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Article(id=1208154042614792575, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1208154038609228128, articleNumber=null, orderNo=null, doi=10.11855/j.issn.0577-7402.2022.02.0197, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1616688000000, receivedDateStr=2021-03-26, revisedDate=null, revisedDateStr=null, acceptedDate=1629820800000, acceptedDateStr=2021-08-25, onlineDate=1765975970175, onlineDateStr=2025-12-17, pubDate=1645977600000, pubDateStr=2022-02-28, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1765975970175, onlineIssueDateStr=2025-12-17, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1765975970175, creator=13701087609, updateTime=1765975970175, updator=13701087609, issue=Issue{id=1208154038609228128, tenantId=1146029695717560320, journalId=1189873630562394117, year='2022', volume='47', issue='2', pageStart='107', pageEnd='212', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=0, createTime=1765975969218, creator=13701087609, updateTime=1765976148463, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1208154790459192257, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1208154038609228128, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1208154790459192258, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1208154038609228128, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=197, endPage=202, ext={EN=ArticleExt(id=1208154043793392043, articleId=1208154042614792575, tenantId=1146029695717560320, journalId=1189873630562394117, language=EN, title=Research progress on the BCG-induced trained immunity: mechanism and role, columnId=1190243275882729994, journalTitle=Medical Journal of Chinese People’s Liberation Army, columnName=Review, runingTitle=null, highlight=null, articleAbstract=

The purpose of Bacillus Calmette-Guérin (BCG) vaccination is to prevent Mycobacterium tuberculosis infection, but studies have shown that BCG activates innate immunity, causes epigenetic reprogramming and metabolic changes of myeloid cells, and forms innate immune memory or trained immunity. When bone marrow-like cells are stimulated by pathogens again, they show enhanced immune response and promote the host's nonspecific defense ability. Innate immune memory is also called training immunity. In recent years, BCG-induced innate immune memory has attracted much attention, and it will guide the design of novel vaccine. This article reviews the application of BCG in prevention and treatment of corone virus disease 2019, the non-specific protection and mechanism of BCG-mediated trained immunity.

, correspAuthors=Bing-Dong Zhu, authorNote=null, correspAuthorsNote=
*E-mail:
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卡介苗(BCG)接种的目的是预防结核分枝杆菌感染，但研究发现BCG可以激活天然免疫，引起髓样细胞表观遗传重编程和代谢改变，形成天然免疫记忆。当髓系细胞再次受到病原体刺激后，诱导产生更强的天然免疫反应，增强了宿主的非特异性防御能力。天然免疫记忆又称为训练免疫，BCG诱导训练免疫的研究近年来受到重视，对于疫苗设计有一定的借鉴意义。本文对BCG介导训练免疫的机制、BCG诱导的非特异性免疫作用，以及BCG在新冠肺炎防治中的应用进行综述。

, correspAuthors=祝秉东, authorNote=null, correspAuthorsNote=
祝秉东，E-mail：
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何朴，硕士研究生，主要从事结核亚单位疫苗的制备及机制研究

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何朴，硕士研究生，主要从事结核亚单位疫苗的制备及机制研究

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何朴，硕士研究生，主要从事结核亚单位疫苗的制备及机制研究

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Cell, 2020, 183(2): 315-323.e9., articleTitle=Activate: randomized clinical trial of BCG vaccination against infection in the elderly, refAbstract=null), Reference(id=1208154053670978369, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1208154042614792575, doi=null, pmid=null, pmcid=null, year=2019, volume=105, issue=2, pageStart=329, pageEnd=338, url=null, language=null, rfNumber=[48], rfOrder=50, authorNames=Dominguez-Andres J, Netea MG, journalName=J Leukoc Biol, refType=null, unstructuredReference=Dominguez-Andres J, Netea MG. Long-term reprogramming of the innate immune system[J]. 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PAMP. 病原体相关分子模式

, figureFileSmall=Yri6Ve/K5dloxooZSURpFg==, figureFileBig=Nuc0d/qTc03faqcY/A/OSQ==, tableContent=null), ArticleFig(id=1208154047937364627, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1208154042614792575, language=EN, label=Tab.1, caption=

