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Article(id=1211268825715184401, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1211268819788632695, articleNumber=null, orderNo=null, doi=10.11855/j.issn.0577-7402.2021.01.12, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1597939200000, receivedDateStr=2020-08-21, revisedDate=1606233600000, revisedDateStr=2020-11-25, acceptedDate=null, acceptedDateStr=null, onlineDate=1766718592336, onlineDateStr=2025-12-26, pubDate=1611763200000, pubDateStr=2021-01-28, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1766718592336, onlineIssueDateStr=2025-12-26, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1766718592336, creator=13701087609, updateTime=1766718592336, updator=13701087609, issue=Issue{id=1211268819788632695, tenantId=1146029695717560320, journalId=1189873630562394117, year='2021', volume='46', issue='1', pageStart='1', pageEnd='100', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=0, createTime=1766718590924, creator=13701087609, updateTime=1766718828068, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1211269814484594852, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1211268819788632695, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1211269814484594853, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1211268819788632695, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=71, endPage=75, ext={EN=ArticleExt(id=1211268826105254693, articleId=1211268825715184401, tenantId=1146029695717560320, journalId=1189873630562394117, language=EN, title=Effect of type 2 innate lymphoid cells on T cells and its role in immunity diseases, columnId=1190243275882729994, journalTitle=Medical Journal of Chinese People’s Liberation Army, columnName=Review, runingTitle=null, highlight=null, articleAbstract=

Type Ⅱ innate lymphoid cell (ILC2), a newly discovered important type of inherent immune cells closely related to T lymphocytes, has a significant regulatory impact on T lymphocytes. Many studies have demonstrated that ILC2 can effectively induce the differentiation of CD4+ T cells to helper T cell (Th)2, thereby contributing to the modulation of host immune homeostasis. In the present paper, we would like to review the update of possible effects of ILC2 on Th2 differentiation and its role in immunity diseases.

, correspAuthors=Yong-Ming Yao, authorNote=null, correspAuthorsNote=
*E-mail:
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Ⅱ型固有淋巴细胞(ILC2)是新近发现的一种与T淋巴细胞密切相关的重要固有免疫细胞，对T淋巴细胞具有显著调控作用。大量研究证实，ILC2可有效诱导CD4+ T细胞向辅助性T细胞(Th)2亚型特异性分化，从而参与调节机体免疫平衡过程。该文就ILC2对于Th2特异性分化的影响及其在免疫性疾病中的作用进行综述。

, correspAuthors=姚咏明, authorNote=null, correspAuthorsNote=
姚咏明，E-mail：
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吴瑶，硕士研究生，主要从事战(创、烧)伤感染与免疫、脓毒症多器官功能障碍综合征发病机制及防治策略方面的研究。E-mail：

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吴瑶，硕士研究生，主要从事战(创、烧)伤感染与免疫、脓毒症多器官功能障碍综合征发病机制及防治策略方面的研究。E-mail：

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吴瑶，硕士研究生，主要从事战(创、烧)伤感染与免疫、脓毒症多器官功能障碍综合征发病机制及防治策略方面的研究。E-mail：

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IL. 白细胞介素；TSLP. 胸腺基质淋巴生成素；ILC2. Ⅱ型固有淋巴细胞；MHC-Ⅱ. 主要组织相容性复合体Ⅱ类抗原；ICOSL. 诱导共刺激分子配体；PD-1. 程序性死亡分子1；PD-L1. 程序性死亡分子配体1；TCR. T细胞受体；ICOS. 诱导共刺激分子；Areg. 双向调节蛋白

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Ⅱ型固有淋巴细胞对T细胞分化的影响及其在免疫性疾病中的作用
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吴瑶 1 , 蒋丽娜 2 , 祝筱梅 1 , 姚咏明 1, *
解放军医学杂志 | 综述 2021,46(1): 71-75
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解放军医学杂志 | 综述 2021, 46(1): 71-75
Ⅱ型固有淋巴细胞对T细胞分化的影响及其在免疫性疾病中的作用
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吴瑶1 , 蒋丽娜2, 祝筱梅1, 姚咏明1, *
作者信息
  • 1解放军总医院医学创新研究部，北京 100048
  • 2河北北方学院医学检验学院，河北 张家口 075000

