Non-coding RNAs: the extensive and interactive regulators of the blood-brain barrier permeability

References

• Abbott NJ, Patabendige AAK, Dolman DEM, et al. Structure and function of the blood–brain barrier. Neurobiol Dis. 2010;37(1):13–25.
   PubMed Web of Science ®Google Scholar
• Burkhart A, Thomsen LB, Thomsen MS, et al. Transfection of brain capillary endothelial cells in primary culture with defined blood–brain barrier properties. Fluids and Barriers of the CNS. 2015;12(1):19. .
   PubMedGoogle Scholar
• Ballabh P, Braun A, Nedergaard M. The blood–brain barrier: an overview. Neurobiol Dis. 2004;16(1):1–13.
   PubMed Web of Science ®Google Scholar
• Gonzalez-Mariscal L, Betanzos A, Nava P, et al. Tight junction proteins. Prog Biophys Mol Biol. 2003;81:1–44.
   PubMed Web of Science ®Google Scholar
• Candelario-Jalil E, Yang Y, Rosenberg GA. Diverse roles of matrix metalloproteinases and tissue inhibitors of metalloproteinases in neuroinflammation and cerebral ischemia. Neuroscience. 2009;158:983–994.
   PubMed Web of Science ®Google Scholar
• Greenwood J. Mechanisms of blood-brain barrier breakdown. Neuroradiology. 1991;33:95–100.
   PubMed Web of Science ®Google Scholar
• Yang R, Liu W, Miao L, et al. Induction of VEGFA and Snail-1 by meningitic Escherichia coli mediates disruption of the blood-brain barrier. Oncotarget. 2016;7:63839–63855.
   PubMedGoogle Scholar
• Yang RC, Qu XY, Xiao SY, et al. Meningitic Escherichia coli-induced upregulation of PDGF-B and ICAM-1 aggravates blood-brain barrier disruption and neuroinflammatory response. J Neuroinflammation. 2019;16:101.
   PubMed Web of Science ®Google Scholar
• Pan YB, Sun ZL, Feng DF. The role of microRNA in traumatic brain injury. Neuroscience. 2017;367:189–199.
   PubMed Web of Science ®Google Scholar
• Sargento-Freitas J, Aday S, Nunes C, et al. Endothelial progenitor cells enhance blood–brain barrier permeability in subacute stroke. Neurology. 2018;90(2):e127–e34. .
   PubMed Web of Science ®Google Scholar
• Schonrock N, Harvey RP, Mattick JS. Long Noncoding RNAs in cardiac development and pathophysiology. Circ Res. 2012;111(10):1349–1362.
   PubMed Web of Science ®Google Scholar
• Clark MB, Amaral PP, Schlesinger FJ, et al. The reality of pervasive transcription. PLoS Biol. 2011;9(7):e1000625. discussion e1102. .
   PubMed Web of Science ®Google Scholar
• Wilusz JE, Sunwoo H, Spector DL. Long noncoding RNAs: functional surprises from the RNA world. Genes Dev. 2009;23(13):1494–1504.
   PubMed Web of Science ®Google Scholar
• Sun P, Liu DZ, Jickling GC, et al. MicroRNA-based therapeutics in central nervous system injuries. J Cereb Blood Flow Metab. 2018;38(7):1125–1148.
   PubMed Web of Science ®Google Scholar
• Roberts TC, Morris KV, Wood MJ. The role of long non-coding RNAs in neurodevelopment, brain function and neurological disease. Philos Trans R Soc Lond B Biol Sci. 2014;369(1652):20130507.
   Web of Science ®Google Scholar
• Jeck WR, Sharpless NE. Detecting and characterizing circular RNAs. Nat Biotechnol. 2014;32(5):453–461.
   PubMed Web of Science ®Google Scholar
• Djebali S, Davis CA, Merkel A, et al. Landscape of transcription in human cells. Nature. 2012;489(7414):101–108. .
   PubMed Web of Science ®Google Scholar
• Zhang L, Wang H. Long non-coding RNA in CNS injuries: a new target for therapeutic intervention. Mol Ther Nucleic Acids. 2019;17:754–766.
