Login Register Cart 0
Generic placeholder image

Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Underlying Mechanisms and Potential Therapeutic Molecular Targets in Blood-Brain Barrier Disruption after Subarachnoid Hemorrhage

Author(s): Yuchen Li, Pei Wu, Ji C. Bihl* and Huaizhang Shi*

Volume 18, Issue 12, 2020

Page: [1168 - 1179] Pages: 12

DOI: 10.2174/1570159X18666200106154203

Price: $65

Abstract

Aneurysmal subarachnoid hemorrhage (aSAH) is a subtype of hemorrhagic stroke with significant morbidity and mortality. Aneurysmal bleeding causes elevated intracranial pressure, decreased cerebral blood flow, global cerebral ischemia, brain edema, blood component extravasation, and accumulation of breakdown products. These post-SAH injuries can disrupt the integrity and function of the blood-brain barrier (BBB), and brain tissues are directly exposed to the neurotoxic blood contents and immune cells, which leads to secondary brain injuries including inflammation and oxidative stress, and other cascades. Though the exact mechanisms are not fully clarified, multiple interconnected and/or independent signaling pathways have been reported to be involved in BBB disruption after SAH. In addition, alleviation of BBB disruption through various pathways or chemicals has a neuroprotective effect on SAH. Hence, BBB permeability plays an important role in the pathological course and outcomes of SAH. This review discusses the recent understandings of the underlying mechanisms and potential therapeutic targets in BBB disruption after SAH, emphasizing the dysfunction of tight junctions and endothelial cells in the development of BBB disruption. The emerging molecular targets, including toll-like receptor 4, netrin-1, lipocalin-2, tropomyosin-related kinase receptor B, and receptor tyrosine kinase ErbB4, are also summarized in detail. Finally, we discussed the emerging treatments for BBB disruption after SAH and put forward our perspectives on future research.

Keywords: Subarachnoid hemorrhage, early brain injury, blood-brain barrier, endothelial cell, tight junction, toll-like receptor 4.

« Previous Next »
Graphical Abstract

[1]
Connolly, E.S., Jr; Rabinstein, A.A.; Carhuapoma, J.R.; Derdeyn, C.P.; Dion, J.; Higashida, R.T.; Hoh, B.L.; Kirkness, C.J.; Naidech, A.M.; Ogilvy, C.S.; Patel, A.B.; Thompson, B.G.; Vespa, P. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/american Stroke Association. Stroke, 2012, 43(6), 1711-1737.
[http://dx.doi.org/10.1161/STR.0b013e3182587839]] [PMID: 22556195]
[2]
van Gijn, J.; Kerr, R.S.; Rinkel, G.J.E. Subarachnoid haemorrhage. Lancet, 2007, 369(9558), 306-318.
[http://dx.doi.org/10.1016/S0140-6736(07)60153-6] [PMID: 17258671]
[3]
Feigin, V.L.; Rinkel, G.J.; Lawes, C.M.; Algra, A.; Bennett, D.A.; van Gijn, J.; Anderson, C.S. Risk factors for subarachnoid hemorrhage: an updated systematic review of epidemiological studies. Stroke, 2005, 36(12), 2773-2780.
[http://dx.doi.org/10.1161/01.STR.0000190838.02954.e8] [PMID: 16282541]
[4]
Daou, B.J.; Koduri, S.; Thompson, B.G.; Chaudhary, N.; Pandey, A.S. Clinical and experimental aspects of aneurysmal subarachnoid hemorrhage. CNS Neurosci. Ther., 2019, 25(10), 1096-1112.
[http://dx.doi.org/10.1111/cns.13222] [PMID: 31583833]
[5]
Hong, C.M.; Tosun, C.; Kurland, D.B.; Gerzanich, V.; Schreibman, D.; Simard, J.M. Biomarkers as outcome predictors in subarachnoid hemorrhage--a systematic review. Biomarkers, 2014, 19(2), 95-108.
[6]
Sehba, F.A.; Hou, J.; Pluta, R.M.; Zhang, J.H. The importance of early brain injury after subarachnoid hemorrhage. Prog. Neurobiol., 2012, 97(1), 14-37.
[http://dx.doi.org/10.1016/j.pneurobio.2012.02.003] [PMID: 22414893]
[7]
Li, Z.; Liang, G.; Ma, T.; Li, J.; Wang, P.; Liu, L.; Yu, B.; Liu, Y.; Xue, Y. Blood-brain barrier permeability change and regulation mechanism after subarachnoid hemorrhage. Metab. Brain Dis., 2015, 30(2), 597-603.
[http://dx.doi.org/10.1007/s11011-014-9609-1] [PMID: 25270004]
[8]
Suzuki, H.; Fujimoto, M.; Kawakita, F.; Liu, L.; Nakatsuka, Y.; Nakano, F. Tenascin-C in brain injuries and edema after subarachnoid hemorrhage: Findings from basic and clinical studies. J. Neurosci. Res., 2018, 98(1), 42-56.
[PMID: 30242870]
[9]
Kahles, T.; Luedike, P.; Endres, M.; Galla, H.J.; Steinmetz, H.; Busse, R.; Neumann-Haefelin, T.; Brandes, R.P. NADPH oxidase plays a central role in blood-brain barrier damage in experimental stroke. Stroke, 2007, 38(11), 3000-3006.
[http://dx.doi.org/10.1161/STROKEAHA.107.489765] [PMID: 17916764]
[10]
Ivanidze, J.; Ferraro, R.A.; Giambrone, A.E.; Segal, A.Z.; Gupta, A.; Sanelli, P.C. Blood-brain barrier permeability in aneurysmal subarachnoid hemorrhage: Correlation with clinical outcomes. AJR Am. J. Roentgenol., 2018, 211(4), 891-895.
