Suppression of microRNA-320 Induces Cerebral Protection Against Ischemia/Reperfusion Injury by Targeting HMGB1/NF-kappaB Axis
Jazyk angličtina Země Česko Médium print
Typ dokumentu časopisecké články
PubMed
38466011
PubMed Central
PMC11019618
DOI
10.33549/physiolres.935081
PII: 935081
Knihovny.cz E-zdroje
- MeSH
- infarkt arteria cerebri media genetika MeSH
- krysa rodu Rattus MeSH
- mikro RNA * genetika metabolismus MeSH
- NF-kappa B metabolismus MeSH
- potkani Sprague-Dawley MeSH
- protein HMGB1 * genetika MeSH
- reperfuzní poškození * genetika prevence a kontrola metabolismus MeSH
- zvířata MeSH
- Check Tag
- krysa rodu Rattus MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- Hbp1 protein, rat MeSH Prohlížeč
- mikro RNA * MeSH
- MIRN320 microRNA, rat MeSH Prohlížeč
- NF-kappa B MeSH
- protein HMGB1 * MeSH
MicroRNAs have been shown to potentially function in cerebral ischemia/reperfusion (IR) injury. This study aimed to examine the expression of microRNA-320 (miR-320) in cerebral IR injury and its involvement in cerebral mitochondrial function, oxidative stress, and inflammatory responses by targeting the HMGB1/NF-kappaB axis. Sprague-Dawley rats were subjected to middle cerebral artery occlusion to simulate cerebral IR injury. The cerebral expression of miR-320 was assessed using qRT-PCR. Neurological function, cerebral infarct volume, mitochondrial function, oxidative stress, and inflammatory cytokines were evaluated using relevant methods, including staining, fluorometry, and ELISA. HMGB1 expression was analyzed through Western blotting. The levels of miR-320, HMGB1, neurological deficits, and cerebral infarction were significantly higher after IR induction. Intracerebral overexpression of miR-320 resulted in substantial neurological deficits, increased infarct volume, elevated levels of 8-isoprostane, NF-kappaBp65, TNF-alpha, IL-1beta, ICAM-1, VCAM-1, and HMGB1 expression. It also promoted the loss of mitochondrial membrane potential and ROS levels while reducing MnSOD and GSH levels. Downregulation of miR-320 and inhibition of HMGB1 activity significantly reversed the outcomes of cerebral IR injury. MiR-320 plays a negative role in regulating cerebral inflammatory/oxidative reactions induced by IR injury by enhancing HMGB1 activity and modulating mitochondrial function.
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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: 10.1016/S1474-4422(21)00252-0. PubMed DOI PMC
Lin L, Wang X, Yu Z. Ischemia-reperfusion Injury in the Brain: Mechanisms and Potential Therapeutic Strategies. Biochem Pharmacol (Los Angel) 2016;5:213. doi: 10.4172/2167-0501.1000213. PubMed DOI PMC
Jurcau A, Simion A. Neuroinflammation in Cerebral Ischemia and Ischemia/Reperfusion Injuries: From Pathophysiology to Therapeutic Strategies. Int J Mol Sci. 2021;23:14. doi: 10.3390/ijms23010014. PubMed DOI PMC
Wu L, Xiong X, Wu X, Ye Y, Jian Z, Zhi Z, Gu L. Targeting Oxidative Stress and Inflammation to Prevent Ischemia-Reperfusion Injury. Front Mol Neurosci. 2020;13:28. doi: 10.3389/fnmol.2020.00028. PubMed DOI PMC
Wong CH, Crack PJ. Modulation of neuro-inflammation and vascular response by oxidative stress following cerebral ischemia-reperfusion injury. Curr Med Chem. 2008;15:1–14. doi: 10.2174/092986708783330665. PubMed DOI
