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Article(id=1208106711106293779, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1208106710208717234, articleNumber=null, orderNo=null, doi=10.11855/j.issn.0577-7402.2022.04.0402, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1619539200000, receivedDateStr=2021-04-28, revisedDate=null, revisedDateStr=null, acceptedDate=1626796800000, acceptedDateStr=2021-07-21, onlineDate=1765964685465, onlineDateStr=2025-12-17, pubDate=1651075200000, pubDateStr=2022-04-28, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1765964685465, onlineIssueDateStr=2025-12-17, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1765964685465, creator=13701087609, updateTime=1765964685465, updator=13701087609, issue=Issue{id=1208106710208717234, tenantId=1146029695717560320, journalId=1189873630562394117, year='2022', volume='47', issue='4', pageStart='321', pageEnd='426', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1765964685250, creator=13701087609, updateTime=1765964685250, updator=13701087609, preIssue=null, nextIssue=null, ext=null, issueFiles=null}, startPage=402, endPage=406, ext={EN=ArticleExt(id=1208106711391506453, articleId=1208106711106293779, tenantId=1146029695717560320, journalId=1189873630562394117, language=EN, title=Research progress on pathological mechanism of celiac disease, columnId=1190243275882729994, journalTitle=Medical Journal of Chinese People’s Liberation Army, columnName=Review, runingTitle=null, highlight=null, articleAbstract=

The pathological mechanism of celiac disease is not completely clear, and environmental factors may trigger the occurrence of intestinal inflammatory response in genetic susceptible individuals. Recent researches indicated that, due to the coordinated action of multiple factors such as abnormal intestinal mucosal barrier function and intestinal microbial changes, the homeostasis of intestinal environment is imbalanced, which aggravates the severity of the disease. Gluten-free diet combined with probiotics and other drugs would regulate intestinal microbiota and be conducive to resume intestinal mucosal barrier function,thereafter effectively alleviate the clinical symptoms of patients. However, both the composition of intestinal flora and its role in pathogenesis of the disease needs further consideration. To explore the pathological mechanism of celiac disease and targeted treatment for those factors will become a new perspective for precise prevention and treatment of celiac disease.

, correspAuthors=Jing Wu, authorNote=null, correspAuthorsNote=
*E-mail:
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乳糜泻(CD)的病理机制尚不完全明确，可能由环境因素触发遗传易感个体肠道内的炎症反应所致。近年研究表明，CD患者肠道黏膜屏障功能异常及肠道微生物改变等多因素的协同作用，可导致肠道内环境稳态失衡，进而加重疾病严重程度。去麦胶饮食配合益生菌等药物的治疗，能调节肠道微生物群，有利于肠道黏膜屏障功能的修复，可有效缓解CD患者的临床症状。但是肠道菌群的组成及其是否为CD诱因的证据尚待进一步考量。深入探究CD的病理机制，针对病理因素进行靶向治疗，是预防及精准诊疗CD的新方向。本文从遗传及环境因素等方面着手，对CD的病理机制进行综述。

, correspAuthors=吴静, authorNote=null, correspAuthorsNote=
吴静，E-mail：
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刘可心，硕士研究生，主要从事中医内科脾胃疾病的相关研究

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刘可心，硕士研究生，主要从事中医内科脾胃疾病的相关研究

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乳糜泻病理机制研究进展
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刘可心 1 , 吴星星 1 , 王卯 2 , 陈雪莲 1 , 吴琪 1 , 吴静 3, *
解放军医学杂志 | 综述 2022,47(4): 402-406
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解放军医学杂志 | 综述 2022, 47(4): 402-406
乳糜泻病理机制研究进展
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刘可心1, 吴星星1, 王卯2, 陈雪莲1, 吴琪1, 吴静3, *
作者信息
  • 1南京中医药大学第一临床医学院，南京 210046
  • 2南京中医药大学附属医院伦理委员会，南京 210029
  • 3南京大学医学院附属鼓楼医院/南京大学中医研究院/南京中医药大学鼓楼临床医学院，南京 210008

