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Article(id=1211268821529268870, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1211268819788632695, articleNumber=null, orderNo=null, doi=10.11855/j.issn.0577-7402.2021.01.03, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1590595200000, receivedDateStr=2020-05-28, revisedDate=1606233600000, revisedDateStr=2020-11-25, acceptedDate=null, acceptedDateStr=null, onlineDate=1766718591338, onlineDateStr=2025-12-26, pubDate=1611763200000, pubDateStr=2021-01-28, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1766718591338, onlineIssueDateStr=2025-12-26, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1766718591338, creator=13701087609, updateTime=1766718591338, 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=11, endPage=17, ext={EN=ArticleExt(id=1211268823458648731, articleId=1211268821529268870, tenantId=1146029695717560320, journalId=1189873630562394117, language=EN, title=Effects of silencing Sema4D on the growth, autophagy and epithelial-mesenchymal transformation of gastric cancer cells SGC-7901, columnId=1190310110212751762, journalTitle=Medical Journal of Chinese People’s Liberation Army, columnName=Basic Research, runingTitle=null, highlight=null, articleAbstract=

Objective To investigate the effects of silencing axon guide protein 4D (Sema4D) on the growth, autophagy and epithelial-mesenchymal transformation of gastric cancer cell SGC-7901. Methods The cells were randomly divided into control group, shRNA-NC group, Sema4D-shRNA1 group, Sema4D-shRNA2 group and Sema4D-shRNA3 group, and transfected into SGC-7901 with shRNA Sema4D vector. The expression of Sema4D mRNA was detected by RT-PCR. The clone formation rate was determined by colony formation assay. Flow cytometry was used to detect apoptosis. Morphological changes of epithelial-mesenchymal transformation were observed microscopically. Western blotting was used to detect the expression levels of Ki67, proliferating cell nuclear antigen (PCNA), Bax, Bcl-2, caspase-3, cleaved caspase-3, Beclin1, p62, LC3Ⅰ, LC3Ⅱ, E-cadherin, N-cadherin, and vimentin proteins. Results The results of RT-PCR showed that compared with the control group, the mRNA levels of Sema4D-shRNA1 group, Sema4D-shRNA2 group and Sema4D-shRNA3 group were significantly lower, and the mRNA level of Sema4D-shRNA3 group was significantly lower than that of Sema4D-shRNA1 group and Sema4D-shRNA2 group (P<0.05).Sema4D-shRNA3 was selected for subsequent experiments. The results of colony forming assay showed that the colony forming efficiency of Sema4D-shRNA3 group was significantly lower than that of the control group (P<0.05). Flow cytometry results showed that compared with the control group, the apoptosis rate of Sema4D-shRNA3 group was significantly increased (P<0.05).Western blotting results showed that compared with the control group, the expression levels of Ki67, PCNA, p62, N-cadherin and vimentin proteins in the Sema4D-shRNA3 group were significantly lower, Beclin1 and E-cadherin proteins were significantly higher, and the ratios of Bax/Bcl-2, cleaved caspase-3/caspase-3 and LC3Ⅱ/LC3Ⅰ were significantly higher (P<0.05). Microscopically, the epithelial-mesenchymal transformation was inhibited in the Sema4D-shRNA3 group. Conclusion shRNA Sema4D can inhibit proliferation, autophagy and epithelial-mesenchymal transformation of SGC-7901 cells and promote apoptosis.

, correspAuthors=Man-Yu Chen, authorNote=null, correspAuthorsNote=
*E-mail:
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目的 探讨沉默轴突导向蛋白4D(Sema4D)对胃癌细胞SGC-7901生长、自噬及上皮-间质转化的影响。方法 将SGC-7901细胞随机分为对照组、shRNA-NC组、Sema4D-shRNA1组、Sema4D-shRNA2组与Sema4D-shRNA3组，构建shRNA Sema4D载体转染至SGC-7901细胞。采用RT-PCR检测各组Sema4D mRNA表达水平；采用克隆形成实验检测细胞克隆形成率；流式细胞仪检测细胞凋亡情况；显微镜观察上皮-间质转化形态学变化；Western blotting检测Ki-67、增殖细胞核抗原(PCNA)、Bax、Bcl-2、caspase-3、cleaved caspase-3、Beclin1、p62、LC3Ⅰ、LC3Ⅱ、E-cadherin、N-cadherin、波形蛋白表达水平。结果 RT-PCR检测结果显示，与对照组比较，Sema4D-shRNA1组、Sema4D-shRNA2组和Sema4D-shRNA3组Sema4D mRNA表达水平均明显降低，且Sema4D-shRNA3组明显低于Sema4D-shRNA1组和Sema4D-shRNA2组(P<0.05)，选择Sema4D-shRNA3进行后续试验。克隆形成实验结果显示，与对照组比较，Sema4D-shRNA3组克隆形成率明显降低(P<0.05)。流式细胞仪检测结果显示，与对照组比较，Sema4D-shRNA3组细胞凋亡率明显升高(P<0.05)。Western blotting检测结果显示，与对照组比较，Sema4D-shRNA3组Ki-67、PCNA、p62、N-cadherin、波形蛋白表达水平明显降低，Beclin1、E-cadherin蛋白表达水平明显升高，Bax/Bcl-2、cleaved caspase-3/caspase-3、LC3Ⅱ/LC3Ⅰ比值明显升高(P<0.05)。显微镜观察可见Sema4D-shRNA3组细胞上皮-间质转化受到抑制。结论 shRNA Sema4D可抑制SGC-7901细胞的增殖、自噬、上皮-间质转化，促进其凋亡。