[http://dx.doi.org/10.2214/AJR.17.18237] [PMID: 30085836]
[11]
Lublinsky, S.; Major, S.; Kola, V.; Horst, V.; Santos, E.; Platz, J.; Sakowitz, O.; Scheel, M.; Dohmen, C.; Graf, R.; Vatter, H.; Wolf, S.; Vajkoczy, P.; Shelef, I.; Woitzik, J.; Martus, P.; Dreier, J.P.; Friedman, A. Early blood-brain barrier dysfunction predicts neurological outcome following aneurysmal subarachnoid hemorrhage. EBioMedicine, 2019, 43, 460-472.
[http://dx.doi.org/10.1016/j.ebiom.2019.04.054] [PMID: 31162113]
[12]
Germanò, A.; d’Avella, D.; Imperatore, C.; Caruso, G.; Tomasello, F. Time-course of blood-brain barrier permeability changes after experimental subarachnoid haemorrhage. Acta Neurochir. (Wien), 2000, 142(5), 575-580.
[http://dx.doi.org/10.1007/s007010050472] [PMID: 10898366]
[13]
Ivanidze, J.; Kesavabhotla, K.; Kallas, O.N.; Mir, D.; Baradaran, H.; Gupta, A.; Segal, A.Z.; Claassen, J.; Sanelli, P.C. Evaluating blood-brain barrier permeability in delayed cerebral infarction after aneurysmal subarachnoid hemorrhage. AJNR Am. J. Neuroradiol., 2015, 36(5), 850-854.
[http://dx.doi.org/10.3174/ajnr.A4207] [PMID: 25572949]
[14]
Abbott, N.J.; Rönnbäck, L.; Hansson, E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci., 2006, 7(1), 41-53.
[http://dx.doi.org/10.1038/nrn1824] [PMID: 16371949]
[15]
Ueno, M. Molecular anatomy of the brain endothelial barrier: an overview of the distributional features. Curr. Med. Chem., 2007, 14(11), 1199-1206.
[http://dx.doi.org/10.2174/092986707780597943] [PMID: 17504140]
[16]
Rhea, E.M.; Banks, W.A. Role of the Blood-Brain Barrier in Central Nervous System Insulin Resistance. Front. Neurosci., 2019, 13, 521.
[http://dx.doi.org/10.3389/fnins.2019.00521] [PMID: 31213970]
[17]
Tietz, S.; Engelhardt, B. Brain barriers: Crosstalk between complex tight junctions and adherens junctions. J. Cell Biol., 2015, 209(4), 493-506.
[http://dx.doi.org/10.1083/jcb.201412147] [PMID: 26008742]
[18]
Reese, T.S.; Karnovsky, M.J. Fine structural localization of a blood-brain barrier to exogenous peroxidase. J. Cell Biol., 1967, 34(1), 207-217.
[http://dx.doi.org/10.1083/jcb.34.1.207] [PMID: 6033532]
[19]
Deng, J.; Huang, Q.; Wang, F.; Liu, Y.; Wang, Z.; Wang, Z. The role of caveolin-1 in blood-brain barrier disruption induced by focused ultrasound combined with microbubbles J. Mol. Neurosci. MN, 2012, 46(3), 677-687.
[20]
Stamatovic, S.M.; Keep, R.F.; Andjelkovic, A.V. Brain endothelial cell-cell junctions: how to “open” the blood brain barrier. Curr. Neuropharmacol., 2008, 6(3), 179-192.
[http://dx.doi.org/10.2174/157015908785777210] [PMID: 19506719]
[21]
Lin, M.; Zhu, L.; Wang, J.; Xue, Y.; Shang, X. 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(3), 525-531.
[http://dx.doi.org/10.1016/j.bbrc.2019.07.075] [PMID: 31375213]
[22]
Kimura, I.; Dohgu, S.; Takata, F.; Matsumoto, J.; Kawahara, Y.; Nishihira, M.; Sakada, S.; Saisho, T.; Yamauchi, A.; Kataoka, Y. Activation of the α7 nicotinic acetylcholine receptor upregulates blood-brain barrier function through increased claudin-5 and occludin expression in rat brain endothelial cells. Neurosci. Lett., 2019, 694, 9-13.
[http://dx.doi.org/10.1016/j.neulet.2018.11.022] [PMID: 30452951]
[23]
Kealy, J.; Greene, C.; Campbell, M. Blood-brain barrier regulation in psychiatric disorders. Neurosci. Lett., 2018, •••133664
[http://dx.doi.org/10.1016/j.neulet.2018.06.033] [PMID: 29966749]
[24]
García-Cáceres, C.; Quarta, C.; Varela, L.; Gao, Y.; Gruber, T.; Legutko, B.; Jastroch, M.; Johansson, P.; Ninkovic, J.; Yi, C.X.; Le Thuc, O.; Szigeti-Buck, K.; Cai, W.; Meyer, C.W.; Pfluger, P.T.; Fernandez, A.M.; Luquet, S.; Woods, S.C.; Torres-Alemán, I.; Kahn, C.R.; Götz, M.; Horvath, T.L.; Tschöp, M.H. Astrocytic Insulin Signaling Couples Brain Glucose Uptake with Nutrient Availability. Cell, 2016, 166(4), 867-880.
[http://dx.doi.org/10.1016/j.cell.2016.07.028] [PMID: 27518562]
[25]
Alvarez, J.I.; Dodelet-Devillers, A.; Kebir, H.; Ifergan, I.; Fabre, P.J.; Terouz, S.; Sabbagh, M.; Wosik, K.; Bourbonnière, L.; Bernard, M.; van Horssen, J.; de Vries, H.E.; Charron, F.; Prat, A. The Hedgehog pathway promotes blood-brain barrier integrity and CNS immune quiescence. Science, 2011, 334(6063), 1727-1731.
