Development of a two-probe competitive enzyme-linked immunosorbent assay for porcine epidemic diarrhea virus based on magnetic nanoparticles.

✅ 全文

基于磁性纳米颗粒的猪流行性腹泻病毒双探针竞争酶联免疫吸附试验的开发

作者 Junrun Sun; Ruiqin Zhu; Mengxiang Wang; Jinxing Song; Lei Zhou; Zhuoya Sun; Yanze Li; Liuyang Jiao; Lu Xia; Hua He; Gaiping Zhang; Yanan Wu 期刊 International journal of biological macromolecules 发表日期 2025 DOI 10.1016/j.ijbiomac.2025.141036 类型 原创研究 (Original Research)

📄 英文摘要 English Abstract

EN

Porcine epidemic diarrhea (PED) causes significant economic losses to the pig farming industry worldwide and currently lacks an effective vaccine. Multiple detection assays and protein purification methods use magnetic nanoparticles due to their biocompatibility, high specific surface area, and solution suspension properties. In this study, a two-probe competitive ELISA based on magnetic nanoparticles for detecting PEDV N protein was developed. MNPs-N and McAb-HRP probes were prepared and the procedure was optimized to identify the ideal reaction conditions. Compared to other methods, the developed method shortens the detection time to 50 min. The coefficient of variation (CV) for intra- and inter-lot replicates was less than 10 %, with reproducibility. The coincidence rate with commercial kits is 93.07 %, making this method reliable and suitable for PED immune monitoring and diagnostics.

📄 中文摘要 Chinese Abstract

中文
猪流行性腹泻(PED)给全球养猪业造成重大经济损失,且目前缺乏有效的疫苗。由于磁性纳米粒子具有良好的生物相容性、高比表面积和溶液悬浮特性,多种检测方法和蛋白质纯化技术均采用了磁性纳米粒子。本研究开发了一种基于磁性纳米粒子的双探针竞争ELISA方法,用于检测PEDV N蛋白。猪流行性腹泻病毒(PEDV)引起猪流行性腹泻(PED),该病具有急性、高度传染性,临床表现为呕吐、腹泻和脱水。PEDV可感染各年龄段的猪,但仔猪死亡率较高。该病于1971年首次在英国被发现,1976年迅速蔓延至整个欧洲,造成了重大经济损失。自20世纪80年代以来,PEDV也在亚洲广泛传播。疫苗株CV777曾提供免疫保护,但2010年变异毒株出现后,即使此前接种过疫苗的猪群也受到影响。PED是养猪业最具毁灭性的流行病之一。PEDV感染导致的仔猪死亡率可达20%–30%,严重影响中国养猪业。鉴于其全球流行性和巨大的经济影响,开发针对PEDV的有效疫苗是当务之急。PEDV编码四种结构蛋白,分别为N、S、M和E蛋白。研究表明,PEDV可与猪δ冠状病毒(PDCoV)和猪传染性胃肠炎病毒(TGEV)等猪冠状病毒共同感染。但即使存在其他蛋白,病毒颗粒的检测仍需依赖PEDV N蛋白。N蛋白即核衣壳蛋白,占病毒蛋白的很大比例,且具有高度的序列保守性,使其成为高灵敏度和高特异性诊断工具的理想靶标,有助于PED的早期检测和准确诊断。磁性纳米粒子(MNPs),又称磁性微球,是纳米材料科学研究的重要课题。它们可通过磁场从液体中快速分离并重复利用。其良好的生物相容性、大比表面积、稳定性和溶液悬浮特性使其在药物递送、制药、分离纯化和废水处理等领域具有广泛应用前景。

📋 英文结构化总结 English Structured Summary

全文整理

EN

Header:

Background

Porcine epidemic diarrhea (PED) causes significant economic losses to the pig farming industry worldwide and currently lacks an effective vaccine. Multiple detection assays and protein purification methods use magnetic nanoparticles due to their biocompatibility, high specific surface area, and solution suspension properties. In this study, a two-probe competitive ELISA based on magnetic nanoparticles for detecting PEDV N protein was developed. Porcine epidemic diarrhea virus (PEDV) causes porcine epidemic diarrhea (PED). It is acute and highly contagious, with clinical manifestations like vomiting, diarrhea, and dehydration. PEDV affects pigs of all ages, but piglets have high mortality rates. First identified in the United Kingdom in 1971, the disease rapidly spread across Europe by 1976, causing significant economic losses. Since the 1980s, PEDV has also spread in Asia. The vaccine strain CV777 provided immunity, but as mutated strains emerged in 2010, the virus affected even those previously vaccinated. PED ranks among the most devastating epidemics in the swine industry. Piglet mortality due to PEDV infection can reach 20 %–30 %, impacting China's pig industry severely. Given the global prevalence and substantial economic impact, developing effective vaccines against PEDV is a priority. PEDV encodes four structural proteins; namely N, S, M, and E protein. Studies indicate that PEDV can co-infect with porcine coronaviruses like PDCoV, and TGEV. But even with other proteins, detection of viral particles requires PEDV N protein. The N protein, or nucleocapsid protein, constitutes a significant portion of the viral proteins and exhibits high sequence conservation. This makes it an ideal target for diagnostic tools with high sensitivity and specificity, facilitating early detection and accurate diagnosis of PED. Magnetic nanoparticles (MNPs), also called magnetic microspheres, are a significant research topic in nanomaterial science. They can be quickly separated from liquids using magnetic fields and reused. Their biocompatibility, large surface area, stability, and solution suspension properties make MNPs ideal in drug delivery mechanisms, pharmaceuticals, separation and purification processes, and wastewater treatment.

Header:

Methods

An MNPs-based two-probe competitive enzyme-linked immunosorbent assay (ELISA) was developed to detect anti-PEDV N protein antibodies. Monoclonal antibodies were generated by immunizing mice with the N protein. These were conjugated with MNPs to prepare MNPs-N probes. The sodium periodate method was used to prepare McAb-HRP probes. Further optimization led to the successful development of the two-probe competitive ELISA. MNPs were converted into MNPs-N probes by coupling their carboxyl groups with the amino groups of N protein. The HRP-McAb probe was generated by labeling monoclonal antibodies (McAb) with horseradish peroxidase (HRP). HRP-McAb competitively binds to MNPs-N with the antibodies from the sample. MNPs have dispersing and suspending properties; hence, MNPs-N can be suspended, reducing the distance between antibodies, and accelerating the formation of MNPS-N antibodies. Materials and reagents included RPMI-1640 medium, DMEM, N-hydroxythiosuccinimide sodium salt (NHC), N-(3-Dimethylaminopropyl)-N′-ethylcarbodiimide hydrochloride (EDC), immunologic adjuvants, 96-well magnetic labeling plate, morpholine ethanesulfonic acid (MES), and horseradish peroxidase (HRP). Positive standard sera for ASFV and pseudorabies virus (PRV) were procured from the China Veterinary Culture Collection Center. Positive serum samples for porcine reproductive and respiratory syndrome virus (PRRSV) and clinical serum samples were also used.

Header:

Results

Compared to other methods, the developed method shortens the detection time to 50 min. The coefficient of variation (CV) for intra- and inter-lot replicates was less than 10 %, with reproducibility. The coincidence rate with commercial kits is 93.07 %, making this method reliable and suitable for PED immune monitoring and diagnostics. Results obtainable in 50 min, excellent inter- and intra-batch reproducibility, and potential for PED immunosurveillance, make this method significant in PED prevention and control.

