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Article(id=1204800732273812022, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1204800727341310425, articleNumber=null, orderNo=null, doi=10.13343/j.cnki.wsxb.20250446, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1749312000000, receivedDateStr=2025-06-08, revisedDate=null, revisedDateStr=null, acceptedDate=1754582400000, acceptedDateStr=2025-08-08, onlineDate=1765176478689, onlineDateStr=2025-12-08, pubDate=1764777600000, pubDateStr=2025-12-04, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1765176478689, onlineIssueDateStr=2025-12-08, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1765176478689, creator=13701087609, updateTime=1765176478689, updator=13701087609, issue=Issue{id=1204800727341310425, tenantId=1146029695717560320, journalId=1192105938417971205, year='2025', volume='65', issue='12', pageStart='5191', pageEnd='5649', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1765176477513, creator=13701087609, updateTime=1765176611928, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1204801291189986067, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1204800727341310425, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1204801291189986068, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1204800727341310425, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=5605, endPage=5616, ext={EN=ArticleExt(id=1204800732559024714, articleId=1204800732273812022, tenantId=1146029695717560320, journalId=1192105938417971205, language=EN, title=Isolation and identification of the porcine hemagglutinating encephalomyelitis virus strain JS-2025, columnId=1192149543992045670, journalTitle=Acta Microbiologica Sinica, columnName=Research Article, runingTitle=null, highlight=null, articleAbstract=

Porcine hemagglutinating encephalomyelitis virus (PHEV), a member of the betacoronavirus genus, is widespread in swine herds and the only known coronavirus causing neurological diseases in pigs. Objective To characterize the genomic features and phylogenetic relationship of a PHEV strain isolated from China. By investigating the biological properties of the virus, we assessed its epidemiological status and identified genetic variation patterns and evolutionary trends, providing a scientific basis for developing targeted prevention and control strategies. Methods RT-PCR detection was performed on suspected PHEV-positive samples collected from a large pig farm in Jiangsu Province, China, followed by virus isolation. The isolated virus was validated by indirect immunofluorescence assay (IFA), transmission electron microscopy (TEM), and whole genome sequencing. Phylogenetic analysis was performed based on the complete genome, S gene, HE gene, and NS2 gene. Results A PHEV strain, designated as PHEV JS-2025, was successfully isolated from the brain tissue sample. IFA showed strong red fluorescence signals in the cytoplasm, and TEM revealed typical coronavirus particles with a diameter of approximate 150 nm. The strain showed vigorous propagation in HRT-18 cells, reaching the peak viral titer at 72 h, with a 50% tissue culture infectious dose (TCID50) of about 104.3 TCID50/mL. PHEV JS-2025 could infect HRT-18, NPTR, and LLC-PK1 cells, and to a lesser extent, human intestinal Caco-2 cells. Whole genome sequencing revealed that the genome of PHEV JS-2025 was 30 044 bp in length, with over 94.9% nucleotide sequence identity to 14 reference PHEV strains, clustering within the rvPHEV-L-1 lineage. Of note, a mutation in the NS2 gene caused a premature termination at amino acid 19, resulting in the functional loss of the NS2 protein. Conclusion A novel PHEV strain JS-2025 from Jiangsu Province was successfully isolated and identified. This strain exhibits unique cellular tropism and can infect human intestinal cell lines, showing a risk of cross-species transmission. The truncated NS2 gene may affect the pathogenic mechanism of this strain. This study aids in understanding the genetic evolutionary characteristics and epidemiological features of PHEV and has implications for the prevention and control of PHE.

, correspAuthors=Mengjia ZHANG, Wentao LI, authorNote=null, correspAuthorsNote=
*E-mail: ZHANG Mengjia, ;
LI Wentao,
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猪血凝性脑脊髓炎病毒(porcine hemagglutinating encephalomyelitis virus, PHEV)属于β冠状病毒属成员，在大多数猪群中流行，也是已知唯一可引起猪神经症状的冠状病毒。 目的 分析中国分离的猪血凝性脑脊髓炎病毒(PHEV)毒株的基因组特征及其系统发育关系。通过深入研究病毒株的生物学特性，系统评估其在我国猪群中的流行病学现状，阐明其遗传变异模式和进化趋势，为开发针对性防控产品提供科学依据。 方法 对中国江苏地区某规模化猪场送检的疑似PHEV阳性样本进行RT-PCR检测，并分离PHEV，通过间接免疫荧光(indirect immunofluorescence assay, IFA)染色和透射电子显微镜(transmission electron microscopy, TEM)对分离的病毒进行验证。根据PHEV JS-2025株全基因组测序结果对全基因组、S基因、HE基因和NS2基因进行了基因组系统发育分析和同源性比较。 结果 成功从脑组织样品中分离获得1株PHEV，命名为PHEV JS-2025。IFA结果显示细胞质中出现明显的荧光信号；电镜观察可见直径约150 nm的典型冠状病毒颗粒。病毒在HRT-18细胞中增殖良好，72 h时病毒滴度达到峰值，半数组织培养感染剂量(tissue culture infectious dose 50%, TCID50)约为104.3 TCID50/mL。PHEV JS-2025能够感染HRT-18、NPTR、LLC-PK1细胞，且对Caco-2细胞具有一定感染性。全基因组测序结果显示，PHEV JS-2025全长30 044 bp，与14个已知PHEV毒株核苷酸一致性均在94.9%以上，属于rvPHEV-L-1谱系，其NS2基因在第19个氨基酸位点出现提前终止导致NS2蛋白功能性缺失。 结论 成功分离并鉴定了1株来自江苏地区的新型PHEV毒株JS-2025。该毒株具有独特的细胞趋向性特征，能够感染人源肠道细胞系，提示其具有潜在的跨种传播风险。NS2基因的截短突变可能影响病毒的致病性。本研究为深入了解PHEV的遗传进化特征和流行病学特点提供了重要的科学依据，对猪血凝性脑脊髓炎(PHE)的防控具有重要意义。

