The Mechanisms of Long Non-coding RNA-XIST in Ischemic Stroke: Insights into Functional Roles and Therapeutic Potential.
Ischemic stroke
LncRNAs
Pathogenesis
XIST
miRNA
Journal
Molecular neurobiology
ISSN: 1559-1182
Titre abrégé: Mol Neurobiol
Pays: United States
ID NLM: 8900963
Informations de publication
Date de publication:
06 Nov 2023
06 Nov 2023
Historique:
received:
01
07
2023
accepted:
18
10
2023
medline:
7
11
2023
pubmed:
7
11
2023
entrez:
6
11
2023
Statut:
aheadofprint
Résumé
Ischemic stroke, which occurs due to the occlusion of cerebral arteries, is a common type of stroke. Recent research has highlighted the important role of long non-coding RNAs (lncRNAs) in the development of cerebrovascular diseases, specifically ischemic stroke. Understanding the functional roles of lncRNAs in ischemic stroke is crucial, given their potential contribution to the disease pathology. One noteworthy lncRNA is X-inactive specific transcript (XIST), which exhibits downregulation during the early stages of ischemic stroke and subsequent upregulation in later stages. XIST exert its influence on the development of ischemic stroke through interactions with multiple miRNAs and transcription factors. These interactions play a significant role in the pathogenesis of the condition. In this review, we have provided a comprehensive summary of the functional roles of XIST in ischemic stroke. By investigating the involvement of XIST in the disease process, we aim to enhance our understanding of the mechanisms underlying ischemic stroke and potentially identify novel therapeutic targets.
Identifiants
pubmed: 37932544
doi: 10.1007/s12035-023-03740-x
pii: 10.1007/s12035-023-03740-x
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Manikandan P, Vijayakumar R, Alshehri B, Senthilkumar S, Al-Aboody MS, Haribaskar R et al (2022) Long non-coding RNAs act as novel therapeutic targets by regulating molecular networks associated with ischemic stroke. J King Saud Univ Sci 34:102119
Feigin VL, Brainin M, Norrving B, Martins S, Sacco RL, Hacke W et al (2022) World Stroke Organization (WSO): global stroke fact sheet 2022. Int J Stroke 17:18–29
pubmed: 34986727
doi: 10.1177/17474930211065917
Gan L, Liao S, Xing Y, Deng S (2021) The regulatory functions of lncRNAs on angiogenesis following ischemic stroke. Front Mol Neurosci 13:613976
pubmed: 33613191
pmcid: 7890233
doi: 10.3389/fnmol.2020.613976
Ollen-Bittle N, Roseborough AD, Wang W, Wu J-LD (2022) Whitehead SN: mechanisms and biomarker potential of extracellular vesicles in stroke. Biology 11:1231
Kuriakose D, Xiao Z (2020) Pathophysiology and treatment of stroke: present status and future perspectives. Int J Mol Sci 21:7609
Şekerdağ E, Solaroğlu I, Gürsoy-özdemir Y (2018) Cell death mechanisms in stroke and novel molecular and cellular treatment options. Current Neuropharmacology 16:1396–1415
pubmed: 29512465
pmcid: 6251049
doi: 10.2174/1570159X16666180302115544
Palazzolo JS, Ale A, Ho H, Jagdale S, Broughton BR, Medcalf RL et al (2023) Platelet-targeted thrombolysis for treatment of acute ischemic stroke. Blood Adv 7:561
Zhong L, Luo Y, Fan J (2022) LncRNAs: promising therapeutic targets and biomarkers for ischemic stroke. Transl Stroke Res 15(1):1–3
