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Article(id=1199337305774321787, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1199337298941804946, articleNumber=null, orderNo=null, doi=10.11855/j.issn.0577-7402.0460.2023.0719, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1680019200000, receivedDateStr=2023-03-29, revisedDate=null, revisedDateStr=null, acceptedDate=1682265600000, acceptedDateStr=2023-04-24, onlineDate=1763873896305, onlineDateStr=2025-11-23, pubDate=1706371200000, pubDateStr=2024-01-28, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1763873896305, onlineIssueDateStr=2025-11-23, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1763873896305, creator=13701087609, updateTime=1763873896305, updator=13701087609, issue=Issue{id=1199337298941804946, tenantId=1146029695717560320, journalId=1189873630562394117, year='2024', volume='49', issue='1', pageStart='1', pageEnd='120', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=0, createTime=1763873894677, creator=13701087609, updateTime=1763874094669, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1199338137823572576, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1199337298941804946, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1199338137823572577, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1199337298941804946, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=108, endPage=114, ext={EN=ArticleExt(id=1199337306067923083, articleId=1199337305774321787, tenantId=1146029695717560320, journalId=1189873630562394117, language=EN, title=Research progress on the mechanism of metachronous gastric cancer after endoscopic submucosal dissection and Helicobacter pylori eradication in early gastric cancer, columnId=1190243275882729994, journalTitle=Medical Journal of Chinese People’s Liberation Army, columnName=Review, runingTitle=null, highlight=null, articleAbstract=

Helicobacter pylori (HP) infection is a Class Ⅰ carcinogen in gastric cancer, closely related to the occurrence of gastric cancer. Many studies have shown that HP eradication has a preventive effect on gastric cancer. However, 2.7%-6.1% of patients with early gastric cancer who have been eradicated after endoscopic submucosal dissection (ESD) can still develop metachronous gastric cancer (MGC), and the mechanism of its occurrence is still unclear. In this review, the atrophy of gastric mucosa and intestinal metaplasia cannot be completely reversed after HP eradication, the excessive proliferation of gastric mucosa epithelial cells, the accumulation of genetic abnormalities, the homeostasis imbalance of the epigenetic group, changes in immune microenvironment, the abnormality of stem cells in gastric mucosa, chromatin accessibility, and changes in chromosome remodeling were discussed in the mechanism of carcinogenesis caused by the above molecular changes after ESD and HP eradication in early gastric cancer.

, correspAuthors=Dong-Feng Chen, authorNote=null, correspAuthorsNote=