Protective effect of BCG against partial virus infection (Adapted from Moorlag et al.[36])

, figureFileSmall=null, figureFileBig=null, tableContent=
研究对象病毒研究类型卡介苗的作用
人类黄热病病毒随机对照试验白细胞介素-1β产生相关的病毒血症减少
人乳头瘤病毒随机对照试验，案例分析改善疣清除率
甲型流感病毒随机对照试验增强抗体产生
单纯疱疹病毒案例分析减少临床单纯疱疹病毒感染发作
动物单纯疱疹病毒1型CD-1小鼠提高生存率
单纯疱疹病毒2型CD-1小鼠提高生存率并防止感染
甲型流感病毒C57BL/6小鼠，CD-1小鼠降低甲型流感病毒的病毒滴度，减少炎症，提高生存率
乙型肝炎病毒C57BL/6小鼠增加抗体产生
日本脑炎病毒BALB/c小鼠减缓症状出现并提高生存率
), ArticleFig(id=1208154048063193750, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1208154042614792575, language=CN, label=表1, caption=

BCG对部分病毒感染的防护作用(改编自Moorlag等[36])

, figureFileSmall=null, figureFileBig=null, tableContent=
研究对象病毒研究类型卡介苗的作用
人类黄热病病毒随机对照试验白细胞介素-1β产生相关的病毒血症减少
人乳头瘤病毒随机对照试验，案例分析改善疣清除率
甲型流感病毒随机对照试验增强抗体产生
单纯疱疹病毒案例分析减少临床单纯疱疹病毒感染发作
动物单纯疱疹病毒1型CD-1小鼠提高生存率
单纯疱疹病毒2型CD-1小鼠提高生存率并防止感染
甲型流感病毒C57BL/6小鼠，CD-1小鼠降低甲型流感病毒的病毒滴度，减少炎症，提高生存率
乙型肝炎病毒C57BL/6小鼠增加抗体产生
日本脑炎病毒BALB/c小鼠减缓症状出现并提高生存率
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卡介苗介导的训练免疫机制与作用
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何朴 , 谭继英 , 李菲 , 牛红霞 , 祝秉东 *
解放军医学杂志 | 综述 2022,47(2): 197-202
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解放军医学杂志 | 综述 2022, 47(2): 197-202
卡介苗介导的训练免疫机制与作用
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何朴, 谭继英, 李菲, 牛红霞, 祝秉东*
作者信息
  • 兰州大学基础医学院病原生物研究所，兰州 730000

    • 何朴，硕士研究生，主要从事结核亚单位疫苗的制备及机制研究

通讯作者:

祝秉东，E-mail：
Research progress on the BCG-induced trained immunity: mechanism and role
Pu He, Ji-Ying Tan, Fei Li, Hong-Xia Niu, Bing-Dong Zhu*
Affiliations
  • Institute of Pathogen Biology, School of Basic Medical Sciences, Lanzhou University, Lanzhou 730000, China
出版时间: 2022-02-28 doi: 10.11855/j.issn.0577-7402.2022.02.0197
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摘要
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卡介苗(BCG)接种的目的是预防结核分枝杆菌感染，但研究发现BCG可以激活天然免疫，引起髓样细胞表观遗传重编程和代谢改变，形成天然免疫记忆。当髓系细胞再次受到病原体刺激后，诱导产生更强的天然免疫反应，增强了宿主的非特异性防御能力。天然免疫记忆又称为训练免疫，BCG诱导训练免疫的研究近年来受到重视，对于疫苗设计有一定的借鉴意义。本文对BCG介导训练免疫的机制、BCG诱导的非特异性免疫作用，以及BCG在新冠肺炎防治中的应用进行综述。

卡介苗  /  训练免疫  /  天然免疫记忆  /  表观遗传重编程

The purpose of Bacillus Calmette-Guérin (BCG) vaccination is to prevent Mycobacterium tuberculosis infection, but studies have shown that BCG activates innate immunity, causes epigenetic reprogramming and metabolic changes of myeloid cells, and forms innate immune memory or trained immunity. When bone marrow-like cells are stimulated by pathogens again, they show enhanced immune response and promote the host's nonspecific defense ability. Innate immune memory is also called training immunity. In recent years, BCG-induced innate immune memory has attracted much attention, and it will guide the design of novel vaccine. This article reviews the application of BCG in prevention and treatment of corone virus disease 2019, the non-specific protection and mechanism of BCG-mediated trained immunity.