Header:

Data Summary

The developed method shortens detection time to 50 min. The coefficient of variation (CV) for intra- and inter-lot replicates was less than 10 %. The coincidence rate with commercial kits is 93.07 %.

Header:

Conclusions

The method is reliable and suitable for PED immune monitoring and diagnostics. Results obtainable in 50 min, excellent inter- and intra-batch reproducibility, and potential for PED immunosurveillance, make this method significant in PED prevention and control.

Header:

Practical Significance

The method has potential for PED immunosurveillance, and is significant in PED prevention and control, making it suitable for real-world applications in immune monitoring and diagnostics of porcine epidemic diarrhea.

📋 中文结构化总结 Chinese Structured Summary

中文

背景:

猪流行性腹泻(PED)给全球养猪业造成重大经济损失,且目前缺乏有效的疫苗。由于磁性纳米粒子具有良好的生物相容性、高比表面积和溶液悬浮特性,多种检测方法和蛋白质纯化技术均采用了磁性纳米粒子。本研究开发了一种基于磁性纳米粒子的双探针竞争ELISA方法,用于检测PEDV N蛋白。猪流行性腹泻病毒(PEDV)引起猪流行性腹泻(PED),该病具有急性、高度传染性,临床表现为呕吐、腹泻和脱水。PEDV可感染各年龄段的猪,但仔猪死亡率较高。该病于1971年首次在英国被发现,1976年迅速蔓延至整个欧洲,造成了重大经济损失。自20世纪80年代以来,PEDV也在亚洲广泛传播。疫苗株CV777曾提供免疫保护,但2010年变异毒株出现后,即使此前接种过疫苗的猪群也受到影响。PED是养猪业最具毁灭性的流行病之一。PEDV感染导致的仔猪死亡率可达20%–30%,严重影响中国养猪业。鉴于其全球流行性和巨大的经济影响,开发针对PEDV的有效疫苗是当务之急。PEDV编码四种结构蛋白,分别为N、S、M和E蛋白。研究表明,PEDV可与猪δ冠状病毒(PDCoV)和猪传染性胃肠炎病毒(TGEV)等猪冠状病毒共同感染。但即使存在其他蛋白,病毒颗粒的检测仍需依赖PEDV N蛋白。N蛋白即核衣壳蛋白,占病毒蛋白的很大比例,且具有高度的序列保守性,使其成为高灵敏度和高特异性诊断工具的理想靶标,有助于PED的早期检测和准确诊断。磁性纳米粒子(MNPs),又称磁性微球,是纳米材料科学研究的重要课题。它们可通过磁场从液体中快速分离并重复利用。其良好的生物相容性、大比表面积、稳定性和溶液悬浮特性使其在药物递送、制药、分离纯化和废水处理等领域具有广泛应用前景。

方法:

开发了一种基于磁性纳米粒子的双探针竞争酶联免疫吸附测定(ELISA)方法,用于检测抗PEDV N蛋白抗体。通过用N蛋白免疫小鼠制备单克隆抗体,将其与磁性纳米粒子偶联制备MNPs-N探针。采用高碘酸钠法制备McAb-HRP探针。经进一步优化,成功建立了双探针竞争ELISA方法。通过将磁性纳米粒子的羧基与N蛋白的氨基偶联,将MNPs转化为MNPs-N探针。HRP-McAb探针通过将单克隆抗体(McAb)标记辣根过氧化物酶(HRP)制备而成。HRP-McAb与样品中的抗体竞争性结合MNPs-N。MNPs具有分散和悬浮特性,因此MNPs-N可悬浮于溶液中,缩短抗体间的距离,加速MNPs-N与抗体的结合。实验所用材料和试剂包括RPMI-1640培养基、DMEM、N-羟基琥珀酰亚胺钠盐(NHC)、N-(3-二甲氨基丙基)-N'-乙基碳二亚胺盐酸盐(EDC)、免疫佐剂、96孔磁性标记板、吗啉乙磺酸(MES)和辣根过氧化物酶(HRP)。非洲猪瘟病毒(ASFV)和伪狂犬病病毒(PRV)阳性标准血清购自中国兽医微生物菌种保藏管理中心。同时使用了猪繁殖与呼吸综合征病毒(PRRSV)阳性血清样本和临床血清样本。

结果:

与其他方法相比,所建立的方法将检测时间缩短至50分钟。批内和批间重复性变异系数(CV)均小于10%,具有良好的重复性。与商业化试剂盒的符合率为93.07%,表明该方法可靠,适用于PED免疫监测和诊断。检测时间仅需50分钟,批间和批内重复性优良,且具有PED免疫监测的潜力,使该方法在PED防控中具有重要意义。

数据总结:

所建立的方法将检测时间缩短至50分钟。批内和批间重复性变异系数(CV)均小于10%。与商业化试剂盒的符合率为93.07%。

结论:

该方法可靠,适用于PED免疫监测和诊断。检测时间仅需50分钟,批间和批内重复性优良,且具有PED免疫监测的潜力,使该方法在PED防控中具有重要意义。

实际意义:

该方法具有PED免疫监测的潜力,在PED防控中具有重要意义,适用于猪流行性腹泻免疫监测和诊断的实际应用场景。

📖 英文全文 English Full Text

EN

International Journal of Biological Macromolecules 305 (2025) 141036 Contents lists available at ScienceDirect

International Journal of Biological Macromolecules journal homepage: www.elsevier.com/locate/ijbiomac

Development of a two-probe competitive enzyme-linked immunosorbent assay for porcine epidemic diarrhea virus based on magnetic nanoparticles Junru Sun a,b,1, Ruiqin Zhu a,b,1, Mengxiang Wang a,b , Jinxing Song c , Lei Zhou a,b, Zhuoya Sun a,b, Yanze Li a,b, Liuyang Jiao a,b, Lu Xia a,b, Hua He a,b, Gaiping Zhang a,b,d,* , Yanan Wu a,b,* a

International Joint Research Center of National Animal Immunology, College of Veterinary Medicine, Henan Agricultural University, Zhengzhou 450046, China Ministry of Education Key Laboratory for Animal Pathogens and Biosafety, College of Veterinary Medicine, Henan Agricultural University, Zhengzhou 450046, China College of Veterinary Medicine, Henan University of Animal Husbandry and Economy, Zhengzhou 450046, China d Longhu Laboratory, Zhengzhou 450046, China b c

A R T I C L E I N F O A B S T R A C T

Keywords: Porcine epidemic diarrhea virus Magnetic nanoparticles N protein Two-probe competitive ELISA

Porcine epidemic diarrhea (PED) causes significant economic losses to the pig farming industry worldwide and currently lacks an effective vaccine. Multiple detection assays and protein purification methods use magnetic nanoparticles due to their biocompatibility, high specific surface area, and solution suspension properties. In this study, a two-probe competitive ELISA based on magnetic nanoparticles for detecting PEDV N protein was developed. MNPs-N and McAb-HRP probes were prepared and the procedure was optimized to identify the ideal reaction conditions. Compared to other methods, the developed method shortens the detection time to 50 min. The coefficient of variation (CV) for intra- and inter-lot replicates was less than 10 %, with reproducibility. The coincidence rate with commercial kits is 93.07 %, making this method reliable and suitable for PED immune monitoring and diagnostics.