[http://dx.doi.org/10.1126/science.1206936] [PMID: 22144466]
[26]
Bell, R.D.; Winkler, E.A.; Singh, I.; Sagare, A.P.; Deane, R.; Wu, Z.; Holtzman, D.M.; Betsholtz, C.; Armulik, A.; Sallstrom, J.; Berk, B.C.; Zlokovic, B.V. Apolipoprotein E controls cerebrovascular integrity via cyclophilin A. Nature, 2012, 485(7399), 512-516.
[http://dx.doi.org/10.1038/nature11087] [PMID: 22622580]
[27]
Yamazaki, Y.; Kanekiyo, T. Blood-Brain Barrier Dysfunction and the Pathogenesis of Alzheimer’s Disease. Int. J. Mol. Sci., 2017, 18(9)E1965
[http://dx.doi.org/10.3390/ijms18091965] [PMID: 28902142]
[28]
Daneman, R.; Prat, A. The blood-brain barrier. Cold Spring Harb. Perspect. Biol., 2015, 7(1)a020412
[http://dx.doi.org/10.1101/cshperspect.a020412] [PMID: 25561720]
[29]
Armulik, A.; Genové, G.; Mäe, M.; Nisancioglu, M.H.; Wallgard, E.; Niaudet, C.; He, L.; Norlin, J.; Lindblom, P.; Strittmatter, K.; Johansson, B.R.; Betsholtz, C. Pericytes regulate the blood-brain barrier. Nature, 2010, 468(7323), 557-561.
[http://dx.doi.org/10.1038/nature09522] [PMID: 20944627]
[30]
Bonkowski, D.; Katyshev, V.; Balabanov, R.D.; Borisov, A.; Dore-Duffy, P. The CNS microvascular pericyte: pericyte-astrocyte crosstalk in the regulation of tissue survival. Fluids Barriers CNS, 2011, 8(1), 8.
[http://dx.doi.org/10.1186/2045-8118-8-8] [PMID: 21349156]
[31]
Winkler, E.A.; Bell, R.D.; Zlokovic, B.V. Central nervous system pericytes in health and disease. Nat. Neurosci., 2011, 14(11), 1398-1405.
[http://dx.doi.org/10.1038/nn.2946] [PMID: 22030551]
[32]
Daneman, R.; Zhou, L.; Kebede, A.A.; Barres, B.A. Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature, 2010, 468(7323), 562-566.
[http://dx.doi.org/10.1038/nature09513] [PMID: 20944625]
[33]
Hamilton, N.B.; Attwell, D.; Hall, C.N. Pericyte-mediated regulation of capillary diameter: a component of neurovascular coupling in health and disease. Front. Neuroenergetics, 2010, 2, 2.
[http://dx.doi.org/10.3389/fnene.2010.00005] [PMID: 20725515]
[34]
Schlageter, K.E.; Molnar, P.; Lapin, G.D.; Groothuis, D.R. Microvessel organization and structure in experimental brain tumors: microvessel populations with distinctive structural and functional properties. Microvasc. Res., 1999, 58(3), 312-328.
[http://dx.doi.org/10.1006/mvre.1999.2188] [PMID: 10527772]
[35]
Zlokovic, B.V. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron, 2008, 57(2), 178-201.
[http://dx.doi.org/10.1016/j.neuron.2008.01.003] [PMID: 18215617]
[36]
Morris, A.W.; Carare, R.O.; Schreiber, S.; Hawkes, C.A. The cerebrovascular basement membrane: Role in the clearance of β-amyloid and cerebral amyloid angiopathy. Front. Aging Neurosci., 2014, 6, 251.
[http://dx.doi.org/10.3389/fnagi.2014.00251] [PMID: 25285078]
[37]
Yousif, L.F.; Di Russo, J.; Sorokin, L. Laminin isoforms in endothelial and perivascular basement membranes. Cell Adhes. Migr., 2013, 7(1), 101-110.
[http://dx.doi.org/10.4161/cam.22680] [PMID: 23263631]
[38]
Baeten, K.M.; Akassoglou, K. Extracellular matrix and matrix receptors in blood-brain barrier formation and stroke. Dev. Neurobiol., 2011, 71(11), 1018-1039.
[http://dx.doi.org/10.1002/dneu.20954] [PMID: 21780303]
[39]
Tilling, T.; Korte, D.; Hoheisel, D.; Galla, H.J. Basement membrane proteins influence brain capillary endothelial barrier function in vitro. J. Neurochem., 1998, 71(3), 1151-1157.
[http://dx.doi.org/10.1046/j.1471-4159.1998.71031151.x] [PMID: 9721740]
[40]
Gu, H.; Fei, Z.H.; Wang, Y.Q.; Yang, J.G.; Zhao, C.H.; Cai, Y.; Zhong, X.M. Angiopoietin-1 and Angiopoietin-2 Expression Imbalance Influence in Early Period After Subarachnoid Hemorrhage. Int. Neurourol. J., 2016, 20(4), 288-295.
[http://dx.doi.org/10.5213/inj.1632692.346] [PMID: 28043115]
[41]
Ostrowski, R.P.; Colohan, A.R.; Zhang, J.H. Molecular mechanisms of early brain injury after subarachnoid hemorrhage. Neurol. Res., 2006, 28(4), 399-414.
[http://dx.doi.org/10.1179/016164106X115008] [PMID: 16759443]
[42]
Song, J.N.; Chen, H.; Zhang, M.; Zhao, Y.L.; Ma, X.D. Dynamic change in cerebral microcirculation and focal cerebral metabolism in experimental subarachnoid hemorrhage in rabbits. Metab. Brain Dis., 2013, 28(1), 33-43.
