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Article(id=1198602007167730254, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1198601997155922872, articleNumber=null, orderNo=null, doi=10.11855/j.issn.0577-7402.2633.2024.0229, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1671984000000, receivedDateStr=2022-12-26, revisedDate=null, revisedDateStr=null, acceptedDate=1678723200000, acceptedDateStr=2023-03-14, onlineDate=1763698587457, onlineDateStr=2025-11-21, pubDate=1719504000000, pubDateStr=2024-06-28, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1763698587457, onlineIssueDateStr=2025-11-21, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1763698587457, creator=13701087609, updateTime=1763698587457, updator=13701087609, issue=Issue{id=1198601997155922872, tenantId=1146029695717560320, journalId=1189873630562394117, year='2024', volume='49', issue='6', pageStart='611', pageEnd='732', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=0, createTime=1763698585070, creator=13701087609, updateTime=1763698770557, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1198602775211901122, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1198601997155922872, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1198602775211901123, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1198601997155922872, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=679, endPage=685, ext={EN=ArticleExt(id=1198602008438604388, articleId=1198602007167730254, tenantId=1146029695717560320, journalId=1189873630562394117, language=EN, title=Effect of VEGF on the expression of genes related to ovarian steroid synthesis in mice and its mechanism, columnId=1190310110212751762, journalTitle=Medical Journal of Chinese People’s Liberation Army, columnName=Basic Research, runingTitle=null, highlight=null, articleAbstract=

Objective To investigate the effect of vascular endothelial growth factor (VEGF) on the expression of genes related to ovarian steroid synthesis in mice and its underlying mechanism. Methods A transgenic mouse model with tetracycline -reversible regulation of VEGF expression was used, and the genotype of mice was identified by polymerase chain reaction (PCR). Twenty mice were divided into normal VEGF expression group (Dox+, n=10) and VEGF expression inhibition group (Dox-, n=10) by feeding them doxycycline. Western blotting was used to detect the expression of VEGF protein in ovarian tissues. Fluorescence quantitative PCR was used to detect the mRNA expression of VEGF, KDR and genes known to play roles in follicle development, such as follicle-stimulating hormone (FSH) and inhibin B (INHBB). HE staining was used to observe changes in ovarian tissue. Total RNA was extracted from mouse ovarian tissues for transcriptome sequencing, and the relevant differential genes were analyzed by FPKM and log2FC values. Results Compared with the Dox+ group, the mRNA and protein levels of VEGF in the Dox- group significantly reduced, and the mRNA levels of KDR also significantly decreased (P<0.05). HE staining results showed that compared with the Dox+ group, follicular development was impaired and atresia follicles appeared in the Dox- group. Sequencing analysis identified that significant differences in follicular development-related genes and steroid synthesis-related genes between the two groups (P<0.05). Enrichment analysis showed that VEGF in mouse ovaries mainly regulates ovarian steroidogenesis and other pathways. Fluorescence quantitative PCR results demonstrated that compared with the Dox+ group, the follicular development-related genes (INHBB and FSHR) in the ovarian tissues of the Dox- group were significantly up-regulated (P<0.05), whereas the key genes of steroid synthesis (StAR, CYP11A1, 3β-HSD) were significantly down-regulated (P<0.05).The quantitative results were basically consistent with the sequencing results. Conclusion Mice with inhibited VEGF exhibited ovarian follicular dysplasia, potentially due to the mechanism whereby VEGF inhibition downregulated the expression of genes associated with steroid synthesis, such as FSH and INHBB, thereby obstructing cholesterol metabolism.