Bacillus Calmette-Guérin  /  trained immunity  /  innate immune memory  /  epigenetic reprogramming
何朴, 谭继英, 李菲, 牛红霞, 祝秉东. 卡介苗介导的训练免疫机制与作用. 解放军医学杂志, 2022 , 47 (2) : 197 -202 . DOI: 10.11855/j.issn.0577-7402.2022.02.0197
Pu He, Ji-Ying Tan, Fei Li, Hong-Xia Niu, Bing-Dong Zhu. Research progress on the BCG-induced trained immunity: mechanism and role[J]. Medical Journal of Chinese People’s Liberation Army, 2022 , 47 (2) : 197 -202 . DOI: 10.11855/j.issn.0577-7402.2022.02.0197
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卡介苗(Bacillus Calmette-Guérin，BCG)是牛分枝杆菌(Mycobacterium bovis，M. bovis)经过连续13年230代体外传代培养后获得的减毒活疫苗[1]。新生儿接种BCG可以预防婴幼儿结核病，尤其是可以预防严重的粟粒性结核及结核性脑膜炎。此外，BCG还可以激活天然免疫，提供非特异性保护作用。
天然免疫也具有“记忆”能力。人们首先在缺乏适应性免疫系统的植物及无脊椎动物中观察到，机体被病原体初次感染或受病原相关模式(pathogen associated molecular patterns，PAMP)分子刺激后，激活天然免疫应答，在病原体二次感染时产生更强的免疫反应，增强对宿主的免疫保护能力。近期在哺乳动物中也发现，不同病原体感染后会产生异源性保护作用[2]。天然免疫系统经病原体刺激后，对二次感染产生更强的免疫应答反应的过程称为“训练免疫”或“天然免疫记忆”[3-4]。BCG等病原体感染可以诱导天然免疫系统产生免疫记忆，对其他病原体的再次感染具有抵抗作用。本文对BCG介导的天然免疫记忆及其产生机制进行综述。
1 BCG介导训练免疫的机制
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机体参与天然免疫记忆效应的细胞主要有巨噬细胞、单核细胞、自然杀伤(NK)细胞及固有淋巴样细胞(innate lymphoid cells，ILC)[5]。天然免疫细胞受到病原体或其他因素刺激时，由静止状态被激活[6]。该表型转变受到特定基因转录、翻译及翻译后修饰等多层次的调控，而基因转录又受DNA甲基化及组蛋白修饰的影响[7-8]。BCG可促进骨髓造血细胞向单核巨噬细胞分化，并通过组蛋白修饰等方式促使特定基因染色质打开，调控相关基因的表达，使以单核巨噬细胞为主的髓系细胞增多[9-10]。BCG的接种方式也对训练免疫效果具有较大影响。静脉接种及黏膜免疫比常规的皮内免疫递送更有效，且能诱导更强的训练免疫[11]。
1.1 BCG促进骨髓造血细胞向髓系分化
训练免疫多为髓系细胞介导。BCG静脉接种可促进造血干细胞向髓系细胞分化，使巨噬细胞及中性粒细胞增多。Kaufmann等[9]发现，BCG刺激骨髓可以促进短期造血干细胞及多能祖细胞群体扩大，同时调控造血干细胞向髓系细胞分化的转录因子Cebpe、Cebpa、Batf2及IRF8表达上调，导致髓系细胞生成增加。Cirovic等[10]发现，人类健康志愿者皮下注射BCG疫苗后，髓系细胞分化的转录因子干扰素调节因子4(IRF4)等表达上调，从而促进髓系细胞的分化。本课题组前期研究也发现应用BCG免疫或结核分枝杆菌抗原ESAT-6等刺激可促进造血干细胞及祖细胞转录因子Batf2、IRF8的表达上调[12]。
1.2 BCG诱导表观遗传学重编程
