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Article(id=1200147893316318013, tenantId=1146029695717560320, journalId=1190317699101192196, issueId=1200147892095779072, articleNumber=1001-2494(2024)11-0970-04, orderNo=null, doi=10.11669/cpj.2024.11.003, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=null, receivedDate=1682611200000, receivedDateStr=2023-04-28, revisedDate=null, revisedDateStr=null, acceptedDate=null, acceptedDateStr=null, onlineDate=1764067155436, onlineDateStr=2025-11-25, pubDate=1717776000000, pubDateStr=2024-06-08, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1764067155436, onlineIssueDateStr=2025-11-25, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1764067155436, creator=13701087609, updateTime=1764067155436, updator=13701087609, issue=Issue{id=1200147892095779072, tenantId=1146029695717560320, journalId=1190317699101192196, year='2024', volume='59', issue='11', pageStart='953', pageEnd='1064', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1764067155144, creator=13701087609, updateTime=1764067375019, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1200148814364508515, tenantId=1146029695717560320, journalId=1190317699101192196, issueId=1200147892095779072, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1200148814364508516, tenantId=1146029695717560320, journalId=1190317699101192196, issueId=1200147892095779072, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=970, endPage=973, ext={EN=ArticleExt(id=1200147893555393342, articleId=1200147893316318013, tenantId=1146029695717560320, journalId=1190317699101192196, language=EN, title=Advance in Role of Circular RNA on Neurovascular Units and its Application, columnId=null, journalTitle=Chinese Pharmaceutical Journal, columnName=null, runingTitle=null, highlight=null, articleAbstract=

Circular RNAs (circRNAs) are a class of single-stranded RNA molecules with covalently closed continuous loops which are involved in the occurrence and development of diseases. Neurovascular units(NVU) refer to the cellular and molecular interfaces between the circulatory system and central nervous system(CNS), mainly composed of microvascular cells, glial cells, neurons, and extracellular matrix, which are of great significance for maintaining brain homeostasis. However, the role of circRNA on NVU remains unknown. This article summarizes the latest research progress, with the aim of providing new targets and strategies for the treatment of related diseases.

, correspAuthors=Honghong YAO, authorNote=null, correspAuthorsNote=null, copyrightStatement=null, 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=Ling SHEN, Honghong YAO), CN=ArticleExt(id=1200147893949657920, articleId=1200147893316318013, tenantId=1146029695717560320, journalId=1190317699101192196, language=CN, title=环状RNA对神经血管单元的调控作用及其应用进展, columnId=1190352408384471863, journalTitle=中国药学杂志, columnName=综述, runingTitle=null, highlight=null, articleAbstract=

环状RNA(circular RNA,circRNA)是一类具有共价闭合环状结构的单链RNA分子,在疾病发生发展中具有重要作用。神经血管单元是指脑微血管细胞、胶质细胞、神经元和细胞外基质等组成的脑功能的基本结构单元,对维持大脑稳态具有重要意义,近年来已成为多种复杂脑疾病的研究热点。然而circRNA对于神经血管单元的调控作用目前尚未明确,本文就circRNA对神经血管单元的调控作用及其应用的研究进展进行综述,以期为相关疾病提供治疗新靶点和新策略。

, correspAuthors=姚红红, authorNote=null, correspAuthorsNote=
*姚红红,女,博士,教授 研究方向:药理学 Tel:(025)83272551
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沈灵,女,硕士,工程师 研究方向:药理学

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沈灵,女,硕士,工程师 研究方向:药理学

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沈灵,女,硕士,工程师 研究方向:药理学

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环状RNA对神经血管单元的调控作用及其应用进展
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沈灵 , 姚红红 *
中国药学杂志 | 综述 2024,59(11): 970-973
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中国药学杂志 | 综述 2024, 59(11): 970-973
环状RNA对神经血管单元的调控作用及其应用进展
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沈灵, 姚红红*
作者信息
  • 东南大学医学院, 南京 210009

