微小RNA在脑缺血再灌注损伤中的研究现状与进展

doi:10.3877/cma.j.issn.2095-5782.2022.01.014

脑缺血性卒中是导致成人死亡和残疾的主要原因之一，血管再通获得及时的再灌注是临床治疗的首选方法，然而再灌注可诱发脑缺血再灌注损伤。研究结果显示，微小RNA（miRs）可作为潜在的治疗靶点，在脑缺血再灌注损伤中发挥重要作用。作为近年研究的热点，miRs的异常表达及功能受到更多关注。尽管已有相关研究提示了调节miRs对治疗脑缺血再灌注损伤的安全性和有效性，然而，目前尚缺乏相关的随机对照临床研究数据来证实，以确定统一标准指导。文章就miRs参与脑缺血再灌注损伤的信号通路、病理机制、以及各种相互作用等进行综述。

关键词: 脑缺血再灌注损伤, 微小RNA, 治疗靶点

Ischemic stroke is one of the leading cause of death and disability in adults. Vascular recanalization to obtain timely reperfusion is the preferred treatment in clinical practice. However, reperfusion can induce cerebral ischemia-reperfusion injury (CIRI). The present research reveal that microRNAs (miRs) have been implicated in CIRI and could serve as therapeutic targets. As a research hotspot, the abnormal expression and function of miRs have been receiving more and more attention. Although relevant studies have suggested the safety and effectiveness of regulating miRs in the treatment of CIRI, there are no randomized controlled trials to formulate uniform standard guideline. This article aims to make a comprehensive review about the current status and progress of the research on the signaling pathways, pathological mechanisms, and various interactions of miRs involved in CIRI.

Key words: Cerebral ischemia-reperfusion injury, MicroRNAs, Therapeutic targets

表1 miRNA在CIRI中的表达

进程	CIRI诱导下调	靶点	参考文献	CIRI诱导上调	靶点	参考文献
凋亡相关
	miR-211	PUMA	[54]	miR-99b	IGF1R	[54]
	miR-874-3p	BCL2LI3	[54]	miR-106-5p	Mcl-1	[54]
	miR-29a	AQP4	[54]	miR-138	SIRT1	[54]
	miR-496	BCL2LI4	[54]	miR-224-3p	FIP200	[54]
	miR-544	IRAK4	[54]	miR-155	GATA3	[54]
	miR-219a-5p	Pde4d	[54]	miR-429	GTAA3	[54]
	miR-26a-5p	DAPK1	[54]	miR-10a	PI3K	[54]
	miR-137	Notch1	[54]	miR-223	IGF1R	[54]
	miR-124	Ku70	[54]	miR-370	SIRT1	[54]
	miR-431	Rho	[54]	miR-128	WNT1	[32]
与氧化应激相关
	miR-144-3p	Brg1	[54]	miR-144	Nrl2	[54]
	miR-652	NOX2	[54]	miR-142-5p	Nrl2	[54]
	miR-124-5p	NOX2	[54]	miR-153	Nrl2	[54]
	miR-7a-5p	a-Syn	[54]	miR-93	Nrl2	[54]
	miR-375	Ctgf	[54]	miR-217	SIRT1	[54]
	miR-29a	PUMA	[54]	miR-135a	GSK-3β	[54]
	miR-455-3p	TP53INP1	[54]	miR-224-3p	FIP200	[54]
				miR-421	MCL1	[54]
				miR-134	Nrf2	[39]
与炎症反应相关
	miR-223	NLRP3	[54]	miR-193b-3p	5-LOX	[54]
	miR-211-5p	COX-2	[54]	miR-19a-3p	IGFBP3	[54]
	miR-338-5p	Ctgf	[54]	miR-155	MafB	[54] [30]
	miR-544	IRAK4	[54]	miR-217	SIRT1	[13][54]
	miR-182-5p	TLR4	[54]	miR-124	RhoA	[28][29]
	miR-146a	IRAK1	[54]
	miR-338-5p	Ctgf	[26]
	miR-1906	JAK2/STAT3	[22]
	miR-22	VEGF	[27]
与兴奋性毒性相关
	miR-1000	VGlut	[54]	miR-107	GLT-1	[54]
	miR-223	GluR2，NR2B	[54]
与细胞自噬相关
	miR-30	Beclin1	[54]	miR-124	PI3K	[54]
	miR-298	Act1	[54]
	miR-138	SIRT1	[54]
	miR-202-5p	eIF4E	[54]
与血脑屏障功能相关
	miR-539	MMP-9	[54]	miR-130a	—	[52]
	miR-21	MAP2K	[52] [54]	miR-150	—	[52]

