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Article(id=1239201874243547595, tenantId=1146029695717560320, journalId=1205117082300743687, issueId=1239201870791627164, articleNumber=null, orderNo=null, doi=10.14109/j.cnki.xyylc.2024.03.03, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=null, receivedDate=1656604800000, receivedDateStr=2022-07-01, revisedDate=null, revisedDateStr=null, acceptedDate=1681401600000, acceptedDateStr=2023-04-14, onlineDate=1773378350077, onlineDateStr=2026-03-13, pubDate=1711296000000, pubDateStr=2024-03-25, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1773378350077, onlineIssueDateStr=2026-03-13, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1773378350077, creator=13701087609, updateTime=1773378350077, updator=13701087609, issue=Issue{id=1239201870791627164, tenantId=1146029695717560320, journalId=1205117082300743687, year='2024', volume='43', issue='3', pageStart='161', pageEnd='240', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1773378349254, creator=13701087609, updateTime=1773378470498, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1239202379392938830, tenantId=1146029695717560320, journalId=1205117082300743687, issueId=1239201870791627164, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1239202379397133135, tenantId=1146029695717560320, journalId=1205117082300743687, issueId=1239201870791627164, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=177, endPage=181, ext={EN=ArticleExt(id=1239201874470040014, articleId=1239201874243547595, tenantId=1146029695717560320, journalId=1205117082300743687, language=EN, title=Anti-inflammatory effects and mechanisms of sodium-glucose cotransporter 2 inhibitors in cardiovascular diseases, columnId=1207314219599499390, journalTitle=Chinese Journal of New Drugs and Clinical Remedies, columnName=Review, runingTitle=null, highlight=null, articleAbstract=

Sodium-glucose cotransporter 2 （SGLT-2） inhibitors comprise a new class of oral hypoglycemic agents that promote the excretion of urine sugar and reduce blood sugar mainly by inhibiting the reabsorption of glucose in proximal renal tubules. Numerous clinical studies have found that SGLT-2 inhibitors have good effects on cardiovascular system. At the same time, many basic studies have found that a variety of SGLT-2 inhibitors exhibit anti-inflammatory activity in both cellular and animal models, and the cardiovascular protective mechanism may be closely related to inhibiting inflammatory response. For example, canagliflozin inhibits inflammatory response by enhancing anti-inflammatory signaling pathways such as AMP activated protein kinase （AMPK） and endothelial nitric oxide synthase （eNOS）. Dapagliflozin significantly reduces the expression of inflammatory factors such as interleukin （IL）-1β, IL-6, and tumor necrosis factor （TNF）-α, and promotes the polarization of macrophages towards anti-inflammatory phenotype. Empagliflozin reduces cardiac inflammation in diabetes cardiomyopathy, hypertension, and heart failure models.

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钠-葡萄糖共转运蛋白（SGLT）-2抑制剂是一类新型口服降血糖药，主要通过抑制肾脏近端小管葡萄糖的重吸收，促进尿糖排泄，降低血糖。大量临床研究发现SGLT-2抑制剂具有良好的心血管保护作用。同时，众多基础研究发现多种SGLT-2抑制剂在细胞及动物模型中表现出良好的抗炎活性，SGLT-2抑制剂的心血管保护机制可能与抑制炎症反应密切相关。如卡格列净通过提高AMP活化蛋白激酶（AMPK）、内皮型一氧化氮合酶（eNOS）等抗炎信号传导抑制炎症反应；达格列净可显著降低白细胞介素（IL）-1β、IL-6及肿瘤坏死因子（TNF）-α等炎症因子的表达，促进巨噬细胞向抗炎表型的极化；恩格列净可以减少糖尿病心肌病、高血压和心力衰竭模型中的心脏炎症。

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吕建峰
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王悦，男，硕士在读，主要从事冠心病与焦虑抑郁的研究，E-mail: 。

吕建峰，男，主任医师，博士，主要从事冠心病与焦虑抑郁的研究，E-mail:

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王悦，男，硕士在读，主要从事冠心病与焦虑抑郁的研究，E-mail: 。

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王悦，男，硕士在读，主要从事冠心病与焦虑抑郁的研究，E-mail: 。

