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Article(id=1208491449142850078, tenantId=1146029695717560320, journalId=1189982191388893191, issueId=1208491447892947355, articleNumber=null, orderNo=null, doi=10.16438/j.0513-4870.2020-1642, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1603123200000, receivedDateStr=2020-10-20, revisedDate=1609257600000, revisedDateStr=2020-12-30, acceptedDate=null, acceptedDateStr=null, onlineDate=1766056414160, onlineDateStr=2025-12-18, pubDate=1623427200000, pubDateStr=2021-06-12, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1766056414160, onlineIssueDateStr=2025-12-18, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1766056414160, creator=13701087609, updateTime=1766056414160, updator=13701087609, issue=Issue{id=1208491447892947355, tenantId=1146029695717560320, journalId=1189982191388893191, year='2021', volume='56', issue='6', pageStart='1513', pageEnd='1748', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1766056413863, creator=13701087609, updateTime=1766137152975, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1208830092319519523, tenantId=1146029695717560320, journalId=1189982191388893191, issueId=1208491447892947355, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1208830092319519524, tenantId=1146029695717560320, journalId=1189982191388893191, issueId=1208491447892947355, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=1537, endPage=1543, ext={EN=ArticleExt(id=1208491449625195098, articleId=1208491449142850078, tenantId=1146029695717560320, journalId=1189982191388893191, language=EN, title=Progress in antitumor activity of baicalin, columnId=1190335348648547107, journalTitle=Acta Pharmaceutica Sinica, columnName=Reviews, runingTitle=null, highlight=null, articleAbstract=

Flavonoids baicalin is the main bioactive component extracted from Scutellaria baicalensis Georgi. Baicalin has high medicinal value and shows extensive pharmacological effects including antitumor, antibiosis, anti-inflammatory, antioxidation, neuro-protection, and significant potential in tumor treatment. Recent studies have shown that baicalin suppresses the growth of many kinds of human cancer. The underlying mechanisms include induction of apoptosis, induction of cell cycle arrest, inhibition of tumor metastasis, suppression of angiogenesis, and so on. This article reviewed the research progress of baicalin on its antitumor pharmacology and possible mechanisms at home and abroad, and provided the basis for its further research.

, correspAuthors=Qing-long GUO, authorNote=null, correspAuthorsNote=null, copyrightStatement=Copyright ©2021 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, authorCompany=null, fund=null, authors=null, authorsList=Bang-yan KONG, li-bin WEI, Qing-long GUO), CN=ArticleExt(id=1208491451378414247, articleId=1208491449142850078, tenantId=1146029695717560320, journalId=1189982191388893191, language=CN, title=黄芩苷的抗肿瘤作用研究进展, columnId=1190335349655180086, journalTitle=药学学报, columnName=综述, runingTitle=null, highlight=null, articleAbstract=

黄芩苷(baicalin)是从唇形科植物黄芩(Scutellaria baicalensis Georgi)中提取的主要生物活性成份，属于黄酮类化合物，黄芩苷药用价值高，具有抗菌、抗炎、抗氧化和保护神经等多种药理作用，并显示出巨大的抗肿瘤潜力。近几年研究发现，黄芩苷对人多种肿瘤具有较好的抑制作用，其作用机制包括诱导肿瘤细胞凋亡、抑制肿瘤迁移侵袭、诱导肿瘤细胞周期阻滞和抑制肿瘤血管生成等。现概述国内外对黄芩苷抗肿瘤药理作用及机制的研究进展，为黄芩苷的深入研究提供依据。

, correspAuthors=郭青龙, authorNote=null, correspAuthorsNote=
*郭青龙, Tel: 13801586679, E-mail:
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No. Indication Cell line IC50/µmol·L-1 (24 h) Target
1 Pancreatic cancer SW1990 < 160 JNK/Foxo1/BIM
2 Liver cancer HepG2 & SMMC-7721 < 40 Intrinsic caspase
3 Colon cancer DLD1 & HCT-116 < 40 Wnt
4 Cervical cancer HeLa & SiHa < 30 PKC/STAT3
5 NSCLC H1299 < 80 SIRT1/AMPK
6 Lung cancer H441 < 400 (48 h) PBK/TOPK
7 Osteosarcoma U-2 OS < 100 Akt/CDK4
8 Breast cancer 4T1 < 40 NF-κB
9 AML HL-60 & HL-60/DOX < 30 PI3K/Akt
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Advances in therapy by baicalin for cancer. JNK: c-Jun N-terminal kinase; Foxo1: Forkhead box protein O1; BIM: Bcl-2 interacting mediator of cell death; PKC: Protein kinase C; STAT: Signal transducer and activator of transcription; NSCLC: Non-small cell lung cancer; SIRT1: Activation of the sirtuin 1 gene; AMPK: Adenosine monophosphate-activated protein kinase gene; PBK/TOPK: PDZ-binding kinase/T-LAK cell-originated protein kinase; Akt: Protein kinase B; CDK: Cyclin dependent kinase; NF-κB: Nuclear factor kappa B; AML: Acute myeloid leukaemia; PI3K: Phosphatidylinositol 3 kinase; IC50: Half maximal inhibitory concentration

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No. Indication Cell line IC50/µmol·L-1 (24 h) Target
1 Pancreatic cancer SW1990 < 160 JNK/Foxo1/BIM
2 Liver cancer HepG2 & SMMC-7721 < 40 Intrinsic caspase
3 Colon cancer DLD1 & HCT-116 < 40 Wnt
4 Cervical cancer HeLa & SiHa < 30 PKC/STAT3
5 NSCLC H1299 < 80 SIRT1/AMPK
6 Lung cancer H441 < 400 (48 h) PBK/TOPK
7 Osteosarcoma U-2 OS < 100 Akt/CDK4
8 Breast cancer 4T1 < 40 NF-κB
9 AML HL-60 & HL-60/DOX < 30 PI3K/Akt
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黄芩苷的抗肿瘤作用研究进展
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孔邦彦 , 魏立彬 , 郭青龙 *
药学学报 | 综述 2021,56(6): 1537-1543
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药学学报 | 综述 2021, 56(6): 1537-1543
黄芩苷的抗肿瘤作用研究进展
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孔邦彦, 魏立彬, 郭青龙*
作者信息
  • 中国药科大学基础医学与临床药学学院, 江苏 南京 211198

通讯作者:

*郭青龙, Tel: 13801586679, E-mail:
Progress in antitumor activity of baicalin
Bang-yan KONG, li-bin WEI, Qing-long GUO*
Affiliations
  • School of Basic Medicine and Clinical Pharmacy, China Pharmaceutical University, Nanjing 211198, China
出版时间: 2021-06-12 doi: 10.16438/j.0513-4870.2020-1642
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摘要
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黄芩苷(baicalin)是从唇形科植物黄芩(Scutellaria baicalensis Georgi)中提取的主要生物活性成份，属于黄酮类化合物，黄芩苷药用价值高，具有抗菌、抗炎、抗氧化和保护神经等多种药理作用，并显示出巨大的抗肿瘤潜力。近几年研究发现，黄芩苷对人多种肿瘤具有较好的抑制作用，其作用机制包括诱导肿瘤细胞凋亡、抑制肿瘤迁移侵袭、诱导肿瘤细胞周期阻滞和抑制肿瘤血管生成等。现概述国内外对黄芩苷抗肿瘤药理作用及机制的研究进展，为黄芩苷的深入研究提供依据。

黄芩苷  /  肿瘤治疗  /  细胞周期  /  凋亡  /  侵袭转移

Flavonoids baicalin is the main bioactive component extracted from Scutellaria baicalensis Georgi. Baicalin has high medicinal value and shows extensive pharmacological effects including antitumor, antibiosis, anti-inflammatory, antioxidation, neuro-protection, and significant potential in tumor treatment. Recent studies have shown that baicalin suppresses the growth of many kinds of human cancer. The underlying mechanisms include induction of apoptosis, induction of cell cycle arrest, inhibition of tumor metastasis, suppression of angiogenesis, and so on. This article reviewed the research progress of baicalin on its antitumor pharmacology and possible mechanisms at home and abroad, and provided the basis for its further research.