E-mail:
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幽门螺杆菌(HP)感染是胃癌的Ⅰ类致癌因子，与胃癌的发生密切相关。众多研究表明根除HP对胃癌有预防作用，但早期胃癌行内镜下黏膜剥离术(ESD)后根除HP仍有2.7%~6.1%的患者可发生异时性胃癌(MGC)，其发生机制尚不清楚。本文从HP根除后胃黏膜萎缩及肠化生不能完全逆转、胃黏膜上皮细胞过度增殖及遗传异常累积、表观组稳态失衡、免疫微环境变化、胃黏膜干细胞异常、染色质可及性、染色体重塑改变等角度，阐述早期胃癌行ESD及HP根除后上述分子改变导致癌变的机制。

, correspAuthors=陈东风, authorNote=null, correspAuthorsNote=
陈东风，E-mail：
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胡馨月，硕士研究生，主要从事慢性肝病与胃癌方面的相关研究

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胡馨月，硕士研究生，主要从事慢性肝病与胃癌方面的相关研究

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胡馨月，硕士研究生，主要从事慢性肝病与胃癌方面的相关研究

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早期胃癌内镜下黏膜剥离术及幽门螺杆菌根除后异时性胃癌的发生机制研究进展
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胡馨月 , 王斌 , 王涛 , 刘凯军 , 文良志 , 陈东风 *
解放军医学杂志 | 综述 2024,49(1): 108-114
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解放军医学杂志 | 综述 2024, 49(1): 108-114
早期胃癌内镜下黏膜剥离术及幽门螺杆菌根除后异时性胃癌的发生机制研究进展
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胡馨月, 王斌, 王涛, 刘凯军, 文良志, 陈东风*
作者信息
  • 陆军军医大学陆军特色医学中心消化内科，重庆 400042

    • 胡馨月，硕士研究生，主要从事慢性肝病与胃癌方面的相关研究

通讯作者:

陈东风，E-mail：
Research progress on the mechanism of metachronous gastric cancer after endoscopic submucosal dissection and Helicobacter pylori eradication in early gastric cancer
Xin-Yue Hu, Bin Wang, Tao Wang, Kai-Jun Liu, Liang-Zhi Wen, Dong-Feng Chen*
Affiliations
  • Department of Gastroenterology, Army Medical Center, Army Medical University, Chongqing 400042, China
出版时间: 2024-01-28 doi: 10.11855/j.issn.0577-7402.0460.2023.0719
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摘要
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幽门螺杆菌(HP)感染是胃癌的Ⅰ类致癌因子，与胃癌的发生密切相关。众多研究表明根除HP对胃癌有预防作用，但早期胃癌行内镜下黏膜剥离术(ESD)后根除HP仍有2.7%~6.1%的患者可发生异时性胃癌(MGC)，其发生机制尚不清楚。本文从HP根除后胃黏膜萎缩及肠化生不能完全逆转、胃黏膜上皮细胞过度增殖及遗传异常累积、表观组稳态失衡、免疫微环境变化、胃黏膜干细胞异常、染色质可及性、染色体重塑改变等角度，阐述早期胃癌行ESD及HP根除后上述分子改变导致癌变的机制。

胃黏膜剥离术  /  幽门螺杆菌  /  根除治疗  /  异时性胃癌  /  发生机制

Helicobacter pylori (HP) infection is a Class Ⅰ carcinogen in gastric cancer, closely related to the occurrence of gastric cancer. Many studies have shown that HP eradication has a preventive effect on gastric cancer. However, 2.7%-6.1% of patients with early gastric cancer who have been eradicated after endoscopic submucosal dissection (ESD) can still develop metachronous gastric cancer (MGC), and the mechanism of its occurrence is still unclear. In this review, the atrophy of gastric mucosa and intestinal metaplasia cannot be completely reversed after HP eradication, the excessive proliferation of gastric mucosa epithelial cells, the accumulation of genetic abnormalities, the homeostasis imbalance of the epigenetic group, changes in immune microenvironment, the abnormality of stem cells in gastric mucosa, chromatin accessibility, and changes in chromosome remodeling were discussed in the mechanism of carcinogenesis caused by the above molecular changes after ESD and HP eradication in early gastric cancer.