    • 吴瑶，硕士研究生，主要从事战(创、烧)伤感染与免疫、脓毒症多器官功能障碍综合征发病机制及防治策略方面的研究。E-mail：

通讯作者:

姚咏明，E-mail：
Effect of type 2 innate lymphoid cells on T cells and its role in immunity diseases
Yao Wu1 , Li-Na Jiang2, Xiao-Mei Zhu1, Yong-Ming Yao1, *
Affiliations
  • 1Medical Innovation and Research Division, the Chinese PLA General Hospital, Beijing 100048, China
  • 2Medical Laboratory College of Hebei North University, Zhangjiakou, Hebei 075000, China
出版时间: 2021-01-28 doi: 10.11855/j.issn.0577-7402.2021.01.12
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摘要
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Ⅱ型固有淋巴细胞(ILC2)是新近发现的一种与T淋巴细胞密切相关的重要固有免疫细胞，对T淋巴细胞具有显著调控作用。大量研究证实，ILC2可有效诱导CD4+ T细胞向辅助性T细胞(Th)2亚型特异性分化，从而参与调节机体免疫平衡过程。该文就ILC2对于Th2特异性分化的影响及其在免疫性疾病中的作用进行综述。

Ⅱ型固有淋巴细胞  /  辅助性T细胞2  /  免疫反应

Type Ⅱ innate lymphoid cell (ILC2), a newly discovered important type of inherent immune cells closely related to T lymphocytes, has a significant regulatory impact on T lymphocytes. Many studies have demonstrated that ILC2 can effectively induce the differentiation of CD4+ T cells to helper T cell (Th)2, thereby contributing to the modulation of host immune homeostasis. In the present paper, we would like to review the update of possible effects of ILC2 on Th2 differentiation and its role in immunity diseases.