[http://dx.doi.org/10.1007/s11011-012-9369-8] [PMID: 23232626]
[43]
Russin, J.J.; Montagne, A.; D’Amore, F.; He, S.; Shiroishi, M.S.; Rennert, R.C.; Depetris, J.; Zlokovic, B.V.; Mack, W.J. Permeability imaging as a predictor of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. J. Cereb. Blood Flow Metab., 2018, 38(6), 973-979.
[http://dx.doi.org/10.1177/0271678X18768670] [PMID: 29611451]
[44]
Suzuki, H.; Nakano, F. To Improve Translational Research in Subarachnoid Hemorrhage. Transl. Stroke Res., 2018, 9(1), 1-3.
[http://dx.doi.org/10.1007/s12975-017-0546-2] [PMID: 28620886]
[45]
Marbacher, S. Grüter, B.; Schöpf, S.; Croci, D.; Nevzati, E.; D’Alonzo, D.; Lattmann, J.; Roth, T.; Bircher, B.; Wolfert, C.; Muroi, C.; Dutilh, G.; Widmer, H.R.; Fandino, J. Systematic Review of In Vivo Animal Models of Subarachnoid Hemorrhage: Species, Standard Parameters, and Outcomes. Transl. Stroke Res., 2018. [Epub ahead of print]
[PMID: 30209798]
[46]
Schwartz, A.Y.; Masago, A.; Sehba, F.A.; Bederson, J.B. Experimental models of subarachnoid hemorrhage in the rat: a refinement of the endovascular filament model. J. Neurosci. Methods, 2000, 96(2), 161-167.
[http://dx.doi.org/10.1016/S0165-0270(00)00156-4] [PMID: 10720681]
[47]
Sugawara, T.; Ayer, R.; Jadhav, V.; Zhang, J.H. A new grading system evaluating bleeding scale in filament perforation subarachnoid hemorrhage rat model. J. Neurosci. Methods, 2008, 167(2), 327-334.
[http://dx.doi.org/10.1016/j.jneumeth.2007.08.004] [PMID: 17870179]
[48]
Jiang, X.; Andjelkovic, A.V.; Zhu, L.; Yang, T.; Bennett, M.V.L.; Chen, J.; Keep, R.F.; Shi, Y. Blood-brain barrier dysfunction and recovery after ischemic stroke. Prog. Neurobiol., 2018, 163-164, 144-171.
[http://dx.doi.org/10.1016/j.pneurobio.2017.10.001] [PMID: 28987927]
[49]
Keep, R.F.; Zhou, N.; Xiang, J.; Andjelkovic, A.V.; Hua, Y.; Xi, G. Vascular disruption and blood-brain barrier dysfunction in intracerebral hemorrhage. Fluids Barriers CNS, 2014, 11, 18.
[http://dx.doi.org/10.1186/2045-8118-11-18] [PMID: 25120903]
[50]
Wang, K.C.; Tang, S.C.; Lee, J.E.; Li, Y.I.; Huang, Y.S.; Yang, W.S.; Jeng, J.S.; Arumugam, T.V.; Tu, Y.K. Cerebrospinal fluid high mobility group box 1 is associated with neuronal death in subarachnoid hemorrhage. J. Cereb. Blood Flow Metab., 2017, 37(2), 435-443.
[http://dx.doi.org/10.1177/0271678X16629484] [PMID: 26823474]
[51]
Suzuki, H. What is early brain injury? Transl. Stroke Res., 2015, 6(1), 1-3.
[http://dx.doi.org/10.1007/s12975-014-0380-8] [PMID: 25502277]
[52]
de Oliveira Manoel, A.L.; Goffi, A.; Zampieri, F.G.; Turkel-Parrella, D.; Duggal, A.; Marotta, T.R.; Macdonald, R.L.; Abrahamson, S. The critical care management of spontaneous intracranial hemorrhage: a contemporary review. Crit. Care, 2016, 20, 272.
[http://dx.doi.org/10.1186/s13054-016-1432-0] [PMID: 27640182]
[53]
Komotar, R.J.; Schmidt, J.M.; Starke, R.M.; Claassen, J.; Wartenberg, K.E.; Lee, K.; Badjatia, N.; Connolly, E.S., Jr; Mayer, S.A. Resuscitation and critical care of poor-grade subarachnoid hemorrhage. Neurosurgery, 2009, 64(3), 397-410.
[http://dx.doi.org/10.1227/01.NEU.0000338946.42939.C7] [PMID: 19240601]
[54]
Sun, X.G.; Duan, H.; Jing, G.; Wang, G.; Hou, Y.; Zhang, M. Inhibition of TREM-1 attenuates early brain injury after subarachnoid hemorrhage via downregulation of p38MAPK/MMP-9 and preservation of ZO-1. Neuroscience, 2019, 406, 369-375.
[http://dx.doi.org/10.1016/j.neuroscience.2019.03.032] [PMID: 30910643]
[55]
Chow, B.W.; Gu, C. The molecular constituents of the blood-brain barrier. Trends Neurosci., 2015, 38(10), 598-608.
[http://dx.doi.org/10.1016/j.tins.2015.08.003] [PMID: 26442694]
[56]
Fujimoto, M.; Shiba, M.; Kawakita, F.; Liu, L.; Shimojo, N.; Imanaka-Yoshida, K.; Yoshida, T.; Suzuki, H. Effects of Tenascin-C Knockout on Cerebral Vasospasm After Experimental Subarachnoid Hemorrhage in Mice. Mol. Neurobiol., 2018, 55(3), 1951-1958.
[http://dx.doi.org/10.1007/s12035-017-0466-x] [PMID: 28244007]
[57]
Chen, S.; Feng, H.; Sherchan, P.; Klebe, D.; Zhao, G.; Sun, X.; Zhang, J.; Tang, J.; Zhang, J.H. Controversies and evolving new mechanisms in subarachnoid hemorrhage. Prog. Neurobiol., 2014, 115, 64-91.
