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Article(id=1200860516534055093, tenantId=1146029695717560320, journalId=1189982191388893191, issueId=1200860506031518620, articleNumber=null, orderNo=null, doi=10.16438/j.0513-4870.2023-1150, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1696867200000, receivedDateStr=2023-10-10, revisedDate=1702656000000, revisedDateStr=2023-12-16, acceptedDate=null, acceptedDateStr=null, onlineDate=1764237058051, onlineDateStr=2025-11-27, pubDate=1715443200000, pubDateStr=2024-05-12, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1764237058051, onlineIssueDateStr=2025-11-27, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1764237058051, creator=13701087609, updateTime=1764237058051, updator=13701087609, issue=Issue{id=1200860506031518620, tenantId=1146029695717560320, journalId=1189982191388893191, year='2024', volume='59', issue='5', pageStart='1101', pageEnd='1508', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1764237055547, creator=13701087609, updateTime=1764241222263, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1200877982563824311, tenantId=1146029695717560320, journalId=1189982191388893191, issueId=1200860506031518620, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1200877982563824312, tenantId=1146029695717560320, journalId=1189982191388893191, issueId=1200860506031518620, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=1271, endPage=1279, ext={EN=ArticleExt(id=1200860517964312850, articleId=1200860516534055093, tenantId=1146029695717560320, journalId=1189982191388893191, language=EN, title=Ameliorative effect of Panax notoginseng saponins eye drops on non-proliferative diabetic retinopathy in rats, columnId=1190335348761793317, journalTitle=Acta Pharmaceutica Sinica, columnName=Original Articles, runingTitle=null, highlight=null, articleAbstract=

Diabetic retinopathy (DR) is a diabetic ocular complication that can lead to poor vision and blindness. This experiment aimed to investigate the ameliorative effect and its mechanism of Panax notoginseng saponins (PNS) eye drops on streptozotocin (STZ)-induced non-proliferative diabetic retinopathy (NPDR) in rats. All experiments were approved by the Animal Research Committee of Shanghai University of Traditional Chinese Medicine. Animal welfare and the animal experimental protocols were strictly consistent with related ethics regulations of Shanghai University of Traditional Chinese Medicine (No. PZSHUTCM 211115004). Diabetes mellitus was induced by a single intraperitoneal injection of STZ into rats. Two months later, PNS solution was dropped binocular twice per day at 6 h intervals at dose of 20, 40, and 80 mg·kg-1 continuously for 1 month. The morphological structure and activation of microglia of the retina were observed by hematoxylin-eosin staining and immunohistochemical assay. The disruption of the blood-retina barrier (BRB) was conducted by the Evans blue dye leakage assay. The number of acellular capillaries in the retina was assessed by digesting and hematoxylin-eosin staining assay. The number of retinal leukocyte adhesion was observed by fluorescein isothiocyanate-coupled concanavalin A lectin labeling assay. The serum expression of inflammatory factors was measured using enzyme-linked immunosorbent assay. Western blot experiments were used to detect the expression of relevant proteins in retinal tissue and transcriptional activation of nuclear factor kappa-B (NF-κB). The results revealed that PNS eye drops significantly increased the thickness of the retina, decreased the number of acellular capillaries, and up-regulated the expression of the tight junction proteins claudin-1 and occludin, thereby alleviating BRB damage. In addition, PNS eye drops were also able to significantly reduce leukocyte adhesion and microglia activation, the expression of inflammatory factors in serum, and the nuclear translocation of retinal p65 proteins, effectively inhibiting the occurrence of retinal inflammation. The above results showed that PNS eye drops played a role in improving NPDR by inhibiting the activation of the NF-κB signaling pathway and reducing inflammation.

