Healthy human serum, urine and saliva were obtained oligonucleotides. However, in some studies, it was found that the from Affiliated Dongfeng Hospital, Hubei University of Medicine, fluorescent biosensor based on GO also has disadvantages, such and approved by Hospital’s Ethics Committee. We selected the as, poor photostability and low solubility in water. Thus, it is exosome surface proteins PD-L1 as the biomarkers in this study. necessary to search for better fluorophors in biosensor. In this work, we take the advantages of reduced graphene oxide The steps of exosome separation are as follows: exosomes were TC (rGO) and magnetic silicon microspheres (MNPs) to propose a extracted and purified following the Exo-Quick Exosome sensitivity and specificity assay for the quantitative detection of Isolation Reagent manufacturer’s protocol with minor revision. In PD-L1 in lung tumors plasma. MNPs have good brief, 400 uL human plasma samples was taken, the PEG in the exosome isolation kit was added into the plasma sample after biocompatibility, easy separation, and ample functional groups centrifugation in the proportion of 1:4, mixture was incubated at for modification (Martín et al.,2015; Altintas, , 2017), thus its can connect capture probes, separate targets, and rGO from 4°C for 30 min and 1,500 g centrifuge for 30 min at 4°C. The substances (Zhang et al., 2014), rGO, the strong absorbing supernatant was removed, and the exosome pellet was re- capability of single-stranded oligonucleotides and weak suspended in 400 mL PBS. The samples are divided into four 230 Human plasma Sensor Review Xudong He et al. Volume 41 · Number 3 · 2021 · 229–234 parts and stored at 80°C; after the experiment, 100 mLexosome Figure 2 Schematic illustration of the fluorescent biosensor assay was taken as the sample to be tested. detection of PD-L1 by using rGO-MNPS and DNase I-mediated target cyclic amplification 2.3 Optimization of sensing conditions The fluorescence of the mixture was carried out on a Hitachi F- 4600 spectrophotometer (Hitachi Co. Ltd, Japan) equipped with a xenon lamp excitation source at room temperature. The excitation was set at 495 nm, and the emission spectra were collected from 510 nm to 600 nm. In this part, the 40 nM FAM labeled PD-L1 Apt and a desired concentration of PD-L1 were first mixed and kept at 37°C for 15 min, and then 60 mg·mL of rGO-MNPS was added. About after 5 min, the reaction solution was added with 6 U·mL DNase I and incubated at 37°C for 3.3 Feasibility for strategy 30 min. Then the solution was diluted to 1 mL. Finally, the To investigate the feasibility of the biosensor for PD-L1 fluorescence intensity at 517.6 nm was used to choose the detection, Figure 3 shows the fluorescence emission spectra of optimal experimental conditions and quantitative determination the Apt under different conditions. Which acted as the control of PD-L1. In control experiments, measurement of fluorescence experiment (curve a), displayed a strong fluorescence emission intensity at 517.6 nm in the absence of PD-L1. Unless otherwise when 30 nM Apt added alone. The introduction of rGO- noted, each fluorescence measurement was repeated three times, MNPS quenched the fluorescence emission (curve d), resulting and the standard deviation was plotted as the error bar. in a fluorescence intensity decreased remarkably, shows the rGO-MNPS enabled strong adsorption of Apt and effective 3. Results and discussion fluorescence quenching. Then DNase I was added to a solution of Apt and rGO-MNPS, the fluorescence intensity not 3.1 Characterization of reduced graphene oxide-MNPS The morphology of the obtained samples was characterized by obviously increase (curve c), indicating that Apt cannot transmission electron microscopy as shown in Figure 1.The high specifically bind to PD-L1, lead to the FAM fluorophores are resolution transmission electron microscopy images were acquired produced of the experiment. However, upon adding PD-L1, a by a Tecnai G2 F30, and transmission electron microscope (FEI, significant enhancement of the fluorescence intensity