首先，在接种BCG后，人单核细胞会发生特异性染色质重编程，编码促炎细胞因子的基因表达增加，促进训练免疫的形成[13-14]。BCG接种引起的表观遗传学修饰主要包括上调组蛋白3第4位赖氨酸三甲基化(H3K4me3)、上调组蛋白3第27位赖氨酸乙酰化(H3K27ac)、下调组蛋白3第9位赖氨酸三甲基化(H3K9me3)。H3K4me3及H3K27ac可上调促炎细胞因子白细胞介素(IL)-1β、IL-6及肿瘤坏死因子(TNF)-α基因的转录，从而诱导天然免疫的产生。而H3K9me3可阻遏基因转录，因此H3K9me3下调会促进炎性细胞因子的表达，介导训练免疫。Kleinnijenhuis等[15]研究发现，接种BCG 3个月后，外周血CD14+单核细胞的IL-1β、TNF-α及TLR4基因启动子处H3K4me3显著增加，促进了IL-1β、TNF-α及TLR4的基因转录。2014年一项在乌干达开展的随机双盲对照试验结果显示，接种BCG的婴儿外周血IL-1β等促炎性细胞因子启动子处H3K4me3增加，H3K9me3减少，促炎性细胞因子表达增高[16]。接种BCG后单核细胞促炎性细胞因子的H3K27ac显著升高，促进了促炎性细胞因子的表达，使机体的抗病毒能力增强，能减轻黄热病病毒疫苗引起的病毒血症[16]。BCG免疫促使髓系细胞活化后，即便初次感染消除，这些稳定的表观修饰(即甲基化或乙酰化)仍然保留。由于这些固有免疫细胞基因处于打开状态，能够对再次刺激做出更强烈的反应(图1)[17]，因此，BCG介导的训练免疫可以维持较长时间。
其次，BCG接种可激活髓系细胞核因子-κB(NF-κB)、激活蛋白-1(activator protein-1，AP-1)及转录激活子(signal transducer and activator of transcription，STAT)等转录因子。激活的转录因子与促炎或抗炎基因的增强子及启动子结合，从而促进或抑制细胞因子的分泌[18]。BCG刺激中性粒细胞诱导JAK-STAT信号传导分子活化，同时使促炎性细胞因子的基因启动子H3K4me3增加，染色体打开，天然免疫激活，增强了中性粒细胞对白色念珠菌的杀伤作用[19]。
最后，组蛋白表观遗传修饰受相关酶活性及长链非编码RNA(lncRNAs)的调节。赖氨酸特异性甲基转移酶(KMT)及脱甲基酶(KDM)介导的组蛋白甲基化修饰可调节细胞因子基因的转录[20-21]。端粒沉默-1-样蛋白(Dot1L)是H3K79的甲基转移酶，它可以选择性地结合IL-6及IFNB1启动子，并促进H3K79甲基化。Dot1L沉默会造成H3K79甲基化减少，从而减少巨噬细胞分泌的IL-6及IL-1β[22]。在单核细胞的训练免疫反应过程中，lncRNAs通过三维拓扑结构与天然免疫相关基因结合，从而将伴侣蛋白甲基转移酶复合物(WD repeat domain 5-mixed lineage leukemia1，WDR5-MLL1)引导至靶基因启动子处，促进H3K4me3募集到靶基因启动子处[23]，从而发挥调节作用。
1.3 代谢改变与表观遗传重编程的相互作用
1.3.1 糖酵解与表观遗传重编程
BCG诱导的单核细胞糖酵解速率加快与Akt/mTOR途径有关。BCG可以诱导Akt及mTOR磷酸化增加，使用mTOR抑制剂雷帕霉素处理后，BCG介导的以细胞因子增加为主的训练免疫减弱或消失。研究发现，BCG主要通过上调mTOR及4种谷氨酸代谢必需酶(HK2、PFKP、GLS、GLUD)启动子处H3K4me3，以及下调上述基因启动子处H3K9me3，使mTOR糖酵解及谷氨酰胺代谢4种必需酶的mRNA表达上调，从而增强单核细胞的糖酵解反应。同时，雷帕霉素还可以逆转BCG介导的单核细胞TNF-α及IL-6启动子处的表观遗传学改变，使上调表达的H3K4me3减少，下调表达的H3K9me3增加，表明代谢与表观遗传重编程相关[24]。
1.3.2 BCG通过糖酵解调控巨噬细胞的极化
M1型巨噬细胞以糖酵解和乳酸代谢为主，而M2型巨噬细胞则更多地依赖氧化磷酸化和脂质代谢。对训练免疫的细胞进行代谢表征研究发现，经BCG诱导的单核细胞和巨噬细胞会转变为M1型，再次刺激时糖酵解增加，乳酸生成增多。使用糖酵解抑制剂(如雷帕霉素)后，基因启动子处的表观遗传学变化消失[25]。进一步研究发现，抑制糖酵解和谷氨酰胺代谢可导致琥珀酸积累，使BCG的训练免疫作用减弱[26]。
