The Dual Role of Microglia in Blood-Brain Barrier Dysfunction after Stroke

Author(s): Ruiqing Kang, Marcin Gamdzyk, Cameron Lenahan, Jiping Tang, Sheng Tan*, John H. Zhang*

Journal Name: Current Neuropharmacology

Volume 18 , Issue 12 , 2020


Become EABM
Become Reviewer
Call for Editor

Graphical Abstract:


Abstract:

It is well-known that stroke is one of the leading causes of death and disability all over the world. After a stroke, the blood-brain barrier subsequently breaks down. The BBB consists of endothelial cells surrounded by astrocytes. Microglia, considered the long-living resident immune cells of the brain, play a vital role in BBB function. M1 microglia worsen BBB disruption, while M2 microglia assist in repairing BBB damage. Microglia can also directly interact with endothelial cells and affect BBB permeability. In this review, we are going to discuss the mechanisms responsible for the dual role of microglia in BBB dysfunction after stroke.

Keywords: Blood-brain barrier, stroke, microglia, polarization, inflammation, endothelial cells.

[1]
Villanueva, M.T. Repurposing CCR5 inhibitors for stroke recovery. Nat. Rev. Drug Discov., 2019. Epub ahead of print
[http://dx.doi.org/10.1038/d41573-019-00038-3] [PMID: 30936507]
[2]
Webb, R.L.; Kaiser, E.E.; Scoville, S.L.; Thompson, T.A.; Fatima, S.; Pandya, C.; Sriram, K.; Swetenburg, R.L.; Vaibhav, K.; Arbab, A.S.; Baban, B.; Dhandapani, K.M.; Hess, D.C.; Hoda, M.N.; Stice, S.L. Human Neural Stem Cell Extracellular Vesicles Improve Tissue and Functional Recovery in the Murine Thromboembolic Stroke Model. Transl. Stroke Res., 2018, 9(5), 530-539.
[http://dx.doi.org/10.1007/s12975-017-0599-2] [PMID: 29285679]
[3]
Flemming, A. Calming inflammation to prevent stroke damage. Nat. Rev. Immunol., 2019, 19(8), 473.
[http://dx.doi.org/10.1038/s41577-019-0197-5] [PMID: 31292539]
[4]
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]
[5]
Dudvarski Stankovic, N.; Teodorczyk, M.; Ploen, R.; Zipp, F.; Schmidt, M.H.H. Microglia-blood vessel interactions: a double-edged sword in brain pathologies. Acta Neuropathol., 2016, 131(3), 347-363.
[http://dx.doi.org/10.1007/s00401-015-1524-y] [PMID: 26711460]
[6]
Sandoval, K.E.; Witt, K.A. Blood-brain barrier tight junction permeability and ischemic stroke. Neurobiol. Dis., 2008, 32(2), 200-219.
[http://dx.doi.org/10.1016/j.nbd.2008.08.005] [PMID: 18790057]
[7]
Hawkins, B.T.; Davis, T.P. The blood-brain barrier/neurovascular unit in health and disease. Pharmacol. Rev., 2005, 57(2), 173-185.
[http://dx.doi.org/10.1124/pr.57.2.4] [PMID: 15914466]
[8]
Ballabh, P.; Braun, A.; Nedergaard, M. The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol. Dis., 2004, 16(1), 1-13.
[http://dx.doi.org/10.1016/j.nbd.2003.12.016] [PMID: 15207256]
[9]
Thurgur, H.; Pinteaux, E. Microglia in the Neurovascular Unit: Blood-Brain Barrier-microglia Interactions After Central Nervous System Disorders. Neuroscience, 2019, 405, 55-67.
[http://dx.doi.org/10.1016/j.neuroscience.2018.06.046] [PMID: 31007172]
[10]
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]
[11]
Alluri, H.; Wiggins-Dohlvik, K.; Davis, M.L.; Huang, J.H.; Tharakan, B. Blood-brain barrier dysfunction following traumatic brain injury. Metab. Brain Dis., 2015, 30(5), 1093-1104.
[http://dx.doi.org/10.1007/s11011-015-9651-7] [PMID: 25624154]
[12]
Turner, R.J.; Sharp, F.R. Implications of MMP9 for Blood Brain Barrier Disruption and Hemorrhagic Transformation Following Ischemic Stroke. Front. Cell. Neurosci., 2016, 10, 56.
[http://dx.doi.org/10.3389/fncel.2016.00056] [PMID: 26973468]
[13]
Abdullahi, W.; Tripathi, D.; Ronaldson, P.T. Blood-brain barrier dysfunction in ischemic stroke: targeting tight junctions and transporters for vascular protection. Am. J. Physiol. Cell Physiol., 2018, 315(3), C343-C356.
[http://dx.doi.org/10.1152/ajpcell.00095.2018] [PMID: 29949404]
[14]
Kleinschnitz, C.; Blecharz, K.; Kahles, T.; Schwarz, T.; Kraft, P.; Göbel, K.; Meuth, S.G.; Burek, M.; Thum, T.; Stoll, G.; Förster, C. Glucocorticoid insensitivity at the hypoxic blood-brain barrier can be reversed by inhibition of the proteasome. Stroke, 2011, 42(4), 1081-1089.
[http://dx.doi.org/10.1161/STROKEAHA.110.592238] [PMID: 21330632]
[15]
Burek, M.; König, A.; Lang, M.; Fiedler, J.; Oerter, S.; Roewer, N.; Bohnert, M.; Thal, S.C.; Blecharz-Lang, K.G.; Woitzik, J.; Thum, T.; Förster, C.Y. Hypoxia-Induced MicroRNA-212/132 Alter Blood-Brain Barrier Integrity Through Inhibition of Tight Junction-Associated Proteins in Human and Mouse Brain Microvascular Endothelial Cells. Transl. Stroke Res., 2019, 10(6), 672-683.
[http://dx.doi.org/10.1007/s12975-018-0683-2] [PMID: 30617994]
[16]
Haley, M.J.; Lawrence, C.B. The blood-brain barrier after stroke: Structural studies and the role of transcytotic vesicles. J. Cereb. Blood Flow Metab., 2017, 37(2), 456-470.
[http://dx.doi.org/10.1177/0271678X16629976] [PMID: 26823471]
[17]
Lorberboym, M.; Lampl, Y.; Sadeh, M. Correlation of 99mTc-DTPA SPECT of the blood-brain barrier with neurologic outcome after acute stroke. J. Nucl. Med., 2003, 44(12), 1898-1904.
[PMID: 14660714]
[18]
Brouns, R.; Wauters, A.; De Surgeloose, D.; Mariën, P.; De Deyn, P.P. Biochemical markers for blood-brain barrier dysfunction in acute ischemic stroke correlate with evolution and outcome. Eur. Neurol., 2011, 65(1), 23-31.