Zhou Z, Ren X, Zheng L, Li A, Zhou W (2022) LncRNA NEAT1 stabilized Wnt3a via U2AF2 and activated Wnt/β-catenin pathway to alleviate ischemia stroke induced injury. Brain Res 1788:147921
pubmed: 35452660
doi: 10.1016/j.brainres.2022.147921
Vasudeva K, Dutta A, Munshi A (2021) Role of lncRNAs in the development of ischemic stroke and their therapeutic potential. Mol Neurobiol 58:3712–3728
pubmed: 33818737
doi: 10.1007/s12035-021-02359-0
Wang Y, Feng F, Zheng P, Wang L, Wang Y, Lv Y et al (2022) Dysregulated lncRNA and mRNA may promote the progression of ischemic stroke via immune and inflammatory pathways: results from RNA sequencing and bioinformatics analysis. Genes Genom 44:97–108
doi: 10.1007/s13258-021-01173-1
Chen J, Liu Y, Min J, Wang H, Li F, Xu C et al (2021) Alternative splicing of lncRNAs in human diseases. Am J Cancer Res 11:624
pubmed: 33791145
pmcid: 7994174
Farzaneh Z, Farzaneh M (2022) Prevention and treatment of hepatocellular carcinoma using miRNAs. Arch Iran Med 25:133–138
pubmed: 35429953
doi: 10.34172/aim.2022.23
Farzaneh M, Ghasemian M, Ghaedrahmati F, Poodineh J, Najafi S, Masoodi T et al (2022) Functional roles of lncRNA-TUG1 in hepatocellular carcinoma. Life Sci 308:120974
pubmed: 36126725
doi: 10.1016/j.lfs.2022.120974
Khan I, Siraj M (2023) An updated review on cell signaling pathways regulated by candidate miRNAs in coronary artery disease. Noncoding RNA Res 8:326–334
pmcid: 10106733
doi: 10.1016/j.ncrna.2023.03.007
Li G, Deng L, Huang N, Sun F (2021) The biological roles of lncRNAs and future prospects in clinical application. Diseases 9:8
pubmed: 33450825
pmcid: 7838801
doi: 10.3390/diseases9010008
Xu W-W, Jin J, Wu X-Y, Ren Q-L, Farzaneh M (2022) MALAT1-related signaling pathways in colorectal cancer. Cancer Cell Int 22:126
pubmed: 35305641
pmcid: 8933897
doi: 10.1186/s12935-022-02540-y
Cao Y, Liu J, Lu Q, Huang K, Yang B, Reilly J et al (2022) An update on the functional roles of long non-coding RNAs in ischemic injury. Int J Mol Med 50:1–15
doi: 10.3892/ijmm.2022.5147
Fan J, Saft M, Sadanandan N, Gonzales-Portillo B, Park YJ, Sanberg PR et al (2020) LncRNAs stand as potent biomarkers and therapeutic targets for stroke. Front Aging Neurosci 12:594571
pubmed: 33192490
pmcid: 7604318
doi: 10.3389/fnagi.2020.594571
Waseem A, Khan AQ, Khan MA, Khan R, Uddin S, Boltze J et al (2023) Unveiling the therapeutic potential of non-coding RNAs in stroke-induced tissue regeneration. Stem Cells 23:1–18
Wang W, Min L, Qiu X, Wu X, Liu C, Ma J et al (2021) Biological function of long non-coding RNA (LncRNA) Xist. Front Cell Dev Biol 9:645647
pubmed: 34178980
doi: 10.3389/fcell.2021.645647
Wang Y, Jiang F, Chen F, Zhang D, Wang J (2022) LncRNA XIST engages in psoriasis via sponging miR-338-5p to regulate keratinocyte proliferation and inflammation. Skin Pharmacol Physiol 35:196–205
pubmed: 35231918
doi: 10.1159/000523781
Bost C, Arleevskaya MI, Brooks WH, Plaza S, Guery JC, Renaudineau Y (2022) Long non-coding RNA Xist contribution in systemic lupus erythematosus and rheumatoid arthritis. Clin Immunol 236:108937
pubmed: 35114365
doi: 10.1016/j.clim.2022.108937