1.3.3 代谢中间体影响表观遗传修饰相关酶活性
代谢中间体可以充当染色质修饰酶的底物、辅因子或抑制剂[27]。糖酵解增强可导致三羧酸循环底物延胡索酸积累，后者可通过调控Akt/mTOR信号通路下游的转录因子低氧诱导因子1α(hypoxia inducible factor 1α，HIF-1α)上调糖酵解基因的表达及IL-1β的产生[28]。此外，糖酵解中间产物可调节表观遗传学修饰。延胡索酸可抑制组蛋白去甲基化酶及去乙酰化酶的活性[29]。单核细胞组蛋白乙酰化需要代谢途径的中间体乙酰辅酶A[30]。
2 BCG诱导的非特异性免疫作用
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BCG接种会激活外周单核细胞及NK细胞等天然免疫细胞，促进炎性细胞因子表达，对其他病原体感染产生非特异性保护[31-32]。
2.1 抗微生物感染的非特异性保护作用
BCG接种可引起机体产生以细胞因子为主的体液及细胞免疫应答，介导机体产生针对细菌、病毒及寄生虫的非特异性防护。在印度尼西亚及日本开展的针对BCG接种人群的保护试验结果表明，接种BCG的老年人群急性上呼吸道感染及肺炎的发病率均有不同程度的下降。新生儿接种BCG可降低出生后第一年的死亡率[16,33-34]。BCG免疫后，肺泡吞噬细胞(alveolar phagocyte，APs)表面高表达T细胞免疫球蛋白及黏蛋白域蛋白4(T cell immunoglobulin domain and mucin domain 4，TIM4)，吞噬杀伤作用增强。用致死剂量的甲型流感病毒攻击BCG免疫小鼠，所有小鼠均能获得保护[35]。给C57BL/6小鼠鼻内接种BCG后，能促进IL-1β的产生，降低黄热病病毒疫苗引起的病毒血症发生率[16](表1)。以上研究提示，接种BCG后，机体对其他细菌及病毒感染也能产生非特异性保护。多项动物实验结果表明，接种BCG能增强机体抗寄生虫感染的能力，对小耳巴贝虫、伯氏疟原虫、弓形虫及克氏锥虫等产生保护性免疫[37]。
2.2 抗肿瘤的非特异性免疫
BCG对于膀胱癌、黑色素瘤等肿瘤具有抑制及治疗作用，目前仍被列为Ⅲ期黑色素瘤的治疗药物[38]。BCG能活化天然免疫，有助于激活肿瘤特异性CD4+及CD8+ T淋巴细胞，诱导产生细胞因子IL-1及IL-2，形成Th1型细胞免疫应答，介导抗肿瘤作用[38]。膀胱灌注BCG可以激活膀胱上皮细胞及抗原递呈细胞，分泌细胞因子及趋化因子，募集中性粒细胞及巨噬细胞，进而吞噬并杀伤肿瘤细胞[39]。将BCG直接注射到黑色素瘤病灶中，可通过激活TLR2、TLR4、TLR8及TLR9，分泌TNF-α、γ干扰素(IFN-γ)及IL-12p40等细胞因子，活化巨噬细胞、树突状细胞及NK细胞，杀伤黑色素瘤等肿瘤细胞[40]，病灶消退率高达65%[41]。
3 BCG在新冠肺炎防治中的应用
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2019年末，由严重急性呼吸系统综合征冠状病毒2型(SARS-CoV-2)引起的新型冠状病毒肺炎(COVID-19)在全球流行并传播。面对COVID-19的大暴发，迫切需要提高人群的免疫反应，BCG通过表观遗传学诱导训练免疫可能具有潜在的保护作用。
2021年，一项来自全球160多个国家及地区的Meta分析结果显示，BCG接种覆盖率超过70%，BCG接种与COVID-19感染减少有关[42]。在很多国家，BCG作为预防结核分枝杆菌感染的疫苗被强制接种。目前已经确认，在实施BCG接种计划的国家，每百万人群中COVID-19的感染及死亡人数均低于未实施BCG疫苗接种计划的国家。2020年，纽约理工学院开展的一项研究发现，在没有普及BCG接种政策的国家，COVID-19感染的严重程度是其他国家的10倍，病死率也很高[43]。在欧洲COVID-19大流行的第1个月，BCG指数与COVID-19病死率之间存在显著的线性相关，BCG指数每增加10%，COVID-19病死率降低10.4%[44]。当然，BCG对COVID-19保护效果的评价受多方面因素的影响，造成不同研究结果间存在较大差异。这些因素包括人口及遗传结构的差异、采取的非药物干预措施的差异(如隔离或社交距离)、COVID-19诊断的差异以及所处流行阶段的不同等[45]。以上多项研究结果均提示BCG接种对COVID-19具有保护作用。然而，BCG接种引起的免疫保护持续时间，何时接种BCG，BCG早期接种比二次接种是否具有更好的保护效果依然是亟待解决的问题，需要更多的机制研究来揭示BCG介导的训练免疫与COVID-19防护的关系。