[http://dx.doi.org/10.1159/000321965] [PMID: 21135557]
[19]
Zhang, C.; Jiang, M.; Wang, W.Q.; Zhao, S.J.; Yin, Y.X.; Mi, Q.J.; Yang, M.F.; Song, Y.Q.; Sun, B.L.; Zhang, Z.Y. Selective mGluR1 negative allosteric modulator reduces blood-brain barrier permeability and cerebral edema after experimental subarachnoid hemorrhage. Transl. Stroke Res., 2019, 11(4), 799-811.
[http://dx.doi.org/10.1007/s12975-019-00758-z] [PMID: 31833035]
[20]
Prakash, R.; Carmichael, S.T. Blood-brain barrier breakdown and neovascularization processes after stroke and traumatic brain injury. Curr. Opin. Neurol., 2015, 28(6), 556-564.
[http://dx.doi.org/10.1097/WCO.0000000000000248] [PMID: 26402408]
[21]
Nimmerjahn, A.; Kirchhoff, F.; Helmchen, F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science, 2005, 308(5726), 1314-1318.
[http://dx.doi.org/10.1126/science.1110647] [PMID: 15831717]
[22]
Li, L.; Tao, Y.; Tang, J.; Chen, Q.; Yang, Y.; Feng, Z.; Chen, Y.; Yang, L.; Yang, Y.; Zhu, G.; Feng, H.; Chen, Z. A Cannabinoid Receptor 2 Agonist Prevents Thrombin-Induced Blood-Brain Barrier Damage via the Inhibition of Microglial Activation and Matrix Metalloproteinase Expression in Rats. Transl. Stroke Res., 2015, 6(6), 467-477.
[http://dx.doi.org/10.1007/s12975-015-0425-7] [PMID: 26376816]
[23]
Kim, S.U.; de Vellis, J. Microglia in health and disease. J. Neurosci. Res., 2005, 81(3), 302-313.
[http://dx.doi.org/10.1002/jnr.20562] [PMID: 15954124]
[24]
Salter, M.W.; Beggs, S. Sublime microglia: expanding roles for the guardians of the CNS. Cell, 2014, 158(1), 15-24.
[http://dx.doi.org/10.1016/j.cell.2014.06.008] [PMID: 24995975]
[25]
Spindler, K.R.; Hsu, T.H. Viral disruption of the blood-brain barrier. Trends Microbiol., 2012, 20(6), 282-290.
[http://dx.doi.org/10.1016/j.tim.2012.03.009] [PMID: 22564250]
[26]
Jackson, L.; Dong, G.; Althomali, W.; Sayed, M.A.; Eldahshan, W.; Baban, B.; Johnson, M.H.; Filosa, J.; Fagan, S.C.; Ergul, A. Delayed administration of angiotensin II type 2 receptor (AT2R) agonist compound 21 prevents the development of post-stroke cognitive impairment in diabetes through the modulation of microglia polarization. Transl. Stroke Res., 2019, 11, 762-775.
[http://dx.doi.org/10.1007/s12975-019-00752-5] [PMID: 31792796]
[27]
Kettenmann, H.; Hanisch, U.K.; Noda, M.; Verkhratsky, A. Physiology of microglia. Physiol. Rev., 2011, 91(2), 461-553.
[http://dx.doi.org/10.1152/physrev.00011.2010] [PMID: 21527731]
[28]
Hanisch, U.K.; Kettenmann, H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat. Neurosci., 2007, 10(11), 1387-1394.
[http://dx.doi.org/10.1038/nn1997] [PMID: 17965659]
[29]
Kreutzberg, G.W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci., 1996, 19(8), 312-318.
[http://dx.doi.org/10.1016/0166-2236(96)10049-7] [PMID: 8843599]
[30]
Borlongan, C.V. Cell therapy for stroke: remaining issues to address before embarking on clinical trials. Stroke, 2009, 40(3)(Suppl.), S146-S148.
[http://dx.doi.org/10.1161/STROKEAHA.108.533091] [PMID: 19064801]
[31]
Blecharz-Lang, K.G.; Wagner, J.; Fries, A.; Nieminen-Kelhä, M.; Rösner, J.; Schneider, U.C.; Vajkoczy, P. Interleukin 6-Mediated Endothelial Barrier Disturbances Can Be Attenuated by Blockade of the IL6 Receptor Expressed in Brain Microvascular Endothelial Cells. Transl. Stroke Res., 2018, 9(6), 631-642.
[http://dx.doi.org/10.1007/s12975-018-0614-2] [PMID: 29429002]
[32]
Lee, J.Y.; Castelli, V.; Bonsack, B.; Coats, A.B.; Navarro-Torres, L.; Garcia-Sanchez, J.; Kingsbury, C.; Nguyen, H.; Vandenbark, A.A.; Meza-Romero, R.; Offner, H.; Borlongan, C.V. Novel partial MHC class II construct, DRmQ, inhibits central and peripheral inflammatory responses to promote neuroprotection in experimental stroke. Transl. Stroke Res., 2019, 11, 831-836.
[33]
Yenari, M.A.; Xu, L.; Tang, X.N.; Qiao, Y.; Giffard, R.G. Microglia potentiate damage to blood-brain barrier constituents: improvement by minocycline in vivo and in vitro. Stroke, 2006, 37(4), 1087-1093.
[http://dx.doi.org/10.1161/01.STR.0000206281.77178.ac] [PMID: 16497985]
[34]
Zipser, B.D.; Johanson, C.E.; Gonzalez, L.; Berzin, T.M.; Tavares, R.; Hulette, C.M.; Vitek, M.P.; Hovanesian, V.; Stopa, E.G. Microvascular injury and blood-brain barrier leakage in Alzheimer’s disease. Neurobiol. Aging, 2007, 28(7), 977-986.
[http://dx.doi.org/10.1016/j.neurobiolaging.2006.05.016] [PMID: 16782234]
[35]
da Fonseca, A.C.; Matias, D.; Garcia, C.; Amaral, R.; Geraldo, L.H.; Freitas, C.; Lima, F.R. The impact of microglial activation on blood-brain barrier in brain diseases. Front. Cell. Neurosci., 2014, 8, 362.
[http://dx.doi.org/10.3389/fncel.2014.00362] [PMID: 25404894]
[36]
Shao, Z.; Tu, S.; Shao, A. Pathophysiological Mechanisms and Potential Therapeutic Targets in Intracerebral Hemorrhage. Front. Pharmacol., 2019, 10, 1079.
[http://dx.doi.org/10.3389/fphar.2019.01079] [PMID: 31607923]
[37]
Pan, W.; Stone, K.P.; Hsuchou, H.; Manda, V.K.; Zhang, Y.; Kastin, A.J. Cytokine signaling modulates blood-brain barrier function. Curr. Pharm. Des., 2011, 17(33), 3729-3740.
[http://dx.doi.org/10.2174/138161211798220918] [PMID: 21834767]
[38]
Franco, R.; Fernández-Suárez, D. Alternatively activated microglia and macrophages in the central nervous system. Prog. Neurobiol., 2015, 131, 65-86.
[http://dx.doi.org/10.1016/j.pneurobio.2015.05.003] [PMID: 26067058]
[39]
Zhang, S. Microglial activation after ischaemic stroke. Stroke Vasc. Neurol., 2019, 4(2), 71-74.