, correspAuthors=陈满宇, authorNote=null, correspAuthorsNote=
陈满宇，E-mail：
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陶正贵，硕士研究生，副主任医师，主要从事胃肠肿瘤疾病诊断与治疗方面的研究。E-mail：

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陶正贵，硕士研究生，副主任医师，主要从事胃肠肿瘤疾病诊断与治疗方面的研究。E-mail：

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陶正贵，硕士研究生，副主任医师，主要从事胃肠肿瘤疾病诊断与治疗方面的研究。E-mail：

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Context-dependent EMT programs in cancer metastasis[J]. J Exp Med, 2019, 216(5): 1016-1026., articleTitle=Context-dependent EMT programs in cancer metastasis, refAbstract=null)], funds=[Fund(id=1211268832879054920, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1211268821529268870, awardId=Q20132605, language=EN, fundingSource=Scientific Research Project of Hubei Health and Education Department(Q20132605), fundOrder=null, country=null), Fund(id=1211268832962941005, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1211268821529268870, awardId=Q20132605, language=CN, fundingSource=湖北省教育厅科研项目(Q20132605), fundOrder=null, country=null)], companyList=[AuthorCompany(id=1211268825761321749, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1211268821529268870, xref=1, ext=[AuthorCompanyExt(id=1211268825773904662, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1211268821529268870, companyId=1211268825761321749, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1Department of General Surgery, Affiliated Hospital of Hubei University of Arts and Science/Xiangyang Central Hospital, Xiangyang, Hubei 441000), AuthorCompanyExt(id=1211268825782293271, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1211268821529268870, companyId=1211268825761321749, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1湖北文理学院附属医院/襄阳市中心医院普外科，湖北 襄阳 441000)]), AuthorCompany(id=1211268825866179355, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1211268821529268870, xref=2, ext=[AuthorCompanyExt(id=1211268825870373660, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1211268821529268870, companyId=1211268825866179355, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2Department of Oncology, Affiliated Hospital of Hubei University of Arts and Science/Xiangyang Central Hospital, Xiangyang, Hubei 441000, China), AuthorCompanyExt(id=1211268825878762269, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1211268821529268870, companyId=1211268825866179355, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2湖北文理学院附属医院/襄阳市中心医院肿瘤科，湖北 襄阳 441000)])], figs=[ArticleFig(id=1211268829959820265, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1211268821529268870, language=EN, label=Fig.1, caption=Comparison of expression levels of Sema4D mRNA in each group of gastric cancer cells, figureFileSmall=tE4as39ZuyEZtKVnqJFaLw==, figureFileBig=5i9bIjFbVOfgFG9Eb/EteA==, tableContent=null), ArticleFig(id=1211268830039512047, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1211268821529268870, language=CN, label=图1, caption=各组胃癌细胞Sema4D mRNA表达水平比较

与对照组比较，(1)P<0.05；与shRNA-NC组比较，(2)P<0.05；与Sema4D-shRNA1组比较，(3)P<0.05；与Sema4D-shRNA2组比较，(4)P<0.05。

, figureFileSmall=tE4as39ZuyEZtKVnqJFaLw==, figureFileBig=5i9bIjFbVOfgFG9Eb/EteA==, tableContent=null), ArticleFig(id=1211268831603986436, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1211268821529268870, language=EN, label=Fig.2, caption=Effect of shRNA Sema4D on proliferation of SGC-7901 cells, figureFileSmall=C1AA5iUt/3poMVQd/n3V4Q==, figureFileBig=qbUjfW59VxV1YQBHdCrKNQ==, tableContent=null), ArticleFig(id=1211268831708844046, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1211268821529268870, language=CN, label=图2, caption=shRNA Sema4D对胃癌细胞SGC-7901细胞增殖的影响

PCNA. 增殖细胞核抗原；A. 克隆形成实验检测细胞增殖情况(×200)；B. 克隆形成率柱状图；C. Western blotting检测Ki-67、PCNA蛋白表达水平；D. Ki-67、PCNA蛋白表达水平柱状图；与对照组比较，(1)P<0.05；与shRNA-NC组比较，(2)P<0.05。