    • 沈灵,女,硕士,工程师 研究方向:药理学

通讯作者:

*姚红红,女,博士,教授 研究方向:药理学 Tel:(025)83272551
Advance in Role of Circular RNA on Neurovascular Units and its Application
Ling SHEN, Honghong YAO*
Affiliations
  • School of Medicine, Southeast University, Nanjing 210009, China
出版时间: 2024-06-08 doi: 10.11669/cpj.2024.11.003
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摘要
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环状RNA(circular RNA,circRNA)是一类具有共价闭合环状结构的单链RNA分子,在疾病发生发展中具有重要作用。神经血管单元是指脑微血管细胞、胶质细胞、神经元和细胞外基质等组成的脑功能的基本结构单元,对维持大脑稳态具有重要意义,近年来已成为多种复杂脑疾病的研究热点。然而circRNA对于神经血管单元的调控作用目前尚未明确,本文就circRNA对神经血管单元的调控作用及其应用的研究进展进行综述,以期为相关疾病提供治疗新靶点和新策略。

环状RNA  /  神经血管单元  /  缺血性脑卒中  /  抑郁症

Circular RNAs (circRNAs) are a class of single-stranded RNA molecules with covalently closed continuous loops which are involved in the occurrence and development of diseases. Neurovascular units(NVU) refer to the cellular and molecular interfaces between the circulatory system and central nervous system(CNS), mainly composed of microvascular cells, glial cells, neurons, and extracellular matrix, which are of great significance for maintaining brain homeostasis. However, the role of circRNA on NVU remains unknown. This article summarizes the latest research progress, with the aim of providing new targets and strategies for the treatment of related diseases.

