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Article(id=1320436285458723197, tenantId=1146029695717560320, journalId=1319373162502258839, issueId=1320436284418544199, articleNumber=null, orderNo=null, doi=10.16016/j.2097-0927.202512028, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=null, receivedDate=1764777600000, receivedDateStr=2025-12-04, revisedDate=1768060800000, revisedDateStr=2026-01-11, acceptedDate=null, acceptedDateStr=null, onlineDate=1792746142972, onlineDateStr=2026-10-23, pubDate=1772208000000, pubDateStr=2026-02-28, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1792746142972, onlineIssueDateStr=2026-10-23, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1792746142972, creator=13701087609, updateTime=1792746142972, updator=13701087609, issue=Issue{id=1320436284418544199, tenantId=1146029695717560320, journalId=1319373162502258839, year='2026', volume='48', issue='4', pageStart='387', pageEnd='522', issueExtLink='null', onlineDate='null', pubDate='1772208000000', pubDateStr='2026-02-28', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1792746142725, creator='13701087609', updateTime=1792750115637, updator='13701087609', preIssue=null, nextIssue=null, articleTotal=null, ext={EN=IssueExt(id=1320452948077953743, tenantId=1146029695717560320, journalId=1319373162502258839, issueId=1320436284418544199, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1320452948077953744, tenantId=1146029695717560320, journalId=1319373162502258839, issueId=1320436284418544199, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null, downloadFileDto=null}, startPage=445, endPage=452, ext={EN=ArticleExt(id=1320436285811044734, articleId=1320436285458723197, tenantId=1146029695717560320, journalId=1319373162502258839, language=EN, title=Functionally impaired CD103+CD39+CD8+ T cell subsets with immune-suppressive properties infiltrating gastric cancer tissues promote tumor progression, columnId=1320434418116837551, journalTitle=Journal of Army Medical University, columnName=Basic Medicine, runingTitle=null, highlight=null, articleAbstract=
Objective

To detect the infiltration level of CD103+CD39+CD8+ T cell subsets in gastric cancer tissues and analyze their response characteristics, clarifying the clinical relevance of this subset.

Methods

Surgical specimens (tumor tissues, adjacent tissues, and peripheral blood) were collected from gastric cancer patients at the Department of General Surgery, Second Affiliated Hospital of Army Medical University between January 2023 and May 2024. Flow cytometry and immunofluorescence staining quantified the proportion and number of CD103+CD39+CD8+ T cells in tumor versus adjacent tissues. Flow cytometry further analyzed CD69, PD-1, and IFN-γ expression in this subset. Peripheral blood mononuclear cells (PBMCs) were isolated and cultured in vitro to assess TGF-β1-induced differentiation. Correlation with disease stage was analyzed by detecting the infrltration level of CD103+CD39+CE8+ T Cell subsets via flow cytometry.

Results

Compared with adjacent tissues, gastric cancer tissues showed significantly increased proportions of CD103+CD39+CD8+ T cells (P<0.05); immunofluorescence confirmed higher numbers in tumor tissues. Relative to CD103+CD39- and CD103-CD39-CD8+ T subsets, CD103+CD39+CD8+ T cells exhibited elevated CD69 and PD-1 expression (P<0.05) but reduced IFN-γ (P<0.05). In vitro TGF-β1 stimulation upregulated co-expression of CD103 and CD39 in CD8+ T cells (P<0.05). Moreover, advanced gastric cancer patients had higher tumor infiltration of this subset than early-stage patients (P<0.05).

Conclusion

CD103+CD39+CD8+ T cell subsets display increased infiltration and functionally impaired responses in gastric cancer, facilitating tumor immune escape.

, authors=Mengqiu HUANG1, Hang ZHONG1, Yuan QIU2, Quanming ZOU3, Liusheng PENG3, Daiyuan MA1, authorsList=Mengqiu HUANG, Hang ZHONG, Yuan QIU, Quanming ZOU, Liusheng PENG, Daiyuan MA, authorCompany=null, correspAuthors=Liusheng PENG, Daiyuan MA, authorNote=null, correspAuthorsNote=null, copyrightStatement=© 2026 Journal of Army Medical University, copyrightOwner=Editorial Office of Journal of Army Medical University, extLink=null, articleAbsUrl=null, sourceXml=null, magXml=null, pdfUrl=null, pdf=null, pdfFileSize=null, pdfExtLink=null, richHtmlUrl=null, mobilePdfUrl=null, reviewReport=null, pdfFirstPage=null, abstractGraph=null, abstractGraphContent=null, abstractVideo=null, citation=null, cebUrl=null, magXmlContent=null, mapNumber=null, fund=null), CN=ArticleExt(id=1320436287086113161, articleId=1320436285458723197, tenantId=1146029695717560320, journalId=1319373162502258839, language=CN, title=胃肿瘤组织中浸润的免疫抑制性CD103+CD39+CD8+ T细胞亚群功能受损并促进肿瘤进展, columnId=1320434418343329969, journalTitle=陆军军医大学学报, columnName=论著·基础医学, runingTitle=null, highlight=null, articleAbstract=
目的