, correspAuthors=Chang-hong WANG, authorNote=null, correspAuthorsNote=null, copyrightStatement=Copyright ©2024 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=Xin SUN, Ya-ru WANG, Xue-mei CHENG, Hong-yu CHEN, Ming CHEN, Shu-sheng LAI, Li-li JI, Xiao-hui WEI, Chang-hong WANG), CN=ArticleExt(id=1200860522146034252, articleId=1200860516534055093, tenantId=1146029695717560320, journalId=1189982191388893191, language=CN, title=三七总皂苷溶液滴眼给药对大鼠非增殖性糖尿病视网膜病变的改善作用, columnId=1190335348896011050, journalTitle=药学学报, columnName=研究论文, runingTitle=null, highlight=null, articleAbstract=

糖尿病视网膜病变(diabetic retinopathy, DR) 是一种累及眼睛的糖尿病并发症, 会导致患者视力低下甚至失明。本文旨在研究三七总皂苷(Panax notoginseng saponins, PNS) 溶液滴眼给药对链脲佐菌素(streptozotocin, STZ) 诱导的大鼠非增殖性糖尿病视网膜病变(non-proliferative diabetic retinopathy, NPDR) 的改善作用及其机制。实验方案经上海中医药大学实验动物福利与伦理委员会审查, 符合实验动物福利与伦理相关规范(伦理号: PZSHUTCM 211115004)。通过对大鼠腹腔单次注射STZ诱导糖尿病模型, 注射两个月后, 分别按照20、40和80 mg·kg-1的剂量双眼滴眼PNS溶液, 每日2次, 每次间隔6 h, 连续1个月。通过对大鼠眼球进行苏木精-伊红染色和免疫组化分析, 观察视网膜的形态结构变化和小胶质细胞的活化情况; 采用伊文思蓝染料渗漏实验, 观察血-视网膜屏障(blood-retina barrier, BRB) 的破坏情况; 利用胰酶消化视网膜并进行染色, 观察视网膜中无细胞毛细血管的数量; 通过尾静脉注射异硫氰酸荧光素偶联刀豆蛋白A凝集素, 观察视网膜中黏附的中性粒细胞数量; 采用酶联免疫实验检测血清中炎症因子的表达; 采用Western blot实验检测视网膜组织中相关蛋白的表达以及核因子κB (nuclear factor kappa-B, NF-κB) 的转录激活。结果发现, PNS溶液滴眼给药能够显著增加视网膜的厚度、减少无细胞毛细血管的数量以及上调紧密连接蛋白claudin-1和occludin的表达, 从而缓解BRB的损伤。此外, PNS溶液滴眼给药也能够显著减少中性粒细胞的黏附和小胶质细胞的活化、降低血清中炎症因子的表达以及视网膜p65蛋白的核转移, 有效抑制视网膜炎症的发生。以上结果表明, PNS溶液滴眼给药可以通过抑制NF-κB信号通路的激活, 降低炎症的发生, 从而发挥改善NPDR的作用。

, correspAuthors=王长虹, authorNote=null, correspAuthorsNote=
*王长虹, Tel: 86-21-51322511, E-mail:
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Scale bar: 50 μm; B: Quantitative analysis of retinal INL thickness. <i>n</i> = 4, $\overline{x} \pm s$. <sup>###</sup><i>P</i> < 0.001 <i>vs</i> control group; <sup>***</sup><i>P</i> < 0.001 <i>vs</i> DM group , figureFileSmall=+2f9bS9+s7HFvFPuLG+kpA==, figureFileBig=T+7nL+AlmSXMadIsQPjwRw==, tableContent=null), ArticleFig(id=1201106667246154518, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1200860516534055093, language=EN, label=null, caption=null, figureFileSmall=ASIUabwr2pTWppm8sOThDg==, figureFileBig=d+MwBZzUrWN/1zCIOc+kPw==, tableContent=null), ArticleFig(id=1201106667468452636, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1200860516534055093, language=CN, label=Figure 3, caption= Effect of PNS on retinal acellular capillaries in diabetic rats. A: Typical diagram of acellular capillaries in retinal tissue. Scale bar: 100 μm, black arrows indicate acellular capillaries; B: Quantitative analysis of the number of acellular capillaries. <i>n</i> = 4, $\overline{x} \pm s$. <sup>###</sup><i>P</i> < 0.001 <i>vs</i> control group; <sup>*</sup><i>P</i> < 0.05 <i>vs</i> DM group , figureFileSmall=ASIUabwr2pTWppm8sOThDg==, figureFileBig=d+MwBZzUrWN/1zCIOc+kPw==, tableContent=null), ArticleFig(id=1201106667636224804, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1200860516534055093, language=EN, label=null, caption=null, figureFileSmall=K0i4lcNynB7E5ozcsT5vsg==, figureFileBig=va5V62kVMWkfOEMz9IaXSA==, tableContent=null), ArticleFig(id=1201106667766248237, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1200860516534055093, language=CN, label=Figure 4, caption= Comparison of the amount of Evans blue dye leakage in the retina of rats in each group. <i>n</i> = 6, $\overline{x} \pm s$. <sup>##</sup><i>P</i> < 0.01 <i>vs</i> control group; <sup>*</sup><i>P</i> < 0.05 <i>vs</i> DM group , figureFileSmall=K0i4lcNynB7E5ozcsT5vsg==, figureFileBig=va5V62kVMWkfOEMz9IaXSA==, tableContent=null), ArticleFig(id=1201106667917243184, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1200860516534055093, language=EN, label=null, caption=null, figureFileSmall=uO9U+cs7RZQJY3fPLs7tUA==, figureFileBig=QsgxpEVZRWwffxrAMAzCpQ==, tableContent=null), ArticleFig(id=1201106668072432441, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1200860516534055093, language=CN, label=Figure 5, caption= Effect of PNS on retinal claudin-1 and occludin expression in diabetic rats. 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三七总皂苷溶液滴眼给药对大鼠非增殖性糖尿病视网膜病变的改善作用
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孙鑫 1 , 王亚茹 1 , 程雪梅 1 , 陈泓谕 1 , 陈明 2 , 赖树生 2 , 季莉莉 1 , 尉小慧 1 , 王长虹 1, *
药学学报 | 研究论文 2024,59(5): 1271-1279
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药学学报 | 研究论文 2024, 59(5): 1271-1279