circular RNA  /  neurovascular unit  /  ischemic stroke  /  depression
沈灵, 姚红红. 环状RNA对神经血管单元的调控作用及其应用进展. 中国药学杂志, 2024 , 59 (11) : 970 -973 . DOI: 10.11669/cpj.2024.11.003
Ling SHEN, Honghong YAO. Advance in Role of Circular RNA on Neurovascular Units and its Application[J]. Chinese Pharmaceutical Journal, 2024 , 59 (11) : 970 -973 . DOI: 10.11669/cpj.2024.11.003
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环状RNA(circular RNA, circRNA)是一类特殊的RNA,通过反向剪切的方式形成一个共价闭环的环状结构[1]。早在40年前,科学家们就发现了circRNA的存在[2]。在这之后的几十年间,不断有circRNA被发现,然而受到彼时科学技术的限制,鲜有对其结构和生物学功能的探索[3-5]。高通量测序技术和生物信息学算法的飞速发展极大程度推动了circRNA的研究。研究者[6-7]发现circRNA广泛存在于真核细胞生物中,具有高物种保守性以及细胞、组织和发育阶段特异性。随着越来越多的circRNA不断被发现,其生物学功能也不断被探明。circRNA可作为转录后调节因子与微小核糖核酸(microRNA, miRNA)结合抑制信使核糖核酸(messenger RNA, mRNA)翻译,或通过与RNA结合蛋白相互作用从而调控基因转录,甚至部分circRNA还具有蛋白翻译功能[8-11]。越来越多的研究表明,circRNA可以调控多种生物学进程,且在疾病发生发展中具有重要作用。
神经血管单元是一个复杂的多细胞结构,主要由脑微血管细胞、胶质细胞、神经元和细胞外基质组成[12]。这些细胞相互关联,功能耦合,是脑结构和功能的基本单位,对于维持大脑微环境稳态具有重要作用[13-14]。近年来,神经血管单元已经成为脑卒中和抑郁症等诸多疾病治疗的热点。卒中后,将保护重点从单一的神经元转移到神经血管单元,强调其组成细胞之间的动态相互作用并联合调控对脑卒中损伤修复具有重要意义[15-16]。无独有偶,神经血管单元稳态失衡(血管屏障通透性增加、神经血管解偶联和神经炎症)在抑郁症的发生发展中也具有重要作用[17]。本文详细综述了circRNA对神经血管单元的调控作用及其应用的相关研究进展,以期为相关疾病提供治疗新靶点和新策略。
1 circRNA对神经血管单元的调控作用
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1.1 circRNA对内皮细胞的调控作用
RNA SCMH1(circular RNA SCMH1, circSCMH1)可促进啮齿与非人灵长类动物缺血性卒中后运动功能修复,是缺血性卒中发生发展的一种关键circRNA分子。而缺血周围区血管修复是改善缺血性卒中长期预后的关键措施,那么circSCMH1对于脑微血管又具有怎样的作用呢?该研究发现circSCMH1可显著促进小鼠和恒河猴卒中后血管修复,促进小鼠卒中后血管新生与成熟,可修复卒中后损伤微血管并增加梗死周围区血管血流灌注,显著改善卒中后血脑屏障损伤。机制研究表明circSCMH1通过泛素化增加脑血管内皮细胞脂肪量与肥胖相关蛋白(fat mass and obesity-associated protein,FTO)从细胞质到细胞核的易位,导致血管发育相关基因——脂质磷酸磷酸酶3(lipid phosphate phosphatase 3,Plpp3)的N6-甲基腺苷(N6-methyladenosine,m6A)修饰降低,从而抑制了内皮细胞中Plpp3的降解,使Plpp3编码的脂质磷脂酶3蛋白(lipid phosphate phosphatase 3,LPP3)水平增加,促进血管修复[19]。
此外,Bai等[20]发现,circDLGAP4水平在急性缺血性脑卒中(acute ischemic stroke,AIS)患者的血浆以及小鼠卒中模型中降低。circDLGAP4 可作为内源性miR-143海绵,其减少导致miR-143的靶蛋白HECT结构域E3泛素蛋白连接酶1(HECT domain E3 ubiquitin protein ligase 1, HECTD1)的表达抑制。circDLGAP4过表达显著抑制内皮-间质转化并保护卒中模型小鼠的血脑屏障完整性,减少脑梗死体积,改善卒中模型小鼠的神经功能[20]。circHECW2可通过竞争性结合miR-30d,促进人自噬相关蛋白5(autophagy protein 5, ATG)表达,ATG5以非自噬的作用途径影响上皮细胞-间充质转化过程,参与血脑屏障完整性的调控[21]。
1.2 circRNA对星形胶质细胞的调控作用
