PCNA与NEDD8作为华支睾吸虫病早期血清学诊断抗原的筛选与效能评价

doi:10.12140/j.issn.1000-7423.2026.02.014

中国寄生虫学与寄生虫病杂志 ›› 2026, Vol. 44 ›› Issue (2): 244-251.doi: 10.12140/j.issn.1000-7423.2026.02.014

PCNA与NEDD8作为华支睾吸虫病早期血清学诊断抗原的筛选与效能评价

李圆圆¹()(), 高宇微¹, 易海波², 杜新月¹, 周品丞³, 吴琛耘¹, 诸廷俊⁴, 郭斯敏⁵, 钱门宝⁴, 王兆军¹^,⁶^,^*()()

¹ 上海交通大学医学院免疫学与微生物学系，上海市免疫学研究所，上海 200025
² 遵义医科大学基础医学院，贵州遵义 563000
³ 福建医科大学医学技术与工程学院，福建福州 350122
⁴ 中国疾病预防控制中心寄生虫病预防控制所（国家热带病研究中心），传染病溯源预警与智能决策全国重点实验室，国家卫生健康委员会寄生虫病原与媒介生物学重点实验室，世界卫生组织热带病合作中心，科技部国家级热带病国际联合研究中心，上海 200025
⁵ 上海交通大学附属瑞金医院感染科，上海 200025
⁶ 上海交通大学医学院国家热带病研究中心全球健康学院，上海 200025

收稿日期:2025-12-02 修回日期:2026-02-25 出版日期:2026-04-30 发布日期:2026-04-17
通讯作者: * 王兆军（ORCID：0000-0003-2853-1850），女，博士，教授，从事感染与免疫研究。E-mail：zjwang@sjtu.edu.cn
作者简介:李圆圆（ORCID：0009-0009-9045-3356），女，硕士，从事寄生虫感染免疫与诊断抗原研究。E-mail：18168856925@163.com
作者贡献
李圆圆负责转录组学数据分析、重组蛋白表达与纯化、ELISA检测和论文撰写，高宇微负责重组质粒构建及蛋白表达与纯化，易海波负责蛋白抗原性分析，周品丞参与蛋白表达与纯化，吴琛耘协助实验操作，诸廷俊、钱门宝负责华支睾吸虫囊蚴的采集、形态学鉴定及论文修改，郭斯敏负责感染患者血清提供，杜新月负责论文修改，王兆军负责论文设计和实验指导。
基金资助:
国家自然科学基金(NSF-32470957);国家自然科学基金(82402049);上海市东方英才计划领军项目

Screening and efficacy evaluation of PCNA and NEDD8 as early serological diagnostic antigens for clonorchiasis

LI Yuanyuan¹()(), GAO Yuwei¹, YI Haibo², DU Xinyue¹, ZHOU Pincheng³, WU Chenyun¹, ZHU Tingjun⁴, GUO Simin⁵, QIAN Menbao⁴, WANG Zhaojun¹^,⁶^,^*()()

¹ Department of Immunology and Microbiology, Shanghai Institute of Immunology, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
² School of Preclinical Medicine, Zunyi Medical University, Zunyi 563000, Guizhou, China
³ School of Medical Technology and Engineering, Fujian Medical University, Fuzhou 350122, Fujian, China
⁴ National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Chinese Center for Tropical Diseases Research;National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases; Key Laboratory on Parasite and Vector Biology, Ministry of Health;WHO Centre for Tropical Diseases; National Center for International Research on Tropical Diseases, Ministry of Science and Technology, Shanghai 200025, China
⁵ Department of Infectious Diseases, Ruijin Hospital Affiliated to Shanghai Jiao Tong University, Shanghai 200025, China
⁶ School of Global Health, Chinese Center for Tropical Diseases Research, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China

