Exploration of Medicine

Table 1. A summary of the functions of autophagy-related circRNAs

circRNAs	Expression	Regulation targets and pathways	Influence on autophagy	Diseases	Refs
circCDYL	Up	circCDYL/miR-1275/ATG7/ULK1 axis	Enhancement	Breast cancer	[76]
circCUL2	Down	circCUL2/miR-142-3p/ROCK2 axis	Enhancement	Gastric cancer	[80]
circHIPK3	Down	circHIPK3/miR-124-3p/STAT3/PRKAA axis	Enhancement	Lung cancer	[81]
circHECTD1	Up	circHECTD1/miR-142/TIPARP axis	Enhancement	Cerebral ischemic stroke	[46]
circSHOC2	Up	circSHOC2/miR-7670-3p/SIRT1 axis	Suppression	Cerebral ischemic stroke	[75]
circ_002581	Up	circ_002581/miR-122/CPEB1 axis	Suppression	Nonalcoholic steatohepatitis	[82]

Return to article view

circCDYL: circular RNA CDYL; ULK1: UNC-51-like kinase 1; circCUL2: circular RNA CUL2; ROCK2: rho-associated coiled-coil-containing protein kinase-2; circHIPK3: circular RNA HIPK3; STAT3: signal transducer and activator of transcription 3; PRKAA: protein kinase AMP-activated catalytic subunit alpha 2; TIPARP: TCDD inducible poly[ADP-ribose] polymerase; circSHOC2: circular RNA SHOC2; SIRT1: sirtuin 1; CPEB1: cytoplasmic polyadenylation element-binding 1

Declarations

Author contributions

YH and LG: Investigation, Writing—original draft, Writing—review & editing. BH: Conceptualization, Validation, Writing—review & editing. HY: Conceptualization, Validation, Writing—review & editing, Supervision. All authors read and approved the submitted version.

Conflicts of interest

The authors declare that they have no conflicts of interest.

Ethical approval

Not applicable.

Consent to participate

Not applicable.

Consent to publication

Not applicable.

Availability of data and materials

Not applicable.

Funding

This work was supported by the Science and Technology innovation 2030-Major Project of the Ministry of Science and Technology of China [2021ZD0202904/2021ZD0202900], the National Natural Science Foundation of Distinguished Young Scholars [82025033], the National Natural Science Foundation of China [82230115, 82003733], the Natural Science Foundation of Jiangsu Province [BK20200358], the Fundamental Research Funds for the Central Universities [2242021R40023], the Jiangsu Provincial Doctors of Entrepreneurship and Innovation Program. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Copyright

References

Owolabi MO, Thrift AG, Mahal A, Ishida M, Martins S, Johnson WD, et al.; Stroke Experts Collaboration Group. Primary stroke prevention worldwide: translating evidence into action. Lancet Public Health. 2022;7:e74–85. [DOI] [PubMed] [PMC]

Du Y, Demillard LJ, Ren J. Catecholamine-induced cardiotoxicity: a critical element in the pathophysiology of stroke-induced heart injury. Life Sci. 2021;287:120106. [DOI] [PubMed]

GBD 2019 Stroke Collaborators. Global, regional, and national burden of stroke and its risk factors, 1990–2019: a systematic analysis for the Global Burden of Disease Study 2019. Lancet Neurol. 2021;20:795–820. [DOI] [PubMed] [PMC]

Campbell BCV, De Silva DA, Macleod MR, Coutts SB, Schwamm LH, Davis SM, et al. Ischaemic stroke. Nat Rev Dis Primers. 2019;5:70.