老年人群是SARS-CoV-2感染引起严重症状的主要群体。衰老造成老年人天然免疫系统防御功能降低，而且老年人适应性免疫系统产生缺陷，缺乏B细胞、CD4+ T细胞及CD8+ T细胞，因此，老年人难以抵抗SARS-CoV-2感染[46]。有研究表明，老年人接种BCG也可形成良好的训练免疫[47]，可能有助于降低SARS-CoV-2感染率及病死率，但尚缺乏确切证据。
综上所述，较多相关研究间接支持了BCG的保护作用，但结论多偏于假设，还需要进一步的详细研究来确认。
4 总结与展望
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经BCG诱导，机体的天然免疫细胞可通过表观遗传及代谢重编程诱导模式识别受体表达，促进促炎性细胞因子分泌，提供非特异性保护。训练免疫导致天然免疫细胞发生长期变化，从而使宿主对再次刺激产生强大的免疫反应。训练免疫早于淋巴细胞介导的抗原特异性免疫记忆，构成机体防御的免疫防线[48]。目前对于BCG诱导的训练免疫机制仍不够明确。蛋白质组学、代谢组学、转录组学及表观基因组学的发展将使人们能够揭示训练免疫的潜在新特征。BCG介导训练免疫的研究为疫苗设计提供了新思路。BCG诱导天然免疫的能力及其对特异性免疫保护作用的影响值得深入研究。
基金
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  • 国家自然科学基金(82001675)
  • 国家“十三五”科技重大专项(2018ZX10302302-002-003)
  • 甘肃省科技计划项目(20YF8FA072)
文献
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2022年第47卷第2期
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文章信息
doi: 10.11855/j.issn.0577-7402.2022.02.0197
  • 接收时间：2021-03-26
  • 首发时间：2025-12-17
  • 出版时间：2022-02-28
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  • 收稿日期：2021-03-26
  • 录用日期：2021-08-25
基金
National Natural Science Foundation of China(82001675)
国家自然科学基金(82001675)
Major Project of "Thirteenth Five-Year" Scientific and Technological Research Projects(2018ZX10302302-002-003)
国家“十三五”科技重大专项(2018ZX10302302-002-003)
Science and Technology Projects of Gansu Province(20YF8FA072)
甘肃省科技计划项目(20YF8FA072)
作者信息
    兰州大学基础医学院病原生物研究所，兰州 730000

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祝秉东，E-mail：
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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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