Generic placeholder image

Current Neuropharmacology

Editor-in-Chief

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

Review Article

NLRP3 Inflammasome in the Pathophysiology of Hemorrhagic Stroke: A Review

Author(s): Yujie Luo, Cesar Reis and Sheng Chen*

Volume 17, Issue 7, 2019

Page: [582 - 589] Pages: 8

DOI: 10.2174/1570159X17666181227170053

Price: $65

Abstract

Hemorrhagic stroke is a devastating disease with high morbidity and mortality. There is still a lack of effective therapeutic approach. The recent studies have shown that the innate immune system plays a significant role in hemorrhagic stroke. Microglia, as major components in innate immune system, are activated and then can release cytokines and chemokines in response to hemorrhagic stroke, and ultimately led to neuroinflammation and brain injury. The NOD-like receptor family, pyrin domain containing 3 (NLRP3) inflammasome is predominantly released by microglia and is believed as the main contributor of neuroinflammation. Several studies have focused on the role of NLRP3 inflammasome in hemorrhagic stroke-induced brain injury, however, the specific mechanism of NLRP3 activation and regulation remains unclear. This review summarized the mechanism of NLRP3 activation and its role in hemorrhagic stroke and discussed the translational significance.

Keywords: NLRP3 inflammasome, hemorrhagic stroke, neuroinflammation, treatment, pathophysiology, innate immune.