   PubMedGoogle Scholar
• Taft RJ, Pang KC, Mercer TR, et al. Non-coding RNAs: regulators of disease. J Pathol. 2010;220:126–139.
   PubMed Web of Science ®Google Scholar
• Qureshi IA, Mehler MF. Emerging roles of non-coding RNAs in brain evolution, development, plasticity and disease. Nat Rev Neurosci. 2012;13(8):528–541.
   PubMed Web of Science ®Google Scholar
• Hafner M, Landthaler M, Burger L, et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell. 2010;141(1):129–141. .
   PubMed Web of Science ®Google Scholar
• Strub GM, Perkins JA. MicroRNAs for the pediatric otolaryngologist. Int J Pediatr Otorhinolaryngol. 2018;112:195–207.
   PubMed Web of Science ®Google Scholar
• Igaz P, Igaz I, Nagy Z, et al. MicroRNAs in adrenal tumors: relevance for pathogenesis, diagnosis, and therapy. Cell Mol Life Sci. 2015;72(3):417–428. .
   PubMed Web of Science ®Google Scholar
• Wienholds E, Plasterk RHA. MicroRNA function in animal development. FEBS Letters. 2005;579(26):5911–5922.
   PubMed Web of Science ®Google Scholar
• Reijerkerk A, Lopez-Ramirez MA, van Het Hof B, et al. MicroRNAs regulate human brain endothelial cell-barrier function in inflammation: implications for multiple sclerosis. J Neurosci. 2013;33(16):6857–6863. .
   PubMed Web of Science ®Google Scholar
• Yang Y, Estrada EY, Thompson JF, et al. Matrix metalloproteinase-mediated disruption of tight junction proteins in cerebral vessels is reversed by synthetic matrix metalloproteinase inhibitor in focal ischemia in rat. J Cereb Blood Flow Metab. 2007;27(4):697–709.
   PubMed Web of Science ®Google Scholar
• Zuo X, Lu J, Manaenko A, et al. MicroRNA-132 attenuates cerebral injury by protecting blood-brain-barrier in MCAO mice. Exp Neurol. 2019;316:12–19.
   PubMed Web of Science ®Google Scholar
• Fan F, Yang J, Xu Y, et al. MiR-539 targets MMP-9 to regulate the permeability of blood–brain barrier in ischemia/reperfusion injury of brain. Neurochem Res. 2018;43(12):2260–2267.
   PubMed Web of Science ®Google Scholar
• Yao X, Wang Y, Zhang D. microRNA-21 Confers Neuroprotection against cerebral ischemia-reperfusion injury and alleviates blood-brain barrier disruption in rats via the MAPK signaling pathway. J Mol Neurosci. 2018;65(1):43–53.
   PubMed Web of Science ®Google Scholar
• Ren X, Engler-Chiurazzi EB, Russell AE, et al. MiR-34a and stroke: assessment of non-modifiable biological risk factors in cerebral ischemia. Neurochem Int. 2019;127:73–79.
   PubMed Web of Science ®Google Scholar
• Bukeirat M, Sarkar SN, Hu H, et al. MiR-34a regulates blood-brain barrier permeability and mitochondrial function by targeting cytochrome c. J Cereb Blood Flow Metab. 2016;36:387–392.
   PubMed Web of Science ®Google Scholar
• Hu H, Hone EA, Provencher EAP, et al. MiR-34a interacts with cytochrome c and shapes stroke outcomes. Sci Rep. 2020;10:3233.
   PubMed Web of Science ®Google Scholar
• Ma Q, Dasgupta C, Li Y, et al. MicroRNA-210 suppresses junction proteins and disrupts blood-brain barrier integrity in neonatal rat hypoxic-ischemic brain injury. Int J Mol Sci. 2017;18:1356.
   PubMed Web of Science ®Google Scholar
• Pena-Philippides JC, Gardiner AS, Caballero-Garrido E, et al. Inhibition of microRNA-155 supports endothelial tight junction integrity following oxygen-glucose deprivation. J Am Heart Assoc. 2018;7:e009244.