, correspAuthors=Xiao-Dan Lu, authorNote=null, correspAuthorsNote=
E-mail:
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目的 探讨血管内皮生长因子(VEGF)对小鼠卵巢类固醇合成相关基因表达的影响及其机制。方法 利用四环素可逆调节VEGF表达的转基因小鼠模型，采用聚合酶链反应(PCR)法鉴定小鼠基因型，通过喂食强力霉素将20只小鼠分为VEGF表达正常组(Dox+)与VEGF表达抑制组(Dox-)(n=10)。采用Western blotting检测卵巢组织中VEGF蛋白的表达情况；荧光定量PCR检测VEGF、VEGF受体2(KDR)及已知在卵泡发育中发挥作用的基因卵泡刺激素(FSH)、抑制素B(INHBB) mRNA的表达情况。HE染色观察卵巢组织的变化。取小鼠卵巢组织提取总RNA进行转录组测序，并通过FPKM、log2FC值分析相关差异基因。结果 与Dox+组比较，Dox-组VEGF mRNA和蛋白水平明显降低，KDR mRNA水平明显降低(P<0.05)。HE染色结果显示，与Dox+组比较，Dox-组卵泡发育障碍，并出现闭锁卵泡。根据测序结果分析筛选出两组小鼠的卵泡发育相关基因、类固醇合成相关基因具有明显差异(P<0.05)；富集分析发现小鼠卵巢中VEGF主要参与调控卵巢类固醇生成等通路。荧光定量PCR结果显示，与Dox+组相比，Dox-组小鼠卵巢组织中卵泡发育相关基因(INHBB、FSHR)明显上调(P<0.05)，类固醇合成的关键基因(StAR、CYP11A1、3β-HSD)明显下调(P<0.05)，定量结果与测序结果基本一致。结论 VEGF抑制可使小鼠卵泡发育障碍，其可能的机制是通过下调卵巢类固醇合成相关基因FSH、INHBB的表达从而阻碍胆固醇代谢来实现的。

, correspAuthors=芦小单, authorNote=null, correspAuthorsNote=
芦小单，E-mail：
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张智慧，硕士研究生，主要从事临床检验诊断方面的研究

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张智慧，硕士研究生，主要从事临床检验诊断方面的研究

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张智慧，硕士研究生，主要从事临床检验诊断方面的研究

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VEGF. 血管内皮生长因子；M. DNA Marker；P. 阳性对照；N. 阴性对照；A. PCR电泳结果；B. 四环素调节VEGF可逆抑制小鼠模型

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VEGF. 血管内皮生长因子；A. qRT-PCR检测VEGF mRNA表达水平(n=6)；B. Western blotting检测VEGF蛋白表达水平(n=3)；*P<0.05；**P<0.01

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蓝色箭头示卵泡，黄色箭头示黄体

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cAMP. 环腺苷酸；TNF. 肿瘤坏死因子；PPAR. 过氧化物酶体增殖物激活受体；Padj. 校正后的P值

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StAR. 类固醇生成急性调节蛋白；CYP11A1. 细胞色素P450胆固醇侧链裂解酶；3β-HSD. 3β-羟基类固醇脱氢酶；KDR. 血管内皮生长因子受体2；INHBB. 抑制素B；FSHR. 促卵泡激素受体；*P<0.05；**P<0.01；***P<0.001

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VEGF. 血管内皮生长因子；StAR. 类固醇生成急性调节蛋白；CYP11A1. 细胞色素P450胆固醇侧链裂解酶；3β-HSD. 3β-羟基类固醇脱氢酶；KDR. 血管内皮生长因子受体2；INHBB. 抑制素B；FSHR. 卵泡刺激素受体

, figureFileSmall=dA4pMzv2X7l/wWNhaHp52Q==, figureFileBig=puwMwSjsX15zeEDdlJwcUw==, tableContent=null), ArticleFig(id=1198602020572726183, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198602007167730254, language=EN, label=Tab.1, caption=

PCR primer sequences

, figureFileSmall=null, figureFileBig=null, tableContent=
基因引物序列(5'-3')

目的片段
(bp)

VEGFF：CGGCAGCGGATCTCTGTCGC野生型400
R：GGAGCTCTGATACTCTTTCGA重组型500
tetR-KrabF：CAGCGCATTAGTGCTGCTTA464
R：TAGCGACTTGATGCTCTTGATC
), ArticleFig(id=1198602021763908523, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198602007167730254, language=CN, label=表1, caption=

PCR引物序列

, figureFileSmall=null, figureFileBig=null, tableContent=
基因引物序列(5'-3')

目的片段
(bp)