Graphical Abstract
[1]
Broderick, J.P.; Adeoye, O.; Elm, J. Evolution of the modified rankin scale and its use in future Stroke Trials. Stroke, 2017, 48(7), 2007-2012. [http://dx.doi.org/10.1161/strokeaha.117.017866]. [PMID:28626052].
[2]
Zhou, Y.; Wang, Y.; Wang, J.; Anne, S.R.; Yang, Q.W. Inflammation in intracerebral hemorrhage: from mechanisms to clinical translation. Prog. Neurobiol., 2014, 115, 25-44. [http://dx.doi.org/10.1016/j.pneurobio.2013.11.003]. [PMID:24291544].
[3]
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].
[4]
Yang, S.J.; Shao, G.F.; Chen, J.L.; Gong, J. The NLRP3 inflammasome: An important driver of neuroinflammation in hemorrhagic stroke. Cell. Mol. Neurobiol., 2018, 38(3), 595-603. [http://dx.doi.org/10.1007/s10571-017-0526-9]. [PMID:28752408].
[5]
Heneka, M.T.; McManus, R.M.; Latz, E. Inflammasome signalling in brain function and neurodegenerative disease. Nat. Rev. Neurosci., 2018. [http://dx.doi.org/10.1038/s41583-018-0055-7]. [PMID:30206330].
[6]
Zeng, J.; Chen, Y.; Ding, R.; Feng, L.; Fu, Z.; Yang, S.; Deng, X.; Xie, Z.; Zheng, S. Isoliquiritigenin alleviates early brain injury after experimental intracerebral hemorrhage via suppressing ROS- and/or NF-kappaB-mediated NLRP3 inflammasome activation by promoting Nrf2 antioxidant pathway. J. Neuroinflam., 2017, 14(1), 119. [http://dx.doi.org/10.1186/s12974-017-0895-5]. [PMID:28610608].
[7]
Cheng, Y.; Wei, Y.; Yang, W.; Song, Y.; Shang, H.; Cai, Y.; Wu, Z.; Zhao, W. Cordycepin confers neuroprotection in mice models of intracerebral hemorrhage via suppressing NLRP3 inflammasome activation. Metab. Brain Dis., 2017, 32(4), 1133-1145. [http://dx.doi.org/10.1007/s11011-017-0003-7]. [PMID:28401330].
[8]
Shao, B.; Cao, Z. Q., Liu, C. Targeting NLRP3 Inflammasome in the treatment of CNS diseases. Front. Mol. Neurosci., 2018, 11, 320. [http://dx.doi.org/10.3389/fnmol.2018.00320]. [PMID:30233319].
[9]
Becker, K.J. Strain-related differences in the immune response: Relevance to human stroke. Transl. Stroke Res., 2016, 7(4), 303-312. [http://dx.doi.org/10.1007/s12975-016-0455-9]. [PMID:26860504].
[10]
Shi, H.; Zheng, K.; Su, Z. Su, H. Zhong., M., He, X., Zhou, C., Chen, H., Xiong, Q. Zhang, Y. Sinomenine enhances microglia M2 polarization and attenuates inflammatory injury in intracerebral hemorrhage. J. Neuroimmunol., 2016, 299, 28-34. [http://dx.doi.org/10.1016/j.jneuroim.2016.08.010]. [PMID:27725118].
[11]
Schneider, U.; Davids, C.; Brandenburg, A.M.; Muller, S.; Elke, A.; Magrini, A.; Atangana, S.; Turkowski, E.K.; Finger, T.; Gutenberg, A.; Gehlhaar, C.; Bruck, W.; Heppner, F.L.; Vajkoczy, P. Microglia inflict delayed brain injury after subarachnoid hemorrhage. Acta Neuropathol., 2015, 130(2), 215-231. [http://dx.doi.org/10.1007/s00401-015-1440-1]. [PMID:25956409].
[12]
Li, R.; Liu, W.; Yin, J.; Chen, Y.; Guo, S.; Fan, H. Li. X., Zhang, X, He, X., Duan, C. TSG-6 attenuates inflammation-induced brain injury via modulation of microglial polarization in SAH rats through the SOCS3/STAT3 pathway. J. Neuroinflam., 2018, 15(1), 231. [http://dx.doi.org/10.1186/s12974-018-1279-1]. [PMID:30126439].
[13]
Pang, J.; Peng, J.; Matei, N.; Yang, P. Kuai, L., Wu, Y., Chen, L., Vitek., M.P., Li, F., Sun, X., Zhang, J.H., Jiang, Y. Apolipoprotein E exerts a whole-brain protective property by promoting M1? microglia quiescence after experimental subarachnoid hemorrhage in mice. Transl. Stroke Res., 2018. [http://dx.doi.org/10.1007/s12975-018-0665-4]. [PMID:30225551].
[14]
Zhao, H.; Garton, T.; Keep, R.F.; Hua, Y.; Xi, G. Microglia/macrophage polarization after experimental intracerebral hemorrhage. Transl. Stroke Res., 2015, 6(6), 407-409. [http://dx.doi.org/10.1007/s12975-015-0428-4]. [PMID:26446073].