    • 刘可心，硕士研究生，主要从事中医内科脾胃疾病的相关研究

通讯作者:

吴静，E-mail：
Research progress on pathological mechanism of celiac disease
Ke-Xin Liu1, Xing-Xing Wu1, Mao Wang2, Xue-Lian Chen1, Qi Wu1, Jing Wu3, *
Affiliations
  • 1The First Clinical Medical College of Nanjing University of Chinese Medicine, Nanjing 210046, China
  • 2Department of Ethics Committee, the Affiliated Hospital of Nanjing University of Chinese Medicine, Nanjing 210029, China
  • 3The Affiliated Drum Tower Hospital of Nanjing University Medical College/Institutes of Chinese Medicine, Nanjing University/Drum Tower Clinical Medical College of Nanjing University of Chinese Medicine, Nanjing 210008, China
出版时间: 2022-04-28 doi: 10.11855/j.issn.0577-7402.2022.04.0402
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摘要
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乳糜泻(CD)的病理机制尚不完全明确，可能由环境因素触发遗传易感个体肠道内的炎症反应所致。近年研究表明，CD患者肠道黏膜屏障功能异常及肠道微生物改变等多因素的协同作用，可导致肠道内环境稳态失衡，进而加重疾病严重程度。去麦胶饮食配合益生菌等药物的治疗，能调节肠道微生物群，有利于肠道黏膜屏障功能的修复，可有效缓解CD患者的临床症状。但是肠道菌群的组成及其是否为CD诱因的证据尚待进一步考量。深入探究CD的病理机制，针对病理因素进行靶向治疗，是预防及精准诊疗CD的新方向。本文从遗传及环境因素等方面着手，对CD的病理机制进行综述。

乳糜泻  /  病理机制  /  遗传因素  /  环境因素  /  肠道稳态

The pathological mechanism of celiac disease is not completely clear, and environmental factors may trigger the occurrence of intestinal inflammatory response in genetic susceptible individuals. Recent researches indicated that, due to the coordinated action of multiple factors such as abnormal intestinal mucosal barrier function and intestinal microbial changes, the homeostasis of intestinal environment is imbalanced, which aggravates the severity of the disease. Gluten-free diet combined with probiotics and other drugs would regulate intestinal microbiota and be conducive to resume intestinal mucosal barrier function,thereafter effectively alleviate the clinical symptoms of patients. However, both the composition of intestinal flora and its role in pathogenesis of the disease needs further consideration. To explore the pathological mechanism of celiac disease and targeted treatment for those factors will become a new perspective for precise prevention and treatment of celiac disease.