1. Introduction Porcine epidemic diarrhea virus (PEDV) causes porcine epidemic diarrhea (PED) [1]. It is acute and highly contagious, with clinical manifestations like vomiting, diarrhea, and dehydration [2]. PEDV af­ fects pigs of all ages, but piglets have high mortality rates [3,4]. First identified in the United Kingdom in 1971, [5] the disease rapidly spread across Europe by 1976, causing significant economic losses [6]. Since the 1980s, PEDV has also spread in Asia [7]. The vaccine strain CV777 provided immunity, but as mutated strains emerged in 2010, the virus affected even those previously vaccinated. PED ranks among the most devastating epidemics in the swine industry [8–10]. Piglet mortality due to PEDV infection can reach 20 %–30 %, impacting China's pig industry severely [11,12]. Given the global prevalence and substantial economic impact, developing effective vaccines against PEDV is a priority [13]. PEDV encodes four structural proteins; namely N, S, M, and E protein [14]. Studies indicate that PEDV can co-infect with porcine

coronaviruses like PDCoV, and TGEV. But even with other proteins, detection of viral particles requires PEDV N protein [15]. The N protein, or nucleocapsid protein, constitutes a significant portion of the viral proteins and exhibits high sequence conservation [16]. This makes it an ideal target for diagnostic tools with high sensitivity and specificity, facilitating early detection and accurate diagnosis of PED [17]. Magnetic nanoparticles (MNPs), also called magnetic microspheres, are a significant research topic in nanomaterial science [18]. They can be quickly separated from liquids using magnetic fields and reused [19]. Their biocompatibility, large surface area, stability, and solution sus­ pension properties [20] make MNPs ideal in drug delivery mechanisms [21,22], pharmaceuticals [23], separation and purification processes [24], and wastewater treatment [25,26]. Current research shows po­ tential beyond these fields, extending to MRI contrast agents [27], green catalysts [28,29], cell labeling [30], controlled drug release [31], and protein separation. MNPs can be categorized into organic and inorganic particles [32]. Organic MNPs are composed of magnetic materials

* Corresponding authors at: International Joint Research Center of National Animal Immunology, College of Veterinary Medicine, Henan Agricultural University, Zhengzhou 450046, China. E-mail addresses: zhanggaip@126.com (G. Zhang), wlyananjiayou@yeah.net (Y. Wu). 1 These authors contributed equally to this work. https://doi.org/10.1016/j.ijbiomac.2025.141036 Received 26 November 2024; Received in revised form 12 February 2025; Accepted 12 February 2025 Available online 17 February 2025 0141-8130/© 2025 Elsevier B.V. All rights are reserved, including those for text and data mining, AI training, and similar technologies.

International Journal of Biological Macromolecules 305 (2025) 141036 Fig. 1. Schematic representation of the two-probe competitive ELISA technique.

combined with natural or synthetic polymers. They are preferred for in vivo drug delivery due to their biocompatibility and degradability [33]. Inorganic MNPs are made from iron, iron oxides, or other metals with inorganic materials. Various types exist, with Fe3O4 magnetic micro­ spheres being the most common. In this study, Fe3O4 magnetic micro­ spheres were used, owing to their advantages of external magnetic field responsiveness, and high thermal and chemical stability, facilitating broader applications [34]. An MNPs-based two-probe competitive enzyme-linked immunosor­ bent assay (ELISA) was developed to detect anti-PEDV N protein anti­ bodies. Monoclonal antibodies were generated by immunizing mice with the N protein. These were conjugated with MNPs to prepare MNPsN probes. The sodium periodate method was used to prepare McAb-HRP probes. Further optimization led to the successful development of the two-probe competitive ELISA. Results obtainable in 50 min, excellent inter- and intra-batch reproducibility, and potential for PED immuno­ surveillance, make this method significant in PED prevention and control. MNPs were converted into MNPs-N probes by coupling their carboxyl groups with the amino groups of N protein. The HRP-McAb probe was generated by labeling monoclonal antibodies (McAb) with horseradish peroxidase (HRP). HRP-McAb competitively binds to MNPsN with the antibodies from the sample. MNPs have dispersing and sus­ pending properties; hence, MNPs-N can be suspended, reducing the distance between antibodies, and accelerating the formation of MNPS-N antibodies. The antigen-antibody competition reaction is expedited and

more sensitive compared to traditional methods. This principle is illus­ trated in Fig. 1. 2. Experiment 2.1. Materials and reagents RPMI-1640 medium and Dulbecco's modified Eagle's medium (DMEM) were procured from Shanghai Yuanpei Biotechnology Co., LTD. (Shanghai, China). N-hydroxythiosuccinimide sodium salt (NHC) and N(3-Dimethylaminopropyl)-N′-ethylcarbodiimide hydrochloride (EDC) were procured from Shanghai Aladdin Biochemical Science and Tech­ nology Co. Ltd. (Shanghai, China). EDC activates MNPs carboxyl group, and NHC is a catalyst. Immunologic adjuvants were purchased from Biodragon (Suzhou, China). The 96-well magnetic labeling plate was purchased from Nanjing Dongna Biotechnology Co. (Nanjing, China). Morpholine ethanesulfonic acid (MES) was purchased from Merck Mil­ lipore (Billerica, MA, USA). Horseradish Peroxidase (HRP) was pur­ chased from Sigma-Aldrich (St. Louis, MO, USA). 2.2. Serum samples Positive standard sera for ASFV and pseudorabies virus (PRV) were procured from the China Veterinary Culture Collection Center (CVCC, Beijing, China). Positive serum samples for porcine reproductive and respiratory syndrome virus (PRRSV) and clinical serum samples were 2

International Journal of Biological Macromolecules 305 (2025) 141036 pre-collected and preserved. dissolved in 1 mL of water to make the final concentration 5 mg/mL, and 200 μL of 0.1 M NaIO4 was added. This was stirred continuously and incubated for 20–30 min, in the dark, at room temperature. The solution was poured into a dialysis bag (8000–14,000 D molecular weight cutoff), and dialyzed in 1 mM sodium acetate buffer (pH = 4.4) for 12 h at 4 ◦ C. 200 μL of 0.2 M (pH = 9.6) borate buffer was added to the dialysate, and the pH was adjusted to 9.5 by adding 1 M NaOH, and 10 mg of purified antibody (4 mg/mL in PBS). This mixture was gently stirred for 12–16 h at 4 ◦ C. 235 μL of freshly prepared 4 mg/mL NaBH4 solution was added (47 μL NaBH4 per 1 mg HRP), mixed well, and kept for 2 h at 4 ◦ C. An equal volume of saturated ammonium sulfate solution was added to precipitate the purified antibody. The solution was kept for 30 min at 4 ◦ C, then centrifuged at 12000 r/min for 30 min at 4 ◦ C. The supernatant was discarded, the precipitate was resuspended in PBS, and the resuspension was dialyzed for 12–16 h in PBS at 4 ◦ C. The dialyzed solution was centrifuged at 12000 r/min for 10 min, and the supernatant was stored at − 80 ◦ C. This was used to label the antibodies. The absorption peak of the McAb-HRP probe was detected using a UV spectrophotometer, and the McAb-HRP probe was characterized by direct ELISA.