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2.生猪健康养殖协同创新中心实验室，湖北 武汉
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2.The Cooperative Innovation Center for Sustainable Pig Production, Wuhan, Hubei, China
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2.生猪健康养殖协同创新中心实验室，湖北 武汉
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Virus Evolution, 2023, 9(2): vead051., articleTitle=Newly identified lineages of porcine hemagglutinating encephalomyelitis virus exhibit respiratory phenotype, refAbstract=null), Reference(id=1217784608863732434, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1204800732273812022, doi=null, pmid=null, pmcid=null, year=2024, volume=34, issue=null, pageStart=5685, pageEnd=5696, url=null, language=null, rfNumber=[27], rfOrder=28, authorNames=GOLDSTEIN SA, FEELEY TM, BABLER KM, HILBERT ZA, DOWNHOUR DM, MOSHIRI N, ELDE NC, journalName=Current Biology, refType=null, unstructuredReference=GOLDSTEIN SA, FEELEY TM, BABLER KM, HILBERT ZA, DOWNHOUR DM, MOSHIRI N, ELDE NC. Hidden evolutionary constraints dictate the retention of coronavirus accessory genes[J]. Current Biology, 2024, 34: 5685-5696. e5683., articleTitle=Hidden evolutionary constraints dictate the retention of coronavirus accessory genes, refAbstract=null)], funds=[Fund(id=1217784604229026289, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1204800732273812022, awardId=CARS-35, language=EN, fundingSource=Fundamental Research Funds for the Earmarked Fund(CARS-35), fundOrder=null, country=null), Fund(id=1217784604371632633, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1204800732273812022, awardId=CARS-35, language=CN, fundingSource=国家现代农业产业技术体系资助项目(CARS-35), fundOrder=null, country=null), Fund(id=1217784604501656064, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1204800732273812022, awardId=2662023DKPY004, language=EN, fundingSource=Fundamental Research Funds for the Central Universities(2662023DKPY004), fundOrder=null, country=null), Fund(id=1217784604589736450, tenantId=1146029695717560320, 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departmentName=null, remark=4.Hubei Hongshan Laboratory, Wuhan, Hubei, China), AuthorCompanyExt(id=1217784597870461003, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1204800732273812022, companyId=1217784597849489482, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=4.湖北洪山实验室，湖北 武汉)])], figs=[ArticleFig(id=1217784602589053334, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1204800732273812022, language=EN, label=Figure 1, caption=Isolation and identification of PHEV from tissue samples. A: N gene fragment amplification results of tissue samples (M: DL2000 molecular weight marker; 1: Tonsil; 2: Brain tissue; 3: PHEV positive control; 4: PHEV negative control); B: Sanger sequencing results (N gene fragment); C: Indirect immunofluorescence results on HRT-18 cells (Red fluorescence represents PHEV virus signal); D: Electron micrograph of the virus., figureFileSmall=0J3G/LmqXElItU+gJp689g==, figureFileBig=YCfQy8pnB1uddEd8EYiUDQ==, tableContent=null), ArticleFig(id=1217784602710688158, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1204800732273812022, language=CN, label=图1, caption=组织样本的PHEV的分离鉴定。A：组织样本的N基因片段扩增结果(M：DL2000分子量标志物；1：扁桃体；2：脑组织；3：PHEV阳性对照；4：PHEV阴性对照)；B：Sanger测序结果(N基因片段)；C：HRT-18细胞上的间接免疫荧光结果(红色荧光代表PHEV病毒信号)；D：病毒电镜图。, figureFileSmall=0J3G/LmqXElItU+gJp689g==, figureFileBig=YCfQy8pnB1uddEd8EYiUDQ==, tableContent=null), ArticleFig(id=1217784602844905895, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1204800732273812022, language=EN, label=Figure 2, caption=Proliferation of PHEV JS-2025 in HRT-18 cells. The growth kinetics of PHEV JS-2025 were analyzed in HRT-18 cells. Cells were infected at an MOI of 0.01 and supernatants were collected at 12, 24, 36, 48, 72, 84, 96, and 108 h post infection (hpi) and analyzed for viral titers through TCID50., figureFileSmall=K+wW2TEm3YxGM8ytF1u6RQ==, figureFileBig=G6H60f9Vfu+QQ/CxYzAOMw==, tableContent=null), ArticleFig(id=1217784602983317934, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1204800732273812022, language=CN, label=图2, caption=PHEV JS-2025在HRT-18细胞中增殖动态。在HRT-18细胞中分析PHEV JS-2025的生长动力学。以 0.01的MOI感染细胞，并在感染后12、24、36、48、72、84、96和108 h (hpi)收集上清，通过TCID50分析病毒滴度。, figureFileSmall=K+wW2TEm3YxGM8ytF1u6RQ==, figureFileBig=G6H60f9Vfu+QQ/CxYzAOMw==, tableContent=null), ArticleFig(id=1217784603092369844, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1204800732273812022, language=EN, label=Figure 3, caption=Tropism of PHEV JS-2025 cells. Cells were fixed and incubated with PHEV mAb overnight. Positive reactions were shown using goat anti-mouse IgG 594 (red). Cell nuclei were counterstained with DAPI (blue). Scale bar 200 μm., figureFileSmall=ioB55sVyXD5XvkvTVEAhXg==, figureFileBig=TeKyspTt0l8INvMeZV9hjQ==, tableContent=null), ArticleFig(id=1217784603201421752, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1204800732273812022, language=CN, label=图3, caption=PHEV JS-2025细胞嗜性。细胞经固定后与PHEV mAb过夜孵育，使用山羊抗鼠IgG 594显示阳性反应(红色)，细胞核用DAPI对比染色(蓝色)。比例尺为200 μm。, figureFileSmall=ioB55sVyXD5XvkvTVEAhXg==, figureFileBig=TeKyspTt0l8INvMeZV9hjQ==, tableContent=null), ArticleFig(id=1217784603335639487, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1204800732273812022, language=EN, label=Figure 4, caption=Phylogenetic analysis based on the nucleotide sequences corresponding to the whole genome sequence. A: Genetic evolution analysis of whole genome nucleotide sequences; B: Genetic evolution analysis of S genome nucleotide sequences; C: Genetic evolution analysis of HE genome nucleotide sequences; D: Characterization of NS2 gene deletion patterns., figureFileSmall=4xTAIJtIMTU1nx7Bkiyq1g==, figureFileBig=P1f1L91oPyV9Xy2caqHQdA==, tableContent=null), ArticleFig(id=1217784603474051525, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1204800732273812022, language=CN, label=图4, caption=基于PHEV JS-2025基因组核苷酸序列的序列分析。A：全基因组核苷酸序列遗传演化分析；B：S基因核苷酸序列遗传演化分析；C：HE基因核苷酸序列遗传演化分析；D：NS2基因缺失分析。, figureFileSmall=4xTAIJtIMTU1nx7Bkiyq1g==, figureFileBig=P1f1L91oPyV9Xy2caqHQdA==, tableContent=null), ArticleFig(id=1217784603612463561, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1204800732273812022, language=EN, label=Table 1, caption=