baicalin  /  tumor therapy  /  cell cycle  /  apoptosis  /  invasion and metastasis
孔邦彦, 魏立彬, 郭青龙. 黄芩苷的抗肿瘤作用研究进展. 药学学报, 2021 , 56 (6) : 1537 -1543 . DOI: 10.16438/j.0513-4870.2020-1642
Bang-yan KONG, li-bin WEI, Qing-long GUO. Progress in antitumor activity of baicalin[J]. Acta Pharmaceutica Sinica, 2021 , 56 (6) : 1537 -1543 . DOI: 10.16438/j.0513-4870.2020-1642
正文
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黄芩是中国传统中草药的大宗品种, 始载于东汉《神农本草经》, 距今已有近两千年人类用药史。黄芩苷是黄芩中所含黄酮类化合物, 是传统中草药黄芩的主要活性成分。目前, 已从黄芩中发现多种黄酮化合物, 其中含量较高且药理作用明显的主要是黄芩苷(baicalin)、黄芩素(baicalein)、汉黄芩苷(wogonoside) 和汉黄芩素(wogonin) 等[1]。传统医学认为黄芩具有清热燥湿和泻火解毒的作用。现代医学发现, 黄芩苷具有抗肿瘤、广谱抗菌、抗炎、抗氧化和保护神经等多种药理作用。黄芩苷在体内可与其苷元黄芩素相互转化[2], 但业内主流观点认为黄芩苷为二者中发挥药理活性的主要物质。
恶性肿瘤作为目前尚未攻克的人类重大疾病, 如何安全、有效地治疗肿瘤一直以来是药学研究的热点问题。天然化合物具有高疗效、低毒性的特点, 在化学预防和化学治疗中的潜在药用价值越来越受到人们的关注。近年来, 国内外研究机构从各个方面对黄芩苷抗肿瘤作用及作用机制做了深入研究, 发现黄芩苷具有温和的抗肿瘤药理活性, 其作用机制包括诱导肿瘤细胞凋亡、抑制肿瘤迁移侵袭、诱导肿瘤细胞周期阻滞、抑制肿瘤血管生成和克服肿瘤耐药性等。黄芩苷作为有着千年用药史的黄酮类天然化合物, 其毒副作用较小, 用药较为安全。本文就黄芩苷抗肿瘤作用及其可能的机制的最新研究进展作一综述, 为黄芩苷的进一步开发和应用于临床提供依据(图 1)。
1 诱导肿瘤细胞凋亡
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细胞凋亡是由基因控制的细胞主动死亡过程。肿瘤细胞凋亡抵抗不仅是肿瘤发生发展的原因, 也会导致肿瘤对治疗产生耐药性。目前, 临床治疗肿瘤中使用的大多数抗癌药物利用凋亡信号通路来触发癌细胞死亡[3]。
有文献报道称, 黄芩苷可促胰腺癌SW1990细胞株凋亡[4]。流式细胞术与4', 6-二脒基-2-苯基吲哚(4', 6-diamidino-2-phenylindole, DAPI) 染色实验显示, 黄芩苷明显促进SW1990细胞凋亡, 与黄芩苷共孵育的SW1990细胞凋亡水平呈剂量依赖性增加。此外, 黄芩苷呈剂量依赖性上调线粒体Bax (Bcl2-associated X protein)、切割型caspase-3和p53表达, 同时显著降低B细胞淋巴瘤因子2 (B-cell leukemia/lymphoma 2, Bcl-2) 蛋白水平。进一步研究表明, 黄芩苷可能通过激活JNK/Foxo1/BIM (c-Jun N-terminal kinase/forkhead box protein O1/Bcl-2 interacting mediator of cell death) 途径促进胰腺癌细胞凋亡。