2.3. Synthesis and characterization of MNPs-N The methodological framework outlined in the preceding publica­ tion was followed [35]. 2 mg MNPs (10 mg/mL) were withdrawn, magnetically separated, washed with MES (0.015 M, pH = 5.5) solution twice, and resuspended. 0.2 mg EDC (10 mg/mL) and NHC (10 mg/mL) were added, and the solution was stirred for 30 min at room tempera­ ture. The mixture was magnetically separated, and the supernatant was discarded. The MNPs were washed with MES solution and resuspended. Of N protein, 40 μg was added, and the solution was incubated, stirring, for 4 h at room temperature. The solution was magnetically separated and washed with PBST buffer (pH = 7.4) twice. The supernatant was retained to detect the coupling efficiency of the MNPs and N protein. The unbound sites on MNPs were blocked by adding 1 % BSA (PBST as solvent) and the solution was stirred for 1 h at room temperature. MNPsN was washed with PBST buffer, resuspended with 0.2 mL of PBST buffer, and stored at 4 ◦ C. Transmission electron microscopy and laser particle size analyzer were used to characterize MNPs-N synthesis.

2.4. Screening and characterization of anti-N protein monoclonal antibodies

5 % BSA solution (200 μL) was added to each well, and the plate was incubated for 1 h at 37 ◦ C. The plate was patted dry and stored at 4 ◦ C. 50 μL each of MNPs-N and McAb-HRP probes were added to each well. Either 50 μL of PEDV-positive serum or the test sample was added, with PBS as a blank control. The plate was gently shaken and then allowed to stand for 30 min at room temperature. The plate was then transferred onto a 96-well magnetic plate, and the solution was magnetically separated for 10 s. The supernatant was discarded, and the plate was washed four times with PBST buffer. 100 μL of color development so­ lution was added and left at room temperature. 50 μL of reaction termination solution was then added. The absorbance was measured at 450 nm, using PBS as a control. The percent inhibition (PI) was calcu­ ( ) nm positive value (P) lated using the formula: PI = 1 − OD450negative × 100%. value (N)

30 μL (1 μg/μL) of purified N protein was emulsified with 30 μL of QuickAntibody-Mouse 5 W Lactic Acid Water Adjuvant to immunize two 6-week-old BALB/c female mice intramuscularly. Mice antibody pro­ duction was monitored using ELISA. The mouse having higher antibody levels was euthanized, and its spleen was ground and fused with SP2/ 0 cells. These hybridoma cells were screened by indirect ELISA for positive results and subsequently subcloned thrice using limited dilu­ tion. Cells secreting N protein-specific antibodies were expanded and cultured to make ascites and were purified using a Protein G affinity chromatography column. Western blotting (WB) was used to assess the reactivity of the monoclonal antibody against the N protein. The N protein sample was mixed with 6× sample buffer, boiled, and separated using 10 % SDSPAGE. The proteins were then transferred to a PVDF membrane, blocked with 5 % skim milk in PBST. A hybridoma supernatant was prepared as the primary antibody, and an enzyme-labeled goat antimouse antibody as the secondary antibody. Immunofluorescence assay (IFA) was used to assess the reactivity of the monoclonal antibody against the N protein. Vero cells cultured in 24well plates were inoculated with PEDV and monitored every 12 h until lesions developed. Upon detecting lesions, the culture medium was washed with PBS thrice. The cells were fixed in paraformaldehyde for 30 min and then washed with PBS. 0.1 % Triton X-100 was added and kept for 15 min at room temperature to permeabilize the cells. After discarding the solution, the cells were rinsed with PBS thrice. The so­ lution was blocked with 5 % BSA for 1 h at room temperature. The blocking solution was discarded, and the wells were washed with PBS thrice. The hybridoma supernatant was added to each well and incu­ bated for 1 h at room temperature. The wells were washed with PBS and then diluted with fluorescein isothiocyanate (FITC)-labeled goat antimouse IgG (1:500) and incubated for 1 h at room temperature in the dark. The wells were washed with PBS, and the samples were stained with DAPI for 30 min. The stain was discarded, and the samples were rinsed with water and PBS, thrice each. The stained cells were observed under a fluorescence microscope. Monoclonal antibody isoforms were determined using a mouse monoclonal antibody isoform kit.

2.7. Optimization of competitive ELISA conditions The optimal concentration of MNPs-N and the dilution of McAb-HRP probes were determined using the checkerboard method. MNPs-N probe concentrations ranged from 0.2 μg/mL to 8 μg/mL in PBS, while McAbHRP probe dilutions ranged from 1:500 to 1:8000. After establishing binding sites, 50 μL of MNPs-N probe was added vertically to the plate, while 50 μL of McAb-HRP probe, horizontally. The remaining steps were the same as in Section 2.5. The optimal concentrations and dilutions were based on observed OD values. Positive sera were diluted with PBS at various ratios (undiluted, 1:1, 1:2, 1:5, 1:10, and 1:20). Equal volumes of MNPs-N and McAb-HRP probe were mixed in each dilution. The mixtures were incubated for 30 min at room temperature. The subsequent steps were executed as previously described. The best serum dilution was the one yielding the highest PI value (1-OD450 nm positive/negative value). Based on the optimized conditions for MNPs-N probe concentration, McAb-HRP probe dilution, and serum dilution, the optimal reaction time was determined. ELISA assays were conducted at room temperature with reaction times ranging from 5 to 35 min. To determine the optimal color development time, TMB solution was added, and the reactions were incubated in the dark for up to 25 min, before adding the termi­ nation solution. Absorbance was measured at 450 nm using a multi­ functional enzyme marker.

2.5. Synthesis and characterization of McAb-HRP probes 2.8. Criteria for determining positivity and negativity Previously published steps were followed. [36]: 5 mg of HRP was To establish critical values, 30 PEDV-negative sera were tested using 3

J. Sun et al. International Journal of Biological Macromolecules 305 (2025) 141036

Fig. 2. Characterization of MNPs and MNPs-N. (a) Representative TEM images of MNPs. (b) Representative TEM image of MNPs-N probe. (c) Particle size distri­ bution of MNPs and MNPs-N.

competitive ELISA, using the optimized conditions. The PI values were computed, and the average inhibition rate (X) and standard deviation (SD) of the samples were calculated. A sample's PI value was deemed negative if PI ≤ X + 2SD, and positive if PI ≥ X + 3SD.

3. Results 3.1. Identification of MNPs-N The carboxyl groups on the MNPs reacted with the EDC and NHC solutions forming an activated ester solution. This solution reacts with the amino groups on the PEDV N protein forming the MNPs-N probe. TEM results(Fig. 2ab) revealed tiny protrusions on the surface of MNPsN, indicating successful N protein attachment. Particle size analysis (Fig. 2c) revealed the average particle size of the original MNPs to be about 500 nm, and MNPS-N about 800 nm. MNPs-N had a significantly larger particle size compared to MNPs, indicating the successful prepa­ ration of the MNPs-N probe.

2.9. Repeatability and specificity assessment Seven sera samples were selected for the assay to calculate inter- and intra-batch coefficients of variation (CV = standard deviation (SD)/ mean × 100 %). This assessed the reproducibility of the competitive ELISA. PRRSV-positive, PRV-positive, PDCoV- positive and ASFV-positive sera were tested under optimized competitive ELISA conditions to assess method specificity. A PEDV-positive serum served as a control.