   PubMed Web of Science ®Google Scholar
• Awad H, Bratasz A, Nuovo G, et al. MiR-155 deletion reduces ischemia-induced paralysis in an aortic aneurysm repair mouse model: utility of immunohistochemistry and histopathology in understanding etiology of spinal cord paralysis. Ann Diagn Pathol. 2018;36:12–20.
   PubMed Web of Science ®Google Scholar
• Zhang T, Tian C, Wu J, et al. MicroRNA-182 exacerbates blood-brain barrier (BBB) disruption by downregulating the mTOR/FOXO1 pathway in cerebral ischemia. FASEB J. 2020;34:13762–13775.
   PubMed Web of Science ®Google Scholar
• Wang Y, Wang MD, Xia YP, et al. MicroRNA-130a regulates cerebral ischemia-induced blood-brain barrier permeability by targeting Homeobox A5. FASEB J. 2018;32:935–944.
   PubMed Web of Science ®Google Scholar
• Fang Z, He QW, Li Q, et al. MicroRNA-150 regulates blood-brain barrier permeability via Tie-2 after permanent middle cerebral artery occlusion in rats. FASEB J. 2016;30:2097–2107.
   PubMed Web of Science ®Google Scholar
• Ma F, Sun P, Zhang X, et al. Endothelium-targeted deletion of the miR-15a/16-1 cluster ameliorates blood-brain barrier dysfunction in ischemic stroke. Sci Signal. 2020;13:eaay5686.
   PubMed Web of Science ®Google Scholar
• Xi T, Jin F, Zhu Y, et al. MicroRNA-126-3p attenuates blood-brain barrier disruption, cerebral edema and neuronal injury following intracerebral hemorrhage by regulating PIK3R2 and Akt. Biochem Biophys Res Commun. 2017;494:144–151.
   PubMed Web of Science ®Google Scholar
• Xi T, Jin F, Zhu Y, et al. MiR-27a-3p protects against blood-brain barrier disruption and brain injury after intracerebral hemorrhage by targeting endothelial aquaporin-11. J Biol Chem. 2018;293:20041–20050.
   PubMed Web of Science ®Google Scholar
• Burek M, Konig A, Lang M, et al. Hypoxia-induced microRNA-212/132 alter blood-brain barrier integrity through inhibition of tight junction-associated proteins in human and mouse brain microvascular endothelial cells. Transl Stroke Res. 2019;10:672–683.
   PubMed Web of Science ®Google Scholar
• Ge X, Han Z, Chen F, et al. MiR-21 alleviates secondary blood-brain barrier damage after traumatic brain injury in rats. Brain Res. 2015;1603:150–157.
   PubMed Web of Science ®Google Scholar
• Aung LL, Mouradian MM, Dhib-Jalbut S, et al. MMP-9 expression is increased in B lymphocytes during multiple sclerosis exacerbation and is regulated by microRNA-320a. J Neuroimmunol. 2015;278:185–189.
   PubMed Web of Science ®Google Scholar
• Lopez-Ramirez MA, Wu D, Pryce G, Simpson JE, Reijerkerk A, King-Robson J, et al. MicroRNA-155 negatively affects blood-brain barrier function during neuroinflammation. FASEB J. 2014;28:2551–2565.
   PubMed Web of Science ®Google Scholar
• Rom S, Dykstra H, Zuluaga-Ramirez V, et al. MiR-98 and let-7g* protect the blood-brain barrier under neuroinflammatory conditions. J Cereb Blood Flow Metab. 2015;35:1957–1965.
   PubMed Web of Science ®Google Scholar
• Bernstein DL, Rom S. Let-7g* and miR-98 reduce stroke-induced production of proinflammatory cytokines in mouse brain. Front Cell Dev Biol. 2020;8:632.
   PubMed Web of Science ®Google Scholar
• Song J, Hu Y, Li H, et al. MiR-1303 regulates BBB permeability and promotes CNS lesions following CA16 infections by directly targeting MMP9. Emerg Microbes Infect. 2018;7:155.