, figureFileSmall=C1AA5iUt/3poMVQd/n3V4Q==, figureFileBig=qbUjfW59VxV1YQBHdCrKNQ==, tableContent=null), ArticleFig(id=1211268831855644689, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1211268821529268870, language=EN, label=Fig.3, caption=Effect of shRNA Sema4D on apoptosis of SGC-7901 cells, figureFileSmall=q+wkj9w4dBrsW5bauekeeQ==, figureFileBig=p4OHg5GPETDt4eDtdo5L/A==, tableContent=null), ArticleFig(id=1211268831985668119, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1211268821529268870, language=CN, label=图3, caption=shRNA Sema4D对胃癌细胞SGC-7901细胞凋亡的影响

A. 流式细胞仪检测各组细胞凋亡；B. 细胞凋亡率柱状图；C. Western blotting检测Bax、Bcl-2、cleaved caspase-3、caspase蛋白表达水平；D. Bax/Bcl-2、cleaved caspase-3/caspase比值柱状图；与对照组比较，(1)P<0.05；与shRNA-NC组比较，(2)P<0.05。

, figureFileSmall=q+wkj9w4dBrsW5bauekeeQ==, figureFileBig=p4OHg5GPETDt4eDtdo5L/A==, tableContent=null), ArticleFig(id=1211268832082137118, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1211268821529268870, language=EN, label=Fig.4, caption=Effect of shRNA Sema4D on the expression levels of Beclin1, p62, LC3Ⅰ and LC3Ⅱ protein in SGC-7901 cells, figureFileSmall=+iMsPq8LZwtnyUBEU+6wYA==, figureFileBig=3e6X4Z7/6K4Lv0LKA1Tg6g==, tableContent=null), ArticleFig(id=1211268832170217506, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1211268821529268870, language=CN, label=图4, caption=shRNA Sema4D对胃癌细胞SGC-7901 Beclin1、p62、LC3Ⅰ、LC3Ⅱ蛋白表达的影响

A. Western blot检测Beclin1、p62、LC3Ⅰ、LC3Ⅱ蛋白表达水平；B. Beclin1、p62蛋白表达水平及LC3Ⅱ/LC3Ⅰ比值柱状图；与对照组比较，(1)P<0.05；与shRNA-NC组比较，(2)P<0.05。

, figureFileSmall=+iMsPq8LZwtnyUBEU+6wYA==, figureFileBig=3e6X4Z7/6K4Lv0LKA1Tg6g==, tableContent=null), ArticleFig(id=1211268832283463720, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1211268821529268870, language=EN, label=Fig.5, caption=Effect of shRNA Sema4D on epithelial-mesenchymal transition of SGC-7901 cells, figureFileSmall=BN/geQx4ppxS7LH5VO9maA==, figureFileBig=+MUcxqNsKJ3yNVwgL85KMQ==, tableContent=null), ArticleFig(id=1211268832367349803, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1211268821529268870, language=CN, label=图5, caption=shRNA Sema4D对胃癌细胞SGC-7901上皮-间质转化的影响(×200), figureFileSmall=BN/geQx4ppxS7LH5VO9maA==, figureFileBig=+MUcxqNsKJ3yNVwgL85KMQ==, tableContent=null), ArticleFig(id=1211268832442847282, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1211268821529268870, language=EN, label=Fig.6, caption=Effect of shRNA Sema4D on the expression levels of E-cadherin, N-cadherin and vimentin protein in SGC-7901 cells, figureFileSmall=2yszt+ThCbG1stKkB7q9ag==, figureFileBig=o5qJr3eayccQU1R7Q/cy9A==, tableContent=null), ArticleFig(id=1211268832526733366, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1211268821529268870, language=CN, label=图6, caption=shRNA Sema4D对胃癌细胞SGC-7901 E-cadherin、N-cadherin、波形蛋白表达的影响

A. Western blotting检测E-cadherin、N-cadherin、波形蛋白表达水平；B. E-cadherin、N-cadherin、波形蛋白表达水平柱状图；与对照组比较，(1)P<0.05；与shRNA-NC组比较，(2)P<0.05。

, figureFileSmall=2yszt+ThCbG1stKkB7q9ag==, figureFileBig=o5qJr3eayccQU1R7Q/cy9A==, tableContent=null), ArticleFig(id=1211268832623202360, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1211268821529268870, language=EN, label=Tab.1, caption=