Primer sequences for PHEV complete genome amplification

, figureFileSmall=null, figureFileBig=null, tableContent=
Primers nameFragment size (bp)Primer sequences (5ʹ→3ʹ)
PHEV-PD1-F4 132GATTGTGAGCGAATTGCGTGCGTG
PHEV-PD1-RCACCATGTGCCATATGGCCGTTAGC
PHEV-PD2-F4 332GCGTAGTGTGTATAAAGCAGCTTGTGTCG
PHEV-PD2-RGTCAATTCAAGACCTGCCGACACAGC
PHEV-PD3-F4 286CTGCCAATACTGGTACGTCTGTTACAG
PHEV-PD3-RGAGAGCCAAATCTGCCATACGCTCC
PHEV-PD4-F4 222GCGACGATTACGCAAAGGACAATACTG
PHEV-PD4-RAAGAGGCTTTCTGATGCAACTGCCAC
PHEV-PD5-F4 564AGGAGCTGGATGCTTTGTGGATGA
PHEV-PD5-RGCTGGAGTCGTACGAAACAAACTCCTG
PHEV-PD6-F4 320AGCTCTGGCAACCTCTACCATCTTT
PHEV-PD6-RAGCCAAGCTTCGATATCGCAATTGG
PHEV-PD7-F4 691CTTCTAGCCTTTGACCAGGATGGTG
PHEV-PD7-RGATCGGCCCACTTAAGGATGCCAT
PHEV-PD8-F1 770GACAGGATAGGCGATACTAGTGGT
PHEV-PD8-RGTGATTCTTCCAATTGGCCATGATTAACTTC
), ArticleFig(id=1217784603767652819, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1204800732273812022, language=CN, label=表1, caption=

PHEV全基因组扩增引物序列

, figureFileSmall=null, figureFileBig=null, tableContent=
Primers nameFragment size (bp)Primer sequences (5ʹ→3ʹ)
PHEV-PD1-F4 132GATTGTGAGCGAATTGCGTGCGTG
PHEV-PD1-RCACCATGTGCCATATGGCCGTTAGC
PHEV-PD2-F4 332GCGTAGTGTGTATAAAGCAGCTTGTGTCG
PHEV-PD2-RGTCAATTCAAGACCTGCCGACACAGC
PHEV-PD3-F4 286CTGCCAATACTGGTACGTCTGTTACAG
PHEV-PD3-RGAGAGCCAAATCTGCCATACGCTCC
PHEV-PD4-F4 222GCGACGATTACGCAAAGGACAATACTG
PHEV-PD4-RAAGAGGCTTTCTGATGCAACTGCCAC
PHEV-PD5-F4 564AGGAGCTGGATGCTTTGTGGATGA
PHEV-PD5-RGCTGGAGTCGTACGAAACAAACTCCTG
PHEV-PD6-F4 320AGCTCTGGCAACCTCTACCATCTTT
PHEV-PD6-RAGCCAAGCTTCGATATCGCAATTGG
PHEV-PD7-F4 691CTTCTAGCCTTTGACCAGGATGGTG
PHEV-PD7-RGATCGGCCCACTTAAGGATGCCAT
PHEV-PD8-F1 770GACAGGATAGGCGATACTAGTGGT
PHEV-PD8-RGTGATTCTTCCAATTGGCCATGATTAACTTC
), ArticleFig(id=1217784603885093341, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1204800732273812022, language=EN, label=Table 2, caption=

PHEV strains used in this study

, figureFileSmall=null, figureFileBig=null, tableContent=
NameGenBankCountryHostYears
PHEV/67N/US/1970MW165134.1USASus scrofa1970
PHEV_CC14MF083115.1ChinaSus scrofa2014
PHEV_JL/2008KY994645.1ChinaSus scrofa2008
PHEV_VW572DQ011855.1BelgiumSus scrofa2006
PHEV-swine/USA/15TOSU1785KY419106.1USASus scrofa2015
PHEV-swine/USA/15TOSU1209KY419107.1USASus scrofa2015
PHEV-swine/USA/15TOSU0582KY419105.1USASus scrofa2015
PHEV-swine/USA/15TOSU1582KY419110.1USASus scrofa2015
PHEV-swine/USA/15TOSU2504KY419103.1USASus scrofa2015
PHEV/HLJ/2017OQ305206.1ChinaSus scrofa2017
PHEV/ZJ/2017OQ305208.1ChinaSus scrofa2017
PHEV/SC/2017OQ305207.1ChinaSus scrofa2017
rvPHEV4OQ798824.1ChinaSus scrofa2019
rvPHEV15OQ798811.1ChinaSus scrofa2019
), ArticleFig(id=1217784604006728163, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1204800732273812022, language=CN, label=表2, caption=