三七总皂苷溶液滴眼给药对大鼠非增殖性糖尿病视网膜病变的改善作用
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孙鑫1, 王亚茹1, 程雪梅1, 陈泓谕1, 陈明2, 赖树生2, 季莉莉1, 尉小慧1, 王长虹1, *
作者信息
  • 1.上海中医药大学中药研究所, 中药标准化教育部重点实验室, 上海市复方中药重点实验室, 上海 201203
  • 2.广西三七综合利用技术重点实验室, 广西 梧州 543000

通讯作者:

*王长虹, Tel: 86-21-51322511, E-mail:
Ameliorative effect of Panax notoginseng saponins eye drops on non-proliferative diabetic retinopathy in rats
Xin SUN1, Ya-ru WANG1, Xue-mei CHENG1, Hong-yu CHEN1, Ming CHEN2, Shu-sheng LAI2, Li-li JI1, Xiao-hui WEI1, Chang-hong WANG1, *
Affiliations
  • 1. The MOE Key Laboratory for Standardization of Chinese Medicines, Shanghai Key Laboratory for Compound Chinese Medicines, Institute of Chinese Materia Medica, Shanghai University of Traditional Chinese Medicine, Shanghai 201203, China
  • 2. Guangxi Key Laboratory of Comprehensive Utilization Technology of Pseudo-ginseng, Wuzhou 543000, China
出版时间: 2024-05-12 doi: 10.16438/j.0513-4870.2023-1150
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摘要
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糖尿病视网膜病变(diabetic retinopathy, DR) 是一种累及眼睛的糖尿病并发症, 会导致患者视力低下甚至失明。本文旨在研究三七总皂苷(Panax notoginseng saponins, PNS) 溶液滴眼给药对链脲佐菌素(streptozotocin, STZ) 诱导的大鼠非增殖性糖尿病视网膜病变(non-proliferative diabetic retinopathy, NPDR) 的改善作用及其机制。实验方案经上海中医药大学实验动物福利与伦理委员会审查, 符合实验动物福利与伦理相关规范(伦理号: PZSHUTCM 211115004)。通过对大鼠腹腔单次注射STZ诱导糖尿病模型, 注射两个月后, 分别按照20、40和80 mg·kg-1的剂量双眼滴眼PNS溶液, 每日2次, 每次间隔6 h, 连续1个月。通过对大鼠眼球进行苏木精-伊红染色和免疫组化分析, 观察视网膜的形态结构变化和小胶质细胞的活化情况; 采用伊文思蓝染料渗漏实验, 观察血-视网膜屏障(blood-retina barrier, BRB) 的破坏情况; 利用胰酶消化视网膜并进行染色, 观察视网膜中无细胞毛细血管的数量; 通过尾静脉注射异硫氰酸荧光素偶联刀豆蛋白A凝集素, 观察视网膜中黏附的中性粒细胞数量; 采用酶联免疫实验检测血清中炎症因子的表达; 采用Western blot实验检测视网膜组织中相关蛋白的表达以及核因子κB (nuclear factor kappa-B, NF-κB) 的转录激活。结果发现, PNS溶液滴眼给药能够显著增加视网膜的厚度、减少无细胞毛细血管的数量以及上调紧密连接蛋白claudin-1和occludin的表达, 从而缓解BRB的损伤。此外, PNS溶液滴眼给药也能够显著减少中性粒细胞的黏附和小胶质细胞的活化、降低血清中炎症因子的表达以及视网膜p65蛋白的核转移, 有效抑制视网膜炎症的发生。以上结果表明, PNS溶液滴眼给药可以通过抑制NF-κB信号通路的激活, 降低炎症的发生, 从而发挥改善NPDR的作用。

三七总皂苷  /  滴眼给药  /  非增殖性糖尿病视网膜病变  /  血-视网膜屏障  /  炎症因子  /  核因子κB

Diabetic retinopathy (DR) is a diabetic ocular complication that can lead to poor vision and blindness. This experiment aimed to investigate the ameliorative effect and its mechanism of Panax notoginseng saponins (PNS) eye drops on streptozotocin (STZ)-induced non-proliferative diabetic retinopathy (NPDR) in rats. All experiments were approved by the Animal Research Committee of Shanghai University of Traditional Chinese Medicine. Animal welfare and the animal experimental protocols were strictly consistent with related ethics regulations of Shanghai University of Traditional Chinese Medicine (No. PZSHUTCM 211115004). Diabetes mellitus was induced by a single intraperitoneal injection of STZ into rats. Two months later, PNS solution was dropped binocular twice per day at 6 h intervals at dose of 20, 40, and 80 mg·kg-1 continuously for 1 month. The morphological structure and activation of microglia of the retina were observed by hematoxylin-eosin staining and immunohistochemical assay. The disruption of the blood-retina barrier (BRB) was conducted by the Evans blue dye leakage assay. The number of acellular capillaries in the retina was assessed by digesting and hematoxylin-eosin staining assay. The number of retinal leukocyte adhesion was observed by fluorescein isothiocyanate-coupled concanavalin A lectin labeling assay. The serum expression of inflammatory factors was measured using enzyme-linked immunosorbent assay. Western blot experiments were used to detect the expression of relevant proteins in retinal tissue and transcriptional activation of nuclear factor kappa-B (NF-κB). The results revealed that PNS eye drops significantly increased the thickness of the retina, decreased the number of acellular capillaries, and up-regulated the expression of the tight junction proteins claudin-1 and occludin, thereby alleviating BRB damage. In addition, PNS eye drops were also able to significantly reduce leukocyte adhesion and microglia activation, the expression of inflammatory factors in serum, and the nuclear translocation of retinal p65 proteins, effectively inhibiting the occurrence of retinal inflammation. The above results showed that PNS eye drops played a role in improving NPDR by inhibiting the activation of the NF-κB signaling pathway and reducing inflammation.