Received:2025-12-02 Revised:2026-02-25 Online:2026-04-30 Published:2026-04-17
Supported by:
National Natural Science Foundation of China(NSF-32470957);National Natural Science Foundation of China(82402049);Shanghai Eastern Talent Plan (Leading Talent Program)

摘要/Abstract

摘要：

目的从5个功能不同的华支睾吸虫候选蛋白中筛选出适用于华支睾吸虫病早期血清学诊断的最佳抗原。方法选取公开数据库NCBI序列读取档案库的华支睾吸虫转录组数据并结合蛋白功能信息，筛选出果糖-1,6-二磷酸醛缩酶（FBA）、半胱氨酸蛋白酶1（CP1）、增殖细胞核抗原（PCNA）、尼曼匹克C2型蛋白（NPC2）和神经前体细胞表达发育下调蛋白8（NEDD8）等5个候选诊断抗原。分析抗原在华支睾吸虫新脱囊幼虫和成虫阶段的表达情况，利用免疫表位数据库和蛋白抗原空间表位预测工具预测抗原表位，并从华支睾吸虫cDNA中PCR扩增对应基因，构建pET-302/NT-His原核表达载体。在大肠埃希菌中经异丙基-β-D-硫代半乳糖苷诱导表达并通过镍-次氮基三乙酸亲和层析纯化重组蛋白。采集经口灌胃感染法感染华支睾吸虫囊蚴后6周的新西兰白兔和BALB/c小鼠阳性血清、华支睾吸虫病早期患者血清（感染后2周~6周）、晚期患者血清（感染后6周以上），及健康对照人群血清和其他寄生虫感染者血清。采用间接ELISA法检测血清中特异性IgM，以华支睾吸虫成虫抗原作为阳性对照，并以阳性血清与阴性血清的标准化450 nm吸光度（ΔA₄₅₀值）的比值（P/N）作为评价指标。使用GraphPad Prism 10软件计算敏感性、特异性，绘制受试者工作特征（ROC）曲线并评估曲线下面积（AUC）。结果转录组学分析表明，5个候选蛋白在新脱囊幼虫和成虫阶段均呈高水平表达。结构及表位预测提示候选蛋白均含多种线性和构象性B细胞表位，关键残基位于表位暴露区域，具有良好抗原潜力。FBA、CP1、PCNA、NPC2和NEDD8等5种蛋白均成功重组表达并纯化，十二烷基硫酸钠聚丙烯酰胺凝胶电泳（SDS-PAGE）显示条带清晰、相对分子质量与理论一致，重组蛋白的纯度分别为86.2%、90.6%、97.1%、82.5%、93.6%，蛋白浓度分别为1 780、514、594、375、1 263 μg/mL。ELISA结果显示，PCNA和NEDD8的IgM反应最强，其P/N值（兔/小鼠）分别为1.675/4.176与1.521/4.076；CP1、FBA和NPC2的反应性相对较弱（1.478/1.870、0.952/2.531、1.040/2.413）。对患者血清的检测结果显示，PCNA、NEDD8及其组合抗原在早期患者中ΔA₄₅₀值明显升高（0.304 ± 0.302、0.506 ± 0.383和0.553 ± 0.358），均高于健康对照组（0.028 ± 0.017、0.066 ± 0.044、0.066 ± 0.041）（Z = 3.924、3.763、4.116，P < 0.01），也高于晚期感染组患者（0.035 ± 0.030、0.070 ± 0.060、0.076 ± 0.071）（Z = 3.890、4.116、4.386，P < 0.01）。在早期感染患者中，PCNA、NEDD8及其组合抗原的敏感性分别为10/14、11/14、12/14，特异性均为95.5%（21/22）。ROC曲线分析显示，PCNA、NEDD8及其组合抗原的AUC分别为0.873 4、0.879 9和0.915 6。结论 PCNA和 NEDD8作为诊断抗原可用于华支睾吸虫早期感染的血清IgM检测，其联合应用可进一步提升早期诊断性能，具有开发为血清学早期诊断试剂的潜力。