本研究所用的PHEV毒株

, figureFileSmall=null, figureFileBig=null, tableContent=
NameGenBankCountryHostYears
PHEV/67N/US/1970MW165134.1USASus scrofa1970
PHEV_CC14MF083115.1ChinaSus scrofa2014
PHEV_JL/2008KY994645.1ChinaSus scrofa2008
PHEV_VW572DQ011855.1BelgiumSus scrofa2006
PHEV-swine/USA/15TOSU1785KY419106.1USASus scrofa2015
PHEV-swine/USA/15TOSU1209KY419107.1USASus scrofa2015
PHEV-swine/USA/15TOSU0582KY419105.1USASus scrofa2015
PHEV-swine/USA/15TOSU1582KY419110.1USASus scrofa2015
PHEV-swine/USA/15TOSU2504KY419103.1USASus scrofa2015
PHEV/HLJ/2017OQ305206.1ChinaSus scrofa2017
PHEV/ZJ/2017OQ305208.1ChinaSus scrofa2017
PHEV/SC/2017OQ305207.1ChinaSus scrofa2017
rvPHEV4OQ798824.1ChinaSus scrofa2019
rvPHEV15OQ798811.1ChinaSus scrofa2019
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猪血凝性脑脊髓炎病毒JS-2025株分离与鉴定
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朱文龙 1, 2, 3 , 张梦迪 1, 2, 3 , 刘长城 1, 2, 3 , 景然 1, 2, 3 , 任方超 1, 2, 3 , 何启盖 1, 2, 3 , 张梦佳 1, 2, 3, 4, * , 李文涛 1, 2, 3, 4, *
微生物学报 | 研究报告 2025,65(12): 5605-5616
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微生物学报 | 研究报告 2025, 65(12): 5605-5616
猪血凝性脑脊髓炎病毒JS-2025株分离与鉴定
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朱文龙1, 2, 3, 张梦迪1, 2, 3, 刘长城1, 2, 3, 景然1, 2, 3, 任方超1, 2, 3, 何启盖1, 2, 3, 张梦佳1, 2, 3, 4, * , 李文涛1, 2, 3, 4, *
作者信息
  • 1.华中农业大学 动物医学院，湖北 武汉
  • 2.生猪健康养殖协同创新中心实验室，湖北 武汉
  • 3.农业微生物资源发掘与利用全国重点实验室，湖北 武汉
  • 4.湖北洪山实验室，湖北 武汉
Isolation and identification of the porcine hemagglutinating encephalomyelitis virus strain JS-2025
Wenlong ZHU1, 2, 3, Mengdi ZHANG1, 2, 3, Changcheng LIU1, 2, 3, Ran JING1, 2, 3, Fangchao REN1, 2, 3, Qigai HE1, 2, 3, Mengjia ZHANG1, 2, 3, 4, * , Wentao LI1, 2, 3, 4, *
Affiliations
  • 1.College of Veterinary Medicine, Huazhong Agricultural University, Wuhan, Hubei, China
  • 2.The Cooperative Innovation Center for Sustainable Pig Production, Wuhan, Hubei, China
  • 3.National Key Laboratory of Agricultural Microbiology, Wuhan, Hubei, China
  • 4.Hubei Hongshan Laboratory, Wuhan, Hubei, China
出版时间: 2025-12-04 doi: 10.13343/j.cnki.wsxb.20250446
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猪血凝性脑脊髓炎病毒(porcine hemagglutinating encephalomyelitis virus, PHEV)属于β冠状病毒属成员，在大多数猪群中流行，也是已知唯一可引起猪神经症状的冠状病毒。 目的 分析中国分离的猪血凝性脑脊髓炎病毒(PHEV)毒株的基因组特征及其系统发育关系。通过深入研究病毒株的生物学特性，系统评估其在我国猪群中的流行病学现状，阐明其遗传变异模式和进化趋势，为开发针对性防控产品提供科学依据。 方法 对中国江苏地区某规模化猪场送检的疑似PHEV阳性样本进行RT-PCR检测，并分离PHEV，通过间接免疫荧光(indirect immunofluorescence assay, IFA)染色和透射电子显微镜(transmission electron microscopy, TEM)对分离的病毒进行验证。根据PHEV JS-2025株全基因组测序结果对全基因组、S基因、HE基因和NS2基因进行了基因组系统发育分析和同源性比较。 结果 成功从脑组织样品中分离获得1株PHEV，命名为PHEV JS-2025。IFA结果显示细胞质中出现明显的荧光信号；电镜观察可见直径约150 nm的典型冠状病毒颗粒。病毒在HRT-18细胞中增殖良好，72 h时病毒滴度达到峰值，半数组织培养感染剂量(tissue culture infectious dose 50%, TCID50)约为104.3 TCID50/mL。PHEV JS-2025能够感染HRT-18、NPTR、LLC-PK1细胞，且对Caco-2细胞具有一定感染性。全基因组测序结果显示，PHEV JS-2025全长30 044 bp，与14个已知PHEV毒株核苷酸一致性均在94.9%以上，属于rvPHEV-L-1谱系，其NS2基因在第19个氨基酸位点出现提前终止导致NS2蛋白功能性缺失。 结论 成功分离并鉴定了1株来自江苏地区的新型PHEV毒株JS-2025。该毒株具有独特的细胞趋向性特征，能够感染人源肠道细胞系，提示其具有潜在的跨种传播风险。NS2基因的截短突变可能影响病毒的致病性。本研究为深入了解PHEV的遗传进化特征和流行病学特点提供了重要的科学依据，对猪血凝性脑脊髓炎(PHE)的防控具有重要意义。