Panax notoginseng saponins  /  eye-dropping administration  /  non-proliferative diabetic retinopathy  /  blood-retinal barrier  /  inflammatory factor  /  nuclear factor kappa-B
孙鑫, 王亚茹, 程雪梅, 陈泓谕, 陈明, 赖树生, 季莉莉, 尉小慧, 王长虹. 三七总皂苷溶液滴眼给药对大鼠非增殖性糖尿病视网膜病变的改善作用. 药学学报, 2024 , 59 (5) : 1271 -1279 . DOI: 10.16438/j.0513-4870.2023-1150
Xin SUN, Ya-ru WANG, Xue-mei CHENG, Hong-yu CHEN, Ming CHEN, Shu-sheng LAI, Li-li JI, Xiao-hui WEI, Chang-hong WANG. Ameliorative effect of Panax notoginseng saponins eye drops on non-proliferative diabetic retinopathy in rats[J]. Acta Pharmaceutica Sinica, 2024 , 59 (5) : 1271 -1279 . DOI: 10.16438/j.0513-4870.2023-1150
正文
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糖尿病视网膜病变(diabetic retinopathy, DR) 是一种糖尿病微血管并发症[1], 是导致成年人视力低下和失明的主要原因, 也是世界卫生组织公布的三大致盲的重点眼科疾病之一。DR的临床症状主要包括视网膜缺血、异常新生血管、血管通透性增加等[2]。DR根据病理特征分为非增殖性DR (non-proliferative DR, NPDR) 和增殖性DR (proliferative DR, PDR)。NPDR是DR的早期阶段, 周细胞丢失致毛细血管稳定性下降, 表现为血管通透性增加和毛细血管闭塞; PDR是DR的晚期阶段, 视网膜出现缺血缺氧, 表现为出现异常的新生血管[3, 4]。PDR对视网膜的损害程度远大于NPDR, NPDR可以进一步恶化演变为PDR。
三七[Panax notoginsen (Burk.) F. H. Chen] 为五加科人参属植物, 是一味活血化瘀类中药, 其中三七总皂苷(Panax notoginseng saponins, PNS) 作为三七的主要化学成分, 具有活血化瘀和消肿定痛等药理作用, 临床上常用于抗栓和抗炎等作用[5]。在DR早期, 高糖导致的视网膜缺血使血管出现堵塞, 继而引发一系列反应对视网膜造成损伤, PNS因其活血化瘀和抗炎作用能够缓解血管堵塞。有研究表明, PNS口服能够改善链脲佐菌素(streptozotocin, STZ) 诱导的NPDR[6], 但是口服给药会使PNS中的主要成分被胃液降解, 还会受到血眼屏障的影响, 导致到达眼部的药物较少[7]。眼部给药可以直接作用于病变部位并且维持较高的药物浓度。常见的眼部给药方式有玻璃体注射、滴眼液和眼周注射等, 其中滴眼液是治疗眼部疾病的首选给药方式[8]。本文旨在研究PNS溶液滴眼给药对STZ诱导的NPDR的改善作用, 探讨其作用机制, 为后续滴眼剂的研制提供依据。
材料与方法
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药物与试剂  PNS (批号: 20220401) 由广西梧州中恒集团有限公司赠送; Accu-Check血糖试纸购自德国Roche公司; 柠檬酸无水(MB8820)、柠檬酸钠二水(MB2492)、STZ (MB1227)、伊文思蓝染料(MB4680)、甲酰胺(MB2593) 购自大连美仑生物技术有限公司; 异硫氰酸荧光素偶联刀豆蛋白A凝集素(fluorescein isothiocyanate-coupled concanavalin A lectin, FITC-ConA, GTX01505) 购自美国Vector Laboratories公司; claudin-1抗体(sc-81796) 购自美国Santa Cruz公司; occludin (ABT146)、核因子κB (NF-κB) p65 (4764T)、磷酸化的NF-κB p65 (p-p65, 3033T)、β-actin (4970T)、lamin B1 (13435S) 抗体、离子钙结合衔接分子1 (ionized