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Article(id=1308842051240813278, tenantId=1146029695717560320, journalId=1189982191388893191, issueId=1308841897058198067, articleNumber=null, orderNo=null, doi=10.16438/j.0513-4870.2025-1480, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=null, receivedDate=1765296000000, receivedDateStr=2025-12-10, revisedDate=1771862400000, revisedDateStr=2026-02-24, acceptedDate=null, acceptedDateStr=null, onlineDate=1789981862125, onlineDateStr=2026-09-21, pubDate=1783785600000, pubDateStr=2026-07-12, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1789981862125, onlineIssueDateStr=2026-09-21, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1789981862125, creator=13701087609, updateTime=1789981862125, updator=13701087609, issue=Issue{id=1308841897058198067, tenantId=1146029695717560320, journalId=1189982191388893191, year='2026', volume='61', issue='7', pageStart='2377', pageEnd='2820', issueExtLink='null', onlineDate='null', pubDate='1783785600000', pubDateStr='2026-07-12', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1789981825365, creator='13701087609', updateTime=1789984154811, updator='13701087609', preIssue=null, nextIssue=null, articleTotal=null, ext={EN=IssueExt(id=1308851667525792021, tenantId=1146029695717560320, journalId=1189982191388893191, issueId=1308841897058198067, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1308851667525792022, tenantId=1146029695717560320, journalId=1189982191388893191, issueId=1308841897058198067, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null, downloadFileDto=null}, startPage=2495, endPage=2501, ext={EN=ArticleExt(id=1308842053136638687, articleId=1308842051240813278, tenantId=1146029695717560320, journalId=1189982191388893191, language=EN, title=Antifungal activity and mechanism of phenanthroline-phenanthroline+ against cutaneous Malassezia furfur infection, columnId=1190335348761793317, journalTitle=Acta Pharmaceutica Sinica, columnName=Original Articles, runingTitle=null, highlight=null, articleAbstract=

Malassezia furfur (M. furfur) is a common lipophilic fungus with strong epidermal colonization ability and high recurrence rates, capable of inducing a wide range of skin diseases in both animals and humans. Traditional antifungal therapies are associated with significant side effect and frequent drug resistance, necessitating the development of new treatment strategies. This study investigated the efficacy of a protonated phenanthroline-phenanthroline+ (ph-ph+) compound, previously developed by our team, in inhibiting the growth and reproduction of M. furfur. The results showed that the minimum inhibitory concentration (MIC) and minimum fungicidal concentration (MFC) of ph-ph+ against M. furfur were 2 and 8 µg·mL-1, respectively. Furthermore, ph-ph+ significantly reduced key virulence characteristics of M. furfur, including biofilm formation, hydrophobicity, and adhesion capacity. Assessments using transmission electron microscopy and Annexin V-FITC/propidium iodide staining confirmed that ph-ph+ kills M. furfur by inducing apoptosis. In a mouse skin infection model induced by M. furfur, topical application of ph-ph+ effectively cleared the fungus from the skin surface without causing skin irritation or other adverse reactions. This study demonstrates that ph-ph+ may represent a novel antimicrobial compound distinct from traditional drugs and provides a potential therapeutic approach for treating skin infections caused by M. furfur or other fungi. The experimental protocol was approved by the Animal Experiment Ethics Committee of Southwest University (approval No.: LAC2024-1-0446), and the experiments were conducted strictly in accordance with the ethical principles for the use and care of animals.

, authors=Yi-xiao FENG, En-ping YANG, Han QIN, Jing-li LI, Ke-jing ZHU, Qi-han LU, Ai-ling FU*, authorsList=Yi-xiao FENG, En-ping YANG, Han QIN, Jing-li LI, Ke-jing ZHU, Qi-han LU, Ai-ling FU, authorCompany=null, correspAuthors=Ai-ling FU, authorNote=null, correspAuthorsNote=null, copyrightStatement=Copyright ©2026 Acta Pharmaceutica Sinica. All rights reserved., copyrightOwner=null, extLink=null, articleAbsUrl=null, sourceXml=null, magXml=null, pdfUrl=null, pdf=null, pdfFileSize=null, pdfExtLink=null, richHtmlUrl=null, mobilePdfUrl=null, reviewReport=null, pdfFirstPage=null, abstractGraph=null, abstractGraphContent=null, abstractVideo=null, citation=null, cebUrl=null, magXmlContent=null, mapNumber=null, fund=null), CN=ArticleExt(id=1308842055615472376, articleId=1308842051240813278, tenantId=1146029695717560320, journalId=1189982191388893191, language=CN, title=质子型双菲啰啉抗糠秕马拉色菌皮肤感染的作用及机制, columnId=1190335348896011050, journalTitle=药学学报, columnName=研究论文, runingTitle=null, highlight=null, articleAbstract=

