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Current Neuropharmacology

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

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Review Article

Neutrophil Extracellular Traps in Cerebral Ischemia/Reperfusion Injury: Friend and Foe

Author(s): Haoyue Luo, Hanjing Guo, Yue Zhou, Rui Fang, Wenli Zhang* and Zhigang Mei*

Volume 21, Issue 10, 2023

Published on: 15 March, 2023

Page: [2079 - 2096] Pages: 18

DOI: 10.2174/1570159X21666230308090351

Price: $65

Abstract

Cerebral ischemic injury, one of the leading causes of morbidity and mortality worldwide, triggers various central nervous system (CNS) diseases, including acute ischemic stroke (AIS) and chronic ischemia-induced Alzheimer's disease (AD). Currently, targeted therapies are urgently needed to address neurological disorders caused by cerebral ischemia/reperfusion injury (CI/RI), and the emergence of neutrophil extracellular traps (NETs) may be able to relieve the pressure. Neutrophils are precursors to brain injury following ischemic stroke and exert complicated functions. NETs extracellularly release reticular complexes of neutrophils, i.e., double-stranded DNA (dsDNA), histones, and granulins. Paradoxically, NETs play a dual role, friend and foe, under different conditions, for example, physiological circumstances, infection, neurodegeneration, and ischemia/reperfusion. Increasing evidence indicates that NETs exert anti-inflammatory effects by degrading cytokines and chemokines through protease at a relatively stable and moderate level under physiological conditions, while excessive amounts of NETs release (NETosis) irritated by CI/RI exacerbate the inflammatory response and aggravate thrombosis, disrupt the blood-brain barrier (BBB), and initiates sequential neuron injury and tissue damage. This review provides a comprehensive overview of the machinery of NETs formation and the role of an abnormal cascade of NETs in CI/RI, as well as other ischemia-induced neurological diseases. Herein, we highlight the potential of NETs as a therapeutic target against ischemic stroke that may inspire translational research and innovative clinical approaches.

Keywords: Ischemic stroke, Alzheimer’s disease, cerebral ischemia, cerebral ischemia-reperfusion, neutrophil extracellular traps, CNS diseases.

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[1]
Lin, H.W.; Lee, R.C.; Lee, M.H.H.; Wu, C.Y.C.; Couto e Silva, A.; Possoit, H.E.; Hsieh, T-H.; Minagar, A. Cerebral ischemia and neuroregeneration. Neural Regen. Res., 2018, 13(3), 373-385.
[http://dx.doi.org/10.4103/1673-5374.228711] [PMID: 29623912]
[2]
Kuriakose, D.; Xiao, Z. Pathophysiology and Treatment of Stroke: Present Status and Future Perspectives. Int. J. Mol. Sci., 2020, 21(20), 7609.
[http://dx.doi.org/10.3390/ijms21207609] [PMID: 33076218]
[3]
Villain, N.; Dubois, B. Alzheimer’s Disease Including Focal Presentations. Semin. Neurol., 2019, 39(2), 213-226.
[http://dx.doi.org/10.1055/s-0039-1681041] [PMID: 30925614]
[4]
Hurford, R.; Sekhar, A.; Hughes, T.A.T.; Muir, K.W. Diagnosis and management of acute ischaemic stroke. Pract. Neurol., 2020, 20(4), 304-316.
[http://dx.doi.org/10.1136/practneurol-2020-002557] [PMID: 32507747]
[5]
Kalogeris, T.; Baines, C.P.; Krenz, M.; Korthuis, R.J. Cell biology of ischemia/reperfusion injury. Int. Rev. Cell Mol. Biol., 2012, 298, 229-317.
[http://dx.doi.org/10.1016/B978-0-12-394309-5.00006-7] [PMID: 22878108]
[6]
Jian, Z.; Liu, R.; Zhu, X.; Smerin, D.; Zhong, Y.; Gu, L.; Fang, W.; Xiong, X. The Involvement and therapy target of immune cells after ischemic stroke. Front. Immunol., 2019, 10, 2167.
[http://dx.doi.org/10.3389/fimmu.2019.02167] [PMID: 31572378]
[7]
Brinkmann, V.; Reichard, U.; Goosmann, C.; Fauler, B.; Uhlemann, Y.; Weiss, D.S.; Weinrauch, Y.; Zychlinsky, A. Neutrophil extracellular traps kill bacteria. Science, 2004, 303(5663), 1532-1535.
[http://dx.doi.org/10.1126/science.1092385] [PMID: 15001782]
[8]
Klopf, J.; Brostjan, C.; Eilenberg, W.; Neumayer, C. Neutrophil extracellular traps and their implications in cardiovascular and inflammatory disease. Int. J. Mol. Sci., 2021, 22(2), 559.
[http://dx.doi.org/10.3390/ijms22020559] [PMID: 33429925]
[9]
Mutua, V.; Gershwin, L.J. A review of neutrophil extracellular traps (NETs) in disease: Potential anti-NETs therapeutics. Clin. Rev. Allergy Immunol., 2021, 61(2), 194-211.
[http://dx.doi.org/10.1007/s12016-020-08804-7] [PMID: 32740860]
[10]
Vorobjeva, N.V.; Chernyak, B.V. NETosis: Molecular mechanisms, role in physiology and pathology. Biochemistry (Mosc.), 2020, 85(10), 1178-1190.
[http://dx.doi.org/10.1134/S0006297920100065] [PMID: 33202203]
[11]
Guo, Y.; Zeng, H.; Gao, C. The role of neutrophil extracellular traps in central nervous system diseases and prospects for clinical application. Oxid Med Cell Longev., 2021, 2021, 1-13.
[http://dx.doi.org/10.1155/2021/9931742] [PMID: 34336122]
[12]
Fuchs, T.A.; Brill, A.; Duerschmied, D.; Schatzberg, D.; Monestier, M.; Myers, D.D., Jr; Wrobleski, S.K.; Wakefield, T.W.; Hartwig, J.H.; Wagner, D.D. Extracellular DNA traps promote thrombosis. Proc. Natl. Acad. Sci. USA, 2010, 107(36), 15880-15885.
[http://dx.doi.org/10.1073/pnas.1005743107] [PMID: 20798043]
[13]
Thålin, C.; Hisada, Y.; Lundström, S.; Mackman, N.; Wallén, H. Neutrophil extracellular traps. Arterioscler. Thromb. Vasc. Biol., 2019, 39(9), 1724-1738.
[http://dx.doi.org/10.1161/ATVBAHA.119.312463] [PMID: 31315434]
[14]
Hahn, J.; Schauer, C.; Czegley, C.; Kling, L.; Petru, L.; Schmid, B.; Weidner, D.; Reinwald, C.; Biermann, M.H.C.; Blunder, S.; Ernst, J.; Lesner, A.; Bäuerle, T.; Palmisano, R.; Christiansen, S.; Herrmann, M.; Bozec, A.; Gruber, R.; Schett, G.; Hoffmann, M.H. Aggregated neutrophil extracellular traps resolve inflammation by proteolysis of cytokines and chemokines and protection from antiproteases. FASEB J., 2019, 33(1), 1401-1414.
[http://dx.doi.org/10.1096/fj.201800752R] [PMID: 30130433]
[15]
Bonaventura, A.; Vecchié, A.; Abbate, A.; Montecucco, F. Neutrophil extracellular traps and cardiovascular diseases: An update. Cells, 2020, 9(1), 231.
[http://dx.doi.org/10.3390/cells9010231] [PMID: 31963447]
[16]
Manda-Handzlik, A.; Demkow, U. The brain entangled: The contribution of neutrophil extracellular traps to the diseases of the central nervous system. Cells, 2019, 8(12), 1477.
[http://dx.doi.org/10.3390/cells8121477] [PMID: 31766346]
[17]
Allen, C.; Thornton, P.; Denes, A.; McColl, B.W.; Pierozynski, A.; Monestier, M.; Pinteaux, E.; Rothwell, N.J.; Allan, S.M. Neutrophil cerebrovascular transmigration triggers rapid neurotoxicity through release of proteases associated with decondensed DNA. J. Immunol., 2012, 189(1), 381-392.
[http://dx.doi.org/10.4049/jimmunol.1200409] [PMID: 22661091]
[18]
Kim, S.W.; Lee, H.; Lee, H.K.; Kim, I.D.; Lee, J.K. Neutrophil extracellular trap induced by HMGB1 exacerbates damages in the ischemic brain. Acta Neuropathol. Commun., 2019, 7(1), 94.
[http://dx.doi.org/10.1186/s40478-019-0747-x] [PMID: 31177989]
[19]
Othman, A.; Sekheri, M.; Filep, J.G. Roles of neutrophil granule proteins in orchestrating inflammation and immunity. FEBS J., 2022, 289(14), 3932-3953.
[http://dx.doi.org/10.1111/febs.15803] [PMID: 33683814]
[20]
Domínguez-Díaz, C.; Varela-Trinidad, G.U.; Muñoz-Sánchez, G.; Solórzano-Castanedo, K.; Avila-Arrezola, K.E.; Iñiguez-Gutiérrez, L.; Delgado-Rizo, V.; Fafutis-Morris, M. To trap a pathogen: Neutrophil extracellular traps and their role in mucosal epithelial and skin diseases. Cells, 2021, 10(6), 1469.
[http://dx.doi.org/10.3390/cells10061469] [PMID: 34208037]
[21]
Urban, C.F.; Ermert, D.; Schmid, M.; Abu-Abed, U.; Goosmann, C.; Nacken, W.; Brinkmann, V.; Jungblut, P.R.; Zychlinsky, A. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog., 2009, 5(10), e1000639.
[http://dx.doi.org/10.1371/journal.ppat.1000639] [PMID: 19876394]
[22]
Rada, B. Neutrophil extracellular traps. Methods Mol. Biol., 2019, 1982, 517-528.
[http://dx.doi.org/10.1007/978-1-4939-9424-3_31] [PMID: 31172493]
[23]
Vallés, J.; Santos, M.T.; Latorre, A.M.; Tembl, J.; Salom, J.; Nieves, C.; Lago, A.; Moscardó, A. Neutrophil extracellular traps are increased in patients with acute ischemic stroke: prognostic significance. Thromb. Haemost., 2017, 117(10), 1919-1929.
[http://dx.doi.org/10.1160/TH17-02-0130] [PMID: 28837206]
[24]
He, Y.; Yang, F.Y.; Sun, E.W. Neutrophil extracellular traps in autoimmune diseases. Chin. Med. J. (Engl.), 2018, 131(13), 1513-1519.
[http://dx.doi.org/10.4103/0366-6999.235122] [PMID: 29941703]
[25]
Carestia, A.; Kaufman, T.; Schattner, M. Platelets: New bricks in the building of neutrophil extracellular traps. Front. Immunol., 2016, 7, 271.
