MicroRNA-210 Suppresses Junction Proteins and Disrupts Blood-Brain Barrier Integrity in Neonatal Rat Hypoxic-Ischemic Brain Injury
Open accessAbstract
Cerebral edema, primarily caused by disruption of the blood-brain barrier (BBB), is one of the serious complications associated with brain injury in neonatal hypoxic-ischemic encephalopathy (HIE). Our recent study demonstrated that the hypoxic-ischemic (HI) treatment significantly increased microRNA-210 (miR-210) in the neonatal rat brain and inhibition of miR-210 provided neuroprotection in neonatal HI brain injury. The present study aims to determine the role of miR-210 in the regulation of BBB integrity in the developing brain. miR-210 mimic was administered via intracerebroventricular injection (i.c.v.) into the brain of rat pups. Forty-eight hours after the injection, a modified Rice-Vannucci model was conducted to produce HI brain injury. Post-assays included cerebral edema analysis, western blotting, and immunofluorescence staining for serum immunoglobulin G (IgG) leakage. The results showed that miR-210 mimic exacerbated cerebral edema and IgG leakage into the brain parenchyma. In contrast, inhibition of miR-210 with its complementary locked nucleic acid oligonucleotides (miR-210-LNA) significantly reduced cerebral edema and IgG leakage. These findings suggest that miR-210 negatively regulates BBB integrity i n the neonatal brain. Mechanistically, the seed sequences of miR-210 were identified complementary to the 3′ untranslated region (3′ UTR) of the mRNA transcripts of tight junction protein occludin and adherens junction protein β-catenin, indicating downstream targets of miR-210. This was further validated by in vivo data showing that miR-210 mimic significantly reduced the expression of these junction proteins in rat pup brains. Of importance, miR-210-LNA preserved the expression of junction proteins occludin and β-catenin from neonatal HI insult. Altogether, the present study reveals a novel mechanism of miR-210 in impairing BBB integrity that contributes to cerebral edema formation after neonatal HI insult, and provides new insights in miR-210-LNA mediated neuroprotection in neonatal HI brain injury.
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Recent findings of a long-range crosstalk between periphery and CNS via miRNA-containing exosomes position the BBB in the center of this communication under physiological and pathophysiological conditions.
“Recent findings of a long-range crosstalk between periphery and CNS via miRNA-containing exosomes position the BBB in the center of this communication (685) under physiological (635, 660) and pathophysiological (378, 493, 498, 587) conditions.”
From Blood-Brain Barrier: From Physiology to Disease and Back (2019) · cites this paper as [378]
The Discussion (page unavailable) reports that miR-210 disrupts BBB integrity after hypoxic-ischemic injury in neonatal rats, supporting a role for miRNA and the BBB under a pathophysiological condition. It does not describe miRNA-containing exosomes or long-range communication between the periphery and CNS. (LLM, conf=0.84)
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Cites
The Blood-Brain Barrier in Health and Chronic Neurodegenerative Disorders
Zlokovic, B. V. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.003 · Cited by 3,280 · see citing works
The blood-brain barrier/neurovascular unit in health and disease
Hawkins, B. T., & Davis, T. P. (2005) · Pharmacological Reviews · doi:10.1124/pr.57.2.4 · Cited by 2,661 · see citing works
Multifunctional strands in tight junctions
Tsukita, S., Furuse, M., & Itoh, M. (2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35067088 · Cited by 2,514 · see citing works
Development, maintenance and disruption of the blood-brain barrier
Obermeier, B., Daneman, R., & Ransohoff, R. M. (2013) · Nature Medicine · doi:10.1038/nm.3407 · Cited by 2,452 · see citing works
Neurovascular regulation in the normal brain and in Alzheimer's disease
Iadecola, C. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1387 · Cited by 2,213 · see citing works
A Semiautomated Method for Measuring Brain Infarct Volume
Swanson, R., Morton, M. T., Tsao-Wu, G., Savalos, R. A., Davidson, C., & Sharp, F. (1990) · Journal of Cerebral Blood Flow and Metabolism · doi:10.1038/jcbfm.1990.47 · Cited by 1,727 · see citing works
MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship
Pasquinelli, A. E. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3162 · Cited by 1,587 · see citing works
Endothelial Cell-to-Cell Junctions: Molecular Organization and Role in Vascular Homeostasis
Bazzoni, G., & Dejana, E. (2004) · Physiological Reviews · doi:10.1152/physrev.00035.2003 · Cited by 1,384 · see citing works
Complex Phenotype of Mice Lacking Occludin, a Component of Tight Junction Strands
Saitou, M., Furuse, M., Sasaki, H., Schulzke, J.-D., Fromm, M., Takano, H., Noda, T., & Tsukita, S. (2000) · Molecular Biology of the Cell · doi:10.1091/mbc.11.12.4131 · Cited by 1,195 · see citing works
Blood-brain barrier tight junction permeability and ischemic stroke
Sandoval, K. E., & WITT, K. A. (2008) · Neurobiology of Disease · doi:10.1016/j.nbd.2008.08.005 · Cited by 957 · see citing works
Fasanaro, P., D'Alessandra, Y., Di Stefano, V., Melchionna, R., Romani, S., Pompilio, G., Capogrossi, M. C., & Martelli, F. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m800731200 · Cited by 912 · see citing works
Brain oedema in focal ischaemia: molecular pathophysiology and theoretical implications
Simard, J. M., Kent, T. A., Chen, M., Tarasov, K. V., & Gerzanich, V. (2007) · The Lancet Neurology · doi:10.1016/s1474-4422(07)70055-8 · Cited by 799 · see citing works
Chan, S. Y., Zhang, Y.-Y., Hemann, C., Mahoney, C. E., Zweier, J. L., & Loscalzo, J. (2009) · Cell Metabolism · doi:10.1016/j.cmet.2009.08.015 · Cited by 702 · see citing works
Lee, A. C., Kozuki, N., Blencowe, H. K., Vos, T., Bahalim, A. N., Darmstadt, G. L., Niermeyer, S., Ellis, M., Robertson, N. J., Cousens, S. N., et al. (2013) · Pediatric Research · doi:10.1038/pr.2013.206 · Cited by 676 · see citing works
HYPOXIC-ISCHEMIC ENCEPHALOPATHY
Vannucci, R. C. (2000) · American Journal of Perinatology · doi:10.1055/s-2000-9293 · Cited by 525 · see citing works
Brain Endothelial Cell-Cell Junctions: How to “Open” the Blood Brain Barrier
Stamatovic, S. M., Keep, R. F., & Andjelkovic, A. V. (2008) · Current Neuropharmacology · doi:10.2174/157015908785777210 · Cited by 516 · see citing works
Desperately seeking microRNA targets
Thomas, M., Lieberman, J., & Lal, A. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1921 · Cited by 476 · see citing works
Dynamics and functions of tight junctions
Steed, E., Balda, M. S., & Matter, K. (2010) · Trends in Cell Biology · doi:10.1016/j.tcb.2009.12.002 · Cited by 418 · see citing works
Dejana, E. (1996) · Journal of Clinical Investigation · doi:10.1172/jci118997 · Cited by 369 · see citing works
Pathogenesis of Brain Edema and Investigation into Anti-Edema Drugs
Michinaga, S., & Koyama, Y. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms16059949 · Cited by 339 · see citing works
Cattelino, A., Liebner, S., Gallini, R., Zanetti, A., Balconi, G., Corsi, A., Bianco, P., Wolburg, H., Moore, R. H., Boussadia, O., et al. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200212157 · Cited by 323 · see citing works
Hypoxia: A master regulator of microRNA biogenesis and activity
Nallamshetty, S., Chan, S. Y., & Loscalzo, J. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.05.022 · Cited by 281 · see citing works
Rosenberg, G. A. (1999) · Progress in Cardiovascular Diseases · doi:10.1016/s0033-0620(99)70003-4 · Cited by 278 · see citing works
Hypoxic-Ischemic Encephalopathy in the Term Infant
Fatemi, A. S., Wilson, M. A., & Johnston, M. V. (2009) · Clinics in Perinatology · doi:10.1016/j.clp.2009.07.011 · Cited by 267 · see citing works
GABAergic regulation of cerebellar NG2 cell development is altered in perinatal white matter injury
Zonouzi, M., Scafidi, J., Li, P., Mcellin, B. M., Edwards, J., Dupree, J. L., Harvey, L. D., Sun, D., Hübner, C. A., Cull-Candy, S. G., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.3990 · Cited by 232 · see citing works
Tran, K. A., Zhang, X., Predescu, D., Huang, X., Machado, R. F., Göthert, J. R., Malik, A. B., Valyi-Nagy, T., & Zhao, Y.-Y. (2016) · Circulation · doi:10.1161/circulationaha.115.015982 · Cited by 219 · see citing works
Förster, C. Y., Silwedel, C., Golenhofen, N., Burek, M., Kietz, S., Mankertz, J., & Drenckhahn, D. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.084038 · Cited by 212 · see citing works