糠秕马拉色菌(Malassezia furfur, M. furfur) 是常见的嗜脂性真菌, 其表皮定植力强、复发率高, 可广泛引发动物及人类的皮肤疾病。传统抗真菌药物治疗存在不良反应大、耐药性频发等问题, 因此亟需开发新的治疗策略。本研究使用前期团队自主研发的质子型双菲啰啉(phenanthroline-phenanthroline+, ph-ph+), 探讨其是否具有高效抑制M. furfur的生长和繁殖的作用。实验结果发现, ph-ph+对M. furfur的最低抑菌浓度和最低杀菌浓度值分别为2和8 µg·mL-1。此外, ph-ph+能使M. furfur的毒力特征——生物膜、疏水率、黏附能力等均显著降低。通过透射电子显微镜和Annexin V-FITC/碘化丙啶染色评估, 证实ph-ph+可通过诱导细胞凋亡杀灭M. furfur。将ph-ph+涂抹于由M. furfur诱发的小鼠皮肤感染模型中, 结果显示ph-ph+能够有效清除小鼠皮肤表面的真菌, 且不引起皮肤刺激或其他不良反应。本研究表明, ph-ph+可能是一种有别于传统药物的新型抗菌化合物, 同时本研究也为治疗M. furfur或其他真菌所致的皮肤感染提供了一种潜在治疗方法。实验方案由西南大学动物实验伦理委员会批准(批准号: LAC2024-1-0446), 严格按照动物使用和护理的伦理原则进行实验操作。

, authors=冯义骁, 阳恩萍, 秦汉, 李景丽, 朱可敬, 卢玘涵, 付爱玲*, authorsList=冯义骁, 阳恩萍, 秦汉, 李景丽, 朱可敬, 卢玘涵, 付爱玲, authorCompany=null, correspAuthors=付爱玲, authorNote=

作者贡献:

冯义骁负责研究设计、实验操作、撰写论文初稿; 阳恩萍负责数据采集、处理和分析; 秦汉、卢玘涵负责动物实验; 李景丽、朱可敬负责论文修改; 付爱玲负责论文修订。

, correspAuthorsNote=
付爱玲, Tel/Fax: 86-23-68251225, E-mail:
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J Invest Dermatol, 2023, 143: 1799-1808., articleTitle=null, refAbstract=null)], funds=null, companyList=[AuthorCompany(id=1308842057435800313, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1308842051240813278, xref=null, ext=[AuthorCompanyExt(id=1308842057444188922, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1308842051240813278, companyId=1308842057435800313, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=College of Pharmaceutical Sciences, Southwest University, Chongqing 400716, China), AuthorCompanyExt(id=1308842057452577531, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1308842051240813278, companyId=1308842057435800313, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=西南大学药学院, 重庆 400716)])], figs=[ArticleFig(id=1308842060032074537, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1308842051240813278, language=EN, label=null, caption=null, figureFileSmall=TAX/sPJhwNLSvalut+Whnw==, figureFileBig=5O4YXRDVuXM1p4+T21irlw==, tableContent=null), ArticleFig(id=1308842060107572010, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1308842051240813278, language=CN, label=Fig.1, caption=Structure of phenanthroline-phenanthroline+, figureFileSmall=TAX/sPJhwNLSvalut+Whnw==, figureFileBig=5O4YXRDVuXM1p4+T21irlw==, tableContent=null), ArticleFig(id=1308842061898539819, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1308842051240813278, language=EN, label=null, caption=null, figureFileSmall=3brJ3eu3w1nq/djkvztR2g==, figureFileBig=OOz4sO5HWVpo1msm1BWDGw==, tableContent=null), ArticleFig(id=1308842061965648684, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1308842051240813278, language=CN, label=Fig.2, caption=ph-ph+ inhibited the radial growth of M. furfur. A, B: Inhibitory effect of different concentrations of ph-ph+ on the radial growth of M. furfur; C: Comparison of the inhibitory effect of ph-ph+, terbinafine, and miconazole on the radial growth of M. furfur. n = 3, mean ± SD. ***P < 0.001, figureFileSmall=3brJ3eu3w1nq/djkvztR2g==, figureFileBig=OOz4sO5HWVpo1msm1BWDGw==, tableContent=null), ArticleFig(id=1308842062032757549, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1308842051240813278, language=EN, label=null, caption=null, figureFileSmall=mH2Tg+qLxS1DmVUvary65A==, figureFileBig=QAR6gT0YAyzLFmNLULfewg==, tableContent=null), ArticleFig(id=1308842062125032238, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1308842051240813278, language=CN, label=Fig.3, caption=Effect of ph-ph+ against M. furfur at 4 or 37 ℃. A: Growth rate of M. furfur; B: Inhibition rate of ph-ph+ at different temperatures, figureFileSmall=mH2Tg+qLxS1DmVUvary65A==, figureFileBig=QAR6gT0YAyzLFmNLULfewg==, tableContent=null), ArticleFig(id=1308842062187946799, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1308842051240813278, language=EN, label=null, caption=null, figureFileSmall=4W2akyB78Jx5NufVtXfuJQ==, figureFileBig=k9zkA34+5j68FClg+PgCaQ==, tableContent=null), ArticleFig(id=1308842062271832880, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1308842051240813278, language=CN, label=Fig.4, caption=Effect of ph-ph+ on spore germination rate. A: Inhibitory effect of different concentrations of ph-ph+ on the spore germination rate of M. furfur; B: Comparison of the inhibitory effect of ph-ph+, terbinafine, and miconazole on the spore germination rate of M. furfur. n = 3, mean ± SD. **P < 0.01, ***P < 0.001, figureFileSmall=4W2akyB78Jx5NufVtXfuJQ==, figureFileBig=k9zkA34+5j68FClg+PgCaQ==, tableContent=null), ArticleFig(id=1308842062343136049, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1308842051240813278, language=EN, label=null, caption=null, figureFileSmall=rfcl/6ddee1THNOXxm6LHw==, figureFileBig=kiCphKzTjmJZ+ID9/LxpFQ==, tableContent=null), ArticleFig(id=1308842062427022130, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1308842051240813278, language=CN, label=Fig.5, caption=Effect of ph-ph+ on the formation of M. furfur biofilm. A, B: Effect of different concentrations of ph-ph+ on the biofilm formation of M. furfur; C: Comparison of the effect of ph-ph+, terbinafine, and miconazole on the biofilm formation ratio of M. furfur. n = 3, mean ± SD. *P < 0.05, **P < 0.01, ***P < 0.001, figureFileSmall=rfcl/6ddee1THNOXxm6LHw==, figureFileBig=kiCphKzTjmJZ+ID9/LxpFQ==, tableContent=null), ArticleFig(id=1308842062510908211, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1308842051240813278, language=EN, label=null, caption=null, figureFileSmall=KPR2PZPQLUVHk4OqGgolkg==, figureFileBig=Q8YzMgZOQnB/4tj0lnvXFg==, tableContent=null), ArticleFig(id=1308842062582211380, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1308842051240813278, language=CN, label=Fig.6, caption=Effect of ph-ph+ on the hydrophobicity of M. furfur. A: Effect of different concentrations of ph-ph+ on the hydrophobicity of M. furfur; B: Comparison of the effect of ph-ph+, terbinafine, and miconazole on the hydrophobicity of M. furfur. n = 3, mean ± SD. *P < 0.05, **P < 0.01, figureFileSmall=KPR2PZPQLUVHk4OqGgolkg==, figureFileBig=Q8YzMgZOQnB/4tj0lnvXFg==, tableContent=null), ArticleFig(id=1308842062657708853, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1308842051240813278, language=EN, label=null, caption=null, figureFileSmall=UAj1zs+50L7lJ5GCUqGL2w==, figureFileBig=L9DLAuAduG4yDKXC7FUC1Q==, tableContent=null), ArticleFig(id=1308842062729012022, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1308842051240813278, language=CN, label=Fig.7, caption=Effect of ph-ph+ on adhesion of M. furfur. A, B: Inhibitory effect of different concentrations of ph-ph+ on adhesion of M. furfur; C: Comparison of the inhibitory effect of ph-ph+, terbinafine, and miconazole on adhesion of M. furfur. n = 3, mean ± SD. **P < 0.01, ***P < 0.001, figureFileSmall=UAj1zs+50L7lJ5GCUqGL2w==, figureFileBig=L9DLAuAduG4yDKXC7FUC1Q==, tableContent=null), ArticleFig(id=1308842062808703800, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1308842051240813278, language=EN, label=null, caption=null, figureFileSmall=s81rBQvGatzW4Ea+vGatHw==, figureFileBig=gbKaab32qmmL4a4hr7vSGA==, tableContent=null), ArticleFig(id=1308842062863229754, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1308842051240813278, language=CN, label=Fig.8, caption=ph-ph+ could induce M. furfur apoptosis, evidenced by Annexin V-FITC/PI, an indicator of cell apoptosis, figureFileSmall=s81rBQvGatzW4Ea+vGatHw==, figureFileBig=gbKaab32qmmL4a4hr7vSGA==, tableContent=null), ArticleFig(id=1308842062913561403, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1308842051240813278, language=EN, label=null, caption=null, figureFileSmall=CLsco3BvCA7aEAxC6QNOqQ==, figureFileBig=C6HPNdFMxNlU7DpO3xSUjA==, tableContent=null), ArticleFig(id=1308842062972281660, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1308842051240813278, language=CN, label=Fig.9, caption=Hyphae and spore morphology of M. furfur under transmission electron microscope after ph-ph+ treatment. The cell contents of both hyphae and spores were degraded and appeared vacuolation, showing typical apoptotic feature, figureFileSmall=CLsco3BvCA7aEAxC6QNOqQ==, figureFileBig=C6HPNdFMxNlU7DpO3xSUjA==, tableContent=null), ArticleFig(id=1308842063077139261, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1308842051240813278, language=EN, label=null, caption=null, figureFileSmall=c1U1LOJiMOXMZMx3vE18EQ==, figureFileBig=1Muprx0nXr87hFpUiciMAg==, tableContent=null), ArticleFig(id=1308842063135859518, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1308842051240813278, language=CN, label=Fig.10, caption=M. furfur could reduce M. furfur infection on mouse skin. 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质子型双菲啰啉抗糠秕马拉色菌皮肤感染的作用及机制
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冯义骁 , 阳恩萍 , 秦汉 , 李景丽 , 朱可敬 , 卢玘涵 , 付爱玲 *
药学学报 | 研究论文 2026,61(7): 2495-2501
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药学学报 |研究论文 2026 , 61 (7) : 2495 -2501
质子型双菲啰啉抗糠秕马拉色菌皮肤感染的作用及机制
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冯义骁, 阳恩萍, 秦汉, 李景丽, 朱可敬, 卢玘涵, 付爱玲*
作者信息
  • 西南大学药学院, 重庆 400716
通讯作者:
付爱玲, Tel/Fax: 86-23-68251225, E-mail:
作者简介:

作者贡献:

冯义骁负责研究设计、实验操作、撰写论文初稿; 阳恩萍负责数据采集、处理和分析; 秦汉、卢玘涵负责动物实验; 李景丽、朱可敬负责论文修改; 付爱玲负责论文修订。

Antifungal activity and mechanism of phenanthroline-phenanthroline+ against cutaneous Malassezia furfur infection
Yi-xiao FENG, En-ping YANG, Han QIN, Jing-li LI, Ke-jing ZHU, Qi-han LU, Ai-ling FU*
Affiliations
  • College of Pharmaceutical Sciences, Southwest University, Chongqing 400716, China
出版时间: 2026-07-12 doi: 10.16438/j.0513-4870.2025-1480
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摘要
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糠秕马拉色菌(Malassezia furfur, M. furfur) 是常见的嗜脂性真菌, 其表皮定植力强、复发率高, 可广泛引发动物及人类的皮肤疾病。传统抗真菌药物治疗存在不良反应大、耐药性频发等问题, 因此亟需开发新的治疗策略。本研究使用前期团队自主研发的质子型双菲啰啉(phenanthroline-phenanthroline+, ph-ph+), 探讨其是否具有高效抑制M. furfur的生长和繁殖的作用。实验结果发现, ph-ph+对M. furfur的最低抑菌浓度和最低杀菌浓度值分别为2和8 µg·mL-1。此外, ph-ph+能使M. furfur的毒力特征——生物膜、疏水率、黏附能力等均显著降低。通过透射电子显微镜和Annexin V-FITC/碘化丙啶染色评估, 证实ph-ph+可通过诱导细胞凋亡杀灭M. furfur。将ph-ph+涂抹于由M. furfur诱发的小鼠皮肤感染模型中, 结果显示ph-ph+能够有效清除小鼠皮肤表面的真菌, 且不引起皮肤刺激或其他不良反应。本研究表明, ph-ph+可能是一种有别于传统药物的新型抗菌化合物, 同时本研究也为治疗M. furfur或其他真菌所致的皮肤感染提供了一种潜在治疗方法。实验方案由西南大学动物实验伦理委员会批准(批准号: LAC2024-1-0446), 严格按照动物使用和护理的伦理原则进行实验操作。

糠秕马拉色菌  /  质子型双菲啰啉  /  凋亡  /  皮肤感染  /  抗真菌机制

Malassezia furfur (M. furfur) is a common lipophilic fungus with strong epidermal colonization ability and high recurrence rates, capable of inducing a wide range of skin diseases in both animals and humans. Traditional antifungal therapies are associated with significant side effect and frequent drug resistance, necessitating the development of new treatment strategies. This study investigated the efficacy of a protonated phenanthroline-phenanthroline+ (ph-ph+) compound, previously developed by our team, in inhibiting the growth and reproduction of M. furfur. The results showed that the minimum inhibitory concentration (MIC) and minimum fungicidal concentration (MFC) of ph-ph+ against M. furfur were 2 and 8 µg·mL-1, respectively. Furthermore, ph-ph+ significantly reduced key virulence characteristics of M. furfur, including biofilm formation, hydrophobicity, and adhesion capacity. Assessments using transmission electron microscopy and Annexin V-FITC/propidium iodide staining confirmed that ph-ph+ kills M. furfur by inducing apoptosis. In a mouse skin infection model induced by M. furfur, topical application of ph-ph+ effectively cleared the fungus from the skin surface without causing skin irritation or other adverse reactions. This study demonstrates that ph-ph+ may represent a novel antimicrobial compound distinct from traditional drugs and provides a potential therapeutic approach for treating skin infections caused by M. furfur or other fungi. The experimental protocol was approved by the Animal Experiment Ethics Committee of Southwest University (approval No.: LAC2024-1-0446), and the experiments were conducted strictly in accordance with the ethical principles for the use and care of animals.