猪血凝性脑脊髓炎病毒  /  分离鉴定  /  遗传演化分析

Porcine hemagglutinating encephalomyelitis virus (PHEV), a member of the betacoronavirus genus, is widespread in swine herds and the only known coronavirus causing neurological diseases in pigs. Objective To characterize the genomic features and phylogenetic relationship of a PHEV strain isolated from China. By investigating the biological properties of the virus, we assessed its epidemiological status and identified genetic variation patterns and evolutionary trends, providing a scientific basis for developing targeted prevention and control strategies. Methods RT-PCR detection was performed on suspected PHEV-positive samples collected from a large pig farm in Jiangsu Province, China, followed by virus isolation. The isolated virus was validated by indirect immunofluorescence assay (IFA), transmission electron microscopy (TEM), and whole genome sequencing. Phylogenetic analysis was performed based on the complete genome, S gene, HE gene, and NS2 gene. Results A PHEV strain, designated as PHEV JS-2025, was successfully isolated from the brain tissue sample. IFA showed strong red fluorescence signals in the cytoplasm, and TEM revealed typical coronavirus particles with a diameter of approximate 150 nm. The strain showed vigorous propagation in HRT-18 cells, reaching the peak viral titer at 72 h, with a 50% tissue culture infectious dose (TCID50) of about 104.3 TCID50/mL. PHEV JS-2025 could infect HRT-18, NPTR, and LLC-PK1 cells, and to a lesser extent, human intestinal Caco-2 cells. Whole genome sequencing revealed that the genome of PHEV JS-2025 was 30 044 bp in length, with over 94.9% nucleotide sequence identity to 14 reference PHEV strains, clustering within the rvPHEV-L-1 lineage. Of note, a mutation in the NS2 gene caused a premature termination at amino acid 19, resulting in the functional loss of the NS2 protein. Conclusion A novel PHEV strain JS-2025 from Jiangsu Province was successfully isolated and identified. This strain exhibits unique cellular tropism and can infect human intestinal cell lines, showing a risk of cross-species transmission. The truncated NS2 gene may affect the pathogenic mechanism of this strain. This study aids in understanding the genetic evolutionary characteristics and epidemiological features of PHEV and has implications for the prevention and control of PHE.