calcium-binding adapter molecule 1, Iba-1, 17198T) 购自美国Cell Signaling Technology公司; 蛋白marker (8~180 kDa, 20350ES72)、胰蛋白酶(40101ES25)、BCA蛋白质测定试剂盒(20201ES76)、过氧化物酶结合的山羊抗兔免疫球蛋白G (IgG) (H+L, 33707ES60)、抗小鼠IgG (H+L, 33207ES60) 购自上海翌圣生物科技股份有限公司; 胞浆胞核提取试剂(78833) 购自美国Thermo Scientific公司; 酶联免疫吸附实验(enzyme-linked immunosorbent assay, ELISA) 试剂盒购自上海威奥生物科技有限公司; 超敏ECL化学发光试剂盒(P0018S) 购自碧云天生物技术有限公司。
主要仪器  Accu-Check血糖仪(德国Roche公司); 解剖镜、IX81荧光倒置显微镜(日本Olympus公司); HL-2D定时数显恒流泵(上海沪西分析仪器厂有限公司); 电热鼓风真空干燥箱(上海一恒科学仪器有限公司); 酶标仪(美国BioTek公司); S0200-230V-EU型涡旋混合器(美国Labnet公司); 低温高速冷冻离心机(德国Eppendorf公司); 蛋白垂直电泳仪、转膜仪(美国Bio-Rad公司); BP211D电子分析天平(德国Sartorins公司); 超纯水过滤仪(美国Millipore公司)。
实验动物  雄性Sprague-Dawley (SD) 大鼠(体重200 ± 20 g), 购自上海斯莱克实验动物技术有限公司, 动物许可证号: SCXK (沪) 2022-0004。饲养于无特殊病原体环境中, 温度为(25 ± 2) ℃, 湿度为(55 ± 15)%, 明暗循环12 h。实验开始前进行习服饲养7天, 自由饮水和鼠粮喂养1周。本文中动物福利和实验过程均遵循上海中医药大学实验动物伦理委员会的规定(伦理号: PZSHUTCM 211115004)。
滴眼用PNS溶液的制备  称取5、10和20 g PNS溶于50 mL纯水中, 分别加入404、358、266 mg氯化钠(NaCl) 调节渗透压至与泪液等渗(300 mOsm·L-1), 即得PNS低(100 mg·mL-1)、中(200 mg·mL-1)、高(400 mg·mL-1) 剂量滴眼溶液。
模型建立[9]  将0.1 mol·L-1柠檬酸溶液与柠檬酸钠溶液以14∶11的比例混匀, 调pH至4.4, 用以配制STZ溶液。称取适量STZ粉末, 避光溶解配成一定浓度。80只已禁食过夜的大鼠按65 mg·kg-1的剂量腹腔注射STZ诱导糖尿病模型。另有20只大鼠腹腔注射柠檬酸钠缓冲液作为正常对照组。造模7天后尾静脉取血检测空腹血糖浓度(fasting blood glucose, FBG), FBG ≥ 16.7 mmol·L-1 (250 mg·dL-1) 视为糖尿病造模成功。
分组与给药  将造模成功的糖尿病大鼠, 按照体重和FBG随机分为模型组、PNS滴眼液低、中、高剂量组, 每组20只。STZ腹腔注射2个月后, 滴眼液低、中、高剂量组分别按照20、40和80 mg·kg-1的剂量分别给予大鼠双眼滴入100、200、400 mg·mL-1的PNS等渗溶液; 正常组和模型组分别给予大鼠双眼滴入生理盐水; 每日2次, 每次间隔6 h, 连续给药1个月。实验期间, 对大鼠的血糖和体重进行记录。给药结束后, 每组4只大鼠进行病理切片、免疫荧光分析和视网膜无细胞毛细血管实验。每组6只大鼠进行伊文思蓝染料渗漏实验。每组4只大鼠进行视网膜中性粒细胞黏附实验。剩余6只大鼠麻醉, 收集血清和视网膜, -80 ℃保存。
病理切片和免疫组化分析  解剖大鼠, 从左心室灌入磷酸盐缓冲盐溶液(phosphate buffered saline, PBS) 以清除血管中的血液。将大鼠左眼固定在眼科固定液中, 嵌入石蜡中, 并进行切片(5 μm)。视网膜切片用苏木精-伊红(hematoxylin-eosin, HE) 染色, 用倒置显微镜拍摄获得切片的图像。将石蜡包埋的视网膜切片(5 μm) 在二甲苯中去掉石蜡, 并在乙醇梯度中用蒸馏水进行再水化。在内源性过氧化物酶活性被淬灭后, 将视网膜切片与5%的牛血清白蛋白孵化, 以减少非特异性结合。将视网膜切片与相应的抗体在4 ℃下孵育过夜, 并与物种匹配的荧光二抗在室温下孵育1 h, 细胞核在室温下用DAPI染色10 min。在荧光倒置显微镜下捕捉图像。