endoscopic submucosal dissection  /  Helicobacter pylori  /  eradication  /  metachronous gastric cancer  /  pathogenesis
胡馨月, 王斌, 王涛, 刘凯军, 文良志, 陈东风. 早期胃癌内镜下黏膜剥离术及幽门螺杆菌根除后异时性胃癌的发生机制研究进展. 解放军医学杂志, 2024 , 49 (1) : 108 -114 . DOI: 10.11855/j.issn.0577-7402.0460.2023.0719
Xin-Yue Hu, Bin Wang, Tao Wang, Kai-Jun Liu, Liang-Zhi Wen, Dong-Feng Chen. Research progress on the mechanism of metachronous gastric cancer after endoscopic submucosal dissection and Helicobacter pylori eradication in early gastric cancer[J]. Medical Journal of Chinese People’s Liberation Army, 2024 , 49 (1) : 108 -114 . DOI: 10.11855/j.issn.0577-7402.0460.2023.0719
正文
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胃癌是我国常见的恶性肿瘤[1]，2021年的数据显示其发病率在恶性肿瘤中排第5位，病死率排第3位，胃癌发病率在不同国家及地区存在明显差异，日本、韩国、中国、东欧及中南美洲国家胃癌发病率较高[2]。胃癌与幽门螺杆菌(Helicobacter pylori，HP)持续感染引起的慢性炎症密切相关[3-4]，从慢性胃炎、萎缩性胃炎(atrophic gastritis，AG)、肠上皮化生(intestinal metaplasia，IM)、肠上皮异型增生发展至胃癌的Correa学说路径已得到业界认可[5-6]。HP也被世界卫生组织(WHO)确定为胃癌的Ⅰ类致癌因子。2015年，《京都全球共识报告》提出，除有制衡因素以外，所有感染HP的人群都应接受根除治疗[7]，成功根除HP可以明显降低胃癌的发生率。数项随机对照试验及荟萃分析也证实，根除HP可减少胃癌的发生，然而学者们发现，即使在早期胃癌内镜下黏膜剥离术(endoscopic submucosal dissection，ESD)后根除HP，仍有2.7%~6.1%的患者会发生异时性胃癌(metachronous gastric cancer，MGC)[8-13]。MGC为早期胃癌(early gastric cancer，EGC)患者行ESD后1年或更长时间在原病灶以外部位发生的胃癌。根除HP后，胃癌的发病率每年约为0.3%，其发生因人而异，甚至成功根除HP后10年以上者仍有可能发生胃癌[14]。本文就根除HP后MGC的发病机制进行综述，以期为MGC的防治提供新思路。
1 HP根除后AG与IM不能完全逆转
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以往学者们认为胃癌前病变中AG及IM一般不能逆转，但最近研究报道显示，部分患者根除HP后其胃黏膜萎缩及肠化生可以逆转[15]。另有研究显示，羔羊胃提取物维生素B12胶囊及塞来昔布单药均能逆转AG及IM，且在羔羊胃提取物维生素B12初始治疗的基础上加用塞来昔布挽救治疗可进一步提高IM的消退率，达85.93%[16]。然而也有学者认为，根除HP虽然可以延缓AG及IM的进展，但不能完全逆转肠化生及异型增生的发生，这可能是由于根除HP后胃黏膜异常的局部微环境仍持续存在，以及胃黏膜上皮细胞遗传及表观遗传重编程的累积改变。因此，相关临床指南建议在发生胃黏膜萎缩前就进行HP根除治疗，以降低胃癌发生风险[17]。