检测CD103+CD39+CD8+ T细胞亚群在胃肿瘤组织中的浸润水平并分析其应答特征，分析CD103+CD39+CD8+ T细胞亚群在人胃肿瘤组织中的的临床相关性。

方法

收集2023年1月至2024年5月在陆军军医大学第二附属医院普外科接受手术切除的32例胃癌患者的肿瘤组织、癌旁组织以及外周血标本。采用流式细胞术结合免疫荧光染色检测CD103+CD39+CD8+ T细胞亚群在胃肿瘤组织及癌旁组织中的应答比例与数目，并通过流式细胞术分析胃肿瘤组织中CD103+CD39+CD8+ T细胞亚群表达的CD69、PD-1与IFN-γ水平；体外分离培养外周血来源的单个核细胞，探究TGF-β1对CD103+CD39+CD8+ T细胞亚群的分化效果；通过流式细胞术检测CD103+CD39+CD8+ T细胞亚群的浸润水平，以分析其与疾病分期的相关性。

结果

与癌旁组织相比，CD103+CD39+CD8+ T细胞亚群在胃肿瘤组织中的比例明显增加（P<0.05）；免疫荧光染色进一步证实，胃肿瘤组织中CD103+CD39+CD8+ T 细胞亚群的数目亦明显多于癌旁组织；与CD103+CD39-和CD103-CD39-CD8+ T细胞亚群相比，CD103+CD39+CD8+ T细胞亚群表达的活化分子CD69和免疫检查点分子PD-1均增加（P<0.05），但功能相关因子IFN-γ的表达则显著下降（P<0.05）；体外TGF-β1刺激可诱导CD8+ T细胞中CD103与CD39的共表达上调（P<0.05）；此外，CD103+CD39+CD8+ T细胞亚群在晚期胃癌患者肿瘤组织中的浸润比例显著高于早期胃癌患者（P<0.05）。

结论

CD103+CD39+CD8+ T细胞亚群在胃肿瘤组织中的浸润增加，并展示出功能受抑的应答特征，从而有助于胃癌的免疫逃逸。

, authors=黄梦秋1, 钟杭1, 邱远2, 邹全明3, 彭六生3, 马代远1, authorsList=黄梦秋, 钟杭, 邱远, 邹全明, 彭六生, 马代远, authorCompany=null, correspAuthors=彭六生, 马代远, authorNote=null, correspAuthorsNote=
马代远，E-mail：
彭六生，E-mail：
MA Daiyuan，E-mail：
PENG Liusheng，E-mail：
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A： Representative dot plots of CD8+ T cells co-expressing CD103 and CD39； B： CD103+CD39+CD8+ T cell proportions

, figureFileSmall=m7/C0R1k6J4CALWaZmXg8Q==, figureFileBig=yl16/lBJB971eWbJ61QuTw==, tableContent=null), ArticleFig(id=1320436293599867326, tenantId=1146029695717560320, journalId=1319373162502258839, articleId=1320436285458723197, language=EN, label=Figure 2, caption=Immunofluorescence images of CD103+CD39+CD8+ T cells in different tissues of GC patients, figureFileSmall=Z5yvFLDfXFyfsB7EkJth/w==, figureFileBig=idtHb9cYK3WnlzNrBTIPsA==, tableContent=null), ArticleFig(id=1320436293725696447, tenantId=1146029695717560320, journalId=1319373162502258839, articleId=1320436285458723197, language=CN, label=图2, caption=胃癌患者不同组织中CD103+CD39+CD8+ T细胞亚群的免疫荧光染色图

Red： CD8； Light blue： CD103； Yellow： CD39； Dark blue： nucleus； White arrow： CD103+CD39+CD8+ T cells

, figureFileSmall=Z5yvFLDfXFyfsB7EkJth/w==, figureFileBig=idtHb9cYK3WnlzNrBTIPsA==, tableContent=null), ArticleFig(id=1320436293792805312, tenantId=1146029695717560320, journalId=1319373162502258839, articleId=1320436285458723197, language=EN, label=Figure 3, caption=Comparison of CD103+CD39+CD8+ T cell proportions between early stage and advanced stage GC patients, figureFileSmall=MN13fiMtOcnuskP7BsSYbw==, figureFileBig=MGa0Z0Gh2EI+T82aqwk1OA==, tableContent=null), ArticleFig(id=1320436293885080001, tenantId=1146029695717560320, journalId=1319373162502258839, articleId=1320436285458723197, language=CN, label=图3, caption=CD103+CD39+CD8+ T细胞亚群在早、晚期胃癌患者肿瘤组织中的比例比较