[15]
Thomas, A.G.; O’Driscoll, C.M.; Bressler, J.; Kaufmann, W.; Rojas, C.J.; Slusher, B.S. Small molecule glutaminase inhibitors block glutamate release from stimulated microglia. Biochem. Biophys. Res. Commun., 2014, 443(1), 32-36. [http://dx.doi.org/10.1016/j.bbrc.2013.11.043]. [PMID:24269238].
[16]
Lim, T.C.; Spector, M. Biomaterials for enhancing CNS repair. Transl. Stroke Res., 2017, 8(1), 57-64. [http://dx.doi.org/10.1007/s12975-016-0470-x]. [PMID:27251413].
[17]
Denes, A.; Pinteaux, E. Rothwell., N.J., Allan, S.M. Interleukin-1 and stroke: biomarker, harbinger of damage, and therapeutic target. Cerebrovasc. Dis., 2011, 32(6), 517-527. [http://dx.doi.org/10.1159/000332205]. [PMID:22104408].
[18]
Zhang, Z.; Liu, Y.; Huang, Q.; Su, Y.; Zhang, Y. Wang, G. Li, F. NF-kappaB activation and cell death after intracerebral hemorrhage in patients. Neurol. Sci., 2014, 35(7), 1097-1102. [http://dx.doi.org/10.1007/s10072-014-1657-0]. [PMID:24510152].
[19]
Yang, G.; Shao, G.F. Elevated serum IL-11, TNF alpha, and VEGF expressions contribute to the pathophysiology of hypertensive intracerebral hemorrhage (HICH). Neurol. Sci., 2016, 37(8), 1253-1259. [http://dx.doi.org/10.1007/s10072-016-2576-z]. [PMID:27115896].
[20]
Young, A.M.; Karri, S.K.; You, W.; Ogilvy, C.S. Specific TNF-alpha inhibition in cerebral aneurysm formation and subarachnoid hemorrhage. Curr. Drug Saf., 2012, 7 (3), 190-6. 22950379].
[21]
Behrouz, R. Re-exploring tumor necrosis factor alpha as a target for therapy in intracerebral hemorrhage. Transl. Stroke Res., 2016, 7(2), 93-96. [http://dx.doi.org/10.1007/s12975-016-0446-x]. [PMID:26762364].
[22]
Wu, W.; Guan, Y.; Zhao, G.; Fu, X.J.; Guo, T.Z.; Liu, Y.T.; Ren, X.L.; Wang, W.; Liu, H.R.; Li, Y.Q. Elevated IL-6 and TNF-alpha levels in cerebrospinal fluid of subarachnoid hemorrhage patients. Mol. Neurobiol., 2016, 53(5), 3277-3285. [http://dx.doi.org/10.1007/s12035-015-9268-1]. [PMID:26063595].
[23]
Starke, R.M.; Raper, D.M.; Ding, D.; Chalouhi, N.; Owens, G.K.; Hasan, D.M.; Medel, R.; Dumont, A.S. Tumor necrosis factor-alpha modulates cerebral aneurysm formation and rupture. Transl. Stroke Res., 2014, 5(2), 269-277. [http://dx.doi.org/10.1007/s12975-013-0287-9]. [PMID:24323710].
[24]
Dziedzic, T.; Bartus, S.; Klimkowicz, A.; Motyl, M.; Slowik, A.; Szczudlik, A. Intracerebral hemorrhage triggers interleukin-6 and interleukin-10 release in blood. Stroke, 2002, 33(9), 2334-2335. [12215608].
[25]
Tanaka, T.; Narazaki, M.; Kishimoto, T. IL-6 in inflammation, immunity, and disease. Cold Spring Harb. Perspect. Biol., 2014, 6(10)a016295 [http://dx.doi.org/10.1101/cshperspect.a016295]. [PMID:25190079].
[26]
Armstead, W.M.; Hekierski, H. Pasto, P. Yarovoi, S., Higazi, A. A., Cines. D.B. Release of IL-6 after stroke contributes to impaired cerebral autoregulation and hippocampal neuronal necrosis through NMDA receptor activation and upregulation of ET-1 and JNK. Transl. Stroke Res., 2018. [http://dx.doi.org/10.1007/s12975-018-0617-z]. [PMID:29476447].
[27]
Owens, T.; Khorooshi, R.; Wlodarczyk, A.; Asgari, N. Interferons in the central nervous system: a few instruments play many tunes. Glia, 2014, 62 (3),339-55. 24588027].
[28]
Mohsenzadegan, M.; Fayazi, M.R.; Abdolmaleki, M.; Bakhshayesh, M.; Seif, F.; Mousavizadeh, K. Direct immunomodulatory influence of IFN-beta on human astrocytoma cells. Immunopharmacol. Immunotoxicol., 2015, 37(2), 214-219. [http://dx.doi.org/10.3109/08923973.2015.1014559]. [PMID:25689952].
[29]