	miR-429	Cxcll	[54]	miR-17	—	[52]
	miR-149-5p	SIPR2	[54]	miR-222	—	[52]
	miR-126	—	[52]	miR-378	—	[52]
	miR-150	—	[52]	miR-20a	—	[52]
				miR-19a/b	—	[52]
低氧（HIF-1）
	miR-613	ATG3轴	[21]	miR-373	—	[52]
	miR-26b	—	[29]	miR-24-1	—	[52]
				miR-181c	—	[52]
				miR-210	—	[52]
				miR-26a-2	—	[52]
				miR-23	—	[52]
				miR-24	—	[52]
				miR-103	—	[52]
				miR-107	—	[52]
其他
	miR-148b-3	—	[57]	miR-292-5p	—	[52]
	miR-488-3p	—	[53]	miR-290	—	[52]
				miR-206	—	[52]
				miR-215	—	[52]
				miR-214	—	[52]
				miR-223	—	[52]
				miR-298	—	[52]
				miR-327	—	[52]
				miR-494	Sox8	[52]
				miR-497	—	[52]
				miR-7674-5p	—	[57]

表1 miRNA在CIRI中的表达

进程	CIRI诱导下调	靶点	参考文献	CIRI诱导上调	靶点	参考文献
凋亡相关
	miR-211	PUMA	[54]	miR-99b	IGF1R	[54]
	miR-874-3p	BCL2LI3	[54]	miR-106-5p	Mcl-1	[54]
	miR-29a	AQP4	[54]	miR-138	SIRT1	[54]
	miR-496	BCL2LI4	[54]	miR-224-3p	FIP200	[54]
	miR-544	IRAK4	[54]	miR-155	GATA3	[54]
	miR-219a-5p	Pde4d	[54]	miR-429	GTAA3	[54]
	miR-26a-5p	DAPK1	[54]	miR-10a	PI3K	[54]
	miR-137	Notch1	[54]	miR-223	IGF1R	[54]
	miR-124	Ku70	[54]	miR-370	SIRT1	[54]
	miR-431	Rho	[54]	miR-128	WNT1	[32]
与氧化应激相关
	miR-144-3p	Brg1	[54]	miR-144	Nrl2	[54]
	miR-652	NOX2	[54]	miR-142-5p	Nrl2	[54]
	miR-124-5p	NOX2	[54]	miR-153	Nrl2	[54]
	miR-7a-5p	a-Syn	[54]	miR-93	Nrl2	[54]
	miR-375	Ctgf	[54]	miR-217	SIRT1	[54]
	miR-29a	PUMA	[54]	miR-135a	GSK-3β	[54]
	miR-455-3p	TP53INP1	[54]	miR-224-3p	FIP200	[54]
				miR-421	MCL1	[54]
				miR-134	Nrf2	[39]
与炎症反应相关
	miR-223	NLRP3	[54]	miR-193b-3p	5-LOX	[54]
	miR-211-5p	COX-2	[54]	miR-19a-3p	IGFBP3	[54]
	miR-338-5p	Ctgf	[54]	miR-155	MafB	[54] [30]
	miR-544	IRAK4	[54]	miR-217	SIRT1	[13][54]
	miR-182-5p	TLR4	[54]	miR-124	RhoA	[28][29]
	miR-146a	IRAK1	[54]
	miR-338-5p	Ctgf	[26]
	miR-1906	JAK2/STAT3	[22]
	miR-22	VEGF	[27]
与兴奋性毒性相关
	miR-1000	VGlut	[54]	miR-107	GLT-1	[54]
	miR-223	GluR2，NR2B	[54]
与细胞自噬相关
	miR-30	Beclin1	[54]	miR-124	PI3K	[54]
	miR-298	Act1	[54]
	miR-138	SIRT1	[54]
	miR-202-5p	eIF4E	[54]
与血脑屏障功能相关
	miR-539	MMP-9	[54]	miR-130a	—	[52]
	miR-21	MAP2K	[52] [54]	miR-150	—	[52]