A： Representative dot plots of CD8+ T cells co-expressing CD103 and CD39； B： CD103+CD39+CD8+ T cell proportions

, figureFileSmall=MN13fiMtOcnuskP7BsSYbw==, figureFileBig=MGa0Z0Gh2EI+T82aqwk1OA==, tableContent=null), ArticleFig(id=1320436293960577474, tenantId=1146029695717560320, journalId=1319373162502258839, articleId=1320436285458723197, language=EN, label=Figure 4, caption=Phenotypic and functional analysis of CD103+CD39+CD8+ T cell subsets in GC tumor tissues, figureFileSmall=t4N6WPjGDhWazDaO9uRmMg==, figureFileBig=NDP/GdNcYgQDceNZPF4KFQ==, tableContent=null), ArticleFig(id=1320436294031880643, tenantId=1146029695717560320, journalId=1319373162502258839, articleId=1320436285458723197, language=CN, label=图4, caption=胃肿瘤组织中CD103+CD39+CD8+ T细胞亚群的表型与功能分析

A： Representative dot plots of tumor-infiltrating CD103+CD39+CD8+， CD103+CD39-CD8+ and CD103-CD39-CD8+ T cell subsets expressing CD69， PD-1 and IFN-γ in GC patients； B： The proportions of CD69， PD-1 and IFN-γ expression

, figureFileSmall=t4N6WPjGDhWazDaO9uRmMg==, figureFileBig=NDP/GdNcYgQDceNZPF4KFQ==, tableContent=null), ArticleFig(id=1320436294119961028, tenantId=1146029695717560320, journalId=1319373162502258839, articleId=1320436285458723197, language=EN, label=Figure 5, caption=Regulation of CD103 and CD39 co-expression on CD8+ T cells by TGF-β1, figureFileSmall=jBgXS83oL7v0l7cUDcuRiQ==, figureFileBig=yiUeSeIS1JbxnU9VzV8kuQ==, tableContent=null), ArticleFig(id=1320436294233207237, tenantId=1146029695717560320, journalId=1319373162502258839, articleId=1320436285458723197, language=CN, label=图5, caption=TGF-β1对CD8+ T细胞中CD103与CD39共表达的调控

A： Representative dot plots of CD8+ T cells co-expressing CD103 and CD39 at day 1 and day 3 in each group； B： CD103+CD39+CD8+ T cell proportions

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胃肿瘤组织中浸润的免疫抑制性CD103+CD39+CD8+ T细胞亚群功能受损并促进肿瘤进展
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黄梦秋 1 , 钟杭 1 , 邱远 2 , 邹全明 3 , 彭六生 3 , 马代远 1
陆军军医大学学报 | 论著·基础医学 2026,48(4): 445-452
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陆军军医大学学报 |论著·基础医学 2026 , 48 (4) : 445 -452
胃肿瘤组织中浸润的免疫抑制性CD103+CD39+CD8+ T细胞亚群功能受损并促进肿瘤进展
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黄梦秋1, 钟杭1, 邱远2, 邹全明3, 彭六生3 , 马代远1
作者信息
  • 1川北医学院附属医院肿瘤科，四川 南充
  • 2陆军军医大学（第三军医大学）第二附属医院普外科，重庆
  • 3陆军军医大学（第三军医大学）药学与检验医学系微生物与生化药学教研室，重庆
通讯作者:
马代远，E-mail：
彭六生，E-mail：
MA Daiyuan，E-mail：
PENG Liusheng，E-mail：
Functionally impaired CD103+CD39+CD8+ T cell subsets with immune-suppressive properties infiltrating gastric cancer tissues promote tumor progression
Mengqiu HUANG1, Hang ZHONG1, Yuan QIU2, Quanming ZOU3, Liusheng PENG3 , Daiyuan MA1
Affiliations
  • 1Affiliated Hospital of North Sichuan Medical College， Nanchong， Sichuan
  • 2Department of General Surgery， Second Affiliated Hospital， Army Medical University （Third Military Medical University）， Chongqing
  • 3Department of Microbiology and Biochemical Pharmacy， Faculty of Pharmacy and Laboratory Medicine， Army Medical University （Third Military Medical University）， Chongqing， China
出版时间: 2026-02-28 doi: 10.16016/j.2097-0927.202512028
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摘要
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目的