Cristante, E., McArthur, S., Mauro, C., Maggioli, E., Romero, I. A., Wylezinska, M., Couraud, P. O., Lopez-Tremoleda, J., Christian, H., Weksler, B. B., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1209362110 · Cited by 197 · see citing works
Hypoxic–ischemic brain injury in the term infant-current concepts
Shalak, L. F., & Perlman, J. M. (2004) · Early Human Development · doi:10.1016/j.earlhumdev.2004.06.003 · Cited by 186 · see citing works
MicroRNA-210 overexpression induces angiogenesis and neurogenesis in the normal adult mouse brain
Zeng, L., He, X., Wang, Y., Tang, Y., Zheng, C., Cai, H., Liu, J., Wang, Y., Fu, Y., & Yang, G. (2013) · Gene Therapy · doi:10.1038/gt.2013.55 · Cited by 168 · see citing works
Boichot, C., WALKER, P. M., Durand, C., Grimaldi, M., Chapuis, S., & Brunotte, F. (2006) · Radiology · doi:10.1148/radiol.2393050027 · Cited by 161 · see citing works
Inhibition of microRNA-181 Reduces Forebrain Ischemia-Induced Neuronal Loss
Moon, J. M., Xu, L., & Giffard, R. G. (2013) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2013.157 · Cited by 158 · see citing works
The Elegance of the MicroRNAs: A Neuronal Perspective
Kosik, K. S., & Krichevsky, A. M. (2005) · Neuron · doi:10.1016/j.neuron.2005.08.019 · Cited by 154 · see citing works
Free Radical Injury and Blood-Brain Barrier Permeability in Hypoxic-Ischemic Encephalopathy
Kumar, A., Mittal, R., Khanna, H. D., & Basu, S. (2008) · PEDIATRICS · doi:10.1542/peds.2008-0269 · Cited by 139 · see citing works
Baburamani, A. A., Ek, C. J., Walker, D. W., & Castillo-Meléndez, M. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00424 · Cited by 137 · see citing works
Ek, C. J., D’Angelo, B., Baburamani, A. A., Lehner, C., Leverin, A., Smith, P. L. P., Nilsson, H., Svedin, P., Hagberg, H., & Mallard, C. E. (2015) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2014.255 · Cited by 127 · see citing works
Ma, Q., Dasgupta, C., Li, Y., Bajwa, N. M., Xiong, F., Harding, B., Hartman, R. E., & Zhang, L. (2016) · Neurobiology of Disease · doi:10.1016/j.nbd.2016.02.011 · Cited by 112 · see citing works
Self-citationSinger, K. L., Stevenson, B. R., Woo, P. L., & Firestone, G. L. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)33979-0 · Cited by 103 · see citing works
Muramatsu, K., Fukuda, A., Togari, H., Wada, Y., & Nishino, H. (1997) · Stroke · doi:10.1161/01.str.28.11.2281 · Cited by 101 · see citing works
Glucocorticoid effects on mouse microvascular endothelial barrier permeability are brain specific
Förster, C. Y., Waschke, J., Burek, M., Leers, J., & Drenckhahn, D. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.106385 · Cited by 97 · see citing works
Irmady, K., Jackman, K. A., Padow, V. A., Shahani, N., Martin, L. A., Cerchietti, L. C. A., Unsicker, K., Iadecola, C., & Hempstead, B. L. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1982-13.2014 · Cited by 90 · see citing works
Zhang, W., Zhang, H., Mu, H., Zhu, W., Jiang, X., Hu, X., Shi, Y., Leak, R. K., Dong, Q., Chen, J., et al. (2016) · Neurobiology of Disease · doi:10.1016/j.nbd.2016.02.020 · Cited by 85 · see citing works
Duration of ischemia influences the development and resolution of ischemic brain edema.
Todd, N. V., Picozzi, P., Crockard, A., & Russell, R. W. R. (1986) · Stroke · doi:10.1161/01.str.17.3.466 · Cited by 85 · see citing works
Kleinschnitz, C., Blecharz, K., Kahles, T., Schwarz, T., Kraft, P., Göbel, K., Meuth, S. G., Burek, M., Thum, T., Stoll, G., et al. (2011) · Stroke · doi:10.1161/strokeaha.110.592238 · Cited by 84 · see citing works
Soul, J. S., Robertson, R. L., Tzika, A. A., du Plessis, A. J., & Volpe, J. J. (2001) · PEDIATRICS · doi:10.1542/peds.108.5.1211 · Cited by 81 · see citing works
Mirza, M. K., Sun, Y., Zhao, Y. D., Potula, H.-H. S. K., Frey, R. S., Vogel, S. M., Malik, A. B., & Zhao, Y. (2010) · The Journal of Experimental Medicine · doi:10.1084/jem.20091857 · Cited by 64 · see citing works
S-Nitrosation of β-Catenin and p120 Catenin
Marín, N., Zamorano, P., Carrasco, R., Mujica, P. E., González, F. G., Quezada, C., Meininger, C. J., Borić, M. P., Durán, W. N., & Sánchez, F. A. (2012) · Circulation Research · doi:10.1161/circresaha.112.274548 · Cited by 63 · see citing works
Role reversal: the regulation of neuronal gene expression by microRNAs
Klein, M. E., Impey, S., & Goodman, R. H. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.08.011 · Cited by 61 · see citing works
Cerebellar vermian atrophy after neonatal hypoxic-ischemic encephalopathy.