[http://dx.doi.org/10.1016/j.pneurobio.2013.09.002] [PMID: 24076160]
[58]
Peeyush Kumar, T.; McBride, D.W.; Dash, P.K.; Matsumura, K.; Rubi, A.; Blackburn, S.L. Endothelial Cell Dysfunction and Injury in Subarachnoid Hemorrhage. Mol. Neurobiol., 2019, 56(3), 1992-2006.
[http://dx.doi.org/10.1007/s12035-018-1213-7] [PMID: 29982982]
[59]
Qi, X.; Liu, J.; Wu, J.; Bi, Y.; Han, C.; Zhang, G.; Lou, M.; Lu, J.; Tang, J. Initiating TrkB/Akt Signaling Cascade Preserves Blood-Brain Barrier after Subarachnoid Hemorrhage in Rats. Cell Transplant., 2019, 28(8), 1002-1008.
[http://dx.doi.org/10.1177/0963689719857649] [PMID: 31208230]
[60]
Caner, B.; Hou, J.; Altay, O.; Fujii, M.; Zhang, J.H. Transition of research focus from vasospasm to early brain injury after subarachnoid hemorrhage. J. Neurochem., 2012, 123(Suppl. 2), 12-21.
[http://dx.doi.org/10.1111/j.1471-4159.2012.07939.x] [PMID: 23050638]
[61]
Keep, R.F.; Andjelkovic, A.V.; Xiang, J.; Stamatovic, S.M.; Antonetti, D.A.; Hua, Y.; Xi, G. Brain endothelial cell junctions after cerebral hemorrhage: Changes, mechanisms and therapeutic targets. J. Cereb. Blood Flow Metab., 2018, 38(8), 1255-1275.
[http://dx.doi.org/10.1177/0271678X18774666] [PMID: 29737222]
[62]
Simard, J.M.; Geng, Z.; Woo, S.K.; Ivanova, S.; Tosun, C.; Melnichenko, L.; Gerzanich, V. Glibenclamide reduces inflammation, vasogenic edema, and caspase-3 activation after subarachnoid hemorrhage. J. Cereb. Blood Flow Metab., 2009, 29(2), 317-330.
[http://dx.doi.org/10.1038/jcbfm.2008.120] [PMID: 18854840]
[63]
Wang, Z; Meng, CJ; Shen, XM; Shu, Z; Ma, C; Zhu, GQ Potential contribution of hypoxia-inducible factor-1alpha, aquaporin-4, and matrix metalloproteinase-9 to blood-brain barrier disruption and brain edema after experimental subarachnoid hemorrhage Journal of molecular neuroscience : MN 2012, 48(1), 273-280.
[64]
Chen, D.; Wei, X.T.; Guan, J.H.; Yuan, J.W.; Peng, Y.T.; Song, L.; Liu, Y.H. Inhibition of c-Jun N-terminal kinase prevents blood-brain barrier disruption and normalizes the expression of tight junction proteins clautin-5 and ZO-1 in a rat model of subarachnoid hemorrhage. Acta Neurochir. (Wien), 2012, 154(8), 1469-1476.
[http://dx.doi.org/10.1007/s00701-012-1328-y] [PMID: 22661329]
[65]
Altay, O.; Suzuki, H.; Hasegawa, Y.; Caner, B.; Krafft, P.R.; Fujii, M.; Tang, J.; Zhang, J.H. Isoflurane attenuates blood-brain barrier disruption in ipsilateral hemisphere after subarachnoid hemorrhage in mice. Stroke, 2012, 43(9), 2513-2516.
[http://dx.doi.org/10.1161/STROKEAHA.112.661728] [PMID: 22773559]
[66]
Chen, J.; Chen, G.; Li, J.; Qian, C.; Mo, H.; Gu, C.; Yan, F.; Yan, W.; Wang, L. Melatonin attenuates inflammatory response-induced brain edema in early brain injury following a subarachnoid hemorrhage: a possible role for the regulation of pro-inflammatory cytokines. J. Pineal Res., 2014, 57(3), 340-347.
[http://dx.doi.org/10.1111/jpi.12173] [PMID: 25187344]
[67]
Chen, Y.; Zhang, Y.; Tang, J.; Liu, F.; Hu, Q.; Luo, C.; Tang, J.; Feng, H.; Zhang, J.H. Norrin protected blood-brain barrier via frizzled-4/β-catenin pathway after subarachnoid hemorrhage in rats. Stroke, 2015, 46(2), 529-536.
[http://dx.doi.org/10.1161/STROKEAHA.114.007265] [PMID: 25550365]
[68]
Xu, T.; Zhang, W.G.; Sun, J.; Zhang, Y.; Lu, J.F.; Han, H.B.; Zhou, C.M.; Yan, J.H. Protective effects of thrombomodulin on microvascular permeability after subarachnoid hemorrhage in mouse model. Neuroscience, 2015, 299, 18-27.
[http://dx.doi.org/10.1016/j.neuroscience.2015.04.058] [PMID: 25936678]
[69]
Zhou, C.; Xie, G.; Wang, C.; Zhang, Z.; Chen, Q.; Zhang, L.; Wu, L.; Wei, Y.; Ding, H.; Hang, C.; Zhou, M.; Shi, J. Decreased progranulin levels in patients and rats with subarachnoid hemorrhage: a potential role in inhibiting inflammation by suppressing neutrophil recruitment. J. Neuroinflammation, 2015, 12, 200.
[http://dx.doi.org/10.1186/s12974-015-0415-4] [PMID: 26527034]
[70]
Zhou, C.H.; Wang, C.X.; Xie, G.B.; Wu, L.Y.; Wei, Y.X.; Wang, Q.; Zhang, H.S.; Hang, C.H.; Zhou, M.L.; Shi, J.X. Fisetin alleviates early brain injury following experimental subarachnoid hemorrhage in rats possibly by suppressing TLR 4/NF-κB signaling pathway. Brain Res., 2015, 1629, 250-259.