Primer sequences of RT-PCR

, figureFileSmall=null, figureFileBig=null, tableContent=
基因序列
Sema4D-shRNA1(Forward)5'-TGTCTGTGGAGTAT-GAGTTTGTGTT-3'
Sema4D-shRNA1(Reverse)5'-GGGTGTAGTTCA-CATCTTTCTTGAT-3'
Sema4D-shRNA2(Forward)5'-GGAUGGGACU-GUCUAUGAUTT3'
Sema4D-shRNA2(Reverse)5'-AUCAUAGA-CAGUCCCAUCCTT-3'
Sema4D-shRNA3(Forward)5'-GAAGCAGCAUGAGGUGUAUTT-3'
Sema4D-shRNA3(Reverse)5'-AUACACCUCAUGCUGCUUCTTA-3
shRNA-NC(Forward)5'-UUCUCCGAACGUGUCACGUTT-3'
shRNA-NC(Reverse)5'-ACGUGACACGUUCGGAGAATT-3'
), ArticleFig(id=1211268832753225792, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1211268821529268870, language=CN, label=表1, caption=

RT-PCR引物序列

, figureFileSmall=null, figureFileBig=null, tableContent=
基因序列
Sema4D-shRNA1(Forward)5'-TGTCTGTGGAGTAT-GAGTTTGTGTT-3'
Sema4D-shRNA1(Reverse)5'-GGGTGTAGTTCA-CATCTTTCTTGAT-3'
Sema4D-shRNA2(Forward)5'-GGAUGGGACU-GUCUAUGAUTT3'
Sema4D-shRNA2(Reverse)5'-AUCAUAGA-CAGUCCCAUCCTT-3'
Sema4D-shRNA3(Forward)5'-GAAGCAGCAUGAGGUGUAUTT-3'
Sema4D-shRNA3(Reverse)5'-AUACACCUCAUGCUGCUUCTTA-3
shRNA-NC(Forward)5'-UUCUCCGAACGUGUCACGUTT-3'
shRNA-NC(Reverse)5'-ACGUGACACGUUCGGAGAATT-3'
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沉默轴突导向蛋白4D对胃癌细胞SGC-7901生长、自噬及上皮-间质转化的影响
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陶正贵 1 , 杜静虎 1 , 田葵 1 , 王东华 1 , 龚伟 2 , 陈满宇 1, *
解放军医学杂志 | 基础研究 2021,46(1): 11-17
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解放军医学杂志 | 基础研究 2021, 46(1): 11-17
沉默轴突导向蛋白4D对胃癌细胞SGC-7901生长、自噬及上皮-间质转化的影响
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陶正贵1 , 杜静虎1, 田葵1, 王东华1, 龚伟2, 陈满宇1, *
作者信息
  • 1湖北文理学院附属医院/襄阳市中心医院普外科，湖北 襄阳 441000
  • 2湖北文理学院附属医院/襄阳市中心医院肿瘤科，湖北 襄阳 441000

    • 陶正贵，硕士研究生，副主任医师，主要从事胃肠肿瘤疾病诊断与治疗方面的研究。E-mail：

通讯作者:

陈满宇，E-mail：
Effects of silencing Sema4D on the growth, autophagy and epithelial-mesenchymal transformation of gastric cancer cells SGC-7901
Zheng-Gui Tao1 , Jing-Hu Du1, Kui Tian1, Dong-Hua Wang1, Wei Gong2, Man-Yu Chen1, *
Affiliations
  • 1Department of General Surgery, Affiliated Hospital of Hubei University of Arts and Science/Xiangyang Central Hospital, Xiangyang, Hubei 441000
  • 2Department of Oncology, Affiliated Hospital of Hubei University of Arts and Science/Xiangyang Central Hospital, Xiangyang, Hubei 441000, China
出版时间: 2021-01-28 doi: 10.11855/j.issn.0577-7402.2021.01.03
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摘要
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目的 探讨沉默轴突导向蛋白4D(Sema4D)对胃癌细胞SGC-7901生长、自噬及上皮-间质转化的影响。方法 将SGC-7901细胞随机分为对照组、shRNA-NC组、Sema4D-shRNA1组、Sema4D-shRNA2组与Sema4D-shRNA3组，构建shRNA Sema4D载体转染至SGC-7901细胞。采用RT-PCR检测各组Sema4D mRNA表达水平；采用克隆形成实验检测细胞克隆形成率；流式细胞仪检测细胞凋亡情况；显微镜观察上皮-间质转化形态学变化；Western blotting检测Ki-67、增殖细胞核抗原(PCNA)、Bax、Bcl-2、caspase-3、cleaved caspase-3、Beclin1、p62、LC3Ⅰ、LC3Ⅱ、E-cadherin、N-cadherin、波形蛋白表达水平。结果 RT-PCR检测结果显示，与对照组比较，Sema4D-shRNA1组、Sema4D-shRNA2组和Sema4D-shRNA3组Sema4D mRNA表达水平均明显降低，且Sema4D-shRNA3组明显低于Sema4D-shRNA1组和Sema4D-shRNA2组(P<0.05)，选择Sema4D-shRNA3进行后续试验。克隆形成实验结果显示，与对照组比较，Sema4D-shRNA3组克隆形成率明显降低(P<0.05)。流式细胞仪检测结果显示，与对照组比较，Sema4D-shRNA3组细胞凋亡率明显升高(P<0.05)。Western blotting检测结果显示，与对照组比较，Sema4D-shRNA3组Ki-67、PCNA、p62、N-cadherin、波形蛋白表达水平明显降低，Beclin1、E-cadherin蛋白表达水平明显升高，Bax/Bcl-2、cleaved caspase-3/caspase-3、LC3Ⅱ/LC3Ⅰ比值明显升高(P<0.05)。显微镜观察可见Sema4D-shRNA3组细胞上皮-间质转化受到抑制。结论 shRNA Sema4D可抑制SGC-7901细胞的增殖、自噬、上皮-间质转化，促进其凋亡。