关键词: 华支睾吸虫, 早期诊断, PCNA, NEDD8, IgM

Abstract:

Objective To identify the optimal antigen for early serological diagnosis of clonorchiasis screened from five functionally distinct Clonorchis sinensis candidate proteins. Methods The transcriptome data of C. sinensis were retrieved from Sequence Read Archive in NCBI, together with protein function information, were used to screen five candidate diagnostic antigens, including fructose-1,6-bisphosphate aldolase (FBA), cysteine protease 1 (CP1), proliferating cell nuclear antigen (PCNA), niemann-pick type C2 protein (NPC2), and neural precursor cell expressed developmentally downregulated protein-8 (NEDD8). The expression of antigens was detected in larvae freshly released from C. sinensis metacercariae and adults. Antigen epitopes were predicted using immune epitope databases and spatial epitope prediction tools for protein antigen, and corresponding genes were amplified from C. sinensis cDNA using PCR assay to construct a prokaryotic expression vector pET-302/NT-His. Following induction in Escherichia coli with isopropyl-β-D-thiogalactoside (IPTG), the recombinant protein was purified by nickel-nitrilotriacetic acid (Ni-NTA) affinity chromatography. Serum samples were collected from New Zealand white rabbits and BALB/c mice infected with C. sinensis metacercariae via oral gavage for 6 weeks, early-stage clonorchiasis patients (infected for 2 to 6 weeks), late-stage clonorchiasis patients (infected for more than 6 weeks), healthy controls and individuals with other parasitic infections. Serum specific IgM antibody was detected using indirect enzyme-linked immunosorbent assay (ELISA), with C. sinensis adult antigen as a positive control, and the ratio of absorbance of positive serum to negative serum (P/N) at 450 nm (ΔA₄₅₀ value) served as an evaluation indicator. The sensitivity and specificity were estimated with the software GraphPad Prism 10, and the area under the receiver operating characteristic (ROC) curves (AUC) was estimated. Results Transcriptomic analysis showed that the five candidate proteins were highly expressed in both larvae freshly released from C. sinensis metacercariae and adults. Structural and epitope predictions suggested that antigen epitopes contained multiple linear and conformational B cell epitopes, and their key residues were located in the epitope-exposed region, indicating high antigenic potential. Recombinant expression of five proteins (FBA, CP1, PCNA, NPC2, and NEDD8) was successfully completed, and these five recombinant proteins were successfully purified. SDS-PAGE displayed clear bands, with relative molecular masses consistent with theoretical values. The purities of recombinant proteins were 86.2%, 90.6%, 97.1%, 82.5%, and 93.6%, and the concentrations of recombinant proteins were 1 780, 514, 594, 375, and 1 263 μg/mL, respectively. ELISA measured the strongest IgM response to PCNA and NEDD8, with P/N values (rabbit/mouse) of 1.675/4.176 and 1.521/4.076, respectively. The IgM responses to CP1, FBA and NPC2 were relatively weak, with P/N values (rabbit/mouse) of 1.478/1.870, 0.952/2.531, 1.040/2.413, respectively. The ΔA₄₅₀ values for PCNA (0.304 ± 0.302), NEDD8 (0.506 ± 0.383), and their combinations (0.553 ± 0.358) were all higher in detection of serum samples from early-stage clonorchiasis patients relative to health controls [(0.028 ± 0.017), (0.066 ± 0.044) and (0.066 ± 0.041)] (Z = 3.924, 3.763 and 4.116; all P < 0.01) or late-stage patients [(0.035 ± 0.030), (0.070 ± 0.060) and (0.076 ± 0.071)] (Z = 3.890, 4.116 and 4.386; all P < 0.01). The sensitivities of PCNA, NEDD8 alone and in combinations were 10/14, 11/14, and 12/14 for diagnosis of serum samples from early-stage clonorchiasis patients, and the specificity was all 95.5% (21/22). ROC curve analysis showed that the AUC of PCNA, NEDD8 alone and in combinations were 0.873 4, 0.879 9, and 0.915 6, respectively. Conclusion PCNA and NEDD8 may be used as diagnostic antigens for detection of serum IgM antibody from individuals with early-stage C. sinensis infections. PCNA-NEDD8T combinations may improve the early diagnostic performance, which has potential for early immunodiagnosis of clonorchiasis.