[http://dx.doi.org/10.1136/svn-2018-000196] [PMID: 31338213]
[40]
Xing, C.; Li, W.; Deng, W.; Ning, M.; Lo, E.H. A potential gliovascular mechanism for microglial activation: differential phenotypic switching of microglia by endothelium versus astrocytes. J. Neuroinflammation, 2018, 15(1), 143.
[http://dx.doi.org/10.1186/s12974-018-1189-2] [PMID: 29764475]
[41]
Iadecola, C.; Zhang, F.; Casey, R.; Nagayama, M.; Ross, M.E. Delayed reduction of ischemic brain injury and neurological deficits in mice lacking the inducible nitric oxide synthase gene. J. Neurosci., 1997, 17(23), 9157-9164.
[http://dx.doi.org/10.1523/JNEUROSCI.17-23-09157.1997] [PMID: 9364062]
[42]
Chen, A.Q.; Fang, Z.; Chen, X.L.; Yang, S.; Zhou, Y.F.; Mao, L.; Xia, Y.P.; Jin, H.J.; Li, Y.N.; You, M.F.; Wang, X.X.; Lei, H.; He, Q.W.; Hu, B. Microglia-derived TNF-α mediates endothelial necroptosis aggravating blood brain-barrier disruption after ischemic stroke. Cell Death Dis., 2019, 10(7), 487.
[http://dx.doi.org/10.1038/s41419-019-1716-9] [PMID: 31221990]
[43]
Taylor, R.A.; Sansing, L.H. Microglial responses after ischemic stroke and intracerebral hemorrhage. Clin. Dev. Immunol., 2013, 2013746068
[http://dx.doi.org/10.1155/2013/746068] [PMID: 24223607]
[44]
Maruo, N.; Morita, I.; Shirao, M.; Murota, S. IL-6 increases endothelial permeability in vitro. Endocrinology, 1992, 131(2), 710-714.
[PMID: 1639018]
[45]
Desai, T.R.; Leeper, N.J.; Hynes, K.L.; Gewertz, B.L. Interleukin-6 causes endothelial barrier dysfunction via the protein kinase C pathway. J. Surg. Res., 2002, 104(2), 118-123.
[http://dx.doi.org/10.1006/jsre.2002.6415] [PMID: 12020130]
[46]
Cohen, S.S.; Min, M.; Cummings, E.E.; Chen, X.; Sadowska, G.B.; Sharma, S.; Stonestreet, B.S. Effects of interleukin-6 on the expression of tight junction proteins in isolated cerebral microvessels from yearling and adult sheep. Neuroimmunomodulation, 2013, 20(5), 264-273.
[http://dx.doi.org/10.1159/000350470] [PMID: 23867217]
[47]
Rochfort, K.D.; Cummins, P.M. The blood-brain barrier endothelium: a target for pro-inflammatory cytokines. Biochem. Soc. Trans., 2015, 43(4), 702-706.
[http://dx.doi.org/10.1042/BST20140319] [PMID: 26551716]
[48]
Chen, S.D.; Yang, D.I.; Lin, T.K.; Shaw, F.Z.; Liou, C.W.; Chuang, Y.C. Roles of oxidative stress, apoptosis, PGC-1α and mitochondrial biogenesis in cerebral ischemia. Int. J. Mol. Sci., 2011, 12(10), 7199-7215.
[http://dx.doi.org/10.3390/ijms12107199] [PMID: 22072942]
[49]
Thiel, V.E.; Audus, K.L. Nitric oxide and blood-brain barrier integrity. Antioxid. Redox Signal., 2001, 3(2), 273-278.
[http://dx.doi.org/10.1089/152308601300185223] [PMID: 11396481]
[50]
Christopoulos, A.; El-Fakahany, E.E. The generation of nitric oxide by G protein-coupled receptors. Life Sci., 1999, 64(1), 1-15.
[http://dx.doi.org/10.1016/S0024-3205(98)00348-8] [PMID: 10027737]
[51]
Khan, M.; Dhammu, T.S.; Sakakima, H.; Shunmugavel, A.; Gilg, A.G.; Singh, A.K.; Singh, I. The inhibitory effect of S-nitrosoglutathione on blood-brain barrier disruption and peroxynitrite formation in a rat model of experimental stroke. J. Neurochem., 2012, 123(Suppl. 2), 86-97.
[http://dx.doi.org/10.1111/j.1471-4159.2012.07947.x] [PMID: 23050646]
[52]
Beckman, J.S.; Koppenol, W.H. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am. J. Physiol., 1996, 271(5 Pt 1), C1424-C1437.
[http://dx.doi.org/10.1152/ajpcell.1996.271.5.C1424] [PMID: 8944624]
[53]
Hobbs, A.J.; Higgs, A.; Moncada, S. Inhibition of nitric oxide synthase as a potential therapeutic target. Annu. Rev. Pharmacol. Toxicol., 1999, 39, 191-220.
[http://dx.doi.org/10.1146/annurev.pharmtox.39.1.191] [PMID: 10331082]
[54]
Song, H.; Cheng, Y.; Bi, G.; Zhu, Y.; Jun, W.; Ma, W.; Wu, H. Release of Matrix Metalloproteinases-2 and 9 by S-Nitrosylated Caveolin-1 Contributes to Degradation of Extracellular Matrix in tPA-Treated Hypoxic Endothelial Cells. PLoS One, 2016, 11(2)e0149269
[http://dx.doi.org/10.1371/journal.pone.0149269] [PMID: 26881424]
[55]
Lambertsen, K.L.; Biber, K.; Finsen, B. Inflammatory cytokines in experimental and human stroke. J. Cereb. Blood Flow Metab., 2012, 32(9), 1677-1698.
[http://dx.doi.org/10.1038/jcbfm.2012.88] [PMID: 22739623]
[56]
Mayhan, W.G. Cellular mechanisms by which tumor necrosis factor-alpha produces disruption of the blood-brain barrier. Brain Res., 2002, 927(2), 144-152.
[http://dx.doi.org/10.1016/S0006-8993(01)03348-0] [PMID: 11821008]
[57]
Sibson, N.R.; Blamire, A.M.; Perry, V.H.; Gauldie, J.; Styles, P.; Anthony, D.C. TNF-alpha reduces cerebral blood volume and disrupts tissue homeostasis via an endothelin- and TNFR2-dependent pathway. Brain, 2002, 125(Pt 11), 2446-2459.
[http://dx.doi.org/10.1093/brain/awf256] [PMID: 12390971]
[58]
Kangwantas, K.; Pinteaux, E.; Penny, J. The extracellular matrix protein laminin-10 promotes blood-brain barrier repair after hypoxia and inflammation in vitro. J. Neuroinflammation, 2016, 13, 25.
[http://dx.doi.org/10.1186/s12974-016-0495-9] [PMID: 26832174]
[59]
Labus, J.; Wöltje, K.; Stolte, K.N.; Häckel, S.; Kim, K.S.; Hildmann, A.; Danker, K. IL-1β promotes transendothelial migration of PBMCs by upregulation of the FN/α5β1 signalling pathway in immortalised human brain microvascular endothelial cells. Exp. Cell Res., 2018, 373(1-2), 99-111.