1.1 细胞周期与IM
胃黏膜上皮细胞发生IM时，细胞凋亡与增殖的比例明显降低，这有利于细胞损伤及突变的积累。50%的胃癌旁IM有p53基因突变，Ⅲ型IM中P53蛋白积聚更明显[18]。IM所致的黏膜屏障功能障碍可导致胃内各种物质不断跨上皮渗透，促进免疫应答局部微环境改变，参与肿瘤的发生。根除HP后不能完全逆转的胃黏膜损伤及IM，与MGC的发生发展关系密切。
1.2 DNA异常高甲基化与IM
根除HP后，尽管IM上皮细胞异常高甲基化有所下调，但仍远高于正常胃黏膜，这些异常DNA甲基化在胃黏膜干细胞中仍能检出，均与胃癌发生相关。有研究还观察到根除HP并不能阻止表观基因组的重编程，癌前病变的DNA甲基异常赋予了细胞持续突变的潜能，这些表观遗传印记变化可致基因表达的永久性改变，促进肠化上皮向MGC演进[19-20]。
2 胃黏膜上皮细胞过度增殖可独立于HP感染
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有研究发现，慢性胃炎及胃癌的胃上皮增殖率增高与HP感染无关[21]。组织病理学检查显示，胃窦HP密度高于胃体，同时其炎症程度也较重。除菌后，胃窦上皮细胞的增殖指数有所降低，但与除菌前比较无明显差异[22]，表明根除HP后，胃窦的炎症仍可持续存在，提示HP感染并不一定是胃黏膜炎症的唯一原因。持续存在的炎症反应及炎症介质可引起胃黏膜上皮细胞损伤，一方面，氧自由基等引起细胞增殖过快，而增殖活跃的细胞DNA合成旺盛，易受基因毒性致癌物质的损伤，导致基因不稳增加而发生上皮内瘤变乃至癌变。若增殖速度超过凋亡速度时，增殖与凋亡失衡，可促进上皮内瘤变发生。另一方面，HP感染可刺激胃黏膜炎性细胞释放C-X-C族的炎性因子，此炎性因子中的ELR片段(谷氨酸-亮氨酸-精氨酸序列)可刺激细胞分裂增生、促进血管生成。当根除HP后，持续存在的炎症反应可能继续促进胃黏膜上皮细胞发生过度增殖，引发恶变。
3 胃黏膜上皮细胞遗传异常的累积
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HP感染可导致胃黏膜上皮细胞增殖自稳态受损，如微卫星不稳定性(microsatellite instability，MSI)、体细胞突变负荷(mutational burden，MB)及点突变，这些改变很难通过根除HP来逆转[23]。
3.1 胃黏膜上皮细胞MB累积
早期胃癌ESD术后实施根除HP治疗，在邻近的非癌黏膜中，发生异时性进展的患者MB往往高于未发生早期胃癌的患者。研究发现RECQL4、JAK3、ARID1A及MagiC1基因的突变与MB结合可促进异时性癌症的发生。ARID1A及MAGI1基因与胃癌的发生有显著相关性[24]。对GC外显子进行序列分析发现，83%的MSI患者存在ARID1A的高频失活突变或蛋白表达缺陷，并与PIK3CA突变及MSI相关[25]。在胃癌细胞中干扰ARIDIA后，Akt磷酸化水平上升，p21表达减少，细胞周期S期增多，G2期减少，细胞体积变大，葡萄糖消耗量增加。这些结果提示ARID1A通过影响Akt的磷酸化水平及细胞周期来调控细胞增殖。ARID1A还可通过影响E-cadherin的转录从而调控肿瘤的迁移、侵袭。且ARID1A的缺陷与MSI相关联，肿瘤抑制基因ARID1A的体细胞突变常在MSI高的胃癌中可以检测到[26]。携带ARID1A变异体的胃早癌患者在邻近非癌黏膜中有高的MB，与根除HP后仍可发生MGC有关。
3.2 胃黏膜上皮细胞点突变及基因扩增累积
HP感染相关的胃癌有相似的遗传学改变，即体细胞点突变及基因扩增。“非可控性炎症”(如持续或低强度的刺激、靶组织处于长期或过度反应状态)产生的细胞因子通过诱导基因突变、改变癌基因及抑癌基因表达、抑制细胞凋亡，炎症信号传导通路异常，诱导血管新生；并且“非可控性炎症”可通过募集多种免疫抑制性细胞(M2型肿瘤相关巨噬细胞、骨髓来源抑制细胞、调节性T细胞等)促进免疫抑制状态的肿瘤微环境建立，最终导致肿瘤发生，这种现象被称为广义的炎癌学说。“非可控性炎症”通过点突变或基因扩增激活已知的癌基因，如ErbB2及PIK3CA，进而活化下游信号通路磷脂酰肌醇-3-激酶(PI3K)/蛋白激酶B(PKB，Akt)/哺乳动物雷帕霉素靶蛋白(mTOR)及促分裂原活化的蛋白激酶(MAPK)途径，抑制细胞凋亡，促进肿瘤血管再生，增强肿瘤细胞的侵袭力[27]。这些变化在HP根除后的非癌黏膜中可持续存在，可能参与了MGC的发生。