检测CD103+CD39+CD8+ T细胞亚群在胃肿瘤组织中的浸润水平并分析其应答特征，分析CD103+CD39+CD8+ T细胞亚群在人胃肿瘤组织中的的临床相关性。

方法

收集2023年1月至2024年5月在陆军军医大学第二附属医院普外科接受手术切除的32例胃癌患者的肿瘤组织、癌旁组织以及外周血标本。采用流式细胞术结合免疫荧光染色检测CD103+CD39+CD8+ T细胞亚群在胃肿瘤组织及癌旁组织中的应答比例与数目，并通过流式细胞术分析胃肿瘤组织中CD103+CD39+CD8+ T细胞亚群表达的CD69、PD-1与IFN-γ水平；体外分离培养外周血来源的单个核细胞，探究TGF-β1对CD103+CD39+CD8+ T细胞亚群的分化效果；通过流式细胞术检测CD103+CD39+CD8+ T细胞亚群的浸润水平，以分析其与疾病分期的相关性。

结果

与癌旁组织相比，CD103+CD39+CD8+ T细胞亚群在胃肿瘤组织中的比例明显增加（P<0.05）；免疫荧光染色进一步证实，胃肿瘤组织中CD103+CD39+CD8+ T 细胞亚群的数目亦明显多于癌旁组织；与CD103+CD39-和CD103-CD39-CD8+ T细胞亚群相比，CD103+CD39+CD8+ T细胞亚群表达的活化分子CD69和免疫检查点分子PD-1均增加（P<0.05），但功能相关因子IFN-γ的表达则显著下降（P<0.05）；体外TGF-β1刺激可诱导CD8+ T细胞中CD103与CD39的共表达上调（P<0.05）；此外，CD103+CD39+CD8+ T细胞亚群在晚期胃癌患者肿瘤组织中的浸润比例显著高于早期胃癌患者（P<0.05）。

结论

CD103+CD39+CD8+ T细胞亚群在胃肿瘤组织中的浸润增加，并展示出功能受抑的应答特征，从而有助于胃癌的免疫逃逸。

胃癌  /  CD8+ T细胞  /  CD103  /  CD39  /  免疫逃逸
Objective

To detect the infiltration level of CD103+CD39+CD8+ T cell subsets in gastric cancer tissues and analyze their response characteristics, clarifying the clinical relevance of this subset.

Methods

Surgical specimens (tumor tissues, adjacent tissues, and peripheral blood) were collected from gastric cancer patients at the Department of General Surgery, Second Affiliated Hospital of Army Medical University between January 2023 and May 2024. Flow cytometry and immunofluorescence staining quantified the proportion and number of CD103+CD39+CD8+ T cells in tumor versus adjacent tissues. Flow cytometry further analyzed CD69, PD-1, and IFN-γ expression in this subset. Peripheral blood mononuclear cells (PBMCs) were isolated and cultured in vitro to assess TGF-β1-induced differentiation. Correlation with disease stage was analyzed by detecting the infrltration level of CD103+CD39+CE8+ T Cell subsets via flow cytometry.

Results

Compared with adjacent tissues, gastric cancer tissues showed significantly increased proportions of CD103+CD39+CD8+ T cells (P<0.05); immunofluorescence confirmed higher numbers in tumor tissues. Relative to CD103+CD39- and CD103-CD39-CD8+ T subsets, CD103+CD39+CD8+ T cells exhibited elevated CD69 and PD-1 expression (P<0.05) but reduced IFN-γ (P<0.05). In vitro TGF-β1 stimulation upregulated co-expression of CD103 and CD39 in CD8+ T cells (P<0.05). Moreover, advanced gastric cancer patients had higher tumor infiltration of this subset than early-stage patients (P<0.05).

Conclusion

CD103+CD39+CD8+ T cell subsets display increased infiltration and functionally impaired responses in gastric cancer, facilitating tumor immune escape.