胃癌  /  轴突导向蛋白4D  /  自噬  /  上皮-间质转化

Objective To investigate the effects of silencing axon guide protein 4D (Sema4D) on the growth, autophagy and epithelial-mesenchymal transformation of gastric cancer cell SGC-7901. Methods The cells were randomly divided into control group, shRNA-NC group, Sema4D-shRNA1 group, Sema4D-shRNA2 group and Sema4D-shRNA3 group, and transfected into SGC-7901 with shRNA Sema4D vector. The expression of Sema4D mRNA was detected by RT-PCR. The clone formation rate was determined by colony formation assay. Flow cytometry was used to detect apoptosis. Morphological changes of epithelial-mesenchymal transformation were observed microscopically. Western blotting was used to detect the expression levels of Ki67, proliferating cell nuclear antigen (PCNA), Bax, Bcl-2, caspase-3, cleaved caspase-3, Beclin1, p62, LC3Ⅰ, LC3Ⅱ, E-cadherin, N-cadherin, and vimentin proteins. Results The results of RT-PCR showed that compared with the control group, the mRNA levels of Sema4D-shRNA1 group, Sema4D-shRNA2 group and Sema4D-shRNA3 group were significantly lower, and the mRNA level of Sema4D-shRNA3 group was significantly lower than that of Sema4D-shRNA1 group and Sema4D-shRNA2 group (P<0.05).Sema4D-shRNA3 was selected for subsequent experiments. The results of colony forming assay showed that the colony forming efficiency of Sema4D-shRNA3 group was significantly lower than that of the control group (P<0.05). Flow cytometry results showed that compared with the control group, the apoptosis rate of Sema4D-shRNA3 group was significantly increased (P<0.05).Western blotting results showed that compared with the control group, the expression levels of Ki67, PCNA, p62, N-cadherin and vimentin proteins in the Sema4D-shRNA3 group were significantly lower, Beclin1 and E-cadherin proteins were significantly higher, and the ratios of Bax/Bcl-2, cleaved caspase-3/caspase-3 and LC3Ⅱ/LC3Ⅰ were significantly higher (P<0.05). Microscopically, the epithelial-mesenchymal transformation was inhibited in the Sema4D-shRNA3 group. Conclusion shRNA Sema4D can inhibit proliferation, autophagy and epithelial-mesenchymal transformation of SGC-7901 cells and promote apoptosis.