3.2. Identification of anti-N McAb and McAb-HRP probe Tail tip blood serum was withdrawn from mice after two immuni­ zations. The serum potency of the immunized mice was measured using indirect ELISA, with the serum diluted from 1:1000 to 1:2,048,000. The results indicated that the serum potency of the immunized mice reached a dilution of 1:2,048,000 (Fig. 3a). Positive mouse 2 was chosen for cell fusion to prepare monoclonal antibodies. The McAb reactivity with N protein was assessed by Western blot (Fig. 3b) and IFA. The IFA results demonstrated that monoclonal anti­ bodies produced specific fluorescence signals with the virus-attached

2.10. Comparison with commercial kits 101 serum samples were tested using the established competitive ELISA methods and commercial kits. The concordance rate between the two methods was calculated, and the compliance rate was expressed as: Compliance rate (%) = (number of negative sera detected similarly + number of positive sera detected similarly)/total serum number × 100 %. 4

J. Sun et al. International Journal of Biological Macromolecules 305 (2025) 141036

Fig. 3. Preparation and characterization of McAb. (a) Indirect ELISA for the detection of specific IgG titer in BALB/c mice. (b) Western blot results of the reaction with N protein McAb. Lane 1 was N protein, lane 2 was S protein negative control. (c) IFA identification. (d) Schematic diagram of McAb subtype identification. (e) SDS-Page electrophoresis results of the purified McAb. Lanes 1–7 are purified antibodies.

Fig. 4. Validation of the McAb-HRP probe. (a) UV–Vis scanning spectra of McAb-HRP. (b) ELISA detection of the McAb-HRP probe.

Vero cells, while the negative control did not exhibit fluorescence sig­ nals (Fig. 3c). The hybridoma cell supernatant (the primary antibody) was identified using the Triple Eagle Mouse Monoclonal Antibody Subtype Identification Kit. The monoclonal antibody subtype was identified as IgG1 with a Kappa chain (Fig. 3d). Ascites were prepared from hybridoma cells and purified (Fig. 3e). High-purity monoclonal antibodies against the N protein were obtained. The synthesized McAb-HRP conjugate was identified using a UV

spectrophotometer and direct ELISA. The absorption peak of McAb-HRP integrates the absorption peaks of McAb and HRP (Fig. 4a). Addition­ ally, the activity of the McAb-HRP probe was assessed using ELISA. McAb within the synthesized probe maintains a high affinity for the N protein (Fig. 4b), indicating that the affinity of McAb for N protein or the catalytic ability of HRP remains unaffected.

5 J. Sun et al. International Journal of Biological Macromolecules 305 (2025) 141036 3.3. Competitive ELISA method condition optimization

Table 1 Determination of the optimal concentration of MNPs-N probe and the optimal dilution of McAb-HRP probe (PI). MNPs-N concentration (μg/mL) 0.2 1 2 4 8

The optimal concentrations of MNPs-N and McAb-HRP probes were determined using the checkerboard method. The MNPs-N probe was diluted in PBS solution to obtain five concentration gradients (0.2 μg/ mL, 1 μg/mL, 2 μg/mL, 4 μg/mL, and 8 μg/mL). The McAb-HRP probe was serially diluted (1:500, 1:1000, 1: 2000, 1:4000, 1:6000, and 1:8000). The highest PI value was observed when the MNPs-N probe at 1 μg/mL and the McAb-HRP probe at 1:2000 dilution (Table 1). A PEDV positive serum was serially diluted (undiluted, 1:1, 1:2, 1:5, 1:10, and 1:20) and tested. OD450 values reading revealed that undiluted serum had the highest PI value. Thus, no dilution was required for optimal performance (Fig. 5a). The optimal reaction time was found to be 30 min (Fig. 5b), and optimal color development duration was determined (Fig. 5c). The final optimized assay conditions were a combination of 50 μL of undiluted serum, 50 μL of MNPs-N (1 μg/mL), and 50 μL of McAb-HRP

Fig. 5. Optimization results of the two-probe competitive ELISA method. (a) Determination of the optimal sample dilution ratio. (b) Determination of the optimal sample reaction time. (c) Determination of the optimal color development time. 6

J. Sun et al. International Journal of Biological Macromolecules 305 (2025) 141036 Table 3 Clinical sample detection. Clinical samples 101 Two-probe competitive ELISA method Commercial Kits No. of negative

No. of positive No. of negative No. of positive 22 79 15 86 Compliance rate (%) 93.07 % diluted at a ratio of 1:2000. The reaction proceeded at room temperature for 30 min, followed by 20-min color development with TMB solution. 3.4. Determination of critical values Optimized competitive ELISA was used to evaluate 30 PEDVnegative sera. The mean (X) sample inhibition rate was 21.83 %, and the standard deviation (SD) was 7.34 %. The result was considered negative if it was less than X + 2 SD = 36.51 %, positive if it was greater than X + 3 SD = 43.85 %, and doubtful if it was between 36.51 % and 43.85 % (Fig. 6).

3.5. Specificity and reproducibility tests PRRSV-positive sera, PRV-positive sera, ASFV-positive sera, PDCoVpositive sera and PEDV-positive serum controls were used to assess the specificity of ELISA (Fig. 7). Good specificity was observed only for PEDV-positive seropositivity. Optimized competitive ELISA was used to assess seven PEDVpositive sera. The intra- and inter-batch coefficients of variation were under 10 % (Table 2), indicating that the method was reproducible and stable. 3.6. Comparison with commercialized kits ELISA was used to assess 101 serum samples stored in the laboratory, and the compliance rate with commercial kits was calculated. ELISA detected 79 positive sera and 22 negative sera, while the commercial­ ized kit identified 86 positive sera and 15 negative sera. Thus, the compliance rate was 93.07 % (Table 3). 4. Discussion During the early stages of the PED epidemic, the classical CV777 strain vaccine was effective. As mutants emerged after 2010, those previously vaccinated were also affected. This caused a critical concern within the pig industry. These variants increased piglet mortality rates to 80–100 % [8]. Currently, there are no medicines or vaccines available to control these outbreaks [37]. Current strategies focus on preventing virus introduction through infected animals and assessing vaccination efficacy in pregnant sows. Several diagnostic techniques are employed for detecting PED, including immunofluorescent antibody technology (IFA), immunohistochemistry, fluorescent quantitative PCR, and ELISA [38]. ELISA stood out for its analysis capacity. It could handle large

Table 2 Results of the repeatability test. Sample no. 1 2 3 4 5 6 7 Inter-assay Intra-assay X SD CV% X SD CV% 0.775758336 0.765830519 0.510580611 0.815300401 0.687837363 0.70776853 0.677427353 0.044226158 0.01922436 0.050990773 0.02932812 0.033734311 0.013555886 0.038854693

5.70 % 2.51 % 9.99 % 3.60 % 4.90 % 1.91 % 5.73 % 0.789205658 0.782005575 0.521748486 0.790702079 0.706612876 0.71069568 0.646453104 0.015811386 0.023897687 0.048385868 0.030065915 0.052708275 0.024768722 0.056974719