gastric cancer  /  CD8+ T cells  /  CD103  /  CD39  /  immune escape
黄梦秋, 钟杭, 邱远, 邹全明, 彭六生, 马代远. 胃肿瘤组织中浸润的免疫抑制性CD103+CD39+CD8+ T细胞亚群功能受损并促进肿瘤进展. 陆军军医大学学报, 2026 , 48 (4) : 445 -452 . DOI: 10.16016/j.2097-0927.202512028
Mengqiu HUANG, Hang ZHONG, Yuan QIU, Quanming ZOU, Liusheng PENG, Daiyuan MA. Functionally impaired CD103+CD39+CD8+ T cell subsets with immune-suppressive properties infiltrating gastric cancer tissues promote tumor progression[J]. Journal of Army Medical University, 2026 , 48 (4) : 445 -452 . DOI: 10.16016/j.2097-0927.202512028
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胃癌是具有高发病率和高病死率的消化道恶性肿瘤，全球有近50%的胃癌发生在我国，严重危害着人民的生命健康［1］。尽管早期胃癌可通过手术切除予以根治，但超过70%的患者就诊时已处于中晚期，使得手术切除效果有限，即使后续辅以药物进行治疗，胃癌患者的预后仍未得到明显改善［2-3］。近年来，以调控机体免疫细胞的功能，进而有效抵抗肿瘤发展的治疗手段取得了新突破［4-5］。因此，深入研究胃癌微环境中免疫细胞的应答调控机理，可为胃癌的临床治疗提供新的方向。
在机体介导抗肿瘤应答的免疫细胞中，CD8+ T细胞被公认为是抵抗肿瘤进展的关键细胞类型［6］。然而，尽管肿瘤微环境中CD8+ T细胞的浸润密度显著增加，但患者的疾病进展往往预示着CD8+ T细胞的浸润密度增高未能有效阻止肿瘤细胞的生长。研究发现，肿瘤浸润的CD8+ T细胞并非均为抗肿瘤活性的免疫细胞群体，而是通过表达不同的表面分子呈现出显著的异质性［7-8］。有文献报道，表达CD103分子的CD8+ T细胞是一类具有抗肿瘤效应的组织驻留记忆型T细胞亚群，而表达CD39分子的CD8+ T细胞却是一类抗肿瘤功能耗竭的T细胞亚群［9-10］。但是，共表达CD103和CD39分子的CD8+ T细胞却又被认为是一类具有肿瘤反应性的T细胞亚群［11］，这提示CD8+ T细胞中CD103和CD39分子的表达模式很可能是决定其抗肿瘤与否的关键。本课题组前期探索了胃癌患者肿瘤组织中的驻留记忆型CD8+ T细胞亚群的应答特征及其临床意义［12］，但是关于CD103+CD39+CD8+ T细胞亚群在胃肿瘤组织中的应答情况及其介导的免疫应答与疾病进展的关联性尚不清楚。因此，本研究拟通过收集胃癌患者的肿瘤组织与癌旁组织，探究CD103+CD39+CD8+ T细胞亚群在胃肿瘤组织中的浸润水平及其应答特征，并分析其与肿瘤进展的关系，以期为胃癌的免疫治疗提供新思路。
1　资料与方法
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1.1　一般资料
本研究经陆军军医大学第二附属医院伦理委员会批准（2022-研第096-01）。在遵循伦理学标准且患者知情同意的基础上，收集2023年1月至2024年5月在陆军军医大学第二附属医院普外科接受手术切除的胃癌患者的肿瘤组织、癌旁组织和外周血标本，纳入研究的患者共32例，男性20例，女性12例，年龄46~71岁，平均60.5岁。纳入标准：①无年龄和性别限制，经病理活检诊断为胃癌；②在术前均未经铂类等化疗药物或其他方法进行治疗。排除伴发有感染性疾病、自身免疫性疾病以及多发肿瘤疾病者。根据国际抗癌联盟第8版恶性肿瘤TNM分期标准［13］将入组的患者进行分组，其中Ⅰ~Ⅱ期10例，Ⅲ~Ⅳ期22例。
1.2　主要试剂与仪器