[http://dx.doi.org/10.3389/fimmu.2016.00271] [PMID: 27458459]
[26]
Chen, R.; Zhang, X.; Gu, L.; Zhu, H.; Zhong, Y.; Ye, Y.; Xiong, X.; Jian, Z. New insight into neutrophils: A potential therapeutic target for cerebral ischemia. Front. Immunol., 2021, 12, 692061.
[http://dx.doi.org/10.3389/fimmu.2021.692061] [PMID: 34335600]
[27]
Rohrbach, A.S.; Hemmers, S.; Arandjelovic, S.; Corr, M.; Mowen, K.A. PAD4 is not essential for disease in the K/BxN murine autoantibody-mediated model of arthritis. Arthritis Res. Ther., 2012, 14(3), R104.
[http://dx.doi.org/10.1186/ar3829] [PMID: 22551352]
[28]
Narasaraju, T.; Yang, E.; Samy, R.P.; Ng, H.H.; Poh, W.P.; Liew, A.A.; Phoon, M.C.; van Rooijen, N.; Chow, V.T. Excessive neutrophils and neutrophil extracellular traps contribute to acute lung injury of influenza pneumonitis. Am. J. Pathol., 2011, 179(1), 199-210.
[http://dx.doi.org/10.1016/j.ajpath.2011.03.013] [PMID: 21703402]
[29]
Ravindran, M.; Khan, M.A.; Palaniyar, N. Neutrophil extracellular trap formation: Physiology, pathology, and pharmacology. Biomolecules, 2019, 9(8), 365.
[http://dx.doi.org/10.3390/biom9080365] [PMID: 31416173]
[30]
van Dam, L.S.; Rabelink, T.J.; van Kooten, C.; Teng, Y.K.O. Clinical implications of excessive neutrophil extracellular trap formation in renal autoimmune diseases. Kidney Int. Rep., 2019, 4(2), 196-211.
[http://dx.doi.org/10.1016/j.ekir.2018.11.005] [PMID: 30775617]
[31]
Douda, D.N.; Khan, M.A.; Grasemann, H.; Palaniyar, N. SK3 channel and mitochondrial ROS mediate NADPH oxidase-independent NETosis induced by calcium influx. Proc. Natl. Acad. Sci. USA, 2015, 112(9), 2817-2822.
[http://dx.doi.org/10.1073/pnas.1414055112] [PMID: 25730848]
[32]
Njeim, R.; Azar, W.S.; Fares, A.H.; Azar, S.T.; Kfoury Kassouf, H.; Eid, A.A. NETosis contributes to the pathogenesis of diabetes and its complications. J. Mol. Endocrinol., 2020, 65(4), R65-R76.
[http://dx.doi.org/10.1530/JME-20-0128] [PMID: 33048064]
[33]
Deng, J.; Zhao, F.; Zhang, Y.; Zhou, Y.; Xu, X.; Zhang, X.; Zhao, Y. Neutrophil extracellular traps increased by hyperglycemia exacerbate ischemic brain damage. Neurosci. Lett., 2020, 738, 135383.
[http://dx.doi.org/10.1016/j.neulet.2020.135383] [PMID: 32937190]
[34]
Dziedzic, A.; Saluk-Bijak, J.; Miller, E.; Bijak, M. Metformin as a potential agent in the treatment of multiple sclerosis. Int. J. Mol. Sci., 2020, 21(17), 5957.
[http://dx.doi.org/10.3390/ijms21175957] [PMID: 32825027]
[35]
Menegazzo, L.; Scattolini, V.; Cappellari, R.; Bonora, B.M.; Albiero, M.; Bortolozzi, M.; Romanato, F.; Ceolotto, G.; Vigili de Kreutzeberg, S.; Avogaro, A.; Fadini, G.P. The antidiabetic drug metformin blunts NETosis in vitro and reduces circulating NETosis biomarkers in vivo. Acta Diabetol., 2018, 55(6), 593-601.
[http://dx.doi.org/10.1007/s00592-018-1129-8] [PMID: 29546579]
[36]
Fousert, E.; Toes, R.; Desai, J. Neutrophil extracellular traps (NETs) take the central stage in driving autoimmune responses. Cells, 2020, 9(4), 915.
[http://dx.doi.org/10.3390/cells9040915] [PMID: 32276504]
[37]
Lee, K.H.; Kronbichler, A.; Park, D.D.Y.; Park, Y.; Moon, H.; Kim, H.; Choi, J.H.; Choi, Y.; Shim, S.; Lyu, I.S.; Yun, B.H.; Han, Y.; Lee, D.; Lee, S.Y.; Yoo, B.H.; Lee, K.H.; Kim, T.L.; Kim, H.; Shim, J.S.; Nam, W.; So, H.; Choi, S.; Lee, S.; Shin, J.I. Neutrophil extracellular traps (NETs) in autoimmune diseases: A comprehensive review. Autoimmun. Rev., 2017, 16(11), 1160-1173.
[http://dx.doi.org/10.1016/j.autrev.2017.09.012] [PMID: 28899799]
[38]
Döring, Y.; Soehnlein, O.; Weber, C. Neutrophil extracellular traps in atherosclerosis and atherothrombosis. Circ. Res., 2017, 120(4), 736-743.
[http://dx.doi.org/10.1161/CIRCRESAHA.116.309692] [PMID: 28209798]
[39]
Qi, H.; Yang, S.; Zhang, L. Neutrophil extracellular traps and endothelial dysfunction in atherosclerosis and thrombosis. Front. Immunol., 2017, 8, 928.
[http://dx.doi.org/10.3389/fimmu.2017.00928] [PMID: 28824648]
[40]
Kessenbrock, K.; Krumbholz, M.; Schönermarck, U.; Back, W.; Gross, W.L.; Werb, Z.; Gröne, H.J.; Brinkmann, V.; Jenne, D.E. Netting neutrophils in autoimmune small-vessel vasculitis. Nat. Med., 2009, 15(6), 623-625.
[http://dx.doi.org/10.1038/nm.1959] [PMID: 19448636]
[41]
Kretzschmar, G.C.; Bumiller-Bini, V.; Gasparetto Filho, M.A.; Zonta, Y.R.; Yu, K.S.T.; de Souza, R.L.R.; Dias-Melicio, L.A.; Boldt, A.B.W. Neutrophil extracellular traps: A perspective of neuroinflammation and complement activation in Alzheimer’s disease. Front. Mol. Biosci., 2021, 8, 630869.
[http://dx.doi.org/10.3389/fmolb.2021.630869] [PMID: 33898514]
[42]
Lim, S.; Kim, T.J.; Kim, Y.J.; Kim, C.; Ko, S.B.; Kim, B.S. Senolytic therapy for cerebral ischemia-reperfusion injury. Int. J. Mol. Sci., 2021, 22(21), 11967.
[http://dx.doi.org/10.3390/ijms222111967] [PMID: 34769397]
[43]
Otxoa-de-Amezaga, A.; Gallizioli, M.; Pedragosa, J.; Justicia, C.; Miró-Mur, F.; Salas-Perdomo, A.; Díaz-Marugan, L.; Gunzer, M.; Planas, A.M. Location of neutrophils in different compartments of the damaged mouse brain after severe ischemia/reperfusion. Stroke, 2019, 50(6), 1548-1557.
[http://dx.doi.org/10.1161/STROKEAHA.118.023837] [PMID: 31084324]
[44]
Goktay, A.Y.; Senturk, C. Endovascular treatment of thrombosis and embolism. Adv. Exp. Med. Biol., 2016, 906, 195-213.
[http://dx.doi.org/10.1007/5584_2016_116] [PMID: 27664152]
[45]
Laridan, E.; Denorme, F.; Desender, L.; François, O.; Andersson, T.; Deckmyn, H.; Vanhoorelbeke, K.; De Meyer, S.F. Neutrophil extracellular traps in ischemic stroke thrombi. Ann. Neurol., 2017, 82(2), 223-232.
[http://dx.doi.org/10.1002/ana.24993] [PMID: 28696508]
[46]
Kim, J.E.; Yoo, H.J.; Gu, J.Y.; Kim, H.K. Histones induce the procoagulant phenotype of endothelial cells through tissue factor up-regulation and thrombomodulin down-regulation. PLoS One, 2016, 11(6), e0156763.
[http://dx.doi.org/10.1371/journal.pone.0156763] [PMID: 27258428]
[47]
Wu, X.; Zeng, H.; Cai, L.; Chen, G. Role of the extracellular traps in central nervous system. Front. Immunol., 2021, 12, 783882.
[http://dx.doi.org/10.3389/fimmu.2021.783882] [PMID: 34868063]
[48]
Vorobjeva, N.V.; Pinegin, B.V. Neutrophil Extracellular Traps: Mechanisms of formation and role in health and disease. Biochemistry (Mosc.), 2014, 79(12), 1286-1296.
[http://dx.doi.org/10.1134/S0006297914120025] [PMID: 25716722]
[49]
Zhou, P.; Li, T.; Jin, J.; Liu, Y.; Li, B.; Sun, Q.; Tian, J.; Zhao, H.; Liu, Z.; Ma, S.; Zhang, S.; Novakovic, V.A.; Shi, J.; Hu, S. Interactions between neutrophil extracellular traps and activated platelets enhance procoagulant activity in acute stroke patients with ICA occlusion. EBioMedicine, 2020, 53, 102671.
[http://dx.doi.org/10.1016/j.ebiom.2020.102671] [PMID: 32114386]
[50]
von Brühl, M.L.; Stark, K.; Steinhart, A.; Chandraratne, S.; Konrad, I.; Lorenz, M.; Khandoga, A.; Tirniceriu, A.; Coletti, R.; Köllnberger, M.; Byrne, R.A.; Laitinen, I.; Walch, A.; Brill, A.; Pfeiler, S.; Manukyan, D.; Braun, S.; Lange, P.; Riegger, J.; Ware, J.; Eckart, A.; Haidari, S.; Rudelius, M.; Schulz, C.; Echtler, K.; Brinkmann, V.; Schwaiger, M.; Preissner, K.T.; Wagner, D.D.; Mackman, N.; Engelmann, B.; Massberg, S. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J. Exp. Med., 2012, 209(4), 819-835.
[http://dx.doi.org/10.1084/jem.20112322] [PMID: 22451716]
[51]
Varjú, I.; Kolev, K. Networks that stop the flow: A fresh look at fibrin and neutrophil extracellular traps. Thromb. Res., 2019, 182, 1-11.
[http://dx.doi.org/10.1016/j.thromres.2019.08.003] [PMID: 31415922]
[52]
Schattner, M. Platelet TLR4 at the crossroads of thrombosis and the innate immune response. J. Leukoc. Biol., 2019, 105(5), 873-880.
[http://dx.doi.org/10.1002/JLB.MR0618-213R] [PMID: 30512209]
[53]
Fuchs, T.A.; Bhandari, A.A.; Wagner, D.D. Histones induce rapid and profound thrombocytopenia in mice. Blood, 2011, 118(13), 3708-3714.