Wang P, Shao BZ, Deng Z, Chen S, Yue Z, Miao CY. Autophagy in ischemic stroke. Prog Neurobiol. 2018;163–164:98–117. [DOI] [PubMed]

Yang Z, Lin P, Chen B, Zhang X, Xiao W, Wu S, et al. Autophagy alleviates hypoxia-induced blood-brain barrier injury via regulation of CLDN5 (claudin 5). Autophagy. 2021;17:3048–67. [DOI] [PubMed] [PMC]

Kuang Y, Zheng X, Zhang L, Ai X, Venkataramani V, Kilic E, et al. Adipose-derived mesenchymal stem cells reduce autophagy in stroke mice by extracellular vesicle transfer of miR-25. J Extracell Vesicles. 2020;10:e12024. [DOI] [PubMed] [PMC]

Tuo QZ, Zhang ST, Lei P. Mechanisms of neuronal cell death in ischemic stroke and their therapeutic implications. Med Res Rev. 2022;42:259–305. [DOI] [PubMed]

Dikic I, Elazar Z. Mechanism and medical implications of mammalian autophagy. Nat Rev Mol Cell Biol. 2018;19:349–64. [DOI] [PubMed]

10.

Marsh T, Debnath J. Autophagy suppresses breast cancer metastasis by degrading NBR1. Autophagy. 2020;16:1164–5. [DOI] [PubMed] [PMC]

11.

Shi Q, Cheng Q, Chen C. The role of autophagy in the pathogenesis of ischemic stroke. Curr Neuropharmacol. 2021;19:629–40. [DOI] [PubMed] [PMC]

12.

Kalachev AV, Yurchenko OV. Microautophagy in nutritive phagocytes of sea urchins. Protoplasma. 2017;254:609–14. [DOI] [PubMed]

13.

Mizushima N, Levine B. Autophagy in human diseases. N Engl J Med. 2020;383:1564–76. [DOI] [PubMed] [PMC]

14.

Ajoolabady A, Wang S, Kroemer G, Penninger JM, Uversky VN, Pratico D, et al. Targeting autophagy in ischemic stroke: from molecular mechanisms to clinical therapeutics. Pharmacol Ther. 2021;225:107848. [DOI] [PubMed] [PMC]

15.

Guan R, Zou W, Dai X, Yu X, Liu H, Chen Q, et al. Mitophagy, a potential therapeutic target for stroke. J Biomed Sci. 2018;25:87. [DOI] [PubMed] [PMC]

16.

From the American Association of Neurological Surgeons (AANS); American Society of Neuroradiology (ASNR); Cardiovascular and Interventional Radiology Society of Europe (CIRSE); Canadian Interventional Radiology Association (CIRA); Congress of Neurological Surgeons (CNS); European Society of Minimally Invasive Neurological Therapy (ESMINT), et al.; Sacks D, Baxter B, Campbell BCV, Carpenter JS, Cognard C, Dippel D, et al. Multisociety consensus quality improvement revised consensus statement for endovascular therapy of acute ischemic stroke. Int J Stroke. 2018;13:612–32. [DOI] [PubMed] [PMC]

17.

Jeck WR, Sorrentino JA, Wang K, Slevin MK, Burd CE, Liu J, et al. Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA. 2013;19:141–57. [DOI] [PubMed] [PMC]

18.

Beermann J, Piccoli MT, Viereck J, Thum T. Non-coding RNAs in development and disease: background, mechanisms, and therapeutic approaches. Physiol Rev. 2016;96:1297–325. [DOI] [PubMed]

19.

Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, et al. Natural RNA circles function as efficient microRNA sponges. Nature. 2013;495:384–8. [DOI] [PubMed]

20.

Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature. 2013;495:333–8. [DOI] [PubMed]

21.

Legnini I, Di Timoteo G, Rossi F, Morlando M, Briganti F, Sthandier O, et al. Circ-ZNF609 is a circular RNA that can be translated and functions in myogenesis. Mol Cell. 2017;66:22–37.e9. [DOI] [PubMed] [PMC]

22.

Wang Y, Mo Y, Peng M, Zhang S, Gong Z, Yan Q, et al. The influence of circular RNAs on autophagy and disease progression. Autophagy. 2022;18:240–53. [DOI] [PubMed] [PMC]

23.