[http://dx.doi.org/10.1016/j.yexcr.2018.10.002] [PMID: 30342992]
[60]
Fiala, M.; Looney, D.J.; Stins, M.; Way, D.D.; Zhang, L.; Gan, X.; Chiappelli, F.; Schweitzer, E.S.; Shapshak, P.; Weinand, M.; Graves, M.C.; Witte, M.; Kim, K.S. TNF-alpha opens a paracellular route for HIV-1 invasion across the blood-brain barrier. Mol. Med., 1997, 3(8), 553-564.
[http://dx.doi.org/10.1007/BF03401701] [PMID: 9307983]
[61]
Nishioku, T.; Matsumoto, J.; Dohgu, S.; Sumi, N.; Miyao, K.; Takata, F.; Shuto, H.; Yamauchi, A.; Kataoka, Y. Tumor necrosis factor-alpha mediates the blood-brain barrier dysfunction induced by activated microglia in mouse brain microvascular endothelial cells. J. Pharmacol. Sci., 2010, 112(2), 251-254.
[http://dx.doi.org/10.1254/jphs.09292SC] [PMID: 20118615]
[62]
Yang, C.; Hawkins, K.E.; Doré, S.; Candelario-Jalil, E. Neuroinflammatory mechanisms of blood-brain barrier damage in ischemic stroke. Am. J. Physiol. Cell Physiol., 2019, 316(2), C135-C153.
[http://dx.doi.org/10.1152/ajpcell.00136.2018] [PMID: 30379577]
[63]
Jolivel, V.; Bicker, F.; Binamé, F.; Ploen, R.; Keller, S.; Gollan, R.; Jurek, B.; Birkenstock, J.; Poisa-Beiro, L.; Bruttger, J.; Opitz, V.; Thal, S.C.; Waisman, A.; Bäuerle, T.; Schäfer, M.K.; Zipp, F.; Schmidt, M.H.H. Perivascular microglia promote blood vessel disintegration in the ischemic penumbra. Acta Neuropathol., 2015, 129(2), 279-295.
[http://dx.doi.org/10.1007/s00401-014-1372-1] [PMID: 25500713]
[64]
Edholm, E.S.; Rhoo, K.H.; Robert, J. Evolutionary Aspects of Macrophages Polarization. Results Probl. Cell Differ., 2017, 62, 3-22.
[http://dx.doi.org/10.1007/978-3-319-54090-0_1] [PMID: 28455703]
[65]
McKinney, E.C.; Haynes, L.; Droese, A.L. Macrophage-like effector of spontaneous cytotoxicity from the shark. Dev. Comp. Immunol., 1986, 10(4), 497-508.
[http://dx.doi.org/10.1016/0145-305X(86)90171-0] [PMID: 3817246]
[66]
Rieger, A.M.; Hall, B.E.; Barreda, D.R. Macrophage activation differentially modulates particle binding, phagocytosis and downstream antimicrobial mechanisms. Dev. Comp. Immunol., 2010, 34(11), 1144-1159.
[http://dx.doi.org/10.1016/j.dci.2010.06.006] [PMID: 20600280]
[67]
Grayfer, L.; Robert, J. Divergent antiviral roles of amphibian (Xenopus laevis) macrophages elicited by colony-stimulating factor-1 and interleukin-34. J. Leukoc. Biol., 2014, 96(6), 1143-1153.
[http://dx.doi.org/10.1189/jlb.4A0614-295R] [PMID: 25190077]
[68]
Mazzolini, J.; Le Clerc, S.; Morisse, G.; Coulonges, C.; Kuil, L.E.; van Ham, T.J.; Zagury, J.F.; Sieger, D. Gene expression profiling reveals a conserved microglia signature in larval zebrafish. Glia, 2020, 68(2), 298-315.
[http://dx.doi.org/10.1002/glia.23717] [PMID: 31508850]
[69]
Qin, Y.; Sun, X.; Shao, X.; Cheng, C.; Feng, J.; Sun, W.; Gu, D.; Liu, W.; Xu, F.; Duan, Y. Macrophage-Microglia Networks Drive M1 Microglia Polarization After Mycobacterium Infection. Inflammation, 2015, 38(4), 1609-1616.
[http://dx.doi.org/10.1007/s10753-015-0136-y] [PMID: 25687640]
[70]
Li, Q.; Cao, Y.; Dang, C.; Han, B.; Han, R.; Ma, H.; Hao, J.; Wang, L. Inhibition of double-strand DNA-sensing cGAS ameliorates brain injury after ischemic stroke. EMBO Mol. Med., 2020, 12(4)e11002
[http://dx.doi.org/10.15252/emmm.201911002] [PMID: 32239625]
[71]
Gamdzyk, M.; Doycheva, D.M.; Araujo, C.; Ocak, U.; Luo, Y.; Tang, J.; Zhang, J.H. cGAS/STING Pathway Activation Contributes to Delayed Neurodegeneration in Neonatal Hypoxia-Ischemia Rat Model: Possible Involvement of LINE-1. Mol. Neurobiol., 2020, 57(6), 2600-2619.
[http://dx.doi.org/10.1007/s12035-020-01904-7] [PMID: 32253733]
[72]
Neumann, H.; Kotter, M.R.; Franklin, R.J. Debris clearance by microglia: an essential link between degeneration and regeneration. Brain, 2009, 132(Pt 2), 288-295.
[http://dx.doi.org/10.1093/brain/awn109] [PMID: 18567623]
[73]
Jin, R.; Yang, G.; Li, G. Inflammatory mechanisms in ischemic stroke: role of inflammatory cells. J. Leukoc. Biol., 2010, 87(5), 779-789.
[http://dx.doi.org/10.1189/jlb.1109766] [PMID: 20130219]
[74]
Colton, C.A.; Mott, R.T.; Sharpe, H.; Xu, Q.; Van Nostrand, W.E.; Vitek, M.P. Expression profiles for macrophage alternative activation genes in AD and in mouse models of AD. J. Neuroinflammation, 2006, 3, 27.
[http://dx.doi.org/10.1186/1742-2094-3-27] [PMID: 17005052]
[75]
Patel, A.R.; Ritzel, R.; McCullough, L.D.; Liu, F. Microglia and ischemic stroke: a double-edged sword. Int. J. Physiol. Pathophysiol. Pharmacol., 2013, 5(2), 73-90.
[PMID: 23750306]
[76]
Hu, X.; Leak, R.K.; Shi, Y.; Suenaga, J.; Gao, Y.; Zheng, P.; Chen, J. Microglial and macrophage polarization—new prospects for brain repair. Nat. Rev. Neurol., 2015, 11(1), 56-64.