Sargent, M. A., Poskitt, K. J., Roland, E. H., Hill, A., & Hendson, G. (2004) · PubMed Central · Cited by 61 · see citing works
Hossain, M. A. (2007) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2007.08.013 · Cited by 59 · see citing works
Hsu, Y.-C., Chang, Y., Lin, Y., Sze, C., Huang, C., & Ho, C.-J. (2014) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2013.244 · Cited by 49 · see citing works
Dissecting gene expression at the blood-brain barrier
Huntley, M. A., Bien‐Ly, N., Daneman, R., & Watts, R. J. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00355 · Cited by 38 · see citing works
Oxygen resuscitation does not ameliorate neonatal hypoxia/ischemia‐induced cerebral edema
Ferrari, D. C., Nešić, O., & Perez-Polo, J. R. (2010) · Journal of Neuroscience Research · doi:10.1002/jnr.22358 · Cited by 34 · see citing works
Perspectives on Neonatal Hypoxia/Ischemia-Induced Edema Formation
Ferrari, D. C., Nešić, O., & Perez-Polo, J. R. (2010) · Neurochemical Research · doi:10.1007/s11064-010-0308-y · Cited by 31 · see citing works
Qiao, M., Latta, P., Meng, S., Tomanek, B., & Tuor, U. I. (2003) · Pediatric Research · doi:10.1203/01.pdr.0000100477.59081.fe · Cited by 30 · see citing works
Role of β-Catenin in Regulating Microvascular Endothelial Cell Hyperpermeability
Sawant, D. A., Tharakan, B., Hunter, F. A., Smythe, W. R., & Childs, E. W. (2011) · The Journal of Trauma: Injury, Infection, and Critical Care · doi:10.1097/ta.0b013e31820b3ed7 · Cited by 22 · see citing works
Advances in Neonatal Neurology 1950-2000
Koenigsberger, M. R. (2000) · Revista de Neurología · doi:10.33588/rn.3103.2000309 · Cited by 12 · see citing works
Reorientation ability of adults and healthy children submitted to whole body horizontal rotations
Zanelli, G., Petrarca, M., Cappa, P., Castelli, E., & Berthoz, A. (2009) · Cognitive Processing · doi:10.1007/s10339-009-0301-z · Cited by 9 · see citing works
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Sweeney, M. D., Zhao, Z., Montagne, A., Nelson, A. R., & Zlokovic, B. V. (2019) · Physiological Reviews · doi:10.1152/physrev.00050.2017 · Cited by 2,294 · see citing works
Jin, Z. Y., Ke, J., Guo, P., Wang, Y., & Wu, H. (2019) · Europe PMC (PubMed Central) · Cited by 652 · see citing works
Michinaga, S., & Koyama, Y. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20030571 · Cited by 263 · see citing works
Occludin regulation of blood–brain barrier and potential therapeutic target in ischemic stroke
Qi, Z., Yuan, S., & Liu, K. (2020) · Brain Circulation · doi:10.4103/bc.bc_29_20 · Cited by 118 · see citing works
New progress in the approaches for blood–brain barrier protection in acute ischemic stroke
Li, Y., Zhong, W., Jiang, Z., & Tang, X. (2018) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2018.11.006 · Cited by 114 · see citing works
Self-citationEmerging Roles of miRNAs in Brain Development and Perinatal Brain Injury
Cho, K. H. T., Xu, B., Blenkiron, C., & Fraser, M. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00227 · Cited by 114 · see citing works
MicroRNA based theranostics for brain cancer: basic principles
Petrescu, G. E. D., Sabo, A. A., Torsin, L. I., Călin, G. A., & Dragomir, M. P. (2019) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-019-1180-5 · Cited by 109 · see citing works
Li, M., Zhao, J., Cao, M., Liu, R., Chen, G., Li, S., Xie, Y., Xie, J., Cheng, Y., Huang, L., et al. (2020) · Biological Research · doi:10.1186/s40659-020-00279-2 · Cited by 88 · see citing works
Self-citationMa, F., Zhang, X., & Yin, K. (2019) · Experimental Neurology · doi:10.1016/j.expneurol.2019.113094 · Cited by 72 · see citing works
Disdier, C., & Stonestreet, B. S. (2020) · Journal of Neuroscience Research · doi:10.1002/jnr.24590 · Cited by 69 · see citing works