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钠-葡萄糖共转运蛋白2抑制剂在心血管疾病中的抗炎作用及机制
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王悦 , 李冰清 , 陈余文 , 李文倩 , 万少枝 , 李册兴 , 孙培媛 , 吕建峰
中国新药与临床杂志 | 综述 2024,43(3): 177-181
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中国新药与临床杂志 | 综述 2024, 43(3): 177-181
钠-葡萄糖共转运蛋白2抑制剂在心血管疾病中的抗炎作用及机制
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王悦 , 李冰清, 陈余文, 李文倩, 万少枝, 李册兴, 孙培媛, 吕建峰
作者信息
  • 三峡大学附属仁和医院　心血管内科，湖北　宜昌　443000

    • 王悦，男，硕士在读，主要从事冠心病与焦虑抑郁的研究，E-mail: 。

    吕建峰，男，主任医师，博士，主要从事冠心病与焦虑抑郁的研究，E-mail:

通讯作者:

吕建峰
Anti-inflammatory effects and mechanisms of sodium-glucose cotransporter 2 inhibitors in cardiovascular diseases
Yue WANG , Bing-qing LI, Yu-wen CHEN, Wen-qian LI, Shao-zhi WAN, Ce-xing LI, Pei-yuan SUN, Jian-feng LÜ
Affiliations
  • Cardiovascular Department, Affiliated Renhe Hospital of China Three Gorges University, Yichang HUBEI 443000, China
出版时间: 2024-03-25 doi: 10.14109/j.cnki.xyylc.2024.03.03
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摘要
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钠-葡萄糖共转运蛋白（SGLT）-2抑制剂是一类新型口服降血糖药，主要通过抑制肾脏近端小管葡萄糖的重吸收，促进尿糖排泄，降低血糖。大量临床研究发现SGLT-2抑制剂具有良好的心血管保护作用。同时，众多基础研究发现多种SGLT-2抑制剂在细胞及动物模型中表现出良好的抗炎活性，SGLT-2抑制剂的心血管保护机制可能与抑制炎症反应密切相关。如卡格列净通过提高AMP活化蛋白激酶（AMPK）、内皮型一氧化氮合酶（eNOS）等抗炎信号传导抑制炎症反应；达格列净可显著降低白细胞介素（IL）-1β、IL-6及肿瘤坏死因子（TNF）-α等炎症因子的表达，促进巨噬细胞向抗炎表型的极化；恩格列净可以减少糖尿病心肌病、高血压和心力衰竭模型中的心脏炎症。

钠-葡萄糖共转运蛋白2抑制剂  /  心血管系统  /  炎症  /  药理作用分子作用机制

Sodium-glucose cotransporter 2 （SGLT-2） inhibitors comprise a new class of oral hypoglycemic agents that promote the excretion of urine sugar and reduce blood sugar mainly by inhibiting the reabsorption of glucose in proximal renal tubules. Numerous clinical studies have found that SGLT-2 inhibitors have good effects on cardiovascular system. At the same time, many basic studies have found that a variety of SGLT-2 inhibitors exhibit anti-inflammatory activity in both cellular and animal models, and the cardiovascular protective mechanism may be closely related to inhibiting inflammatory response. For example, canagliflozin inhibits inflammatory response by enhancing anti-inflammatory signaling pathways such as AMP activated protein kinase （AMPK） and endothelial nitric oxide synthase （eNOS）. Dapagliflozin significantly reduces the expression of inflammatory factors such as interleukin （IL）-1β, IL-6, and tumor necrosis factor （TNF）-α, and promotes the polarization of macrophages towards anti-inflammatory phenotype. Empagliflozin reduces cardiac inflammation in diabetes cardiomyopathy, hypertension, and heart failure models.