研究表明, 黄芩苷可诱导肝癌细胞系HepG2和SMMC-7721细胞凋亡[5], 且半数抑制浓度(half maximal inhibitory concentration, IC50) 皆小于40 μmol·L-1。根据对Bax、Bcl-2和聚腺苷酸二磷酸核糖转移酶-1 (poly ADP-ribose polymerase-1, PARP-1) 等多种介导凋亡的细胞因子分析, 黄芩苷促进肝癌细胞凋亡的机制可能是激活线粒体介导的内源性caspase途径。同时, 体内研究也表明黄芩苷具有选择性杀伤肿瘤细胞的能力。用50和100 mg·kg-1黄芩苷能显著抑制裸鼠异位异种移植瘤的生长, 对小鼠体重无明显影响。
此外, 还有研究表明黄芩苷可以通过抑制Wnt (wingless-related integration) 信号通路诱导结肠癌细胞凋亡[6]。Wnt信号通路与许多人类肿瘤, 特别是与结直肠癌的发生发展密切相关[7, 8]。黄芩苷处理后结肠癌DLD1和HCT-116细胞的凋亡率均显著增加。黄芩苷通过miR217/DKK1 (microRNA-217/dickkopf) 抑制Wnt信号通路, 降低其下游β-连环蛋白和c-Myc原癌基因蛋白(MYC proto-oncogene, c-Myc) 的表达引起细胞凋亡。
黄芩苷与其他药物联合应用对白血病有良好的疗效。六亚甲基双乙酰胺(hexamethylene bis-acetamide, HMBA) 可增强黄芩苷诱导人白血病细胞凋亡的作用[9]。HMBA和黄芩苷均具有抗白血病活性, 二者联合应用可协同抑制急性髓系白血病(acute myeloid leukemia, AML) 细胞增殖, 诱导细胞凋亡, 效果大于二者单一用药效果的总和。联合治疗诱导的凋亡事件比单一治疗组更明显, 通过Bcl-2/Bax、Bcl-XL/Bax比值降低、caspase-9激活等内源性途径及Fas和caspase-8激活介导的外源性途径触发细胞凋亡。二者联合用药对单核细胞毒性较弱。以上结果表明, 黄芩苷和HMBA联合应用可能是一种有前途的AML治疗方案。
2 抑制肿瘤的侵袭和转移
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侵袭与转移是恶性肿瘤显著的生物学特性, 在肿瘤复发、化疗失败的事件中扮演着重要角色。研究表明, 增强的侵袭能力将增加肿瘤细胞从原发性肿瘤块中逃逸的能力, 这是导致肿瘤复发的关键因素。基质金属蛋白酶家族(mitochondrial membrane potential, MMPs), 尤其是基质金属蛋白酶-2 (MMP2)、基质金属蛋白酶-9 (MMP9) 两种酶在提高多种肿瘤侵袭转移能力方面扮演着重要的作用[10]。
多项研究表明, 黄芩苷能够通过抑制MMP2和MMP9的表达水平及活性, 有效抑制多种肿瘤的体外侵袭、迁移和黏附能力。黄芩苷呈剂量依赖性抑制人宫颈癌细胞系HeLa和SiHa细胞的迁移和侵袭[11]。其通过抑制宫颈癌细胞中蛋白激酶C和信号转导与转录激活因子3 (protein kinase C/signal transducer and activator of transcription 3, PKCζ/STAT3) 信号传导, 以浓度依赖性方式下调MMP2、MMP9和生存素等PKCζ/STAT3信号通路靶基因的蛋白表达水平。此外, 黄芩苷还可通过p38-MAPK通路下调MMP2、MMP9的表达水平来抑制宫颈癌HeLa细胞的迁移和侵袭, 并在一定程度内呈现浓度依赖效应[12]。
腺苷酸活化蛋白激酶(AMP-activated protein kinase, AMPK) 广泛存在于真核生物中, 调控细胞能量代谢, 与肿瘤进展相关。AMPK磷酸化可导致基质金属蛋白酶表达, 促进肿瘤的侵袭与转移[13]。You等[14]发现黄芩苷在体外呈剂量依赖性抑制人非小细胞肺癌A549和H1299细胞的存活、迁移和侵袭。黄芩苷通过激活雷帕霉素靶蛋白(mammalian target of rapamycin, mTOR) 与SIRT1/AMPK信号通路, 下调MMP的表达, 抑制非小细胞肺癌的迁移和侵袭。