Huang等[22]发现,在严重抑郁症患者和慢性不可预测应激(chronic unpredictable stress, CUS)模型小鼠血浆中显著下调,circSTAG1的过表达显著减轻了CUS诱导的星形胶质细胞功能障碍和抑郁样行为。进一步研究表明,过表达的circSTAG1捕获了alkB同族体5(alkB homolog 5, ALKBH5),并减少了ALKBH5进入细胞核的转运,导致星形胶质细胞中脂肪酸酰胺水解酶(fatty acid amide hydrolase, FAAH)mRNA的m6A甲基化增加和FAAH降解,进而降低了抑郁样行为和皮质酮体外诱导的星形胶质细胞损伤。
Han等[23]的研究表明,在缺血性脑卒中小鼠大脑和AIS患者的血浆中增加。circHECTD1 作为内源性 miR-142海绵抑制其活性,导致下游靶标 TCDD 诱导型多聚[ADP-核糖]聚合酶表达的增加,进而通过自噬启动阶段膜突蛋白样BCL相互作用蛋白(moesin-like BCL2 interacting protein,Beclin-1)、参与自噬溶酶体膜延伸的微管相关蛋白轻链3B(microtubule-associated proteins light chain 3B,LC3B)以及连接LC3B-Ⅱ与泛素化的底物的受体蛋白死骨片1(sequestosome 1, p62),3种自噬蛋白激活星形胶质细胞。敲低 circHECTD1 改善了脑缺血后星形胶质细胞活化,减少了脑梗死面积,减弱了神经功能缺陷。此外,Huang等[24]的研究阐明了circHIPK2/miR-124/σ-1R轴可通过协同调控自噬和内质网应激,最终调节星形胶质细胞活化过程。
1.3 circRNA对小胶质细胞的调控作用
Zhang等[25]发现,无论是在重度抑郁症患者的外周血中,还是CUS诱导的抑郁样模型小鼠的外周血中,circDYM的表达水平显著降低。而升高circDYM的表达能够显著改善小鼠抑郁样行为,这种改善是通过减少抑郁导致的脑内小胶质细胞活化来实现的。该研究还进一步探讨了circDYM改善小鼠抑郁样行为的分子机制,发现circDYM作为海绵吸附miR-9并抑制其活性,导致miR-9下游靶向的HECTD1表达增加,致使热休克蛋白90(heat shock protein 90, HSP90)泛素化增多,从而减少小胶质细胞活化。Yu等[26]进一步研究发现,circDYM还可以通过与TATA 盒结合蛋白相关因子1结合,抑制小鼠脑部小胶质细胞的活化,抑制中枢神经炎症,从而缓解抑郁症症状。
1.4 circRNA对神经元的调控作用
Yang等[18]在先前的研究基础上,进一步发现circSCMH1显著逆转神经元的可塑性损伤,增加树突复杂性、促进轴突生长和增加神经元树突棘密度。转录组学、蛋白质组学及RNA免疫沉淀等分子生物学手段揭示,circSCMH1直接与神经可塑性的关键分子甲基-CpG 结合蛋白 2(methyl-CpG-binding protein 2, MeCP2)氨基酸序列的26-76aa 处结合。circSCMH1“扣押”MeCP2于胞质,阻止入核,从而抑制MeCP2 对 Mobp、Igfbp3、Fxyd1、Prodh 等神经可塑性相关基因的转录调控。
除circSCMH1,Wu等[27]还发现circTLK1表达在小鼠脑局部缺血和再灌注后明显上调,敲低circTLK1可显著降低脑梗死体积,减轻神经元损伤,改善神经功能缺损。circTLK1可竞争性结合miR-335-3p并抑制miR-335-3p活性,进而增加下游靶蛋白TIPARP的表达,从而导致神经元损伤并加重脑梗死和神经功能缺损,提示circTLK1可能是脑卒中后神经元损伤的一个新机制。在神经干细胞(neural stem cell,NSC)的分化过程中,circHIPK2 的表达逐渐降低。敲低circHIPK2可通过下游蛋白Smox促进NSC向神经元分化增多,提高小鼠神经可塑性,改善小鼠神经功能[28]。
2 circRNA的临床应用
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2.1 circRNA作为疾病诊断和预后评估的生物学标志物
目前,AIS的诊断主要依赖影像学诊断,尚无可靠的血液学生物标志物可用于诊断AIS和预测卒中预后。Han[23]等的研究表明,circRNA从多方面参与AIS的病理进程,且因其所具有的共价连接的闭环结构而在外周血中稳定存在,因此有望作为AIS的理想生物标志物[23]。Zuo等[29]发现circFUNDC1、circPDS5B和circCDC14A在AIS患者血浆中显著增加。将3条circRNA 结合绘制AIS诊断的接收者操作特征曲线,其曲线下面积(area under the curve,AUC)为0.875,灵敏度和特异度分别为 91%以及 71.5%。入院7 d之内circRNAs水平的变化率对预测卒中预后具有重要意义。circFUNDC1、circPDS5B、circCDC14A和3条circRNA 结合起来的 AUC 分别为 0.884、0.953、0.943和0.960。这说明外周循环中 circRNA 所组成的群体(circFUNDC1、circPDS5B和circCDC14A)不仅具有作为 AIS 诊断生物标志物的潜能,而且有望应用于评估卒中预后。