Juliana, C.; Fernandes-Alnemri, T.; Kang, S.; Farias, A.; Qin, F.; Alnemri, E.S. Non-transcriptional priming and deubiquitination regulate NLRP3 inflammasome activation. J. Biol. Chem., 2012, 287(43), 36617-36622. [http://dx.doi.org/10.1074/jbc.M112.407130]. [PMID:22948162].
[30]
Braga, T.T.; Forni, M.F.; Correa-Costa, M. Ramos., R.N., Barbuto, J.A., Branco, P., Castoldi., A. Hiyane., M.I., Davanso., M.R., Latz, E., Franklin, B.S., Kowaltowski, A.J., Camara, N.O. Soluble Uric Acid Activates the NLRP3 Inflammasome. Sci. Rep., 2017, 7, 39884. [http://dx.doi.org/10.1038/srep39884]. [PMID:28084303].
[31]
Hornung, V.; Bauernfeind, F.; Halle, A.; Samstad, E.O.; Kono, H.; Rock, K.L.; Fitzgerald, K.A.; Latz, E. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol., 2008, 9(8), 847-856. [http://dx.doi.org/10.1038/ni.1631]. [PMID:18604214].
[32]
Dutra, F.F.; Alves, L.S.; Rodrigues, D.; Fernandez, P.L.; de Oliveira, R.B.; Golenbock, D.T.; Zamboni, D.S.; Bozza, M.T. Hemolysis-induced lethality involves inflammasome activation by heme. Proc. Natl. Acad. Sci. USA, 2014, 111(39), E4110-E4118. [http://dx.doi.org/10.1073/pnas.1405023111]. [PMID:25225402].
[33]
Gurung, P.; Paras, K.; Anand, P.K.; Malireddi, S. R.K., Vande, W.L., Van Opdenbosch, N., Christopher, P. D., Weinlich, R., Douglas, R. G., Lamkanfi., M., Kanneganti, T.D. FADD and caspase-8 mediate priming and activation of the canonical and noncanonical Nlrp3 inflammasomes. J. Immunol., 2014, 192(4), 1835-1846. [http://dx.doi.org/10.4049/jimmunol.1302839]. [PMID:24453255].
[34]
Lamkanfi, M.; Dixit, V.M. Mechanisms and functions of inflammasomes. Cell, 2014, 157(5), 1013-1022. [http://dx.doi.org/10.1016/j.cell.2014.04.007]. [PMID:24855941].
[35]
Munoz-Planillo, R.; Kuffa, P.; Martinez-Colon, G.; Smith, B.L.; Rajendiran, T.M.; Nunez, G.K. (+) efflux is the common trigger of NLRP3 inflammasome activation by bacterial toxins and particulate matter. Immunity, 2013, 38(6), 1142-1153. [http://dx.doi.org/10.1016/j.immuni.2013.05.016]. [PMID:23809161].
[36]
Zhou, R. Yazdi., A.S., Menu, P. Tschopp, J. A role for mitochondria in NLRP3 inflammasome activation. Nature, 2011, 469(7329), 221-225. [http://dx.doi.org/10.1038/nature09663]. [PMID:21124315].
[37]
Iyer, S.S.; He, Q.; Janczy, J.R.; Elliott, E.I.; Zhong, Z.; Olivier, A.K.; Sadler, J.J.; Knepper-Adrian, V.; Han, R.; Qiao, L.; Eisenbarth, S.C.; Nauseef, W.M.; Cassel, S.L.; Sutterwala, F.S. Mitochondrial cardiolipin is required for Nlrp3 inflammasome activation. Immunity, 2013, 39(2), 311-323. [http://dx.doi.org/10.1016/j.immuni.2013.08.001]. [PMID:23954133].
[38]
Gross, C.J. Mishra., R., Schneider., K.S., Medard, G., Wettmarshausen, J., Dittlein., D.C., Shi, H., Gorka, O., Koenig., P.A., Fromm, S., Magnani, G., Cikovic, T., Hartjes, L., Smollich, J., Robertson A.A.B., Cooper, M.A., Schmidt-Supprian, M., Schuster, M. Schroder, K., Broz, P., Traidl-Hoffmann, C., Beutler, B. Kuster., B. Ruland, J, Schneider, S. Perocchi, F., Gross, O. K(+) efflux-independent NLRP3 inflammasome activation by small molecules targeting mitochondria. Immunity, 2016, 45(4), 761-773. [http://dx.doi.org/10.1016/j.immuni.2016.08.010]. [PMID:27692612].
[39]
Casson, C.N. Copenhaver., A.M., Zwack, E.E., Nguyen, H.T., Strowig, T., Javdan, B., Bradley, W.P. Fung, T.C., Flavell, R.A., Brodsky, I.E., Shin, S. Caspase-11 activation in response to bacterial secretion systems that access the host cytosol. PLoS Pathog., 2013, 9(6)e1003400 [http://dx.doi.org/10.1371/journal.ppat.1003400]. [PMID:23762026].
[40]