   PubMed Web of Science ®Google Scholar
• Mishra R, Singh SK. HIV-1 Tat C modulates expression of miRNA-101 to suppress VE-cadherin in human brain microvascular endothelial cells. J Neurosci. 2013;33:5992–6000.
   PubMed Web of Science ®Google Scholar
• Barker KR, Lu Z, Kim H, et al. MiR-155 modifies inflammation, endothelial activation and blood-brain barrier dysfunction in cerebral malaria. Mol Med. 2017;23:24–33.
   PubMed Web of Science ®Google Scholar
• Liu W, Cai H, Lin M, et al. MicroRNA-107 prevents amyloid-beta induced blood-brain barrier disruption and endothelial cell dysfunction by targeting Endophilin-1. Exp Cell Res. 2016;343:248–257.
   PubMed Web of Science ®Google Scholar
• Lin M, Zhu L, Wang J, et al. MiR-424-5p maybe regulate blood-brain barrier permeability in a model in vitro with Abeta incubated endothelial cells. Biochem Biophys Res Commun. 2019;517:525–531.
   PubMed Web of Science ®Google Scholar
• Toyama K, Spin JM, Deng AC, et al. MicroRNA-mediated therapy modulating blood-brain barrier disruption improves vascular cognitive impairment. Arterioscler Thromb Vasc Biol. 2018;38:1392–1406.
   PubMed Web of Science ®Google Scholar
• Song J, Yoon SR, Kim OY. MiR-Let7a controls the cell death and tight junction density of brain endothelial cells under high glucose condition. Oxid Med Cell Longev. 2017;2017:6051874.
   PubMed Web of Science ®Google Scholar
• Yang MC, You FL, Wang Z, et al. Salvianolic acid B improves the disruption of high glucose-mediated brain microvascular endothelial cells via the ROS/HIF-1alpha/VEGF and miR-200b/VEGF signaling pathways. Neurosci Lett. 2016;630:233–240.
   PubMed Web of Science ®Google Scholar
• Kalani A, Kamat PK, Familtseva A, et al. Role of microRNA29b in blood-brain barrier dysfunction during hyperhomocysteinemia: an epigenetic mechanism. J Cereb Blood Flow Metab. 2014;34:1212–1222.
   PubMed Web of Science ®Google Scholar
• Bai Y, Zhang Y, Hua J, et al. Silencing microRNA-143 protects the integrity of the blood-brain barrier: implications for methamphetamine abuse. Sci Rep. 2016;6:35642.
   PubMed Web of Science ®Google Scholar
• Tominaga N, Kosaka N, Ono M, et al. Brain metastatic cancer cells release microRNA-181c-containing extracellular vesicles capable of destructing blood-brain barrier. Nat Commun. 2015;6:6716.
   PubMed Web of Science ®Google Scholar
• Chen SP, Chang YA, Chou CH, et al. Circulating microRNAs associated with reversible cerebral vasoconstriction syndrome. Ann Neurol. 2021;89:459–473.
   PubMed Web of Science ®Google Scholar
• Yang R, Huang F, Fu J, et al. Differential transcription profiles of long non-coding RNAs in primary human brain microvascular endothelial cells in response to meningitic Escherichia coli. Sci Rep. 2016;6:38903.
   PubMed Web of Science ®Google Scholar
• Vemuganti R. All’s well that transcribes well: non-coding RNAs and post-stroke brain damage. Neurochem Int. 2013;63:438–449.
   PubMed Web of Science ®Google Scholar
• Iyer MK, Niknafs YS, Malik R, et al. The landscape of long non-coding RNAs in the human transcriptome. Nat Genet. 2015;47:199–208.
   PubMed Web of Science ®Google Scholar
• Yao RW, Wang Y, Chen LL. Cellular functions of long non-coding RNAs. Nat Cell Biol. 2019;21:542–551.
