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Article(id=1259888460442231321, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1259888457367806489, articleNumber=null, orderNo=null, doi=10.13343/j.cnki.wsxb.20260024, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1767974400000, receivedDateStr=2026-01-10, revisedDate=null, revisedDateStr=null, acceptedDate=1770739200000, acceptedDateStr=2026-02-11, onlineDate=1778310416565, onlineDateStr=2026-05-09, pubDate=1777824000000, pubDateStr=2026-05-04, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1778310416565, onlineIssueDateStr=2026-05-09, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1778310416565, creator=13701087609, updateTime=1778310416565, updator=13701087609, issue=Issue{id=1259888457367806489, tenantId=1146029695717560320, journalId=1192105938417971205, year='2026', volume='66', issue='5', pageStart='2031', pageEnd='2556', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=0, articleOrder=1, issueType=-1, specialIssue=null, createTime=1778310415832, creator=13701087609, updateTime=1778320153326, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1259929299465921482, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1259888457367806489, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1259929299465921483, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1259888457367806489, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=2321, endPage=2338, ext={EN=ArticleExt(id=1259888460861661723, articleId=1259888460442231321, tenantId=1146029695717560320, journalId=1192105938417971205, language=EN, title=n-butanol extract of Pulsatilla decoction alleviates vulvovaginal candidiasis by inducing autophagy and inhibiting apoptosis, columnId=1192149543992045670, journalTitle=Acta Microbiologica Sinica, columnName=Research Article, runingTitle=null, highlight=null, articleAbstract=

Vulvovaginal candidiasis (VVC) is a prevalent fungal infection affecting the female reproductive tract. Although conventional therapeutic approaches for VVC are relatively well-established, they still exhibit certain limitations. Pulsatilla decoction, a classic traditional Chinese medicine formula, has demonstrated significant clinical efficacy in the treatment of VVC. However, its precise mechanism of action remains incompletely elucidated. Objective To clarify the therapeutic mechanism of the n-butanol extract of Pulsatilla decoction (BEPD) on VVC through network pharmacology and animal experiments. Methods A mouse model of VVC was established and the therapeutic effect of BEPD on VVC was evaluated. Network pharmacology was employed to screen the potential signaling pathways of BEPD on VVC. Western blotting, immunofluorescence, immunohistochemistry, and real-time fluorescence quantitative PCR were employed to measure the changes in autophagy, apoptosis, and related pathway proteins in the vaginal mucosa of mice. Results Network pharmacology analysis identified PIK3R1 and AKT1 as key targets of Pulsatilla decoction in exerting antifungal activity against VVC. KEGG pathway enrichment analysis indicated that Pulsatilla decoction exerted its therapeutic effects on VVC by regulating the PI3K-Akt signaling pathway. Animal experiments confirmed that compared with the VVC model group, the BEPD treatment down-regulated the expression of PI3K, p-Akt, and p-mTOR, significantly up-regulated the expression of autophagy-related proteins LC3B and ATG5, significantly inhibited the expression of apoptosis-related proteins Bax and Cleaved-Caspase-3, and significantly promoted the expression of anti-apoptosis-related protein Bcl-2. Conclusion BEPD may promote autophagy and inhibit apoptosis of vaginal epithelial cells by inhibiting the PI3K-Akt-mTOR signaling pathway, thereby restoring the homeostasis of the vaginal mucosal epithelial barrier and alleviating VVC.

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E-mail: WANG Tianming, ;
WANG Changzhong,
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外阴阴道念珠菌病(vulvovaginal candidiasis, VVC)是女性生殖道常见的真菌感染性疾病。尽管针对VVC的传统治疗手段已相对成熟，但仍存在一定局限性。白头翁汤作为中国医学的经典方剂在临床上已被证实对VVC具有明确疗效，但其具体作用机制尚未完全阐明。 目的 通过网络药理学及动物实验阐明中药白头翁汤正丁醇提取物(n-butanol extract of Pulsatilla decoction, BEPD)对VVC的作用机制。 方法 构建VVC小鼠模型，评估BEPD对VVC的疗效；通过网络药理学筛选出BEPD对VVC潜在的作用信号通路，并采用蛋白印迹法、免疫荧光、免疫组化、实时荧光定量PCR检测小鼠阴道黏膜组织中自噬、凋亡及其相关通路蛋白的变化水平。 结果 网络药理学分析显示，白头翁汤发挥抗真菌活性、治疗VVC的关键靶点包括PIK3RA和AKT1等；KEGG分析结果表明，白头翁汤可能通过调控PI3K-Akt信号通路发挥治疗VVC的作用。动物实验证实，相对于VVC模型组，BEPD治疗后，PI3K、p-Akt、p-mTOR蛋白表达下降，自噬相关蛋白LC3B和ATG5表达显著增加，凋亡相关蛋白Bax和Cleaved-Caspase-3的表达则明显下调，抗凋亡相关蛋白Bcl-2表达明显上调。 结论 BEPD可能通过抑制PI3K-Akt-mTOR信号通路促进阴道上皮细胞自噬并抑制凋亡，从而恢复阴道黏膜上皮屏障稳态，缓解VVC。