VEGFF：CGGCAGCGGATCTCTGTCGC野生型400
R：GGAGCTCTGATACTCTTTCGA重组型500
tetR-KrabF：CAGCGCATTAGTGCTGCTTA464
R：TAGCGACTTGATGCTCTTGATC
), ArticleFig(id=1198602021881349035, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198602007167730254, language=EN, label=Tab.2, caption=

qRT-PCR primer sequences

, figureFileSmall=null, figureFileBig=null, tableContent=
基因引物序列(5'-3')目的片段(bp)
VEGFF：GATCATGCGGATCAAACCTC105
R：AATGCTTTCTCCGCTCTGAA
KDRF：CTGGAGCCTACAAGTGCTCG179
R：GAGGTTTGAAATCGACCCTCG
StARF：ATGTTCCTCGCTACGTTCAAG122
R：CCCAGTGCTCTCCAGTTGAG
CYP11A1F：ACACTGAGACTCCACCCCAT137
R：CTCGACCCATGGCAAAGCTA
3β-HSDF：AGCTCTGGACAAAGTATTCCGA234
R：GCCTCCAATAGGTTCTGGGT
INHBBF：AACTGCTCCCCTATGTCCTGG127
R：CCGCTACGTTTCAGGTCCAC
FSHRF： ATGTGTTCTCCAACCTACCCA145
R： GCTGGCAAGTGTTTAATGCCTG
18sF：CGCCGCTAGAGGTGAAATTC101
R：CGAACCTCCGACTTTCGTTCT
), ArticleFig(id=1198602021994595248, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198602007167730254, language=CN, label=表2, caption=

qRT-PCR引物序列

, figureFileSmall=null, figureFileBig=null, tableContent=
基因引物序列(5'-3')目的片段(bp)
VEGFF：GATCATGCGGATCAAACCTC105
R：AATGCTTTCTCCGCTCTGAA
KDRF：CTGGAGCCTACAAGTGCTCG179
R：GAGGTTTGAAATCGACCCTCG
StARF：ATGTTCCTCGCTACGTTCAAG122
R：CCCAGTGCTCTCCAGTTGAG
CYP11A1F：ACACTGAGACTCCACCCCAT137
R：CTCGACCCATGGCAAAGCTA
3β-HSDF：AGCTCTGGACAAAGTATTCCGA234
R：GCCTCCAATAGGTTCTGGGT
INHBBF：AACTGCTCCCCTATGTCCTGG127
R：CCGCTACGTTTCAGGTCCAC
FSHRF： ATGTGTTCTCCAACCTACCCA145
R： GCTGGCAAGTGTTTAATGCCTG
18sF：CGCCGCTAGAGGTGAAATTC101
R：CGAACCTCCGACTTTCGTTCT
), ArticleFig(id=1198602022095258547, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198602007167730254, language=EN, label=Tab.3, caption=

Selected related differential genes in ovarian tissue in mice

, figureFileSmall=null, figureFileBig=null, tableContent=
基因编号差异倍数(Dox-/Dox+)P基因名称
ENSMUSG000000315740.015342889<0.0001StAR
ENSMUSG000000239510.079371166<0.0001VEGF
ENSMUSG000000323230.180817292<0.0001CYP11A1
ENSMUSG000000278710.7014817730.021563β-HSD
ENSMUSG000000629600.3848318490.00110KDR
ENSMUSG0000003703510.53237967<0.0001INHBB
ENSMUSG000000329372.7652525220.00082FSHR
), ArticleFig(id=1198602022200116152, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1198602007167730254, language=CN, label=表3, caption=

小鼠卵巢组织中筛选出的相关差异基因

, figureFileSmall=null, figureFileBig=null, tableContent=
基因编号差异倍数(Dox-/Dox+)P基因名称
ENSMUSG000000315740.015342889<0.0001StAR
ENSMUSG000000239510.079371166<0.0001VEGF
ENSMUSG000000323230.180817292<0.0001CYP11A1
ENSMUSG000000278710.7014817730.021563β-HSD
ENSMUSG000000629600.3848318490.00110KDR
ENSMUSG0000003703510.53237967<0.0001INHBB
ENSMUSG000000329372.7652525220.00082FSHR
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VEGF对小鼠卵巢类固醇合成相关基因表达的影响及其机制
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张智慧 1, 2 , 高鸿霞 2 , 王国庆 2 , 侯巍 2 , 邹畅 2 , 芦小单 1, 2, *
解放军医学杂志 | 基础研究 2024,49(6): 679-685
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解放军医学杂志 | 基础研究 2024, 49(6): 679-685
VEGF对小鼠卵巢类固醇合成相关基因表达的影响及其机制
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张智慧1, 2, 高鸿霞2, 王国庆2, 侯巍2, 邹畅2, 芦小单1, 2, *
作者信息
  • 1吉林省人民医院精准分子医学中心，吉林长春 130000
  • 2北华大学医学技术学院，吉林省吉林市 132000

    • 张智慧，硕士研究生，主要从事临床检验诊断方面的研究

通讯作者:

芦小单，E-mail：
Effect of VEGF on the expression of genes related to ovarian steroid synthesis in mice and its mechanism
Zhi-Hui Zhang1, 2, Hong-Xia Gao2, Guo-Qing Wang2, Wei Hou2, Chang Zou2, Xiao-Dan Lu1, 2, *
Affiliations
  • 1Precision Medicine Center, Jilin Province People's Hospital, Changchun, Jilin 130000, China
  • 2School of Medical Technology, Beihua University, Jilin, Jilin 132000, China
出版时间: 2024-06-28 doi: 10.11855/j.issn.0577-7402.2633.2024.0229
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摘要
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目的 探讨血管内皮生长因子(VEGF)对小鼠卵巢类固醇合成相关基因表达的影响及其机制。方法 利用四环素可逆调节VEGF表达的转基因小鼠模型，采用聚合酶链反应(PCR)法鉴定小鼠基因型，通过喂食强力霉素将20只小鼠分为VEGF表达正常组(Dox+)与VEGF表达抑制组(Dox-)(n=10)。采用Western blotting检测卵巢组织中VEGF蛋白的表达情况；荧光定量PCR检测VEGF、VEGF受体2(KDR)及已知在卵泡发育中发挥作用的基因卵泡刺激素(FSH)、抑制素B(INHBB) mRNA的表达情况。HE染色观察卵巢组织的变化。取小鼠卵巢组织提取总RNA进行转录组测序，并通过FPKM、log2FC值分析相关差异基因。结果 与Dox+组比较，Dox-组VEGF mRNA和蛋白水平明显降低，KDR mRNA水平明显降低(P<0.05)。HE染色结果显示，与Dox+组比较，Dox-组卵泡发育障碍，并出现闭锁卵泡。根据测序结果分析筛选出两组小鼠的卵泡发育相关基因、类固醇合成相关基因具有明显差异(P<0.05)；富集分析发现小鼠卵巢中VEGF主要参与调控卵巢类固醇生成等通路。荧光定量PCR结果显示，与Dox+组相比，Dox-组小鼠卵巢组织中卵泡发育相关基因(INHBB、FSHR)明显上调(P<0.05)，类固醇合成的关键基因(StAR、CYP11A1、3β-HSD)明显下调(P<0.05)，定量结果与测序结果基本一致。结论 VEGF抑制可使小鼠卵泡发育障碍，其可能的机制是通过下调卵巢类固醇合成相关基因FSH、INHBB的表达从而阻碍胆固醇代谢来实现的。

血管内皮生长因子  /  卵泡发育  /  性类固醇激素  /  转录组测序

Objective To investigate the effect of vascular endothelial growth factor (VEGF) on the expression of genes related to ovarian steroid synthesis in mice and its underlying mechanism. Methods A transgenic mouse model with tetracycline -reversible regulation of VEGF expression was used, and the genotype of mice was identified by polymerase chain reaction (PCR). Twenty mice were divided into normal VEGF expression group (Dox+, n=10) and VEGF expression inhibition group (Dox-, n=10) by feeding them doxycycline. Western blotting was used to detect the expression of VEGF protein in ovarian tissues. Fluorescence quantitative PCR was used to detect the mRNA expression of VEGF, KDR and genes known to play roles in follicle development, such as follicle-stimulating hormone (FSH) and inhibin B (INHBB). HE staining was used to observe changes in ovarian tissue. Total RNA was extracted from mouse ovarian tissues for transcriptome sequencing, and the relevant differential genes were analyzed by FPKM and log2FC values. Results Compared with the Dox+ group, the mRNA and protein levels of VEGF in the Dox- group significantly reduced, and the mRNA levels of KDR also significantly decreased (P<0.05). HE staining results showed that compared with the Dox+ group, follicular development was impaired and atresia follicles appeared in the Dox- group. Sequencing analysis identified that significant differences in follicular development-related genes and steroid synthesis-related genes between the two groups (P<0.05). Enrichment analysis showed that VEGF in mouse ovaries mainly regulates ovarian steroidogenesis and other pathways. Fluorescence quantitative PCR results demonstrated that compared with the Dox+ group, the follicular development-related genes (INHBB and FSHR) in the ovarian tissues of the Dox- group were significantly up-regulated (P<0.05), whereas the key genes of steroid synthesis (StAR, CYP11A1, 3β-HSD) were significantly down-regulated (P<0.05).The quantitative results were basically consistent with the sequencing results. Conclusion Mice with inhibited VEGF exhibited ovarian follicular dysplasia, potentially due to the mechanism whereby VEGF inhibition downregulated the expression of genes associated with steroid synthesis, such as FSH and INHBB, thereby obstructing cholesterol metabolism.