type 2 innate lymphoid cell  /  helper T cell 2  /  immune response
吴瑶, 蒋丽娜, 祝筱梅, 姚咏明. Ⅱ型固有淋巴细胞对T细胞分化的影响及其在免疫性疾病中的作用. 解放军医学杂志, 2021 , 46 (1) : 71 -75 . DOI: 10.11855/j.issn.0577-7402.2021.01.12
Yao Wu, Li-Na Jiang, Xiao-Mei Zhu, Yong-Ming Yao. Effect of type 2 innate lymphoid cells on T cells and its role in immunity diseases[J]. Medical Journal of Chinese People’s Liberation Army, 2021 , 46 (1) : 71 -75 . DOI: 10.11855/j.issn.0577-7402.2021.01.12
正文
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Ⅱ型固有淋巴细胞(type 2 innate lymphoid cell，ILC2)是近年来发现的固有淋巴细胞亚群，可持续参与机体固有免疫和适应性免疫反应过程，对免疫系统中多种细胞功能具有显著影响，其中对T淋巴细胞的调控作用尤为突出。ILC2可影响CD8+ T细胞、CD4+ T细胞甚至记忆性T细胞等不同类型的T淋巴细胞，且在功能特性上与辅助性T细胞(helper T cell，Th)2具有高度相似性，因此被界定为Th2细胞在固有免疫系统中的“镜像”细胞。有资料显示，ILC2与Th2不仅在转录因子表达和细胞因子分泌方面存在共同点，同时能够通过诱导Th2细胞亚群的特异性分化或与其产生协同作用来参与机体的Th2型免疫反应，甚至成为抗寄生虫免疫反应和过敏性疾病的重要环节[1]。ILC2主要通过自身抗原呈递作用以及分泌2型细胞因子等途径直接或间接调节T淋巴细胞的功能，最终诱导机体Th2型免疫应答。
1 ILC2对Th2细胞分化的直接诱导作用
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ILC2是体内重要的固有免疫细胞，不仅可在接受外界抗原刺激信号数小时内迅速作出防御反应，还能够发挥抗原呈递作用，将刺激信号向T、B淋巴细胞进一步传递。尤其是在对T淋巴细胞的调控过程中，ILC2通过高表达主要组织相容性复合体Ⅱ类抗原(major histocompatibility complex class Ⅱantigen，MHC-Ⅱ)及协同刺激分子，将信号传递给CD4+ T细胞，有效刺激Th2细胞亚群的活化，在启动机体Th2型免疫应答中发挥重要作用[2-3](图1)。协同刺激因素包括OX40-OX40L、可诱导共刺激分子(inducible costimulator，ICOS)及其配体(ICOSL)、CD40-CD154等。作为T淋巴细胞的第二刺激信号，上述因素与MHC-Ⅱ类分子具有协同效应，参与诱导Th2细胞的分化[1,4]。例如，在过敏性炎症小鼠模型中，经白细胞介素(interleukin，IL)-33激活后，ILC2通过其所表达的共刺激分子与幼稚T细胞表面相应配体结合，并在幼稚CD4+ T细胞上发生相互作用并产生信号，进一步刺激转录因子GATA结合蛋白3(GATA binding protein 3，GATA3)活化，促进Th2细胞甚至调节性T细胞(regulatory T cell，Treg)增多[5]。其中，存在于多种免疫细胞的OX40L仅表达于激活的ILC2，其他免疫细胞甚至树突细胞(dendritic cell，DC)则未见表达。活化的ILC所表达的OX40L在与T细胞共刺激受体Tnfrsf4(OX40)相互作用下，参与Th2细胞甚至Treg细胞反应，引起组织中Th2和Treg细胞增多。反之，当ILC2中OX40L缺失时(Il7raCre/+Tnfsf4fl/fl小鼠)，上述效应则消失。由此可见，OX40L-OX40的结合为Th2细胞的存活和增殖提供了重要信号，可通过T细胞受体诱导并表达于Th2细胞，是Th2高效反应的重要途径之一[6]。
在ILC2表达的MHC-Ⅱ作用下，T淋巴细胞可通过产生细胞因子IL-2和IL-4与ILC2相应受体结合，进而实现ILC2对于自身功能的活化，从而维持细胞的增殖能力及细胞因子的产生和释放。基于上述调控机制，MHC-Ⅱ显著增强了ILC2细胞的功能及其诱生Th2类细胞因子的作用，使ILC2与T淋巴细胞之间形成了反馈作用[7-8]。在体外实验中，ILC2与幼稚CD4+ T细胞共培养可增强细胞增殖活性和细胞因子的分泌[9]。同样，ILC2所表达的MHC-Ⅱ类分子在IL-2和IL-4作用下能够有效维持ILC2的功能状态。由此可见，MHC-Ⅱ和共刺激分子途径可能是ILC2参与机体Th2型免疫反应的重要路径，而ILC2与T淋巴细胞的相互作用则进一步促进了ILC2自身的增殖活性以及Th2型细胞因子的产生。