2.00 % 3.06 % 9.27 % 3.80 % 7.46 % 3.48 % 8.81 % 7 J. Sun et al. International Journal of Biological Macromolecules 305 (2025) 141036

sample volumes efficiently and could measure antibody titers in serum and colostrum, thereby assessing vaccination responses [39]. An indi­ rect ELISA for the detection of PEDV serum developed by Yang et al. [40], an indirect ELISA targeting IgA antibodies by Wang et al. [41], and a novel double-antibody sandwich quantitative ELISA by Han et al. [42] are some recent advancements. All these methods have high sensitivity, specificity, and simplicity. Maternal antibodies could confer neonatal protection against PEDV, and monitoring sow antibody levels is imperative [43]. Although easy to use, traditional ELISA could be complex and require time. MNPs offer a promising alternative, functioning as solid supports that facilitate rapid antigen-antibody binding via a magnetic field [44]. MNPs versatility extends to hormones [45], neurotransmitters [46], cytokines [47], and tumor-associated antigens [48] too. This feature enables more research to resolve the complicated and time-consuming operation of traditional ELISA. In this study, MNPs are used to enhance PED diagnostics. The ELISA involved a 30-minute incubation with MNPs-N and McAbHRP probes, followed by colorimetric analysis after washing. The wells were washed four times with PBST, and the color-developing solution was added. This was incubated for 20 min in the dark. OD450 value was read after adding the stop solution to determine if the samples were positive. The critical value was determined by evaluating 30 negative sera. The specificity and reproducibility were assessed and compared with commercial assay kits. The final results showed a 93.07 % compliance of the competitive ELISA with the kit. Due to its specific detection method, only positive sera PRRSV, PRV, PDCoV and ASFV were detected. Other porcine diarrhea diseases could not be detected, indicating the need for improvements in future tests. The intra- and inter-batch coefficients of variation were less than 10 %, indicating good reproducibility. The assay was completed in 50 min, faster than other traditional ELISA methods. This optimized competitive ELISA supports the epidemiological investigation, clinical diagnosis, and PED epidemic control.

Centre for providing PDCOV-positive sera, and Professor Ma Shijie from Henan Agricultural University for providing PEDV-positive sera.

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中文

# 基于磁性纳米颗粒的双探针竞争酶联免疫吸附法检测猪流行性腹泻病毒的研究

国际生物大分子杂志 305 (2025) 141036

## 目录列表可在ScienceDirect获取

**国际生物大分子杂志** 期刊主页:www.elsevier.com/locate/ijbiomac

## 基于磁性纳米颗粒的猪流行性腹泻病毒双探针竞争酶联免疫吸附法的建立

孙俊茹 a,b,1,朱瑞琴 a,b,1,王梦翔 a,b,宋金星 c,周磊 a,b,孙卓雅 a,b,李彦泽 a,b,焦刘洋 a,b,夏璐 a,b,何华 a,b,张改平 a,b,d,*,吴亚楠 a,b,*

a 河南农业大学兽医学院,国家动物免疫学国际联合研究中心,郑州 450046,中国 b 河南农业大学兽医学院,动物病原体与生物安全教育部重点实验室,郑州 450046,中国 c 河南牧业经济学院兽医学院,郑州 450046,中国 d 龙湖实验室,郑州 450046,中国

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**摘要**

**关键词:** 猪流行性腹泻病毒;磁性纳米颗粒;N蛋白;双探针竞争ELISA

猪流行性腹泻(PED)给全球养猪业造成重大经济损失,且目前缺乏有效的疫苗。磁性纳米颗粒因其生物相容性、高比表面积和溶液悬浮特性,被广泛应用于多种检测方法和蛋白质纯化技术。本研究建立了一种基于磁性纳米颗粒的双探针竞争ELISA方法,用于检测PEDV N蛋白。制备了MNPs-N和McAb-HRP探针,并对实验流程进行了优化以确定最佳反应条件。与其他方法相比,所建立的方法将检测时间缩短至50分钟。批内和批间重复性变异系数(CV)均小于10%,具有良好的重复性。与商业试剂盒的符合率为93.07%,表明该方法可靠,适用于PED的免疫监测和诊断。

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## 1. 引言

猪流行性腹泻病毒(PEDV)引起猪流行性腹泻(PED)[1]。该病具有急性和高度传染性,临床表现为呕吐、腹泻和脱水[2]。PEDV可感染各年龄段的猪,但仔猪的死亡率较高[3,4]。该病于1971年首次在英国被发现[5],到1976年迅速蔓延至欧洲,造成了重大经济损失[6]。自20世纪80年代以来,PEDV也在亚洲广泛传播[7]。疫苗株CV777曾提供免疫保护,但2010年变异株出现后,即使先前接种过疫苗的猪群也受到影响。PED被列为养猪业最具毁灭性的流行病之一[8-10]。PEDV感染导致的仔猪死亡率可达20%~30%,严重影响了中国养猪业[11,12]。鉴于其全球流行性和巨大的经济影响,开发针对PEDV的有效疫苗已成为当务之急[13]。

PEDV编码四种结构蛋白,分别为N、S、M和E蛋白[14]。研究表明,PEDV可与猪δ冠状病毒(PDCoV)和猪传染性胃肠炎病毒(TGEV)等猪冠状病毒共同感染。但即使使用其他蛋白,病毒颗粒的检测仍需依赖PEDV N蛋白[15]。N蛋白即核衣壳蛋白,占病毒蛋白的很大比例,且具有高度的序列保守性[16]。这使其成为高灵敏度和特异性诊断工具的理想靶标,有助于PED的早期检测和准确诊断[17]。

磁性纳米颗粒(MNPs),又称磁性微球,是纳米材料科学研究的重要课题[18]。它们可通过磁场从液体中快速分离并重复使用[19]。其生物相容性、大比表面积、稳定性和溶液悬浮特性[20]使其在药物递送系统[21,22]、制药[23]、分离纯化过程[24]和废水处理[25,26]中具有理想的应用前景。当前研究表明,其应用潜力已超越上述领域,延伸至MRI造影剂[27]、绿色催化剂[28,29]、细胞标记[30]、控释给药[31]和蛋白质分离等领域。磁性纳米颗粒可分为有机和无机颗粒[32]。有机磁性纳米颗粒由磁性材料与天然或合成聚合物结合而成,因其生物相容性和可降解性而被优先用于体内药物递送[33]。无机磁性纳米颗粒由铁、铁氧化物或其他金属与无机材料制成,种类繁多,其中Fe₃O₄磁性微球最为常见。本研究选用Fe₃O₄磁性微球,因其具有外磁场响应性以及高热稳定性和化学稳定性等优势,有利于更广泛的应用[34]。

本研究建立了一种基于MNPs的双探针竞争酶联免疫吸附法(ELISA),用于检测抗PEDV N蛋白抗体。通过N蛋白免疫小鼠制备单克隆抗体,将其与MNPs偶联制备MNPs-N探针,采用高碘酸钠法制备McAb-HRP探针。经进一步优化,成功建立了双探针竞争ELISA方法。该方法可在50分钟内获得结果,批间和批内重复性良好,具有PED免疫监测的潜力,在PED防控中具有重要意义。

MNPs通过其羧基与N蛋白的氨基偶联转化为MNPs-N探针。HRP-McAb探针通过将辣根过氧化物酶(HRP)标记于单克隆抗体(McAb)上制备。HRP-McAb与样品中的抗体竞争结合MNPs-N。MNPs具有分散和悬浮特性,因此MNPs-N可悬浮于溶液中,缩短抗体间的距离,加速MNPs-N抗体复合物的形成。与传统方法相比,抗原-抗体竞争反应更加快速和灵敏。该原理如图1所示。