组织保存液与组织消化酶购自德国Miltenyi公司，DMEM培养基购自美国Hyclone公司，胎牛血清购自美国Gibco公司。采用流式细胞术进行检测时，所用的抗体包括：标记细胞活性的染料FVS700、APC-H7标记的鼠抗人CD3抗体、BV605标记的鼠抗人CD39抗体与淋巴细胞活化剂（美国BD公司），FITC标记的鼠抗人CD69抗体、FITC标记的鼠抗人IFN-γ抗体、APC标记的鼠抗人CD103抗体、PE标记的鼠抗人PD-1抗体、PerCP/Cy5.5标记的鼠抗人CD8抗体、PE-Cy7标记的鼠抗人CD45抗体（美国BioLegend公司）。细胞固定通透剂购自美国Invitrogen公司，人淋巴细胞分离管购自深圳达科为生物工程有限公司，纯化的鼠抗人CD3和CD28抗体购自美国BioLegend公司，重组人的TGF-β1购自美国Peprotech公司，0.01 mol/L的PBS购自中国博士德生物技术有限公司。纯化的鼠抗人CD8抗体购自武汉赛维尔生物科技有限公司，纯化的兔抗人CD103和CD39抗体购自美国Abcam公司，HRP标记的山羊抗鼠或山羊抗兔二抗以及iF440-Tyramide、iF555-Tyramide和iF647-Tyramide标记的酪胺购自武汉赛维尔生物科技有限公司。生物安全柜和HF240恒温培养箱购自上海力康生物医疗科技控股有限公司，200目细胞筛网购自上海碧云天生物技术有限公司，全自动组织分离器购自德国美天旎公司，台式高速离心机购自美国Beckman公司，流式细胞仪购自美国BD公司。
1.3　标本处理
手术切除的胃癌患者标本放入组织保存液中，利用冰盒运回实验室。取出组织，利用无菌PBS清洗后进行剪取，剪取的肿瘤组织与癌旁组织间距至少5 cm；随后肿瘤组织与癌旁组织分别分成2部分，一部分经4%多聚甲醛固定后进行苏木精-伊红染色（hematoxylin and eosin staining， HE）以区分肿瘤组织与癌旁组织；另一部分则继续剪成小片后转移至组织分离管中，并加入含有组织消化酶的DMEM培养基，将分离管倒置于全自动组织分离器上，设定组织处理程序后进行处理，取出分离管，放入37 ℃孵箱旋转消化1 h，经筛网过滤，滤液在室温下以500×g离心5 min，收集细胞沉淀，用PBS或DMEM培养基重悬沉淀成单细胞悬液备用。
1.4　流式细胞术检测
不同组织消化的单细胞悬液直接加入细胞活性的染料FVS700，室温孵育10 min后洗涤。加入不同荧光标记的鼠抗人抗体（CD45-PE-Cy7、CD3-APC-H7、CD8-PercP-Cy5.5、CD39-BV605、CD103-APC、PD-1-PE和CD69-FITC），放入4 ℃冰箱避光染色20 min，PBS洗涤，以室温、500×g离心5 min后，上机检测并采集数据；若检测细胞中的IFN-γ的表达水平，单细胞悬液需在96孔板中经淋巴细胞活化剂刺激6 h，再收集细胞，经PBS洗涤，加入不同荧光标记的鼠抗人抗体（CD45-PE-Cy7、CD3-APC-H7、CD8-PercP-Cy5.5、CD39-BV605、CD103-APC）染色，对细胞进行固定，并通透处理20 min，加入FITC标记的鼠抗人IFN-γ抗体在4 ℃冰箱避光孵育30 min，经PBS洗涤，在室温下以500×g离心5 min，上机检测并采集数据。
1.5　免疫荧光染色实验
石蜡包埋的组织块经组织切片后，按照以下顺序处理切片：二甲苯脱蜡、乙醇梯度水化、EDTA修复液进行抗原修复、3%双氧水去除内源性过氧化物酶、3%BSA封闭，加鼠抗人CD8抗体，4 ℃孵育过夜后加HRP标记的二抗，室温孵育1 h，加入iF555-Tyramide标记的酪胺，室温避光孵育10 min，采用TBST和抗体洗脱液进行洗涤；随后3%BSA封闭，加兔抗人CD39抗体，4 ℃孵育过夜后加HRP标记的二抗，室温孵育1 h，加入iF647-Tyramide标记的酪胺，室温避光孵育10 min，采用TBST和抗体洗脱液进行洗涤；随后3%BSA封闭，加兔抗人CD103抗体，4 ℃孵育过夜后加HRP标记的二抗，室温孵育1 h，加入iF440-Tyramide标记的酪胺，室温避光孵育10 min，TBST洗涤后滴加DAPI复染细胞核10 min，PBS洗涤后滴加自发荧光淬灭剂5 min，PBS清洗后采用抗荧光淬灭封片剂封片，用全信息组织切片扫描仪采集图片。
1.6　外周血单个核细胞的分离与培养
PBS以1∶1的体积比稀释胃癌患者的外周血，然后将其加入人淋巴细胞分离管中，以室温、800×g离心20 min，吸走部分血浆后直接将含有细胞的上层倒入新的离心管中，DMEM培养基洗涤后重悬，用细胞计数仪进行计数，调整细胞的浓度为2×106个/mL。取出已在37 ℃下经鼠抗人CD3和CD28抗体包被2 h的96孔板，吸弃包被液后，加入200 μL的细胞悬液，同时加入终浓度为50 ng/mL的重组人细胞因子TGF-β1，设置未包被鼠抗人CD3和CD28抗体且无TGF-β1刺激的细胞孔为对照组，预包被鼠抗人CD3和CD28抗体但无TGF-β1刺激的细胞孔为未刺激组，预包被鼠抗人CD3和CD28抗体且有TGF-β1刺激的细胞孔为TGF-β1刺激组，分别在培养后第1、3天收集细胞，采用流式细胞术检测CD8+ T细胞中共表达CD103和CD39的水平。
1.7　统计学分析