Malassezia furfur  /  phenanthroline-phenanthroline+  /  apoptosis  /  skin infection  /  antifungal mechanism
冯义骁, 阳恩萍, 秦汉, 李景丽, 朱可敬, 卢玘涵, 付爱玲. 质子型双菲啰啉抗糠秕马拉色菌皮肤感染的作用及机制. 药学学报, 2026 , 61 (7) : 2495 -2501 . DOI: 10.16438/j.0513-4870.2025-1480
Yi-xiao FENG, En-ping YANG, Han QIN, Jing-li LI, Ke-jing ZHU, Qi-han LU, Ai-ling FU. Antifungal activity and mechanism of phenanthroline-phenanthroline+ against cutaneous Malassezia furfur infection[J]. Acta Pharmaceutica Sinica, 2026 , 61 (7) : 2495 -2501 . DOI: 10.16438/j.0513-4870.2025-1480
正文
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最近20年间, 糠秕马拉色菌(Malassezia furfur, M. furfur) 的研究颠覆了人们对它的认知。作为人体皮肤微生态中最主要的共生真菌之一, 它长期定居于皮脂腺丰富的区域, 曾被视作“无害共生菌”的微生物, 如今已处于危害人类以及犬、猫等宠物皮肤健康的中心位置[1, 2]。现代技术的进步逐渐揭示M. furfur不仅是花斑癣、脂溢性皮炎和毛囊炎的元凶, 更深度参与了特应性皮炎、脱发, 甚至某些系统性感染如胰腺癌的发病进程[3-6]。
目前, 临床治疗M. furfur感染主要依赖唑类和烯丙胺类抗真菌药物。唑类药物通过抑制麦角固醇合成关键酶ERG11, 破坏真菌细胞膜完整性, 如局部应用的酮康唑、咪康唑及系统性使用的伊曲康唑、氟康唑等[7, 8]。烯丙胺类药物以特比萘芬为代表, 通过抑制角鲨烯环氧化酶阻断麦角固醇合成[9, 10]。然而, 真菌对这些药物的耐药率因靶点突变和外排泵激活而持续上升, 特比萘芬的耐药性在部分地区也已超过10%[11, 12]。总体而言, 现有抗M. furfur药物种类有限, 耐药性问题日益严峻, 亟需开发新型作用机制的抗真菌药物。
质子型双菲啰啉(phenanthroline-phenanthroline+, ph-ph+) 是本团队自主合成的质子型氢键二聚体化合物(图1)。前期的研究表明, ph-ph+具有广谱抗菌性, 能有效抑制红色毛癣菌、白色念珠菌等多种真菌生长和繁殖[13, 14]。为此, 本研究聚焦于临床耐药严峻的糠秕马拉色菌, 旨在探究ph-ph+对其的抗菌活性及作用机制, 以寻找潜在的替代治疗方案。
材料与方法
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实验菌株  糠秕马拉色菌(ATCC 44344) 购自北京保藏生物科技有限公司。
实验试剂和材料  ph-ph+由本实验室合成, mDxion培养基购于青岛北岸实验科技有限公司; 氟康唑购于上海源叶生物科技有限公司; 特比萘芬购于上海阿拉丁生化科技股份有限公司; 线粒体呼吸链复合物Ⅰ~Ⅳ检测试剂盒购于南京草本源生物科技有限公司; Annexin V-FITC/碘化丙啶购于北京索莱宝科技有限公司; MMP检测试剂盒(JC-1)、ATP含量检测试剂盒购于上海碧云天生物技术有限公司。
动物  健康雄性昆明种小鼠购于湖南斯莱克景达实验动物有限公司, 饲养于西南大学药学院SPF级实验动物中心。动物实验经西南大学实验动物伦理审查委员会批准(批准号: LAC2024-1-0446)。
真菌悬液的制备  从4 ℃保存的mDxion固体培养板上挑取M. furfur单菌落接种到mDxion培养液中, 37 ℃震荡培养至对数生长期, 用血细胞计数板调整M. furfur菌液浓度为1×106 CFU·mL-1。
最低抑菌浓度(minimum inhibitory concentration, MIC) 和最低杀菌浓度(minimum fungicidal concentration, MFC) 的检测  在96孔板的每孔中加入100 μL mDxion液体培养基, 然后加入等比稀释的ph-ph+溶液, 浓度从256 µg·mL-1至0.5 µg·mL-1, 将50 μL M. furfur菌悬液接种到每个培养孔, 随后把96孔板置于37 ℃的恒温培养箱中, 在培养24 h后, 肉眼观察培养基的浑浊程度, 同时通过酶标仪检测每孔的A600, 以确定MIC的数值。随后吸取澄清的孔内溶液20 μL于mDxion固体培养基上, 置于37 ℃的恒温培养箱中培养24 h, 没有菌落的最低ph-ph+溶液浓度即为MFC100%。同时使用同样的方法检测咪康唑和特比萘芬对M. furfur的MIC和MFC。