[http://dx.doi.org/10.1182/blood-2011-01-332676] [PMID: 21700775]
[54]
Peña-Martínez, C.; Durán-Laforet, V.; García-Culebras, A.; Cuartero, M.I.; Moro, M.Á.; Lizasoain, I. Neutrophil extracellular trap targeting protects against ischemic damage after fibrin-rich thrombotic stroke despite non-reperfusion. Front. Immunol., 2022, 13, 790002.
[http://dx.doi.org/10.3389/fimmu.2022.790002] [PMID: 35250974]
[55]
Sambrano, G.R.; Huang, W.; Faruqi, T.; Mahrus, S.; Craik, C.; Coughlin, S.R. Cathepsin G activates protease-activated receptor-4 in human platelets. J. Biol. Chem., 2000, 275(10), 6819-6823.
[http://dx.doi.org/10.1074/jbc.275.10.6819] [PMID: 10702240]
[56]
Mihara, K.; Ramachandran, R.; Renaux, B.; Saifeddine, M.; Hollenberg, M.D. Neutrophil elastase and proteinase-3 trigger G protein-biased signaling through proteinase-activated receptor-1 (PAR1). J. Biol. Chem., 2013, 288(46), 32979-32990.
[http://dx.doi.org/10.1074/jbc.M113.483123] [PMID: 24052258]
[57]
Li, C.; Xing, Y.; Zhang, Y.; Hua, Y.; Hu, J.; Bai, Y. Neutrophil extracellular traps exacerbate ischemic brain damage. Mol. Neurobiol., 2022, 59(1), 643-656.
[http://dx.doi.org/10.1007/s12035-021-02635-z] [PMID: 34748205]
[58]
Tadie, J.M.; Bae, H.B.; Jiang, S.; Park, D.W.; Bell, C.P.; Yang, H.; Pittet, J.F.; Tracey, K.; Thannickal, V.J.; Abraham, E.; Zmijewski, J.W. HMGB1 promotes neutrophil extracellular trap formation through interactions with Toll-like receptor 4. Am. J. Physiol. Lung Cell. Mol. Physiol., 2013, 304(5), L342-L349.
[http://dx.doi.org/10.1152/ajplung.00151.2012] [PMID: 23316068]
[59]
Kim, S.W.; Lee, J.K. Role of HMGB1 in the Interplay between NETosis and thrombosis in ischemic stroke: A review. Cells, 2020, 9(8), 1794.
[http://dx.doi.org/10.3390/cells9081794] [PMID: 32731558]
[60]
Martinod, K.; Wagner, D.D. Thrombosis: tangled up in NETs. Blood, 2014, 123(18), 2768-2776.
[http://dx.doi.org/10.1182/blood-2013-10-463646] [PMID: 24366358]
[61]
Seners, P.; Turc, G.; Maïer, B.; Mas, J.L.; Oppenheim, C.; Baron, J.C. Incidence and predictors of early recanalization after intravenous thrombolysis. Stroke, 2016, 47(9), 2409-2412.
[http://dx.doi.org/10.1161/STROKEAHA.116.014181] [PMID: 27462117]
[62]
Farrera, C.; Fadeel, B. Macrophage clearance of neutrophil extracellular traps is a silent process. J. Immunol., 2013, 191(5), 2647-2656.
[http://dx.doi.org/10.4049/jimmunol.1300436] [PMID: 23904163]
[63]
Zhang, S.; Cao, Y.; Du, J.; Liu, H.; Chen, X.; Li, M.; Xiang, M.; Wang, C.; Wu, X.; Liu, L.; Wang, C.; Wu, Y.; Li, Z.; Fang, S.; Shi, J.; Wang, L. Neutrophil extracellular traps contribute to tissue plasminogen activator resistance in acute ischemic stroke. FASEB J., 2021, 35(9), e21835.
[http://dx.doi.org/10.1096/fj.202100471RR] [PMID: 34449927]
[64]
Ducroux, C.; Di Meglio, L.; Loyau, S.; Delbosc, S.; Boisseau, W.; Deschildre, C.; Ben Maacha, M.; Blanc, R.; Redjem, H.; Ciccio, G.; Smajda, S.; Fahed, R.; Michel, J.B.; Piotin, M.; Salomon, L.; Mazighi, M.; Ho-Tin-Noe, B.; Desilles, J.P. Thrombus neutrophil extracellular traps content impair tPA-induced thrombolysis in acute ischemic stroke. Stroke, 2018, 49(3), 754-757.
[http://dx.doi.org/10.1161/STROKEAHA.117.019896] [PMID: 29438080]
[65]
Cahilog, Z.; Zhao, H.; Wu, L.; Alam, A.; Eguchi, S.; Weng, H.; Ma, D. The role of neutrophil NETosis in organ injury: Novel inflammatory cell death mechanisms. Inflammation, 2020, 43(6), 2021-2032.
[http://dx.doi.org/10.1007/s10753-020-01294-x] [PMID: 32830308]
[66]
Liu, K.; Mori, S.; Takahashi, H.K.; Tomono, Y.; Wake, H.; Kanke, T.; Sato, Y.; Hiraga, N.; Adachi, N.; Yoshino, T.; Nishibori, M. Anti‐high mobility group box 1 monoclonal antibody ameliorates brain infarction induced by transient ischemia in rats. FASEB J., 2007, 21(14), 3904-3916.
[http://dx.doi.org/10.1096/fj.07-8770com] [PMID: 17628015]
[67]
Denorme, F.; Portier, I.; Rustad, J.L.; Cody, M.J.; de Araujo, C.V.; Hoki, C.; Alexander, M.D.; Grandhi, R.; Dyer, M.R.; Neal, M.D.; Majersik, J.J.; Yost, C.C.; Campbell, R.A. Neutrophil extracellular traps regulate ischemic stroke brain injury. J. Clin. Invest., 2022, 132(10), e154225.
[http://dx.doi.org/10.1172/JCI154225] [PMID: 35358095]
[68]
Vogel, S.; Bodenstein, R.; Chen, Q.; Feil, S.; Feil, R.; Rheinlaender, J.; Schäffer, T.E.; Bohn, E.; Frick, J.S.; Borst, O.; Münzer, P.; Walker, B.; Markel, J.; Csanyi, G.; Pagano, P.J.; Loughran, P.; Jessup, M.E.; Watkins, S.C.; Bullock, G.C.; Sperry, J.L.; Zuckerbraun, B.S.; Billiar, T.R.; Lotze, M.T.; Gawaz, M.; Neal, M.D. Platelet-derived HMGB1 is a critical mediator of thrombosis. J. Clin. Invest., 2015, 125(12), 4638-4654.
[http://dx.doi.org/10.1172/JCI81660] [PMID: 26551681]
[69]
El-Benna, J.; Hurtado-Nedelec, M.; Marzaioli, V.; Marie, J.C.; Gougerot-Pocidalo, M.A.; Dang, P.M.C. Priming of the neutrophil respiratory burst: role in host defense and inflammation. Immunol. Rev., 2016, 273(1), 180-193.
[http://dx.doi.org/10.1111/imr.12447] [PMID: 27558335]
[70]
Wang, J.; Jiang, Y.; Zeng, D.; Zhou, W.; Hong, X. Prognostic value of plasma HMGB1 in ischemic stroke patients with cerebral ischemia-reperfusion injury after intravenous thrombolysis. J. Stroke Cerebrovasc. Dis., 2020, 29(9), 105055.
[http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2020.105055] [PMID: 32807461]
[71]
Chen, Y.; Zhang, H.; Hu, X.; Cai, W.; Ni, W.; Zhou, K. Role of NETosis in central nervous system injury. Oxid. Med. Cell. Longev., 2022, 2022, 3235524.
[http://dx.doi.org/10.1155/2022/3235524] [PMID: 35028005]
[72]
Jorch, S.K.; Kubes, P. An emerging role for neutrophil extracellular traps in noninfectious disease. Nat. Med., 2017, 23(3), 279-287.
[http://dx.doi.org/10.1038/nm.4294] [PMID: 28267716]
[73]
Chen, S.; Chen, H.; Du, Q.; Shen, J. Targeting myeloperoxidase (MPO) mediated oxidative stress and inflammation for reducing brain ischemia injury: Potential application of natural compounds. Front. Physiol., 2020, 11, 433.
[http://dx.doi.org/10.3389/fphys.2020.00433] [PMID: 32508671]
[74]
Furtmüller, P.G.; Obinger, C.; Hsuanyu, Y.; Dunford, H.B. Mechanism of reaction of myeloperoxidase with hydrogen peroxide and chloride ion. Eur. J. Biochem., 2000, 267(19), 5858-5864.
[http://dx.doi.org/10.1046/j.1432-1327.2000.01491.x] [PMID: 10998045]
[75]
Yap, Y.W.; Whiteman, M.; Cheung, N.S. Chlorinative stress: An under appreciated mediator of neurodegeneration? Cell. Signal., 2007, 19(2), 219-228.
[http://dx.doi.org/10.1016/j.cellsig.2006.06.013] [PMID: 16959471]
[76]
Weiss, S.J.; Klein, R.; Slivka, A.; Wei, M. Chlorination of taurine by human neutrophils. Evidence for hypochlorous acid generation. J. Clin. Invest., 1982, 70(3), 598-607.
[http://dx.doi.org/10.1172/JCI110652] [PMID: 6286728]
[77]
Schraufstätter, I.U.; Browne, K.; Harris, A.; Hyslop, P.A.; Jackson, J.H.; Quehenberger, O.; Cochrane, C.G. Mechanisms of hypochlorite injury of target cells. J. Clin. Invest., 1990, 85(2), 554-562.
[http://dx.doi.org/10.1172/JCI114472] [PMID: 2153710]
[78]
Prütz, W.A. Hypochlorous acid interactions with thiols, nucleotides, DNA, and other biological substrates. Arch. Biochem. Biophys., 1996, 332(1), 110-120.
[http://dx.doi.org/10.1006/abbi.1996.0322] [PMID: 8806715]
[79]
Panasenko, O.M. The mechanism of the hypochlorite-induced lipid peroxidation. Biofactors, 1997, 6(2), 181-190.
[http://dx.doi.org/10.1002/biof.5520060212] [PMID: 9260000]
[80]
Hawkins, C.L.; Pattison, D.I.; Davies, M.J. Hypochlorite-induced oxidation of amino acids, peptides and proteins. Amino Acids, 2003, 25(3-4), 259-274.
[http://dx.doi.org/10.1007/s00726-003-0016-x] [PMID: 14661089]
[81]
Pattison, D.I.; Hawkins, C.L.; Davies, M.J. Hypochlorous acid-mediated oxidation of lipid components and antioxidants present in low-density lipoproteins: absolute rate constants, product analysis, and computational modeling. Chem. Res. Toxicol., 2003, 16(4), 439-449.