gastric cancer  /  Sema4D  /  autophagy  /  epithelial-mesenchymal transition
陶正贵, 杜静虎, 田葵, 王东华, 龚伟, 陈满宇. 沉默轴突导向蛋白4D对胃癌细胞SGC-7901生长、自噬及上皮-间质转化的影响. 解放军医学杂志, 2021 , 46 (1) : 11 -17 . DOI: 10.11855/j.issn.0577-7402.2021.01.03
Zheng-Gui Tao, Jing-Hu Du, Kui Tian, Dong-Hua Wang, Wei Gong, Man-Yu Chen. Effects of silencing Sema4D on the growth, autophagy and epithelial-mesenchymal transformation of gastric cancer cells SGC-7901[J]. Medical Journal of Chinese People’s Liberation Army, 2021 , 46 (1) : 11 -17 . DOI: 10.11855/j.issn.0577-7402.2021.01.03
正文
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胃癌是一种起源于胃黏膜上皮的常见恶性肿瘤，是全球第二大致死性肿瘤，其发病率呈逐渐增高趋势，仅我国每年就有超过60万新发病例[1]。尽管外科手术、放射疗法和化学疗法等胃癌治疗方法有所进步，但由于多数患者确诊时已处于中晚期，导致其预后较差，目前的远期生存率仍低于30%[2]。因此，探索胃癌诊断的新的标志物及治疗靶标非常重要[3]。轴突导向蛋白4D (semaphorin 4D，Sema4D)又称CD100，是Semaphorin家族成员之一，属于免疫系统的一种跨膜型的同源二聚体糖蛋白[4]。Sema4D在多种肿瘤的增殖、血管生成及转移等过程中发挥重要作用，其表达与肿瘤的进展呈正相关[5-6]。已有研究发现，Sema4D在胃癌中呈高表达，可通过促进肿瘤血管新生而加速胃癌细胞的浸润、转移[7-8]，可作为判定胃癌患者预后的参考。但Sema4D在胃癌中的具体作用机制尚不明确。本研究探讨了沉默Sema4D对胃癌细胞SGC-7901生长、自噬及上皮-间质转化的影响，以期为胃癌的防治提供理论依据。
1 材料与方法
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1.1 主要试剂及仪器
RPMI 1640培养基(61870-127)、胎牛血清(26400-036)、青链霉素(15140-122)、胰蛋白酶(25200-056)购自美国Gibco公司(Grand Island，NY)；BCA蛋白浓度测定试剂盒(P0012S)、LipoRNAiTM转染试剂(C0535)、Annexin V-FITC细胞凋亡检测试剂盒(C1062S)、辣根过氧化物酶标记山羊抗兔IgG (A0208)购自上海碧云天生物技术研究所；兔抗Ki-67 (ab15580)、增殖细胞核抗原(proliferating cell nuclear antigen，PCNA)(ab18197)、Bax (ab53154)、Bcl-2 (ab196495)、caspase-3 (ab13847)、cleaved caspase-3 (ab2302)、Beclin1 (ab62557)、p62 (ab56416)、LC3Ⅱ/LC3Ⅰ(ab128025)、E-cadherin (ab15148)、N-cadherin(ab18203)、波形蛋白(ab137321)、GAPDH (ab9485)单克隆抗体购自英国Abcam公司(Cambridge，MA)。Nano-Drop分光光度计购自赛默飞世尔科技公司；FACSCalibur流式细胞仪购自美国BD公司；FluorChem HD2凝胶成像系统购自美国ProteinSimple公司。
1.2 细胞培养
人胃腺癌细胞SGC-7901来源于美国典型培养物保藏中心(Manassas，Virginia，USA)。将SGC-7901细胞培养于含10%胎牛血清和1%青链霉素的RPMI 1640培养基中，置于37 ℃、含5%CO2的培养箱，每24 h更换新鲜培养基，1:2传代。
1.3 细胞处理及分组
为了防止脱靶效应，共设计3对shRNA序列及1对shRNA-NC序列干扰Sema4D的表达。通过RT-PCR检测选择效果最好的Sema4D-shRNA进行后续试验。取对数生长期细胞，构建shRNA Sema4D载体，采用LipoRNAiTM转染试剂转染SGC-7901细胞，将细胞随机分为对照组、shRNA-NC组、Sema4D-shRNA1组、Sema4D-shRNA2组与Sema4D-shRNA3组。对照组不做处理，shRNA-NC组转染阴性对照shRNA-NC载体，Sema4D-shRNA组转染shRNA Sema4D载体。引物序列如表1所示。
1.4 RT-PCR检测Sema4D mRNA表达水平
采用Trizol法提取SGC-7901细胞总RNA，用Nanodrop分光光度计测定吸光度(A260/A280)，计算RNA浓度。按照试剂盒说明书进行cDNA合成和PCR扩增，反应条件为94 ℃预变性5 min，94 ℃变性30 s，55 ℃退火30 s，72 ℃延伸30 s，扩增35个循环，72 ℃延长10 min，存储在4 ℃条件下。反应产物用2%琼脂糖凝胶电泳分离，用2–ΔΔCt法计算各目的基因的相对表达量。