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作者贡献声明

邱薇：实验操作、数据收集和处理；李璨：提供技术支持；吴惠：协助实验操作；施高翔：参与论文讨论；吴大强：数据分析；汪天明：研究构思和设计；汪长中：论文撰写和修改。

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A: Local vaginal signs of VVC mice; B: Fungal load in vaginal secretions; C: Morphology of C. albicans in vaginal secretions (200×, scale bar=100 µm); D: HE staining of vaginal tissues (200×, scale bar=100 µm); E: IL-1β level; F: TNF-α level; G: LDH level; H: WB bands; I-K: Quantification of ZO-1, Claudin-1 and Occludin in the vagina of mice. Compared to the control group, *** P<0.001; Compared to the VVC model group, #P<0.05, ##P<0.01, ###P<0.001., figureFileSmall=EUrNI4bzZmDKTMmoAJJFyA==, figureFileBig=t2/boQLW84sqbiNxIAShdg==, tableContent=null), ArticleFig(id=1259928470151356673, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1259888460442231321, language=CN, label=图2, caption=BEPD缓解VVC小鼠阴道炎症和黏膜屏障损伤, figureFileSmall=EUrNI4bzZmDKTMmoAJJFyA==, figureFileBig=t2/boQLW84sqbiNxIAShdg==, tableContent=null), ArticleFig(id=1259928471061520649, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1259888460442231321, language=EN, label=Figure 3, caption=Potential mechanism of BEPD in treating VVC based on network pharmacology analysis. A: Venn diagram of “drug-disease” intersection gene targets; B: PPI network; C: GO enrichment analysis; D: KEGG enrichment analysis., figureFileSmall=2QB6G+Zs+pd1oLfEzDnptw==, figureFileBig=z3b55Zj2h7c9PVWBu0z75g==, tableContent=null), ArticleFig(id=1259928472688910615, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1259888460442231321, language=CN, label=图3, caption=基于网络药理学分析BEPD治疗VVC的潜在机制, figureFileSmall=2QB6G+Zs+pd1oLfEzDnptw==, figureFileBig=z3b55Zj2h7c9PVWBu0z75g==, tableContent=null), ArticleFig(id=1259928474010116387, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1259888460442231321, language=EN, label=Figure 4, caption=BEPD-induced activation of autophagy in vaginal epithelial cells of VVC mice. A, B: Immunohistochemistry and quantification of LC3B in the vagina of mice (200×, scale bar=100 µm); C, D: Immunofluorescence and quantification of ATG5 in the vagina of mice (200×, scale bar=100 µm); E-G: WB bands and quantification of LC3B Ⅰ, LC3B Ⅱ, and ATG5 in the vagina of mice; H and I: mRNA expression of ATG5 and LC3B in the vagina of mice. Compared to the control group, *: P<0.05, ***: P<0.001; Compared to the VVC model group, #P<0.05, ##P<0.01, ###P<0.001., figureFileSmall=8Nz4WCkL6H5x61wJmvTRzg==, figureFileBig=Wn72ZnBJOw6GrCWz7EZZLw==, tableContent=null), ArticleFig(id=1259928475192910128, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1259888460442231321, language=CN, label=图4, caption=BEPD诱导VVC小鼠阴道上皮细胞自噬的激活, figureFileSmall=8Nz4WCkL6H5x61wJmvTRzg==, figureFileBig=Wn72ZnBJOw6GrCWz7EZZLw==, tableContent=null), ArticleFig(id=1259928476430229819, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1259888460442231321, language=EN, label=Figure 5, caption=BEPD inhibits apoptosis of vaginal epithelial cells in VVC mice. A, B: Fluorescence and quantification of Cleaved-Caspase-3 in the vagina of mice (200×, scale bar=100 µm); C-F: WB bands and quantification of Bax, Bcl-2, and Cleaved-Caspase-3 in the vagina of mice; G-I: mRNA expression of Bax, Bcl-2, and Caspase-3 in the vagina of mice. Compared to the control group, ** P<0.01, *** P<0.001; Compared to the VVC model group, # P<0.05, ##P<0.01, ###P<0.001., figureFileSmall=+AX2l8ylty9OLI7/xPVruA==, figureFileBig=7Uim49xvcMZc9pDOAljJeg==, tableContent=null), ArticleFig(id=1259928480683254090, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1259888460442231321, language=CN, label=图5, caption=BEPD抑制VVC小鼠阴道上皮细胞凋亡, figureFileSmall=+AX2l8ylty9OLI7/xPVruA==, figureFileBig=7Uim49xvcMZc9pDOAljJeg==, tableContent=null), ArticleFig(id=1259928483153699152, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1259888460442231321, language=EN, label=Figure 6, caption=BEPD inhibits the activation of the PI3K/Akt/mTOR signaling pathway. A-F: WB bands and quantification of PI3K, p-Akt, Akt, p-mTOR, and mTOR in the vagina of mice; G, H: mRNA expression of Akt and mTOR in the vagina of mice. Compared to the control group, ** P<0.01, *** P<0.001; Compared to the VVC model group, #P<0.05, ##P<0.01, ###P<0.001., figureFileSmall=0wXjggjOjXS9wCBjveyuyw==, figureFileBig=EU79KfT9TGxG08eudcEYfw==, tableContent=null), ArticleFig(id=1259928484084834655, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1259888460442231321, language=CN, label=图6, caption=BEPD抑制PI3K/Akt/mTOR信号通路的激活, figureFileSmall=0wXjggjOjXS9wCBjveyuyw==, figureFileBig=EU79KfT9TGxG08eudcEYfw==, tableContent=null), ArticleFig(id=1259928485645115750, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1259888460442231321, language=EN, label=Table 1, caption=

Primers sequences used for RT-qPCR

, figureFileSmall=null, figureFileBig=null, tableContent=
GenePrimer directionPrimer sequences (5′→3′)
GAPDH-mouseForwardCATCACTGCCACCCAGAAGACTG
ReverseATGCCAGTGAGCTTCCCGTTCAG
PI3K-mouseForwardCAAACCACCCAAGCCCACTACT
ReverseCCATCAGCAGTGTCTCGGAGTT
AKT-mouseForwardGGACTACTTGCACTCCGAGAAG
ReverseCATAGTGGCACCGTCCTTGATC
mTOR-mouseForwardAGAAGGGTCTCCAAGGACGACT
ReverseGCAGGACACAAAGGCAGCATTG
LC3B-mouseForwardGTCCTGGACAAGACCAAGTTCC
ReverseCCATTCACCAGGAGGAAGAAGG
ATG5-mouseForwardCTTGCATCAAGTTCAGCTCTTCC
ReverseAAGTGAGCCTCAACCGCATCCT
CASP3-mouseForwardGGAGTCTGACTGGAAAGCCGAA
ReverseCTTCTGGCAAGCCATCTCCTCA
BAX-mouseForwardAGGATGCGTCCACCAAGAAGCT
ReverseTCCGTGTCCACGTCAGCAATCA
Bcl-2-mouseForwardCCTGTGGATGACTGAGTACCTG
ReverseAGCCAGGAGAAATCAAACAGAGG
), ArticleFig(id=1259928487834542452, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1259888460442231321, language=CN, label=表1, caption=

RT-qRCR所需的引物

, figureFileSmall=null, figureFileBig=null, tableContent=
GenePrimer directionPrimer sequences (5′→3′)
GAPDH-mouseForwardCATCACTGCCACCCAGAAGACTG
ReverseATGCCAGTGAGCTTCCCGTTCAG
PI3K-mouseForwardCAAACCACCCAAGCCCACTACT
ReverseCCATCAGCAGTGTCTCGGAGTT
AKT-mouseForwardGGACTACTTGCACTCCGAGAAG
ReverseCATAGTGGCACCGTCCTTGATC
mTOR-mouseForwardAGAAGGGTCTCCAAGGACGACT
ReverseGCAGGACACAAAGGCAGCATTG
LC3B-mouseForwardGTCCTGGACAAGACCAAGTTCC
ReverseCCATTCACCAGGAGGAAGAAGG
ATG5-mouseForwardCTTGCATCAAGTTCAGCTCTTCC
ReverseAAGTGAGCCTCAACCGCATCCT
CASP3-mouseForwardGGAGTCTGACTGGAAAGCCGAA
ReverseCTTCTGGCAAGCCATCTCCTCA
BAX-mouseForwardAGGATGCGTCCACCAAGAAGCT
ReverseTCCGTGTCCACGTCAGCAATCA
Bcl-2-mouseForwardCCTGTGGATGACTGAGTACCTG
ReverseAGCCAGGAGAAATCAAACAGAGG
), ArticleFig(id=1259928490258850173, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1259888460442231321, language=EN, label=Table 2, caption=