Key words: Clonorchis sinensis, Early diagnosis, PCNA, NEDD8, IgM

中图分类号:

R532.23

李圆圆, 高宇微, 易海波, 杜新月, 周品丞, 吴琛耘, 诸廷俊, 郭斯敏, 钱门宝, 王兆军. PCNA与NEDD8作为华支睾吸虫病早期血清学诊断抗原的筛选与效能评价[J]. 中国寄生虫学与寄生虫病杂志, 2026, 44(2): 244-251.

LI Yuanyuan, GAO Yuwei, YI Haibo, DU Xinyue, ZHOU Pincheng, WU Chenyun, ZHU Tingjun, GUO Simin, QIAN Menbao, WANG Zhaojun. Screening and efficacy evaluation of PCNA and NEDD8 as early serological diagnostic antigens for clonorchiasis[J]. Chinese Journal of Parasitology and Parasitic Diseases, 2026, 44(2): 244-251.

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参考文献 33

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蛋白名称 Protein name	基因 ID Gene ID	引物（5'→3'） Primer (5'→3')	内切酶 Endonuclease	长度/bp Length/bp
FBA	CLF_105235	F：GCGG GAATTCAATGTCTCTACCAAAGTACTTGC	EcoRⅠ	1 089
FBA	CLF_105235	R：CGTA CCTAGGTCAGTAAGCATGGCTTGGG	AvrⅡ
CP1	AY273802.1	F：CCGG GAATTCAAGAACTACTCAAGTTGAGCC	BamHⅠ	927
CP1	AY273802.1	R：AACC GGATCCCTATTTGATAATCGCTG	EcoRⅠ
PCNA	CLF_109756	F：TTAA CTCGAGATGTTCGAGGCCCGCCTCAA	XhoⅠ	783
PCNA	CLF_109756	R：CGCG CCTAGGTTAATCAGCATCATCTTCGATCTT	AvrⅡ
NPC2	CLF_109784	F：TATA CTCGAGCAATGGATGAACCCACTA	XhoⅠ	402
NPC2	CLF_109784	R：ATAT GGATCCTTAGTCGTGGATTACCGC	BamHⅠ
NEDD8	CLF_112635	F：CGCG GAATTCAATGTTGATCAAGGTGAAAACCCT	EcoRⅠ	237
NEDD8	CLF_112635	R：ATAT CCTAGGTCAACGAGAGCCGCCACGTA	AvrⅡ

抗原 Antigen	真阳性/例 True positive/case	假阳性/例 False positive/case	假阴性/例 False negative/case	真阴性/例 True negative/case	曲线下面积（95% CI）AUC (95% CI)	截断值Cut-off	敏感性（95% CI） Sensitivity（95% CI）	特异性/%（95% CI）Specificity/%（95% CI）
PCNA	10	1	4	21	0.873 4（0.726 9~1.000）	0.062 3	10/14（45.4%~88.3%）	95.5（78.2%~99.8%）
NEDD8	11	1	3	21	0.879 9（0.733 9~1.000）	0.169 3	11/14（52.4%~92.4%）	95.5（78.2%~99.8%）
PCNA + NEDD8	12	1	2	21	0.915 6（0.784 0~1.000）	0.144 7	12/14（60.1%~97.5%）	95.5（78.2%~99.8%）

PCNA与NEDD8作为华支睾吸虫病早期血清学诊断抗原的筛选与效能评价

Screening and efficacy evaluation of PCNA and NEDD8 as early serological diagnostic antigens for clonorchiasis