2 ILC2对Th2细胞的间接调节效应
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在启动机体Th2型免疫反应的过程中，细胞因子是ILC2调控T淋巴细胞的另一重要途径。ILC2在激活状态下可迅速分泌大量Th2型细胞因子，并通过这些细胞因子发挥免疫防御效应。同时，细胞因子还可影响其他免疫细胞的功能，间接诱导Th2细胞分化以及启动机体的Th2型免疫反应(图1)。
既往研究发现，存在于肠道黏膜中的ILC2在IL-33的刺激作用下，可分泌产生IL-4、IL-5、IL-9、IL-13等Th2型细胞因子，并在这些细胞因子的诱导下，启动Th2型免疫反应。由ILC2介导的体内Th2型免疫反应在促进寄生虫虫体排出和防止其传播方面具有重要意义[10-11]。来源于ILC2的细胞因子IL-9和IL-13有助于及时有效地驱除巴西日圆线虫等。上述细胞因子通过促进替代性活化巨噬细胞以及抑制蠕虫感染所致炎症反应，发挥机体抗寄生虫免疫保护作用[12-13]。
在过敏性免疫反应状态下，ILC2可影响Th2细胞的功能，甚至可通过调控DC功能间接作用于T淋巴细胞，诱导其向Th2亚群特异性分化，最终启动Th2型免疫应答[14]。当ILC2受到过敏原及其信号刺激后，可分泌IL-13、IL-4、IL-5、IL-9等细胞因子，与肥大细胞和嗜酸性粒细胞相互作用，造成气道的高敏状态。同时，IL-13可调节DC的免疫功能，促进Th2细胞的分化，参与机体Th2型免疫反应以及记忆性Th2细胞反应。在气道过敏性炎症反应小鼠模型中，在IL-33的刺激作用下，ILC2可迅速分泌大量的IL-13；而IL-13在与DC表面的特异性受体IL-13受体及IL-4受体结合后，可对DC的功能进行调节，诱导幼稚CD4+ T细胞向Th2细胞分化，参与Th2型免疫应答过程。进一步观察发现，IL-13主要通过调节前列腺素E2受体相关信号通路，促进CCR7+ DC的迁移，使外周组织中DC在遭遇抗原后向引流淋巴结聚集；而成熟活化的DC将抗原呈递给CD4+ T细胞，诱导其向Th2细胞亚群特异性分化；相反，在ILC2缺乏状态下，则会因为IL-13水平不足，影响DC向淋巴结的迁移，致使Th2型免疫反应随之受损；当ILC2被过继转移至ILC2特异性缺乏的Rorasg/sg BMT小鼠体内后，小鼠Th2细胞受损状态可得到明显的改善[14]。此外，在由木瓜蛋白酶反复刺激所致的记忆性Th2细胞反应过程中，活化的ILC2可通过IL-13诱导肺组织CD11b+ CD103– DC趋化因子CCL17表达上调，促进CCR4+记忆性Th2细胞向过敏原暴露部位募集[15]。因此，当致敏ICOS-T动物中ILC2被清除后，ILC2缺乏致使动物肺组织中记忆性Th2细胞数量明显减少，而重新给予过敏原处理后，细胞因子IL-13及记忆性Th2细胞趋化因子均可在活化的ILC2中迅速表达[15]。由此可见，ILC2是机体Th2细胞功能效应的有效补充，以IL-13间接调控为主的Th2细胞分化路径则是一种不依赖于IL-4经典途径的全新作用途径。这一作用途径在启动由适应性Th2细胞免疫介导的过敏性气道炎症反应中具有显著的病理生理意义。
3 其他免疫调节分子及其信号转导机制
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业已明确，程序性死亡分子配体1(programmed death ligand 1，PD-L1)是具有负向免疫调节作用的B7家族成员之一[16]，可选择性表达于小鼠T淋巴细胞、B淋巴细胞、DC、巨噬细胞、间充质干细胞，并在抑制细胞活化或诱导免疫耐受方面发挥重要作用[17]。程序性死亡分子1(programmed death 1，PD-1)则是CD28家族中的一种重要免疫抑制分子，主要表达于活化的成熟T淋巴细胞。尽管PD-1、PD-L1可通过不同信号通路来传递抑制性信号，减少机体抗原特异性T淋巴细胞的增殖，或通过对T淋巴细胞活性的影响诱导免疫耐受。存在于T淋巴细胞表面的PD-1也能够通过与PD-L1或PD-L2配体结合而发挥抑制作用。其中，PD-1与PD-L1在激活的T淋巴细胞表面结合后，甚至可启动T淋巴细胞的程序性死亡。而表达于DC和巨噬细胞等机体固有免疫细胞的PD-L2，则主要与Th2型免疫反应相关[18]。
新近研究表明，作为机体重要的负向免疫调控细胞，ILC2与PD-L1、PD-1等抑制性免疫分子具有明显的相关性。例如，在巴西圆线虫等蠕虫感染期间，PD-L1特异性表达于IL-2或IL-33活化后的ILC2，并通过与CD4+ T细胞的PD-1受体相互作用，促进炎症条件下Th2细胞的分化并增强其免疫功能[19]。表达于ILC2上的PD-L1参与Th2细胞的功能调节，在诱导和维持Th2型免疫反应中发挥重要作用。另据报道，作为受体表达于T淋巴细胞的抑制性分子PD-1，除存在于小鼠骨髓ILC祖细胞外[20]，在肺部炎症组织ILC2上的表达也明显上调[21]。PD-1在ILC向其他亚群分化的过程中表达逐渐减弱，并特异性表达于ILC2，对该细胞亚群的发育和功能产生影响。因此，PD-1缺乏的ILC2，即使是在IL-33持续作用下，其细胞因子分泌仍然明显减少。而体内试验中，ILC2表面PD-1表达的缺失不仅影响IL-5和IL-13的产生和有效维持，甚至可能引起糖皮质激素诱导的肿瘤坏死因子受体(glucocorticoid-induced TNF receptor，GITR)、ICOS等重要刺激分子的表达改变[22]。有研究发现，在粉尘引起的过敏性反应小鼠中，PD-1缺乏可造成过敏反应加重以及病程恶化[23]，表明ILC2可能是导致Th2型细胞因子产生减少和CD4+ T细胞反应受损的重要因素。