Information on the effective components of compound Pulsatilla decoction

, figureFileSmall=null, figureFileBig=null, tableContent=
Mol IDMolecular nameHerb
MOL0019843beta, 23-dihydroxy-lup-20(29)-ene-28-O-alpha-L-rhamnopyranosyl-(1-4)-beta-D-glucopyranosyl(1-6)-beta-D-glucopyranoside_qtPulsatilla Chinensis (Bunge) Regel
MOL001978AureusidinPulsatilla Chinensis (Bunge) Regel
MOL000358Beta-sitosterolPulsatilla Chinensis (Bunge) Regel
MOL000354IsorhamnetinPulsatilla Chinensis (Bunge) Regel
MOL001979LANPulsatilla Chinensis (Bunge) Regel
MOL000211MairinPulsatilla Chinensis (Bunge) Regel
MOL001971Pulchinenoside C_qtPulsatilla Chinensis (Bunge) Regel
MOL001973Sitosteryl acetatePulsatilla Chinensis (Bunge) Regel
MOL000449StigmasterolPulsatilla Chinensis (Bunge) Regel
MOL001985ZINC01615307Pulsatilla Chinensis (Bunge) Regel
MOL001987β-sitosterolPulsatilla Chinensis (Bunge) Regel
MOL001454BerberineCoptis chinensis Franch
MOL013352ObacunoneCoptis chinensis Franch
MOL002894BerberrubineCoptis chinensis Franch
MOL002897EpiberberineCoptis chinensis Franch
MOL002903(R)-canadineCoptis chinensis Franch
MOL002904BerlambineCoptis chinensis Franch
MOL002907Corchoroside A_qtCoptis chinensis Franch
MOL000622MagnograndiolideCoptis chinensis Franch
MOL000762Palmidin ACoptis chinensis Franch
MOL000785PalmatineCoptis chinensis Franch
MOL000098QuercetinCoptis chinensis Franch
MOL001458CoptisineCoptis chinensis Franch
MOL002668WorenineCoptis chinensis Franch
MOL008647MoupinamideCoptis chinensis Franch
MOL000098QuercetinPhellodendron chinense Schneid
MOL000358Beta-sitosterolPhellodendron chinense Schneid
MOL000449StigmasterolPhellodendron chinense Schneid
MOL000622MagnograndiolidePhellodendron chinense Schneid
MOL000762Palmidin APhellodendron chinense Schneid
MOL000785PalmatinePhellodendron chinense Schneid
MOL000787FumarinePhellodendron chinense Schneid
MOL000790IsocorypalminePhellodendron chinense Schneid
MOL001131Phellamurin_qtPhellodendron chinense Schneid
MOL001454BerberinePhellodendron chinense Schneid
MOL001455S-canadinePhellodendron chinense Schneid
MOL001458CoptisinePhellodendron chinense Schneid
MOL001771Poriferast-5-en-3beta-olPhellodendron chinense Schneid
MOL002636Kihadalactone APhellodendron chinense Schneid
MOL002641Phellavin_qtPhellodendron chinense Schneid
MOL002643Delta 7-stigmastenolPhellodendron chinense Schneid
MOL002644PhellopterinPhellodendron chinense Schneid
MOL002651Dehydrotanshinone II APhellodendron chinense Schneid
MOL002652Delta7-dehydrosophoraminePhellodendron chinense Schneid
MOL002656DihydroniloticinPhellodendron chinense Schneid
MOL002659Kihadanin APhellodendron chinense Schneid
MOL002660NiloticinPhellodendron chinense Schneid
MOL002662RutaecarpinePhellodendron chinense Schneid
MOL002663SkimmianinPhellodendron chinense Schneid
MOL002666ChelerythrinePhellodendron chinense Schneid
MOL002668WoreninePhellodendron chinense Schneid
MOL002670CavidinePhellodendron chinense Schneid
MOL002671Candletoxin APhellodendron chinense Schneid
MOL002672Hericenone HPhellodendron chinense Schneid
MOL002673HispidonePhellodendron chinense Schneid
MOL002894BerberrubinePhellodendron chinense Schneid
MOL005438CampesterolPhellodendron chinense Schneid
MOL006392DihydroniloticinPhellodendron chinense Schneid
MOL006401MelianonePhellodendron chinense Schneid
MOL006413PhellochinPhellodendron chinense Schneid
MOL006422ThalifendinePhellodendron chinense Schneid
MOL013352ObacunonePhellodendron chinense Schneid
MOL000358Beta-sitosterolFraxinus rhynchophylla Hance
MOL006709AIDS214634Fraxinus rhynchophylla Hance
MOL0067108-(beta-D-glucopyranosyloxy)-7-hydroxy-6-methoxy-2H-1-benzopyran-2-oneFraxinus rhynchophylla Hance
), ArticleFig(id=1259928491944960392, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1259888460442231321, language=CN, label=表2, caption=