celiac disease  /  pathogenesis  /  genetic factors  /  environmental factors  /  intestinal homeostasis
刘可心, 吴星星, 王卯, 陈雪莲, 吴琪, 吴静. 乳糜泻病理机制研究进展. 解放军医学杂志, 2022 , 47 (4) : 402 -406 . DOI: 10.11855/j.issn.0577-7402.2022.04.0402
Ke-Xin Liu, Xing-Xing Wu, Mao Wang, Xue-Lian Chen, Qi Wu, Jing Wu. Research progress on pathological mechanism of celiac disease[J]. Medical Journal of Chinese People’s Liberation Army, 2022 , 47 (4) : 402 -406 . DOI: 10.11855/j.issn.0577-7402.2022.04.0402
正文
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乳糜泻(celiac disease，CD)又称麦胶敏感性肠病、非热带性脂肪泻，是一种免疫介导的胃肠疾病，由对麦胶产生的固有免疫及适应性免疫反应所致[1]。CD患者小肠黏膜的绒毛萎缩、扁平，导致小肠吸收不良[2]，去麦胶饮食(gluten-free diet，GFD)能使其症状得以缓解、小肠黏膜恢复正常及抗麦胶抗体(anti-gliadin antibody，AGA)消失，然而再次进食含有麦胶的食物又可迅速复发。因此，当CD患者进食含麦胶类食物时，在有高度遗传易感基因人群的小肠中将引起炎症反应。有研究发现，全球范围内CD的发病率为1%[3]，在北美、北欧及澳大利亚，CD的发病率较高，拉丁美洲的发病率与欧洲相近[4]，CD遗传易感基因频率较低及麦胶消耗量较低的国家和地区(如日本、亚撒哈拉地区等)发病率则较低。由于CD的临床表现各异，在未进行血清学筛查的情况下，一些CD病例可能未被发现[5]。在过去20年中，CD发病率显著增高，一方面可能是由于使用了更敏感的诊断工具，另一方面是因为筛查率的提高使更多患有CD的高风险个体被检出。尽管如此，目前仍有很多病例未被诊断[6]。提高对CD临床表现的认识有助于临床诊断，而深化对CD发病机制的认识则有助于进一步理解CD表现的多样性。本文从CD的发病机制入手，以遗传因素、环境因素为主，介绍CD在病理机制方面的最新研究进展，以期提高医务工作者对CD的认识，推动CD的早期预防与诊治。
1 CD的遗传因素
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目前公认CD是典型的多基因遗传易感性疾病，主要组织相容性复合物(major histocompatibility complexes，MHC)与CD密切相关[7]。人类白细胞抗原(human leukocyte antigen，HLA)-Ⅰ类基因及HLA-Ⅱ类基因位于MHC的第6对染色体上，这些基因编码糖蛋白，与多肽类物质相结合，形成HLA-多肽复合物，被小肠黏膜中的特异性T细胞所识别。其中存在HLA-DQ2或HLA-DQ8基因型的个体具有CD遗传易感倾向[8]。一项针对北欧人群的研究表明，95%的CD患者为HLA-DQ2基因型，其余则为HLA-DQ8基因型的携带者[3]。Ting等[9]的研究表明，在DQ2的多个同型异构体中，DQ2.5发生CD的风险最高。然而，也有小于1%的CD患者同时缺乏DQ2及DQ8基因[3]。因HLA的分型检测有较高的阴性预测价值，若没有HLA-DQ2/DQ8型基因，则可以排除可疑病例存在CD的可能性[3]。对于CD易感患者，麸质在体内不能彻底分解，其降解产物可与抗组织转谷氨酰胺酶抗体(anti-tissue transglutaminase antibody，tTGA)形成复合物，被HLA-DQ2/HLA-DQ8呈递给免疫细胞，产生抗tTGA及抗AGA抗体，进而引发一系列炎症反应[10]。