上皮-间充质细胞转化(epithelial-mesenchymal transition, EMT) 是一种细胞形态的转化过程, 在多种生物学过程中都起到至关重要的作用, 是促进肿瘤细胞侵袭和扩散、发生远端转移的关键因素[15, 16]。TGF-β1 (transforming growth factor-β1) 是EMT重要诱导因子, 在肿瘤细胞中高表达。黄芩苷在体内与体外通过抑制TGF-β1信号通路, 上调E-钙黏蛋白、下调p-Smad3与波形蛋白的表达抑制EMT, 从而抑制乳腺癌的浸润与转移[17]。黄芩苷可通过多途径调节EMT, 是安全且有效的潜在抗肿瘤侵袭转移药物, 在改善肿瘤患者预后质量方面有很大潜力[18]。
3 诱导细胞周期阻滞
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细胞分裂的正常过程通过细胞周期发生。细胞周期是一系列高度调节的步骤, 由与细胞周期蛋白依赖性激酶(cyclin dependent kinases, CDKs) 联合作用的特定细胞周期蛋白(cyclins) 在分子水平上协同调节[19]。药物干预失控的细胞周期可以抑制肿瘤细胞的过度增殖。
Diao等[20]发现, 黄芩苷抑制人肺癌细胞株H441细胞的体内外生长。PDZ结合激酶和T-LAK细胞源蛋白激酶(PDZ-binding kinase/T-LAK cell-originated protein kinase, PBK/TOPK) 是有丝分裂的调节剂, 参与调控纺锤体的形成和胞质分裂, 黄芩苷可以直接靶向PBK/TOPK蛋白激酶, 通过阻断PBK/TOPK通路从而抑制肺癌的增殖。在体外与体内实验中, 实验剂量黄芩苷对于正常细胞无明显影响, 这体现出黄芩苷具有较好的安全性。
黄芩苷作用于人结直肠癌癌细胞, 使细胞周期滞留在G1期[21]。黄芩苷处理结直肠癌RKO和HCT116细胞48 h后, 诱导G1期细胞停滞; 与黄芩苷的剂量紧密相关。相应地, 黄芩苷能明显降低G2/M期细胞的百分比, 但S期细胞百分比基本不变。黄芩苷诱导的人结直肠癌细胞周期停滞与cyclin D1、cyclin E1、cyclin B1等细胞周期蛋白水平的直接降低相关, 不依赖于p53/p21/p27通路的激活。
黄芩苷对人肺癌A549、SK-LU-1和SK-MES-1细胞系具有细胞毒性, 诱导细胞周期停滞[22]。在不同细胞中, 黄芩苷通过下调多种细胞周期蛋白的表达, 将细胞周期阻滞在S期或者G0/G1期。值得注意的是, 黄芩苷对于正常人肺纤维母细胞具有细胞毒性, 可诱导细胞周期停滞。然而, 包含黄芩苷的黄芩粗提物却具有选择性, 对正常人肺纤维母细胞无明显影响。
黄芩苷通过抑制蛋白激酶B (protein kinase B, PKB, 又称Akt) 通路促进人骨肉瘤细胞周期停滞[23]。在多数类型的癌症中, Akt通路被认为是最重要的致癌途径之一[24]。在骨肉瘤中, Akt通路经常被过度激活, 在肿瘤发生发展中起着关键作用[25]。黄芩苷诱导人骨肉瘤U-2 OS细胞株在G0/G1期阻滞, S期细胞的百分比明显降低。进一步研究表明, 黄芩苷可抑制Akt通路的过度激活, 进而抑制cyclin D1、CDK4等Akt通路的下游效应物诱导细胞周期停滞, 发挥抗肿瘤作用。
4 抑制肿瘤血管生成
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肿瘤新生血管形成是一种病理生理过程, 新血管由原发性肿瘤中的现有血管形成, 以向癌细胞提供足够的氧气和营养, 用于癌细胞的增殖和向远处器官的转移生长。血管生成是肿瘤导致新血管形成的过程, 是癌症的标志之一[26], 也是肿瘤生长、进展和转移的关键因素[27]。