microRNAs Orchestrate Pathophysiology of Breast Cancer Brain Metastasis: Advances in Therapy
Kanchan, R. K., Siddiqui, J. A., Mahapatra, S., Batra, S. K., & Nasser, M. W. (2020) · Molecular Cancer · doi:10.1186/s12943-020-1140-x · Cited by 69 · see citing works
MicroRNA in Brain pathology: Neurodegeneration the Other Side of the Brain Cancer
Godlewski, J. A., Lenart, J., & Salińska, E. (2019) · Non-Coding RNA · doi:10.3390/ncrna5010020 · Cited by 67 · see citing works
Sun, P., Hamblin, M. H., & Yin, K. (2022) · Fluids and Barriers of the CNS · doi:10.1186/s12987-022-00317-z · Cited by 66 · see citing works
Ren, Z., Yu, J., Wu, Z., Si, W., Li, X., Liu, Y., Zhou, J., Deng, R., & Chen, D. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00388 · Cited by 60 · see citing works
Neuroprotective effect of Vanillin on hypoxic-ischemic brain damage in neonatal rats
Lan, X., Wang, Q., Yang, J., Ma, L., Zhang, W., Zheng, P., Sun, T., Niu, J., Liu, N., & Yu, J. (2019) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2019.109196 · Cited by 58 · see citing works
Davis, C., Savitz, S. I., & Satani, N. (2021) · Cells · doi:10.3390/cells10040767 · Cited by 51 · see citing works
Epigenetics in blood–brain barrier disruption
Ihezie, S. A., Mathew, I. E., McBride, D. W., Dienel, A., Blackburn, S., & Pandit, P. K. T. (2021) · Fluids and Barriers of the CNS · doi:10.1186/s12987-021-00250-7 · Cited by 47 · see citing works
Chen, Z., Hu, Y., Lu, R., Ge, M., & Zhang, L. (2020) · Life Sciences · doi:10.1016/j.lfs.2020.117664 · Cited by 46 · see citing works
Self-citationNon-coding RNAs: the extensive and interactive regulators of the blood-brain barrier permeability
Yang, R., Xu, B., Yang, B., Fu, J., Chen, H., & Wang, X. (2021) · RNA Biology · doi:10.1080/15476286.2021.1950465 · Cited by 45 · see citing works
Emerging therapeutic targets for cerebral edema
Jha, R. M., Raikwar, S. P., Mihaljević, S., Casabella, A. M., Catapano, J. S., Rani, A., Desai, S. M., Gerzanich, V., & Simard, J. M. (2021) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2021.2010045 · Cited by 41 · see citing works
Clinical Implications of Epigenetic Dysregulation in Perinatal Hypoxic-Ischemic Brain Damage
Bustelo, M., Barkhuizen, M., van den Hove, D., Steinbusch, H. W. M., Bruno, M. A., Loidl, C. F., & Gavilanes, A. W. D. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.00483 · Cited by 41 · see citing works
Ma, Q., Dasgupta, C., Li, Y., Huang, L., & Zhang, L. (2019) · Molecular Neurobiology · doi:10.1007/s12035-019-1491-8 · Cited by 39 · see citing works
Self-citationTargeting microRNAs to Regulate the Integrity of the Blood–Brain Barrier
Wang, J., Xu, F., Zhu, X., Li, X., Li, Y., & Li, J. (2021) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2021.673415 · Cited by 36 · see citing works
Self-citationPage, S., Raut, S., & Al-Ahmad, A. J. (2019) · NeuroMolecular Medicine · doi:10.1007/s12017-019-08531-z · Cited by 34 · see citing works
Bhardwaj, U., & Singh, S. K. (2021) · Molecular Neurobiology · doi:10.1007/s12035-021-02548-x · Cited by 32 · see citing works
Therapeutic perspective on vascular cognitive impairment
Toyama, K., Spin, J. M., Mogi, M., & Tsao, P. S. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2019.104266 · Cited by 31 · see citing works
Cao, Y., Liu, H., Zhang, J., & Dong, Y. (2020) · Artificial Cells Nanomedicine and Biotechnology · doi:10.1080/21691401.2020.1725536 · Cited by 29 · see citing works
MicroRNAs in the Blood-Brain Barrier in Hypoxic-Ischemic Brain Injury
Shen, G., & Ma, Q. (2020) · Current Neuropharmacology · doi:10.2174/1570159x18666200429004242 · Cited by 27 · see citing works
Self-citationPaz, A. A., & González‐Candia, A. (2022) · Biochemical Pharmacology · doi:10.1016/j.bcp.2022.115356 · Cited by 27 · see citing works