复方白头翁汤的活性成分

, figureFileSmall=null, figureFileBig=null, tableContent=
Mol IDMolecular nameHerb
MOL0019843beta, 23-dihydroxy-lup-20(29)-ene-28-O-alpha-L-rhamnopyranosyl-(1-4)-beta-D-glucopyranosyl(1-6)-beta-D-glucopyranoside_qtPulsatilla Chinensis (Bunge) Regel
MOL001978AureusidinPulsatilla Chinensis (Bunge) Regel
MOL000358Beta-sitosterolPulsatilla Chinensis (Bunge) Regel
MOL000354IsorhamnetinPulsatilla Chinensis (Bunge) Regel
MOL001979LANPulsatilla Chinensis (Bunge) Regel
MOL000211MairinPulsatilla Chinensis (Bunge) Regel
MOL001971Pulchinenoside C_qtPulsatilla Chinensis (Bunge) Regel
MOL001973Sitosteryl acetatePulsatilla Chinensis (Bunge) Regel
MOL000449StigmasterolPulsatilla Chinensis (Bunge) Regel
MOL001985ZINC01615307Pulsatilla Chinensis (Bunge) Regel
MOL001987β-sitosterolPulsatilla Chinensis (Bunge) Regel
MOL001454BerberineCoptis chinensis Franch
MOL013352ObacunoneCoptis chinensis Franch
MOL002894BerberrubineCoptis chinensis Franch
MOL002897EpiberberineCoptis chinensis Franch
MOL002903(R)-canadineCoptis chinensis Franch
MOL002904BerlambineCoptis chinensis Franch
MOL002907Corchoroside A_qtCoptis chinensis Franch
MOL000622MagnograndiolideCoptis chinensis Franch
MOL000762Palmidin ACoptis chinensis Franch
MOL000785PalmatineCoptis chinensis Franch
MOL000098QuercetinCoptis chinensis Franch
MOL001458CoptisineCoptis chinensis Franch
MOL002668WorenineCoptis chinensis Franch
MOL008647MoupinamideCoptis chinensis Franch
MOL000098QuercetinPhellodendron chinense Schneid
MOL000358Beta-sitosterolPhellodendron chinense Schneid
MOL000449StigmasterolPhellodendron chinense Schneid
MOL000622MagnograndiolidePhellodendron chinense Schneid
MOL000762Palmidin APhellodendron chinense Schneid
MOL000785PalmatinePhellodendron chinense Schneid
MOL000787FumarinePhellodendron chinense Schneid
MOL000790IsocorypalminePhellodendron chinense Schneid
MOL001131Phellamurin_qtPhellodendron chinense Schneid
MOL001454BerberinePhellodendron chinense Schneid
MOL001455S-canadinePhellodendron chinense Schneid
MOL001458CoptisinePhellodendron chinense Schneid
MOL001771Poriferast-5-en-3beta-olPhellodendron chinense Schneid
MOL002636Kihadalactone APhellodendron chinense Schneid
MOL002641Phellavin_qtPhellodendron chinense Schneid
MOL002643Delta 7-stigmastenolPhellodendron chinense Schneid
MOL002644PhellopterinPhellodendron chinense Schneid
MOL002651Dehydrotanshinone II APhellodendron chinense Schneid
MOL002652Delta7-dehydrosophoraminePhellodendron chinense Schneid
MOL002656DihydroniloticinPhellodendron chinense Schneid
MOL002659Kihadanin APhellodendron chinense Schneid
MOL002660NiloticinPhellodendron chinense Schneid
MOL002662RutaecarpinePhellodendron chinense Schneid
MOL002663SkimmianinPhellodendron chinense Schneid
MOL002666ChelerythrinePhellodendron chinense Schneid
MOL002668WoreninePhellodendron chinense Schneid
MOL002670CavidinePhellodendron chinense Schneid
MOL002671Candletoxin APhellodendron chinense Schneid
MOL002672Hericenone HPhellodendron chinense Schneid
MOL002673HispidonePhellodendron chinense Schneid
MOL002894BerberrubinePhellodendron chinense Schneid
MOL005438CampesterolPhellodendron chinense Schneid
MOL006392DihydroniloticinPhellodendron chinense Schneid
MOL006401MelianonePhellodendron chinense Schneid
MOL006413PhellochinPhellodendron chinense Schneid
MOL006422ThalifendinePhellodendron chinense Schneid
MOL013352ObacunonePhellodendron chinense Schneid
MOL000358Beta-sitosterolFraxinus rhynchophylla Hance
MOL006709AIDS214634Fraxinus rhynchophylla Hance
MOL0067108-(beta-D-glucopyranosyloxy)-7-hydroxy-6-methoxy-2H-1-benzopyran-2-oneFraxinus rhynchophylla Hance
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白头翁汤正丁醇提取物通过调控自噬与凋亡缓解外阴阴道念珠菌病
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邱薇 , 李璨 , 吴惠 , 施高翔 , 吴大强 , 汪天明 , 汪长中
微生物学报 | 研究报告 2026,66(5): 2321-2338
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微生物学报 | 研究报告 2026, 66(5): 2321-2338
白头翁汤正丁醇提取物通过调控自噬与凋亡缓解外阴阴道念珠菌病
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邱薇, 李璨, 吴惠, 施高翔, 吴大强, 汪天明 , 汪长中
作者信息
  • 安徽中医药大学 中西医结合学院，安徽 合肥
n-butanol extract of Pulsatilla decoction alleviates vulvovaginal candidiasis by inducing autophagy and inhibiting apoptosis
Wei QIU, Can LI, Hui WU, Gaoxiang SHI, Daqiang WU, Tianming WANG , Changzhong WANG
Affiliations
  • School of Integrated Traditional Chinese and Western Medicine, Anhui University of Chinese Medicine, Hefei, Anhui, China
出版时间: 2026-05-04 doi: 10.13343/j.cnki.wsxb.20260024
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外阴阴道念珠菌病(vulvovaginal candidiasis, VVC)是女性生殖道常见的真菌感染性疾病。尽管针对VVC的传统治疗手段已相对成熟，但仍存在一定局限性。白头翁汤作为中国医学的经典方剂在临床上已被证实对VVC具有明确疗效，但其具体作用机制尚未完全阐明。 目的 通过网络药理学及动物实验阐明中药白头翁汤正丁醇提取物(n-butanol extract of Pulsatilla decoction, BEPD)对VVC的作用机制。 方法 构建VVC小鼠模型，评估BEPD对VVC的疗效；通过网络药理学筛选出BEPD对VVC潜在的作用信号通路，并采用蛋白印迹法、免疫荧光、免疫组化、实时荧光定量PCR检测小鼠阴道黏膜组织中自噬、凋亡及其相关通路蛋白的变化水平。 结果 网络药理学分析显示，白头翁汤发挥抗真菌活性、治疗VVC的关键靶点包括PIK3RA和AKT1等；KEGG分析结果表明，白头翁汤可能通过调控PI3K-Akt信号通路发挥治疗VVC的作用。动物实验证实，相对于VVC模型组，BEPD治疗后，PI3K、p-Akt、p-mTOR蛋白表达下降，自噬相关蛋白LC3B和ATG5表达显著增加，凋亡相关蛋白Bax和Cleaved-Caspase-3的表达则明显下调，抗凋亡相关蛋白Bcl-2表达明显上调。 结论 BEPD可能通过抑制PI3K-Akt-mTOR信号通路促进阴道上皮细胞自噬并抑制凋亡，从而恢复阴道黏膜上皮屏障稳态，缓解VVC。

白头翁汤正丁醇提取物  /  外阴阴道念珠菌病  /  自噬  /  凋亡  /  PI3K-Akt-mTOR信号通路

Vulvovaginal candidiasis (VVC) is a prevalent fungal infection affecting the female reproductive tract. Although conventional therapeutic approaches for VVC are relatively well-established, they still exhibit certain limitations. Pulsatilla decoction, a classic traditional Chinese medicine formula, has demonstrated significant clinical efficacy in the treatment of VVC. However, its precise mechanism of action remains incompletely elucidated. Objective To clarify the therapeutic mechanism of the n-butanol extract of Pulsatilla decoction (BEPD) on VVC through network pharmacology and animal experiments. Methods A mouse model of VVC was established and the therapeutic effect of BEPD on VVC was evaluated. Network pharmacology was employed to screen the potential signaling pathways of BEPD on VVC. Western blotting, immunofluorescence, immunohistochemistry, and real-time fluorescence quantitative PCR were employed to measure the changes in autophagy, apoptosis, and related pathway proteins in the vaginal mucosa of mice. Results Network pharmacology analysis identified PIK3R1 and AKT1 as key targets of Pulsatilla decoction in exerting antifungal activity against VVC. KEGG pathway enrichment analysis indicated that Pulsatilla decoction exerted its therapeutic effects on VVC by regulating the PI3K-Akt signaling pathway. Animal experiments confirmed that compared with the VVC model group, the BEPD treatment down-regulated the expression of PI3K, p-Akt, and p-mTOR, significantly up-regulated the expression of autophagy-related proteins LC3B and ATG5, significantly inhibited the expression of apoptosis-related proteins Bax and Cleaved-Caspase-3, and significantly promoted the expression of anti-apoptosis-related protein Bcl-2. Conclusion BEPD may promote autophagy and inhibit apoptosis of vaginal epithelial cells by inhibiting the PI3K-Akt-mTOR signaling pathway, thereby restoring the homeostasis of the vaginal mucosal epithelial barrier and alleviating VVC.