porcine hemagglutinating encephalomyelitis virus  /  isolation and identification  /  genetic evolutionary analysis
朱文龙, 张梦迪, 刘长城, 景然, 任方超, 何启盖, 张梦佳, 李文涛. 猪血凝性脑脊髓炎病毒JS-2025株分离与鉴定. 微生物学报, 2025 , 65 (12) : 5605 -5616 . DOI: 10.13343/j.cnki.wsxb.20250446
Wenlong ZHU, Mengdi ZHANG, Changcheng LIU, Ran JING, Fangchao REN, Qigai HE, Mengjia ZHANG, Wentao LI. Isolation and identification of the porcine hemagglutinating encephalomyelitis virus strain JS-2025[J]. Acta Microbiologica Sinica, 2025 , 65 (12) : 5605 -5616 . DOI: 10.13343/j.cnki.wsxb.20250446
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猪血凝性脑脊髓炎(porcine hemagglutinating encephalomyelitis, PHE)是由猪血凝性脑脊髓炎病毒(porcine hemagglutinating encephalomyelitis virus, PHEV)引起的一种高度接触性传染病，又称冠状病毒性脑膜脑炎，主要感染1-3周龄哺乳仔猪。该病以呕吐和脑脊髓炎为特征性临床表现，是目前已知唯一可感染猪神经系统的冠状病毒[1-2]。自1958年在加拿大安大略省首次暴发以来[3]，该病已在全球范围内蔓延，部分养殖场发病率高达100%，显著影响仔猪存活率，给养猪业造成重大经济损失[2]。
PHEV属于冠状病毒科(Coronaviridae) β冠状病毒属(Betacoronavirus, β-CoV)，是一种有包膜的非分节段单链正义RNA病毒。电镜下观察呈球形，直径在100-150 nm之间，具有典型的“冠状”结构特征。其结构蛋白包括：刺突蛋白(S)、膜蛋白(M)、血凝素酯酶蛋白(HE)、核衣壳蛋白(N)和小膜蛋白(SM或E)[4]。S蛋白作为病毒颗粒表面的糖蛋白，介导冠状病毒的吸附和侵入。M蛋白是病毒包膜中含量最丰富的结构蛋白，对病毒颗粒的形态起决定性作用[2]。E蛋白也是病毒颗粒包膜的组成部分。N蛋白是含量最丰富的病毒蛋白，在稳定基因组RNA功能方面发挥重要作用[5]。M蛋白与E蛋白以及N蛋白相互作用，在子代病毒的组装和出芽过程中具有重要作用[2,6]。HE蛋白是一种特殊的糖蛋白，是由二硫键连接的2个亚基组成的二聚体蛋白[7-8]。HE蛋白仅存在于β属冠状病毒A亚群和C型流感病毒中，推测是冠状病毒与流感病毒进化过程中通过重组获得的，其作用可能与流感病毒的NA类似[9]。
在自然条件下PHEV仅感染猪，其中育肥猪和成年猪多表现为亚临床症状或潜伏感染，感染率极高，是主要传染源。该病毒主要经呼吸道传播，在宿主呼吸道中复制[10]，随后可通过周围神经系统扩散至中枢神经系统[11]，引起宿主出现临床症状。目前市面上尚无有效的PHEV疫苗，因此预防哺乳仔猪感染的有效方式是诱导母猪产生母源抗体，从而为哺乳仔猪提供被动免疫保护。
目前，PHEV的诊断主要结合临床综合诊断和实验室诊断。临床诊断是通过结合临床症状和病理变化进行，如对感染动物的脑、脊髓和肌间神经丛进行病理切片观察[12]。实验室诊断则依据实验技术对病原体及其抗体进行鉴定和确认，包括逆转录PCR (reverse transcription-PCR, RT-PCR)、病毒分离和免疫学方法。其中，RT-PCR主要用于扁桃体、脊髓和口腔液样本中PHEV的鉴定。PHEV可在多种细胞中增殖，如PK-15、N2a和猪次代甲状腺细胞(SPTh)，其中PK-15和SPTh已被证实是对该病毒最敏感的细胞[13]，但其对其他细胞的感染性尚待系统研究。
本研究采集江苏地区猪场疑似感染猪的脑组织样品，经PCR检测和病毒分离鉴定后确定为PHEV感染，将分离得到的毒株命名为PHEV JS-2025株，并进一步对分离株进行生物学特性和遗传进化分析，以期为江苏地区可能流行的PHEV毒株研究提供参考，为我国PHEV研究提供重要材料。
1 材料与方法
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1.1 样品处理
在江苏省出现疑似PHEV感染病例时，采集病死仔猪组织样本进行PHEV检测。收集扁桃体和脑组织样本，保存于DMEM培养基中。将PHEV阳性的脑组织样本用磷酸盐缓冲液(0.1 mol/L，pH 7.2)制备成10%的组织匀浆。将悬液在4 ℃、4 500×g离心10 min，经0.22 μm注射器滤器过滤后用作病毒分离接种物。
1.2 核酸提取和RT-PCR检测
总RNA提取按照TRIzol试剂盒(Invitrogen公司)说明书进行，具体操作如下：取200 μL样品与1 mL TRIzol裂解液混合，室温孵育5 min；随后加入200 μL氯仿，剧烈涡旋混匀后置于冰上10 min；4 ℃、12 000×g离心10 min后，小心收集上清并与等体积异丙醇混合。将混合液颠倒混匀后室温静置10 min，再次离心。弃去上清，加入1 mL无水乙醇洗涤，4 ℃、12 000×g离心10 min后自然干燥。最后将RNA溶解于RNase-free水中，分装后保存于-80 ℃。
使用PrimeScriptTM RT试剂盒(TaKaRa公司)对每个样本进行cDNA合成。按照说明书，采用高保真酶(PrimeSTAR Max DNA Polymerase，TaKaRa公司)进行PHEV-N基因片段(289 bp)的RT-PCR检测。扩增所用引物为PHEV-N-F (5′- TGCTGCCACGATGGTACTTT-3′)和PHEV-N-R (5′-CTACGCGATCCTGAACTAGG-3′)。
1.3 病毒的分离鉴定
将过滤后的悬液接种于HRT-18细胞，37 ℃、5% CO2培养。吸附1 h后，加入含1%血清的DMEM，培养5 d后将剩余上清接种HRT-18细胞进行传代培养，盲传3代并通过RT-PCR、间接免疫荧光试验进行初步鉴定，然后通过透射电镜观察进行进一步鉴定，观察病毒颗粒形态。病毒培养液经2 500×g离心30 min去除细胞碎片后，上清液以30 000×g离心120 min，沉淀重悬于水中。样品经磷钨酸(pH 6.4)染色后喷雾于200目铜网上，然后进行透射电镜观察。
1.4 间接免疫荧光试验
将PHEV JS-2025以0.01的病毒感染复数(multiplicity of infection, MOI)感染HRT-18细胞，感染后72 h收取细胞样品。用PBS洗涤3次，4%多聚甲醛室温固定15 min，0.1% Triton X-100透化15 min，5%牛血清白蛋白(bovine serum albumin, BSA)室温封闭2 h，4 ℃ PHEV S1 mAb (1:2 000)孵育过夜。用PBST洗涤3次后，用Alexa Fluor® 594驴抗小鼠IgG (H+L)在37 ℃下孵育45 min。最后用PBST洗涤细胞3次，用4′,6-二氨基-2-苯基吲哚(4′,6-diamidino-2-phenylindole, DAPI)染色液孵育5 min，最后在倒置荧光显微镜下观察图像。