1.5 克隆形成实验检测细胞增殖情况
在培养皿中培养各组细胞至融合度为30%，继续培养4 d，吹散为单个细胞，用6孔板培养，每孔约500个细胞，培养14 d，弃去培养基，用乙醇固定30 min，0.5%结晶紫染色，去离子水漂洗晾干，拍照后用Image-Pro Plus计算每孔中细胞克隆形成的数目。
1.6 流式细胞仪检测细胞凋亡率
收集各组细胞，悬浮于10 ml离心管中，调整细胞密度为3×106/ml，1000 r/min离心5 min，弃去培养液，用孵育缓冲液洗涤1次，1000 r/min离心5 min，用100 μl标记溶液重悬细胞，室温下避光孵育15 min，1000 r/min离心5 min，沉淀细胞用孵育缓冲液洗涤1次，加入SA-FLOUS溶液4 ℃下孵育20 min，按照Annexin V-FITC细胞凋亡检测试剂盒说明书进行流式细胞仪上机分析。
1.7 上皮-间质转化形态学观察
取对数生长期细胞，于倒置显微镜下观察上皮-间质转化形态的改变。
1.8 Western blotting检测蛋白表达水平
将各组待测细胞用PBS清洗3次，加入含蛋白酶抑制剂的细胞裂解液提取总蛋白，依据BCA试剂盒说明书步骤测定蛋白质含量。提取等量的蛋白质样品(20 mg)，100 ℃变性5 min，然后进行SDS-PAGE凝胶电泳分离并转移至PVDF膜上，5% BSA室温封闭1~2 h，加入一抗(1:1000) 4 ℃孵育过夜；次日，PBS洗涤后加入辣根过氧化物酶标记的二抗(1:3000)，室温孵育1 h，PBS洗涤。加入发光液，采用凝胶成像仪曝光拍照，用ImageJ软件统计灰度值并计算Ki-67、PCNA、Bax、Bcl-2、caspase、cleaved caspase-3、Beclin1、p62、LC3Ⅰ、LC3Ⅱ、E-cadherin、N-cadherin、波形蛋白相对表达量，以GAPDH作为内参。每个实验至少重复3次。
1.9 统计学处理
采用SPSS 17.0软件进行统计分析。所得数据以$\bar{x}±s$表示，多组间比较采用单因素方差分析，进一步两两比较采用LSD法。P<0.05为差异有统计学意义。
2 结果
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2.1 各组Sema4D mRNA表达水平比较
RT-PCR检测结果显示，与对照组比较，Sema4D-shRNA1组、Sema4D-shRNA2组和Sema4D-shRNA3组Sema4D mRNA相对表达水平(分别为0.41±0.04、0.50±0.04、0.16±0.04)均明显降低(P<0.05)，且Sema4D-shRNA3组明显低于Sema4D-shRNA1组和Sema4D-shRNA2组(P<0.05，图1)。选择shRNA3 Sema4D进行后续试验。
2.2 shRNA Sema4D对SGC-7901细胞增殖的影响
克隆形成实验结果显示，与对照组比较，Sema4D-shRNA3组克隆形成率明显降低[(58.35±7.01) %vs. (11.43±6.55) %，P<0.05，图2A、B]；Western blotting检测结果显示，与对照组比较，Sema4D-shRNA3组Ki-67、PCNA蛋白表达水平明显降低(0.55±0.05 vs. 0.07±0.01；0.18±0.06 vs.0.02±0.01，P<0.05，图2C、D)。
2.3 shRNA Sema4D对SGC-7901细胞凋亡的影响
流式细胞仪检测结果显示，与对照组比较，Sema4D-shRNA3组细胞凋亡率明显升高[(3.1±1.0) % vs.(31.2±5.0) %，P<0.05，图3A、B]。Western blotting检测结果显示，与对照组比较，Sema4D-shRNA3组Bax/Bcl-2、cleaved caspase-3/caspase-3比值明显升高(0.05±0.03 vs. 6.80±0.70；0.006±0.004 vs.0.210±0.025，P<0.05，图3C、D)。
2.4 shRNA Sema4D对SGC-7901细胞中Beclin1、LC3Ⅱ、LC3Ⅰ、p62蛋白表达的影响
Western blotting检测结果显示，与对照组比较，Sema4D-shRNA3组Beclin1蛋白的表达水平和LC3Ⅱ/LC3Ⅰ比值明显升高(0.05±0.03 vs. 0.26±0.05；0.05±0.04 vs. 1.65±0.16，P<0.05)，p62蛋白的表达水平明显降低(0.94±0.07 vs. 0.18±0.06，P<0.05，图4)。
2.5 shRNA Sema4D对SGC-7901细胞上皮-间质转化
荧光显微镜下观察可见，对照组及shRNA-NC组细胞呈连接松散的类圆或纺锤体样，细胞间黏附力降低，细胞由上皮向间质转化，发生了典型的上皮-间质形态变化；Sema4D-shRNA3组细胞间排列聚集，细胞呈圆形、椭圆形(图5)，表明shRNA Sema4D可抑制SGC-7901细胞的上皮-间质转化。
2.6 shRNA Sema4D对SGC-7901细胞E-cadherin、N-cadherin、波形蛋白表达的影响
Western blotting检测结果显示，与对照组比较，Sema4D-shRNA3组E-cadherin蛋白的表达水平明显升高(0.05±0.02 vs.0.31±0.04，P<0.05)，N-cadherin、波形蛋白的表达水平明显降低(0.49±0.04 vs. 0.05±0.03；0.36±0.05 vs. 0.04±0.01，P<0.05，图6)。
3 讨论