无细胞毛细血管数量分析[6]  取出大鼠右眼, 用4%多聚甲醛(paraformaldehyde, PFA) 固定24 h, 之后用PBS清洗4次。将视网膜剥离, 然后用3%的胰蛋白酶在37 ℃下消化1 h, 从视网膜组织中分离出视网膜血管。为了量化视网膜中的无细胞毛细血管, 对分离出的视网膜血管进行HE染色, 用倒置显微镜对视野内的视网膜无细胞毛细血管进行观察并拍照, 计算3个视野下的无细胞毛细血管总数量, 以平均值代表视网膜样本中无细胞毛细血管的数量。
视网膜伊文思蓝染料渗漏实验  将伊文思蓝染料溶解于PBS中, 配制浓度为20 g·L-1溶液, 以10 μL·g-1进行大鼠腹腔注射, 循环2 h后, 左心室灌洗PBS以清除大鼠体循环中的伊文思蓝染料。摘取眼球, 剥离出视网膜组织, 放于真空干燥箱中55 ℃真空干燥5 h, 称取视网膜组织干燥后质量。加入120 μL甲酰胺, 于70 ℃水浴18 h萃取出伊文思蓝染料。萃取液10 000 r·min-1离心1 h, 吸取100 μL萃取液的上清, 用酶标仪在620 nm波长处测量吸光度值, 代入标准曲线, 计算出伊文思蓝染料的量, 计算伊文思蓝染料的量与视网膜组织干燥后质量的比值, 即得视网膜组织中伊文思蓝染料渗漏量(ng·g-1)。
中性粒细胞黏附实验[10]#160; 大鼠尾静脉注射600 μL 5 mg·mL-1 FITC-ConA以标记黏附的白细胞和血管内皮细胞。体循环2 h后, 解剖大鼠, 从左心室灌注PBS以去除红细胞和非黏附的白细胞。取出左眼在4% PFA中固定2 h, 然后将视网膜分离并置于载玻片上。为了量化黏附在视网膜上的白细胞, 用荧光倒置显微镜对视野内的白细胞数量进行观察并拍照, 计算3个视野下黏附的中性粒细胞的总数量, 以平均值代表视网膜样本黏附的中性粒细胞的数量。
ELISA#160; 大鼠血液于4 000 r·min-1离心10 min, 移取上层血清, 血清中的肿瘤坏死因子-α (tumor necrosis factor-α, TNF-α)、白细胞介素-6 (interleukin-6, IL-6) 和白细胞介素-1β (interleukin-1β, IL-1β) 检测按照ELISA试剂盒方法操作。
Western blot实验  提取总蛋白样品: 将视网膜从-80 ℃冰箱取出, 在冰上解冻后, 加入裂解液, 静置5 min, 在组织匀浆机中匀浆至均匀且无明显组织块的液体, 液氮反复冻融5次, 15 000 r·min-1、4 ℃离心10 min, 上清即为总蛋白样本。
提取胞浆胞核样品: 视网膜在冰上解冻后, 加入胞浆胞核抽提试剂盒中的CRI液, 在组织匀浆机中匀浆至均匀且无明显组织块的液体, 冰上静置2 h, 加入CR II液, 涡旋5 s, 15 000 r·min-1、4 ℃离心10 min, 上清即为胞浆样品。在胞浆沉淀中加入NR溶液, 反复涡旋6次后, 15 000 r·min-1、4 ℃离心10 min, 上清即为胞浆样品。
使用BCA蛋白定量试剂盒测定样本的蛋白浓度, 将所有样品统一到相等的蛋白浓度。蛋白质样品通过SDS-PAGE分离, 然后转移到PVDF膜上。用5% BSA在TBST中封闭2 h后, 在4 ℃下用相应的一抗将膜孵化过夜。用TBST清洗3次, 每次10 min, 在室温下用相应的二抗孵育1 h。最后, 用化学发光试剂观察蛋白的表达, 并通过计算目标蛋白印迹与内部对照的灰色密度进行量化。
统计学分析  实验数据以$\overline{x} \pm s$表示, 使用GraphPad Prism 8统计软件进行分析, 组间差异的显著性通过单因素方差分析进行评估, 然后进行Bonferroni事后检验。P < 0.05为差异有统计学意义。
结果
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1 体重和FBG
正常对照组大鼠的体重在整个实验过程中稳步上升, 糖尿病大鼠的体重则无明显变化(P < 0.001); 此外, 糖尿病大鼠的FBG在第7天后趋于稳定, 且明显高于正常对照组大鼠(P < 0.001)。然而, 研究结果显示PNS溶液滴眼给药(20、40和80 mg·kg-1) 治疗并不影响糖尿病大鼠的体重和FBG (图 1)。
2 病理切片分析
与正常对照组大鼠的视网膜相比, 模型组糖尿病大鼠的视网膜细胞数量减少, 细胞间的排列变得松散。与模型组相比, PNS溶液滴眼给药组大鼠的视网膜细胞数量减少的情况得到了改善(图 2A)。此外, 细胞数量的减少会导致糖尿病大鼠的视网膜内核层(inner nuclear layer, INL) 厚度明显减少(P < 0.001), PNS溶液滴眼给药(40和80 mg·kg-1) 治疗的糖尿病大鼠, 视网膜INL厚度的减少明显增加(P < 0.001, 图 2B)。
3 无细胞毛细血管数量分析