was USA) operating at an acceleration voltage of 300 kV. These results observed (curve b), as the result of the stronger binding affinity clearly indicated the successful synthesis of rGO-MNPS. between PD-L1 and their corresponding aptamers induced unwinding of PD-L1 Apt from the rGO-MNPS surface. More 3.2 Principle for detection of PD-L1 importantly, the DNase I-aided target recycling results in the As shown in Figure 2, based on the strong absorb capability of significant fluorescence amplification. Taking these results rGO with single-stranded oligonucleotides via p-p stacking together, the feasibility of the proposed aptasensor for PD-L1 interaction, but weak interaction with double-stranded DNA- detection by our sensing method was achieved. RNA hybrids (Huang and Liu, 2013). Thus, in the absence of PD-L1, the rGO-MNPS enabled strong adsorption of Apt to the 3.4 Optimization of experimental conditions surface of rGO-MNPS, leading to the effective fluorescence The optimal performance of the fluorescent sensing protocol quenching. Correspondingly, in the presence of PD-L1, because strongly affected the main experimental conditions, such as the of double-stranded DNA-RNA hybrids, the Apt/PD-L1 complex was away from rGO-MNPS and resulting in the recovery of Figure 3 Feasibility analysis of the biosensor quenched fluorescence. Meanwhile, when the DNase I is added, basedonthe DNase I enzyme-aided signalamplification and leading to the release of PD-L1 and FAM fluorophores. The released PD-L1 is recycled repeatedly, resulting in the accumulation of free FAM fluorophores. The quantities of PD- L1 can be achieved by fluorescence increment. Figure 1 TEM images of rGO-MNPS 231 Human plasma Sensor Review Xudong He et al. Volume 41 · Number 3 · 2021 · 229–234 concentration of rGO-MNPS and DNase I, the enzyme 3.5 Sensitivity and specificity digestion reaction time and the reaction temperature. The F To investigate the sensitivity and specificity of the proposed and F represent the fluorescence intensity of the solution in sensing strategy, various concentrations of PD-L1 were measured under the optimized experimental conditions. As the presence and absence of PD-L1, respectively. As shown in shown in Figure 5(a), increasing fluorescence intensity with Figure 4(a), Maximum F /F value was observed when the 1 0 increasing PD-L1 concentration from 0 to 200 ng·mL .It concentration of rGO-MNPS was 60 mg·mL , when illustrates a highly concentration dependence of the sensor for increasing the concentration of rGO-MNPS; however, F /F 1 0 the detection of PD-L1. Notably, a good linear correlation value decreases obviously along with the increasing of rGO- between the fluorescence intensity and the concentration of MNPS concentration. Thus, the concentration of rGO-MNPS 1 1 PD-L1 in the range from 100 pg·mL to 100 ng·mL [shown of 60 mg·mL was confirmed as the optimized concentration. in Figure 5(b)]. The calibration plot of the linear equation is According to Figure 4(b), maximum F /F values are observed 1 0 given as y = 137.91·lg c – 112.89 (R = 0.9935), where lg c is when the concentration of DNase I is 6 U·mL and then the logarithm of PD-L1 concentration and Y is the fluorescence decreased gradually because of an accelerated increase in intensity. Furthermore, the detection limit is low to background fluorescent signal; therefore, 6 U·mL is selected 10 pg·mL . In addition, the selectivity of this detection as the optimum DNase I concentration. strategy was assessed by measuring and recording the In addition, Figure 4(c) shows the effect of enzyme digestion fluorescence response of other different targets such as CA125, reaction time on the fluorescence intensity at the emission CD63, VEGF and EPCAM; Figure 6 displays the high wavelength of 517.6 nm. The fluorescence intensity and the fluorescence signal in the presence of the PD-L1 (10 ng·mL ) value of F /F is related to the enzyme digestion reaction time; 1 0 with in the presence of other control proteins (50 ng·mL ). the value of F /F increased gradually along with the increasing 1 0 This comparison