4 表观组稳态失衡
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表观遗传学是一系列影响基因表达而不影响DNA一级序列的染色质改变，如异常甲基化。DNA异常高甲基化与不适当的转录沉默及基因功能缺失密切相关[28]。正常组织中表观遗传学改变的积累将会形成表观组稳态失衡，可能与HP相关胃炎及胃癌发生密切相关。研究表明胃癌患者的正常胃黏膜在根除HP后的甲基化水平可反映胃黏膜干细胞的DNA异常甲基化，与MGC的发生风险显著相关[29]。
4.1 DNA异常甲基化持续存在
HP感染后胃黏膜DNA甲基化的改变可持续存在并累积，暂时性甲基化很可能在祖细胞或分化细胞中被诱导，这些改变触发凋亡，引起胃黏膜上皮细胞脱落更新。永久性DNA甲基化很可能在胃黏膜干细胞中被诱导并终身存在。根除HP后，胃黏膜上皮细胞的甲基化水平没有明显下降，可能与MGC的发生有关。端粒的缩短及DNA甲基转移酶1(DNMT1)的高表达是根除HP后胃黏膜异常甲基化诱导的重要机制。除此之外，甲基化水平与炎性细胞浸润密切相关，即使根除HP，胃黏膜间质的炎症仍会存在，可持续诱导DNA甲基化。吸烟、饮酒等不良生活习惯及激素也可以诱导异常的DNA甲基化，长期接触烟草增加了DNA甲基转移酶3B(DNMT3B)的表达，并招募DNMT3B到BUB1、HDAC2等基因的启动子区域，促进这些基因的高甲基化，导致胃黏膜上皮细胞突变[30]。
4.2 CpG岛启动子异常甲基化
DNA甲基转移酶(DNA methyltransferases，DNMTs)的差异表达也可能诱导哺乳动物细胞中CpG的整体DNA低甲基化向DNA高甲基化演进，导致表观遗传不稳定[31]。CpG岛启动子的异常甲基化导致包括肿瘤抑制基因在内的多个基因如RUNX3、LOX、PTEN及CDH1的表观遗传沉默，这些基因参与DNA修复、调节细胞周期、信号转导等多个细胞生理过程，是肿瘤发生的重要机制之一[32]。PTEN蛋白对P13K/Akt信号通路有负性调控作用，当PTEN失活时，PIP3不能去磷酸化为PIP2，过多的PIP3积聚会激活Akt通路，通过调控P27、BAD、FOXO、mTOR、GSK-3等下游分子，发挥抑制细胞凋亡、促进细胞存活及增殖的作用。除调控Akt通路外，胞质内的PTEN还可抑制表皮生长因子(epidermal growth factor，EGF)刺激引起的原癌基因Shc磷酸化，进而抑制Ras/MAPK通路的活化；亦可通过FAK脱磷酸化等途径抑制细胞迁移、伸展及黏附。胞核内的PTEN具有重要的生物学功能，核内的PTEN可下调cyclin D1水平，诱导细胞G0-G1期阻滞，抑制肿瘤生长。还可通过非磷酸酶依赖的方式与着丝粒蛋白CENP-C结合，维持着丝粒稳定；也可与E2F1协同，激活Rad51转录，调控DNA双链断裂(DNA double-strand breaks，DSBs)的修复，抑制因DSBs引起的染色体不稳定。RUNX3可以通过上调miR-30a的表达从而抑制上皮-间充质转化(epithelial mesenchymal transition， EMT)中关键的间质标志分子波形蛋白的表达，从而抑制EMT的发生及胃癌细胞侵袭转移。
CpG岛启动子异常甲基化导致多个抑癌基因的表观遗传沉默，将会破坏细胞稳态，影响细胞增殖与凋亡、迁移及黏附。当肿瘤抑制基因下调，胃黏膜微环境中可触发一系列炎症反应，包括释放促炎细胞因子白细胞介素(IL)-1、IL-6、IL-8及肿瘤坏死因子(TNF)-α，激活核因子(NF)-κB途径。IL-8上调是甲基化炎症的共同特征，IL-6又可反向诱导DNA甲基化，这些途径的激活导致黏膜微环境中持续的慢性炎症，共同促进MGC的发生。