Menzies FM, Fleming A, Caricasole A, Bento CF, Andrews SP, Ashkenazi A, et al. Autophagy and neurodegeneration: pathogenic mechanisms and therapeutic opportunities. Neuron. 2017;93:1015–34. [DOI] [PubMed]

24.

Griffey CJ, Yamamoto A. Macroautophagy in CNS health and disease. Nat Rev Neurosci. 2022;23:411–27. [DOI] [PubMed] [PMC]

25.

Xia Y, Ling X, Hu G, Zhu Q, Zhang J, Li Q, et al. Small extracellular vesicles secreted by human iPSC-derived MSC enhance angiogenesis through inhibiting STAT3-dependent autophagy in ischemic stroke. Stem Cell Res Ther. 2020;11:313. [DOI] [PubMed] [PMC]

26.

Ahsan A, Liu M, Zheng Y, Yan W, Pan L, Li Y, et al. Natural compounds modulate the autophagy with potential implication of stroke. Acta Pharm Sin B. 2021;11:1708–20. [DOI] [PubMed] [PMC]

27.

Peker N, Gozuacik D. Autophagy as a cellular stress response mechanism in the nervous system. J Mol Biol. 2020;432:2560–88. [DOI] [PubMed]

28.

Lugovaya AV, Emanuel TS, Kalinina NM, Mitreikin VP, Artemova AV, Makienko AA. The role of autophagy in the regulation of neuroinflammation in acute ischemic stroke (review of literature). Klin Lab Diagn. 2022;67:391–8. [DOI] [PubMed]

29.

Das G, Shravage BV, Baehrecke EH. Regulation and function of autophagy during cell survival and cell death. Cold Spring Harb Perspect Biol. 2012;4:a008813. [DOI] [PubMed] [PMC]

30.

Shi R, Weng J, Zhao L, Li XM, Gao TM, Kong J. Excessive autophagy contributes to neuron death in cerebral ischemia. CNS Neurosci Ther. 2012;18:250–60. [DOI] [PubMed] [PMC]

31.

Puyal J, Ginet V, Grishchuk Y, Truttmann AC, Clarke PG. Neuronal autophagy as a mediator of life and death: contrasting roles in chronic neurodegenerative and acute neural disorders. Neuroscientist. 2012;18:224–36. [DOI] [PubMed]

32.

Wang Y, Han R, Liang ZQ, Wu JC, Zhang XD, Gu ZL, et al. An autophagic mechanism is involved in apoptotic death of rat striatal neurons induced by the non-N-methyl-D-aspartate receptor agonist kainic acid. Autophagy. 2008;4:214–26. [DOI] [PubMed]

33.

Wang Y, Dong XX, Cao Y, Liang ZQ, Han R, Wu JC, et al. p53 induction contributes to excitotoxic neuronal death in rat striatum through apoptotic and autophagic mechanisms. Eur J Neurosci. 2009;30:2258–70. [DOI] [PubMed]

34.

Galluzzi L, Bravo-San Pedro JM, Blomgren K, Kroemer G. Autophagy in acute brain injury. Nat Rev Neurosci. 2016;17:467–84. [DOI] [PubMed]

35.

Zhang X, Yan H, Yuan Y, Gao J, Shen Z, Cheng Y, et al. Cerebral ischemia-reperfusion-induced autophagy protects against neuronal injury by mitochondrial clearance. Autophagy. 2013;9:1321–33. [DOI] [PubMed]

36.

Yin Y, Sun G, Li E, Kiselyov K, Sun D. ER stress and impaired autophagy flux in neuronal degeneration and brain injury. Ageing Res Rev. 2017;34:3–14. [DOI] [PubMed] [PMC]

37.

Viscomi MT, D’Amelio M, Cavallucci V, Latini L, Bisicchia E, Nazio F, et al. Stimulation of autophagy by rapamycin protects neurons from remote degeneration after acute focal brain damage. Autophagy. 2012;8:222–35. [DOI] [PubMed]

38.