	miR-429	Cxcll	[54]	miR-17	—	[52]
	miR-149-5p	SIPR2	[54]	miR-222	—	[52]
	miR-126	—	[52]	miR-378	—	[52]
	miR-150	—	[52]	miR-20a	—	[52]
				miR-19a/b	—	[52]
低氧（HIF-1）
	miR-613	ATG3轴	[21]	miR-373	—	[52]
	miR-26b	—	[29]	miR-24-1	—	[52]
				miR-181c	—	[52]
				miR-210	—	[52]
				miR-26a-2	—	[52]
				miR-23	—	[52]
				miR-24	—	[52]
				miR-103	—	[52]
				miR-107	—	[52]
其他
	miR-148b-3	—	[57]	miR-292-5p	—	[52]
	miR-488-3p	—	[53]	miR-290	—	[52]
				miR-206	—	[52]
				miR-215	—	[52]
				miR-214	—	[52]
				miR-223	—	[52]
				miR-298	—	[52]
				miR-327	—	[52]
				miR-494	Sox8	[52]
				miR-497	—	[52]
				miR-7674-5p	—	[57]

表2 在CIRI中miRs的影响

促CIRI发生发展	信号通路/轴	参考文献	改善CIRI预后	信号通路/轴	参考文献
miR-217	NF-κB	[13]	miR-579-3p	NF-κB	[14]
miR-22	PI3K/AKT/mTOR JAK/STAT3	[27]	miR-193b-3p	NF-κB	[15]
miR-10a	PI3K/Akt/mTOR	[19]	miR-429	NF-κB	[16]
miR-455-3p	TP53INP1轴	[34]	miR-26b-5p	NF-κB	[17]
miR-134	CREB/Nrf2	[39]	miR-1906	NF-κB	[18]
miR-148b-3p	Sestrin2/Nrf2/ARE轴	[40]	miR-182-5p	NF-κB	[18]
miR-302b3p	GSK-3β)/Nrf2/ARE轴	[41]	miR-372-3p	NF-κB	[18]
miR-199a-5p	Brg1)/Nrf2/HO-1轴	[42]	miR-26	PTEN轴	[19]
miR-10a	caspase-3活性和Bax	[19]	miRNA-26b-5p	PTEN轴	[20]
miR-224-3p	caspase-3	[54]	miR-216a	JAK2/STAT3	[22]
miR-155	caspase-3	[54]	miR-1906	JAK2/STAT3	[22]
miR-429	caspase-3	[54]	miR-26a	PI3K/Akt、MAPK/ERK	[19]
miR-10a	PI3K/Akt/ mTOR	[54]	miR-338-5p	AMPK/mTOR	[26]
miR-370	SIRT6	[54]	miR-375	p21/PI3K/Akt	[19]
miR-144	Nrf2/ARE轴	[54]	miR-124	PI3K/Akt/ mTOR	[29]
miR-142-5p	Nrf2/ARE轴	[54]	miR-128-3p	MAPK WNT1	[32][33]
miR-153	Nrf2/ARE轴	[54]	miR-30b	PI3K/Akt/eNOS	[44]
miR-93	Nrf2/ARE轴	[54]	miR-424	PI3K/Akt/eNOS	[44]
miR-217	SIRT1	[54]	miR-126	PI3K/Akt/eNOS	[29]
miR-135a	GSK-3β	[54]	miR-451a	靶向Rac1	[45]
miR-421	MCL1	[54]	miR-193b-3p	5-脂氧合酶	[15]
miR-224-3p	FIP200	[54]	miR-204-5p	NF-κB	[46]
miR-193b-3p	5-LOX	[54]	miR-579-3p	炎性细胞因子TNF-a	[14]
miR-19a-3p	IGFBP3	[54]	miR-193b-3p	抑制TGF-β活性	[15]
miR-155	MafB	[54]	miR-22-3p	caspase-3活性和Bax	[49]
				BMF/BMP2轴
miR-217	SIRT1	[54]	miR-579-3p	caspase-3活性和Bax	[14]
miR-107	GLT-1	[54]	miR-26a	caspase-3活性和Bax	[19]
miR-124	PI3K/Akt/eNOS	[54]	miR-488-3p	靶向VPS4B	[53]