Wang C, Dong J, Sun J, Huang S, Wu F, Zhang X et al (2021) Silencing of lncRNA XIST impairs angiogenesis and exacerbates cerebral vascular injury after ischemic stroke. Mol Ther-Nucleic Acids 26:148–160
pubmed: 34513301
pmcid: 8413678
doi: 10.1016/j.omtn.2021.06.025
Sun P, Hamblin MH, Yin K-J (2022) Non-coding RNAs in the regulation of blood-brain barrier functions in central nervous system disorders. Fluids Barriers CNS 19:27–27
pubmed: 35346266
pmcid: 8959280
doi: 10.1186/s12987-022-00317-z
Cao Y, Liu J, Lu Q, Huang K, Yang B, Reilly J et al (2022) An update on the functional roles of long non-coding RNAs in ischemic injury (Review). Int J Mol Med 50:91
pubmed: 35593308
pmcid: 9170192
doi: 10.3892/ijmm.2022.5147
Huarte M (2015) The emerging role of lncRNAs in cancer. Nat Med 21:1253–1261
pubmed: 26540387
doi: 10.1038/nm.3981
Soibam B (2017) Super-lncRNAs: identification of lncRNAs that target super-enhancers via RNA: DNA: DNA triplex formation. Rna 23:1729–1742
pubmed: 28839111
pmcid: 5648039
doi: 10.1261/rna.061317.117
Bhan A, Soleimani M, Mandal SS (2017) Long noncoding RNA and cancer: a new paradigm. Cancer Res 77:3965–3981
pubmed: 28701486
pmcid: 8330958
doi: 10.1158/0008-5472.CAN-16-2634
Cuevas-Diaz Duran R, Wei H, Kim DH, Wu JQ (2019) Invited Review: Long non-coding RNAs: important regulators in the development, function and disorders of the central nervous system. Neuropathol Appl Neurobiol 45:538–556
pubmed: 30636336
doi: 10.1111/nan.12541
Toiyama Y, Okugawa Y, Goel A (2014) DNA methylation and microRNA biomarkers for noninvasive detection of gastric and colorectal cancer. Biochem Biophys Res Commun 455:43–57
pubmed: 25128828
pmcid: 4250419
doi: 10.1016/j.bbrc.2014.08.001
Statello L, Guo C-J, Chen L-L, Huarte M (2021) Gene regulation by long non-coding RNAs and its biological functions. Nat Rev Mol Cell Biol 22:96–118
pubmed: 33353982
doi: 10.1038/s41580-020-00315-9
Fico A, Fiorenzano A, Pascale E, Patriarca EJ, Minchiotti G (2019) Long non-coding RNA in stem cell pluripotency and lineage commitment: functions and evolutionary conservation. Cell Mol Life Sci 76:1459–1471
pubmed: 30607432
pmcid: 6439142
doi: 10.1007/s00018-018-3000-z
Elazazy O, Midan HM, Shahin RK, Elesawy AE, Elballal MS, Sallam A-AM et al (2023) Long non-coding RNAs and rheumatoid arthritis: pathogenesis and clinical implications. Pathol-Res Pract 55(7):25487
Le LT, Nhu CX (2023) The role of long non-coding RNAs in cardiovascular diseases. Int J Mol Sci 24:13805
pubmed: 37762106
pmcid: 10531487
doi: 10.3390/ijms241813805
Liang J, Wang Q, Li J-Q, Guo T, Yu D (2020) Long non-coding RNA MEG3 promotes cerebral ischemia-reperfusion injury through increasing pyroptosis by targeting miR-485/AIM2 axis. Exp Neurol 325:113139
pubmed: 31794744
doi: 10.1016/j.expneurol.2019.113139
Yan XW, Liu HJ, Hong YX, Meng T, Du J, Chang C (2022) lncRNA XIST induces Aβ accumulation and neuroinflammation by the epigenetic repression of NEP in Alzheimer’s disease. J Neurogenet 36:11–20
pubmed: 35098860
doi: 10.1080/01677063.2022.2028784
Xu X, Liang Y, Gareev I, Liang Y, Liu R, Wang N et al (2023) LncRNA as potential biomarker and therapeutic target in glioma. Mol Biol Rep 50:841–851
pubmed: 36331751
doi: 10.1007/s11033-022-08056-y