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## 2. 实验

### 2.1. 材料与试剂

RPMI-1640培养基和Dulbecco改良Eagle培养基(DMEM)购自上海源培生物科技有限公司(中国上海)。N-羟基琥珀酰亚胺钠盐(NHC)和N-(3-二甲氨基丙基)-N'-乙基碳二亚胺盐酸盐(EDC)购自上海阿拉丁生化科技股份有限公司(中国上海)。EDC用于活化MNPs的羧基,NHC为催化剂。免疫佐剂购自百奥龙(中国苏州)。96孔磁性标记板购自南京东纳生物科技有限公司(中国南京)。吗啉乙磺酸(MES)购自默克密理博(美国马萨诸塞州比尔里卡)。辣根过氧化物酶(HRP)购自西格玛奥德里奇(美国密苏里州圣路易斯)。

### 2.2. 血清样品

非洲猪瘟病毒(ASFV)和伪狂犬病病毒(PRV)阳性标准血清购自中国兽医微生物菌种保藏管理中心(CVCC,北京,中国)。猪繁殖与呼吸综合征病毒(PRRSV)阳性血清和临床血清样品为预先采集保存。

### 2.3. MNPs-N的合成与表征

参照先前发表的方法框架[35]。取2 mg MNPs(10 mg/mL),磁性分离后,用MES溶液(0.015 M,pH=5.5)洗涤两次并重悬。加入0.2 mg EDC(10 mg/mL)和NHC(10 mg/mL),室温搅拌30分钟。磁性分离后弃上清。用MES溶液洗涤MNPs并重悬。加入40 μg N蛋白,室温搅拌孵育4小时。磁性分离后用PBST缓冲液(pH=7.4)洗涤两次。保留上清用于检测MNPs与N蛋白的偶联效率。加入1% BSA(PBST为溶剂)封闭MNPs上未结合位点,室温搅拌1小时。用PBST缓冲液洗涤MNPs-N,用0.2 mL PBST缓冲液重悬,4℃保存。

采用透射电子显微镜和激光粒度分析仪对MNPs-N合成进行表征。

### 2.4. 抗N蛋白单克隆抗体的筛选与表征

将纯化的N蛋白(30 μL,1 μg/μL)与30 μL QuickAntibody-Mouse 5W乳酸水佐剂乳化后,肌肉免疫两只6周龄BALB/c雌性小鼠。采用ELISA监测小鼠抗体产生情况。选择抗体水平较高的小鼠处死,取脾脏研磨后与SP2/0细胞融合。通过间接ELISA筛选阳性杂交瘤细胞,随后采用有限稀释法进行三次亚克隆。扩增分泌N蛋白特异性抗体的细胞并培养制备腹水,使用Protein G亲和层析柱纯化。

采用蛋白质印迹(WB)评估单克隆抗体与N蛋白的反应性。将N蛋白样品与6×上样缓冲液混合,煮沸后采用10% SDS-PAGE分离。将蛋白转印至PVDF膜,用5%脱脂奶粉PBST封闭。以杂交瘤上清为一酶,酶标山羊抗小鼠抗体为二抗。

采用免疫荧光试验(IFA)评估单克隆抗体与N蛋白的反应性。在24孔板中培养Vero细胞,接种PEDV后每12小时观察一次直至出现病变。发现病变后用PBS洗涤培养液三次。用多聚甲醛固定细胞30分钟,再用PBS洗涤。加入0.1% Triton X-100,室温孵育15分钟使细胞通透。弃去溶液后用PBS洗涤三次。用5% BSA室温封闭1小时。弃去封闭液后用PBS洗涤三次。每孔加入杂交瘤上清,室温孵育1小时。用PBS洗涤后加入异硫氰酸荧光素(FITC)标记的山羊抗小鼠IgG(1:500稀释),室温避光孵育1小时。用PBS洗涤后用DAPI染色30分钟。弃去染色液后用水和PBS各洗涤三次。在荧光显微镜下观察染色细胞。

采用小鼠单克隆抗体亚型鉴定试剂盒测定单克隆抗体亚型。

### 2.5. McAb-HRP探针的合成与表征

参照先前发表的步骤[36]:将5 mg HRP溶于1 mL水中,使终浓度为5 mg/mL,加入200 μL 0.1 M NaIO₄。室温避光持续搅拌孵育20-30分钟。将溶液倒入透析袋(8000-14,000 Da截留分子量),在1 mM醋酸钠缓冲液(pH=4.4)中4℃透析12小时。向透析液中加入200 μL 0.2 M硼酸盐缓冲液(pH=9.6),加入1 M NaOH调节pH至9.5,再加入10 mg纯化抗体(4 mg/mL,PBS溶解)。将混合物在4℃轻柔搅拌12-16小时。加入235 μL新配制的4 mg/mL NaBH₄溶液(每1 mg HRP加入47 μL NaBH₄),混匀后于4℃静置2小时。加入等体积饱和硫酸铵溶液沉淀纯化抗体。4℃静置30分钟后,4℃、12000 r/min离心30分钟。弃去沉淀,用PBS重悬沉淀,4℃下在PBS中透析12-16小时。将透析液12000 r/min离心10分钟,上清保存于-80℃。此产物用于标记抗体。

采用紫外分光光度计检测McAb-HRP探针的吸收峰,并通过直接ELISA对McAb-HRP探针进行表征。

### 2.6. 双探针竞争ELISA方法

每孔加入200 μL 5% BSA溶液,37℃孵育1小时。拍干后4℃保存。每孔加入50 μL MNPs-N和McAb-HRP探针。分别加入50 μL PEDV阳性血清或待检样品,以PBS为空白对照。轻柔振荡后室温静置30分钟。将板转移至96孔磁性板上,磁性分离10秒。弃去上清,用PBST缓冲液洗涤四次。加入100 μL显色液,室温孵育。然后加入50 μL终止液。在450 nm处测定吸光度值,以PBS为对照。按以下公式计算抑制率(PI):PI = (1 - OD₄₅₀阳性值/OD₄₅₀阴性值) × 100%。

### 2.7. 竞争ELISA条件的优化

采用棋盘格法确定MNPs-N最佳浓度和McAb-HRP探针最佳稀释度。MNPs-N探针浓度范围为0.2 μg/mL至8 μg/mL(PBS稀释),McAb-HRP探针稀释度范围为1:500至1:8000。封闭后,每孔纵向加入50 μL MNPs-N探针,横向加入50 μL McAb-HRP探针。其余步骤同2.5节。根据观察到的OD值确定最佳浓度和稀释度。

将阳性血清按不同比例用PBS稀释(不稀释、1:1、1:2、1:5、1:10和1:20)。将等体积MNPs-N和McAb-HRP探针加入各稀释度中。室温孵育30分钟。后续步骤按前述方法进行。产生最高PI值的血清稀释度为最佳稀释度。

在MNPs-N探针浓度、McAb-HRP探针稀释度和血清稀释度优化的基础上,确定最佳反应时间。在室温下进行ELISA检测,反应时间范围为5至35分钟。为确定最佳显色时间,加入TMB溶液后避光孵育最长25分钟,然后加入终止液。使用多功能酶标仪在450 nm处测定吸光度值。

### 2.8. 阳性和阴性判定标准的建立

为建立临界值,采用优化后的竞争ELISA检测30份PEDV阴性血清。计算PI值,并计算样品的平均抑制率(X)和标准差(SD)。若样品的PI值≤ X + 2SD,则判定为阴性;若PI值≥ X + 3SD,则判定为阳性。