4.3 DNA异常甲基化导致肿瘤抑制因子表达下调
异常甲基化可引起miR-124a表达下调，特别是肿瘤抑制因子miR124a-3，它是预测MGC发生风险的标志分子[33]。SPHK1是miR-124的靶基因，miR-124直接与SPHK1的3'-UTR结合并下调其表达，发挥抗增殖作用。当miR-124异常甲基化时，SPHK1的过度表达导致AKT激活，进而导致FOXO1的抑制，并因此下调细胞周期蛋白抑制分子p21Cip1及p27Kip1的表达。miR-124还可通过NF-κB信号通路阻断EMT，抑制肿瘤细胞浸润及转移。异常甲基化导致肿瘤抑制因子SOCS3功能障碍，促进STAT3信号转导的持续激活[34]，SOCS3异常甲基化的胃黏膜中P-STAT3表达较高，可促进细胞的异常增殖。根除HP后，在SOCS3甲基化活跃的早期胃癌患者的非肿瘤性胃黏膜中，P-STAT3及Ki-67的表达水平仍较高[35]。STAT3还可通过与COX-2启动子结合上调COX-2，其产物PGS可进入核内，反向调节IL-6/STAT3信号转导，形成正反馈[36]，从而促进胃黏膜上皮细胞异常增殖。
5 机体免疫系统异常
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HP感染胃黏膜后，可迁徙至胃淋巴结，影响与慢性胃炎相关的细胞免疫及体液免疫，有助于MGC的发生。根除HP后，HP抗体滴度的缓慢降低提示侵入淋巴结的HP并未被迅速清除，这可能增加了MGC的发生风险。细胞毒素相关蛋白A(cytotoxin associated protein A，CagA)深易位可能与CagA抗体滴度的缓慢下降及胃癌的发展有关。根除HP 0.5~2.0年，较多患者仍有高滴度的HP抗体，提示HP阴性患者可能存在假阴性可能。定植于胃黏膜上皮细胞外的HP主要毒力因子CagA及空泡毒素(VacA)可通过多种方式抑制自噬上游信号活化及自噬溶酶体成熟，使癌前病变胃黏膜细胞的自噬受到抑制。这一变化可导致HP无法通过自噬被有效清除，CagA及VacA持续存在引起胃黏膜上皮细胞过度增殖及凋亡异常，从而增加了DNA损伤的机会，并促进胃黏膜组织的炎症[37]、氧化应激、凋亡及增殖异常等一系列恶性生物学过程。HP感染还能够诱导以Thl为主、调节性T细胞(Treg)及Thl7混合的T淋巴细胞免疫反应，有利于感染的慢性化过程。上述环节通过激活活性氧(ROS)、上调DNA突变酶胞苷脱氨酶(activation-induced cytidine deaminase，AID)的转录、诱导DNMTs错误定位等，导致肿瘤相关基因突变、染色体错配、异常DNA甲基化，从而导致癌基因激活、抑癌基因失活、DNA修复失调及染色体不稳定等。即使HP感染已被根除，癌变过程仍然继续进展。HP感染所致的炎症介质释放还可促进胃黏膜化生或异型增生，如IL-8是EMT的诱导因子；IL-6可以诱导DNA甲基化，增强COX-2诱导，促进细胞增殖及血管生成；NF-κB的激活可诱导肿瘤坏死因子受体相关因子1(TRAF1)的表达上调，而TRAF1具有抗凋亡作用；活化的NF-кB可结合在许多靶基因的启动子上，通过增强子与启动子之间的作用，迅速诱导mRNA的合成，这些改变与MGC的发生密切相关。
6 胃黏膜干细胞异常
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有研究发现，HP可激活胃黏膜干细胞并增加上皮细胞的分化及转归[38]，HP不仅感染胃小凹顶端的胃上皮细胞，也可侵入到胃底腺的深处，此处也是胃腺体的干细胞区域[39]。HP根除后，干细胞的持续增殖可能参与了MGC的发生及发展。
6.1 胃黏膜干细胞Axin2+/LGR5-细胞信号转导异常激活