1.5 半数组织培养感染剂量(tissue culture infectious dose 50%, TCID50)的测定
提前24 h以5×103/mL的细胞密度将HRT-18细胞铺于96孔细胞板中准备感染，将PHEV进行连续10倍倍比稀释至10-8，然后将稀释好的病毒加入各细胞孔中，每孔100 μL，每个稀释度重复8个孔，同时设置不加病毒的正常细胞作对照。37 ℃培养72 h之后弃去上清，采用间接免疫荧光试验进行TCID50的测定，步骤同1.4节。最后用Reed-Muench方法计算TCID50。
1.6 病毒生长曲线的绘制
以0.01 MOI感染HRT-18细胞，于37 ℃细胞培养箱中培养，分别在感染后12、24、36、48、72、84、96和108 h (hpi)收集上清。利用间接免疫荧光(indirect immunofluorescence assay, IFA)试验读取细胞病变孔数，应用Reed-Muench法计算每个时间点的TCID50 (步骤同1.5节)，以收毒时间点为横坐标，TCID50的对数为纵坐标建立病毒的多步生长曲线。
1.7 病毒的细胞嗜性
为研究PHEV的细胞感染谱，将相同感染复数(MOI=0.01)的PHEV接种于不同细胞系中，包括Caco-2、Vero、HeLa、HEK-293T、Marc145、HRT-18、NPTR、LLC-PK1和N2a细胞。感染72 h后，使用实验室制备的靶向PHEV-S蛋白的单克隆抗体进行IFA试验以观察病毒在各细胞系中的感染情况。
1.8 病毒基因组扩增与测序
根据NCBI数据库(https://www.ncbi.nlm.nih.gov/)中可获得的PHEV毒株全基因组序列信息，使用DNA Club Primer Permier 5.0和DNAMAN软件设计全基因组扩增引物。使用PrimeSTAR Max试剂盒对该毒株的cDNA进行扩增、回收和测序。通过整合参考序列组装和从头组装的结果获得最终的组装序列。序列数据已提交至GenBank数据库，登录号为PV730382。扩增所用的引物序列的详细信息见表1。
1.9 基于全基因组、S基因、N基因和M基因的系统发育与同源性分析
从GenBank数据库获取了来自不同流行国家的15个PHEV全基因组序列。这些序列的GenBank登录号、分离年份和国家信息详见表2。将本研究获得的序列与不同流行国家的病毒毒株进行比对。首先使用DNAStar软件(v7.0)中MegAlign功能的ClustalW方法进行序列比对，随后使用MEGA软件(v12.0)的邻接(neighbor-joining, NJ)法构建系统发育树，自展值设为1 000。
2 结果与分析
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2.1 PHEV分离结果
使用PHEV-N特异性引物对处理好的样本进行RT-PCR检测，结果如图1A所示。2个测试样本均成功扩增出289 bp的片段，且经测序确认样本扩增的基因为PHEV-N (图1B)，这表明样本中存在PHEV。
为进一步确认诊断结果，使用PHEV阳性的脑组织进行病毒分离。将脑组织样本上清接种于HRT-18细胞中进行病毒分离。间接免疫荧光试验(IFA)显示，细胞质中可见明显的红色阳性信号(图1C)。此外，对分离的病毒颗粒进行负染电镜形态学观察(图1D)，分析显示存在典型的、直径约150 nm的冠状病毒样颗粒。综合特征性临床症状、PHEV特异性片段的成功扩增，以及IFA和电镜观察等结果，确认该病毒为PHEV，并将其命名为PHEV JS-2025。
2.2 PHEV JS-2025在HRT-18细胞中增殖动态
根据Reed-Muench法，增殖动态监测显示该病毒接种HRT-18细胞后病毒滴度在24-72 h逐渐提高，在72 h病毒滴度达到峰值，约为104.3 TCID50/mL，随后开始缓慢下降(图2)。
2.3 病毒的细胞嗜性
PHEV以相同的病毒剂量(MOI=0.01)分别感染Caco-2、Vero、HeLa、HEK-293T、Marc145、HRT-18、NPTR、LLC-PK1和N2a细胞72 h。随后通过免疫荧光试验(IFA)检测PHEV在各细胞系中的感染情况。如图3所示，PHEV能够成功感染HRT-18、NPTR和LLC-PK1细胞。虽然未观察到明显的细胞病变效应，但PHEV在HRT-18细胞中表现出最佳的感染性。此外，PHEV还能感染少部分Caco-2细胞，而在其他受试细胞系中未见成功感染。
2.4 基于全基因组、S、HE的基因分析
为全面了解所分离的PHEV JS-2025毒株的遗传特征及其与其他PHEV毒株的关系，本研究成功获得了PHEV JS-2025毒株的全基因组序列，其全长为30 044 bp。对PHEV JS-2025株全基因组核苷酸序列进行分析发现，PHEV JS-2025与其他14个毒株在核苷酸水平上具有94.9%以上的遗传相似性。其中，它与1972年在比利时分离出的VW572株相似性最高，一致性达99.2%；而与PHEV/HLJ/2017的遗传亲缘性较低，为94.9%。全基因组的系统发育树分析表明，PHEV JS-2025株所在的分支与VW572毒株分支亲缘关系较近(图4A)。
对S基因的分析结果呈现出不同情况。PHEV JS-2025株与rvPHEV4的相似性最高，其亲缘关系与PHEV/SC/2017毒株较近，属于rvPHEV-L-1谱系。这一结果与HE基因比对结果相似。对基因组NS2同源性和系统发育树进行分析后发现，PHEV JS-2025株的NS2基因在第19个氨基酸处出现了提前终止的现象，导致缺乏功能性NS2蛋白(图4B-4D)。
3 讨论与结论
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冠状病毒分为α、β、γ和δ 4个属。β属冠状病毒包括PHEV、牛冠状病毒(BCoV)、人冠状病毒(HCoV-OC43和HCoV-HKU1)以及严重急性呼吸综合征冠状病毒(SARS-CoV)。同属β属冠状病毒的SARS-CoV-2已被确认可能源自动物[14]。这种具有高致病性的β冠状病毒的人兽共患暴发凸显了冠状病毒显著的适应能力、基因可塑性以及广泛的宿主感染范围[15]。因此，本研究进一步探究了另一种哺乳动物β冠状病毒PHEV的进化特征。
自1958年加拿大首次发现PHE以来，多项血清学调查表明PHEV感染已在全球广泛传播[16-17]。中国首次记录的PHE暴发发生在1985年。1994年，中国台湾暴发PHE，致死率高达近100%，给当地养猪业造成重大经济损失[18]。目前，PHE的典型临床表现为新生仔猪出现呕吐和消瘦综合征(VWD)或脑脊髓炎[1,19]。然而，PHEV呈地方性流行，在个别养殖场更常见成年猪的亚临床或隐性感染[12,18]。病毒通过长期隐性传播很可能发生基因突变，导致毒力随时间增强。因此，了解该病原体的遗传特征和流行病学趋势至关重要。