vascular endothelial growth factor  /  follicular development  /  sexual steroid hormones  /  transcriptome sequencing
张智慧, 高鸿霞, 王国庆, 侯巍, 邹畅, 芦小单. VEGF对小鼠卵巢类固醇合成相关基因表达的影响及其机制. 解放军医学杂志, 2024 , 49 (6) : 679 -685 . DOI: 10.11855/j.issn.0577-7402.2633.2024.0229
Zhi-Hui Zhang, Hong-Xia Gao, Guo-Qing Wang, Wei Hou, Chang Zou, Xiao-Dan Lu. Effect of VEGF on the expression of genes related to ovarian steroid synthesis in mice and its mechanism[J]. Medical Journal of Chinese People’s Liberation Army, 2024 , 49 (6) : 679 -685 . DOI: 10.11855/j.issn.0577-7402.2633.2024.0229
正文
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血管内皮生长因子(vascular endothelial growth factor，VEGF)作为血管生成过程的主要成员之一[1]，可通过与其受体(vascular endothelial growth factor receptor 2，VEGFR2，又名KDR)结合参与卵泡的血管化及氧合作用，进而参与卵母细胞的成熟和胚胎发育过程[2-3]；这些新生的血管保证并增加了促性腺激素、生长因子、氧、类固醇激素和其他促卵泡生长物质的供应[4-6]。随着研究的逐渐深入，越来越多的证据表明，血管生成可通过促卵泡生长物质的供应成为卵泡发育和闭锁的关键调节因素，并在多个物种(如鸡[7]、猪[8]和牛[9])中得到证实。本研究利用四环素可逆调节系统抑制VEGF表达的转基因小鼠模型(VEGFtetO/tetO：βAKtg/tg)[10]，分析类固醇激素合成相关基因在卵巢中的表达情况，并探讨相关机制，旨在揭示VEGF与类固醇激素合成调节的关系，为其发挥卵泡发育调节作用提供参考。
1 材料与方法
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1.1 主要试剂
TransZol购自北京全式金生物技术有限公司；琼脂糖购自北京达科为生物技术有限公司；MinuteTM动物组织总蛋白提取试剂盒购自北京Invent生物技术有限公司；BCA蛋白浓度测定试剂盒、10×蛋白上样缓冲液、DL2000 DNA Marker、PCR试剂盒、反转录试剂盒、荧光定量PCR反应试剂盒、ECL化学发光试剂盒购自南京诺唯赞生物科技股份有限公司；VEGF抗体(货号：ab183100)购自英国Abcam公司；GAPDH抗体(货号：sc-166574)购自美国Santa Cruz公司；HE染色试剂盒购自北京索莱宝科技有限公司。
1.2 实验动物及分组
四环素调节VEGF可逆抑制小鼠模型[10]由东北师范大学郑耀武教授惠赠，饲养于东北师范大学转基因动物实验中心SPF级动物房独立通气(individual ventilated cages，IVC)笼中，恒温22 ℃，维持12 h的光暗循环，自由饮食。本研究获吉林省人民医院医学伦理委员会审批(2022001)，实验过程符合国家及单位有关实验动物的管理及使用规定。将20只12周龄雌性小鼠分为VEGF正常表达组(Dox+)和VEGF抑制表达组(Dox-)，每组10只。所有小鼠选用的基因型为VEGFtetO/tetO：βAKtg/tg，喂食四环素条件下度过哺乳期后即可分为Dox+组和Dox-组用于实验。
1.3 小鼠基因型鉴定