Li S, Wang H, Zhou Y. JAK2/STAT3 pathway mediates beneficial effects of pterostilbene on cardiac contractile and electrical function in the setting of myocardial reperfusion injury. Physiol Res. 2022;71:489–499. doi: 10.33549/physiolres.934919. PubMed DOI PMC
Ye Y, Zeng Z, Jin T, Zhang H, Xiong X, Gu L. The Role of High Mobility Group Box 1 in Ischemic Stroke. Front Cell Neurosci. 2019;13:127. doi: 10.3389/fncel.2019.00127. PubMed DOI PMC
Shi Y, Zhang L, Teng J, Miao W. HMGB1 mediates microglia activation via the TLR4/NF-κB pathway in coriaria lactone induced epilepsy. Mol Med Rep. 2018;17:5125–5131. doi: 10.3892/mmr.2018.8485. PubMed DOI PMC
Xie W, Zhu T, Dong X, Nan F, Meng X, Zhou P, Sun G, Sun X. HMGB1-triggered inflammation inhibition of notoginseng leaf triterpenes against cerebral ischemia and reperfusion injury via MAPK and NF-κB signaling pathways. Biomolecules. 2019;9:512. doi: 10.3390/biom9100512. PubMed DOI PMC
Machackova T, Vychytilova-Faltejskova P, Souckova K, Laga R, Androvič L, Mixová G, Slaby O. Barriers in systemic delivery and preclinical testing of synthetic microRNAs in animal models: an experimental study on miR-215-5p mimic. Physiol Res. 2021;70:481–487. doi: 10.33549/physiolres.934571. PubMed DOI PMC
Neag MA, Mitre AO, Burlacu CC, Inceu AI, Mihu C, Melincovici CS, Bichescu M, Buzoianu AD. miRNA Involvement in Cerebral Ischemia-Reperfusion Injury. Front Neurosci. 2022;16:901360. doi: 10.3389/fnins.2022.901360. PubMed DOI PMC
Zhu XA, Gao LF, Zhang ZG, Xiang DK. Down-regulation of miR-320 exerts protective effects on myocardial I-R injury via facilitating Nrf2 expression. Eur Rev Med Pharmacol Sci. 2019;23:1730–1741. doi: 10.26355/eurrev_201902_17135. PubMed DOI
Tian ZQ, Jiang H, Lu ZB. MiR-320 regulates cardiomyocyte apoptosis induced by ischemia-reperfusion injury by targeting AKIP1. Cell Mol Biol Lett. 2018;23:41. doi: 10.1186/s11658-018-0105-1. PubMed DOI PMC
Liang L, Wang J, Yuan Y, Zhang Y, Liu H, Wu C, Yan Y. MicRNA-320 facilitates the brain parenchyma injury via regulating IGF-1 during cerebral I/R injury in mice. Biomed Pharmacother. 2018;102:86–93. doi: 10.1016/j.biopha.2018.03.036. PubMed DOI
He F, Shi E, Yan L, Li J, Jiang X. Inhibition of micro-ribonucleic acid-320 attenuates neurologic injuries after spinal cord ischemia. J Thorac Cardiovasc Surg. 2015;17:398–406. doi: 10.1016/j.jtcvs.2015.03.066. PubMed DOI
Ren XP, Wu J, Wang X, Sartor MA, Qian J, Jones K, Qian J, Nicolaou P, Pritchard TJ, Fan GC. MicroRNA-320 Is Involved in the Regulation of Cardiac Ischemia/Reperfusion Injury by Targeting Heat-Shock Protein 20. Circulation. 2009;119:2357–2366. doi: 10.1161/CIRCULATIONAHA.108.814145. PubMed DOI PMC
Tang H, Lee M, Sharpe O, Salamone L, Noonan EJ, Hoang CD, Levine S, et al. Oxidative stress-responsive microRNA-320 regulates glycolysis in diverse biological systems. FASEB J. 2012;26:4710–4721. doi: 10.1096/fj.11-197467. PubMed DOI PMC
Yan J, Ying S, Cai X. MicroRNA-Mediated Regulation of HMGB1 in Human Hepatocellular Carcinoma. Biomed Res Int. 2018;2018:2754941. doi: 10.1155/2018/2754941. PubMed DOI PMC
Kim SW, Lee H, Lee HK, Kim ID, Lee JK. Neutrophil extracellular trap induced by HMGB1 exacerbates damages in the ischemic brain. Acta Neuropathol Commun. 2019;7:94. doi: 10.1186/s40478-019-0747-x. PubMed DOI PMC