径向生长抑制实验  用打孔器将滤纸加工成直径为0.5 cm的圆形纸片, 灭菌后备用。在mDxion培养基中添加ph-ph+溶液, 使培养基中ph-ph+的浓度分别为2、4和8 µg·mL-1, 同时设置相应的空白对照组。将滤纸片平放在固体培养基表面, 吸取10 µL菌液接种到滤纸片的中央位置, 待菌液自然风干后, 置于37 ℃的恒温培养箱中培养24 h。培养结束后, 对培养皿进行拍照记录, 测量并记录菌落的生长直径。每个培养基上放置3个滤纸片, 并且每组实验均重复进行3次。菌落径向生长(cm) 的计算方式为: 菌落直径平均值减0.5 cm; 抑制菌落径向生长百分率(%) 的计算公式为: (空白组菌落直径-实验组菌落直径) ÷空白组菌落直径×100%, 用同样的方法检测M. furfur在8 µg·mL-1特比萘芬和咪康唑作用下的径向生长并计算抑制率, 同时与相同浓度的ph-ph+进行比较。
ph-ph+活性与温度关系  将相同浓度的M. furfur菌悬液分别置于4和37 ℃两种实验温度中, 通过肉汤稀释法检测在4和37 ℃下ph-ph+的抗菌活性, 每隔4 h使用酶标仪检测600 nm处菌液的吸光度。ph-ph+的浓度分别为2、4和8 µg·mL-1。以生理盐水作为空白对照, 计算不同温度下ph-ph+对M. furfur的抑菌率。抑菌率计算公式: 抑菌率(%) = [(A实验组-A空白组)/(A阴性对照-A空白对照)]×100%。
孢子萌发率的检测  使用灭菌漏斗和两层灭菌滤纸过滤M. furfur菌悬液, 如此操作重复两次得到孢子悬液。将终浓度为2、4或8 μg·mL-1 ph-ph+溶液分别加入到孢子悬液中, 每组3次平行实验。将试管放置于37 ℃恒温培养箱中培养24 h后取出。每管样品取5 μL滴加在载玻片上, 在显微镜下随机选取3个视野, 使用计数器分别记录每个视野中的总孢子数和已萌发孢子数。孢子萌发率计算公式: 每个视野的萌发率(%) = (已萌发孢子数÷总孢子数) ×100%, 用同样的方法检测M. furfur在8 µg·mL-1特比萘芬和咪康唑作用下的孢子萌发率, 同时与相同浓度的ph-ph+进行比较。
生物膜抑制实验  在96孔板中加入100 μL mDxion液体培养基, 然后加入等比稀释的ph-ph+溶液100 μL, 终浓度依次从256 µg·mL-1到0.5 µg·mL-1, 接种入1×106 CFU·mL-1 M. furfur后, 置于37 ℃恒温培养箱中培养24 h。培养结束后, 倒掉96孔板中的培养基, 无菌PBS轻轻冲洗孔板3次后, 每孔加入100 μL 0.1%结晶紫溶液, 室温下染色20 min, 然后用无菌蒸馏水冲洗孔板。待孔板自然干燥后, 加入100 μL 33%冰醋酸溶液, 振荡10 min以溶解结合在生物膜上的结晶紫, 酶标仪检测每孔的A570值, 用同样的方法检测M. furfur在8 µg·mL-1特比萘芬和咪康唑作用下的生物膜的抑制情况, 同时与相同浓度的ph-ph+进行比较。
疏水率检测实验  将ph-ph+溶液加入到菌悬液中, 终浓度分别为2、4或8 μg·mL-1。将试管放置于37 ℃恒温培养箱中培养24 h后取出。离心收集每管的M. furfur, PBS洗涤2次后加入适量无菌生理盐水, 重悬细胞, 调整细胞悬液的浓度至A600为0.5, 记为初始吸光度值(A0)。然后加入与样品等体积的正十六烷, 用涡旋振荡器剧烈振荡试管5 min, 使细胞充分分散在水相和有机相的界面, 室温静置30 min, 弃去有机相, 用分光光度计在600 nm波长下测定吸光度值, 记为A1。疏水率的计算公式为疏水率(%) = (1-A1/A0) ×100%, 用同样的方法检测M. furfur在8 μg·mL-1特比萘芬和咪康唑作用下的疏水率, 同时与相同浓度的ph-ph+进行比较。
黏附能力抑制实验  离心收集试管中经ph-ph+处理的M. furfur, 用PBS洗涤2次后, 用无菌生理盐水调至1×106 CFU·mL-1。将100 μL菌液置于固体培养基上在37 ℃恒温培养箱中培养4 h, 使用无菌的PBS洗涤2次, 观测其黏附能力。用同样的方法检测M. furfur在8 µg·mL-1特比萘芬和咪康唑作用下的黏附能力, 同时与相同浓度的ph-ph+进行比较。
ph-ph+诱导M. furfur凋亡的检测  使用Annexin V-FITC凋亡检测试剂盒检测M. furfur的凋亡。将终浓度分别为2、4或8 μg·mL-1 ph-ph+溶液加入400 μL菌悬液中, 放置于37 ℃恒温培养箱中培养3 h后取出, 离心收集菌体并用PBS洗涤, 调整菌液浓度为1×106 CFU·mL-1。向菌悬液中加入5 μL Annexin V-FITC, 轻轻混匀, 避光孵育15 min, 然后加入10 μL PI染液, 轻轻混匀, 避光孵育5 min。取3 μL染色后的悬液滴在载玻片上, 盖上盖玻片, 在荧光显微镜下分别用FITC和PI的激发滤光片观察。
透射电子显微镜观察  使用透射电子显微镜观察8 μg·mL-1 ph-ph+处理3 h的M. furfur形态。
制备小鼠皮肤感染模型实验  将32只健康小鼠麻醉后进行背部脱毛处理, 将一小块胶带粘贴至小鼠背部再撕下, 更换新鲜的胶带重复操作5次, 破坏皮肤屏障以至其轻微渗出血, 每天2次, 连续3天。随后用一次性医用棉签蘸取M. furfur橄榄油菌悬液均匀涂抹在小鼠背部, 当小鼠背部皮肤出现明显的红斑、瘙痒、脱屑、渗出等症状时, 随机将小鼠分为4组, 分别为空白组、模型组、特比萘芬对照组、ph-ph+实验组。特比萘芬组凝胶的用量为1.0 mg·cm-2 (每克含特比萘芬0.01 mg), 每日2次; 实验组涂抹制备好的ph-ph+凝胶, 用量为1.0 mg·cm-2 (每克含ph-ph+ 0.01 mg), 每日2次; 空白组和模型组涂抹未含有任何药物的空白凝胶, 记录小鼠感染M. furfur部位的皮肤状况。