采用GraphPad Prism 8.0软件进行统计学分析，符合正态分布的数据采用x¯±s表示，两组之间比较采用独立样本t检验，多组之间的比较采用单因素方差分析后，再采用Tukey事后检验进行组间多重比较，P<0.05为差异具有统计学意义。
2　结果
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2.1　CD103+CD39+CD8+ T细胞亚群在肿瘤组织中的浸润水平增加
采用流式细胞术检测胃癌患者外周血和组织来源的单细胞悬液中CD8+ T细胞共表达CD103和CD39的水平，结果显示：与外周血相比，癌旁组织和肿瘤组织中CD103+CD39+CD8+ T 细胞亚群占CD8+ T细胞的比例显著增加 （P<0.001）；与癌旁组织相比，胃肿瘤组织中CD103+CD39+CD8+ T 细胞亚群占CD8+ T细胞的比例亦明显增加（P<0.05，图1）。免疫荧光染色进一步证实，胃肿瘤组织中CD103+CD39+CD8+ T 细胞亚群的数量亦明显多于癌旁组织（图2），提示CD103+CD39+CD8+ T 细胞亚群在肿瘤组织中的浸润水平增加。
2.2　肿瘤组织中CD103+CD39+CD8+ T细胞亚群的浸润水平与疾病进展成正相关
根据肿瘤组织中CD103+CD39+CD8+ T 细胞亚群的比例，比较分析其在早期患者（Ⅰ~Ⅱ期）和晚期患者（Ⅲ~Ⅳ期）中的差异。结果显示：与早期患者相比，晚期患者肿瘤组织中CD103+CD39+CD8+ T细胞亚群的比例显著增加（P<0.05，图3），提示肿瘤组织中CD103+CD39+CD8+ T细胞亚群的浸润水平与疾病进展成正相关。
2.3　CD103+CD39+CD8+ T细胞亚群中CD69和PD-1的表达增加但IFN-γ的表达下降
基于肿瘤组织中CD8+ T 细胞表达的CD103和CD39情况，将其分为CD103+CD39+CD8+、CD103+CD39- CD8+与CD103-CD39-CD8+ T 3个细胞亚群进行比较分析。结果显示：与CD103+CD39-CD8+和CD103-CD39- CD8+ T细胞相比，CD103+CD39+CD8+ T细胞亚群显著上调表面分子CD69和PD-1的表达（P<0.05，图4），而功能相关因子IFN-γ的表达水平则明显下降（P<0.05）；此外，CD103+CD39-CD8+ T细胞中CD69与PD-1的表达水平亦明显高于CD103-CD39-CD8+ T细胞（P<0.05），但其IFN-γ的表达水平则与CD103-CD39-CD8+ T细胞基本相当，差异无统计学意义（图4），提示肿瘤组织中CD103+CD39+CD8+ T细胞亚群呈现出激活的免疫抑制性表型与功能特征。
2.4　TGF-β1诱导CD8+ T细胞中CD103+CD39+亚群的分化增加
体外TGF-β1刺激培养显示：培养1 d时，对照组、未刺激组和TGF-β1刺激组中CD103+CD39+CD8+ T细胞亚群的比例均未出现明显改变；培养3 d时，未刺激组与TGF-β1刺激组中CD103+CD39+CD8+ T细胞亚群的比例均显著高于对照组（P<0.01）；同时，与培养3 d的未刺激组相比，培养3 d的TGF-β1刺激组中CD103+CD39+CD8+ T细胞亚群比例亦明显增加（P<0.05，图5），提示TGF-β1刺激可诱导CD8+ T细胞中CD103+CD39+亚群的分化增加。
3　讨论
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胃癌是严重威胁人类健康的消化道恶性肿瘤之一。尽管全球胃癌的发病率呈逐年下降的趋势，但我国胃癌的发病率却依然居高不下［14］。肿瘤的发生发展与机体免疫应答失调的密切关系已被公认，而T细胞——特别是CD8+ T细胞介导的抗肿瘤功能下降则是导致肿瘤进展的关键。近年来，随着研究人员对肿瘤微环境中CD8+ T细胞应答特征的深入探索，发现一群共表达CD103和CD39分子的CD8+ T细胞即CD103+CD39+CD8+ T细胞亚群在机体介导抗肿瘤免疫应答中十分关键［15］。然而，这群细胞在胃癌微环境中的浸润水平及其应答特征尚不明确。
3.1　探索CD103+CD39+ CD8+ T细胞亚群在肿瘤组织中的浸润变化具有重要意义