n-butanol extract of Pulsatilla decoction (BEPD)  /  vulvovaginal candidiasis (VVC)  /  autophagy  /  apoptosis  /  PI3K-Akt-mTOR signaling pathway
邱薇, 李璨, 吴惠, 施高翔, 吴大强, 汪天明, 汪长中. 白头翁汤正丁醇提取物通过调控自噬与凋亡缓解外阴阴道念珠菌病. 微生物学报, 2026 , 66 (5) : 2321 -2338 . DOI: 10.13343/j.cnki.wsxb.20260024
Wei QIU, Can LI, Hui WU, Gaoxiang SHI, Daqiang WU, Tianming WANG, Changzhong WANG. n-butanol extract of Pulsatilla decoction alleviates vulvovaginal candidiasis by inducing autophagy and inhibiting apoptosis[J]. Acta Microbiologica Sinica, 2026 , 66 (5) : 2321 -2338 . DOI: 10.13343/j.cnki.wsxb.20260024
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白念珠菌(Candida albicans)是人体最常见的条件致病性真菌，常定殖于皮肤、口腔、肠道、阴道等部位，在机体免疫力下降或菌群失衡时会引发黏膜感染甚至系统性感染。外阴阴道念珠菌病(vulvovaginal candidiasis, VVC)是女性生殖道黏膜常见的感染性疾病，白念珠菌是导致该病的主要致病菌[1]。VVC发生时，白念珠菌从酵母相转变为菌丝相，黏附并侵袭阴道黏膜上皮，通过产生多种毒力因子(侵袭素、念珠菌溶素、水解酶等)破坏黏膜屏障结构，诱发局部免疫炎症反应[2]，引起外阴瘙痒、红肿、烧灼感，以及白色凝乳状或淡黄色豆渣样阴道分泌物等症状，严重影响患者生活质量[3]。流行病学数据显示，约75%的女性在其一生中至少经历一次VVC感染，其中40%-45%的患者会出现2次或以上复发[4]。若未得到及时有效的治疗，VVC可能发展为难治性外阴阴道念珠菌病(recurrent vulvovaginal candidiasis, RVVC)[5]。因此，对VVC进行有效干预具有重要的临床意义。
VVC的发生不仅与白念珠菌的毒力因子相关，还取决于宿主自身的免疫状态，尤其是阴道局部的免疫防御功能[6]。阴道上皮细胞(vaginal epithelial cells, VECs)是阴道黏膜屏障的核心组成部分[7]。白念珠菌感染时，上皮细胞不仅为其定植及后续侵袭提供附着位点和营养支持，同时还可以通过调控免疫应答以及自噬等过程维持细胞稳态，恢复黏膜屏障的完整性[8]。
自噬是高度保守的细胞内降解与回收过程，在包括上皮细胞在内的多种细胞类型中参与清除真菌、细菌和病毒感染，以及受损的细胞器和蛋白质，维持细胞的正常生理功能[9]。在感染过程中，病原体可被细胞表面或胞质内的多种模式识别受体(pattern recognition receptors, PRR)识别，随之激活下游自噬通路，从而促进对病原体或病原体相关分子模式(pathogen-associated molecular patterns, PAMP)的捕获与清除；除直接介导病原体清除外，自噬还在抗原呈递以及固有免疫应答中发挥重要作用[10-12]。Shroff等[13]研究发现，具备自噬功能的阴道上皮细胞可有效抵抗白念珠菌感染所致的细胞损伤，而自噬功能缺陷的细胞则在感染后发生死亡。这表明自噬在阴道上皮细胞抵御白念珠菌感染过程中起着关键作用。
自噬在感染等应激状态下所诱导的细胞凋亡方面也发挥调控作用[14-15]。自噬在多个层面与多种凋亡相关信号分子形成交互调控，共同决定细胞最终命运[16-19]。Shroff等[13]研究报道，在白念珠菌感染下转染了野生型自噬相关基因5 (autophagy related 5, ATG5)质粒的阴道上皮细胞中，凋亡与坏死的比例比未转染的显著降低；而转染了突变型ATG5质粒的细胞则表现出更高的细胞死亡率。可见，自噬以及与其互作的凋亡的调控在阴道上皮细胞抵御白念珠菌感染以维持细胞稳态中发挥关键的保护作用，从而可能成为治疗VVC的潜在靶点。
目前，治疗VVC的一线药物主要为氟康唑、咪康唑和酮康唑等唑类抗真菌药。然而，长期广泛使用此类药物导致耐药菌株的检出率逐年上升，菌株耐药性已成为临床上治疗VVC面临的重要挑战。另外，新型抗真菌药物的研发通常面临投入成本高、研发周期长等现实困难[20]。这些问题的出现为中医药干预提供了潜在的应用空间。
白头翁汤出自中国传统医学典籍《伤寒论》，由白头翁、黄连、黄柏和秦皮四味中药材组成。临床上，该方药常用于治疗细菌性痢疾和溃疡性结肠炎，近年来也被应用于治疗VVC[21]。本课题组Hu等[22]分别采用石油醚、氯仿、乙酸乙酯和正丁醇等不同极性溶剂对白头翁汤进行萃取，获得相应的提取物，经比较证实，白头翁汤正丁醇提取物(n-butanol extract of Pulsatilla decoction, BEPD)的抗真菌活性最好，其主要活性成分包括白头翁皂苷B4、小檗碱、秦皮甲素、秦皮乙素、药根碱以及黄柏碱等；还发现BEPD可以显著改善VVC的阴道炎症[22]。然而，关于BEPD能否通过调控自噬/凋亡以维持阴道上皮细胞的稳态尚不明确。因此，本研究基于网络药理学和实验验证，从自噬/凋亡对阴道黏膜上皮稳态的影响以及相应的调控信号通路的角度阐明BEPD抗VVC的机制。
1 材料与方法
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1.1 菌株、动物与药物
白念珠菌SC5314由海军军医大学姜远英教授惠赠。该菌株首先接种于YPD固体培养基进行培养，随后转接至YPD液体培养基中活化，在37 ℃、200 r/min培养14-16 h。采用3 000×g离心5 min收集真菌，弃去上清液，用PBS稀释调整至2×108个/mL。
6-7周龄雌性C57BL/6小鼠共60只，体重为18-22 g，购自杭州子源实验动物科技有限公司(合格证书SCXK2019-004)。将小鼠随机分为6组，每组10只，饲养于无病环境中，湿度为50%-55%，温度为(22±2) ℃，采用12 h光照/12 h黑暗循环，并给予自由取食和饮水。本研究所有动物实验均获得安徽中医药大学医学研究所动物伦理委员会批准(编号为AHUCM-mouse-2025038)，并遵循中国关于实验动物伦理使用和护理的立法指导方针。
白头翁汤由白头翁、黄连、黄柏、秦皮组成，购自安徽中医药大学第一附属医院中药房，并经刘守金教授鉴定，四味中药分别按照5:2:4:4的比例混合[1]。首先将药材用80%乙醇浸泡过夜，然后进行水浴加热，在70 ℃回流3 h，重复此步骤3次，并收集合并滤液。接着按不同极性梯度溶液(石油醚、乙酸乙酯、正丁醇)萃取5-6次，最后在80 ℃下旋转蒸发至干燥得到BEPD。
1.2 主要试剂和仪器