本研究对疑似感染猪的样本进行RT-PCR检测，基于RT-PCR结果和后续的测序分析初步诊断确认为PHEV感染。将组织上清接种到HRT-18细胞上并盲传至第3代，随后使用PHEV单克隆抗体进行免疫荧光验证。实验结果显示明显的阳性信号，为确认病原体为PHEV提供了进一步证据。此外，通过负染电镜观察确认了PHEV的存在，进一步证实了诊断结果。
人兽共患病的传播对全球公共卫生构成重大威胁。在最受关注的病原体中，人兽共患冠状病毒表现出向人类和其他重要家养物种跨种传播的较高倾向[20]。蝙蝠已被确认可能是所有影响动物和人类的冠状病毒的来源[21]。同时，PHEV被认为起源于牛冠状病毒，而牛冠状病毒可能是通过啮齿类适应进化自蝙蝠病毒[22]。为研究PHEV对不同类型细胞的感染性和选择性，并深入了解其宿主嗜性和传播倾向，本研究使用PHEV JS-2025毒株进行了细胞趋向性试验。结果表明，PHEV JS-2025毒株能在人肠道细胞(HRT-18和Caco-2细胞)、猪呼吸道细胞(NPTR细胞)和猪肾细胞(LLC-PK1)中复制。这提示随着自然进化和循环，该病毒可能扩大其宿主范围并感染人类。这些发现为理解PHEV JS-2025的生物学特性、跨种传播潜力以及病毒在不同宿主环境中的选择性偏好提供了重要信息。尽管PHEV JS-2025是从猪脑组织中分离获得的，但其在体外未能有效感染N2a细胞，这可能是在脑组织分离过程中病毒主要来源于感染的胶质细胞[23]。这些非神经元细胞可能充当病毒在中枢神经系统(CNS)中的主要宿主，支持其体内神经嗜性，但分离株在体外传代后偏好非神经元细胞系。
全基因组序列分析显示，PHEV JS-2025与之前报道的14个PHEV毒株的核苷酸相似性超过94.9%，与1972年在比利时分离的VW572毒株的相似性最高(99.2%)。这种跨地理区域和时间段的高度保守性表明PHEV具有相当的基因组稳定性，这与之前对其他冠状病毒的观察结果一致[12,15,24]。然而，基于S和HE基因的系统发育分析显示出与全基因组分析不同的进化关系，这表明PHEV JS-2025与rvPHEV4和PHEV/SC/2017的亲缘关系更密切，属于rvPHEV-L-1谱系。这些基因特异性系统发育之间的差异可能反映了作用于单个病毒基因的不同进化压力或PHEV进化过程中潜在的重组事件。需要注意的是，本研究在数据可及性方面存在一定局限性。目前，GenBank数据库中PHEV完整基因组序列的地理覆盖范围相对有限，这在一定程度上制约了对该病毒全球分布格局和进化动态的深入解析。为更全面地阐明PHEV的分子流行病学特征和进化规律，未来研究亟需构建多国协作的病原体基因组监测体系，通过标准化的数据采集和共享机制，在严格遵循生物安全伦理规范和数据隐私保护原则的前提下实现全球范围内PHEV基因组数据的实时整合与分析。
β-冠状病毒中的NS2蛋白作为2′,5′-磷酸二酯酶(PDE)发挥作用，拮抗OAS-RNase L通路，从而通过降解2′-5′寡腺苷酸并阻止RNase L激活，使病毒能够逃避宿主先天免疫反应，这种酶活性在A谱系β-冠状病毒中是保守的，包括小鼠肝炎病毒(MHV)和猪血凝性脑脊髓炎病毒(PHEV)，这强调了其在感染期间抑制抗病毒防御的作用[25]。第19个氨基酸位置的过早终止可能截断NS2的功能结构域，潜在地改变病毒复制适应性并赋予变异株诸如增强呼吸道嗜性等适应性[26]。与其他β-冠状病毒NS2变异的比较分析揭示了缺失或过早终止的模式，如在PHEV呼吸道变异株(rvPHEV)和相关毒株如HKU14中观察到的，表明进化压力倾向于组织特异性适应或宿主免疫逃避[27]。
JS-2025中NS2编码的提前终止可能影响其毒力、复制效率或免疫逃避能力。此外，尽管缺乏功能性NS2蛋白，JS-2025仍能在多种细胞类型中有效复制，这表明NS2可能并非PHEV复制的必需基因，或者其功能可能被其他病毒蛋白所补偿。
综上所述，本研究成功分离并鉴定了一株来自中国江苏省的新型PHEV毒株。PHEV JS-2025表现出独特的细胞趋向性和遗传特征，尤其是NS2基因的提前终止。这些发现为PHEV毒株的遗传关系和进化模式提供了重要信息，揭示了其潜在的起源、传播途径，以及监测病毒突变和进化的重要性，表明该病毒在地方性压力下会发生显著的进化。
作者贡献声明
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朱文龙：数据分析，撰写文章；张梦迪：方法论，项目管理；刘长城：验证；景然：软件程序；任方超：实验验证，监督管理；何启盖：方法论，审阅，项目支持；张梦佳：获取基金、提供资源；李文涛：提出概念，撰写、审阅。
作者利益冲突公开声明
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作者声明不存在任何可能会影响本文所报告工作的已知经济利益或个人关系。
基金
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  • 国家现代农业产业技术体系资助项目(CARS-35)
  • 中央高校基本科研业务费专项资金(2662023DKPY004)
  • 湖北省自然科学基金(2023AFB437)
  • 国家自然科学基金(32473007)
文献
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参考文献 引证文献
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doi: 10.13343/j.cnki.wsxb.20250446
  • 接收时间：2025-06-08
  • 首发时间：2025-12-08
  • 出版时间：2025-12-04
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  • 收稿日期：2025-06-08
  • 录用日期：2025-08-08
基金
Fundamental Research Funds for the Earmarked Fund(CARS-35)
国家现代农业产业技术体系资助项目(CARS-35)
Fundamental Research Funds for the Central Universities(2662023DKPY004)
中央高校基本科研业务费专项资金(2662023DKPY004)
Natural Science Foundation of Hubei Province(2023AFB437)
湖北省自然科学基金(2023AFB437)
National Natural Science Foundation of China(32473007)
国家自然科学基金(32473007)
作者信息
    1.华中农业大学 动物医学院，湖北 武汉
    2.生猪健康养殖协同创新中心实验室，湖北 武汉
    3.农业微生物资源发掘与利用全国重点实验室，湖北 武汉
    4.湖北洪山实验室，湖北 武汉

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2种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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