[http://dx.doi.org/10.1021/tx025670s] [PMID: 12703960]
[82]
Thai, T.; Zhong, F.; Dang, L.; Chan, E.; Ku, J.; Malle, E.; Geczy, C.L.; Keaney, J.F., Jr; Thomas, S.R. Endothelial-transcytosed myeloperoxidase activates endothelial nitric oxide synthase via a phospholipase C-dependent calcium signaling pathway. Free Radic. Biol. Med., 2021, 166, 255-264.
[http://dx.doi.org/10.1016/j.freeradbiomed.2020.12.448] [PMID: 33539947]
[83]
Guan, W.; Zhao, Y.; Xu, C. A Combined treatment with taurine and intra-arterial thrombolysis in an embolic model of stroke in rats: Increased neuroprotective efficacy and extended therapeutic time window. Transl. Stroke Res., 2011, 2(1), 80-91.
[http://dx.doi.org/10.1007/s12975-010-0050-4] [PMID: 24323587]
[84]
Ayloo, S.; Gu, C. Transcytosis at the blood-brain barrier. Curr. Opin. Neurobiol., 2019, 57, 32-38.
[http://dx.doi.org/10.1016/j.conb.2018.12.014] [PMID: 30708291]
[85]
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]
[86]
Strecker, J.K.; Schmidt, A.; Schäbitz, W.R.; Minnerup, J. Neutrophil granulocytes in cerebral ischemia - Evolution from killers to key players. Neurochem. Int., 2017, 107, 117-126.
[http://dx.doi.org/10.1016/j.neuint.2016.11.006] [PMID: 27884770]
[87]
Jian-gang, M.; Gang, Y. Advances in the study of neutrophil extracellular traps in ischemic stroke. Hainan Med J., 2021, 32(19), 2561-2564.
[88]
Lee, C.Z.; Xue, Z.; Zhu, Y.; Yang, G.Y.; Young, W.L. Matrix metalloproteinase-9 inhibition attenuates vascular endothelial growth factor-induced intracerebral hemorrhage. Stroke, 2007, 38(9), 2563-2568.
[http://dx.doi.org/10.1161/STROKEAHA.106.481515] [PMID: 17673717]
[89]
Nakamura, K.; Nakayama, H.; Sasaki, S.; Takahashi, K.; Iwabuchi, K. Mycobacterium avium-intracellulare complex promote release of pro-inflammatory enzymes matrix metalloproteinases by inducing neutrophil extracellular trap formation. Sci. Rep., 2022, 12(1), 5181.
[http://dx.doi.org/10.1038/s41598-022-09017-y] [PMID: 35410994]
[90]
Yabluchanskiy, A.; Ma, Y.; Iyer, R.P.; Hall, M.E.; Lindsey, M.L. Matrix metalloproteinase-9: Many shades of function in cardiovascular disease. Physiology (Bethesda), 2013, 28(6), 391-403.
[http://dx.doi.org/10.1152/physiol.00029.2013] [PMID: 24186934]
[91]
Ballabh, P.; Braun, A.; Nedergaard, M. The blood-brain barrier: an overview. Neurobiol. Dis., 2004, 16(1), 1-13.
[http://dx.doi.org/10.1016/j.nbd.2003.12.016] [PMID: 15207256]
[92]
Li, Y.; Zhong, W.; Jiang, Z.; Tang, X. New progress in the approaches for blood-brain barrier protection in acute ischemic stroke. Brain Res. Bull., 2019, 144, 46-57.
[http://dx.doi.org/10.1016/j.brainresbull.2018.11.006] [PMID: 30448453]
[93]
Sifat, A.E.; Vaidya, B.; Abbruscato, T.J. Blood-brain barrier protection as a therapeutic strategy for acute ischemic stroke. AAPS J., 2017, 19(4), 957-972.
[http://dx.doi.org/10.1208/s12248-017-0091-7] [PMID: 28484963]
[94]
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]
[95]
Kang, L.; Yu, H.; Yang, X.; Zhu, Y.; Bai, X.; Wang, R.; Cao, Y.; Xu, H.; Luo, H.; Lu, L.; Shi, M.J.; Tian, Y.; Fan, W.; Zhao, B.Q. Neutrophil extracellular traps released by neutrophils impair revascularization and vascular remodeling after stroke. Nat. Commun., 2020, 11(1), 2488.
[http://dx.doi.org/10.1038/s41467-020-16191-y] [PMID: 32427863]
[96]
Santos-Lima, B.; Pietronigro, E.C.; Terrabuio, E.; Zenaro, E.; Constantin, G. The role of neutrophils in the dysfunction of central nervous system barriers. Front. Aging Neurosci., 2022, 14, 965169.
[http://dx.doi.org/10.3389/fnagi.2022.965169] [PMID: 36034148]
[97]
Saffarzadeh, M.; Juenemann, C.; Queisser, M.A.; Lochnit, G.; Barreto, G.; Galuska, S.P.; Lohmeyer, J.; Preissner, K.T. Neutrophil extracellular traps directly induce epithelial and endothelial cell death: a predominant role of histones. PLoS One, 2012, 7(2), e32366.
[http://dx.doi.org/10.1371/journal.pone.0032366] [PMID: 22389696]
[98]
Cuartero, M.I.; Ballesteros, I.; Moraga, A.; Nombela, F.; Vivancos, J.; Hamilton, J.A.; Corbí, Á.L.; Lizasoain, I.; Moro, M.A. N2 neutrophils, novel players in brain inflammation after stroke: modulation by the PPARγ agonist rosiglitazone. Stroke, 2013, 44(12), 3498-3508.
[http://dx.doi.org/10.1161/STROKEAHA.113.002470] [PMID: 24135932]
[99]
Cai, W.; Liu, S.; Hu, M.; Huang, F.; Zhu, Q.; Qiu, W.; Hu, X.; Colello, J.; Zheng, S.G.; Lu, Z. Functional dynamics of neutrophils after ischemic stroke. Transl. Stroke Res., 2020, 11(1), 108-121.
[http://dx.doi.org/10.1007/s12975-019-00694-y] [PMID: 30847778]
[100]
Gou, X.; Ying, J.; Yue, Y.; Qiu, X.; Hu, P.; Qu, Y.; Li, J.; Mu, D. The roles of high mobility group box 1 in cerebral ischemic injury. Front. Cell. Neurosci., 2020, 14, 600280.
[http://dx.doi.org/10.3389/fncel.2020.600280] [PMID: 33384585]
[101]
Scaffidi, P.; Misteli, T.; Bianchi, M.E. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature, 2002, 418(6894), 191-195.
[http://dx.doi.org/10.1038/nature00858] [PMID: 12110890]
[102]
Xie, W.; Zhu, T.; Dong, X.; Nan, F.; Meng, X.; Zhou, P.; Sun, G.; Sun, X. HMGB1-triggered inflammation inhibition of notoginseng leaf triterpenes against cerebral ischemia and reperfusion injury via MAPK and NF-κB signaling pathways. Biomolecules, 2019, 9(10), 512.
[http://dx.doi.org/10.3390/biom9100512] [PMID: 31547018]
[103]
Lok, K.Z.; Basta, M.; Manzanero, S.; Arumugam, T.V. Intravenous immunoglobulin (IVIg) dampens neuronal toll-like receptor-mediated responses in ischemia. J. Neuroinflammation, 2015, 12(1), 73.
[http://dx.doi.org/10.1186/s12974-015-0294-8] [PMID: 25886362]
[104]
Yu, G.; Liang, Y.; Zheng, S.; Zhang, H. Inhibition of myeloperoxidase by N-acetyl lysyltyrosylcysteine amide reduces oxidative stress-mediated inflammation, neuronal damage, and neural stem cell injury in a murine model of stroke. J. Pharmacol. Exp. Ther., 2018, 364(2), 311-322.
[http://dx.doi.org/10.1124/jpet.117.245688] [PMID: 29255000]
[105]
Virani, S.S.; Alonso, A.; Aparicio, H.J.; Benjamin, E.J.; Bittencourt, M.S.; Callaway, C.W.; Carson, A.P.; Chamberlain, A.M.; Cheng, S.; Delling, F.N.; Elkind, M.S.V.; Evenson, K.R.; Ferguson, J.F.; Gupta, D.K.; Khan, S.S.; Kissela, B.M.; Knutson, K.L.; Lee, C.D.; Lewis, T.T.; Liu, J.; Loop, M.S.; Lutsey, P.L.; Ma, J.; Mackey, J.; Martin, S.S.; Matchar, D.B.; Mussolino, M.E.; Navaneethan, S.D.; Perak, A.M.; Roth, G.A.; Samad, Z.; Satou, G.M.; Schroeder, E.B.; Shah, S.H.; Shay, C.M.; Stokes, A.; VanWagner, L.B.; Wang, N.Y.; Tsao, C.W. Heart disease and stroke statistics—2021 update. Circulation, 2021, 143(8), e254-e743.
[http://dx.doi.org/10.1161/CIR.0000000000000950] [PMID: 33501848]
[106]
Qiu, Y.; Zhang, C.; Chen, A.; Wang, H.; Zhou, Y.; Li, Y.; Hu, B. Immune cells in the BBB disruption after acute ischemic stroke: targets for immune therapy? Front. Immunol., 2021, 12, 678744.
[http://dx.doi.org/10.3389/fimmu.2021.678744] [PMID: 34248961]
[107]
Powers, W.J.; Rabinstein, A.A.; Ackerson, T.; Adeoye, O.M.; Bambakidis, N.C.; Becker, K.; Biller, J.; Brown, M.; Demaerschalk, B.M.; Hoh, B.; Jauch, E.C.; Kidwell, C.S.; Leslie-Mazwi, T.M.; Ovbiagele, B.; Scott, P.A.; Sheth, K.N.; Southerland, A.M.; Summers, D.V.; Tirschwell, D.L. Guidelines for the early management of patients with acute ischemic stroke: 2019 update to the 2018 guidelines for the early management of acute ischemic stroke: a guideline for healthcare professionals from the american heart association/american stroke association. Stroke, 2019, 50(12), e344-e418.
[http://dx.doi.org/10.1161/STR.0000000000000211] [PMID: 31662037]
[108]
Turc, G.; Bhogal, P.; Fischer, U.; Khatri, P.; Lobotesis, K.; Mazighi, M.; Schellinger, P.D.; Toni, D.; de Vries, J.; White, P.; Fiehler, J. European stroke organisation (ESO)- european society for minimally invasive neurological therapy (ESMINT) guidelines on mechanical thrombectomy in acute ischemic stroke. J. Neurointerv. Surg., 2019, 11(6), 535-538.