氟康唑(fluconazole, Flu)，上海源叶生物科技有限公司；苯甲酸雌二醇，上海笛柏生物科技有限公司；乙醇，江苏强盛功能化学股份有限公司；石油醚、乙酸乙酯、正丁醇，国药集团化学试剂有限公司；多聚甲醛、免疫组化试剂盒、RIPA裂解液、BCA试剂盒，山东白鲨生物技术有限公司；革兰氏染色试剂盒，珠海贝索生物技术有限公司；酵母浸出粉葡萄糖琼脂培养基、YPD液体培养基，青岛高科技工业园海博生物技术有限公司；小鼠肿瘤坏死因子-α (tumor necrosis factor-alpha, TNF-α)、小鼠白细胞介素1β (interleukin-1β, IL-1β) ELISA试剂盒、乳酸脱氢酶(lactate dehydrogenase, LDH)酶联免疫吸附试剂盒，上海爱萌优宁生物技术有限公司；TRIzol、ECL发光试剂盒，山东思科捷生物技术有限公司；GAPDH、LC3B、ATG5、Bax、Cleaved-Caspase-3、mTOR、p-mTOR、Occludin和PI3K，成都正能生物技术有限责任公司；Akt、p-Akt，沈阳万类生物科技有限公司；ZO-1，武汉三鹰生物技术有限公司；Bax、Bcl-2和Claudin-1，Immunoway公司；Hieff qPCR SYBR Green Master Mix，翌圣生物科技(上海)股份有限公司。
正置显微镜，广州市明美光电技术有限公司；高速离心机，北京雷勃尔医疗器械有限公司；医用洁净工作台，上海博讯实业有限公司；激光共聚焦显微镜，Leica公司；实时荧光定量PCR仪，Roche公司；发光成像分析仪，上海天能科技有限公司。
1.3 VVC模型的建立与治疗
小鼠随机分为6组：空白对照组(Control)、模型组(Model)、BEPD低剂量组(BEPD-L, 20 mg/kg）、BEPD中剂量组(BEPD-M, 40 mg/kg)、BEPD高剂量组(BEPD-H, 80 mg/kg)、阳性药物氟康唑组(Flu, 20 mg/kg)。按照本课题组Hu等[22]报道的方法进行操作。除对照组小鼠外，其余各组小鼠每隔一天在颈部皮下注射以无菌食用油溶解的苯甲酸雌二醇0.1 mg，共注射3次。随后，连续一周将含有2×108个/mL真菌悬液接种至小鼠阴道(不包括空白对照组)。接种后，将小鼠倒挂5 min以确保真菌悬液与阴道黏膜充分接触。模型建立后，模型组和空白对照组接受生理盐水灌胃，Flu组每天给予20 mg/kg Flu灌胃，BEPD组每天分别给予20、40、80 mg/kg的BEPD灌胃，持续7 d。在感染后第1、3、7、14天采集阴道灌洗液用于后续实验。图1为造模和给药具体流程图，图片制作由biogdp.com提供服务[23]。
1.4 革兰氏染色
在感染后第1、3、7、14天分别收集各组小鼠阴道灌洗液。取20 μL阴道灌洗液均匀涂抹至黏附载玻片上，自然晾干。按照革兰氏染色试剂盒说明书操作，检测小鼠阴道冲洗液中白念珠菌的形态。
1.5 真菌载荷
在感染后第1、3、7、14天分别收集各组小鼠阴道灌洗液。取50 μL灌洗液分别稀释至10-3和10-4，涂布于YPD培养基上，将其置于37 ℃培养箱中培养48 h，之后对真菌菌落进行计数。
1.6 酶联免疫吸附测定
收集阴道灌洗液，于4 ℃、3 000×g离心10 min。使用ELISA试剂分别对IL-1β、TNF-α和LDH的水平进行定量检测。
1.7 苏木素-伊红染色
处死小鼠后，取其阴道组织，用10%多聚甲醛固定，经脱水、包埋处理后，制备厚度为5 μm的组织切片。切片采用二甲苯脱蜡，随后进行苏木素-伊红染色(hematoxylin and eosin, HE)染色以评估小鼠阴道组织的损伤程度。在光学显微镜下，以200倍放大倍数对每只感染小鼠的阴道组织进行观察与分析。
1.8 网络药理学预测BEPD抗VVC的作用机制
本研究采用网络药理学方法，利用TCMSP在线平台(https://old.tcmsp-e.com/tcmsp.php)和Swiss Target Prediction database数据库(http://www.swisstargetprediction.ch/)对口服生物利用度(oral bioavailability, OB)≥30%和药物相似度(drug-likeness, DL)≥0.18的白头翁汤中潜在的活性化合物和靶点进行筛选。随后通过UniProt数据库(https://www.uniprot.org/)进行基因名标准化。与真菌感染和VVC相关的疾病靶点检索自GeneCards数据库(https://www.genecards.org/)、OMIM数据库(https://www.omim.org/)和Therapeutic Target Database数据库(TTD,https://db.idrblab.net/ttd/)，进行整合、去重和整理。通过维恩图绘制药物-疾病交集靶点，蛋白质-蛋白质相互作用网络通过向STRING数据库(https://cn.string-db.org/)提交交集靶点生成，并通过Cytoscape 3.9.1选出度值前15个的作为核心靶点。最后利用Metascape数据库(https://metascape.org/)对交集靶点的基因本体(gene ontology, GO)功能[分子功能(molecular function, MF)；生物过程(biological process, BP)；细胞组分(acellular component, CC)]和京都基因与基因组数据库(Kyoto encyclopedia of genes and genomes, KEGG)通路进行富集分析。
1.9 免疫组化和免疫荧光
小鼠阴道组织切片经脱蜡和水化处理后，进行抗原修复，随后采用内源性过氧化物酶阻断法进行封闭。接着滴加正常山羊血清以进一步封闭非特异性结合位点。在4 ℃，加入LC3B (1:100)一抗，置于湿盒中孵育过夜。次日，依照免疫组化(immunohistochemistry, IHC)检测试剂盒说明书的标准操作程序进行后续染色步骤。染色完成后，使用中性树胶封片，并在光学显微镜下进行观察与图像采集。
对于免疫荧光(immunofluorescence, IF)染色实验，制备小鼠阴道组织切片用于检测。分别向切片中加入ATG5 (1:100)和Cleaved-Caspase-3 (1:100)的一抗及其相应二抗(1:200)，于37 ℃孵育1 h。最后加入DAPI溶液，于37 ℃避光孵育10 min，随后进行封片处理，并在共聚焦显微镜下进行观察与图像采集。
1.10 蛋白印迹分析(Western blotting, WB)
用RIPA裂解液提取阴道组织蛋白。采用BCA试剂盒对提取的蛋白质进行定量，随后进行十二烷基硫酸钠-聚丙烯酰胺凝胶电泳(SDS-PAGE)。将分离后的蛋白质转移至PVDF膜上，于4 ℃与一抗(ZO-1:1:10 000，其余1:1 000)孵育过夜，然后在37 ℃使用二抗(1:15 000)孵育2 h。利用ECL发光试剂盒及发光成像分析仪对蛋白条带进行化学发光显影与图像采集。以GAPDH作为内参蛋白，采用ImageJ软件对所得图像进行半定量分析。
1.11 实时定量聚合酶链反应(RT-qPCR)
使用TRIzol从阴道组织中提取总RNA，然后反转录为cDNA。使用Hieff qPCR SYBR Green Master Mix在实时荧光定量PCR仪上进行检测，以甘油醛-3-磷酸脱氢酶(glyceraldehyde-3-phosphate dehydrogenase, GAPDH)为内参。PCR反应体系(20 μL)：Hieff qPCR SYBR Green Master Mix (No Rox） 10 µL，上、下游引物(10 µmol/L)各0.4 µL，DNA模板1 µL，ddH2O 8.2 µL。反应条件：95 ℃预变性60 s；58 ℃退火20 s，72 ℃延伸20 s，共40个循环。引物序列见表1。目标基因的相对表达量按2-ΔΔCt法计算。