HLA-DQ8及CD4+ T细胞在细胞毒性T细胞介导的肠上皮细胞(intestinal epithelial cells，IECs)溶解中起关键性作用[7]。另外，γ-干扰素(Interferon-γ，IFN-γ)及转谷氨酰胺酶2(transglutaminase 2，TG2)对肠组织的破坏也起着重要作用，TG2在存在HLA-DQ2或HLA-DQ8分子的情况下，可增强抗麦胶T细胞反应，而HLA-DQ8可促进并放大IFN-γ下游通路[7]。同时，含有TG2的特异性B细胞可通过其表面抗TG2-Ig分子摄取麦胶-TG2复合物后，经由HLA-DQ分子将麦胶多肽呈递给麦胶反应T细胞[11]。由此可以解释为何上述抗体只在表现为HLA-DQ2/DQ8基因型且食用麦胶的个体中形成[11]。然而，TG2作为CD的自身抗原仍存在争议。虽然体外细胞破裂或坏死将从细胞中释放TG2，但是在疾病状态下，TG2是否仍存在于细胞内尚不明确[12]。TG2在肠道中不具有活性，可能是由病毒信号激活INF-γ诱导其发挥作用。但是，对于TG2在病理生理环境中被激活的原因，仍有待进一步研究[11]。
2 CD的环境因素
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2.1 麦胶
麦胶是目前公认的CD环境因素，CD的另一个名称“麦胶敏感性肠病”(gluten sensitive enteropathy，GSE)即由此得名。麦胶是多种谷物(如小麦、大麦、黑麦等)中的主要蛋白质成分，可被管腔内及刷状缘上的酶类分解成氨基酸及多肽[8]，其中麦醇溶蛋白是麦胶的醇溶部分且含有大量的有毒成分[13]，未消化的醇溶蛋白分子可能在肠道感染或肠道通透性增加时通过肠上皮屏障与固有层的抗原递呈细胞(antigen presenting cell，APC)相互作用[13]。其中，麦胶的非免疫显性肽段及免疫显性肽段在CD的病理机制中均具有重要作用[14]。
2.1.1 非免疫显性肽段
如α-麦醇溶蛋白31-43肽段(P31-43)，主要通过固有免疫反应引起上皮改变。P31-43肽段可通过上调MHC来激活分裂原活化蛋白(mitogen activated protein，MAP)激酶，不仅使肠道细胞形态以及肌动蛋白细胞骨架发生改变，还可诱导体内体外的肌动蛋白重组[15]。刺激角质细胞生长因子(keratinocyte growth factor，KGF)可诱发麦醇溶蛋白产生破坏性影响的条件，促使白细胞介素(interleukin，IL)-15的表达上调[5]，激活上皮内淋巴细胞(intraepithelial lymphocyte，IEL)表达活化NK-G2D受体[13]，从而对具有MHC-Ⅰ类分子的肠道细胞产生细胞毒作用，进而杀死肠道细胞。IL-15还可损伤CD的Treg细胞功能[16]。然而，由于麦胶中富含谷氨酸及脯氨酸，人体胃肠道内的转谷氨酰胺酶及脯氨酸肽酶缺乏，导致麦胶不能完全消化而产生免疫原性肽。在固有免疫介导下，肠道细胞凋亡后向细胞内释放组织转谷氨酰胺酶(tissue transglutaminase，tTG)，使麦醇溶蛋白被部分脱酰胺[17-18]。脱酰胺的麦醇溶蛋白被DQ2+/DQ8+相关的APC识别，随后被递呈给辅助性T细胞[18]。同时，辅助性T细胞可触发B细胞的活化与成熟[19]，产生针对tTG的IgM、IgG、IgA抗体，使其成为具有免疫源性的分子，从而影响适应性免疫反应。
2.1.2 免疫显性肽段
免疫显性肽段如33-mer肽段主要通过适应性免疫引起肠道固有层发生改变。在固有层中，CD4+ T细胞可激活适应性免疫反应，麦胶不完全降解生成33-mer，刺激T细胞的反应。因肽段中富含谷氨酰胺，经tTG脱酰胺生成带负电荷的谷氨酸，增加了与树突状细胞表面DQ2/DQ8的亲和力，通过CD4+ T细胞诱导适应性免疫反应，释放大量促炎性细胞因子，如INF-γ、INF-α，增加肠道通透性，并协同细胞毒性T细胞引发肠病[20]。同时，33-mer肽段会促使B细胞的增殖分化，生成AGA、抗肌内膜抗体(EMA)及tTGA等抗体[21]。由于受损的肠细胞在其顶侧可表达CD71转运蛋白，导致分泌型IgA-麦醇溶蛋白复合物通过逆转胞吞作用，增强麦胶从管腔向固有层的运输[5]。最终，肠道固有层中的CD4+ T细胞与麦醇溶蛋白之间的相互作用诱导其活化及增殖，并通过基质细胞产生促炎性细胞因子、金属蛋白酶及KGF，诱发隐窝增生，并且在IECs死亡后继发绒毛变钝[5]。