表2 在CIRI中miRs的影响

促CIRI发生发展	信号通路/轴	参考文献	改善CIRI预后	信号通路/轴	参考文献
miR-217	NF-κB	[13]	miR-579-3p	NF-κB	[14]
miR-22	PI3K/AKT/mTOR JAK/STAT3	[27]	miR-193b-3p	NF-κB	[15]
miR-10a	PI3K/Akt/mTOR	[19]	miR-429	NF-κB	[16]
miR-455-3p	TP53INP1轴	[34]	miR-26b-5p	NF-κB	[17]
miR-134	CREB/Nrf2	[39]	miR-1906	NF-κB	[18]
miR-148b-3p	Sestrin2/Nrf2/ARE轴	[40]	miR-182-5p	NF-κB	[18]
miR-302b3p	GSK-3β)/Nrf2/ARE轴	[41]	miR-372-3p	NF-κB	[18]
miR-199a-5p	Brg1)/Nrf2/HO-1轴	[42]	miR-26	PTEN轴	[19]
miR-10a	caspase-3活性和Bax	[19]	miRNA-26b-5p	PTEN轴	[20]
miR-224-3p	caspase-3	[54]	miR-216a	JAK2/STAT3	[22]
miR-155	caspase-3	[54]	miR-1906	JAK2/STAT3	[22]
miR-429	caspase-3	[54]	miR-26a	PI3K/Akt、MAPK/ERK	[19]
miR-10a	PI3K/Akt/ mTOR	[54]	miR-338-5p	AMPK/mTOR	[26]
miR-370	SIRT6	[54]	miR-375	p21/PI3K/Akt	[19]
miR-144	Nrf2/ARE轴	[54]	miR-124	PI3K/Akt/ mTOR	[29]
miR-142-5p	Nrf2/ARE轴	[54]	miR-128-3p	MAPK WNT1	[32][33]
miR-153	Nrf2/ARE轴	[54]	miR-30b	PI3K/Akt/eNOS	[44]
miR-93	Nrf2/ARE轴	[54]	miR-424	PI3K/Akt/eNOS	[44]
miR-217	SIRT1	[54]	miR-126	PI3K/Akt/eNOS	[29]
miR-135a	GSK-3β	[54]	miR-451a	靶向Rac1	[45]
miR-421	MCL1	[54]	miR-193b-3p	5-脂氧合酶	[15]
miR-224-3p	FIP200	[54]	miR-204-5p	NF-κB	[46]
miR-193b-3p	5-LOX	[54]	miR-579-3p	炎性细胞因子TNF-a	[14]
miR-19a-3p	IGFBP3	[54]	miR-193b-3p	抑制TGF-β活性	[15]
miR-155	MafB	[54]	miR-22-3p	caspase-3活性和Bax	[49]
				BMF/BMP2轴
miR-217	SIRT1	[54]	miR-579-3p	caspase-3活性和Bax	[14]
miR-107	GLT-1	[54]	miR-26a	caspase-3活性和Bax	[19]
miR-124	PI3K/Akt/eNOS	[54]	miR-488-3p	靶向VPS4B	[53]

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Research status and progress of microRNA in cerebral ischemia-reperfusion injury

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Research status and progress of microRNA in cerebral ischemia-reperfusion injury