剪取出生两周龄小鼠鼠尾约0.5 cm置于1.5 ml EP管中，每管中加入100 μl 鼠尾消化液(GNTK，每1 ml GNTK加入8 μl蛋白酶K)，于56 ℃水浴锅中消化过夜。第2天将消化好的鼠尾充分混匀后沸水浴10 min使蛋白酶失去活性从而终止消化，12 000 r/min离心1 min后进行PCR鉴定，取上清用作PCR反应的模板进行PCR反应。PCR扩增反应体系根据试剂盒使用说明书，按照25 μl反应体系进行扩增反应，分别加入Taq mix 12.5 μl、F引物(10 μmol/L)1 μl、R引物(10 μmol/L)1 μl、DNA模板2 μl，再加入双蒸水补足至25 μl。扩增条件：94 ℃预变性5 min；94 ℃ 30 s、54 ℃ 30 s、72 ℃ 1 min，30个循环；72 ℃ 10 min后回温至4 ℃。利用琼脂糖凝胶电泳鉴定PCR产物，引物序列见表1。
1.4 实时荧光定量PCR测定卵巢组织中相关基因的表达
以Trizol法从小鼠卵巢中提取总RNA。按照说明书使用HiScript RT-PCR试剂盒对纯化的1 μg RNA进行反转录。根据ChamQ Universal SYBR qPCR Master Mix试剂盒说明书，以20 μl反应体系进行扩增反应，分别加入：2×ChamQ SYBR qPCR Master Mix 10 μl、F引物(10 μmol/L)0.4 μl、R引物(10 μmol/L)0.4 μl、cDNA 2 μl，加入双蒸水补足至20 μl。qRT-PCR分析在7500 fast real-time PCR系统上进行，PCR条件为：98 ℃ 变性5 min；60 ℃ 退火 30 s，72 ℃ 延伸1 min，40个循环。以18s为内参照，使用2-ΔΔCt法计算相对表达量。引物序列见表2。
1.5 Western blotting检测小鼠卵巢组织中VEGF蛋白的表达
取适量小鼠卵巢组织，按照MinuteTM动物组织总蛋白提取试剂盒说明书提取组织总蛋白。BCA法测定总蛋白浓度，取20 μg/孔总蛋白进行10%十二烷基磺酸钠-聚丙烯酰胺凝胶(SDS-PAGE)电泳，PVDF膜湿转2 h，随后用5%脱脂奶粉室温封闭1 h。VEGF、GAPDH一抗在4 ℃孵育过夜(TBS缓冲液=1:1000)，次日用TBST洗涤3次，5 min/次，在室温下与HRP标记的二抗(TBS缓冲液=1:2000)孵育2 h。以GAPDH为内参照，通过ECL化学发光检测试剂曝光显影，重复3次。使用ImageJ软件分析蛋白条带灰度值，计算目的蛋白/GAPDH的灰度值，所得结果即为目的蛋白相对表达量。
1.6 HE染色观察卵巢组织形态学变化
卵巢组织固定24 h后，经70%~100%乙醇梯度脱水，石蜡包埋、切片(厚度5 μm)。切片经二甲苯脱蜡及由高到低梯度浓度(100%~70%)乙醇水洗后，苏木精染色7 min、水洗3 min，重复4次；分化液分化30 s、自来水浸泡10 min、伊红染液染色2 min、水洗3 min，重复4次；经常规脱水晾干后用中性树胶封片，镜检，观察卵巢形态学变化。
1.7 RNA文库构建及测序
提取的RNA经0.8%的琼脂糖凝胶电泳检测RNA降解程度以及是否存在污染。文库构建及测序均由中科基因生物科技有限公司完成。具体步骤如下：将所提RNA以带有Oligo(dT)的磁珠富集成含polyA尾的mRNA；随后加入片段化酶将mRNA片段化后进行反转录，再合成cDNA双链形成双链DNA；将合成的双链DNA末端修复并5'端磷酸化，3'端形成突出1个“A”的黏末端，再连接1个3'端有凸出“T”的测序接头；连接产物通过特异引物进行PCR扩增；并使用AMPure XP beads纯化PCR产物，即得到最终文库。对构建好的文库进行质检，合格后测序。
1.8 生物信息学分析
通过HISAT2软件将测序获得的核苷酸长度(reads)比对至小鼠全基因组，使用edgeR软件包计算基因差异表达情况，根据差异表达倍数(fold change，FC)、P值和表达量(FPKM)筛选差异表达的mRNA(|log2FC|>1，P<0.05且FPKM>0.5)。
1.9 统计学处理
采用SPSS 20.0软件进行统计分析。计量资料均以$\bar{x}±s$表示，组间比较采用两独立样本t检验。P<0.05为差异有统计学意义。
2 结果
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2.1 转基因小鼠模型筛选
实验筛选出同时含有VEGFtetO及tetR-Krab目的片段的1-10、12-15号双转基因小鼠(图1A)，在喂食常规鼠粮时，四环素阻遏蛋白融合蛋白(tetracycline repressor，tetR-Krab)与四环素操纵子(tetracycline operator，tetO)结合，抑制了VEGF的表达；当鼠粮中含有强力霉素(doxycycline，Dox)时，由于Dox与tetR的结合能力更强，构型因此发生改变，导致tetR-Krab从tetO上脱落，最终实现VEGF的正常表达(图1B)。