[http://dx.doi.org/10.1136/neurintsurg-2018-014568] [PMID: 31152058]
[109]
Menon, B.K.; Al-Ajlan, F.S.; Najm, M.; Puig, J.; Castellanos, M.; Dowlatshahi, D.; Calleja, A.; Sohn, S.I.; Ahn, S.H.; Poppe, A.; Mikulik, R.; Asdaghi, N.; Field, T.S.; Jin, A.; Asil, T.; Boulanger, J.M.; Smith, E.E.; Coutts, S.B.; Barber, P.A.; Bal, S.; Subramanian, S.; Mishra, S.; Trivedi, A.; Dey, S.; Eesa, M.; Sajobi, T.; Goyal, M.; Hill, M.D.; Demchuk, A.M. Association of clinical, imaging, and thrombus characteristics with recanalization of visible intracranial occlusion in patients with acute ischemic stroke. JAMA, 2018, 320(10), 1017-1026.
[http://dx.doi.org/10.1001/jama.2018.12498] [PMID: 30208455]
[110]
Baron, J.C. Author Correction: Protecting the ischaemic penumbra as an adjunct to thrombectomy for acute stroke. Nat. Rev. Neurol., 2019, 15(3), 184.
[http://dx.doi.org/10.1038/s41582-019-0148-6] [PMID: 30742037]
[111]
Su, X.T.; Wang, L.; Ma, S.M.; Cao, Y.; Yang, N.N.; Lin, L.L.; Fisher, M.; Yang, J.W.; Liu, C.Z. Mechanisms of acupuncture in the regulation of oxidative stress in treating ischemic stroke. Oxid. Med. Cell. Longev., 2020, 2020, 1-15.
[http://dx.doi.org/10.1155/2020/7875396] [PMID: 33178387]
[112]
Kahles, T.; Brandes, R.P. NADPH oxidases as therapeutic targets in ischemic stroke. Cell. Mol. Life Sci., 2012, 69(14), 2345-2363.
[http://dx.doi.org/10.1007/s00018-012-1011-8] [PMID: 22618244]
[113]
Chen, H.; Yoshioka, H.; Kim, G.S.; Jung, J.E.; Okami, N.; Sakata, H.; Maier, C.M.; Narasimhan, P.; Goeders, C.E.; Chan, P.H. Oxidative stress in ischemic brain damage: mechanisms of cell death and potential molecular targets for neuroprotection. Antioxid. Redox Signal., 2011, 14(8), 1505-1517.
[http://dx.doi.org/10.1089/ars.2010.3576] [PMID: 20812869]
[114]
Nathan, C.; Ding, A. SnapShot: Reactive oxygen intermediates (ROI). Cell, 2010, 140(6), 951-951.e2.
[http://dx.doi.org/10.1016/j.cell.2010.03.008] [PMID: 20303882]
[115]
Allen, C.L.; Bayraktutan, U. Oxidative stress and its role in the pathogenesis of ischaemic stroke. Int. J. Stroke, 2009, 4(6), 461-470.
[http://dx.doi.org/10.1111/j.1747-4949.2009.00387.x] [PMID: 19930058]
[116]
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]
[117]
Casas, A.I.; Geuss, E.; Kleikers, P.W.M.; Mencl, S.; Herrmann, A.M.; Buendia, I.; Egea, J.; Meuth, S.G.; Lopez, M.G.; Kleinschnitz, C.; Schmidt, H.H.H.W. NOX4-dependent neuronal autotoxicity and BBB breakdown explain the superior sensitivity of the brain to ischemic damage. Proc. Natl. Acad. Sci. USA, 2017, 114(46), 12315-12320.
[http://dx.doi.org/10.1073/pnas.1705034114] [PMID: 29087944]
[118]
Canty, T.G., Jr; Boyle, E.M., Jr; Farr, A.; Morgan, E.N.; Verrier, E.D.; Pohlman, T.H. Oxidative stress induces NF-kappaB nuclear translocation without degradation of IkappaBalpha. Circulation, 1999, 100(19), II361-II364.
[PMID: 10567330]
[119]
Kleinschnitz, C.; Grund, H.; Wingler, K.; Armitage, M.E.; Jones, E.; Mittal, M.; Barit, D.; Schwarz, T.; Geis, C.; Kraft, P.; Barthel, K.; Schuhmann, M.K.; Herrmann, A.M.; Meuth, S.G.; Stoll, G.; Meurer, S.; Schrewe, A.; Becker, L.; Gailus-Durner, V.; Fuchs, H.; Klopstock, T.; de Angelis, M.H.; Jandeleit-Dahm, K.; Shah, A.M.; Weissmann, N.; Schmidt, H.H.H.W. Post-stroke inhibition of induced NADPH oxidase type 4 prevents oxidative stress and neurodegeneration. PLoS Biol., 2010, 8(9), e1000479.
[http://dx.doi.org/10.1371/journal.pbio.1000479] [PMID: 20877715]
[120]
Fuchs, T.A.; Abed, U.; Goosmann, C.; Hurwitz, R.; Schulze, I.; Wahn, V.; Weinrauch, Y.; Brinkmann, V.; Zychlinsky, A. Novel cell death program leads to neutrophil extracellular traps. J. Cell Biol., 2007, 176(2), 231-241.
[http://dx.doi.org/10.1083/jcb.200606027] [PMID: 17210947]
[121]
Lood, C.; Blanco, L.P.; Purmalek, M.M.; Carmona-Rivera, C.; De Ravin, S.S.; Smith, C.K.; Malech, H.L.; Ledbetter, J.A.; Elkon, K.B.; Kaplan, M.J. Neutrophil extracellular traps enriched in oxidized mitochondrial DNA are interferogenic and contribute to lupus-like disease. Nat. Med., 2016, 22(2), 146-153.
[http://dx.doi.org/10.1038/nm.4027] [PMID: 26779811]
[122]
Gaul, D.S.; Weber, J.; van Tits, L.J.; Sluka, S.; Pasterk, L.; Reiner, M.F.; Calatayud, N.; Lohmann, C.; Klingenberg, R.; Pahla, J.; Vdovenko, D.; Tanner, F.C.; Camici, G.G.; Eriksson, U.; Auwerx, J.; Mach, F.; Windecker, S.; Rodondi, N.; Lüscher, T.F.; Winnik, S.; Matter, C.M. Loss of Sirt3 accelerates arterial thrombosis by increasing formation of neutrophil extracellular traps and plasma tissue factor activity. Cardiovasc. Res., 2018, 114(8), 1178-1188.
[http://dx.doi.org/10.1093/cvr/cvy036] [PMID: 29444200]
[123]
Vogelgesang, A.; Lange, C.; Blümke, L.; Laage, G.; Rümpel, S.; Langner, S.; Bröker, B.M.; Dressel, A.; Ruhnau, J. Ischaemic stroke and the recanalization drug tissue plasminogen activator interfere with antibacterial phagocyte function. J. Neuroinflammation, 2017, 14(1), 140.
[http://dx.doi.org/10.1186/s12974-017-0914-6] [PMID: 28732504]
[124]
Papayannopoulos, V.; Metzler, K.D.; Hakkim, A.; Zychlinsky, A. Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J. Cell Biol., 2010, 191(3), 677-691.
[http://dx.doi.org/10.1083/jcb.201006052] [PMID: 20974816]
[125]
Schindler, L.; Smyth, L.C.D.; Bernhagen, J.; Hampton, M.B.; Dickerhof, N. Macrophage migration inhibitory factor (MIF) enhances hypochlorous acid production in phagocytic neutrophils. Redox Biol., 2021, 41, 101946.
[http://dx.doi.org/10.1016/j.redox.2021.101946] [PMID: 33823474]
[126]
Hwang, T.L.; Aljuffali, I.A.; Hung, C.F.; Chen, C.H.; Fang, J.Y. The impact of cationic solid lipid nanoparticles on human neutrophil activation and formation of neutrophil extracellular traps (NETs). Chem. Biol. Interact., 2015, 235, 106-114.
[http://dx.doi.org/10.1016/j.cbi.2015.04.011] [PMID: 25920576]
[127]
Hwang, T.L.; Sung, C.T.; Aljuffali, I.A.; Chang, Y.T.; Fang, J.Y. Cationic surfactants in the form of nanoparticles and micelles elicit different human neutrophil responses: A toxicological study. Colloids Surf. B Biointerfaces, 2014, 114, 334-341.
[http://dx.doi.org/10.1016/j.colsurfb.2013.10.021] [PMID: 24246197]
[128]
Zheng, S.; Wang, S.; Zhang, Q.; Zhang, Z.; Xu, S. Avermectin inhibits neutrophil extracellular traps release by activating PTEN demethylation to negatively regulate the PI3K-ERK pathway and reducing respiratory burst in carp. J. Hazard. Mater., 2020, 389, 121885.
[http://dx.doi.org/10.1016/j.jhazmat.2019.121885] [PMID: 31879111]
[129]
Yin, K.; Cui, Y.; Qu, Y.; Zhang, J.; Zhang, H.; Lin, H. Hydrogen sulfide upregulates miR-16-5p targeting PiK3R1 and RAF1 to inhibit neutrophil extracellular trap formation in chickens. Ecotoxicol. Environ. Saf., 2020, 194, 110412.
[http://dx.doi.org/10.1016/j.ecoenv.2020.110412] [PMID: 32155482]
[130]
Leinweber, J.; Mizurini, D.M.; Francischetti, I.M.B.; Fleischer, M.; Hermann, D.M.; Kleinschnitz, C.; Langhauser, F. Elastase inhibitor agaphelin protects from acute ischemic stroke in mice by reducing thrombosis, blood-brain barrier damage, and inflammation. Brain Behav. Immun., 2021, 93, 288-298.
[http://dx.doi.org/10.1016/j.bbi.2020.12.027] [PMID: 33401017]
[131]
De Meyer, S.F.; Denorme, F.; Langhauser, F.; Geuss, E.; Fluri, F.; Kleinschnitz, C. Thromboinflammation in stroke brain damage. Stroke, 2016, 47(4), 1165-1172.
[http://dx.doi.org/10.1161/STROKEAHA.115.011238] [PMID: 26786115]
[132]
Burkard, P.; Vögtle, T.; Nieswandt, B. Platelets in thrombo-inflammation: Concepts, mechanisms, and therapeutic strategies for ischemic stroke. Hamostaseologie, 2020, 40(2), 153-164.
[http://dx.doi.org/10.1055/a-1151-9519] [PMID: 32455457]
[133]
Nieswandt, B.; Kleinschnitz, C.; Stoll, G. Ischaemic stroke: a thrombo-inflammatory disease? J. Physiol., 2011, 589(17), 4115-4123.
[http://dx.doi.org/10.1113/jphysiol.2011.212886] [PMID: 21768262]
[134]
Martinod, K.; Deppermann, C. Immunothrombosis and thromboinflammation in host defense and disease. Platelets, 2021, 32(3), 314-324.
[http://dx.doi.org/10.1080/09537104.2020.1817360] [PMID: 32896192]
[135]
Maugeri, N.; Campana, L.; Gavina, M.; Covino, C.; De Metrio, M.; Panciroli, C.; Maiuri, L.; Maseri, A.; D’Angelo, A.; Bianchi, M.E.; Rovere-Querini, P.; Manfredi, A.A. Activated platelets present high mobility group box 1 to neutrophils, inducing autophagy and promoting the extrusion of neutrophil extracellular traps. J. Thromb. Haemost., 2014, 12(12), 2074-2088.