clearly indicates the high selectivity of our enzyme digestion reaction time in the range from 5 to 30 min, sensing method. and the maximum F /F values are observed when the enzyme 1 0 digestion time is 30 min. Thus, 30 min was selected as the 3.6 Analysis of PD-L1 in real samples optimal hybridization time. According to Figure 4(d), the F /F 1 0 To further assess the effectiveness of the sensor in biological value was affected at different levels with the rise of the samples, the detection of PD-L1 in real samples was carried hybridization temperature; the F /F value reached a maximum 1 0 out. First, the detection of PD-L1 was spiked with 10% diluted when enzyme digestion temperature was 37°C and then with buffer solution to human urine, saliva and serum, and the decreased gradually; thus, 37°C of enzyme digestion reaction final concentration of 10 ng·mL was performed. Herein, a temperature was selected for the rest of the experiments. significant increase of fluorescence in the presence of 10 ng·mL PD-L1 in various biological samples, compared Figure 4 (a) and (b) shows the effect of rGO-MNPS and DNase I with no spiking biological samples[shown in Figure 7(a)]. In concentration on the fluorescence response of this method, respectively; addition, as shown in Figure 7(b), higher PD-L1 levels were (c) and (d) shows the effect of Enzyme digestion reaction time and observed in serum samples from lung cancer patients than reaction temperature on the fluorescence intensity at the emission healthy controls, suggesting that maybe PD-L1 is an important wavelength of 517.6 nm, respectively biomarker for lung cancer diagnosis. In summary, these results demonstrate that this sensor has considerable application potential to analyze biomarkers in real biological samples, and Figure 5 (a) Fluorescence emission spectra of the biosensor in the presence of PD-L1 with different concentrations: from bottom to top: 0, 10, 100, 500, 1,000, 5,000, 10,000, 50,000, 100,000 and 200,000 pg·mL , respectively. (b) The relationship curve of the fluorescence intensity as a function of PD-L1 concentration 232 Human plasma Sensor Review Xudong He et al. Volume 41 · Number 3 · 2021 · 229–234 Altintas, Z. (2017), “Applications of magnetic nanomaterials in Figure 6 Fluorescence intensity (at the emission wavelength of biosensors and diagnostics”, Biosensors and Nanotechnology: 517.6 nm) of the sensor in the presence of PD-L1 (10 ng·mL ), CA125 1 1 1 Applications in Health Care Diagnostics, Vol. 73, pp. 277-296. (50 ng·mL ), CD63 (50 ng·mL ), VEGF (50 ng·mL ), EPCAM Chudgar, N.P., Bucciarelli, P.R., Jeffries, E.M., Rizk, N.P., (50 ng·mL ) and black, respectively Park, B.J., Adusumilli, P.S. and Jones, D.R. (2015), “Results of the national lung cancer screening trial: where are we now?”, Thoracic Surgery Clinics, Vol. 25 No. 2, pp. 145-153. Dholaria, B., Hammond, W., Shreders, A. and Lou, Y. (2016), “Emerging therapeutic agents for lung cancer”, Journal of Hematology & Oncology, Vol. 9 No. 1, p. 138. D’Incecco, A., Andreozzi, M., Ludovini, V., Rossi, E., Capodanno, A., Landi, L., Tibaldi, C., Minuti, G., Salvini, J. and Coppi, E. 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(2018), nanoprobes”, Analytical Methods, Vol. 8 No. 25, “Trends and advances in electrochemiluminescence pp. 5001-5008. nanobiosensors”, Sensors, Vol. 18 No. 2, pp. 1-28. Xia, Y., Liu, M., Wang, L., Yan, A., He, W., Chen, M., Lan, J., Corresponding authors Xu, J., Guan, L. and Chen, J. (2017), “A visible and Qinhua Chen can be contacted at: cqh77@163.com and colorimetric aptasensor based on DNA-capped single-walled Fengying Ran can be contacted at: ranfengying13@163.com For instructions on how to order reprints of this article, please visit our website: www.emeraldgrouppublishing.com/licensing/reprints.htm Or contact us for further details: permissions@emeraldinsight.com
Sensor Review – Emerald Publishing
Published: Aug 10, 2021
Keywords: Biosensors; Sensor networks; Programmed death-ligand 1; Cancer diagnosis; Fluorescence Biosensor
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