2.2 VEGF在小鼠卵巢组织中的表达情况
qRT-PCR结果显示，与Dox+组小鼠比较，Dox-组小鼠VEGF mRNA水平也明显降低(P<0.05，图2A)。Western blotting检测结果显示，与Dox+组小鼠比较，Dox-组小鼠卵巢组织中的VEGF蛋白表达水平明显降低(P<0.01，图2B)。
2.3 HE染色观察小鼠卵巢组织的形态学变化
HE染色结果显示，与Dox+组比较，Dox-组卵泡膜增殖减少，卵泡核浓缩，卵泡塌陷，轮廓曲折，卵泡发育障碍开始发生闭锁，黄体膨大，卵巢基质和间质腺出现增生现象(图3)。
2.4 生物信息学分析
对Dox+组和Dox-组小鼠卵巢组织进行转录组学分析，得到VEGF及其受体KDR、与类固醇合成(StAR、CYP11A1、3β-HSD)和调节卵泡刺激素(FSH)相关基因(INHBB、FSHR)的相对表达趋势，具体结果见表3。将筛选出的所有差异基因进行KEGG通路富集分析，结果显示，差异基因主要富集于过氧化物酶体增殖激活受体(peroxisome proliferators-activated receptors，PPAR)、卵巢类固醇生成、凝血与补体级联反应、类固醇激素生物合成等信号通路(图4)。qRT-PCR检测结果显示，KDR、StAR、CYP11A1、3β-HSD mRNA水平均明显降低(P<0.05或P<0.01)，INHBB、FSHR mRNA水平明显升高(P<0.05或P<0.001)(图5)，与测序结果基本一致。
3 讨论
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卵巢血管生成受促血管生成因子和抗血管生成因子之间的平衡调节，是一个复杂的过程[11]。在正常生理条件下，血管生成是一个严格调控的过程，卵巢作为成年动物中少数经历重复血管形成、成熟和退化的组织之一，为血管生成过程研究提供了独特的机会[12]。卵巢内的卵泡发生、排卵和黄体形成等生理过程中，营养物质及类固醇激素均需经血管从卵巢运输至卵泡，若营养物质和激素供给不足，卵泡更倾向于发育为闭锁状态，因此，任何影响正常血管生成过程的因素均可能导致卵巢功能障碍，甚至不孕[13]。VEGF作为调节卵巢血管生成的关键因子之一，可将原始卵泡募集到生长的卵泡池，且通过血管依赖性和血管非依赖性机制成为初级和晚期卵泡的存活因子[14]。体内研究表明，抑制血管内皮生长因子A和KDR可抑制卵泡发育或阻止排卵[15]。充足的血管供应是优势卵泡选择和成熟的限速步骤，而血液供应不足时，卵泡生长则受限、闭锁，且性类固醇生成减少[16]。本研究通过形态学观察发现，VEGF受到抑制会使卵泡发育障碍，卵泡膜的增殖明显减少，最终导致卵巢颗粒细胞的增殖和性类固醇产生减少，提示VEGF在卵泡发育中发挥重要作用，但其具体机制尚不明确。本研究还通过高通量转录组测序技术对可逆抑制VEGF表达的转基因小鼠模型进行了生物信息学分析，明确了VEGF在卵巢发育中的调控作用，差异基因主要富集到PPAR、卵巢类固醇生成、凝血与补体级联反应、类固醇激素生物合成等信号通路。
作为雌性哺乳动物的性腺，卵巢的主要功能是排卵及分泌类固醇激素，即发挥卵巢的生殖功能和内分泌功能[17]。卵泡合成性类固醇激素的过程复杂，需要多种酶的参与。首先，胆固醇作为合成类固醇激素的前体物质，可通过脂蛋白受体转运到卵泡的膜细胞中，也可以从头合成。类固醇生成StAR将胆固醇从细胞质内化到线粒体中，这是类固醇激素合成的初始步骤。随后，胆固醇在CYP11A1的作用下被转化为孕烯醇酮，后者从线粒体转运至内质网后，分别通过3β-HSD或17α-羟化酶-17，20desmolase (cytochrome P450 family 17 subfamily A member 1，CYP17A1)转化为孕酮或脱氢表雄酮。最后，孕酮和脱氢表雄酮分别通过CYP17A1或3β-HSD转化为雄激素雄烯二酮[18]。雄烯二酮可通过17β-羟基类固醇脱氢酶(17β-hydroxysteroid dehydrogenases，17β-HSD)或芳香酶(cytochrome P450 family 19 subfamily A member 1，CYP19A1)转化为睾酮或雌酮[19]。睾酮和雌酮在卵巢分别通过CYP19A1或17β-HSD转化为最有效的雌激素雌二醇(E2)[20]，具体过程见图6。E2产生后即可被运输到其他靶组织发挥各种作用。有研究发现，卵泡液中VEGF水平对卵母细胞成熟有促进作用，提示卵泡液中VEGF与E2水平升高存在相关性[21]。因此，本研究通过高通量转录组测序技术分析初步认为，VEGF对卵巢卵泡发育的影响可能是通过下调重要的卵巢类固醇合成相关基因的表达从而阻碍胆固醇代谢来实现的。