皮肤组织病理学检测  将小鼠麻醉后, 使用游标卡尺轻压皮肤, 测量背部皮肤厚度, 每个部位测3次取均值, HE染色观测皮肤组织。此外, 取小鼠感染背部皮肤进行匀浆, 然后用PBS将匀浆液稀释100倍, 将60 µL匀浆液均匀地接种到mDixon固体培养基上, 放置于恒温生化培养箱中, 37 ℃培养24 h后统计真菌菌落数。
统计学分析  数据表示为平均值±标准差(SD), 所有统计分析均使用IBM SPSS 22.0软件进行。使用单因素方差分析(ANOVA) 检验分析平均值的显著差异(P < 0.05) 和高度显著差异(P < 0.01)。
结果
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1　MIC和MFC的测定
测定结果显示, ph-ph+抑制M. furfur的MIC和MFC值分别为2和8 µg·mL-1, 与特比萘芬相同(特比萘芬MIC和MFC为2和8 µg·mL-1), 而咪康唑的MIC和MFC值分别为8和64 µg·mL-1。ph-ph+的MIC和MFC值分别为咪康唑的1/4和1/8, 表明ph-ph+和特比萘芬对M. furfur的抑菌效果和杀菌效果相当, 且均优于咪康唑。此外, 本研究团队[14]前期检测了ph-ph+对临床真菌红色毛癣菌(T. rubrum) 的MIC值为2 µg·mL-1, MFC值为8 µg·mL-1, 对白色念珠菌(C. albicans) 的MIC和MFC值分别为2、8 µg·mL-1[13], 其结果说明ph-ph+对多种真菌具有良好的抑菌效果和杀菌效果。
2　ph-ph+可抑制M. furfur的径向生长
如图2A、B所示, ph-ph+可明显抑制M. furfur的径向生长, 且抑制效果呈现剂量依赖性。当ph-ph+的浓度为8 µg·mL-1时, 其抑制生长率可达到100%。8 µg·mL-1特比萘芬抑制效果和同浓度的ph-ph+相当, 且远优于相同浓度的咪康唑。
3　温度对ph-ph+的抑菌活性的影响
真菌对温度的耐受范围较广, 具有较强的抵抗不良环境的能力。选取4 ℃和人体温度37 ℃作为实验温度, 结果如图3A所示, M. furfur在37 ℃下生长活性较高, 4 ℃时仍保留着微弱的生长活性。但加入ph-ph+后, 无论4或37 ℃, ph-ph+对M. furfur的抑制率均呈剂量依赖性, 且几乎没有差别(图3B), 证明温度对ph-ph+的抑菌活性影响较小。
4　ph-ph+可抑制M. furfur的孢子萌发
如图4A显示, 随着ph-ph+浓度的增加, M. furfur孢子萌发率呈现明显的下降趋势。在2 µg·mL-1 ph-ph+处理组中, M. furfur孢子萌发率虽有一定程度降低, 但仍维持在相对较高水平。但当药物浓度达到4 µg·mL-1时, M. furfur孢子萌发率显著降低。图4B显示, 8 µg·mL-1 ph-ph+和特比萘芬作用后的M. furfur孢子萌发率几乎在同一水平, 且远低于8 µg·mL-1咪康唑处理后的M. furfur孢子萌发率。
5　ph-ph+抑制M. furfur生物膜的形成
M. furfur的生物膜是由该菌自身分泌的胞外多聚物(如多糖、蛋白质等) 包裹菌体细胞所形成的结构, 具有保护菌体、增强对环境压力的抵抗力等作用。生物膜的存在增强了真菌的黏附能力, 使其能够牢固地附着在宿主皮肤角质层表面, 逃避宿主免疫细胞的识别和清除, 同时为自身提供了一个物理屏障, 能有效阻挡外界环境中的不利因素, 如抗菌药物、宿主免疫系统的攻击等。随着ph-ph+的剂量增大, M. furfur生物膜断裂程度越明显, 表明ph-ph+可抑制M. furfur生物膜的形成(图5A)。8 µg·mL-1 ph-ph+和特比萘芬作用后的M. furfur生物膜成膜率几乎在同一水平, 且远低于8 µg·mL-1咪康唑处理后的M. furfur生物膜成膜率(图5B)。
6　ph-ph+对M. furfur疏水率的影响
M. furfur的疏水率在其生存与致病过程中具有重要的作用。较高的疏水率使该菌更有效地附着在亲脂性的皮肤表面以及毛囊等特定部位, 同时M. furfur凭借疏水特性, 可逃避外界不利因素的影响, 为自身在皮肤环境中的生存、繁殖以及致病过程发挥关键作用。本实验结果显示, M. furfur的疏水率随着ph-ph+的剂量增大而显著降低, 证明ph-ph+可降低M. furfur的疏水率(图6A)。8 µg·mL-1 ph-ph+和特比萘芬作用后的M. furfur疏水率几乎在同一水平, 且低于8 µg·mL-1咪康唑处理后的M. furfur疏水率(图6B)。
7　ph-ph+可降低真菌的黏附能力
如图7A、B所示, ph-ph+可影响M. furfur的黏附能力, 能够抑制M. furfur对环境的黏附, 且抑制效果呈现剂量依赖性。图7C显示, 8 µg·mL-1 ph-ph+和特比萘芬作用后的M. furfur黏附率几乎在同一水平, 且低于8 µg·mL-1咪康唑处理后的M. furfur黏附率。
8　ph-ph+可诱导M. furfur细胞凋亡