sodium-glucose cotransporter 2 inhibitor  /  cardiovascular system  /  inflammatory  /  molecular mechanisms of pharmacological action
王悦, 李冰清, 陈余文, 李文倩, 万少枝, 李册兴, 孙培媛, 吕建峰. 钠-葡萄糖共转运蛋白2抑制剂在心血管疾病中的抗炎作用及机制. 中国新药与临床杂志, 2024 , 43 (3) : 177 -181 . DOI: 10.14109/j.cnki.xyylc.2024.03.03
Yue WANG, Bing-qing LI, Yu-wen CHEN, Wen-qian LI, Shao-zhi WAN, Ce-xing LI, Pei-yuan SUN, Jian-feng LÜ. Anti-inflammatory effects and mechanisms of sodium-glucose cotransporter 2 inhibitors in cardiovascular diseases[J]. Chinese Journal of New Drugs and Clinical Remedies, 2024 , 43 (3) : 177 -181 . DOI: 10.14109/j.cnki.xyylc.2024.03.03
正文
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钠-葡萄糖共转运蛋白（sodium-glucose cotran-sporter, SGLT）-2抑制剂作为一类新型口服降血糖药物，在调节肾脏重吸收葡萄糖过程中发挥重要的作用，可以阻断近曲小管对葡萄糖的重吸收，排出多余的葡萄糖，从而达到降低血糖的目的[1]。大量随机双盲对照临床研究显示SGLT-2抑制剂具有心血管保护作用，其潜在作用机制可能是系统性地改善早期血流动力学以及直接的心肌和血管保护作用，如调控血管重构、抑制氧化应激、维持离子稳态、抑制炎症反应等[2,3]。本文探究SGLT-2抑制剂对炎症的干预作用，综述其在心血管疾病治疗及预防中的作用机制，为以炎症作为靶点治疗心血管疾病提供理论依据。
SGLT-2抑制剂的心血管保护作用
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多项随机双盲对照临床研究显示SGLT-2抑制剂具有良好的心血管保护作用[4]。在2型糖尿病（T2DM）合并心血管相关危险因素的人群中，EMPA-REG OUTCOME、CANVAS[5]及DECLARE-TIMI 58[6]等研究显示了SGLT-2抑制剂可降低全因死亡率、心血管死亡率及心力衰竭（心衰）再住院风险；在无论是否合并T2DM的心衰患者中，DAPA-HF[7]、EMPEROR-Reduced[8]和EMPEROR-Preserved[9]等临床研究均展现出SGLT-2抑制剂降低心血管死亡和心衰再住院风险的优势。不论是对于T2DM合并心血管疾病或心血管高危因素，亦或是单纯的心血管疾病，SGLT-2抑制剂均表现出不同程度的心血管保护作用。
抗炎在心血管疾病治疗中的潜力
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炎症反应在心血管系统疾病进程中普遍存在并起着关键作用。同时炎症也是许多其他疾病如慢性肾脏病、T2DM、癌症、抑郁症等的危险因素。炎症反应的特征属性是免疫细胞释放各种细胞因子，例如与促炎相关的白细胞介素（IL）-1β、IL-6、IL-8、IL-13、IL-18、C反应蛋白（CRP）、肿瘤坏死因子（TNF）-α、核因子（NF）-κB、基质金属蛋白酶（MMP）-9、单核细胞趋化蛋白（MCP）-1、血管细胞黏附分子（VCAM）-1和细胞间黏附分子（ICAM）-1等，以及与抗炎相关的IL-10、转化生长因子（TGF）-β等[10-13]，参与心血管疾病促炎与抗炎的调节。炎症是冠状动脉粥样硬化性心脏病重要的发病机制，血管内皮损伤后，内皮细胞分泌相关趋化因子，如MCP-1等。单核细胞、中性粒细胞、T细胞、B细胞、肥大细胞等趋化黏附于内膜下，单核细胞分化为巨噬细胞后摄取氧化低密度脂蛋白（ox-LDL）形成泡沫细胞，同时巨噬细胞等炎症细胞活化后释放大量炎症因子如IL-1、IL-6、TNF-α等，进而参与粥样斑块的形成与发展。IL-6、CRP和髓过氧化物酶（MPO）等炎症标志物的水平还可作为动脉粥样硬化风险预后的衡量指标[14]。因此，通过阻断动脉粥样硬化的相关炎症途径来降低远期心血管风险是一个有效的治疗策略[15]。如针对TNF-α的单克隆抗体研究，在类风湿关节炎及银屑病的患者中TNF-α抗体治疗后可观察到更低的粥样斑块发生率和更低的心血管事件发生率[16,17]。此外，靶向抑制IL-1β的单克隆抗体canakinumab导致心血管事件的复发率显著低于安慰剂[18,19]。基于许多心血管疾病共有的炎症反应这一病理基础，SGLT-2抑制剂作为一种具有多效性作用的药物，其抗炎活性或许是治疗心血管疾病的一个共同机制。寻找疾病的共用分子机制并定义药物更多的适应证可以为患者提供更加个体化、精准化治疗方案。在心血管疾病的治疗方面，SGLT-2抑制剂或许可以作为一种有潜力的抗炎调节剂。