卵巢类固醇的生成受垂体促性腺激素、FSH和促黄体生成素的调节。正常情况下，女性生理周期中一定水平的INHBB可适时抑制FSH的分泌，这是卵泡优势化过程的重要环节[22]。有研究发现，多囊卵巢综合征患者卵泡内环境发生改变，INHBB水平升高并过度抑制垂体FSH的合成与分泌，使患者卵泡内的FSH水平降低，从而影响性类固醇激素的生成，使卵泡发育发生障碍，且卵泡募集和优势卵泡形成受阻，窦卵泡群集，无卵泡成熟，最终导致排卵障碍[23]。本研究利用可逆抑制VEGF小鼠模型发现，抑制VEGF会导致INHBB、FSHR高表达，从而抑制小鼠卵巢中卵泡的生长发育，且与类固醇激素的合成密切相关。以上结果提示INHBB、FSHR、StAR、CYP11A1、3β-HSD基因可能是VEGF参与调控小鼠卵巢卵泡发育的重要基因。
卵巢产生正常水平的性类固醇激素的能力对于生殖和身体健康极其重要。低水平的性类固醇激素与多种疾病有关，包括自身免疫性疾病、不孕症、抑郁症、骨质疏松症和心血管疾病等[24]；高水平的性类固醇激素则会增加乳腺癌和结肠癌的风险[25-26]。
综上所述，本研究初步证实VEGF对卵巢卵泡发育的影响可能是通过调节重要的卵巢类固醇合成相关通路，从而阻碍胆固醇代谢实现的，因此，研究VEGF与类固醇激素合成调节的关系对由VEGF引起的类固醇激素合成异常的相关疾病，尤其是生殖方面的疾病有重要意义。但本研究尚存在不足之处：转录组测序未设置生物学重复，在一定程度上削弱了数据结果的可靠性；未进一步在蛋白水平阐明VEGF对卵巢类固醇生成等通路的调控作用。因此，后续应针对上述不足进一步探索VEGF调控卵泡发育的机制，为防治此类疾病的相关药物研发提供合理的科学依据。
基金
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  • 吉林省自然科学基金(20240101007JC)
  • 吉林省自然科学基金项目(YDZJ202201ZYTS148)
  • 吉林省科技厅创新团队项目(20220508080RC)
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2024年第49卷第6期
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doi: 10.11855/j.issn.0577-7402.2633.2024.0229
  • 接收时间：2022-12-26
  • 首发时间：2025-11-21
  • 出版时间：2024-06-28
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  • 收稿日期：2022-12-26
  • 录用日期：2023-03-14
基金
Natural Science Foundation of Jilin Province(20240101007JC)
吉林省自然科学基金(20240101007JC)
Natural Science Foundation of Jilin Province(YDZJ202201ZYTS148)
吉林省自然科学基金项目(YDZJ202201ZYTS148)
Jilin Provincial Science and Technology Department Innovation Team Project(20220508080RC)
吉林省科技厅创新团队项目(20220508080RC)
作者信息
    1吉林省人民医院精准分子医学中心，吉林长春 130000
    2北华大学医学技术学院，吉林省吉林市 132000

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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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