[http://dx.doi.org/10.1016/j.brainres.2015.10.016] [PMID: 26475978]
[71]
Chen, T.; Wang, W.; Li, J.R.; Xu, H.Z.; Peng, Y.C.; Fan, L.F.; Yan, F.; Gu, C.; Wang, L.; Chen, G. PARP inhibition attenuates early brain injury through NF-κB/MMP-9 pathway in a rat model of subarachnoid hemorrhage. Brain Res., 2016, 1644, 32-38.
[http://dx.doi.org/10.1016/j.brainres.2016.05.005] [PMID: 27157545]
[72]
Fujimoto, M.; Shiba, M.; Kawakita, F.; Liu, L.; Shimojo, N.; Imanaka-Yoshida, K.; Yoshida, T.; Suzuki, H. Deficiency of tenascin-C and attenuation of blood-brain barrier disruption following experimental subarachnoid hemorrhage in mice. J. Neurosurg., 2016, 124(6), 1693-1702.
[http://dx.doi.org/10.3171/2015.4.JNS15484] [PMID: 26473781]
[73]
Fang, R.; Zheng, X.; Zhang, M. Ethyl pyruvate alleviates early brain injury following subarachnoid hemorrhage in rats. Acta Neurochir. (Wien), 2016, 158(6), 1069-1076.
[http://dx.doi.org/10.1007/s00701-016-2795-3] [PMID: 27072679]
[74]
Ying, G.Y.; Jing, C.H.; Li, J.R.; Wu, C.; Yan, F.; Chen, J.Y.; Wang, L.; Dixon, B.J.; Chen, G. Neuroprotective Effects of Valproic Acid on Blood-Brain Barrier Disruption and Apoptosis-Related Early Brain Injury in Rats Subjected to Subarachnoid Hemorrhage Are Modulated by Heat Shock Protein 70/Matrix Metalloproteinases and Heat Shock Protein 70/AKT Pathways. Neurosurgery, 2016, 79(2), 286-295.
[http://dx.doi.org/10.1227/NEU.0000000000001264] [PMID: 27244466]
[75]
Liu, X.; Zhang, X.; Ma, K.; Zhang, R.; Hou, P.; Sun, B.; Yuan, S.; Wang, Z.; Liu, Z. Matrine alleviates early brain injury after experimental subarachnoid hemorrhage in rats: possible involvement of PI3K/Akt-mediated NF-κB inhibition and Keap1/Nrf2-dependent HO-1 inductionn. Cell. Mol. Biol., 2016, 62(11), 38-44.
[PMID: 27755950]
[76]
Pang, J.; Wu, Y.; Peng, J.; Yang, P.; Kuai, L.; Qin, X.; Cao, F.; Sun, X.; Chen, L.; Vitek, M.P.; Jiang, Y. Potential implications of Apolipoprotein E in early brain injury after experimental subarachnoid hemorrhage: Involvement in the modulation of blood-brain barrier integrity. Oncotarget, 2016, 7(35), 56030-56044.
[http://dx.doi.org/10.18632/oncotarget.10821] [PMID: 27463015]
[77]
Yuan, J.; Liu, W.; Zhu, H.; Zhang, X.; Feng, Y.; Chen, Y.; Feng, H.; Lin, J. Curcumin attenuates blood-brain barrier disruption after subarachnoid hemorrhage in mice. J. Surg. Res., 2017, 207, 85-91.
[http://dx.doi.org/10.1016/j.jss.2016.08.090] [PMID: 27979493]
[78]
Fan, R.; Enkhjargal, B.; Camara, R.; Yan, F.; Gong, L. ShengtaoYao; Tang, J.; Chen, Y.; Zhang, J.H. Critical role of EphA4 in early brain injury after subarachnoid hemorrhage in rat. Exp. Neurol., 2017, 296, 41-48.
[http://dx.doi.org/10.1016/j.expneurol.2017.07.003] [PMID: 28698029]
[79]
Qian, H.; Dou, Z.; Ruan, W.; He, P.; Zhang, J.H.; Yan, F. ErbB4 Preserves Blood-Brain Barrier Integrity via the YAP/PIK3CB Pathway After Subarachnoid Hemorrhage in Rats. Front. Neurosci., 2018, 12, 492.
[http://dx.doi.org/10.3389/fnins.2018.00492] [PMID: 30087588]
[80]
Friedrich, V.; Flores, R.; Sehba, F.A. Cell death starts early after subarachnoid hemorrhage. Neurosci. Lett., 2012, 512(1), 6-11.
[http://dx.doi.org/10.1016/j.neulet.2012.01.036] [PMID: 22306092]
[81]
Ayer, RE; Zhang, JH Oxidative stress in subarachnoid haemorrhage: significance in acute brain injury and vasospasm Acta neurochirurgica Supplement, 2008, 104, 33-41.
[82]
Okada, T.; Suzuki, H. Toll-like receptor 4 as a possible therapeutic target for delayed brain injuries after aneurysmal subarachnoid hemorrhage. Neural Regen. Res., 2017, 12(2), 193-196.
[http://dx.doi.org/10.4103/1673-5374.200795] [PMID: 28400792]
[83]
Chen, G.; Zhang, S.; Shi, J.; Ai, J.; Hang, C. Effects of recombinant human erythropoietin (rhEPO) on JAK2/STAT3 pathway and endothelial apoptosis in the rabbit basilar artery after subarachnoid hemorrhage. Cytokine, 2009, 45(3), 162-168.