虽然麦胶摄入会增加患CD风险这一观点已被广泛接受，但目前还没有研究能完全解释并非所有携带遗传易感倾向HLA-DQ2/DQ8基因的个体在食用麦胶后均发生CD这一疑问[22]，尚需进一步研究证实。
2.2 肠道内环境
2.2.1 肠道黏膜屏障
肠上皮是由单细胞层组成，是肠道针对外部环境最重要的保护屏障。在生理状态时，IECs在绝大多数情况下不会渗透麦胶或麦醇溶蛋白。但在病理状态时，CD患者的肠道黏膜中肠上皮紧密连接的完整性被破坏，其细胞旁(上皮细胞间隙)通透性增加，这将会促使麦醇溶蛋白可以跨越肠道屏障，进而激活肠道内的免疫系统，加重肠上皮屏障功能障碍。同时，肠道通透性在CD的发展过程中也起着重要作用，且肠道通透性的增加可能发生于CD之前[23]。IECs以其完整的细胞间连接发挥屏障作用，在生理情况下，少量抗原碎片可以通过小肠防御屏障经两种途径被吸收[23-25]。在大多数(>90%)可被吸收的蛋白质中，一种途径是经跨细胞膜途径通过小肠黏膜屏障后被溶酶体降解，使蛋白质转化为非免疫原性多肽[24]；另一种途径是通过细胞间紧密连接的吸收，可诱导抗原耐受。若细胞间紧密连接系统的完整性受损，宿主对环境中抗原成分(如麦胶)的免疫应答就会持续进展[25]。因此，在CD的病理生理机制中，部分消化的麦醇溶蛋白片段与位于上皮顶侧的趋化因子受体3相互作用，诱导髓样分化因子88(myeloid differentiation factor 88，MyD88)释放连蛋白(zonulin)[5,22]，促使肠通透性增加，使肠道黏膜免疫功能受到破坏，导致非自身抗原通过细胞旁通道由管腔向固有层移位，进而与免疫系统相互作用[26]。麦醇溶蛋白肽也将触发IL-15、KGF及IL-8的释放，可在固有层中大量募集嗜中性粒细胞[5]。同时，致病菌、病毒及小麦中的非麦胶蛋白成分(如淀粉酶-胰蛋白酶抑制剂)，也可能诱导树突状细胞成熟及促进炎性细胞因子的产生，调节CD4+ T细胞反应[27]。以上因素将导致肠道屏障功能破坏，微生物抗原及内毒素从管腔转移至固有层，从而引发促炎的微环境[28]，造成肠道稳态失衡，进而加重肠道损伤及炎症反应。如果此过程持续进行，便会诱发机体内适应性免疫反应应答，加剧促炎因子的释放，使细胞旁通路被激活，形成恶性循环，最终导致CD患者肠道内炎症的持续进展[28]。
2.2.2 肠道微生物
肠道内环境中的微生物群越来越受到重视[29]。人体内富含多种微生物群，而细菌是最主要的微生物群，其数量远远超过人体细胞总量，微生物数量与人体细胞数量的比例是1.3:1[30]。有研究指出，肠道微生物群在某种程度上影响了CD的发病与进展[31]。Caminero等[32]的研究表明，肠道微生物群之间的不平衡也会影响CD的发病，其中主要的肠道内细菌可能在麦胶水解过程中发挥至关重要的作用。大多数研究强调，CD的肠道微生态失调主要表现为革兰阴性杆菌及拟杆菌增加，双歧杆菌及乳酸杆菌减少。由于肠道微生物群可能参与调节细胞因子环境，不利的微生物群会增强CD患者对麦醇溶蛋白的免疫反应，而应用益生菌则可能会减少促炎细胞因子的产生。因此，肠道菌群失调可能是CD发病机制中的另一个重要环境因素。虽然人体内的消化蛋白酶对麦胶蛋白的作用已为人所熟知，但是肠道微生物群在蛋白代谢中的作用却常常被低估[32]。有报道指出，麦胶-微生物及宿主-微生物的相互作用会驱动麦胶介导的免疫反应的发生与变化[33]。在长期严格的GFD过程中，人体内的微生物群可能发生改变，而这一改变可能具有潜在的致病性，将促使胃肠道症状持续存在[34]。因而，对于伴有严重并发症及难治性的CD患者，仅单一使用GFD治疗效果并不理想[35]。虽然GFD对微生物群调节的研究数据有时存在矛盾[36]，但目前已有足够的证据证实，将GFD与益生菌联合应用可改变肠道微生物群的组成，进而缓解CD患者的胃肠道症状，同时其不仅能下调参与CD发病的细胞因子，还可改善肠道黏膜炎症反应的严重程度。越来越多的证据支持肠道微生物群的组成及功能变化与包括CD在内的多种慢性炎症性疾病可能相关[37]。Xu等[38]研究发现，使用双向孟德尔随机化方法有助于阐述肠道微生物与复杂疾病的关系。有研究通过全基因组相关性分析，发现了遗传变异与肠道微生物的相关性[39]。但目前对肠道微生物的组成及其与CD的因果关系尚无定论。