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[3]	吴雨洪, 邓雪玲, 黄世圣, 吴美欣, 罗柳春, 傅晓茵, 战廷正, 李青, 唐泽丽. 不同时段华支睾吸虫排泄分泌产物的免疫原性及其诊断价值[J]. 中国寄生虫学与寄生虫病杂志, 2025, 43(3): 440-445.
[4]	胡生宝, 黄海涛, 肖富浩, 杜子友, 郭冬黎, 才拉加. 青海格尔木华支睾吸虫感染1例[J]. 中国寄生虫学与寄生虫病杂志, 2025, 43(3): 449-451.
[5]	吴银娟, 易雪晴, 李美玉, 徐安远, 武奥迅, 钟籽丰, 李学荣. 华支睾吸虫外泌体源Csi-miR-125a致肝纤维化作用及其机制[J]. 中国寄生虫学与寄生虫病杂志, 2025, 43(2): 198-204.
[6]	武奥迅, 钟籽丰, 徐安远, 潘筱雯, 易雪晴, 吴银娟, 李学荣. 华支睾吸虫miRNA在胆管癌发生发展中作用机制的研究进展[J]. 中国寄生虫学与寄生虫病杂志, 2025, 43(2): 269-273.
[7]	祝雨莺, 赵甲光, 周长海, 诸廷俊, 黄继磊, 孟军, 蒋智华, 周晓农, 李石柱, 钱门宝. 2022年广西宾阳县华支睾吸虫感染状况及其影响因素[J]. 中国寄生虫学与寄生虫病杂志, 2024, 42(6): 701-714.
[8]	蔡泽政, 杨萍, 廖倩倩. 儿童并殖吸虫复杂性感染1例[J]. 中国寄生虫学与寄生虫病杂志, 2024, 42(6): 813-816.
[9]	兰炜明, 曾玉凤, 邱婷婷, 周长海, 陈喆, 葛军, 曾小军, 诸廷俊. 2020—2022年江西省信丰县人群华支睾吸虫感染现状分析[J]. 中国寄生虫学与寄生虫病杂志, 2024, 42(5): 659-663.
[10]	柴应植, 陈华良, 余可根, 张轩, 王笑笑, 张家祺, 徐文婕, 阮卫. 2013—2022年浙江省华支睾吸虫感染监测结果分析[J]. 中国寄生虫学与寄生虫病杂志, 2024, 42(4): 469-474.
[11]	王居锋, 薛诗杰, 刘江永, 赖德华, 伦照荣. 我国多个地区麦穗鱼华支睾吸虫囊蚴感染情况及其鉴定分析[J]. 中国寄生虫学与寄生虫病杂志, 2024, 42(4): 475-480.
[12]	刘柳, 张静, 李健科, 张浩, 张凤玉. 华支睾吸虫体内神经递质5-羟色胺的分布[J]. 中国寄生虫学与寄生虫病杂志, 2024, 42(1): 78-82.
[13]	赵磊, 李佳, 莫刚, 李醇, 黄国洋, 彭小红. 华支睾吸虫感染对小鼠肝纤维化和免疫调节功能的影响[J]. 中国寄生虫学与寄生虫病杂志, 2023, 41(6): 760-765.
[14]	李晓芹, 赖雅诗, 陈豫, 吕嘉慧, 韦帅, 张立林, 何姗姗, 石云良, 李艳文. 华支睾吸虫囊蚴脱囊的超微结构观察[J]. 中国寄生虫学与寄生虫病杂志, 2023, 41(5): 601-608.
[15]	徐银, 刘婷, 徐慧, 曾小军, 兰炜明, 龚志红, 戴坤教, 邱婷婷, 郝先, 谢曙英. PCR-CRISPR/Cas12a华支睾吸虫囊蚴检测方法的建立和应用[J]. 中国寄生虫学与寄生虫病杂志, 2023, 41(4): 421-426.