Wang L, Klionsky DJ, Shen HM. The emerging mechanisms and functions of microautophagy. Nat Rev Mol Cell Biol. 2023;24:186–203. [DOI] [PubMed]

39.

Bourdenx M, Martín-Segura A, Scrivo A, Rodriguez-Navarro JA, Kaushik S, Tasset I, et al. Chaperone-mediated autophagy prevents collapse of the neuronal metastable proteome. Cell. 2021;184:2696–714.e25. [DOI] [PubMed] [PMC]

40.

Yang QQ, Zhou JW. Neuroinflammation in the central nervous system: symphony of glial cells. Glia. 2019;67:1017–35. [DOI] [PubMed]

41.

Belgrad J, De Pace R, Fields RD. Autophagy in myelinating glia. J Neurosci. 2020;40:256–66. [DOI] [PubMed] [PMC]

42.

Ma YL, Zhang LX, Liu GL, Fan Y, Peng Y, Hou WG. N-myc downstream-regulated gene 2 (Ndrg2) is involved in ischemia-hypoxia-induced astrocyte apoptosis: a novel target for stroke therapy. Mol Neurobiol. 2017;54:3286–99. [DOI] [PubMed]

43.

Yamagata K. Astrocyte-induced synapse formation and ischemic stroke. J Neurosci Res. 2021;99:1401–13. [DOI] [PubMed]

44.

Wang JL, Xu CJ. Astrocytes autophagy in aging and neurodegenerative disorders. Biomed Pharmacother. 2020;122:109691. [DOI] [PubMed]

45.

Su PW, Zhai Z, Wang T, Zhang YN, Wang Y, Ma K, et al. Research progress on astrocyte autophagy in ischemic stroke. Front Neurol. 2022;13:951536. [DOI] [PubMed] [PMC]

46.

Han B, Zhang Y, Zhang Y, Bai Y, Chen X, Huang R, et al. Novel insight into circular RNA HECTD1 in astrocyte activation via autophagy by targeting MIR142-TIPARP: implications for cerebral ischemic stroke. Autophagy. 2018;14:1164–84. [DOI] [PubMed] [PMC]

47.

Kasprowska D, Machnik G, Kost A, Gabryel B. Time-dependent changes in apoptosis upon autophagy inhibition in astrocytes exposed to oxygen and glucose deprivation. Cell Mol Neurobiol. 2017;37:223–34. [DOI] [PubMed]

48.

Hou K, Li G, Yu J, Xu K, Wu W. Receptors, channel proteins, and enzymes involved in microglia-mediated neuroinflammation and treatments by targeting microglia in ischemic stroke. Neuroscience. 2021;460:167–80. [DOI] [PubMed]

49.

Yang Z, Zhong L, Zhong S, Xian R, Yuan B. Hypoxia induces microglia autophagy and neural inflammation injury in focal cerebral ischemia model. Exp Mol Pathol. 2015;98:219–24. [DOI] [PubMed]

50.

Xia CY, Zhang S, Chu SF, Wang ZZ, Song XY, Zuo W, et al. Autophagic flux regulates microglial phenotype according to the time of oxygen-glucose deprivation/reperfusion. Int Immunopharmacol. 2016;39:140–8. [DOI] [PubMed]

51.

Li Z, Song Y, He T, Wen R, Li Y, Chen T, et al. M2 microglial small extracellular vesicles reduce glial scar formation via the miR-124/STAT3 pathway after ischemic stroke in mice. Theranostics. 2021;11:1232–48. [DOI] [PubMed] [PMC]

52.

Koyama Y. Signaling molecules regulating phenotypic conversions of astrocytes and glial scar formation in damaged nerve tissues. Neurochem Int. 2014;78:35–42. [DOI] [PubMed]

53.

Wu S, Yin Y, Du L. FUS aggregation following ischemic stroke favors brain astrocyte activation through inducing excessive autophagy. Exp Neurol. 2022;355:114144. [DOI] [PubMed]

54.