使用Annexin V-FITC/PI双荧光染色鉴定ph-ph+是否能够诱导M. furfur的凋亡。如图8所示, 浓度为2 μg·mL-1 ph-ph+绿色荧光相对较多, 表明细胞多处于凋亡早期, 当浓度增加到8 μg·mL-1时红色荧光更加明显, 表明该浓度下细胞多处于凋亡晚期。本实验说明, ph-ph+呈剂量相关性诱导M. furfur细胞凋亡。
9　透射电子显微镜观察
为观测ph-ph+作用于M. furfur后的分生孢子和菌丝的显微结构变化, 研究采用透射电镜, 对正常和经ph-ph+处理的M. furfur进行观察。结果如图9所示, 正常的分生孢子和菌丝具有完整的细胞结构, 且细胞紧密, 内容物完整。然而, ph-ph+作用后M. furfur的细胞内容物降解消融直至空泡化, 呈现出典型凋亡样貌。
10　ph-ph+抑制皮肤M. furfur感染
如图10所示, 空白对照的8只小鼠皮肤正常, 但模型组的8只小鼠背部均有大量皮屑、褶皱和红斑。模型组小鼠均有皮肤瘙痒症状, 抓挠次数增多。对模型小鼠背部给药3天后, 特比萘芬阳性对照组和ph-ph+凝胶实验组的小鼠背部红肿现象基本消退, 只留存极少量的皮屑, 背部皮肤基本恢复光滑。
11　皮肤菌量检测
为了判断给药后小鼠病变部位皮肤是否含有真菌, 在处死小鼠后分别取3处不同位置的小鼠背部皮肤组织进行真菌培养。如图11所示, 模型组的皮肤组织中可培养出大量的真菌, 但经ph-ph+或特比萘芬处理后, 培养基上没有真菌生长, 表明真菌已被清除, 并且特比萘芬和ph-ph+二者治疗效果良好且不分伯仲。
12　小鼠皮肤组织HE染色
给药3天后处死小鼠, 分离皮肤组织并进行切片和染色。HE结果如图12所示, 模型组小鼠皮肤呈现出显著的病理改变, 包括角质层增厚、颗粒层细胞增多、皮脂腺增生等, 而ph-ph+组和特比萘芬阳性对照组小鼠的角质层恢复正常, 棘层和颗粒层厚度减小, 皮肤整体恢复正常。
讨论
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本研究评估了ph-ph+对M. furfur的抗菌活性及可能机制, 结果证明了ph-ph+在体外和体内均表现出显著的抗真菌效果, 其机制涉及诱导细胞凋亡, 本研究为开发新型抗M. furfur药物提供了重要依据。
体外实验结果表明, ph-ph+具有良好的杀菌能力, 其MIC和MFC值分别为2和8 µg·mL-1, 与目前临床一线药物特比萘芬相当。进一步研究显示, ph-ph+不仅能有效抑制M. furfur的径向生长和孢子萌发, 还可显著削弱其毒力因子, 包括生物膜形成能力、细胞表面疏水性及黏附能力等, 从而降低M. furfur在宿主皮肤上的定植能力和致病性, 提示ph-ph+可多方面抑制真菌感染。
值得关注的是, 在本研究合成的一系列结构类似化合物中, 仅ph-ph+表现出对M. furfur的显著抗菌活性, 其余同类化合物在相同浓度下均未检测到抑制效果。这一结果说明ph-ph+的抗真菌作用具有结构特异性, 而非源于非选择性的细胞毒性, 为其选择性抗真菌潜力提供了化学基础。
机制研究表明, ph-ph+通过诱导M. furfur细胞凋亡发挥杀菌作用。Annexin V-FITC/PI荧光染色结果证明, 随着ph-ph+的浓度升高, 细胞由早期凋亡过渡为晚期凋亡; 透射电镜观察进一步证实, ph-ph+处理后的菌体出现内容物降解和空泡化等典型凋亡特征。以往的研究显示, ph-ph+可通过破坏线粒体呼吸链功能而发挥作用。该机制与目前广泛使用的抗真菌药物(如唑类和烯丙胺类) 通过抑制麦角固醇合成途径有所不同, 有望避免现有药物的耐药性问题。
在动物模型中, ph-ph+表现出良好的治疗效果, 能够显著改善M. furfur感染引起的皮肤红斑、脱屑及增厚等病理症状, 其疗效与特比萘芬相当。组织培养与病理切片进一步证实, ph-ph+可彻底清除皮肤中的真菌, 且未引起明显皮肤刺激或不良反应, 显示出良好的生物相容性和应用前景。
综上所述, ph-ph+作为一种结构新颖的质子型化合物, 具有强效的抗M. furfur活性, 其作用机制主要通过诱导细胞凋亡实现。该化合物不仅具备与传统药物相当的疗效, 还可能具有多靶点、低耐药的特性。未来的研究可进一步探索其在不同真菌感染模型中的适用性, 为推动其临床转化提供更多实验支持。

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doi: 10.16438/j.0513-4870.2025-1480
  • 接收时间：2025-12-10
  • 首发时间：2026-09-21
  • 出版时间：2026-07-12
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  • 收稿日期：2025-12-10
  • 修回日期：2026-02-24
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    西南大学药学院, 重庆 400716

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2种不同金属材料的力学参数
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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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