   PubMed Web of Science ®Google Scholar
• Rinn JL, Chang HY. Genome regulation by long non-coding RNAs. Annu Rev Biochem. 2012;81:145–166.
   PubMed Web of Science ®Google Scholar
• Anfossi S, Babayan A, Pantel K, et al. Clinical utility of circulating non-coding RNAs-an update. Nat Rev Clin Oncol. 2018;15:541–563.
   PubMed Web of Science ®Google Scholar
• Peng H, Li H. The encouraging role of long non-coding RNA small nuclear RNA host gene 16 in epithelial-mesenchymal transition of bladder cancer via directly acting on miR-17-5p/metalloproteinases 3 axis. Mol Carcinog. 2019;58:1465–1480.
   PubMed Web of Science ®Google Scholar
• Yin KJ, Hamblin M, Chen YE. Non-coding RNAs in cerebral endothelial pathophysiology: emerging roles in stroke. Neurochem Int. 2014;77:9–16.
   PubMed Web of Science ®Google Scholar
• Li K, Blum Y, Verma A, et al. A non-coding antisense RNA in tie-1 locus regulates tie-1 function in vivo. Blood. 2010;115:133–139.
   PubMed Web of Science ®Google Scholar
• Zhou W, Chen C, Shi Y, et al. Targeting glioma stem cell-derived pericytes disrupts the blood-tumor barrier and improves chemotherapeutic efficacy. Cell Stem Cell. 2017;21:591–603 e4.
   PubMed Web of Science ®Google Scholar
• Sun Y, Ma L. New insights into long non-coding RNA MALAT1 in cancer and metastasis. Cancers (Basel). 2019;11:216.
   PubMed Web of Science ®Google Scholar
• Ma J, Wang P, Yao Y, et al. Knockdown of long non-coding RNA MALAT1 increases the blood-tumor barrier permeability by up-regulating miR-140. Biochim Biophys Acta. 2016;1859:324–338.
   PubMed Web of Science ®Google Scholar
• Naganuma T, Hirose T. Paraspeckle formation during the biogenesis of long non-coding RNAs. RNA Biol. 2013;10:456–461.
   PubMed Web of Science ®Google Scholar
• Guo J, Cai H, Zheng J, et al. Long non-coding RNA NEAT1 regulates permeability of the blood-tumor barrier via miR-181d-5p-mediated expression changes in ZO-1, Occludin, and claudin-5. Biochim Biophys Acta Mol Basis Dis. 2017;1863:2240–2254.
   PubMed Web of Science ®Google Scholar
• Guo J, Shen S, Liu X, et al. Role of linc00174/miR-138-5p (miR-150-5p)/FOSL2 feedback loop on regulating the blood-tumor barrier permeability. Mol Ther Nucleic Acids. 2019;18:1072–1090.
   PubMedGoogle Scholar
• Young TL, Matsuda T, Cepko CL. The non-coding RNA taurine up-regulated gene 1 is required for differentiation of the murine retina. Curr Biol. 2005;15:501–512.
   PubMed Web of Science ®Google Scholar
• Cai H, Xue Y, Wang P, et al. The long non-coding RNA TUG1 regulates blood-tumor barrier permeability by targeting miR-144. Oncotarget. 2015;6:19759–19779.
   PubMedGoogle Scholar
• Ma SC, Li Q, Peng JY, et al. CLDN5 affects lncRNAs acting as ceRNA dynamics contributing to regulating blood brain barrier permeability in tumor brain metastasis. Oncol Rep. 2018;39:1441–1453.
   PubMed Web of Science ®Google Scholar
• Zhu L, Lin M, Ma J, et al. The role of LINC00094/miR-224-5p (miR-497-5p)/Endophilin-1 axis in memantine mediated protective effects on blood-brain barrier in AD microenvironment. J Cell Mol Med. 2019;23:3280–3292.
   PubMed Web of Science ®Google Scholar
• Leng X, Ma J, Liu Y, et al. Mechanism of piR-DQ590027/MIR17HG regulating the permeability of glioma conditioned normal BBB. J Exp Clin Cancer Res. 2018;37:246.