Alizadeh J, Kochan MM, Stewart VD, Drewnik DA, Hannila SS, Ghavami S. Inhibition of autophagy flux promotes secretion of chondroitin sulfate proteoglycans in primary rat astrocytes. Mol Neurobiol. 2021;58:6077–91. [DOI] [PubMed]

55.

Dewar D, Underhill SM, Goldberg MP. Oligodendrocytes and ischemic brain injury. J Cereb Blood Flow Metab. 2003;23:263–74. [DOI] [PubMed]

56.

Guardia Clausi M, Paez PM, Campagnoni AT, Pasquini LA, Pasquini JM. Intranasal administration of aTf protects and repairs the neonatal white matter after a cerebral hypoxic-ischemic event. Glia. 2012;60:1540–54. [DOI] [PubMed]

57.

Kim KA, Shin D, Kim JH, Shin YJ, Rajanikant GK, Majid A, et al. Role of autophagy in endothelial damage and blood-brain barrier disruption in ischemic stroke. Stroke. 2018;49:1571–9. [DOI] [PubMed]

58.

Abbott NJ, Rönnbäck L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci. 2006;7:41–53. [DOI] [PubMed]

59.

Xu H, Zhang Y, Ren J. ALDH2 and stroke: a systematic review of the evidence. Adv Exp Med Biol. 2019;1193:195–210. [DOI] [PubMed]

60.

Sandoval KE, Witt KA. Blood-brain barrier tight junction permeability and ischemic stroke. Neurobiol Dis. 2008;32:200–19. [DOI]

61.

Li Z, Li J, Tang N. Long noncoding RNA Malat1 is a potent autophagy inducer protecting brain microvascular endothelial cells against oxygen-glucose deprivation/reoxygenation-induced injury by sponging miR-26b and upregulating ULK2 expression. Neuroscience. 2017;354:1–10. [DOI] [PubMed]

62.

Jin Z, Wu J, Yan LJ. Chemical conditioning as an approach to ischemic stroke tolerance: mitochondria as the target. Int J Mol Sci. 2016;17:351. [DOI] [PubMed] [PMC]

63.

Redmann M, Dodson M, Boyer-Guittaut M, Darley-Usmar V, Zhang J. Mitophagy mechanisms and role in human diseases. Int J Biochem Cell Biol. 2014;53:127–33. [DOI] [PubMed] [PMC]

64.

Yang YD, Li ZX, Hu XM, Wan H, Zhang Q, Xiao R, et al. Insight into crosstalk between mitophagy and apoptosis/necroptosis: mechanisms and clinical applications in ischemic stroke. Curr Med Sci. 2022;42:237–48. [DOI] [PubMed]

65.

Roos V, Gunnarsson L, Fick J, Larsson DG, Rudén C. Prioritising pharmaceuticals for environmental risk assessment: towards adequate and feasible first-tier selection. Sci Total Environ. 2012;421–422:102–10. [DOI] [PubMed]

66.

Sundaram K, Mather AR, Marimuthu S, Shah PP, Snider AJ, Obeid LM, et al. Loss of neutral ceramidase protects cells from nutrient- and energy -deprivation-induced cell death. Biochem J. 2016;473:743–55. [DOI] [PubMed] [PMC]

67.

Farre JC, Manjithaya R, Mathewson RD, Subramani S. PpAtg30 tags peroxisomes for turnover by selective autophagy. Dev Cell. 2008;14:365–76. [DOI] [PubMed] [PMC]

68.

Kraft C, Deplazes A, Sohrmann M, Peter M. Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nat Cell Biol. 2008;10:602–10. [DOI] [PubMed]

69.

Jiang T, Yu JT, Zhu XC, Zhang QQ, Tan MS, Cao L, et al. Ischemic preconditioning provides neuroprotection by induction of AMP-activated protein kinase-dependent autophagy in a rat model of ischemic stroke. Mol Neurobiol. 2015;51:220–9. [DOI] [PubMed]

70.