与正常对照组大鼠相比, 模型组糖尿病大鼠的视网膜无细胞毛细血管数量明显增加(P < 0.001); 与模型组相比, PNS溶液滴眼给药(20、40和80 mg·kg-1) 治疗的糖尿病大鼠的视网膜无细胞毛细血管数量明显减少(P < 0.05, 图 3)。
4 伊文思蓝染料检测血管渗漏
与正常对照组大鼠相比, 模型组糖尿病大鼠的视网膜伊文思蓝染料的渗漏量显著增加, 说明STZ造模后, 糖尿病大鼠的视网膜血管的通透性增加。与模型组相比, PNS溶液滴眼给药组(40和80 mg·kg-1) 的伊文思蓝染料渗漏量显著降低(P < 0.05), 说明PNS溶液滴眼给药可以有效地降低血管的通透性, 改善NPDR模型的血管功能(图 4)。
5 Claudin-1和occludin的Western blot分析
Claudin-1和occludin作为视网膜组织中的紧密连接蛋白, 通过增加紧密连接蛋白的表达可以改善BRB的通透性。与正常对照组大鼠相比, 模型组糖尿病大鼠的视网膜组织中紧密连接蛋白claudin-1和occludin的表达明显下降(P < 0.001, P < 0.01)。与模型组相比, PNS溶液滴眼给药(40和80 mg·kg-1) 治疗的糖尿病大鼠的视网膜claudin-1和occludin的蛋白表达明显上调(图 5)。
6 视网膜小胶质细胞的活化情况
在糖尿病视网膜病变的发展过程中, 小胶质细胞发挥着重要作用; Iba-1作为小胶质细胞理想的生物标记物, 常被用来判断小胶质细胞的活化状态。与正常对照组大鼠相比, 模型组糖尿病大鼠的视网膜神经节细胞层、外丛状层和内丛状层中Iba-1的数量增加, 表明糖尿病大鼠的小胶质细胞被激活, PNS溶液滴眼给药治疗能够抑制糖尿病大鼠视网膜中小胶质细胞的活化(图 6)。
7 中性粒细胞黏附分析
与正常对照组大鼠相比, 模型组糖尿病大鼠的视网膜血管内皮细胞上黏附的中性粒细胞数量显著增加(P < 0.001), 用PNS溶液滴眼给药(20、40和80 mg·kg-1) 治疗后, 糖尿病大鼠视网膜血管内皮细胞上白细胞黏附数量的增加被明显逆转(P < 0.01, P < 0.001, P < 0.001, 图 7)。
8 ELISA检测血清中炎症因子的表达
与正常对照组大鼠相比, 模型组糖尿病大鼠的血清中TNF-α、IL-6和IL-1β的表达量显著升高; 与模型组相比, PNS溶液滴眼给药(20、40和80 mg·kg-1) 治疗可以有效降低糖尿病大鼠血清中TNF-α、IL-6和IL-1β的表达(图 8)。
9 NF-κB的转录激活机制研究
与正常对照组大鼠相比, 模型组糖尿病大鼠视网膜组织中胞核p65蛋白表达量增加(P < 0.001); 与模型组相比, PNS溶液滴眼给药(20、40和80 mg·kg-1) 治疗后, 糖尿病大鼠胞核中p65的蛋白表达量明显减少(P < 0.05, P < 0.01, P < 0.001, 图 9)。
讨论
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DR是慢性进行性糖尿病导致的视网膜微血管渗漏和阻塞, 是糖尿病常见的微血管并发症之一, 也是导致视力低下和失明的主要原因。临床上, DR主要表现为神经变性、血管渗漏、血管新生[11], 视网膜脱离, 甚至是失明[12]。DR根据是否出现新生血管分为NPDR和PDR[13], 在大鼠模型中, 通常采用STZ造模后观察两个月, 给药1个月的实验方案研究药物对NPDR大鼠的药效[6, 14]。
在NPDR大鼠模型中, 视网膜神经变性通常发生在血管损伤之前, 表现为视网膜细胞凋亡导致的视网膜层变薄和神经元活动丧失[15-17]。结果显示, PNS溶液滴眼给药1个月后显著抑制了视网膜神经细胞的损伤, 有效改善了视网膜病变。BRB破坏引起的视网膜通透性增强是视网膜血管功能性损伤的重要特征, 无细胞毛细血管增加是视网膜血管形态学损伤的重要特征。本研究通过伊文思蓝染料渗漏实验观察视网膜的血管功能, 无细胞毛细血管实验监测视网膜血管的形态, 结果显示PNS溶液滴眼给药可以显著改善视网膜血管的损伤。紧密连接蛋白的表达量与BRB的破坏密切相关。BRB由内部和外部屏障组成, 其中视网膜的内部BRB由视网膜毛细血管内皮细胞之间的紧密连接组成, 外部BRB由视网膜色素上皮细胞之间的紧密连接组成[18]。Claudin-1和occludin是主要的紧密连接蛋白, 对维持BRB的完整性至关重要[13], 其蛋白表达减少会增加BRB的破坏。PNS溶液滴眼给药能够通过增加claudin-1和occludin蛋白的表达, 减少BRB的破坏。如果结合视网膜电图(electroretinogram, ERG)、光学相干断层扫描(optical coherence tomography, OCT) 等眼底造影技术, 将能够更加直观地观察视网膜形态和血管的变化。