[http://dx.doi.org/10.1038/nrneurol.2014.207] [PMID: 25385337]
[77]
Zheng, Z.V.; Lyu, H.; Lam, S.Y.E.; Lam, P.K.; Poon, W.S.; Wong, G.K.C. The Dynamics of Microglial Polarization Reveal the Resident Neuroinflammatory Responses After Subarachnoid Hemorrhage. Transl. Stroke Res., 2019, 11, 433-449.
[http://dx.doi.org/10.1007/s12975-019-00728-5] [PMID: 31628642]
[78]
Driessler, F.; Venstrom, K.; Sabat, R.; Asadullah, K.; Schottelius, A.J. Molecular mechanisms of interleukin-10-mediated inhibition of NF-kappaB activity: a role for p50. Clin. Exp. Immunol., 2004, 135(1), 64-73.
[http://dx.doi.org/10.1111/j.1365-2249.2004.02342.x] [PMID: 14678266]
[79]
Garcia, J.M.; Stillings, S.A.; Leclerc, J.L.; Phillips, H.; Edwards, N.J.; Robicsek, S.A.; Hoh, B.L.; Blackburn, S.; Doré, S. Role of Interleukin-10 in Acute Brain Injuries. Front. Neurol., 2017, 8, 244.
[http://dx.doi.org/10.3389/fneur.2017.00244] [PMID: 28659854]
[80]
Cai, Y.; Liu, X.; Chen, W.; Wang, Z.; Xu, G.; Zeng, Y.; Ma, Y. TGF-β1 prevents blood-brain barrier damage and hemorrhagic transformation after thrombolysis in rats. Exp. Neurol., 2015, 266, 120-126.
[http://dx.doi.org/10.1016/j.expneurol.2015.02.013] [PMID: 25708985]
[81]
Mori, S.; Maher, P.; Conti, B. Neuroimmunology of the Interleukins 13 and 4. Brain Sci., 2016, 6(2)E18
[http://dx.doi.org/10.3390/brainsci6020018] [PMID: 27304970]
[82]
Röcken, M.; Racke, M.; Shevach, E.M. IL-4-induced immune deviation as antigen-specific therapy for inflammatory autoimmune disease. Immunol. Today, 1996, 17(5), 225-231.
[http://dx.doi.org/10.1016/0167-5699(96)80556-1] [PMID: 8991384]
[83]
Raphael, I.; Nalawade, S.; Eagar, T.N.; Forsthuber, T.G. T cell subsets and their signature cytokines in autoimmune and inflammatory diseases. Cytokine, 2015, 74(1), 5-17.
[http://dx.doi.org/10.1016/j.cyto.2014.09.011] [PMID: 25458968]
[84]
Veremeyko, T.; Siddiqui, S.; Sotnikov, I.; Yung, A.; Ponomarev, E.D. IL-4/IL-13-dependent and independent expression of miR-124 and its contribution to M2 phenotype of monocytic cells in normal conditions and during allergic inflammation. PLoS One, 2013, 8(12)e81774
[http://dx.doi.org/10.1371/journal.pone.0081774] [PMID: 24358127]
[85]
Elkabes, S.; DiCicco-Bloom, E.M.; Black, I.B. Brain microglia/macrophages express neurotrophins that selectively regulate microglial proliferation and function. J. Neurosci., 1996, 16(8), 2508-2521.
[http://dx.doi.org/10.1523/JNEUROSCI.16-08-02508.1996] [PMID: 8786427]
[86]
Zhao, X.; Eyo, U.B.; Murugan, M.; Wu, L.J. Microglial interactions with the neurovascular system in physiology and pathology. Dev. Neurobiol., 2018, 78(6), 604-617.
[http://dx.doi.org/10.1002/dneu.22576] [PMID: 29318762]
[87]
Yang, F.; Wang, Z.; Wei, X.; Han, H.; Meng, X.; Zhang, Y.; Shi, W.; Li, F.; Xin, T.; Pang, Q.; Yi, F. NLRP3 deficiency ameliorates neurovascular damage in experimental ischemic stroke. J. Cereb. Blood Flow Metab., 2014, 34(4), 660-667.
[http://dx.doi.org/10.1038/jcbfm.2013.242] [PMID: 24424382]
[88]
Shao, A.; Wu, H.; Hong, Y.; Tu, S.; Sun, X.; Wu, Q.; Zhao, Q.; Zhang, J.; Sheng, J. Hydrogen-Rich Saline Attenuated Subarachnoid Hemorrhage-Induced Early Brain Injury in Rats by Suppressing Inflammatory Response: Possible Involvement of NF-κB Pathway and NLRP3 Inflammasome. Mol. Neurobiol., 2016, 53(5), 3462-3476.
[http://dx.doi.org/10.1007/s12035-015-9242-y] [PMID: 26091790]
[89]
Swanson, K.V.; Deng, M.; Ting, J.P. The NLRP3 inflammasome: molecular activation and regulation to therapeutics. Nat. Rev. Immunol., 2019, 19(8), 477-489.
[http://dx.doi.org/10.1038/s41577-019-0165-0] [PMID: 31036962]
[90]
Ren, H.; Kong, Y.; Liu, Z.; Zang, D.; Yang, X.; Wood, K.; Li, M.; Liu, Q. Selective NLRP3 (Pyrin Domain-Containing Protein 3) Inflammasome Inhibitor Reduces Brain Injury After Intracerebral Hemorrhage. Stroke, 2018, 49(1), 184-192.
[http://dx.doi.org/10.1161/STROKEAHA.117.018904] [PMID: 29212744]
[91]
Szalay, G.; Martinecz, B.; Lénárt, N.; Környei, Z.; Orsolits, B.; Judák, L.; Császár, E.; Fekete, R.; West, B.L.; Katona, G.; Rózsa, B.; Dénes, Á. Microglia protect against brain injury and their selective elimination dysregulates neuronal network activity after stroke. Nat. Commun., 2016, 7, 11499.
[http://dx.doi.org/10.1038/ncomms11499] [PMID: 27139776]
[92]
Webster, C.M.; Hokari, M.; McManus, A.; Tang, X.N.; Ma, H.; Kacimi, R.; Yenari, M.A. Microglial P2Y12 deficiency/inhibition protects against brain ischemia. PLoS One, 2013, 8(8)e70927
[http://dx.doi.org/10.1371/journal.pone.0070927] [PMID: 23940669]
[93]
Lou, N.; Takano, T.; Pei, Y.; Xavier, A.L.; Goldman, S.A.; Nedergaard, M. Purinergic receptor P2RY12-dependent microglial closure of the injured blood-brain barrier. Proc. Natl. Acad. Sci. USA, 2016, 113(4), 1074-1079.
[http://dx.doi.org/10.1073/pnas.1520398113] [PMID: 26755608]
[94]
Ma, Y.; Wang, J.; Wang, Y.; Yang, G.Y. The biphasic function of microglia in ischemic stroke. Prog. Neurobiol., 2017, 157, 247-272.
[http://dx.doi.org/10.1016/j.pneurobio.2016.01.005] [PMID: 26851161]
[95]
Alessandrini, A.; Namura, S.; Moskowitz, M.A.; Bonventre, J.V. MEK1 protein kinase inhibition protects against damage resulting from focal cerebral ischemia. Proc. Natl. Acad. Sci. USA, 1999, 96(22), 12866-12869.