Jia, H., Qu, M., Fan, G., Wu, H., & Wang, L. (2019) · Neuroscience Research · doi:10.1016/j.neures.2019.12.002 · Cited by 26 · see citing works
Chen, A., Teng, C., Wei, J., Wu, X., Zhang, H., Chen, P., Cai, D., Qian, H., Zhu, H., Zheng, X., et al. (2025) · Gut Microbes · doi:10.1080/19490976.2025.2471015 · Cited by 25 · see citing works
Exosomes; multifaceted nanoplatform for targeting brain cancers
Mardi, N., Salahpour‐Anarjan, F., Nemati, M., Baher, N. S., Rahbarghazi, R., & Zarebkohan, A. (2023) · Cancer Letters · doi:10.1016/j.canlet.2023.216077 · Cited by 25 · see citing works
The Role of miR-210 in the Biological System: A Current Overview
Xu, H., Al-Ward, H., Shaher, F., Liu, C., & Liu, N. (2019) · Human Heredity · doi:10.1159/000509280 · Cited by 23 · see citing works
Li, Y., Song, R., Shen, G., Huang, L., Xiao, D., Ma, Q., & Zhang, L. (2023) · Stroke · doi:10.1161/strokeaha.122.041651 · Cited by 21 · see citing works
Self-citationWang, X., Zhou, H., Cheng, R., Zhou, X., Hou, X., Chen, J., & Qiu, J. (2020) · Molecular Brain · doi:10.1186/s13041-020-00579-4 · Cited by 20 · see citing works
Song, R., Hu, X., Romero, M., Holguin, M., Kagabo, W., Xiao, D., Wilson, S. M., & Zhang, L. (2020) · Cardiovascular Research · doi:10.1093/cvr/cvaa089 · Cited by 19 · see citing works
Self-citationMicroRNAs: Possible Regulatory Molecular Switch Controlling the BBB Microenvironment
Chakraborty, C., Sharma, A. R., Sharma, G., Bhattacharya, M., & Lee, S. (2020) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2019.12.024 · Cited by 18 · see citing works
Vázquez-Villaseñor, I., Smith, C. I., Thang, Y. J. R., Heath, P. R., Wharton, S. B., Blackburn, D. J., Ridger, V. C., & Simpson, J. E. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23115913 · Cited by 16 · see citing works
The Role of microRNAs in Epigenetic Regulation of Signaling Pathways in Neurological Pathologies
Tregub, P. P., Ibrahimli, I., Сергеевич, А. А., Salmina, A. B., Litvitskiy, P. F., Manasova, Z. S., & Popova, I. A. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241612899 · Cited by 16 · see citing works
Chen, R., Wang, M., Fu, S., Cao, F., Duan, P.-K., & Lu, J. (2019) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2019.7936 · Cited by 15 · see citing works
MicroRNA therapeutic targets in neonatal hypoxic–ischemic brain injury: a narrative review
Peeples, E. S. (2022) · Pediatric Research · doi:10.1038/s41390-022-02196-4 · Cited by 15 · see citing works
Targeting Non-Coding RNA for CNS Injuries: Regulation of Blood-Brain Barrier Functions
Zhang, L., Bai, W., Sun, L., Lin, Y., & Tian, M. (2023) · Neurochemical Research · doi:10.1007/s11064-023-03892-1 · Cited by 15 · see citing works
Self-citationMiceli, V., Russelli, G., Iannolo, G., Gallo, A., Re, V. L., Agnese, V., Sparacia, G., Conaldi, P. G., & Bulati, M. (2020) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2020.111332 · Cited by 14 · see citing works
Engineering extracellular vesicles to transiently permeabilize the blood–brain barrier
Tomatis, F., Rosa, S. C., Simões, S. M. N., Barão, M., Jesus, C., Novo, J. P., Barth, E., Marz, M., & Ferreira, L. (2024) · Journal of Nanobiotechnology · doi:10.1186/s12951-024-03019-w · Cited by 13 · see citing works
Cao, H., Baranova, A. V., Yue, W., Yu, H., Zhu, Z., Zhang, F., & Liu, D. (2020) · Frontiers in Genetics · doi:10.3389/fgene.2020.00149 · Cited by 13 · see citing works
Circulating MicroRNAs and Blood-Brain-Barrier Function in Breast Cancer Metastasis
Curtaz, C. J., Schmitt, C., Blecharz-Lang, K. G., Roewer, N., Wöckel, A., & Burek, M. (2020) · Current Pharmaceutical Design · doi:10.2174/1381612826666200316151720 · Cited by 13 · see citing works
Involvement of noncoding RNA in blood-brain barrier integrity in central nervous system disease
Liu, X., Shen, L., Han, B., & Yao, H. (2021) · Non-coding RNA Research · doi:10.1016/j.ncrna.2021.06.003 · Cited by 13 · see citing works