通过利用胃癌患者的临床标本，本研究发现，CD103+CD39+CD8+ T细胞亚群在肿瘤组织中的占比显著增加，这与前期关于这群细胞在胰腺肿瘤组织浸润增加的文献报道一致［16］。然而，随着疾病的进展，本研究亦发现这群细胞在晚期胃癌患者肿瘤组织中的占比明显高于早期胃癌患者，这提示肿瘤微环境很可能参与调控其在肿瘤组织中的浸润变化。有文献报道，肿瘤来源的调节性细胞因子TGF-β1不仅与疾病的进展密切相关，而且能够调节CD8+ T细胞的分化［17］。本研究发现，尽管T细胞受体的激活在一定程度上可促进CD103+CD39+CD8+ T细胞亚群的分化增加，但是在T细胞受体活化的同时加入TGF-β1刺激，却使CD103+CD39+CD8+ T细胞亚群的分化比例显著上调，提示在早期胃癌中，CD8+ T细胞很可能仅通过依赖肿瘤抗原的识别以上调CD103和CD39的共表达；但是随着胃癌进展至中晚期，由于肿瘤抗原的慢性刺激以及TGF-β1水平的增加，CD103+CD39+CD8+ T细胞亚群在肿瘤微环境中得以进一步分化。由于CD103+CD39+CD8+ T细胞亚群具有识别和杀伤肿瘤细胞的能力，理论上这群细胞在胃肿瘤组织中随疾病进展而增多预示着机体抵抗肿瘤的特异性CD8+ T细胞增加，进而很可能改善晚期胃癌患者的临床预后。但肿瘤组织中CD103+CD39+CD8+ T细胞亚群的应答水平与患者预后的确切关系还需进一步证实。
3.2　明确CD103+CD39+ CD8+ T细胞亚群在肿瘤组织中的表型与功能特征可提供潜在靶标
肿瘤微环境不仅调控了CD103+CD39+CD8+ T细胞亚群的应答分化，而且对其表型和功能特征进行了重塑［18-20］。本研究发现，在肿瘤组织中，CD103+CD39+CD8+ T细胞亚群表达的活化分子CD69和免疫检查点分子PD-1水平明显高于CD103+CD39-CD8+和CD103-CD39-CD8+ T细胞亚群，提示这群细胞虽然处于持续识别肿瘤抗原的活化状态，但是PD-1介导的免疫抑制信号很可能导致其杀伤肿瘤细胞的能力下降。而本研究后续对CD8+ T细胞不同亚群的IFN-γ水平检测则证实肿瘤组织中CD103+CD39+CD8+ T细胞亚群的抗肿瘤活性显著下降，由此导致胃癌细胞得以逃避这群细胞的识别与杀伤。因此，靶向干预PD-1信号很可能有助于提升CD103+CD39+CD8+ T细胞亚群的抗肿瘤效应功能，进而延长胃癌患者的生存时间。
由于胃癌患者临床样本收集存在一定的困难，本研究存在样本量较小的局限性。同时，本研究检测CD103+CD39+CD8+ T细胞亚群的功能受抑依赖于IFN-γ水平的下降，其它抗肿瘤细胞毒性分子如颗粒酶B以及穿孔素是否也发生改变未能明确。再次，胃癌微环境中CD103+CD39+CD8+ T细胞亚群功能变化的免疫学机制及其与患者预后的关系亦值得深入探索。
综上所述，本研究探究了一个新的CD103+CD39+CD8+ T细胞亚群在肿瘤组织中的应答特征，并分析临床相关性，发现其在胃癌患者肿瘤组织中的应答水平与疾病进展密切相关，这群细胞的抗肿瘤活性下降可能是导致胃癌免疫逃逸的重要因素。因此，后续研究将进一步增加胃癌患者的临床样本收集，深入探索CD103+CD39+CD8+ T细胞亚群的功能变化及其影响疾病进展的潜在机理，进而为开发胃癌的免疫治疗新策略提供理论支撑。

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2026年第48卷第4期
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doi: 10.16016/j.2097-0927.202512028
  • 接收时间：2025-12-04
  • 首发时间：2026-10-23
  • 出版时间：2026-02-28
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  • 收稿日期：2025-12-04
  • 修回日期：2026-01-11
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    1川北医学院附属医院肿瘤科，四川 南充
    2陆军军医大学（第三军医大学）第二附属医院普外科，重庆
    3陆军军医大学（第三军医大学）药学与检验医学系微生物与生化药学教研室，重庆

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马代远，E-mail：
彭六生，E-mail：
MA Daiyuan，E-mail：
PENG Liusheng，E-mail：
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2种不同金属材料的力学参数
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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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