Wnt/β-catenin信号转导在许多组织中对干细胞稳态调节及上皮细胞的再生有重要作用[40]。经典的Wnt靶基因Axin2主要表达于胃底腺及胃幽门腺的下峡部，此处也是胃干细胞存在的区域。HP感染增加了胃腺体间质R-spondin3的表达，Axin2及LGR5的表达都需要基质来源的R-spondin3来维持干细胞池的微环境。R-spondin3是胃黏膜上皮Wnt信号的调节因子，可促进胃干细胞特异性Axin2+/LGR5-细胞信号转导的效应及Axin2+细胞的增殖，并形成Axin2+细胞池，发挥胃小凹上皮细胞由基底向小凹顶端有序增殖并迁徙的调节作用。Axin2+/LGR5-细胞构成了一个高度增殖、无分化的区域，维持胃腺体的再生，其中R-spondin3作为一个关键的特异性调节因子来协调干细胞的稳态及增殖动力学[39]。即使根除HP后，干细胞特异性Axin2+/LGR5-细胞信号转导途径可能持续激活导致过度增殖，促进MGC的发生。
6.2 胃黏膜干细胞Wnt/β-catenin信号通路异常激活
有研究表明，HP感染可通过CagA以细胞间质上皮转换因子(cellular-mesenchymal epithelial transition factor，c-Met)和(或)丝氨酸/苏氨酸蛋白激酶(Akt)依赖的方式介导C端Ser675及Ser552残基β-catenin磷酸化，并以此激活Wnt/β-catenin信号通路。Nanog及Oct4是Wnt/β-catenin信号通路的下游靶基因，是肿瘤干细胞(cancer stem cells，CSCs)自我更新、特异性标志物表达及多能性维持所必需的[41-43]，具有诱导CSCs产生及增强EMT的能力[44-45]。HP可通过Wnt/β-catenin信号通路上调Nanog及Oct4的表达，促进CSCs的自我更新并上调CSCs标志物的表达，其启动子活性在HP感染过程中增强。EMT可诱导具有干细胞特性的CD44+细胞出现，CD44+信号激活后通过STAT3导致胃黏膜上皮化生及异常增生性病变。除此之外，CagA蛋白可直接与GSK-3β结合，抑制β-catenin降解[46]，还可促进以C-Met和(或)Akt依赖的方式诱导Ser552及Ser675处的β-catenin磷酸化，导致β-catenin在胞质中的大量聚集并入核与淋巴细胞增强因子/T细胞因子结合形成异二聚体，启动相关癌基因及有丝分裂原基因的转录等。HP感染还可通过NF-κB依赖性机制诱导RAS蛋白激活剂2(RASAL2)表达，NF-κB直接与RASAL2启动子结合，激活其转录，通过基因沉默及异位过表达，上调β-catenin转录活性。根除HP后，CSCs的异常持续增殖更新与MGC的发生密切相关。
6.3 胃黏膜干细胞DNA双链异常断裂
DNA双链断裂(DSBS)是HP依赖于Ⅳ型分泌系统(T4SS)由XPF/XPG核酸内切酶引入导致，进而引发NF-κB靶基因激活及细胞增殖。DSBS通过经典途径激活的NF-κB，将会发生异二聚体p50及RelA/p65的核位移，激活与炎症、细胞存活、生长等相关基因；通过非经典途径激活的NF-κB，促使淋巴样器官形成、B细胞存活。HP长期感染会导致胃黏膜细胞不精确修复，发生遗传不稳定性及频繁的染色体畸变，从而参与胃癌的发生。在不同细胞系及胃底或下峡部的干细胞中，DSBS以时间及剂量依赖的方式积累，在根除HP后可能会继续保持诱变特性[47]。除此之外，此前有研究在增强子上发现了一种DSBS转录耦合修复机制，这种耦合修复机制支持致癌超级增强子的激活。超级增强子是基因组中的独特区域，区域大，密集地与转录因子/辅助因子结合，可控制多种癌症驱动因素的超转录，是相关癌基因高表达所必需的，几乎参与所有肿瘤的进展。上述研究提示HP感染引起DSBS修复可通过超级增强子的重塑参与MGC的发生。
7 染色质可及性、染色体重塑及染色体重塑子的改变