[http://dx.doi.org/10.1016/j.cyto.2008.11.015] [PMID: 19144539]
[84]
Singhal, A.K.; Symons, J.D.; Boudina, S.; Jaishy, B.; Shiu, Y.T. Role of Endothelial Cells in Myocardial Ischemia-Reperfusion Injury. Vasc. Dis. Prev., 2010, 7, 1-14.
[http://dx.doi.org/10.2174/1874120701007010001] [PMID: 25558187]
[85]
Sabri, M.; Ai, J.; Macdonald, R.L. Dissociation of vasospasm and secondary effects of experimental subarachnoid hemorrhage by clazosentan. Stroke, 2011, 42(5), 1454-1460.
[http://dx.doi.org/10.1161/STROKEAHA.110.604728] [PMID: 21454820]
[86]
Shamir, A.; Kwon, O.B.; Karavanova, I.; Vullhorst, D.; Leiva-Salcedo, E.; Janssen, M.J.; Buonanno, A. The importance of the NRG-1/ErbB4 pathway for synaptic plasticity and behaviors associated with psychiatric disorders. J. Neurosci., 2012, 32(9), 2988-2997.
[http://dx.doi.org/10.1523/JNEUROSCI.1899-11.2012] [PMID: 22378872]
[87]
Lok, J.; Sardi, S.P.; Guo, S.; Besancon, E.; Ha, D.M.; Rosell, A.; Kim, W.J.; Corfas, G.; Lo, E.H. Neuregulin-1 signaling in brain endothelial cells. J. Cereb. Blood Flow Metab., 2009, 29(1), 39-43.
[http://dx.doi.org/10.1038/jcbfm.2008.94] [PMID: 18728681]
[88]
Zhao, X.; Peng, X.; Sun, S.; Park, A.Y.; Guan, J.L. Role of kinase-independent and -dependent functions of FAK in endothelial cell survival and barrier function during embryonic development. J. Cell Biol., 2010, 189(6), 955-965.
[http://dx.doi.org/10.1083/jcb.200912094] [PMID: 20530207]
[89]
Xie, Z.; Enkhjargal, B.; Reis, C.; Huang, L.; Wan, W.; Tang, J.; Cheng, Y.; Zhang, J.H. Netrin-1 Preserves Blood-Brain Barrier Integrity Through Deleted in Colorectal Cancer/Focal Adhesion Kinase/RhoA Signaling Pathway Following Subarachnoid Hemorrhage in Rats. J. Am. Heart Assoc., 2017, 6(5)e005198
[http://dx.doi.org/10.1161/JAHA.116.005198] [PMID: 28526701]
[90]
Podjaski, C.; Alvarez, J.I.; Bourbonniere, L.; Larouche, S.; Terouz, S.; Bin, J.M.; Lécuyer, M.A.; Saint-Laurent, O.; Larochelle, C.; Darlington, P.J.; Arbour, N.; Antel, J.P.; Kennedy, T.E.; Prat, A. Netrin 1 regulates blood-brain barrier function and neuroinflammation. Brain, 2015, 138(Pt 6), 1598-1612.
[http://dx.doi.org/10.1093/brain/awv092] [PMID: 25903786]
[91]
Wen, J.; Qian, S.; Yang, Q.; Deng, L.; Mo, Y.; Yu, Y. Overexpression of netrin-1 increases the expression of tight junction-associated proteins, claudin-5, occludin, and ZO-1, following traumatic brain injury in rats. Exp. Ther. Med., 2014, 8(3), 881-886.
[http://dx.doi.org/10.3892/etm.2014.1818] [PMID: 25120618]
[92]
Aijaz, S.; Balda, M.S.; Matter, K. Tight junctions: molecular architecture and function. Int. Rev. Cytol., 2006, 248, 261-298.
[http://dx.doi.org/10.1016/S0074-7696(06)48005-0] [PMID: 16487793]
[93]
Fujii, M.; Duris, K.; Altay, O.; Soejima, Y.; Sherchan, P.; Zhang, J.H. Inhibition of Rho kinase by hydroxyfasudil attenuates brain edema after subarachnoid hemorrhage in rats. Neurochem. Int., 2012, 60(3), 327-333.
[http://dx.doi.org/10.1016/j.neuint.2011.12.014] [PMID: 22226843]
[94]
Kondo, T.; Hafezi-Moghadam, A.; Thomas, K.; Wagner, D.D.; Kahn, C.R. Mice lacking insulin or insulin-like growth factor 1 receptors in vascular endothelial cells maintain normal blood-brain barrier. Biochem. Biophys. Res. Commun., 2004, 317(2), 315-320.
[http://dx.doi.org/10.1016/j.bbrc.2004.03.043] [PMID: 15063759]
[95]
Guo, Z.; Sun, X.; He, Z.; Jiang, Y.; Zhang, X.; Zhang, J.H. Matrix metalloproteinase-9 potentiates early brain injury after subarachnoid hemorrhage. Neurol. Res., 2010, 32(7), 715-720.
[http://dx.doi.org/10.1179/016164109X12478302362491] [PMID: 19703360]
[96]
Suzuki, H.; Ayer, R.; Sugawara, T.; Chen, W.; Sozen, T.; Hasegawa, Y.; Kanamaru, K.; Zhang, J.H. Protective effects of recombinant osteopontin on early brain injury after subarachnoid hemorrhage in rats. Crit. Care Med., 2010, 38(2), 612-618.
[http://dx.doi.org/10.1097/CCM.0b013e3181c027ae] [PMID: 19851092]
[97]
Okada, T.; Kawakita, F.; Nishikawa, H.; Nakano, F.; Liu, L.; Suzuki, H. Selective Toll-Like Receptor 4 Antagonists Prevent Acute Blood-Brain Barrier Disruption After Subarachnoid Hemorrhage in Mice. Mol. Neurobiol., 2019, 56(2), 976-985.