Zhao H, Wang L, Zhang L, Zhao H (2023) Phytochemicals targeting lncRNAs: a novel direction for neuroprotection in neurological disorders. Biomed Pharmacother 162:114692
pubmed: 37058817
doi: 10.1016/j.biopha.2023.114692
Mattick JS, Amaral PP, Carninci P, Carpenter S, Chang HY, Chen L-L et al (2023) Long non-coding RNAs: definitions, functions, challenges and recommendations. Nat Rev Mol Cell Biol 24:430–447
pubmed: 36596869
doi: 10.1038/s41580-022-00566-8
Deng X, Berletch JB, Nguyen DK, Disteche CM (2014) X chromosome regulation: diverse patterns in development, tissues and disease. Nat Rev Genet 15:367–378
pubmed: 24733023
pmcid: 4117651
doi: 10.1038/nrg3687
Li J, Ming Z, Yang L, Wang T, Liu G, Ma Q (2022) Long noncoding RNA XIST: Mechanisms for X chromosome inactivation, roles in sex-biased diseases, and therapeutic opportunities. Genes Dis 9:1478–1492
Waldron D (2016) Xist as a recruitment tool. Nat Rev Genet 17:580–580
pubmed: 27573373
doi: 10.1038/nrg.2016.116
Bar S, Seaton LR, Weissbein U, Eldar-Geva T, Benvenisty N (2019) Global characterization of X chromosome inactivation in human pluripotent stem cells. Cell Rep 27(20-29):e23
Strehle M, Guttman M (2020) Xist drives spatial compartmentalization of DNA and protein to orchestrate initiation and maintenance of X inactivation. Curr Opin Cell Biol 64:139–147
pubmed: 32535328
doi: 10.1016/j.ceb.2020.04.009
Yu B, van Tol HT, Stout TA, Roelen BA (2020) Initiation of X chromosome inactivation during bovine embryo development. Cells 9:1016
pubmed: 32325818
pmcid: 7226380
doi: 10.3390/cells9041016
Rebuzzini P, Zuccotti M, Garagna S (2020) X-Chromosome inactivation during preimplantation development and in pluripotent stem cells. Cytogenet Genome Res 160:283–294
pubmed: 32575101
doi: 10.1159/000508610
Okamoto I, Patrat C, Thépot D, Peynot N, Fauque P, Daniel N et al (2011) Eutherian mammals use diverse strategies to initiate X-chromosome inactivation during development. Nature 472:370–374
pubmed: 21471966
doi: 10.1038/nature09872
Sahakyan A, Yang Y, Plath K (2018) The role of Xist in X-chromosome dosage compensation. Trends Cell Biol 28:999–1013
pubmed: 29910081
pmcid: 6249047
doi: 10.1016/j.tcb.2018.05.005
Charles Richard JL, Ogawa Y (2015) Understanding the complex circuitry of lncRNAs at the X-inactivation center and its implications in disease conditions. Long Non–coding RNAs in Human Disease 394:1–27
Sidorenko J, Kassam I, Kemper KE, Zeng J, Lloyd-Jones LR, Montgomery GW et al (2019) The effect of X-linked dosage compensation on complex trait variation. Nat Commun 10:1–11
doi: 10.1038/s41467-019-10598-y
Aguilar R, Spencer KB, Kesner B, Rizvi NF, Badmalia MD, Mrozowich T et al (2022) Targeting Xist with compounds that disrupt RNA structure and X inactivation. Nature 604:160–166
pubmed: 35355011
doi: 10.1038/s41586-022-04537-z
Markaki Y, Chong JG, Wang Y, Jacobson EC, Luong C, Tan SY et al (2021) Xist nucleates local protein gradients to propagate silencing across the X chromosome. Cell 184(6174-6192):e6132
Gendrel A-V, Heard E (2014) Noncoding RNAs and epigenetic mechanisms during X-chromosome inactivation. Annu Rev Cell Dev Biol 30:561–580
pubmed: 25000994
doi: 10.1146/annurev-cellbio-101512-122415