   PubMed Web of Science ®Google Scholar
• Zhang J, Dong B, Hao J, et al. LncRNA Snhg3 contributes to dysfunction of cerebral microvascular cells in intracerebral hemorrhage rats by activating the TWEAK/Fn14/STAT3 pathway. Life Sci. 2019;237:116929.
   PubMed Web of Science ®Google Scholar
• Zhang ZG, Zhang L, Jiang Q, et al. VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain. J Clin Invest. 2000;106:829–838.
   PubMed Web of Science ®Google Scholar
• Ren L, Wei C, Li K, et al. LncRNA MALAT1 up-regulates VEGF-A and ANGPT2 to promote angiogenesis in brain microvascular endothelial cells against oxygen-glucose deprivation via targetting miR-145. Biosci Rep. 2019;39:BSR20180226.
   PubMed Web of Science ®Google Scholar
• Zhang L, Luo X, Chen F, et al. LncRNA SNHG1 regulates cerebrovascular pathologies as a competing endogenous RNA through HIF-1alpha/VEGF signaling in ischemic stroke. J Cell Biochem. 2018;119:5460–5472.
   PubMed Web of Science ®Google Scholar
• Wang Z, Wang R, Wang K, et al. Up-regulated long non-coding RNA Snhg1 promotes the angiogenesis of brain microvascular endothelial cells after oxygen-glucose deprivation treatment by targeting miR-199a. Can J Physiol Pharmacol. 2018;96:909–915.
   PubMed Web of Science ®Google Scholar
• Wu L, Ye Z, Pan Y, et al. Vascular endothelial growth factor aggravates cerebral ischemia and reperfusion-induced blood-brain-barrier disruption through regulating LOC102640519/HOXC13/ZO-1 signaling. Exp Cell Res. 2018;369:275–283.
   PubMed Web of Science ®Google Scholar
• Chen LL. The biogenesis and emerging roles of circular RNAs. Nat Rev Mol Cell Biol. 2016;17:205–211.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Liang W, Zhang P, et al. Circular RNAs: emerging cancer biomarkers and targets. J Exp Clin Cancer Res. 2017;36:152.
   PubMed Web of Science ®Google Scholar
• Salzman J. Circular RNA expression: its potential regulation and function. Trends Genet. 2016;32:309–316.
   PubMed Web of Science ®Google Scholar
• Salzman J, Gawad C, Wang PL, et al. Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PloS One. 2012;7:e30733.
   PubMed Web of Science ®Google Scholar
• Memczak S, Jens M, Elefsinioti A, et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature. 2013;495:333–338.
   PubMed Web of Science ®Google Scholar
• Ashwal-Fluss R, Meyer M, Pamudurti NR, et al. CircRNA biogenesis competes with pre-mRNA splicing. Mol Cell. 2014;56:55–66.
   PubMed Web of Science ®Google Scholar
• Filippenkov IB, Kalinichenko EO, Limborska SA, et al. Circular RNAs-one of the enigmas of the brain. Neurogenetics. 2017;18:1–6.
   PubMed Web of Science ®Google Scholar
• Gao Y, Ma H, Lv C, et al. Exosomes and exosomal microRNA in non-targeted radiation bystander and abscopal effects in the central nervous system. Cancer Lett. 2021;499:73–84.
   PubMed Web of Science ®Google Scholar
• Li Y, Zheng Q, Bao C, et al. Circular RNA is enriched and stable in exosomes: a promising biomarker for cancer diagnosis. Cell Res. 2015;25:981–984.
   PubMed Web of Science ®Google Scholar
• Hanan M, Soreq H, Kadener S. CircRNAs in the brain. RNA Biol. 2017;14:1028–1034.
   PubMed Web of Science ®Google Scholar
• Hsiao KY, Sun HS, Tsai SJ. Circular RNA - New member of non-coding RNA with novel functions. Exp Biol Med (Maywood). 2017;242:1136–1141.