Guo QQ, Wang SS, Zhang SS, Xu HD, Li XM, Guan Y, et al. ATM-CHK2-Beclin 1 axis promotes autophagy to maintain ROS homeostasis under oxidative stress. EMBO J. 2020;39:e103111. [DOI] [PubMed] [PMC]

71.

Xu W, Xiao P, Fan S, Chen Y, Huang W, Chen X, et al. Blockade of Nogo-A/Nogo-66 receptor 1 (NgR1) inhibits autophagic activation and prevents secondary neuronal damage in the thalamus after focal cerebral infarction in hypertensive rats. Neuroscience. 2020;431:103–14. [DOI] [PubMed]

72.

Zhou LY, Zhai M, Huang Y, Xu S, An T, Wang YH, et al. The circular RNA ACR attenuates myocardial ischemia/reperfusion injury by suppressing autophagy via modulation of the Pink1/ FAM65B pathway. Cell Death Differ. 2019;26:1299–315. [DOI] [PubMed] [PMC]

73.

Mehta SL, Dempsey RJ, Vemuganti R. Role of circular RNAs in brain development and CNS diseases. Prog Neurobiol. 2020;186:101746. [DOI] [PubMed] [PMC]

74.

Zhang J, Wang P, Wan L, Xu S, Pang D. The emergence of noncoding RNAs as Heracles in autophagy. Autophagy. 2017;13:1004–24. [DOI] [PubMed] [PMC]

75.

Chen W, Wang H, Zhu Z, Feng J, Chen L. Exosome-shuttled circSHOC2 from IPASs regulates neuronal autophagy and ameliorates ischemic brain injury via the miR-7670-3p/SIRT1 axis. Mol Ther Nucleic Acids. 2020;22:657–72. [DOI] [PubMed] [PMC]

76.

Liang G, Ling Y, Mehrpour M, Saw PE, Liu Z, Tan W, et al. Autophagy-associated circRNA circCDYL augments autophagy and promotes breast cancer progression. Mol Cancer. 2020;19:65. [DOI] [PubMed] [PMC]

77.

Yuan X, Li Y, Wen S, Xu C, Wang C, He Y, et al. CircLDLR acts as a sponge for miR-667-5p to regulate SIRT1 expression in non-alcoholic fatty liver disease. Lipids Health Dis. 2022;21:127. [DOI] [PubMed] [PMC]

78.

He Z, Cai K, Zeng Z, Lei S, Cao W, Li X. Autophagy-associated circRNA circATG7 facilitates autophagy and promotes pancreatic cancer progression. Cell Death Dis. 2022;13:233. [DOI] [PubMed] [PMC]

79.

Yang Z, Huang C, Wen X, Liu W, Huang X, Li Y, et al. Circular RNA circ-FoxO3 attenuates blood-brain barrier damage by inducing autophagy during ischemia/reperfusion. Mol Ther. 2022;30:1275–87. [DOI] [PubMed] [PMC]

80.

Peng L, Sang H, Wei S, Li Y, Jin D, Zhu X, et al. CircCUL2 regulates gastric cancer malignant transformation and cisplatin resistance by modulating autophagy activation via miR-142-3p/ROCK2. Mol Cancer. 2020;19:156. [DOI] [PubMed] [PMC]

81.

Chen X, Mao R, Su W, Yang X, Geng Q, Guo C, et al. Circular RNA circHIPK3 modulates autophagy via MIR124-3p-STAT3-PRKAA/AMPK α signaling in STK11 mutant lung cancer. Autophagy. 2020;16:659–71. [DOI] [PubMed] [PMC]

82.

Jin X, Gao J, Zheng R, Yu M, Ren Y, Yan T, et al. Antagonizing circRNA_002581-miR-122-CPEB1 axis alleviates NASH through restoring PTEN-AMPK-mTOR pathway regulated autophagy. Cell Death Dis. 2020;11:123. [DOI] [PubMed] [PMC]

83.