Banks WA, Hansen KM, Erickson MA, Crews FT. High-mobility group box 1 (HMGB1) crosses the BBB bidirectionally. Brain Behav Immun. 2023;111:386–394. doi: 10.1016/j.bbi.2023.04.018. PubMed DOI
Stoicea N, Du A, Lakis DC, Tipton C, Arias-Morales CE, Bergese SD. The MiRNA journey from theory to practice as a CNS biomarker. Front Genet. 2016;7:11. doi: 10.3389/fgene.2016.00011. PubMed DOI PMC
Schaar KL, Brenneman MM, Savitz SI. Functional assessments in the rodent stroke model. Exp Trans Stroke Med. 2010;2:13. doi: 10.1186/2040-7378-2-13. PubMed DOI PMC
De-Ugarte L, Balcells S, Nogues X, Grinberg D, Diez-Perez A, Garcia-Giralt N. Pro-osteoporotic miR-320a impairs osteoblast function and induces oxidative stress. PLoS One. 2018;13:e0208131. doi: 10.1371/journal.pone.0208131. PubMed DOI PMC
Wu S, Xu H, Peng J, Wang C, Jin Y, Liu K, Sun H, Qin J. Potent anti-inflammatory effect of dioscin mediated by suppression of TNF-α-induced VCAM-1, ICAM-1and EL expression via the NF-κB pathway. Biochimie. 2015;110:62–72. doi: 10.1016/j.biochi.2014.12.022. PubMed DOI
Jover-Mengual T, Hwang JY, Byun HR, Court-Vazquez BL, Centeno JM, Burguete MC, Zukin RS. The Role of NF-κB Triggered Inflammation in Cerebral Ischemia. Front Cell Neurosci. 2021;15:633610. doi: 10.3389/fncel.2021.633610. PubMed DOI PMC
Yang L, Tao LY, Chen XP. Roles of NF-kappaB in central nervous system damage and repair. Neurosci Bull. 2007;23:307–313. doi: 10.1007/s12264-007-0046-6. PubMed DOI PMC
Sun SC. The non-canonical NF-κB pathway in immunity and inflammation. Nat Rev Immunol. 2017;17:545–558. doi: 10.1038/nri.2017.52. PubMed DOI PMC
Liu X, Lin R, Zhao B, Guan R, Li T, Jin R. Correlation between oxidative stress and the NF-κB signaling pathway in the pulmonary tissues of obese asthmatic mice. Mol Med Rep. 2016;13:1127–1134. doi: 10.3892/mmr.2015.4663. PubMed DOI PMC
Musiek ES, Yin H, Milne GL, Morrow JD. Recent advances in the biochemistry and clinical relevance of the isoprostane pathway. Lipids. 2005;40:987–994. doi: 10.1007/s11745-005-1460-7. PubMed DOI
Bauer J, Ripperger A, Frantz S, Ergün S, Schwedhelm E, Benndorf RA. Pathophysiology of isoprostanes in the cardiovascular system: implications of isoprostane-mediated thromboxane A2 receptor activation. Br J Pharmacol. 2014;171:3115–3131. doi: 10.1111/bph.12677. PubMed DOI PMC
Yin C, Wang X, Kukreja RC. Endogenous microRNAs induced by heat-shock reduce myocardial infarction following ischemia-reperfusion in mice. FEBS Lett. 2008;582:4137–4142. doi: 10.1016/j.febslet.2008.11.014. PubMed DOI PMC
Jayawardena E, Medzikovic L, Ruffenach G, Eghbali M. Role of miRNA-1 and miRNA-21 in Acute Myocardial Ischemia-Reperfusion Injury and Their Potential as Therapeutic Strategy. Int J Mol Sci. 2022;23:1512. doi: 10.3390/ijms23031512. PubMed DOI PMC
Nakata K, Okazaki M, Shimizu D, Suzawa K, Shien K, Miyoshi K, Otani S, et al. Protective effects of anti-HMGB1 monoclonal antibody on lung ischemia reperfusion injury in mice. Biochem Biophys Res Commun. 2021;573:164–170. doi: 10.1016/j.bbrc.2021.08.015. PubMed DOI
Mardente S, Mari E, Consorti F, Di Gioia C, Negri R, Etna M, Zicari A, Antonaci A. HMGB1 induces the overexpression of miR-222 and miR-221 and increases growth and motility in papillary thyroid cancer cells. Oncol Rep. 2012;28:2285–2289. doi: 10.3892/or.2012.2058. PubMed DOI