肝细胞癌(hepatic cell carcinoma, HCC) 是一种高度血管化的肿瘤, 血管生成在其发生进展中发挥着重要作用[28], 抗血管生成策略是肝癌治疗中的最新发展趋势。黄芩苷可抑制小鼠HCC的新生血管生成, 显著降低小鼠肿瘤中内皮细胞标志物血小板-内皮细胞黏附分子1 (platelet endothelial cell adhesion molecule-1, cd31) 的表达[29]。有证据表明黄芩苷可通过激活eEF2激酶(eukaryotic cell translation extension factor kinase), 使eEF2失活, 并通过调节AMPK/mTOR/ eEF2K/eEF2通路, 调控肝癌细胞新生蛋白合成抑制血管生成。这表明以黄芩苷为主要成分的黄连解毒汤是一种潜在的肝细胞癌治疗剂, 它能抑制肝癌的发生发展并阻断血管生成。
在鸡胚绒毛尿囊膜模型中, 黄芩苷对于血管生成呈剂量依赖性的双重效应, 低剂量时促进血管生成, 高剂量时抑制血管生成[30]。黄芩苷在低浓度(10~50 μg·mL-1) 时上调神经纤毛蛋白1、转化生长因子β2和血管内皮生长因子C等10种血管生成基因和生长因子的表达, 导致血管中细胞增殖增加, 促进血管生成。黄芩苷在高浓度(5 mg·mL-1及以上) 时, 下调多种血管生成相关基因和生长因子。通过抑制细胞生长, 进而抑制肿瘤新生血管形成。这表明在将黄芩苷应用于临床试验之前, 需要在动物模型中进行更多的剂量依赖性和药代动力学研究, 仔细监测黄芩苷的浓度, 根据疾病类型及期望药效选择合适的用药量。
5 克服肿瘤细胞耐药性
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肿瘤细胞会对化学疗法和放射疗法产生抗性, 肿瘤耐药性严重影响肿瘤治疗效果和患者预后情况, 导致肿瘤复发、扩散和死亡。肿瘤多药耐药已成为癌症化疗成功的最大障碍[31]。
许多化疗药物和放疗都能激活NF-κB (nuclear factor kappa B) 通路。近年来基础研究和临床研究表明, NF-κB通路的激活是肿瘤细胞产生耐药性的主要原因[32]。研究表明, 黄芩苷可抑制NF-κB激酶的激活, 是一种天然的NF-κB抑制剂。当黄芩苷与其他化疗药物联合使用时, 它抑制肿瘤耐药性相关的基因和糖蛋白, 从而克服肿瘤细胞耐药性。
黄芩苷可增强多西他赛在乳腺癌细胞中的抗肿瘤活性, 减轻耐药性。对人乳腺癌MDA-MB-231和4T1细胞株, 黄芩苷与现有化疗药物多西他赛联合用药, 产生协同效应, 增强细胞毒性, 提高了细胞对多西他赛的敏感性[33]。这可能是因为黄芩苷抑制NF-κB和生存素、Bcl-2等NF-κB所调控的抗凋亡蛋白水平, 减轻多西他赛引起的NF-κB通路的异常激活。黄芩苷与多西他赛协同用药, 在不增加毒性的情况下减轻化疗耐药, 可用作乳腺癌的辅助化疗。
多柔比星与黄芩苷合用可以明显协同抑制白血病HL-60/DOX细胞的生长[34]。黄芩苷对白血病细胞具有较好的生长抑制作用, 并抑制多柔比星耐药。小剂量黄芩苷(5和10 mol·L-1) 可通过增加细胞内多柔比星的积累, 抑制HL-60/DOX细胞的生长, 与多柔比星产生协同作用。有研究表明, 黄芩苷可通过抑制PI3K/Akt信号通路, 随后抑制肺耐药相关蛋白(lung resistance-related protein, LRP)、Bcl-2等多重耐药性相关基因及抗凋亡基因的表达, 提高多柔比星在HL-60/DOX细胞内的蓄积进而发挥作用[35]。