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胃癌是一种临床常见的消化道肿瘤，其发病率和病死率居恶性肿瘤前列[9]。随着基因治疗技术的发展，分子靶向治疗有望为胃癌的治疗提供新的方向。
胃癌细胞具有高度增殖能力，致使其早期可发生转移，因此，抑制胃癌细胞的增殖对于控制胃癌的进展具有重要意义[10]。Ki-67是一种与细胞增殖相关的核蛋白，是指导治疗、判断肿瘤预后的重要指标。有研究发现，Ki-67在胃癌组织中呈高表达[11]，而抑制Ki-67的表达可有效降低胃癌细胞的增殖潜能。PCNA是一种与细胞增殖状态有关的核蛋白，在胃癌组织中的表达高于正常组织及癌前病变组织，且随着临床分期的增加和淋巴结转移，其表达水平逐渐增高，可反映肿瘤细胞的增殖活性和所处周期[12]。陈武桂等[13]发现，siRNA沉默Sema4D可抑制MDA-MB-231细胞的增殖和迁移。Tasaka等[14]发现，低氧诱导因子能够促进乳腺癌Sema4D的表达，并诱导内皮细胞发生迁移，导致乳腺癌细胞增殖。本研究发现，shRNA Sema4D可下调SGC-7901细胞Ki-67、PCNA蛋白的表达，提示shRNA Sema4D可抑制SGC-7901细胞的增殖。
细胞凋亡紊乱是肿瘤发生发展的关键。Caspase蛋白的改变是细胞凋亡发生的重要标志，而caspase-3以无活性的pro-caspase 3形式存在，在细胞接收到一系列的凋亡信号后，经过剪切成为活化的执行因子caspase-3，后者是细胞凋亡不可逆的标志[15]。Bcl-2家族的抗凋亡蛋白Bcl-2和促凋亡蛋白Bax是细胞凋亡的关键调节因子，提高Bax/Bcl-2的比值可促进细胞凋亡，而降低Bax/Bcl-2的比值则会抑制细胞凋亡[16]。相关研究表明，在胃癌中caspase-3表达下调，Bcl-2表达明显高于癌旁组织，且与Bax的表达存在负相关关系[17]。Jiang等[18]发现，敲低Sema4D的表达能促进乳腺癌细胞的增殖、侵袭及迁移，并诱导其凋亡。Wang等[19]发现，敲低Sema4D的表达可促进食管鳞状细胞癌细胞的凋亡。本研究发现，shRNA Sema4D可升高Bax/Bcl-2、cleaved caspase-3/caspase-3比值，提示shRNA Sema4D可促进SGC-7901细胞凋亡。
自噬是维持细胞平衡的一种自我保护机制，但在某些应激条件下，自噬则是肿瘤细胞逃避凋亡的重要机制[20]。Beclin1是酵母Atg6基因在人类基因中的同源体，可激活自噬过程，是维持细胞自噬活性的关键。Beclin1在胃癌组织中的表达阳性率较低，而上调Beclin1的表达可诱导胃癌细胞自噬的发生[21]。自噬标记蛋白p62是多泛素化结合蛋白，自噬发生缺陷可上调p62的表达，p62在胃癌中表达率较高且聚集[22]。LC3蛋白是一种自噬标志物，检测LC3Ⅱ与LC3Ⅰ的比值可在一定程度上反映自噬体的数量[23]。本研究发现，shRNA Sema4D可升高SGC-7901细胞Beclin1蛋白的表达水平及LC3Ⅱ/LC3Ⅰ的比值，降低p62蛋白的表达水平，提示shRNA Sema4D可抑制SGC-7901细胞的自噬。
上皮-间质转化是正常上皮细胞失去上皮特性转变为间质样肿瘤细胞的重要过程[24]。多项研究发现，上皮-间质转化的异常活化与胃癌的发生、侵袭和转移密切相关[25-26]。上皮-间质转化的主要特征为E-cadherin表达减少、N-cadherin表达增加、细胞角蛋白细胞骨架转化为以波形蛋白为主的细胞骨架及形态上具有间充质细胞[27]。本研究发现，shRNA Sema4D可升高SGC-7901细胞E-cadherin蛋白的表达水平，降低N-cadherin、波形蛋白的表达水平，提示shRNA Sema4D可抑制SGC-7901细胞的上皮-间质转化。
综上所述，沉默Sema4D可抑制SGC-7901细胞的生长、自噬、上皮-间质转化，促进其凋亡。本研究的不足之处在于未能在体内试验验证沉默Sema4D对胃癌细胞自噬、上皮-间质转化和凋亡的影响。
基金
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  • 湖北省教育厅科研项目(Q20132605)
文献
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参考文献 引证文献
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2021年第46卷第1期
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doi: 10.11855/j.issn.0577-7402.2021.01.03
  • 接收时间：2020-05-28
  • 首发时间：2025-12-26
  • 出版时间：2021-01-28
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  • 收稿日期：2020-05-28
  • 修回日期：2020-11-25
基金
Scientific Research Project of Hubei Health and Education Department(Q20132605)
湖北省教育厅科研项目(Q20132605)
作者信息
    1湖北文理学院附属医院/襄阳市中心医院普外科，湖北 襄阳 441000
    2湖北文理学院附属医院/襄阳市中心医院肿瘤科，湖北 襄阳 441000

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