[http://dx.doi.org/10.1073/pnas.96.22.12866] [PMID: 10536014]
[96]
Gonzalez-Zulueta, M.; Feldman, A.B.; Klesse, L.J.; Kalb, R.G.; Dillman, J.F.; Parada, L.F.; Dawson, T.M.; Dawson, V.L. Requirement for nitric oxide activation of p21(ras)/extracellular regulated kinase in neuronal ischemic preconditioning. Proc. Natl. Acad. Sci. USA, 2000, 97(1), 436-441.
[http://dx.doi.org/10.1073/pnas.97.1.436] [PMID: 10618436]
[97]
Hu, B.R.; Wieloch, T. Tyrosine phosphorylation and activation of mitogen-activated protein kinase in the rat brain following transient cerebral ischemia. J. Neurochem., 1994, 62(4), 1357-1367.
[http://dx.doi.org/10.1046/j.1471-4159.1994.62041357.x] [PMID: 7510779]
[98]
Kozawa, O.; Tokuda, H.; Miwa, M.; Ito, H.; Matsuno, H.; Niwa, M.; Kato, K.; Uematsu, T. Involvement of p42/p44 mitogen-activated protein kinase in prostaglandin f(2alpha)-stimulated induction of heat shock protein 27 in osteoblasts. J. Cell. Biochem., 1999, 75(4), 610-619.
[http://dx.doi.org/10.1002/(SICI)1097-4644(19991215)75:4<610:AID-JCB7>3.0.CO;2-8] [PMID: 10572244]
[99]
Xi, G.; Hua, Y.; Keep, R.F.; Duong, H.K.; Hoff, J.T. Activation of p44/42 mitogen activated protein kinases in thrombin-induced brain tolerance. Brain Res., 2001, 895(1-2), 153-159.
[http://dx.doi.org/10.1016/S0006-8993(01)02064-9] [PMID: 11259772]
[100]
D’Haese, J.G.; Friess, H.; Ceyhan, G.O. Therapeutic potential of the chemokine-receptor duo fractalkine/CX3CR1: an update. Expert Opin. Ther. Targets, 2012, 16(6), 613-618.
[http://dx.doi.org/10.1517/14728222.2012.682574] [PMID: 22530606]
[101]
Cardona, A.E.; Huang, D.; Sasse, M.E.; Ransohoff, R.M. Isolation of murine microglial cells for RNA analysis or flow cytometry. Nat. Protoc., 2006, 1(4), 1947-1951.
[http://dx.doi.org/10.1038/nprot.2006.327] [PMID: 17487181]
[102]
Sumi, N.; Nishioku, T.; Takata, F.; Matsumoto, J.; Watanabe, T.; Shuto, H.; Yamauchi, A.; Dohgu, S.; Kataoka, Y. Lipopolysaccharide-activated microglia induce dysfunction of the blood-brain barrier in rat microvascular endothelial cells co-cultured with microglia. Cell. Mol. Neurobiol., 2010, 30(2), 247-253.
[http://dx.doi.org/10.1007/s10571-009-9446-7] [PMID: 19728078]
[103]
Chen, H.; Guan, B.; Wang, B.; Pu, H.; Bai, X.; Chen, X.; Liu, J.; Li, C.; Qiu, J.; Yang, D.; Liu, K.; Wang, Q.; Qi, S.; Shen, J. Glycyrrhizin Prevents Hemorrhagic Transformation and Improves Neurological Outcome in Ischemic Stroke with Delayed Thrombolysis Through Targeting Peroxynitrite-Mediated HMGB1 Signaling. Transl. Stroke Res., 2019, 11, 967-982.
[http://dx.doi.org/10.1007/s12975-019-00772-1] [PMID: 31872339]
[104]
del Zoppo, G.J.; Milner, R.; Mabuchi, T.; Hung, S.; Wang, X.; Berg, G.I.; Koziol, J.A. Microglial activation and matrix protease generation during focal cerebral ischemia. Stroke, 2007, 38(2)(Suppl.), 646-651.
[http://dx.doi.org/10.1161/01.STR.0000254477.34231.cb] [PMID: 17261708]
[105]
Zhang, Z.G.; Zhang, L.; Jiang, Q.; Zhang, R.; Davies, K.; Powers, C.; Bruggen, Nv.; Chopp, M. VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain. J. Clin. Invest., 2000, 106(7), 829-838.
[http://dx.doi.org/10.1172/JCI9369] [PMID: 11018070]
[106]
Potente, M.; Gerhardt, H.; Carmeliet, P. Basic and therapeutic aspects of angiogenesis. Cell, 2011, 146(6), 873-887.
[http://dx.doi.org/10.1016/j.cell.2011.08.039] [PMID: 21925313]
[107]
Drieu, A.; Buendia, I.; Levard, D.; Helie, P.; Brodin, C.; Vivien, D.; Rubio, M. Immune responses and anti-inflammatory strategies in a clinically relevant model of thromboembolic ischemic stroke with reperfusion. Transl. Stroke Res., 2019, 11, 481-495.
[http://dx.doi.org/10.1007/s12975-019-00733-8] [PMID: 31522409]
[108]
Xiong, X.Y.; Liu, L.; Yang, Q.W. Functions and mechanisms of microglia/macrophages in neuroinflammation and neurogenesis after stroke. Prog. Neurobiol., 2016, 142, 23-44.
[http://dx.doi.org/10.1016/j.pneurobio.2016.05.001] [PMID: 27166859]
[109]
Tikka, T.; Fiebich, B.L.; Goldsteins, G.; Keinanen, R.; Koistinaho, J. Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J. Neurosci., 2001, 21(8), 2580-2588.
[http://dx.doi.org/10.1523/JNEUROSCI.21-08-02580.2001] [PMID: 11306611]
[110]
Machado, L.S.; Kozak, A.; Ergul, A.; Hess, D.C.; Borlongan, C.V.; Fagan, S.C. Delayed minocycline inhibits ischemia-activated matrix metalloproteinases 2 and 9 after experimental stroke. BMC Neurosci., 2006, 7, 56.
[http://dx.doi.org/10.1186/1471-2202-7-56] [PMID: 16846501]
[111]
Yang, Y.; Salayandia, V.M.; Thompson, J.F.; Yang, L.Y.; Estrada, E.Y.; Yang, Y. Attenuation of acute stroke injury in rat brain by minocycline promotes blood-brain barrier remodeling and alternative microglia/macrophage activation during recovery. J. Neuroinflammation, 2015, 12, 26.
[http://dx.doi.org/10.1186/s12974-015-0245-4] [PMID: 25889169]
[112]
Mok, K.W.; Mruk, D.D.; Lie, P.P.; Lui, W.Y.; Cheng, C.Y. Adjudin, a potential male contraceptive, exerts its effects locally in the seminiferous epithelium of mammalian testes. Reproduction, 2011, 141(5), 571-580.