   PubMed Web of Science ®Google Scholar
• Qu S, Zhong Y, Shang R, et al. The emerging landscape of circular RNA in life processes. RNA Biol. 2017;14:992–999.
   PubMed Web of Science ®Google Scholar
• Zhang S, Zhu D, Li H, et al. Characterization of circRNA-associated-ceRNA networks in a senescence-accelerated mouse prone 8 brain. Mol Ther. 2017;25:2053–2061.
   PubMed Web of Science ®Google Scholar
• Lin SP, Ye S, Long Y, et al. Circular RNA expression alterations are involved in OGD/R-induced neuron injury. Biochem Biophys Res Commun. 2016;471:52–56.
   PubMed Web of Science ®Google Scholar
• Yang R, Xu B, Yang B, et al. Circular RNA transcriptomic analysis of primary human brain microvascular endothelial cells infected with meningitic Escherichia coli. Mol Ther Nucleic Acids. 2018;13:651–664.
   PubMedGoogle Scholar
• Kumar L, Shamsuzzama S, Jadiya P, et al. Functional characterization of novel circular RNA molecule, circzip-2 and its synthesizing gene zip-2 in C. elegans model of Parkinson’s disease. Mol Neurobiol. 2018;55(8):6914–6926.
   PubMed Web of Science ®Google Scholar
• Liu W, Jia C, Luo L, et al. Novel circular RNAs expressed in brain microvascular endothelial cells after oxygen-glucose deprivation/recovery. Neural Regen Res. 2019;14(12):2104–2111. .
   PubMed Web of Science ®Google Scholar
• Wu P, Gao Y, Shen S, et al. KHDRBS3 regulates the permeability of blood–tumor barrier via cDENND4C/miR-577 axis. Cell Death Dis. 2019;10(7):536. .
   PubMedGoogle Scholar
• Yang L, Han B, Zhang Y, et al. Engagement of circular RNA HECW2 in the nonautophagic role of ATG5 implicated in the endothelial-mesenchymal transition. Autophagy. 2018;14(3):404–418. .
   PubMed Web of Science ®Google Scholar
• Bai Y, Zhang Y, Han B, 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(1):32–50. .
   PubMed Web of Science ®Google Scholar
• Yang R, Chen J, Xu B, et al. Circ_2858 helps blood-brain barrier disruption by increasing VEGFA via sponging miR-93-5p during Escherichia coli meningitis. Mol Ther Nucleic Acids. 2020;22:708–721.
   PubMedGoogle Scholar
• Mone P, Gambardella J, Wang X, et al. MiR-24 targets the transmembrane glycoprotein Neuropilin-1 in human brain microvascular endothelial cells. Noncoding RNA. 2021;7:9.
   PubMed Web of Science ®Google Scholar
• Morad G, Daisy CC, Otu HH, et al. Cdc42-dependent transfer of mir301 from breast cancer-derived extracellular vesicles regulates the matrix modulating ability of astrocytes at the blood–brain barrier. Int J Mol Sci. 2020;21(11):3851.
   PubMed Web of Science ®Google Scholar
• Michinaga S, Koyama Y. Dual roles of astrocyte-derived factors in regulation of blood-brain barrier function after brain damage. Int J Mol Sci. 2019;20(3):571.
   PubMed Web of Science ®Google Scholar
• Liu Q, Yang Y, Fan X. Microvascular pericytes in brain-associated vascular disease. Biomed Pharmacother. 2020;121:109633.
   PubMed Web of Science ®Google Scholar
• Hellstrom M, Gerhardt H, Kalen M, et al. Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol. 2001;153(3):543–554. .
   PubMed Web of Science ®Google Scholar
• Underly RG, Levy M, Hartmann DA, et al. Pericytes as inducers of rapid, matrix metalloproteinase-9-dependent capillary damage during ischemia. J Neurosci. 2017;37(1):129–140.
   PubMed Web of Science ®Google Scholar
• Winkler EA, Bell RD, Zlokovic BV. Central nervous system pericytes in health and disease. Nat Neurosci. 2011;14(11):1398–1405.
   PubMed Web of Science ®Google Scholar