顺铂是一种目前用于治疗多种癌症的关键化疗药物, 主要通过产生脱氧核糖核酸-铂复合物和随后的脱氧核糖核酸损伤反应在肿瘤细胞中发挥细胞毒性作用[36, 37]。但肿瘤对药物产生耐药性会导致化疗失败, 是临床治疗面临的一大障碍。黄芩苷通过下调微管亲和性调控激酶2 (microtubule-affinity regulating kinase 2, MARK2) 和p-Akt, 降低肺癌对顺铂的耐药性[38]。黄芩苷和顺铂具有协同抑制人肺癌细胞增殖和侵袭的作用, 无论肺癌细胞是否已经对顺铂产生耐药性, 黄芩苷都会增加肺癌细胞对顺铂的敏感度并降低其耐药性。与正常A549肺癌细胞相比, 顺铂耐药的A549肺癌细胞的MARK2和p-Akt表达明显更高, 黄芩苷呈剂量依赖性显著降低MARK2和p-Akt在顺铂耐药细胞中的表达, 可能通过抑制药物外流、下调耐药蛋白表达、促进细胞凋亡和抑制细胞增殖等方式减轻肺癌顺铂的耐药性[39]。这表明黄芩苷是一种极具前景的降低顺铂耐药性的药物。
6 调控肿瘤相关炎性微环境
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目前普遍认为促肿瘤性炎症是癌症的标志之一[40]。炎症是癌症的诱因和后果, 炎症环境加速肿瘤微环境的形成, 有利于基因组突变和其他致癌作用。据估计, 大约25%的癌症与慢性炎症和感染存在病因学联系[41]。大量研究报道了黄芩苷的潜在抗炎特性和可能存在的作用机制。
所有已知的癌症特征都涉及NF-κB通路的激活。NF-κB作为炎症反应的重要转录因子, 是联系慢性炎症与癌症的重要分子之一[42]。众多研究表明, 黄芩苷是一种活性较强的NF-κB激活抑制剂[43, 44]。常规炎症反应由多种细胞因子介导, 肿瘤坏死因子-α (tumor necrosis factor-α, TNF-α) 和白介素-1β (interleukin-1β, IL-1β) 是关键的促炎细胞因子。在乳腺癌细胞中, 黄芩苷抑制了TNF-α和IL-1β的表达, 并通过NF-κB抑制蛋白(inhibitor a of NF-κB, IκB) 激酶活性抑制NF-κB通路的活化, 达到减缓乳腺癌发展的作用[45]。MAPK-p38信号通路在调控炎性微环境中发挥着重要作用。黄芩苷可呈剂量依赖性抑制MAPK-p38信号通路, 降低动脉粥样硬化诱导的IL-6、TNF-α、sVE-钙黏蛋白等炎性细胞因子水平, 发挥抗炎作用[46]。
皮肤癌是常见恶性肿瘤之一, 阳光中的紫外线(UV) 可直接损伤皮肤细胞DNA, 改变多种细胞因子和炎性介质表达, 是皮肤癌发生发展的重要危险因素[47]。紫外线照射激活炎症过程被认为是皮肤癌发生发展的关键介质。黄芩苷可起到抗炎作用, 在小鼠角质形成细胞中显著降低紫外线照射后的炎症和细胞死亡。Toll样受体(Toll-like receptors, TLRs) 通路参与了由紫外线照射介导的炎症过程, 诱导炎症关键调节因子COX2的激活。黄芩苷通过调节TLR4信号, 抑制炎症级联反应, 并通过减少髓样分化因子88 (myeloid differentiation factor 88, MyD88)、诱生型NOS (inducible NOS, iNOS) 等多种炎症生物标志物水平发挥抗炎作用[48]。以上结果显示, 黄芩苷在预防皮肤癌方面的巨大潜力。
7 调控氧化应激预防肿瘤发生
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氧化应激是指体内氧化与抗氧化作用处于失衡的状态, 会对机体产生细胞基因组损伤、细胞膜通透性流动性改变等负面作用[49]。研究表明, 肿瘤高危人群常处于低抗氧化状态, 体内会存在活性氧(reactive oxygen species, ROS) 的蓄积, 高水平ROS则会作用于生物大分子, 成为肿瘤等疾病发生的重要推动力。同时, 氧化应激的失调在肿瘤的发生发展、侵袭转移和放化疗耐药方面发挥着重要作用[50, 51]。抗氧化剂可调控人体内氧化应激水平, 从而发挥肿瘤预防作用。
黄酮类化合物因其结构中含有酚羟基, 普遍具有较好的抗氧化能力[52], 具有干预肿瘤发生的前景。黄芩苷含有2个酚羟基, 可充当氢或电子供体, 具有较强的抗氧化作用。