[http://dx.doi.org/10.1111/jth.12710] [PMID: 25163512]
[136]
Ma, Y.H.; Ma, T.; Wang, C.; Wang, H.; Chang, D.Y.; Chen, M.; Zhao, M.H. High-mobility group box 1 potentiates antineutrophil cytoplasmic antibody-inducing neutrophil extracellular traps formation. Arthritis Res. Ther., 2016, 18(1), 2.
[http://dx.doi.org/10.1186/s13075-015-0903-z] [PMID: 26739852]
[137]
Karmakar, M.; Katsnelson, M.A.; Dubyak, G.R.; Pearlman, E. Neutrophil P2X7 receptors mediate NLRP3 inflammasome-dependent IL-1β secretion in response to ATP. Nat. Commun., 2016, 7(1), 10555.
[http://dx.doi.org/10.1038/ncomms10555] [PMID: 26877061]
[138]
Feng, L.; Chen, Y.; Ding, R.; Fu, Z.; Yang, S.; Deng, X.; Zeng, J. P2X7R blockade prevents NLRP3 inflammasome activation and brain injury in a rat model of intracerebral hemorrhage: involvement of peroxynitrite. J. Neuroinflammation, 2015, 12(1), 190.
[http://dx.doi.org/10.1186/s12974-015-0409-2] [PMID: 26475134]
[139]
Chen, Y.; Yao, Y.; Sumi, Y.; Li, A.; To, U.K.; Elkhal, A.; Inoue, Y.; Woehrle, T.; Zhang, Q.; Hauser, C.; Junger, W.G. Purinergic signaling: a fundamental mechanism in neutrophil activation. Sci. Signal., 2010, 3(125), ra45.
[http://dx.doi.org/10.1126/scisignal.2000549] [PMID: 20530802]
[140]
Wang, X.; Chen, D. Purinergic regulation of neutrophil function. Front. Immunol., 2018, 9, 399.
[http://dx.doi.org/10.3389/fimmu.2018.00399] [PMID: 29545806]
[141]
Sofoluwe, A.; Bacchetta, M.; Badaoui, M.; Kwak, B.R.; Chanson, M. ATP amplifies NADPH-dependent and -independent neutrophil extracellular trap formation. Sci. Rep., 2019, 9(1), 16556.
[http://dx.doi.org/10.1038/s41598-019-53058-9] [PMID: 31719610]
[142]
Brea, D.; Blanco, M.; Ramos-Cabrer, P.; Moldes, O.; Arias, S.; Pérez-Mato, M.; Leira, R.; Sobrino, T.; Castillo, J. Toll-like receptors 2 and 4 in ischemic stroke: Outcome and therapeutic values. J. Cereb. Blood Flow Metab., 2011, 31(6), 1424-1431.
[http://dx.doi.org/10.1038/jcbfm.2010.231] [PMID: 21206505]
[143]
Durán-Laforet, V.; Peña-Martínez, C.; García-Culebras, A.; Cuartero, M.I.; Lo, E.H.; Moro, M.Á.; Lizasoain, I. Role of TLR4 in neutrophil dynamics and functions: Contribution to stroke pathophysiology. Front. Immunol., 2021, 12, 757872.
[http://dx.doi.org/10.3389/fimmu.2021.757872] [PMID: 34745132]
[144]
Waisberg, M.; Molina-Cruz, A.; Mizurini, D.M.; Gera, N.; Sousa, B.C.; Ma, D.; Leal, A.C.; Gomes, T.; Kotsyfakis, M.; Ribeiro, J.M.C.; Lukszo, J.; Reiter, K.; Porcella, S.F.; Oliveira, C.J.; Monteiro, R.Q.; Barillas-Mury, C.; Pierce, S.K.; Francischetti, I.M.B. Plasmodium falciparum infection induces expression of a mosquito salivary protein (Agaphelin) that targets neutrophil function and inhibits thrombosis without impairing hemostasis. PLoS Pathog., 2014, 10(9), e1004338.
[http://dx.doi.org/10.1371/journal.ppat.1004338] [PMID: 25211214]
[145]
Ikegame, Y.; Yamashita, K.; Hayashi, S.; Yoshimura, S.; Nakashima, S.; Iwama, T. Neutrophil elastase inhibitor prevents ischemic brain damage via reduction of vasogenic edema. Hypertens. Res., 2010, 33(7), 703-707.
[http://dx.doi.org/10.1038/hr.2010.58] [PMID: 20485441]
[146]
Stowe, A.M.; Adair-Kirk, T.L.; Gonzales, E.R.; Perez, R.S.; Shah, A.R.; Park, T.S.; Gidday, J.M. Neutrophil elastase and neurovascular injury following focal stroke and reperfusion. Neurobiol. Dis., 2009, 35(1), 82-90.
[http://dx.doi.org/10.1016/j.nbd.2009.04.006] [PMID: 19393318]
[147]
Forghani, R.; Kim, H.J.; Wojtkiewicz, G.R.; Bure, L.; Wu, Y.; Hayase, M.; Wei, Y.; Zheng, Y.; Moskowitz, M.A.; Chen, J.W. Myeloperoxidase propagates damage and is a potential therapeutic target for subacute stroke. J. Cereb. Blood Flow Metab., 2015, 35(3), 485-493.
[http://dx.doi.org/10.1038/jcbfm.2014.222] [PMID: 25515211]
[148]
Forghani, R.; Wojtkiewicz, G.R.; Zhang, Y.; Seeburg, D.; Bautz, B.R.M.; Pulli, B.; Milewski, A.R.; Atkinson, W.L.; Iwamoto, Y.; Zhang, E.R.; Etzrodt, M.; Rodriguez, E.; Robbins, C.S.; Swirski, F.K.; Weissleder, R.; Chen, J.W. Demyelinating diseases: myeloperoxidase as an imaging biomarker and therapeutic target. Radiology, 2012, 263(2), 451-460.
[http://dx.doi.org/10.1148/radiol.12111593] [PMID: 22438365]
[149]
Yenari, M.A.; Liu, J.; Zheng, Z.; Vexler, Z.S.; Lee, J.E.; Giffard, R.G. Antiapoptotic and anti-inflammatory mechanisms of heat-shock protein protection. Ann. N. Y. Acad. Sci., 2005, 1053(1), 74-83.
[http://dx.doi.org/10.1196/annals.1344.007] [PMID: 16179510]
[150]
Zheng, Z.; Kim, J.Y.; Ma, H.; Lee, J.E.; Yenari, M.A. Anti-inflammatory effects of the 70 kDa heat shock protein in experimental stroke. J. Cereb. Blood Flow Metab., 2008, 28(1), 53-63.
[http://dx.doi.org/10.1038/sj.jcbfm.9600502] [PMID: 17473852]
[151]
Kim, H.J.; Wei, Y.; Wojtkiewicz, G.R.; Lee, J.Y.; Moskowitz, M.A.; Chen, J.W. Reducing myeloperoxidase activity decreases inflammation and increases cellular protection in ischemic stroke. J. Cereb. Blood Flow Metab., 2019, 39(9), 1864-1877.
[http://dx.doi.org/10.1177/0271678X18771978] [PMID: 29673284]
[152]
Yang, J.; Wu, Z.; Long, Q.; Huang, J.; Hong, T.; Liu, W.; Lin, J. Insights into immunothrombosis: the interplay among neutrophil extracellular trap, von willebrand factor, and ADAMTS13. Front. Immunol., 2020, 11, 610696.
[http://dx.doi.org/10.3389/fimmu.2020.610696] [PMID: 33343584]
[153]
Guo, J.; Wang, J.; Sun, W.; Liu, X. The advances of post-stroke depression: 2021 update. J. Neurol., 2022, 269(3), 1236-1249.
[http://dx.doi.org/10.1007/s00415-021-10597-4] [PMID: 34052887]
[154]
Popa-Wagner, A.; Sandu, R.E.; Buga, A.M.; Uzoni, A.; Petcu, E.B. Neuroinflammation and comorbidities are frequently ignored factors in CNS pathology. Neural Regen. Res., 2015, 10(9), 1349-1355.
[http://dx.doi.org/10.4103/1673-5374.165208] [PMID: 26604877]
[155]
Wen, H.; Weymann, K.B.; Wood, L.; Wang, Q.M. Inflammatory signaling in post-stroke fatigue and depression. Eur. Neurol., 2018, 80(3-4), 138-148.
[http://dx.doi.org/10.1159/000494988] [PMID: 30448848]
[156]
Swardfager, W.; Winer, D.A.; Herrmann, N.; Winer, S.; Lanctôt, K.L. Interleukin-17 in post-stroke neurodegeneration. Neurosci. Biobehav. Rev., 2013, 37(3), 436-447.
[http://dx.doi.org/10.1016/j.neubiorev.2013.01.021] [PMID: 23370232]
[157]
Park, H.; Li, Z.; Yang, X.O.; Chang, S.H.; Nurieva, R.; Wang, Y.H.; Wang, Y.; Hood, L.; Zhu, Z.; Tian, Q.; Dong, C. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol., 2005, 6(11), 1133-1141.
[http://dx.doi.org/10.1038/ni1261] [PMID: 16200068]
[158]
Huang, S.U.S.; O’Sullivan, K.M. The Expanding role of extracellular traps in inflammation and autoimmunity: The new players in casting dark webs. Int. J. Mol. Sci., 2022, 23(7), 3793.
[http://dx.doi.org/10.3390/ijms23073793] [PMID: 35409152]
[159]
Mora-Ruíz, M.D.; Blanco-Favela, F.; Chávez Rueda, A.K.; Legorreta-Haquet, M.V.; Chávez-Sánchez, L. Role of interleukin-17 in acute myocardial infarction. Mol. Immunol., 2019, 107, 71-78.
[http://dx.doi.org/10.1016/j.molimm.2019.01.008] [PMID: 30660992]
[160]
Liao, Y.H.; Xia, N.; Zhou, S.F.; Tang, T.T.; Yan, X.X.; Lv, B.J.; Nie, S.F.; Wang, J.; Iwakura, Y.; Xiao, H.; Yuan, J.; Jevallee, H.; Wei, F.; Shi, G.P.; Cheng, X. Interleukin-17A contributes to myocardial ischemia/reperfusion injury by regulating cardiomyocyte apoptosis and neutrophil infiltration. J. Am. Coll. Cardiol., 2012, 59(4), 420-429.
[http://dx.doi.org/10.1016/j.jacc.2011.10.863] [PMID: 22261166]
[161]
Hu, J.; Zhou, W.; Zhou, Z.; Yang, Q.; Han, J.; Yan, Y.; Dong, W. Predictive value of inflammatory indicators for post-stroke depression in patients with ischemic stroke. Nan Fang Yi Ke Da Xue Xue Bao, 2019, 39(6), 665-671.