SGLT-2抑制剂的抗炎作用及机制
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1　卡格列净（canagliflozin）
卡格列净对SGLT-1有轻度抑制作用。SGLT-2在心肌细胞中不表达，但SGLT-1在心肌中大量表达，其表达与心肌氧化应激、促纤维化及促炎症呈正相关。KONDO等[20]离体培养心脏手术患者的活检心肌组织细胞，高糖培养72 h模拟糖尿病环境，10 μmol·L-1卡格列净处理60 min或24 h，结果发现卡格列净可通过SGLT-1/AMP活化蛋白激酶（AMPK）/ Ras相关C3肉毒毒素底物1（Rac1）信号通路直接抑制NADPH氧化酶来源的氧化应激，抑制炎症和凋亡途径。卡格列净还可抑制SGLT-1，增加细胞内AMP/ATP比值，激活AMPK/一氧化氮合酶（NOS）信号通路，增加一氧化氮（NO）水平，而NO又可以抑制促炎信号通路，此外，AMPK的激活还可以抑制Rac1的激活以及Rac1和p47phox的膜转位，从而降低NADPH氧化酶活性和超氧化物的产生，在人心肌中发挥抗炎和抗凋亡作用[21]。另外有研究表明，T2DM患者动脉粥样硬化斑块中活跃的炎症反应可能与内皮细胞中SGLT-2的高表达有关，卡格列净处理后减少了粥样斑块中巨噬细胞的浸润，提高了沉默调节蛋白（SIRT）6的表达，降低了SGLT-2的蛋白和mRNA水平，并降低了NF-κB和MMP-9的蛋白表达，导致斑块胶原含量的增加和纤维帽的增厚，从而增加了斑块的稳定性，提示SGLT-2/SIRT6通路在糖尿病动脉粥样硬化病变的炎症过程中起关键作用[22]。HASAN等[23]采用异丙肾上腺素（ISO）诱导大鼠心脏氧化损伤模型，给予卡格列净5 mg·kg-1·d-1治疗2周，结果显示，卡格列净可增强抗炎信号传导，涉及AMPK、eNOS、红系衍生的核因子2相关因子2（Nrf2）等，卡格列净还可抑制NADPH氧化酶NOX4的过表达，NOX4是产生超氧自由基导致氧化应激和炎症的关键酶，表明卡格列净可通过多种途径发挥抗炎作用从而保护心脏。
2　达格列净（dapagliflozin）
在急性心肌梗死大鼠模型中，达格列净降低了IL-1β和IL-6 mRNA水平，并通过活性氧和活性氮依赖性STAT3途径介导了抗炎M2型巨噬细胞极化，上调抗炎细胞因子IL-10 mRNA水平，表明达格列净促进巨噬细胞向抗炎表型极化，从而实现其抗炎作用[24]。YE等[25]研究发现达格列净可通过降低T2DM小鼠核苷酸结合寡聚结构域样受体（NLRP）3炎症小体来减少心脏炎症。NLRP3炎症小体是一种IL-1β家族细胞因子激活的多蛋白信号复合物，在T2DM患者心脏中上调，并与心脏炎症相关，导致随后的糖尿病性心肌病[26]。在YE等[25]的研究中小鼠模型的NLRP3、IL-1β、IL-6、TNF-α mRNA水平明显增加，达格列净干预8周后上述指标显著下降，同时该研究的体外实验排除了达格列净的全身效应，在含有达格列净的培养基中孵育小鼠成纤维细胞16 h后，达格列净可使T2DM心肌成纤维细胞NLRP3、IL-1β和caspase-1 mRNA水平降低。由此可见，达格列净的抗炎作用可能与SGLT-2全身效应和降血糖作用无关，在体外模型中可观察到同样的效应，说明达格列净具有相对独立的抗炎作用。
3　恩格列净（empagliflozin）
有研究显示，在肥胖合并T2DM造成的心脏损伤小鼠模型中，模型组心肌间质纤维化、冠状动脉周围纤维化加重、冠状动脉增厚、心肌间质巨噬细胞浸润加重，恩格列净治疗10周后心肌间质纤维化、冠状动脉周围纤维化、冠状动脉增厚及心肌间质巨噬细胞浸润明显改善，心肌超氧化物水平显著降低[27,28]。在自发性高血压大鼠模型中，心肌组织中细胞凋亡加重，进行性心室收缩舒张功能障碍加重，TNF-α转录水平显著升高，恩格列净治疗12周后心肌组织中TNF-α表达显著降低，并明显改善了心功能及心肌纤维化[29,30]。此外，恩格列净可减弱斑马鱼胚胎心衰模型的促炎性细胞因子环氧合酶-2（COX-2）和IL-1β的表达[31]。以上证据表明，恩格列净可以减轻糖尿病心肌病、高血压和心衰模型中的心脏炎症。