目前,由于抑郁症病因以及病理机制复杂、症状表现范围广泛等原因,临床诊断通常依赖于量表,诊断一致性较差,因此亟须一个稳定客观的诊断标志物。Zhang等[25]发现circDYM表达水平与抑郁症有关,重度抑郁症患者外周血中circDYM表达水平显著降低。且circDYM水平越低,早期负性生活事件评分越高,抑郁症状越严重。这说明circDYM有望成为重度抑郁症诊断的客观生物标志物。
2.2 circRNA作为疾病治疗靶点
Yang等[18]发现,AIS患者和卒中模型小鼠血浆中,circSCMH1水平显著降低,过表达circSCMH1显著促进卒中模型小鼠感觉运动功能恢复,改善梗死体积,增强神经元可塑性,抑制梗死周围区胶质细胞活化,抑制外周免疫浸润,从而促进卒中后脑修复[18]。此外,过表达circSCMH1还可通过FTO依赖方式调控Plpp3的m6A修饰,增加血管生成相关基因Plpp3及其编码蛋白LPP3表达,促进卒中后血管修复和运动功能修复[19]。此外,AIS患者和卒中模型小鼠血浆中,circTLK1/circHECTD1水平也显著降低,敲低circTLK1可增强神经元可塑性,抑制星形胶质细胞活化,从而促进卒中后脑修复[23,27]。
在抑郁症小鼠血浆中,circDYM和circSTAG1显著降低,过表达circDYM和circSTAG1显著抑制CUS小鼠海马脑区小胶质细胞活化,减少星形胶质细胞丢失,减少血脑屏障损伤,抑制外周免疫细胞浸润,显著改善CUS小鼠抑郁样行为[22,25],有望成为AIS和抑郁症的治疗靶点。
2.3 circRNA作为新型核酸药物
随着精准医学的发展,药物靶点从传统的蛋白质扩展到 RNA领域,核酸药物研发蓄势待发,而具有高稳定性的环状RNA类核酸药物更具开发潜力。Yang等[18]和Yu等[26]创新性利用外泌体靶向递送siRNA的新方法,对溶酶体相关膜蛋白 2(lysosome-associated membrane glycoprotein 2, LAMP2)进行改造,并与神经元特异性狂犬病毒糖蛋白(glycoprotein,RVG) 进行融合形成RVG-lamp2b融合蛋白的外泌体。进一步利用该靶向性外泌体包裹circRNA,从而成功地将环状RNA开发为核酸药物。研究表明RVG-circDYM-EVs和RVG-circSCMH1-EVs具有较高的安全性和稳定性,对CUS诱导的小鼠抑郁样行为以及缺血性脑卒中模型小鼠感觉运动功能具有较好的改善作用。
3 展望
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大脑中固有细胞呈现多样性,并且多种细胞彼此沟通紧密,以神经血管单元形式执行神经功能。随着单细胞测序,空间转录组测序等技术的不断成熟,如何解析不同细胞之间的相互作用和交流是深入阐明诸多疾病复杂病理机制的关键问题。此外,虽然本研究已经阐明了多种疾病状态下circRNA表达水平的变化,但其生物合成的核心分子机制等方面尚不清楚,是亟待解决的重要科学问题。
基金
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  • 国家自然科学基金项目资助(82025033)
  • 国家自然科学基金项目资助(82230115)
  • 科技创新-2030重大项目资助(2021ZD0202904/2021ZD0202900)
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2024年第59卷第11期
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doi: 10.11669/cpj.2024.11.003
  • 接收时间：2023-04-28
  • 首发时间：2025-11-25
  • 出版时间：2024-06-08
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  • 收稿日期：2023-04-28
基金
国家自然科学基金项目资助(82025033)
国家自然科学基金项目资助(82230115)
科技创新-2030重大项目资助(2021ZD0202904/2021ZD0202900)
作者信息
    东南大学医学院, 南京 210009

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*姚红红,女,博士,教授 研究方向:药理学 Tel:(025)83272551
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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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