[http://dx.doi.org/10.1530/REP-10-0464] [PMID: 21307270]
[113]
Shao, J.; Liu, T.; Xie, Q.R.; Zhang, T.; Yu, H.; Wang, B.; Ying, W.; Mruk, D.D.; Silvestrini, B.; Cheng, C.Y.; Xia, W. Adjudin attenuates lipopolysaccharide (LPS)- and ischemia-induced microglial activation. J. Neuroimmunol., 2013, 254(1-2), 83-90.
[http://dx.doi.org/10.1016/j.jneuroim.2012.09.012] [PMID: 23084372]
[114]
Liu, T.; Zhang, T.; Yu, H.; Shen, H.; Xia, W. Adjudin protects against cerebral ischemia reperfusion injury by inhibition of neuroinflammation and blood-brain barrier disruption. J. Neuroinflammation, 2014, 11, 107.
[http://dx.doi.org/10.1186/1742-2094-11-107] [PMID: 24927761]
[115]
Ward, R.; Li, W.; Abdul, Y.; Jackson, L.; Dong, G.; Jamil, S.; Filosa, J.; Fagan, S.C.; Ergul, A. NLRP3 inflammasome inhibition with MCC950 improves diabetes-mediated cognitive impairment and vasoneuronal remodeling after ischemia. Pharmacol. Res., 2019, 142, 237-250.
[http://dx.doi.org/10.1016/j.phrs.2019.01.035] [PMID: 30818045]
[116]
Li, L.; Yun, D.; Zhang, Y.; Tao, Y.; Tan, Q.; Qiao, F.; Luo, B.; Liu, Y.; Fan, R.; Xian, J.; Yu, A. A cannabinoid receptor 2 agonist reduces blood-brain barrier damage via induction of MKP-1 after intracerebral hemorrhage in rats. Brain Res., 2018, 1697, 113-123.
[http://dx.doi.org/10.1016/j.brainres.2018.06.006] [PMID: 29886251]
[117]
Wang, Z.; Li, Y.; Cai, S.; Li, R.; Cao, G. Cannabinoid receptor 2 agonist attenuates blood brain barrier damage in a rat model of intracerebral hemorrhage by activating the Rac1 pathway. Int. J. Mol. Med., 2018, 42(5), 2914-2922.
[http://dx.doi.org/10.3892/ijmm.2018.3834] [PMID: 30132506]
[118]
Van den Bosch, F.; Kruithof, E.; De Vos, M.; De Keyser, F.; Mielants, H. Crohn’s disease associated with spondyloarthropathy: effect of TNF-alpha blockade with infliximab on articular symptoms. Lancet, 2000, 356(9244), 1821-1822.
[http://dx.doi.org/10.1016/S0140-6736(00)03239-6] [PMID: 11117919]
[119]
Kocic, I.; Kowianski, P.; Rusiecka, I.; Lietzau, G.; Mansfield, C.; Moussy, A.; Hermine, O.; Dubreuil, P. Neuroprotective effect of masitinib in rats with postischemic stroke. Naunyn Schmiedebergs Arch. Pharmacol., 2015, 388(1), 79-86.
[http://dx.doi.org/10.1007/s00210-014-1061-6] [PMID: 25344204]
[120]
Shiba, M.; Suzuki, H.; Fujimoto, M.; Shimojo, N.; Imanaka-Yoshida, K.; Yoshida, T.; Kanamaru, K.; Matsushima, S.; Taki, W. Role of platelet-derived growth factor in cerebral vasospasm after subarachnoid hemorrhage in rats. Acta Neurochir. Suppl. (Wien), 2013, 115, 219-223.
[http://dx.doi.org/10.1007/978-3-7091-1192-5_40] [PMID: 22890672]
[121]
Zhan, Y.; Krafft, P.R.; Lekic, T.; Ma, Q.; Souvenir, R.; Zhang, J.H.; Tang, J. Imatinib preserves blood-brain barrier integrity following experimental subarachnoid hemorrhage in rats. J. Neurosci. Res., 2015, 93(1), 94-103.
[http://dx.doi.org/10.1002/jnr.23475] [PMID: 25196554]
[122]
Piette, F.; Belmin, J.; Vincent, H.; Schmidt, N.; Pariel, S.; Verny, M.; Marquis, C.; Mely, J.; Hugonot-Diener, L.; Kinet, J.P.; Dubreuil, P.; Moussy, A.; Hermine, O. Masitinib as an adjunct therapy for mild-to-moderate Alzheimer’s disease: a randomised, placebo-controlled phase 2 trial. Alzheimers Res. Ther., 2011, 3(2), 16.
[http://dx.doi.org/10.1186/alzrt75] [PMID: 21504563]
[123]
Vermersch, P.; Benrabah, R.; Schmidt, N.; Zéphir, H.; Clavelou, P.; Vongsouthi, C.; Dubreuil, P.; Moussy, A.; Hermine, O. Masitinib treatment in patients with progressive multiple sclerosis: a randomized pilot study. BMC Neurol., 2012, 12, 36.
[http://dx.doi.org/10.1186/1471-2377-12-36] [PMID: 22691628]
[124]
Adzemovic, M.V.; Zeitelhofer, M.; Eriksson, U.; Olsson, T.; Nilsson, I. Imatinib ameliorates neuroinflammation in a rat model of multiple sclerosis by enhancing blood-brain barrier integrity and by modulating the peripheral immune response. PLoS One, 2013, 8(2)e56586
[http://dx.doi.org/10.1371/journal.pone.0056586] [PMID: 23437178]
[125]
Tebib, J.; Mariette, X.; Bourgeois, P.; Flipo, R.M.; Gaudin, P.; Le Loët, X.; Gineste, P.; Guy, L.; Mansfield, C.D.; Moussy, A.; Dubreuil, P.; Hermine, O.; Sibilia, J. Masitinib in the treatment of active rheumatoid arthritis: results of a multicentre, open-label, dose-ranging, phase 2a study. Arthritis Res. Ther., 2009, 11(3), R95.
[http://dx.doi.org/10.1186/ar2740] [PMID: 19549290]
[126]
Humbert, M.; de Blay, F.; Garcia, G.; Prud’homme, A.; Leroyer, C.; Magnan, A.; Tunon-de-Lara, J.M.; Pison, C.; Aubier, M.; Charpin, D.; Vachier, I.; Purohit, A.; Gineste, P.; Bader, T.; Moussy, A.; Hermine, O.; Chanez, P. Masitinib, a c-kit/PDGF receptor tyrosine kinase inhibitor, improves disease control in severe corticosteroid-dependent asthmatics. Allergy, 2009, 64(8), 1194-1201.
[http://dx.doi.org/10.1111/j.1398-9995.2009.02122.x] [PMID: 19614621]
[127]
Paul, C.; Sans, B.; Suarez, F.; Casassus, P.; Barete, S.; Lanternier, F.; Grandpeix-Guyodo, C.; Dubreuil, P.; Palmérini, F.; Mansfield, C.D.; Gineste, P.; Moussy, A.; Hermine, O.; Lortholary, O. Masitinib for the treatment of systemic and cutaneous mastocytosis with handicap: a phase 2a study. Am. J. Hematol., 2010, 85(12), 921-925.