He, W.T. Wan. H., Hu, L., Chen, P., Wang, X., Huang, Z., Zhang—Hua, Y., Zhong, C.Q., Han, J. Gasdermin D is an executor of pyroptosis and required for interleukin-1beta secretion. Cell Res., 2015, 25(12), 1285-1298. [http://dx.doi.org/10.1038/cr.2015.139]. [PMID:26611636].
[41]
Rathinam, V.A.; Vanaja, S.K.; Waggoner, L. Sokolovska, A., Becker, C., Stuart,L.M., Leong, J.M., Fitzgerald, K.A. TRIF licenses caspase-11-dependent NLRP3 inflammasome activation by gram-negative bacteria. Cell, 2012, 150(3), 606-619. [http://dx.doi.org/10.1016/j.cell.2012.07.007]. [PMID:22819539].
[42]
Cunha, L.D.; Silva, A.L.N. Ribeiro., J.M., Mascarenhas, D.P.A., Quirino, G.F.S., Santos, L.L., Flavel, R.A., Zamboni, D.S. AIM2 engages active but unprocessed caspase-1 to induce noncanonical activation of the NLRP3 inflammasome. Cell Rep., 2017, 20(4), 794-805. [http://dx.doi.org/10.1016/j.celrep.2017.06.086]. [PMID:28746866].
[43]
Netea, M.G.; Nold-Petry, C.A.; Nold, M.F.; Joosten, L.A.; Opitz, B.; van der Meer, J.H.; van de Veerdonk, F.L.; Ferwerda, G.; Heinhuis, B.; Devesa, I.; Funk, C.J.; Mason, R.J.; Kullberg, B.J.; Rubartelli, A.; van der Meer, J.W.; Dinarello, C.A. Differential requirement for the activation of the inflammasome for processing and release of IL-1beta in monocytes and macrophages. Blood, 2009, 113(10), 2324-2335. [http://dx.doi.org/10.1182/blood-2008-03-146720]. [PMID:19104081].
[44]
Gaidt, M.M.; Ebert, T.S.; Chauhan, D.; Schmidt, T.; Schmid-Burgk, J.L.; Rapino, F.; Robertson, A.A.; Cooper, M.A.; Graf, T.; Hornung, V. Human monocytes engage an alternative inflammasome pathway. Immunity, 2016, 44(4), 833-846. [http://dx.doi.org/10.1016/j.immuni.2016.01.012]. [PMID:27037191].
[45]
Gaidt, M.M.; Hornung, V. Alternative inflammasome activation enables IL-1beta release from living cells. Curr. Opin. Immunol., 2017, 44, 7-13. [http://dx.doi.org/10.1016/j.coi.2016.10.007]. [PMID:27842238].
[46]
Ye, X.; Zuo, D.; Yu, L.; Zhang, L.; Tang, J.; Cui, C.; Bao, L.; Zan, K.; Zhang, Z.; Yang, X.; Chen, H.; Tang, H.; Zu, J.; Shi, H.; Cui, G. ROS/TXNIP pathway contributes to thrombin induced NLRP3 inflammasome activation and cell apoptosis in microglia. Biochem. Biophys. Res. Commun., 2017, 485(2), 499-505. [http://dx.doi.org/10.1016/j.bbrc.2017.02.019]. [PMID:28202418].
[47]
Allam, R.; Lawlor, K.E.; Yu, E.C.; Mildenhall, A.L.; Moujalled, D.M. Lewis., R.S., Ke, F., Mason, K.D., White, M.J., Stacey, K.J., Strasser, A., O’Reilly, L.A., Alexander, W., Kile., B.T., Vaux, D.L., Vince, J.E. Mitochondrial apoptosis is dispensable for NLRP3 inflammasome activation but non-apoptotic caspase-8 is required for inflammasome priming. EMBO Rep., 2014, 15(9), 982-990. [http://dx.doi.org/10.15252/embr.201438463]. [PMID:24990442].
[48]
Zhang, N.; Fu, L.; Bu, Y.; Yao, Y.; Wang, Y. Downregulated expression of miR-223 promotes Toll-like receptor-activated inflammatory responses in macrophages by targeting RhoB. Mol. Immunol., 2017, 91, 42-48. [http://dx.doi.org/10.1016/j.molimm.2017.08.026]. [PMID:28881218].
[49]
Franchi, L.; Eigenbrod, T.; Munoz-Planillo, R.; Ozkurede, U.; Kim, Y.G. Arindam, C., Gale, M. Jr., Silverman, R.H., Colonna, M., Akira, S., Nunez, G. Cytosolic double-stranded RNA activates the NLRP3 inflammasome via MAVS-induced membrane permeabilization and K+ efflux. J. Immunol., 2014, 193(8), 4214-4222. [http://dx.doi.org/10.4049/jimmunol.1400582]. [PMID:25225670].
[50]
Asgari, E.; Le Friec, G.; Yamamoto, H.; Perucha, E.; Sacks, S.S.; Kohl, J.; Cook, H.T.; Kemper, C. C3a modulates IL-1beta secretion in human monocytes by regulating ATP efflux and subsequent NLRP3 inflammasome activation. Blood, 2013, 122(20), 3473-3481. [http://dx.doi.org/10.1182/blood-2013-05-502229]. [PMID:23878142].
[51]