Creamer KM, Lawrence JB (2017) XIST RNA: a window into the broader role of RNA in nuclear chromosome architecture. Philos Trans R Soc Lond Ser B Biol Sci 72(1733):20160360
Nickbarg EB, Spencer KB, Mortison JD, Lee JT (2023) Targeting RNA with small molecules: lessons learned from Xist RNA. RNA 29:463–472
pubmed: 36725318
pmcid: 10019374
doi: 10.1261/rna.079523.122
Hugues A, Jacobs CS, Roudier F (2020) Mitotic inheritance of PRC2-mediated silencing: mechanistic insights and developmental perspectives. Front Plant Sci 11:262
pubmed: 32211012
pmcid: 7075419
doi: 10.3389/fpls.2020.00262
Gujar H, Weisenberger DJ, Liang G (2019) The roles of human DNA methyltransferases and their isoforms in shaping the epigenome. Genes 10:172
pubmed: 30813436
pmcid: 6409524
doi: 10.3390/genes10020172
Loda A, Heard E (2019) Xist RNA in action: past, present, and future. PLoS Genet 15:e1008333
pubmed: 31537017
pmcid: 6752956
doi: 10.1371/journal.pgen.1008333
Huang J, Yang J, Li J, Chen Z, Guo X, Huang S et al (2019) Association of long noncoding RNA H19 polymorphisms with the susceptibility and clinical features of ischemic stroke in southern Chinese Han population. Metab Brain Dis 34:1011–1021
pubmed: 31041585
doi: 10.1007/s11011-019-00417-0
Pan Y, Jiao Q, Wei W, Zheng T, Yang X, Xin W (2021) Emerging role of LncRNAs in ischemic stroke-novel insights into the regulation of inflammation. J Inflamm Res 14:4467–4483
pubmed: 34522116
pmcid: 8434908
doi: 10.2147/JIR.S327291
Bao MH, Szeto V, Yang BB, Zhu SZ, Sun HS, Feng ZP (2018) Long non-coding RNAs in ischemic stroke. Cell Death Dis 9:281
pubmed: 29449542
pmcid: 5833768
doi: 10.1038/s41419-018-0282-x
Yao J, Du Y, Liu J, Gareev I, Yang G, Kang X et al (2021) Hypoxia related long non-coding RNAs in ischemic stroke. Non-coding RNA Research 6:153–158
pubmed: 34703955
pmcid: 8511691
doi: 10.1016/j.ncrna.2021.10.001
Zhang X, Tang X, Liu K, Hamblin MH, Yin K-J (2017) Long noncoding RNA Malat1 regulates cerebrovascular pathologies in ischemic stroke. J Neurosci 37:1797–1806
pubmed: 28093478
pmcid: 5320610
doi: 10.1523/JNEUROSCI.3389-16.2017
Guo Y, Yang JH, He Y, Zhou HF, Wang Y, Ding ZS et al (2022) Protocatechuic aldehyde prevents ischemic injury by attenuating brain microvascular endothelial cell pyroptosis via lncRNA Xist. Phytomedicine 94:153849
pubmed: 34775360
doi: 10.1016/j.phymed.2021.153849
Ma W, Li C-Y, Zhang S-J, Zang C-H, Yang J-W, Wu Z et al (2022) Neuroprotective effects of long noncoding RNAs involved in ischemic postconditioning after ischemic stroke. Neural Regen Res 17:1299–1309
pubmed: 34782575
doi: 10.4103/1673-5374.327346
Zhang H, Xia J, Hu Q, Xu L, Cao H, Wang X et al (2021) Long non-coding RNA XIST promotes cerebral ischemia/reperfusion injury by modulating miR-27a-3p/FOXO3 signaling. Mol Med Rep 24:566
pubmed: 34254504
pmcid: 8201472
doi: 10.3892/mmr.2021.12205
Kenyon CJ (2010) The genetics of ageing. Nature 464:504–512
pubmed: 20336132
doi: 10.1038/nature08980
Guo D, Ma J, Li T, Yan L (2018) Up-regulation of miR-122 protects against neuronal cell death in ischemic stroke through the heat shock protein 70-dependent NF-κB pathway by targeting FOXO3. Exp Cell Res 369:34–42
pubmed: 29715465
doi: 10.1016/j.yexcr.2018.04.027