1.12 数据分析
数据分析使用SPSS 26.0软件，数据可视化使用GraphPad Prism 9.5软件。数据以平均值±标准差表示，至少有3个生物重复。组间差异采用单因素方差分析比较，P<0.05表示差异有统计学意义。
2 结果与分析
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2.1 BEPD对VVC小鼠阴道的治疗作用
结果显示，模型组小鼠阴道口可见白色分泌物，并伴有明显的红肿现象。经BEPD治疗后，局部阴道体征有所改善，BEPD-L组和BEPD-M组分泌物减少，但阴道口仍存在轻微红肿；BEPD-H组和Flu组小鼠的阴道症状显著改善，基本恢复至正常水平(图2A)。进一步对各组小鼠阴道灌洗液进行稀释涂布并培养。与模型组相比，BEPD-M组和BEPD-H组显著降低小鼠阴道内白念珠菌的载荷量(图2B)。
革兰氏染色结果表明，除空白对照组外，其余各组小鼠灌洗液中均可见广泛伸长且相互交织的菌丝；经BEPD干预后，各治疗组中白念珠菌的数量均有所减少，且菌丝长度显著缩短，其中以BEPD-H组和Flu组尤为明显(图2C)。
HE染色结果显示，空白对照组小鼠阴道黏膜表面覆盖较厚的角质层，结构完整、层次清晰；而VVC模型组阴道黏膜几乎完全脱落，角质层消失，并伴有大量炎症细胞浸润。随着BEPD浓度的增加，角质层逐渐增厚，炎症细胞浸润明显减少。BEPD-H组及Flu组中，角质层基本恢复至正常水平，黏膜组织结构保持完整(图2D)。ELISA实验结果显示，与空白对照组相比，模型组阴道分泌物中TNF-α、IL-1β和LDH的水平显著升高；经药物干预后，上述炎症因子和LDH水平均有所降低，且在BEPD-M、BEPD-H及Flu组中差异具有统计学意义(图2E-2G)。
WB结果显示，在VVC模型小鼠中，阴道黏膜组织中ZO-1、Claudin-1和Occludin蛋白的表达水平显著低于空白对照组；经BEPD治疗后，上述紧密连接蛋白的表达均有所回升，其中以BEPD-H组的恢复效果最为明显(图2H-2K)。
综上所述，BEPD可通过抑制炎症因子的释放和上调紧密连接蛋白的表达，有效减轻阴道组织的炎症反应，改善阴道黏膜屏障的损伤。
2.2 基于网络药理学分析BEPD治疗VVC的潜在机制
通过TCMSP数据库检索共获得生物活性物质65个，其中包括白头翁11个、黄柏37个、黄连14个、秦皮3个(表2)。随后，整合GeneCards、OMIM和TTD数据库信息，获取与真菌感染及VVC相关的疾病靶点2 050个。利用VENNY 2.1在线平台构建维恩图，识别出142个“药物-疾病”交集基因靶点，这些靶点与白头翁汤对VVC的治疗作用相关(图3A)。基于上述交集靶点，构建初步的蛋白质-蛋白质相互作用(protein-protein interaction, PPI)网络，并将结果导入Cytoscape 3.9.1软件进行分析与可视化。根据度值(degree)排名筛选前15位的靶点作为核心靶点，构建核心靶点的PPI互作网络图(图3B)，最终获得包含15个节点和94条边的网络。筛选出的核心靶点包括TP53、AKT1、SRC、JUN、ESR1、TNF、IL6、PRKACA、CCND1、MAPK1、HSP90AB1、PIK3R1、CXCL8、RELA和CDK1。
GO功能富集结果显示，共筛选出2 198个具有统计学意义的GO条目，其中包括1 855个生物学过程、106个细胞组分和237个分子功能条目。条形图展示了基因数最多的前10项BP、CC和MF富集结果(图3C)。同时，KEGG通路富集分析共识别出201条显著富集的信号通路，主要包括PI3K-Akt通路、Kaposi肉瘤相关通路、HPV感染相关通路、IL-17通路、C型凝集素通路等。
在开展网络药理学分析的同时，本研究梳理了近年来VVC发病机制的相关文献，发现阴道上皮细胞稳态中自噬与凋亡的调控尤为关键。KEGG富集结果中的PI3K-Akt通路明确报道参与调控自噬与凋亡。因此，后续将围绕PI3K-Akt通路及其介导的自噬与凋亡，探讨BEPD通过调节阴道上皮细胞稳态缓解VVC的作用机制(图3D)。
2.3 BEPD对VVC小鼠阴道黏膜上皮细胞自噬的影响
IHC结果显示，随着BEPD浓度的增加，LC3B的表达水平呈剂量依赖性升高，与模型组相比差异具有统计学意义(图4A、4B)。IF结果表明，经BEPD-M和BEPD-H处理后，ATG5的荧光信号显著增强(图4C、4D)。此外，WB与RT-qPCR检测结果一致显示，在VVC小鼠模型中，LC3B Ⅱ/LC3B Ⅰ及ATG5的蛋白和mRNA表达水平均显著下调；而BEPD干预可有效恢复上述分子的表达(图4E-4I)。
2.4 BEPD对VVC小鼠阴道黏膜上皮细胞凋亡的影响
IF结果表明，与空白对照组相比，模型组中Cleaved-Caspase-3的表达水平显著升高，随着BEPD治疗浓度的增高，Cleaved-Caspase-3的荧光强度逐渐下降(图5A、5B)。WB结果显示，模型组中促凋亡蛋白Bax和Cleaved-Caspase-3表达量显著上调，抑凋亡蛋白Bcl-2的表达量显著下调，而BEPD则显著拮抗了这种趋势(图5C-5F)。RT-qPCR检测显示相同趋势，即BEPD可以降低促凋亡基因Bax和Caspase-3的表达，促进抗凋亡基因Bcl-2的表达(图5G-5I)。
2.5 BEPD对PI3K-Akt-mTOR信号通路的影响
RT-qPCR和WB结果表明，在模型组小鼠中，PI3K、p-Akt和p-mTOR的表达水平显著升高；经BEPD中高剂量处理后，PI3K、p-Akt及p-mTOR的表达则逐渐下调(图6A-6H)。上述结果提示，随着BEPD剂量的增加，Akt与mTOR的活化程度呈梯度性抑制，推测PI3K-Akt-mTOR信号通路的抑制可能介导了BEPD诱导阴道水平细胞自噬并抑制细胞凋亡的生物学效应。
3 讨论与结论
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白念珠菌作为一种常见的引起女性生殖道黏膜感染的致病菌，可通过释放念珠菌溶素等毒力因子造成阴道黏膜损伤，严重影响女性生活质量。白念珠菌虽是引发VVC的直接诱因，但宿主的免疫应答也会影响疾病的发生与发展。VVC患者的临床表现严重程度并非单纯由阴道内白念珠菌的载荷量决定，而与阴道黏膜上皮的过度免疫应答密切相关[24]。常规抗真菌药物主要通过靶向菌体不同结构或组分发挥作用，尚未发现通过对宿主的机能调控而达到抗真菌感染作用[25]。鉴于中药具有多成分、多靶点、综合调节及免疫调控等独特优势，其在VVC治疗中或许可通过调控黏膜屏障发挥作用。在本研究中，经BEPD低剂量治疗后症状缓解不明显；但中高剂量治疗后，VVC小鼠阴道分泌物减少，分泌物中所含有的促炎因子水平显著降低，阴道红肿症状显著改善。
阴道上皮细胞是黏膜防御的第一道防线。正常上皮细胞之间的相互作用由细胞间多种紧密连接蛋白(如Claudin-1、Occludin和ZO-1等)连接组成，这些连接蛋白控制细胞旁通透性，维持黏膜屏障功能和黏膜稳态[26-27]。Doan等[28]研究表明，热带念珠菌和白念珠菌的感染会下调紧密连接蛋白的表达，降低肠道屏障的通透性。在本研究中，受白念珠菌感染的小鼠阴道组织中紧密连接蛋白表达下调，经BEPD中高剂量治疗后，紧密连接蛋白表达逐渐恢复至正常水平，表明BEPD可通过恢复损伤的阴道上皮屏障结构缓解VVC。