2.3 其他环境因素
2.3.1 母乳喂养与维生素D摄入
在大多数研究中，母乳喂养被认为可能是保护婴儿免于罹患CD的有利环境因素之一[40]。母乳中的麦胶特异性IgA抗体及免疫系统调节剂可诱导耐受，母乳喂养也可减少麦胶及牛奶的摄入，调整婴儿的肠道微生态。然而，对于维生素D的应用则说法不一。近期有报道指出，有CD遗传易感倾向的个体，补充维生素D可能会增加患CD的风险[41]，然而，Mårild等[42]的研究则发现，母亲孕期或新生儿维生素D水平与儿童期罹患CD的风险无关。但因该研究的样本量有限，且混杂了日照时间等因素，故维生素D是否作为独立因素影响CD，目前尚无定论。
2.3.2 高脂饮食与TCR-γδ
CD肠上皮淋巴细胞中T细胞受体(T cell receptor，TCR)-γδ的比例增高[43]。斯堪的纳维亚高脂饮食对CD具有平衡保护作用，有作者推测其可能是通过TCR尤其是TCR-γδ识别脂质而作用的[44]。当人体摄取高脂饮食后，体内的TCR-γδ会对已消化的脂质做出反应。处于活动期的CD患者空肠上皮内淋巴细胞的TCR-γδ表达量增多，而TCR-γδ水平升高可能体现了其对CD患者的免疫保护作用[44]。但是TCR-γδ发挥作用的分子机制不清楚，尚待进一步研究。
2.3.3 病原体感染
对于CD患者的反复胃肠道感染，有研究认为轮状病毒感染可能是增加婴儿罹患CD的风险之一[8]。研究发现，在接触病原体特别是对胃肠道有影响的病原体(如呼肠孤病毒)后，可能通过抑制外周Treg细胞的转化促进CD自身免疫反应的发生，但该研究发现，伯氏疏螺旋体感染与CD不存在因果关系[45]。
3 总结与展望
收起
近年来CD越来越受到关注，国内外大量研究指出，CD的病理机制以麦胶为主要诱发因素，协调多种因素共同起作用，包括遗传因素、肠道微生态、肠黏膜屏障、病原体感染、喂养方式等。假使相关环节出现异常，必然会促使肠道内出现炎症级联反应，进而加重疾病的严重程度。目前CD特定微生物群的特征尚未明确，并且针对各病理因素本身的致病性与各因素间的关联研究还不充分。因此，未来需进一步深化对CD病理机制的认识，探讨CD的一级预防措施，以实现针对CD的精准医疗。
基金
收起
  • 国家自然科学基金面上项目(81873160)
  • 2021 Jiangsu Postgraduate Science and Innovation Program(KYCX21_1661)
文献
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doi: 10.11855/j.issn.0577-7402.2022.04.0402
  • 接收时间：2021-04-28
  • 首发时间：2025-12-17
  • 出版时间：2022-04-28
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  • 收稿日期：2021-04-28
  • 录用日期：2021-07-21
基金
National Natural Science Foundation of China(81873160)
国家自然科学基金面上项目(81873160)
2021 Jiangsu Postgraduate Science and Innovation Program(KYCX21_1661)
作者信息
    1南京中医药大学第一临床医学院，南京 210046
    2南京中医药大学附属医院伦理委员会，南京 210029
    3南京大学医学院附属鼓楼医院/南京大学中医研究院/南京中医药大学鼓楼临床医学院，南京 210008

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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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