Yu S, Yu M, Bu Z, He P, Feng J (2020) FKBP5 exacerbates impairments in cerebral ischemic stroke by inducing autophagy via the AKT/FOXO3 pathway. Front Cell Neurosci 14:193
Zhou F, Wang Y-K, Zhang C-G, Wu B-Y (2021) miR-19a/b-3p promotes inflammation during cerebral ischemia/reperfusion injury via SIRT1/FoxO3/SPHK1 pathway. J Neuroinflammation 18:122
pubmed: 34051800
pmcid: 8164774
doi: 10.1186/s12974-021-02172-5
Xiong F, Wei WP, Liu YB, Wang Y, Zhang HY, Liu R (2021) Long noncoding RNA XIST enhances cerebral ischemia-reperfusion injury by regulating miR-486-5p and GAB2. Eur Rev Med Pharmacol Sci 25:2013–2020
pubmed: 33660813
Wang G, Pan X-L, Cui P-J, Wang Y, Ma J-F, Ren R-J et al (2011) Association study of the GAB2 gene with the risk of Alzheimer disease in the Chinese population. Alzheimer Dis Assoc Disord 25(3):283–5
Wang J, Fu Z, Wang M, Lu J, Yang H, Lu H (2021) Knockdown of XIST attenuates cerebral ischemia/reperfusion injury through regulation of miR-362/ROCK2 axis. Neurochem Res 46(8):2167–2180
Wang QM, Stalker TJ, Gong Y, Rikitake Y, Scalia R, Liao JK (2012) Inhibition of Rho-kinase attenuates endothelial-leukocyte interaction during ischemia-reperfusion injury. Vasc Med 17:379–385
pubmed: 23015643
pmcid: 3807093
doi: 10.1177/1358863X12459790
Rikitake Y, Kim HH, Huang Z, Seto M, Yano K, Asano T et al (2005) Inhibition of Rho kinase (ROCK) leads to increased cerebral blood flow and stroke protection. Stroke 36:2251–2257
pubmed: 16141422
pmcid: 2633591
doi: 10.1161/01.STR.0000181077.84981.11
Hyun Lee J, Zheng Y, Von Bornstadt D, Wei Y, Balcioglu A, Daneshmand A et al (2014) Selective ROCK 2 inhibition in focal cerebral ischemia. Ann Clin Transl Neurol 1:2–14
doi: 10.1002/acn3.19
Weng S, Wang S, Jiang J (2021) Long noncoding RNA X-inactive specific transcript regulates neuronal cell apoptosis in ischemic stroke through miR-98/BACH1 axis. DNA Cell Biol 40:979–987
pubmed: 34227845
doi: 10.1089/dna.2020.6354
Ahmed S, Bott D, Gomez A, Tamblyn L, Rasheed A, Cho T et al (2015) Loss of the mono-ADP-ribosyltransferase, Tiparp, increases sensitivity to dioxin-induced steatohepatitis and lethality. J Biol Chem 290:16824–16840
pubmed: 25975270
pmcid: 4505429
doi: 10.1074/jbc.M115.660100
Han B, Zhang Y, Zhang Y, Bai Y, Chen X, Huang R et al (2018) Novel insight into circular RNA HECTD1 in astrocyte activation via autophagy by targeting MIR142-TIPARP: implications for cerebral ischemic stroke. Autophagy 14:1164–1184
pubmed: 29938598
pmcid: 6103660
doi: 10.1080/15548627.2018.1458173
Wu F, Han B, Wu S, Yang L, Leng S, Li M et al (2019) Circular RNA TLK1 aggravates neuronal injury and neurological deficits after ischemic stroke via miR-335-3p/TIPARP. J Neurosci 39:7369–7393
pubmed: 31311824
pmcid: 6759031
doi: 10.1523/JNEUROSCI.0299-19.2019
Wang Y, Li Y, Ma C, Zhou T, Lu C, Ding L et al (2021) LncRNA XIST promoted OGD-induced neuronal injury through modulating/miR-455-3p/TIPARP axis. Neurochem Res 46:1447–1456
pubmed: 33738662
doi: 10.1007/s11064-021-03286-1
Yang K, Zeng L, Ge A, Wang S, Zeng J, Yuan X et al (2022) A systematic review of the research progress of non-coding RNA in neuroinflammation and immune regulation in cerebral infarction/ischemia-reperfusion injury. Front Immunol 13:930171