网络药理学近年来广泛应用于分析中药治疗相关疾病涉及的关键基因或信号通路。本研究采用网络药理学方法分析了BEPD在治疗VVC中的潜在作用机制，筛选出AKT1等多个靶点以及PI3K-Akt等多个信号通路。同时，本研究查阅分析了近年来关于VVC发病机制的主要文献发现，其涉及阴道黏膜上皮稳态的自噬与凋亡的调控，而上述KEGG富集通路中的PI3K-Akt通路即参与了对自噬和凋亡的调控。因此，下文将从PI3K-Akt通路介导的自噬和凋亡角度探讨BEPD通过调控阴道上皮细胞稳态缓解VVC的作用机制。
自噬作为细胞内部高度保守的分解代谢过程，在调控免疫应答和炎症反应中起着关键作用。它不仅能够维持细胞内稳态，清除受损或衰老的细胞器及蛋白质聚集体，还能够选择性地识别并清除入侵的病原微生物(如细菌、病毒和真菌)[29-30]。自噬体通过双层膜结构包裹细胞质中的大分子物质、受损细胞器或病原体，并将其运送至溶酶体进行降解与再循环，从而提供能量和代谢前体，并参与抗原呈递等免疫调节功能。Lapaquette等[31]研究发现，在白念珠菌感染上皮细胞过程中会招募多种自噬相关蛋白到白念珠菌入侵部位，促进溶酶体胞吐作用，参与质膜的修复，并保护上皮细胞免受白念珠菌诱导的细胞死亡。自噬在细胞感染期间与凋亡相互作用，共同维持细胞命运平衡。自噬通常在应激早期被诱导，通过清除受损的线粒体、内质网等细胞器以及错误折叠的蛋白质，从而抑制过度凋亡，维持细胞存活[32]。在细胞凋亡的调控过程中，促凋亡蛋白Bax与抗凋亡蛋白Bcl-2发挥核心调控作用。当细胞受到外界应激刺激时，Bax/Bcl-2比值升高，导致线粒体膜通透性增加，并激活半胱天冬酶-3 (caspase-3)，表明细胞凋亡开始[33]。自噬与凋亡之间的关系为理解感染性疾病、炎症相关病理过程及潜在治疗策略提供了重要视角。本研究结果显示，对VVC小鼠进行BEPD治疗后，中高剂量组中的Bax和Cleaved-Caspase-3的表达均显著下调，而LC3B Ⅱ/LC3B Ⅰ、ATG5和抗凋亡蛋白Bcl-2的表达则显著上调，表明BEPD对阴道上皮细胞具有明显的激活保护性自噬和抗凋亡作用，也提示上皮屏障的恢复可能与此相关。
PI3K-Akt信号通路主要介导细胞增殖、分化、迁移及代谢过程，并在调控自噬与凋亡过程中发挥关键作用[34-35]。哺乳动物雷帕霉素靶蛋白(mammalian target of rapamycin, mTOR)被认为是调节自噬的核心因子，是多条信号通路交汇的关键节点，其中包括磷脂酰肌醇3-激酶(phosphatidylinositol 3-kinase, PI3K)/蛋白激酶B (protein kinase B, Akt)/mTOR以及单磷酸腺苷活化蛋白激酶(AMP-activated protein kinase, AMPK)/mTOR等通路[36-37]。Akt的激活在调控细胞生理过程中具有重要意义，已被证实可通过多个层面抑制哺乳动物细胞的自噬活性[38]。此外，多种Akt下游效应分子，如mTORC1、mTORC2、GSK3β和TSC1/2，均定位于溶酶体——即自噬发生的主要场所[39]。Akt可通过磷酸化并抑制TSC1/2复合物，维持RHEB GTP酶的活性状态，从而激活mTORC1，最终抑制自噬的启动[40]。Wang等[41]研究表明，Akt还可直接磷酸化自噬关键蛋白ULK1 (ATG1)和Beclin1 (ATG6)，该作用独立于mTOR通路，进一步增强对自噬的负向调控。此外，Akt在体外和体内均可磷酸化抗凋亡蛋白Bcl-2，促进其从细胞质向线粒体外膜转位，释放活化的Bcl-2蛋白，进而阻止线粒体释放细胞色素C，抑制下游半胱天冬酶(caspase)的激活，最终阻断细胞凋亡过程[42]。因此，mTOR与Akt通常被视为连接自噬与细胞凋亡的关键分子枢纽。在本研究中，BEPD影响这一通路的能力为自噬激活和凋亡抑制的发生提供了一个合理的解释。本研究表明，VVC模型组小鼠PI3K、p-Akt和p-mTOR的表达水平显著上调；BEPD治疗后，PI3K、p-Akt和p-mTOR的表达明显下调。上述结果提示，BEPD有可能通过调控PI3K-Akt-mTOR信号通路，促进阴道上皮细胞自噬，抑制细胞凋亡，从而发挥治疗VVC中的作用。
综上所述，对于VVC的治疗，中药提取物BEPD具有独特的优势，其缓解VVC与促进阴道上皮细胞自噬、抑制细胞凋亡、改善黏膜屏障、减轻炎症反应密切相关，这些作用可能涉及调控PI3K-Akt-mTOR信号通路，这一发现为上皮屏障在VVC等黏膜感染性疾病中发挥保护作用提供了新的理论依据。当然，本研究的工作仍存在一定的局限性。首先，本研究主要基于小鼠的VVC模型验证网络药理学中PI3K-Akt通路在BEPD治疗VVC的潜在作用，缺乏核心靶点与通路的关联机制。其次，虽然小鼠VVC模型在致病过程、炎症反应等方面具有可重复性高、操作性强等优点，但其与人类阴道的复杂微环境(如菌群构成、免疫系统差异、激素周期波动及上皮结构等)仍存在一定的区别。因此，未来也需要更多基于人类细胞模型或临床样本的研究加以验证。
基金
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  • 国家自然科学基金(82374173)
  • 国家自然科学基金(81774034)
  • 国家自然科学基金(81573725)
文献
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2026年第66卷第5期
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doi: 10.13343/j.cnki.wsxb.20260024
  • 接收时间：2026-01-10
  • 首发时间：2026-05-09
  • 出版时间：2026-05-04
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  • 收稿日期：2026-01-10
  • 录用日期：2026-02-11
基金
The National Natural Science Foundation of China(82374173)
国家自然科学基金(82374173)
The National Natural Science Foundation of China(81774034)
国家自然科学基金(81774034)
The National Natural Science Foundation of China(81573725)
国家自然科学基金(81573725)
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    安徽中医药大学 中西医结合学院，安徽 合肥
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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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