Role of miRNAs in neurovascular injury and repair
Sawant, H., Sun, B., Mcgrady, E., & Bihl, J. C. (2024) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x241254772 · Cited by 12 · see citing works
Regulatory Mechanism of MicroRNA-30b on Neonatal Hypoxic-Ischemic Encephalopathy (HIE)
Wang, W., & Jia, L. (2020) · Journal of Stroke and Cerebrovascular Diseases · doi:10.1016/j.jstrokecerebrovasdis.2020.105553 · Cited by 12 · see citing works
Li, Y., Chen, J., Tu, H., Ma, Q., Wang, M., Chen, M., & Chen, M. (2023) · BMC Complementary Medicine and Therapies · doi:10.1186/s12906-023-04195-2 · Cited by 11 · see citing works
Self-citationA simple novel approach for detecting blood–brain barrier permeability using GPCR internalization
Csaba, Z., Vitalis, T., Charriaut‐Marlangue, C., Margaill, I., Coqueran, B., Léger, P., Parente, I., Jacquens, A., Titomanlio, L., Constans, C., et al. (2020) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12665 · Cited by 10 · see citing works
Zhai, Y., Liu, B., Mo, X., Zou, M., Mei, X., Chen, W., Huang, G., & Wu, L. (2021) · The Kaohsiung Journal of Medical Sciences · doi:10.1002/kjm2.12486 · Cited by 9 · see citing works
Hypoxia ischemia results in blood brain barrier damage via AKT/GSK-3β/CREB pathway in neonatal rats
Liu, C., Wang, C., Zhang, H., Gao, X., Xiao, P., Yu, M., Wang, X., Wang, X., & Wang, X. (2023) · Brain Research · doi:10.1016/j.brainres.2023.148640 · Cited by 9 · see citing works
Deletion of hypoxia‐responsive microRNA‐210 results in a sex‐specific decrease in nephron number
Hemker, S. L., Cerqueira, D. M., Bodnar, A. J., Cargill, K. R., Clugston, A. S., Anslow, M. J., Sims‐Lucas, S., Kostka, D., & Ho, J. (2020) · The FASEB Journal · doi:10.1096/fj.201902767r · Cited by 8 · see citing works
LncRNA SNHG15 regulates hypoxic-ischemic brain injury via miR-153-3p/SETD7 axis.
Fu, J., Huang, Y., & Xian, L. (2022) · PubMed · doi:10.14670/hh-18-489 · Cited by 8 · see citing works
Figueroa, E. G., Caballero-Román, A., Grau, J. R. T., Carmona, M. M., Nardi-Ricart, A., & González‐Candia, A. (2022) · Current Research in Pharmacology and Drug Discovery · doi:10.1016/j.crphar.2022.100129 · Cited by 8 · see citing works
Klepper, S., Jung, S., Dittmann, L., Geppert, C. I., Hartmann, A., Beier, N. L., & Trollmann, R. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23158693 · Cited by 6 · see citing works
Sun, A., Blecharz-Lang, K. G., Małecki, A., Meybohm, P., Nowacka-Chmielewska, M. M., & Burek, M. (2022) · Frontiers in Drug Delivery · doi:10.3389/fddev.2022.1027098 · Cited by 6 · see citing works
Khan, M. S., Wong, G. L., Zhuang, C., Najjar, M. K., & Lo, H. (2024) · Frontiers in Oncology · doi:10.3389/fonc.2024.1436942 · Cited by 5 · see citing works
Yang, L., Zhang, L., Zhu, J. K., Wang, Y., Zou, N., Liu, Z., & Wang, Y. (2023) · International Journal of Experimental Pathology · doi:10.1111/iep.12475 · Cited by 4 · see citing works
Self-citationYang, X., Liao, K., Deng, I. B., & Zhang, L. (2022) · Ibrain · doi:10.1002/ibra.12067 · Cited by 3 · see citing works
Self-citationNiu, Y., Du, S. Z., & He, R. (2023) · Ibrain · doi:10.1002/ibra.12089 · Cited by 3 · see citing works
Zhang, L., Tian, Q., & Chunming, X. (2024) · Neuroscience · doi:10.1016/j.neuroscience.2024.09.029 · Cited by 2 · see citing works
Self-citationRole of MicroRNAs in Stroke Pathology and Recovery
Kumari, N., Abbas, M. S., Amin, F., Yadav, S., Naqvi, S., & Raza, S. S. (2022) · Springer eBooks · doi:10.1007/978-981-16-8562-0_9 · Cited by 2 · see citing works
MicroRNAs in Ischemic Stroke Pathophysiology: Special Emphasis on Early Molecular Events
Rajanikant, G. K., Gressèns, P., Nampoothiri, S. S., Surendran, G., & Bokobza, C. (2020) · Springer eBooks · doi:10.1007/978-981-15-4798-0_3 · Cited by 2 · see citing works