炎症早已被认为是DR发展和恶化的一个因素。小胶质细胞是视网膜上的免疫细胞, 其活化会诱导视网膜炎性损伤的发生[19]。Iba-1是一个常用的小胶质细胞的生物标志物。本实验结果显示, PNS溶液滴眼给药后能够减少Iba-1的数量, 抑制小胶质细胞的激活。此外, 在炎症条件下, 白细胞迁移的能力增强, 白细胞黏附在视网膜血管内皮上是DR中炎症可识别的特征之一[20], 可导致内皮细胞损伤和坏死、BRB破坏和血管通透性增加[21, 22]。PNS溶液滴眼给药可以减少白细胞对视网膜的黏附。
NF-κB是促炎症基因转录的显著调节因子, 在DR进展过程中对调节视网膜炎症至关重要[23]。NF-κB信号通路的激活可以调节炎症因子TNF-α、IL-1β和IL-6以及趋化因子的表达, 进一步诱发神经变性、BRB破坏、白细胞黏附和血管损伤。在本研究中, PNS溶液滴眼给药降低炎症因子TNF-α、IL-1β和IL-6的表达量, 减少p65从细胞质到细胞核的核转位, 说明PNS溶液滴眼给药能够通过抑制NF-κB信号通路的激活而改善视网膜炎症。
综上所述, PNS溶液滴眼给药可以通过抑制NF-κB信号通路的激活, 抑制DR发生和发展过程中的视网膜炎症, 从而明显减轻糖尿病大鼠的视网膜损伤和BRB的渗漏。此外, 课题组前期的研究结果显示口服PNS溶液也是通过抑制NF-κB信号通路的激活, 达到改善DR的作用[6]。然而, 伊文思蓝染料渗漏量的指标检测结果显示, PNS口服剂量需要达到160 mg·kg-1时才能够显著减少伊文思蓝染料的渗漏量(P < 0.05), 而PNS溶液滴眼给药剂量为40 mg·kg-1时就能够显著降低伊文思蓝染料的渗漏量(P < 0.05), 说明滴眼给药剂量达到口服剂量1/4时, 两者的疗效相当。眼部给药的安全性也至关重要, 在PNS溶液滴眼给药过程中未发现大鼠眼部出现分泌物和红肿等情况。另一项采用家兔对PNS温敏凝胶滴眼剂的刺激性进行评价, 结果也未发现不良刺激性(数据另文发表)。说明PNS滴眼给药是一种安全的给药方式, 在DR的治疗中具有巨大的应用潜力。
作者贡献: 孙鑫负责完成动物实验、采集数据、分析数据和撰写文章; 王亚茹负责动物实验、分析数据和修改文稿; 陈泓谕负责动物实验; 程雪梅、陈明、赖树生、季莉莉、尉小慧负责指导实验方案; 王长虹负责指导实验方案、文章的审阅和修改。
利益冲突: 本研究与任何组织和个人均不存在利益冲突。
基金
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  • 上海市卫健委中医药传承创新发展三年行动计划建设项目(ZY(2021-2023)-0215)
  • 广西科技基地和人才专项(Guike AD20297068)
  • 上海中医药大学三七研究中心项目(SQZX202103)
文献
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2024年第59卷第5期
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doi: 10.16438/j.0513-4870.2023-1150
  • 接收时间：2023-10-10
  • 首发时间：2025-11-27
  • 出版时间：2024-05-12
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  • 收稿日期：2023-10-10
  • 修回日期：2023-12-16
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上海市卫健委中医药传承创新发展三年行动计划建设项目(ZY(2021-2023)-0215)
广西科技基地和人才专项(Guike AD20297068)
上海中医药大学三七研究中心项目(SQZX202103)
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    1.上海中医药大学中药研究所, 中药标准化教育部重点实验室, 上海市复方中药重点实验室, 上海 201203
    2.广西三七综合利用技术重点实验室, 广西 梧州 543000

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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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