紫外线辐射通过产生ROS降低细胞的抗氧化状态, 导致氧化应激。黄芩苷具有光保护活性, 抑制ROS和ROS介导的细胞损伤, 从而抑制紫外线辐射的致癌作用[53]。黄芩苷在体内的代谢产物黄芩素同样具备较强的抗氧化作用[54]。
值得注意的是, 肿瘤细胞中高水平的ROS可引起肿瘤细胞自噬与凋亡。有报道称黄芩苷对氧自由基损伤的人神经母细胞瘤细胞具有保护作用, 可减轻氧自由基造成的损伤、抑制细胞的凋亡[55]。这提示黄芩苷的抗氧化能力, 在肿瘤发生发展过程中可能扮演两种作用, 即在癌前病变阶段通过调节氧化应激起到化学预防作用, 在癌症发生后通过降低肿瘤细胞内部氧化应激水平对肿瘤细胞起到保护作用。
黄芩苷的抗氧化作用在肿瘤治疗, 特别是与其他药物联用时可能发挥负面影响。因此, 临床使用黄芩苷治疗时需要考虑肿瘤发生发展不同阶段, 根据药物经济学决定具体用药。同时, 目前关于黄芩苷与氧化应激的研究大多局限于中枢系统疾病领域, 其作为抗氧化剂在肿瘤预防领域的应用还有待进一步研究。
8 总结与展望
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恶性肿瘤严重危害人类健康, 虽然目前临床可通过手术、放化疗和细胞疗法等多种方式治疗, 但复发率较高, 治愈率不理想, 不良反应较严重。因此, 寻找新颖高效低毒的抗肿瘤药物已成为国内外研究的重点。作为传统中草药黄芩的有效成分之一, 黄芩苷的药效十分广泛, 其临床应用价值有待进一步开发。
近年来研究表明, 黄芩苷是一种理想的抗肿瘤药物, 可在体内外抑制多种类型肿瘤的发生发展、浸润、转移, 具有温和的抗肿瘤药理活性(表 1)。
但目前, 多数黄芩苷抗肿瘤作用的研究局限于细胞和动物实验。由于黄芩苷作用位点较多, 药理机制尚不完全清楚, 同时较差的水溶性及脂溶性导致生物利用度较低, 限制了其疗效。黄芩苷在临床上的应用价值、用药剂量及用药方式还有待进一步探究, 多角度的认识、改造、应用黄芩苷还有待研究者进一步探索(图 2)。
作者贡献: 孔邦彦负责综述的文献调研与撰写; 魏立彬和郭青龙负责论文的指导与审阅。
利益冲突: 所有作者均声明不存在利益冲突。
基金
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  • 国家科技重大专项-重大新药创制(2018ZX09711001-003-007)
文献
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doi: 10.16438/j.0513-4870.2020-1642
  • 接收时间：2020-10-20
  • 首发时间：2025-12-18
  • 出版时间：2021-06-12
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  • 收稿日期：2020-10-20
  • 修回日期：2020-12-30
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国家科技重大专项-重大新药创制(2018ZX09711001-003-007)
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    中国药科大学基础医学与临床药学学院, 江苏 南京 211198

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2种不同金属材料的力学参数
科
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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