Metwally, N. G., Mohamad, S., & Bruchhaus, I. (2026) · Frontiers in Malaria · doi:10.3389/fmala.2026.1849845 · Cited by 1 · see citing works
Tregub, P. P. (2022) · Journal of Evolutionary Biochemistry and Physiology · doi:10.1134/s0022093022030127 · Cited by 1 · see citing works
Kong, X.-Y., Chen, D., Zhong, H., Qiao, R., Chen, S., Kasimu, A., Zhang, Y., Zhu, J., & Li, B. (2025) · World Journal of Traditional Chinese Medicine · doi:10.4103/wjtcm.wjtcm_101_24 · Cited by 1 · see citing works
Epigenetic Factors in Hypoxic-Ischemic Brain Affections in Children
Леонидович, С. П., Moscow, R. F., Chebanenko, N. V., & Romanov, P. A. (2021) · Doctor Ru · doi:10.31550/1727-2378-2021-20-10-68-72 · Cited by 1 · see citing works
Kubota, T. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19092720 · Cited by 1 · see citing works
Wang, T.-H., Bai, X., Xiong, L., Li, T., Fang, C., Xia, Q.-J., Wang, Q., & Yang, S. (2021) · Research Square · doi:10.21203/rs.3.rs-814664/v1
Application For Nanotechnology For the Treatment of Brain Diseases and Disorders
(2024) · Frontiers research topics · doi:10.3389/978-2-8325-5185-1
Li, M., Zhao, J., Cao, M., Liu, R., Chen, G., Li, S., Xie, Y., Xie, J., Cheng, Y., Huang, L., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12028617
Self-citationLi, Y., Chen, J., Tu, H., Ma, Q., Wang, M., Chen, J., & Chen, M. (2024) · Figshare · doi:10.6084/m9.figshare.26633094
Self-citationLi, M., Zhao, J., Cao, M., Liu, R., Chen, G., Li, S., Xie, Y., Xie, J., Cheng, Y., Huang, L., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12028608
Self-citationHu, S. X., Lopez-Robles, Y., Liu, E., Lin, Y., Chen, W., Manjunath, C., Zhao, Z., Zhang, L., & Ma, Q. (2026) · Fluids and Barriers of the CNS · doi:10.1186/s12987-025-00755-5
Self-citationDuarte, R., & Silva, A. C. A. (2026) · Next Nanotechnology · doi:10.1016/j.nxnano.2026.100813
- Authors
- Ma, Q., Dasgupta, C., Li, Y., Huang, L., & Zhang, L.
- Affiliations
- Loma Linda University (US)
- Center for Neonatal Biology, Division of Pharmacology, Department of Basic Sciences, School of Medicine, Loma Linda University, Loma Linda, CA 92350, USA
- Corresponding author
- Ma, Qingyi
- Venue
- International Journal of Molecular Sciences
- Publisher
- MDPI AG
- Published
- 2017-06-24
- Volume
- 18
- Issue
- 7
- Pages
- 1356
- ISSN
- 1422-0067 (ISSN-L)
- PMC
- PMC5535849
- OpenAlex
- W2642416886
- Cited by
- 76
- References
- 58
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 5 · 2023: 8 · 2022: 11 · 2021: 10 · 2020: 20 · 2019: 13 · 2018: 4
- FWCI
- 5.04
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- International Journal of Molecular Sciences (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- The Scholars Repository - LLU (Loma Linda University) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- eScholarship (California Digital Library) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Funders
- American Heart Association WSA winter 2015 Beginning Grant-in-Aid (15BGIA25750063)
- National Institutes of Health (HL118861)
- Topics
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Neonatal and fetal brain pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Keywords
- miR-210, blood-brain barrier integrity, hypoxic-ischemic brain injury, neonatal hypoxic-ischemic encephalopathy, cerebral edema, occludin, β-catenin, tight junction proteins, adherens junction proteins, neuroprotection, 3' untranslated region, Rice-Vannucci model
- MeSH terms
- Animals, Animals, Newborn, Blood-Brain Barrier, Brain Edema, Disease Models, Animal, Female, Gene Expression Regulation, Immunoglobulin G, Intercellular Junctions, Male, Permeability, Biomarkers, Hypoxia-Ischemia, Brain, RNA Interference, MicroRNAs, beta Catenin, Rats, Occludin
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