[162]
Beck, H.; Plate, K.H. Angiogenesis after cerebral ischemia. Acta Neuropathol., 2009, 117(5), 481-496.
[http://dx.doi.org/10.1007/s00401-009-0483-6] [PMID: 19142647]
[163]
Essig, F.; Kollikowski, A.M.; Pham, M.; Solymosi, L.; Stoll, G.; Haeusler, K.G.; Kraft, P.; Schuhmann, M.K. Immunohistological analysis of neutrophils and neutrophil extracellular traps in human thrombemboli causing acute ischemic stroke. Int. J. Mol. Sci., 2020, 21(19), 7387.
[http://dx.doi.org/10.3390/ijms21197387] [PMID: 33036337]
[164]
Tissue plasminogen activator for acute ischemic stroke. N. Engl. J. Med., 1995, 333(24), 1581-1588.
[http://dx.doi.org/10.1056/NEJM199512143332401] [PMID: 7477192]
[165]
Wang, R.; Zhu, Y.; Liu, Z.; Chang, L.; Bai, X.; Kang, L.; Cao, Y.; Yang, X.; Yu, H.; Shi, M.J.; Hu, Y.; Fan, W.; Zhao, B.Q. Neutrophil extracellular traps promote tPA-induced brain hemorrhage via cGAS in mice with stroke. Blood, 2021, 138(1), 91-103.
[http://dx.doi.org/10.1182/blood.2020008913] [PMID: 33881503]
[166]
Neeli, I.; Khan, S.N.; Radic, M. Histone deimination as a response to inflammatory stimuli in neutrophils. J. Immunol., 2008, 180(3), 1895-1902.
[http://dx.doi.org/10.4049/jimmunol.180.3.1895] [PMID: 18209087]
[167]
Luo, Y.; Arita, K.; Bhatia, M.; Knuckley, B.; Lee, Y.H.; Stallcup, M.R.; Sato, M.; Thompson, P.R. Inhibitors and inactivators of protein arginine deiminase 4: functional and structural characterization. Biochemistry, 2006, 45(39), 11727-11736.
[http://dx.doi.org/10.1021/bi061180d] [PMID: 17002273]
[168]
Hamam, H.J.; Palaniyar, N. Post-Translational Modifications in NETosis and NETs-Mediated Diseases. Biomolecules, 2019, 9(8), 369.
[http://dx.doi.org/10.3390/biom9080369] [PMID: 31416265]
[169]
Wang, Y.; Li, M.; Stadler, S.; Correll, S.; Li, P.; Wang, D.; Hayama, R.; Leonelli, L.; Han, H.; Grigoryev, S.A.; Allis, C.D.; Coonrod, S.A. Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J. Cell Biol., 2009, 184(2), 205-213.
[http://dx.doi.org/10.1083/jcb.200806072] [PMID: 19153223]
[170]
Li, P.; Li, M.; Lindberg, M.R.; Kennett, M.J.; Xiong, N.; Wang, Y. PAD4 is essential for antibacterial innate immunity mediated by neutrophil extracellular traps. J. Exp. Med., 2010, 207(9), 1853-1862.
[http://dx.doi.org/10.1084/jem.20100239] [PMID: 20733033]
[171]
Bicker, K.L.; Thompson, P.R. The protein arginine deiminases: Structure, function, inhibition, and disease. Biopolymers, 2013, 99(2), 155-163.
[http://dx.doi.org/10.1002/bip.22127] [PMID: 23175390]
[172]
Li, C.; Li, Q.; Mei, Q.; Lu, T. Pharmacological effects and pharmacokinetic properties of icariin, the major bioactive component in Herba Epimedii. Life Sci., 2015, 126, 57-68.
[http://dx.doi.org/10.1016/j.lfs.2015.01.006] [PMID: 25634110]
[173]
Zhang, D.; Zhang, J.; Fong, C.; Yao, X.; Yang, M. Herba epimedii flavonoids suppress osteoclastic differentiation and bone resorption by inducing G2/M arrest and apoptosis. Biochimie, 2012, 94(12), 2514-2522.
[http://dx.doi.org/10.1016/j.biochi.2012.06.033] [PMID: 22796380]
[174]
Liu, Y.Q.; Yang, Q.X.; Cheng, M.C.; Xiao, H.B. Synergistic inhibitory effect of Icariside II with Icaritin from Herba Epimedii on pre-osteoclastic RAW264.7 cell growth. Phytomedicine, 2014, 21(12), 1633-1637.
[http://dx.doi.org/10.1016/j.phymed.2014.07.016] [PMID: 25442270]
[175]
Liu, M.; Wang, W.; Gao, J.; Li, F.; Shi, J.; Gong, Q. Icariside II attenuates cerebral ischemia/reperfusion-induced blood-brain barrier dysfunction in rats via regulating the balance of MMP9/TIMP1. Acta Pharmacol. Sin., 2020, 41(12), 1547-1556.
[http://dx.doi.org/10.1038/s41401-020-0409-3] [PMID: 32488170]
[176]
Liu, S.; Li, X.; Gao, J.; Liu, Y.; Shi, J.; Gong, Q. Icariside II, a phosphodiesterase-5 inhibitor, attenuates beta-amyloid-induced cognitive deficits via BDNF/TrkB/CREB signaling. Cell. Physiol. Biochem., 2018, 49(3), 1010-1025.
[http://dx.doi.org/10.1159/000493232] [PMID: 30196289]
[177]
Zheng, Y.; Deng, Y.; Gao, J.; Lv, C.; Lang, L.; Shi, J.; Yu, C.; Gong, Q. Icariside II inhibits lipopolysaccharide-induced inflammation and amyloid production in rat astrocytes by regulating IKK/IκB/NF-κB/BACE1 signaling pathway. Acta Pharmacol. Sin., 2020, 41(2), 154-162.
[http://dx.doi.org/10.1038/s41401-019-0300-2] [PMID: 31554962]
[178]
Yost, C.C.; Schwertz, H.; Cody, M.J.; Wallace, J.A.; Campbell, R.A.; Vieira-de-Abreu, A.; Araujo, C.V.; Schubert, S.; Harris, E.S.; Rowley, J.W.; Rondina, M.T.; Fulcher, J.M.; Koening, C.L.; Weyrich, A.S.; Zimmerman, G.A. Neonatal NET-inhibitory factor and related peptides inhibit neutrophil extracellular trap formation. J. Clin. Invest., 2016, 126(10), 3783-3798.
[http://dx.doi.org/10.1172/JCI83873] [PMID: 27599294]
[179]
Kim, S.W.; Davaanyam, D.; Seol, S.I.; Lee, H.K.; Lee, H.; Lee, J.K. Adenosine triphosphate accumulated following cerebral ischemia induces neutrophil extracellular trap formation. Int. J. Mol. Sci., 2020, 21(20), 7668.
[http://dx.doi.org/10.3390/ijms21207668] [PMID: 33081303]
[180]
Oboudiyat, C.; Glazer, H.; Seifan, A.; Greer, C.; Isaacson, R. Alzheimer’s Disease. Semin. Neurol., 2013, 33(4), 313-329.
[http://dx.doi.org/10.1055/s-0033-1359319] [PMID: 24234352]
[181]
Querfurth, H.W.; LaFerla, F.M. Alzheimer’s disease. N. Engl. J. Med., 2010, 362(4), 329-344.
[http://dx.doi.org/10.1056/NEJMra0909142] [PMID: 20107219]
[182]
Qiu, C.; Kivipelto, M.; von Strauss, E. Epidemiology of Alzheimer’s disease: occurrence, determinants, and strategies toward intervention. Dialogues Clin. Neurosci., 2009, 11(2), 111-128.
[http://dx.doi.org/10.31887/DCNS.2009.11.2/cqiu] [PMID: 19585947]
[183]
Hays, C.C.; Zlatar, Z.Z.; Wierenga, C.E. The utility of cerebral blood flow as a biomarker of preclinical Alzheimer’s disease. Cell. Mol. Neurobiol., 2016, 36(2), 167-179.
[http://dx.doi.org/10.1007/s10571-015-0261-z] [PMID: 26898552]
[184]
Bracko, O.; Njiru, B.N.; Swallow, M.; Ali, M.; Haft-Javaherian, M.; Schaffer, C.B. Increasing cerebral blood flow improves cognition into late stages in Alzheimer’s disease mice. J. Cereb. Blood Flow Metab., 2020, 40(7), 1441-1452.
[http://dx.doi.org/10.1177/0271678X19873658] [PMID: 31495298]
[185]
Zenaro, E.; Pietronigro, E.; Bianca, V.D.; Piacentino, G.; Marongiu, L.; Budui, S.; Turano, E.; Rossi, B.; Angiari, S.; Dusi, S.; Montresor, A.; Carlucci, T.; Nanì, S.; Tosadori, G.; Calciano, L.; Catalucci, D.; Berton, G.; Bonetti, B.; Constantin, G. Neutrophils promote Alzheimer’s disease-like pathology and cognitive decline via LFA-1 integrin. Nat. Med., 2015, 21(8), 880-886.
[http://dx.doi.org/10.1038/nm.3913] [PMID: 26214837]
[186]
Liu, Y.; Tang, G.; Li, Y.; Wang, Y.; Chen, X.; Gu, X.; Zhang, Z.; Wang, Y.; Yang, G.Y. Metformin attenuates blood-brain barrier disruption in mice following middle cerebral artery occlusion. J. Neuroinflammation, 2014, 11(1), 177.
[http://dx.doi.org/10.1186/s12974-014-0177-4] [PMID: 25315906]
[187]
Cruz Hernández, J.C.; Bracko, O.; Kersbergen, C.J.; Muse, V.; Haft-Javaherian, M.; Berg, M.; Park, L.; Vinarcsik, L.K.; Ivasyk, I.; Rivera, D.A.; Kang, Y.; Cortes-Canteli, M.; Peyrounette, M.; Doyeux, V.; Smith, A.; Zhou, J.; Otte, G.; Beverly, J.D.; Davenport, E.; Davit, Y.; Lin, C.P.; Strickland, S.; Iadecola, C.; Lorthois, S.; Nishimura, N.; Schaffer, C.B. Neutrophil adhesion in brain capillaries reduces cortical blood flow and impairs memory function in Alzheimer’s disease mouse models. Nat. Neurosci., 2019, 22(3), 413-420.
[http://dx.doi.org/10.1038/s41593-018-0329-4] [PMID: 30742116]
[188]
Grammas, P.; Samany, P.G.; Thirumangalakudi, L. Thrombin and inflammatory proteins are elevated in Alzheimer’s disease microvessels: Implications for disease pathogenesis. J. Alzheimers Dis., 2006, 9(1), 51-58.