[http://dx.doi.org/10.1007/s12035-018-1145-2] [PMID: 29855971]
[98]
Liu, L.; Kawakita, F.; Fujimoto, M.; Nakano, F.; Imanaka-Yoshida, K.; Yoshida, T.; Suzuki, H. Role of Periostin in Early Brain Injury After Subarachnoid Hemorrhage in Mice. Stroke, 2017, 48(4), 1108-1111.
[http://dx.doi.org/10.1161/STROKEAHA.117.016629] [PMID: 28242775]
[99]
Nishikawa, H.; Suzuki, H. Implications of periostin in the development of subarachnoid hemorrhage-induced brain injuries. Neural Regen. Res., 2017, 12(12), 1982-1984.
[http://dx.doi.org/10.4103/1673-5374.221150] [PMID: 29323034]
[100]
Shiba, M.; Suzuki, H. Lessons from tenascin-C knockout mice and potential clinical application to subarachnoid hemorrhage. Neural Regen. Res., 2019, 14(2), 262-264.
[http://dx.doi.org/10.4103/1673-5374.244789] [PMID: 30531008]
[101]
Nakatsuka, Y.; Shiba, M.; Nishikawa, H.; Terashima, M.; Kawakita, F.; Fujimoto, M.; Suzuki, H. pSEED group. Acute-Phase Plasma Osteopontin as an Independent Predictor for Poor Outcome After Aneurysmal Subarachnoid Hemorrhage. Mol. Neurobiol., 2018, 55(8), 6841-6849.
[http://dx.doi.org/10.1007/s12035-018-0893-3] [PMID: 29353454]
[102]
Nishikawa, H.; Liu, L.; Nakano, F.; Kawakita, F.; Kanamaru, H.; Nakatsuka, Y.; Okada, T.; Suzuki, H. Modified Citrus Pectin Prevents Blood-Brain Barrier Disruption in Mouse Subarachnoid Hemorrhage by Inhibiting Galectin-3. Stroke, 2018, 49(11), 2743-2751.
[http://dx.doi.org/10.1161/STROKEAHA.118.021757] [PMID: 30355205]
[103]
Suzuki, H.; Hasegawa, Y.; Kanamaru, K.; Zhang, J.H. Mechanisms of osteopontin-induced stabilization of blood-brain barrier disruption after subarachnoid hemorrhage in rats. Stroke, 2010, 41(8), 1783-1790.
[http://dx.doi.org/10.1161/STROKEAHA.110.586537] [PMID: 20616319]
[104]
Suzuki, H.; Nishikawa, H.; Kawakita, F. Matricellular proteins as possible biomarkers for early brain injury after aneurysmal subarachnoid hemorrhage. Neural Regen. Res., 2018, 13(7), 1175-1178.
[http://dx.doi.org/10.4103/1673-5374.235022] [PMID: 30028318]
[105]
Shao, A.; Zhou, Y.; Yao, Y.; Zhang, W.; Zhang, J.; Deng, Y. The role and therapeutic potential of heat shock proteins in haemorrhagic stroke. J. Cell. Mol. Med., 2019, 23(9), 5846-5858.
[http://dx.doi.org/10.1111/jcmm.14479] [PMID: 31273911]
[106]
Nag, S.; Manias, J.L.; Stewart, D.J. Pathology and new players in the pathogenesis of brain edema. Acta Neuropathol., 2009, 118(2), 197-217.
[http://dx.doi.org/10.1007/s00401-009-0541-0] [PMID: 19404652]
[107]
Toyota, Y.; Wei, J.; Xi, G.; Keep, R.F.; Hua, Y. White matter T2 hyperintensities and blood-brain barrier disruption in the hyperacute stage of subarachnoid hemorrhage in male mice: The role of lipocalin-2. CNS Neurosci. Ther., 2019, 25(10), 1207-1214.
[http://dx.doi.org/10.1111/cns.13221] [PMID: 31568658]
[108]
Xu, W.; Gao, L.; Li, T.; Zheng, J.; Shao, A.; Zhang, J. Apelin-13 Alleviates Early Brain Injury after Subarachnoid Hemorrhage via Suppression of Endoplasmic Reticulum Stress-mediated Apoptosis and Blood-Brain Barrier Disruption: Possible Involvement of ATF6/CHOP Pathway. Neuroscience, 2018, 388, 284-296.
[http://dx.doi.org/10.1016/j.neuroscience.2018.07.023] [PMID: 30036660]
[109]
Tran, K.A.; Zhang, X.; Predescu, D.; Huang, X.; Machado, R.F.; Göthert, J.R.; Malik, A.B.; Valyi-Nagy, T.; Zhao, Y.Y. Endothelial β-Catenin Signaling Is Required for Maintaining Adult Blood-Brain Barrier Integrity and Central Nervous System Homeostasis. Circulation, 2016, 133(2), 177-186.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.115.015982] [PMID: 26538583]
[110]
Zuo, S.; Ge, H.; Li, Q.; Zhang, X.; Hu, R.; Hu, S.; Liu, X.; Zhang, J.H.; Chen, Y.; Feng, H. Artesunate Protected Blood-Brain Barrier via Sphingosine 1 Phosphate Receptor 1/Phosphatidylinositol 3 Kinase Pathway After Subarachnoid Hemorrhage in Rats. Mol. Neurobiol., 2017, 54(2), 1213-1228.
[http://dx.doi.org/10.1007/s12035-016-9732-6] [PMID: 26820677]
[111]
Shang, S.; Hua, F.; Hu, Z.W. The regulation of β-catenin activity and function in cancer: therapeutic opportunities. Oncotarget, 2017, 8(20), 33972-33989.
[http://dx.doi.org/10.18632/oncotarget.15687] [PMID: 28430641]

Rights & Permissions Print Cite
Article Metrics
27
© 2024 Bentham Science Publishers | Privacy Policy