4　伊格列净（ipragliflozin）
血管周围脂肪组织（PVAT）在心血管疾病的发病机制中起着重要作用。在肥胖或T2DM中，PVAT主要分泌促炎和促动脉粥样硬化细胞因子，这可能导致局部内皮功能障碍，从而导致全身和局部血管疾病的进展[32]。有研究发现伊格列净可以增加西方饮食模型小鼠腹部PVAT的脂肪细胞大小，下调促炎基因Ccl2、Ccr2和Emr1及促纤维化基因Col1a1、Col1a2和Fn1的表达[33]，提示伊格列净对PVAT中的炎症具有抑制作用。伊格列净还可降低糖尿病诱导内皮功能损伤模型小鼠腹主动脉中MCP-1、VCAM-1、ICAM -1等炎症因子的表达，表明伊格列净抑制了糖尿病状态下内皮细胞的炎症激活[34]；伊格列净还可降低链脲佐菌素诱导的糖尿病大鼠血浆IL-6、TNF-α、MCP-1和CRP水平，并且呈现剂量依赖性[35]。
5　其他SGLT-2抑制剂
在高脂饮食喂养的大鼠/小鼠模型中，可观察到托格列净（tofogliflozin）[36]及瑞格列净（remogliflozin）[37]对炎症相关细胞及因子的抑制作用。在T2DM小鼠模型中，鲁格列净（luseogliflozin）治疗可降低巨噬细胞标志物F4/80和促炎性细胞因子基因的表达[38]。这些SGLT-2抑制剂目前研究较少，其抗炎作用不甚明确。索格列净（sotagliflozin）是SGLT-1和SGLT-2双重抑制剂，在人体中，索格列净对SGLT-2的选择性比SGLT-1高20倍[39]。在一项对血糖正常、心脏压力超负荷小鼠模型的研究中，索格列净组出现一定程度心脏纤维化、左心室肌细胞肥大或散在的白细胞浸润等病理改变的比例更高，未观察到其对炎症的相关影响[40]。一项关于艾格列净（ertugliflozin）的临床研究[41]，将3期慢性肾脏病合并糖尿病患者随机分为安慰剂组和艾格列净组，在随访26周和52周时检测血浆生物标志物的变化，发现2组血浆中炎症、纤维化、氧化应激等标志物的变化无显著差异，这可能是由于观察时间不足，还有待进一步研究以及在较大队列中进行长期随访，以确定艾格列净对炎症生物标志物的影响。
总结与展望
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SGLT-2抑制剂在各项大型临床研究中均表现出良好的心血管预后[42]。但目前，SGLT-2抑制剂缓解炎症反应的研究主要集中在动物及离体细胞实验阶段，其在人体的确切疗效和机制有待更多的临床研究数据加以支持。以炎症相关通路作为靶点来治疗心血管疾病在未来的药物研发中或许是一个有潜力的领域，SGLT-2抑制剂更进一步的应用还需要更多基础及临床研究予以揭示和阐明。
基金
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  • 湖北省卫生健康委员会科研项目(WJ2021F061)
  • 湖北省卫生健康委中医药科研立项项目(ZY2021F018)
文献
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参考文献 引证文献
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2024年第43卷第3期
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doi: 10.14109/j.cnki.xyylc.2024.03.03
  • 接收时间：2022-07-01
  • 首发时间：2026-03-13
  • 出版时间：2024-03-25
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  • 收稿日期：2022-07-01
  • 录用日期：2023-04-14
基金
湖北省卫生健康委员会科研项目(WJ2021F061)
湖北省卫生健康委中医药科研立项项目(ZY2021F018)
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    三峡大学附属仁和医院　心血管内科，湖北　宜昌　443000

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吕建峰
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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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