[http://dx.doi.org/10.3233/JAD-2006-9105] [PMID: 16627934]
[189]
Grammas, P.; Ovase, R. Inflammatory factors are elevated in brain microvessels in Alzheimer’s disease. Neurobiol. Aging, 2001, 22(6), 837-842.
[http://dx.doi.org/10.1016/S0197-4580(01)00276-7] [PMID: 11754990]
[190]
Keshari, R.S.; Jyoti, A.; Dubey, M.; Kothari, N.; Kohli, M.; Bogra, J.; Barthwal, M.K.; Dikshit, M. Cytokines induced neutrophil extracellular traps formation: implication for the inflammatory disease condition. PLoS One, 2012, 7(10), e48111.
[http://dx.doi.org/10.1371/journal.pone.0048111] [PMID: 23110185]
[191]
Jarre, A.; Gowert, N.S.; Donner, L.; Münzer, P.; Klier, M.; Borst, O.; Schaller, M.; Lang, F.; Korth, C.; Elvers, M. Pre-activated blood platelets and a pro-thrombotic phenotype in APP23 mice modeling Alzheimer’s disease. Cell. Signal., 2014, 26(9), 2040-2050.
[http://dx.doi.org/10.1016/j.cellsig.2014.05.019] [PMID: 24928203]
[192]
Gowert, N.S.; Donner, L.; Chatterjee, M.; Eisele, Y.S.; Towhid, S.T.; Münzer, P.; Walker, B.; Ogorek, I.; Borst, O.; Grandoch, M.; Schaller, M.; Fischer, J.W.; Gawaz, M.; Weggen, S.; Lang, F.; Jucker, M.; Elvers, M. Blood platelets in the progression of Alzheimer’s disease. PLoS One, 2014, 9(2), e90523.
[http://dx.doi.org/10.1371/journal.pone.0090523] [PMID: 24587388]
[193]
Ferrer-Raventós, P.; Beyer, K. Alternative platelet activation pathways and their role in neurodegenerative diseases. Neurobiol. Dis., 2021, 159, 105512.
[http://dx.doi.org/10.1016/j.nbd.2021.105512] [PMID: 34537329]
[194]
Donner, L.; Feige, T.; Freiburg, C.; Toska, L.M.; Reichert, A.S.; Chatterjee, M.; Elvers, M. Impact of amyloid-β on platelet mitochondrial function and platelet-mediated amyloid aggregation in Alzheimer’s disease. Int. J. Mol. Sci., 2021, 22(17), 9633.
[http://dx.doi.org/10.3390/ijms22179633] [PMID: 34502546]
[195]
Paudel, Y.N.; Angelopoulou, E.; Piperi, C.; Othman, I.; Aamir, K.; Shaikh, M.F. Impact of HMGB1, RAGE, and TLR4 in Alzheimer’s disease (AD): From risk factors to therapeutic targeting. Cells, 2020, 9(2), 383.
[http://dx.doi.org/10.3390/cells9020383] [PMID: 32046119]
[196]
Kong, Z.H.; Chen, X.; Hua, H.P.; Liang, L.; Liu, L.J. The oral pretreatment of glycyrrhizin prevents surgery-induced cognitive impairment in aged mice by reducing neuroinflammation and Alzheimer’s-related pathology via HMGB1 inhibition. J. Mol. Neurosci., 2017, 63(3-4), 385-395.
[http://dx.doi.org/10.1007/s12031-017-0989-7] [PMID: 29034441]
[197]
Fujita, K.; Motoki, K.; Tagawa, K.; Chen, X.; Hama, H.; Nakajima, K.; Homma, H.; Tamura, T.; Watanabe, H.; Katsuno, M.; Matsumi, C.; Kajikawa, M.; Saito, T.; Saido, T.; Sobue, G.; Miyawaki, A.; Okazawa, H. HMGB1, a pathogenic molecule that induces neurite degeneration via TLR4-MARCKS, is a potential therapeutic target for Alzheimer’s disease. Sci. Rep., 2016, 6(1), 31895.
[http://dx.doi.org/10.1038/srep31895] [PMID: 27557632]
[198]
Volkman, R.; Ben-Zur, T.; Kahana, A.; Garty, B.Z.; Offen, D. Myeloperoxidase deficiency inhibits cognitive decline in the 5XFAD mouse model of Alzheimer’s disease. Front. Neurosci., 2019, 13, 990.
[http://dx.doi.org/10.3389/fnins.2019.00990] [PMID: 31611761]
[199]
Zenaro, E.; Piacentino, G.; Constantin, G. The blood-brain barrier in Alzheimer’s disease. Neurobiol. Dis., 2017, 107, 41-56.
[http://dx.doi.org/10.1016/j.nbd.2016.07.007] [PMID: 27425887]
[200]
Ishihara, K.; Yamaguchi, Y.; Uchino, S.; Furuhashi, T.; Yamada, S.; Kihara, S.; Mori, K.; Ogawa, M. ICAM-1 signal transduction in cells stimulated with neutrophil elastase. Dig. Dis. Sci., 2006, 51(11), 2102-2112.
[http://dx.doi.org/10.1007/s10620-006-9178-1] [PMID: 17024574]
[201]
Moussa, C.; Hebron, M.; Huang, X.; Ahn, J.; Rissman, R.A.; Aisen, P.S.; Turner, R.S. Resveratrol regulates neuro-inflammation and induces adaptive immunity in Alzheimer’s disease. J. Neuroinflammation, 2017, 14(1), 1.
[http://dx.doi.org/10.1186/s12974-016-0779-0] [PMID: 28086917]
[202]
Wang, Y.; Rosen, H.; Madtes, D.K.; Shao, B.; Martin, T.R.; Heinecke, J.W.; Fu, X. Myeloperoxidase inactivates TIMP-1 by oxidizing its N-terminal cysteine residue: an oxidative mechanism for regulating proteolysis during inflammation. J. Biol. Chem., 2007, 282(44), 31826-31834.
[http://dx.doi.org/10.1074/jbc.M704894200] [PMID: 17726014]
[203]
Itoh, Y.; Nagase, H. Preferential inactivation of tissue inhibitor of metalloproteinases-1 that is bound to the precursor of matrix metalloproteinase 9 (progelatinase B) by human neutrophil elastase. J. Biol. Chem., 1995, 270(28), 16518-16521.
[http://dx.doi.org/10.1074/jbc.270.28.16518] [PMID: 7622455]
[204]
Gilthorpe, J.D.; Oozeer, F.; Nash, J.; Calvo, M.; Bennett, D.L.H.; Lumsden, A.; Pini, A. Extracellular histone H1 is neurotoxic and drives a pro-inflammatory response in microglia. F1000 Res., 2013, 2, 148.
[http://dx.doi.org/10.12688/f1000research.2-148.v1] [PMID: 24358859]
[205]
Duce, J.A.; Smith, D.P.; Blake, R.E.; Crouch, P.J.; Li, Q.X.; Masters, C.L.; Trounce, I.A. Linker histone H1 binds to disease associated amyloid-like fibrils. J. Mol. Biol., 2006, 361(3), 493-505.
[http://dx.doi.org/10.1016/j.jmb.2006.06.038] [PMID: 16854430]
[206]
Pietronigro, E.C.; Della Bianca, V.; Zenaro, E.; Constantin, G. NETosis in Alzheimer’s Disease. Front. Immunol., 2017, 8, 211.
[http://dx.doi.org/10.3389/fimmu.2017.00211] [PMID: 28303140]
[207]
Nan, K.; Han, Y.; Fang, Q.; Huang, C.; Yu, L.; Ge, W.; Xiang, F.; Tao, Y.X.; Cao, H.; Li, J. HMGB1 gene silencing inhibits neuroinflammation via down-regulation of NF-κB signaling in primary hippocampal neurons induced by Aβ25-35. Int. Immunopharmacol., 2019, 67, 294-301.
[http://dx.doi.org/10.1016/j.intimp.2018.12.027] [PMID: 30572254]
[208]
Powers, W.J.; Derdeyn, C.P.; Biller, J.; Coffey, C.S.; Hoh, B.L.; Jauch, E.C.; Johnston, K.C.; Johnston, S.C.; Khalessi, A.A.; Kidwell, C.S.; Meschia, J.F.; Ovbiagele, B.; Yavagal, D.R. 2015 American heart association/american stroke association focused update of the 2013 guidelines for the early management of patients with acute ischemic stroke regarding endovascular treatment. Stroke, 2015, 46(10), 3020-3035.
[http://dx.doi.org/10.1161/STR.0000000000000074] [PMID: 26123479]
[209]
Hollist, M.; Morgan, L.; Cabatbat, R.; Au, K.; Kirmani, M.F.; Kirmani, B.F. Acute stroke management: Overview and recent updates. Aging Dis., 2021, 12(4), 1000-1009.
[http://dx.doi.org/10.14336/AD.2021.0311] [PMID: 34221544]
[210]
Lim, H.H.; Jeong, I.H.; An, G.D.; Woo, K.S.; Kim, K.H.; Kim, J.M.; Yun, S.H.; Park, J.I.; Cha, J.K.; Kim, M.H.; Han, J.Y. Evaluation of neutrophil extracellular traps as the circulating marker for patients with acute coronary syndrome and acute ischemic stroke. J. Clin. Lab. Anal., 2020, 34(5), e23190.
[http://dx.doi.org/10.1002/jcla.23190] [PMID: 31907963]
[211]
Wang, Y.; Liu, M.; Pu, C. 2014 Chinese guidelines for secondary prevention of ischemic stroke and transient ischemic attack. Int. J. Stroke, 2017, 12(3), 302-320.
[http://dx.doi.org/10.1177/1747493017694391] [PMID: 28381199]
[212]
Shinohara, Y.; Yanagihara, T.; Abe, K.; Yoshimine, T.; Fujinaka, T.; Chuma, T.; Ochi, F.; Nagayama, M.; Ogawa, A.; Suzuki, N.; Katayama, Y.; Kimura, A.; Minematsu, K., II II. Cerebral infarction/transient ischemic attack (TIA). J. Stroke Cerebrovasc. Dis., 2011, 20(4), S31-S73.
[http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2011.05.004] [PMID: 21835356]
[213]
Xu, L.; Gao, Y.; Hu, M.; Dong, Y.; Xu, J.; Zhang, J.; Lv, P. Edaravone dexborneol protects cerebral ischemia reperfusion injury through activating Nrf2/HO‐1 signaling pathway in mice. Fundam. Clin. Pharmacol., 2022, 36(5), 790-800.
[http://dx.doi.org/10.1111/fcp.12782] [PMID: 35470467]
[214]
Huang, Y.; Zhang, X.; Zhang, C.; Xu, W.; Li, W.; Feng, Z.; Zhang, X.; Zhao, K. Edaravone dexborneol downregulates neutrophil extracellular trap expression and ameliorates blood-brain barrier permeability in acute ischemic stroke. Mediators Inflamm., 2022, 2022, 1-11.
[http://dx.doi.org/10.1155/2022/3855698] [PMID: 36032782]

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