### 2.9. 重复性和特异性评估

选取7份血清样品进行检测,计算批间和批内变异系数(CV = 标准差/均值 × 100%),以评估竞争ELISA的重复性。

在优化的竞争ELISA条件下检测PRRSV阳性、PRV阳性、PDCoV阳性和ASFV阳性血清,以评估方法的特异性。以PEDV阳性血清作为对照。

### 2.10. 与商业试剂盒的比较

采用所建立的竞争ELISA方法和商业试剂盒同时检测101份血清样品。计算两种方法的符合率,符合率计算公式为:符合率(%)=(同样检测为阴性的血清数 + 同样检测为阳性的血清数)/血清总数 × 100%。

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## 3. 结果

### 3.1. MNPs-N的鉴定

MNPs上的羧基与EDC和NHC溶液反应形成活化酯溶液。该溶液与PEDV N蛋白上的氨基反应形成MNPs-N探针。TEM结果(图2a、b)显示MNPs-N表面有微小突起,表明N蛋白成功连接。粒径分析(图2c)显示原始MNPs的平均粒径约为500 nm,MNPs-N约为800 nm。MNPs-N的粒径显著大于MNPs,表明MNPs-N探针制备成功。

### 3.2. 抗N蛋白McAb及McAb-HRP探针的鉴定

小鼠免疫两次后取尾尖血血清。采用间接ELISA测定免疫小鼠的血清效价,血清稀释度从1:1000至1:2,048,000。结果表明免疫小鼠的血清效价达到1:2,048,000稀释度(图3a)。选择2号阳性小鼠进行细胞融合以制备单克隆抗体。

通过Western blot(图3b)和IFA评估McAb与N蛋白的反应性。IFA结果显示,单克隆抗体与病毒感染的Vero细胞产生特异性荧光信号,而阴性对照组未显示荧光信号(图3c)。采用三鹰小鼠单克隆抗体亚型鉴定试剂盒鉴定杂交瘤细胞上清(一抗)。鉴定结果显示单克隆抗体亚型为IgG1,轻链为Kappa链(图3d)。制备杂交瘤细胞腹水并纯化(图e)。获得了高纯度的抗N蛋白单克隆抗体。

采用紫外分光光度计和直接ELISA对合成的McAb-HRP偶联物进行鉴定。McAb-HRP的吸收峰整合了McAb和HRP的吸收峰(图4a)。此外,采用ELISA评估McAb-HRP探针的活性。合成探针中的McAb对N蛋白保持高亲和力(图4b),表明McAb对N蛋白的亲和力或HRP的催化能力未受影响。

### 3.3. 竞争ELISA方法条件的优化

采用棋盘格法确定MNPs-N和McAb-HRP探针的最佳浓度。将MNPs-N探针用PBS溶液稀释为五个浓度梯度(0.2 μg/mL、1 μg/mL、2 μg/mL、4 μg/mL和8 μg/mL)。将McAb-HRP探针系列稀释(1:500、1:1000、1:2000、1:4000、1:6000和1:8000)。当MNPs-N探针浓度为1 μg/mL、McAb-HRP探针稀释度为1:2000时,PI值最高(表1)。

将PEDV阳性血清系列稀释(不稀释、1:1、1:2、1:5、1:10和1:20)后进行检测。OD₄₅₀读数显示不稀释血清的PI值最高。因此,无需稀释即可获得最佳性能(图5a)。最佳反应时间为30分钟(图5b),最佳显色时间也已确定(图5c)。

最终优化的检测条件为:50 μL不稀释血清、50 μL MNPs-N(1 μg/mL)和50 μL McAb-HRP(1:2000稀释)的组合。室温反应30分钟后,加入TMB溶液显色20分钟。

### 3.4. 临界值的确定

采用优化的竞争ELISA评估30份PEDV阴性血清。样品平均抑制率(X)为21.83%,标准差(SD)为7.34%。若PI值 < X + 2SD = 36.51%,则判定为阴性;若PI值 > X + 3SD = 43.85%,则判定为阳性;若PI值在36.51%至43.85%之间,则判定为可疑(图6)。

### 3.5. 特异性和重复性检测

采用PRRSV阳性血清、PRV阳性血清、ASFV阳性血清、PDCoV阳性血清和PEDV阳性血清对照评估ELISA的特异性(图7)。仅PEDV阳性血清表现出良好的特异性。

采用优化的竞争ELISA评估7份PEDV阳性血清。批间和批内变异系数均小于10%(表2),表明该方法具有良好的重复性和稳定性。

### 3.6. 与商业化试剂盒的比较

采用ELISA检测实验室保存的101份血清样品,并计算与商业试剂盒的符合率。ELISA检测出79份阳性血清和22份阴性血清,而商业化试剂盒检测出86份阳性血清和15份阴性血清。因此,符合率为93.07%(表3)。

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## 4. 讨论

在PED流行的早期阶段,经典的CV777株疫苗是有效的。2010年变异株出现后,即使先前接种过疫苗的猪群也受到影响,这在养猪业中引起了严重关切。这些变异株将仔猪死亡率提高至80%~100%[8]。目前,尚无药物或疫苗可用于控制这些疫情[37]。目前的策略侧重于通过防止引入受感染的动物以及评估妊娠母猪的疫苗接种效果来控制病毒。PED的诊断技术包括免疫荧光抗体技术(IFA)、免疫组织化学、荧光定量PCR和ELISA[38]。ELISA因其分析能力突出而受到关注,可高效处理大批量样品,并测定血清和初乳中的抗体滴度,从而评估疫苗接种应答[39]。Yang等人[40]建立了检测PEDV血清的间接ELISA,Wang等人[41]建立了靶向IgA抗体的间接ELISA,Han等人[42]建立了新型双抗体夹心定量ELISA,这些都是近期的进展。所有这些方法均具有高灵敏度、特异性和简便性。母源抗体可为新生仔猪提供针对PEDV的保护,监测母猪抗体水平至关重要[43]。尽管传统ELISA使用简便,但操作复杂且耗时。

MNPs作为一种有前景的替代方案,可作为固相载体通过磁场促进快速抗原-抗体结合[44]。MNPs的多功能性还延伸至激素[45]、神经递质[46]、细胞因子[47]和肿瘤相关抗原[48]等领域。这一特性使更多研究能够解决传统ELISA操作复杂和耗时的问题。本研究将MNPs应用于PED诊断的改进。

该ELISA方法包括与MNPs-N和McAb-HRP探针孵育30分钟,洗涤后进行比色分析。用PBST洗涤四次后加入显色液,避光孵育20分钟。加入终止液后读取OD₄₅₀值以判定样品是否为阳性。通过评估30份阴性血清确定临界值,评估了特异性和重复性,并与商业检测试剂盒进行了比较。最终结果显示,竞争ELISA与试剂盒的符合率为93.07%。由于其特异性检测方法,仅检测到PRRSV、PRV、PDCoV和ASFV阳性血清,其他猪腹泻疾病无法被检测,表明未来检测需要改进。批间和批内变异系数均小于10%,表明重复性良好。该检测在50分钟内完成,快于其他传统ELISA方法。该优化的竞争ELISA为流行病学调查、临床诊断和PED疫情控制提供了有力支持。

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**致谢**

感谢提供PDCoV阳性血清的中心,以及河南农业大学马世杰教授提供PEDV阳性血清。