在寄生虫感染性疾病的相关研究中发现，ILC2的PD-1表达能力与其组织来源有关，且可因IL-33的刺激而增强；相反，ILC2的细胞因子产生能力会减弱[24]。因此，在寄生虫感染过程中，IL-33激活肠道黏膜上皮ILC2，可分泌Th2型细胞因子并上调KLRG1。但当表达于KLRG1+ ILC2上的PD-1作为信号转导及转录激活因子(signal transducer and activator of transcription，STAT)5依赖的负向调控分子[25]与PD-L1结合后，可特异性下调信号转导因子STAT5的活性，形成PD-1对KLRG1+ ILC2亚群的负向调控[26]，进而影响KLRG1+ ILC2亚群的细胞增殖和细胞因子分泌，阻断其在驱除蠕虫过程的重要作用。因此，在抗寄生虫感染的过程中，阻断PD-1可能造成机体向2型免疫反应方向发展，从而增强机体的抗寄生虫免疫反应。
也有研究发现，在以PD-1为靶点的抗PD-1抗体治疗肿瘤过程中，由PD-1所介导的ILC功能通常会被阻断[27]，并且这一现象也同时存在于胰腺导管腺癌(PDAC)的PD-1+肿瘤ILC2和PD-1+T细胞[28]。而ILC2在IL-33的活化作用下，不仅可形成局部组织浸润，同时还能够通过激活组织特异性抗肿瘤免疫反应来抑制肿瘤生长[28]。因此，将活化的肿瘤ILC2确定为抗PD-1免疫疗法的靶标，被认为可有效增强组织特异性的抗癌免疫反应和抗PD-1免疫疗法的功效。
另有资料提示，DC表达的PD-L2参与介导Th2型免疫反应过程[29]，而ILC2在促进Th2型免疫反应及记忆性Th2细胞反应中发挥着重要的调控效应，因此对于ILC2和DC与PD-1/PD-L2之间是否存在关联，尚待进一步深入探究。
4 总结与展望
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ILC2在促进T淋巴细胞向Th2细胞亚群特异性分化以及启动机体Th2型免疫应答方面发挥着重要作用，可通过多条途径调控T淋巴细胞的免疫状态，甚至诱导其向Th2细胞等具有抑制效应的亚群分化。这对于诱导机体免疫耐受和通过改善免疫紊乱状态来维持免疫平衡具有重要意义。虽然目前已初步明确了ILC2在气道过敏性炎症反应和抗寄生虫感染等病理生理过程中的免疫调控效应，但该细胞亚群的确切作用机制和临床意义尚有待澄清，且ILC2自身也具有明显的异质性。现阶段研究主要集中在黏膜组织相关性疾病方面，对于ILC2在机体其他组织器官中的潜在作用及其调节途径值得进一步深入探讨。
基金
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  • 国家自然科学基金(81730057)
  • 国家重点基础研究发展计划(2017YFC1103302)
文献
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2021年第46卷第1期
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doi: 10.11855/j.issn.0577-7402.2021.01.12
  • 接收时间：2020-08-21
  • 首发时间：2025-12-26
  • 出版时间：2021-01-28
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  • 收稿日期：2020-08-21
  • 修回日期：2020-11-25
基金
National Natural Science Foundation of China(81730057)
国家自然科学基金(81730057)
National Key Research and Development Plan(2017YFC1103302)
国家重点基础研究发展计划(2017YFC1103302)
作者信息
    1解放军总医院医学创新研究部，北京 100048
    2河北北方学院医学检验学院，河北 张家口 075000

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鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
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