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染色质可及性提供转录因子结合的结构，以调节与肿瘤进展及侵袭相关的多个基因的激活。染色质重塑可被遗传及表观遗传的改变所破坏，并作为驱动因素参与表观稳态缺陷的形成[48]。染色质重塑子通过调节染色质可及性及染色体重塑参与转录调控，如ARID1A、SMARCA1、SMARCA2及SMARCA4在胃癌中常常发生突变，参与胃癌的发生发展。SMARCA1及SMARCA2还是胃癌的抑癌基因，SMARCA1或SMARCA2突变在胃癌细胞系中会促进其生长。SMARCA1在正常胃组织中表达丰富，其表达可能因暴露于HP而暂时受到抑制，从而导致对异常甲基化诱导的易感性增加。根除HP后，胃黏膜干细胞中异常甲基化而沉默的SMARCA1可能促进了MGC的发生。DNA甲基化及组蛋白修饰相互关联，并在胃癌发生过程中影响表观遗传修饰，共同作用于染色质重塑[49]。在HP相关性胃炎的IM中，EZH2的表达明显高于非IM组，而EZH2可催化组蛋白及DNA的甲基化。BET家族含有能够识别乙酰化组蛋白赖氨酸残基的蛋白质，可作为活性启动子或增强子积聚在高乙酰化染色质区域上，作为支架招募转录因子及多蛋白复合物促进靶基因的转录，从而可能改变全局染色质的可及性[50]。高表达的EZH2还可通过与PTEN启动子结合来诱导胃癌细胞获得上皮-间充质转化表型，下调E-cadherin的表达，从而增强癌细胞的迁移及侵袭能力，特别是EZH2可增强胃癌细胞的成球能力，说明其在肿瘤干细胞富集过程中具有促进作用。HP根除后，发生在干细胞中的DNA甲基化及组蛋白修饰是相对“永久性的”，因此癌旁胃黏膜及化生上皮可能存在这些表观遗传稳态缺陷，参与MGC的发生。
8 总结与建议
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早期胃癌ESD术后根除HP后MGC受到临床越来越多的关注，HP根除及定期内镜监测是预防MGC发生的有效措施，根除HP能降低MGC发生率，但不能完全消除其风险。根除HP后，胃黏膜上皮细胞仍可通过持续异常增殖、遗传及表观遗传重编程的累积改变、干细胞突变转化及染色体可及性异常调节等环节逐渐演进发生MGC。因此，建议接受ESD治疗的早期胃癌患者于术前、术后常规检测HP，发现感染后尽快进行根除治疗。在早期胃癌ESD术后根除HP后建议患者每年进行1~2次内镜随访，具有高危因素的患者可适当缩短随访间隔，便于早期发现及治疗MGC。大部分MGC是分化良好的黏膜内癌，可继续选择内镜ESD治疗，少数进展期胃癌可选择外科手术、化疗、靶向或免疫治疗，长期预后良好。MGC的发生机制及相关标志物值得深入研究。
基金
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  • 国家重点研发计划(2022YFA1105302)
文献
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2024年第49卷第1期
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doi: 10.11855/j.issn.0577-7402.0460.2023.0719
  • 接收时间：2023-03-29
  • 首发时间：2025-11-23
  • 出版时间：2024-01-28
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  • 收稿日期：2023-03-29
  • 录用日期：2023-04-24
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National Key Research and Development Program of China(2022YFA1105302)
国家重点研发计划(2022YFA1105302)
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    陆军军医大学陆军特色医学中心消化内科，重庆 400042

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陈东风，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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