Chen M, Lai X, Wang X, Ying J, Zhang L, Zhou B, et al. Long non-coding RNAs and circular RNAs: insights into microglia and astrocyte mediated neurological diseases. Front Mol Neurosci. 2021;14:745066. [DOI] [PubMed] [PMC]

84.

Bazan HA, Hatfield SA, Brug A, Brooks AJ, Lightell DJ Jr, Woods TC. Carotid plaque rupture is accompanied by an increase in the ratio of serum circR-284 to miR-221 levels. Circ Cardiovasc Genet. 2017;10:e001720. [DOI] [PubMed] [PMC]

85.

Ostolaza A, Blanco-Luquin I, Urdánoz-Casado A, Rubio I, Labarga A, Zandio B, et al. Circular RNA expression profile in blood according to ischemic stroke etiology. Cell Biosci. 2020;10:34. [DOI] [PubMed] [PMC]

86.

Zu J, Zuo L, Zhang L, Wang Z, Shi Y, Gu L, et al. Circular RNA FUNDC1 for prediction of acute phase outcome and long-term survival of acute ischemic stroke. Front Neurol. 2022;13:846198. [DOI] [PubMed] [PMC]

87.

Yang L, Han B, Zhang Z, Wang S, Bai Y, Zhang Y, et al. Extracellular vesicle-mediated delivery of circular RNA SCMH1 promotes functional recovery in rodent and nonhuman primate ischemic stroke models. Circulation. 2020;142:556–74. [DOI] [PubMed]

88.

Chen W, Wang H, Feng J, Chen L. Overexpression of circRNA circUCK2 attenuates cell apoptosis in cerebral ischemia-reperfusion injury via miR-125b-5p/GDF11 signaling. Mol Ther Nucleic Acids. 2020;22:673–83. [DOI] [PubMed] [PMC]

89.

Liu Y, Li Y, Zang J, Zhang T, Li Y, Tan Z, et al. CircOGDH is a penumbra biomarker and therapeutic target in acute ischemic stroke. Circ Res. 2022;130:907–24. [DOI] [PubMed]

90.

Zuo L, Xie J, Liu Y, Leng S, Zhang Z, Yan F. Down-regulation of circular RNA CDC14A peripherally ameliorates brain injury in acute phase of ischemic stroke. J Neuroinflammation. 2021;18:283. [DOI] [PubMed] [PMC]

91.

Wu F, Han B, Wu S, Yang L, Leng S, Li M, et al. Circular RNA TLK1 aggravates neuronal injury and neurological deficits after ischemic stroke via miR-335-3p/TIPARP. J Neurosci. 2019;39:7369–93. [DOI] [PubMed] [PMC]

92.

Bai Y, Zhang Y, Han B, Yang L, Chen X, Huang R, et al. Circular RNA DLGAP4 ameliorates ischemic stroke outcomes by targeting miR-143 to regulate endothelial-mesenchymal transition associated with blood-brain barrier integrity. J Neurosci. 2018;38:32–50. [DOI] [PubMed] [PMC]

93.

Tang C, Ou J, Kou L, Deng J, Luo S. Circ_016719 plays a critical role in neuron cell apoptosis induced by I/R via targeting miR-29c/Map2k6. Mol Cell Probes. 2020;49:101478. [DOI] [PubMed]

94.

Xu L, Ji H, Jiang Y, Cai L, Lai X, Wu F, et al. Exosomes derived from circAkap7-modified adipose-derived mesenchymal stem cells protect against cerebral ischemic injury. Front Cell Dev Biol. 2020;8:569977. [DOI] [PubMed] [PMC]

95.

Zhou D, Huang Z, Zhu X, Hong T, Zhao Y. Circular RNA 0025984 ameliorates ischemic stroke injury and protects astrocytes through miR-143-3p/TET1/ORP150 pathway. Mol Neurobiol. 2021;58:5937–53. [DOI] [PubMed]