[http://dx.doi.org/10.1002/ajh.21894] [PMID: 21108325]
[128]
Rieckmann, P. Imatinib buys time for brain after stroke. Nat. Med., 2008, 14(7), 712-713.
[http://dx.doi.org/10.1038/nm0708-712] [PMID: 18607366]
[129]
Dhawan, G.; Floden, A.M.; Combs, C.K. Amyloid-β oligomers stimulate microglia through a tyrosine kinase dependent mechanism. Neurobiol. Aging, 2012, 33(10), 2247-2261.
[http://dx.doi.org/10.1016/j.neurobiolaging.2011.10.027] [PMID: 22133278]
[130]
Dhawan, G.; Combs, C.K. Inhibition of Src kinase activity attenuates amyloid associated microgliosis in a murine model of Alzheimer’s disease. J. Neuroinflammation, 2012, 9, 117.
[http://dx.doi.org/10.1186/1742-2094-9-117] [PMID: 22673542]
[131]
Romeo, U.; Palaia, G.; Fantozzi, P.J.; Tenore, G.; Bosco, D. A Rare Case of Melanosis of the Hard Palate Mucosa in a Patient with Chronic Myeloid Leukemia. Case Rep. Dent., 2015, 2015817094
[http://dx.doi.org/10.1155/2015/817094] [PMID: 26451262]
[132]
Capdeville, R.; Buchdunger, E.; Zimmermann, J.; Matter, A. Glivec (STI571, imatinib), a rationally developed, targeted anticancer drug. Nat. Rev. Drug Discov., 2002, 1(7), 493-502.
[http://dx.doi.org/10.1038/nrd839] [PMID: 12120256]
[133]
Rizzo, A.N.; Aman, J.; van Nieuw Amerongen, G.P.; Dudek, S.M. Targeting Abl kinases to regulate vascular leak during sepsis and acute respiratory distress syndrome. Arterioscler. Thromb. Vasc. Biol., 2015, 35(5), 1071-1079.
[http://dx.doi.org/10.1161/ATVBAHA.115.305085] [PMID: 25814671]
[134]
Corada, M.; Mariotti, M.; Thurston, G.; Smith, K.; Kunkel, R.; Brockhaus, M.; Lampugnani, M.G.; Martin-Padura, I.; Stoppacciaro, A.; Ruco, L.; McDonald, D.M.; Ward, P.A.; Dejana, E. Vascular endothelial-cadherin is an important determinant of microvascular integrity in vivo. Proc. Natl. Acad. Sci. USA, 1999, 96(17), 9815-9820.
[http://dx.doi.org/10.1073/pnas.96.17.9815] [PMID: 10449777]
[135]
Aman, J.; van Bezu, J.; Damanafshan, A.; Huveneers, S.; Eringa, E.C.; Vogel, S.M.; Groeneveld, A.B.; Vonk Noordegraaf, A.; van Hinsbergh, V.W.; van Nieuw Amerongen, G.P. Effective treatment of edema and endothelial barrier dysfunction with imatinib. Circulation, 2012, 126(23), 2728-2738.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.112.134304] [PMID: 23099479]
[136]
Chislock, E.M.; Pendergast, A.M. Abl family kinases regulate endothelial barrier function in vitro and in mice. PLoS One, 2013, 8(12)e85231
[http://dx.doi.org/10.1371/journal.pone.0085231] [PMID: 24367707]
[137]
Rizzo, A.N.; Sammani, S.; Esquinca, A.E.; Jacobson, J.R.; Garcia, J.G.; Letsiou, E.; Dudek, S.M. Imatinib attenuates inflammation and vascular leak in a clinically relevant two-hit model of acute lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol., 2015, 309(11), L1294-L1304.
[http://dx.doi.org/10.1152/ajplung.00031.2015] [PMID: 26432864]
[138]
Stephens, R.S.; Servinsky, L.E.; Rentsendorj, O.; Kolb, T.M.; Pfeifer, A.; Pearse, D.B. Protein kinase G increases antioxidant function in lung microvascular endothelial cells by inhibiting the c-Abl tyrosine kinase. Am. J. Physiol. Cell Physiol., 2014, 306(6), C559-C569.
[http://dx.doi.org/10.1152/ajpcell.00375.2012] [PMID: 24401847]
[139]
Tanaka, S.; Chen-Yoshikawa, T.F.; Kajiwara, M.; Menju, T.; Ohata, K.; Takahashi, M.; Kondo, T.; Hijiya, K.; Motoyama, H.; Aoyama, A.; Masuda, S.; Date, H. Protective Effects of Imatinib on Ischemia/Reperfusion Injury in Rat Lung. Ann. Thorac. Surg., 2016, 102(5), 1717-1724.
[http://dx.doi.org/10.1016/j.athoracsur.2016.05.037] [PMID: 27460916]
[140]
Reber, L.L.; Starkl, P.; Balbino, B.; Sibilano, R.; Gaudenzio, N.; Rogalla, S.; Sensarn, S.; Kang, D.; Raghu, H.; Sokolove, J.; Robinson, W.H.; Contag, C.H.; Tsai, M.; Galli, S.J. The tyrosine kinase inhibitor imatinib mesylate suppresses uric acid crystal-induced acute gouty arthritis in mice. PLoS One, 2017, 12(10)e0185704
[http://dx.doi.org/10.1371/journal.pone.0185704] [PMID: 28982129]
[141]
Azizi, G.; Haidari, M.R.; Khorramizadeh, M.; Naddafi, F.; Sadria, R.; Javanbakht, M.H.; Sedaghat, R.; Tofighi Zavareh, F.; Mirshafiey, A. Effects of imatinib mesylate in mouse models of multiple sclerosis and in vitro determinants. Iran. J. Allergy Asthma Immunol., 2014, 13(3), 198-206.
[PMID: 24659124]
[142]
Su, E.J.; Fredriksson, L.; Geyer, M.; Folestad, E.; Cale, J.; Andrae, J.; Gao, Y.; Pietras, K.; Mann, K.; Yepes, M.; Strickland, D.K.; Betsholtz, C.; Eriksson, U.; Lawrence, D.A. Activation of PDGF-CC by tissue plasminogen activator impairs blood-brain barrier integrity during ischemic stroke. Nat. Med., 2008, 14(7), 731-737.
[http://dx.doi.org/10.1038/nm1787] [PMID: 18568034]
[143]
Gągało, I.; Rusiecka, I.; Kocić, I. Tyrosine Kinase Inhibitor as a new Therapy for Ischemic Stroke and other Neurologic Diseases: is there any Hope for a Better Outcome? Curr. Neuropharmacol., 2015, 13(6), 836-844.
[http://dx.doi.org/10.2174/1570159X13666150518235504] [PMID: 26630962]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 18
ISSUE: 12
Year: 2020
Page: [1237 - 1249]
Pages: 13
DOI: 10.2174/1570159X18666200529150907
Price: $65

Article Metrics

PDF: 40
HTML: 1