Haggadone, M.D.; Grailer, J.J.; Fattahi, F.; Zetoune, F.S.; Ward, P.A. Bidirectional crosstalk between C5a receptors and the NLRP3 inflammasome in macrophages and monocytes. Mediators Inflamm., 2016, 20161340156 [http://dx.doi.org/10.1155/2016/1340156]. [PMID:27382187].
[52]
Arbore, G.; Kemper, C. A novel “complement-metabolism-inflammasome axis” as a key regulator of immune cell effector function. Eur. J. Immunol., 2016, 46(7), 1563-1573. [http://dx.doi.org/10.1002/eji.201546131]. [PMID:27184294].
[53]
Oury, C. CD36: linking lipids to the NLRP3 inflammasome, atherogenesis and atherothrombosis. Cell. Mol. Immunol., 2014, 11(1), 8-10. [http://dx.doi.org/10.1038/cmi.2013.48]. [PMID:24097033].
[54]
Shi, H.; Wang, Y.; Li, X.; Zhan, X.; Tang, M.; Fina, M.; Su, L. Pratt, D., Bu, C.H., Hildebrand, S. Lyon., S., Scott, L., Quan, J., Sun, Q., Russell, J., Arnett, S., Jurek, P., Chen, D., Kravchenko, V.V., Mathison, J.C., Moresco, E.M., Monson, N.L., Ulevitch, R.J., Beutler, B. NLRP3 activation and mitosis are mutually exclusive events coordinated by NEK7, a new inflammasome component. Nat. Immunol., 2016, 17(3), 250-258. [http://dx.doi.org/10.1038/ni.3333]. [PMID:26642356].
[55]
He, Y.; Zeng, M.Y.; Yang, D.; Motro, B.; Nunez, G. NEK7 is an essential mediator of NLRP3 activation downstream of potassium efflux. Nature, 2016, 530(7590), 354-357. [http://dx.doi.org/10.1038/nature16959]. [PMID:26814970].
[56]
He, Y.; Franchi, L.; Nunez, G. The protein kinase PKR is critical for LPS-induced iNOS production but dispensable for inflammasome activation in macrophages. Eur. J. Immunol., 2013, 43(5), 1147-1152. [http://dx.doi.org/10.1002/eji.201243187]. [PMID:23401008].
[57]
Yoshida, K.; Okamura, H.; Hiroshima, Y.; Abe, K.; Kido, J.I.; Shinohara, Y.; Ozaki, K. PKR induces the expression of NLRP3 by regulating the NF-kappaB pathway in porphyromonas gingivalis-infected osteoblasts. Exp. Cell Res., 2017, 354(1), 57-64. [http://dx.doi.org/10.1016/j.yexcr.2017.03.028]. [PMID:28341446].
[58]
Shenoy, A.R.; Wellington, D.A.; Kumar, P.; Kassa, H.; Booth, C.J.; Cresswell, P.; MacMicking, J.D. GBP5 promotes NLRP3 inflammasome assembly and immunity in mammals. Science, 2012, 336(6080), 481-485. [http://dx.doi.org/10.1126/science.1217141]. [PMID:22461501].
[59]
Meunier, E.; Dick, M.S.; Dreier, R.F.; Schurmann, N.; Kenzelmann, B.D.; Warming, S.; Roose-Girma, M.; Bumann, D.; Kayagaki, N.; Takeda, M.; Yamamoto, K.; Broz, P. Caspase-11 activation requires lysis of pathogen-containing vacuoles by IFN-induced GTPases. Nature, 2014, 509(7500), 366-370. [http://dx.doi.org/10.1038/nature13157]. [PMID:24739961].
[60]
Xiong, X.Y.; Yang, Q.W. Rethinking the roles of inflammation in the intracerebral hemorrhage. Transl. Stroke Res., 2015, 6(5), 339-341. [http://dx.doi.org/10.1007/s12975-015-0402-1]. [PMID:25940771].
[61]
Schlunk, F.; Greenberg, S.M. The Pathophysiology of intracerebral hemorrhage formation and expansion. Transl. Stroke Res., 2015, 6(4), 257-263. [http://dx.doi.org/10.1007/s12975-015-0410-1]. [PMID:26073700].
[62]
Baxter, P.; Chen, Y.; Xu, Y.; Swanson, R.A. Mitochondrial dysfunction induced by nuclear poly(ADP-ribose) polymerase-1: a treatable cause of cell death in stroke. Transl. Stroke Res., 2014, 5(1), 136-144. [http://dx.doi.org/10.1007/s12975-013-0283-0]. [PMID:24323707].
[63]
Shimada, K.; Crother, T.R.; Karlin, J.; Dagvadorj, J.; Chiba, N. Chen. S., Ramanujan, V.K., Wolf., A.J., Vergnes, L., Ojcius, D.M., Rentsendorj, A., Vargas, M., Guerrero, C., Wang, Y., Fitzgerald K.A., Underhill, D.M., Town, T., Arditi, M. Oxidized mitochondrial DNA activates the NLRP3 inflammasome during apoptosis. Immunity, 2012, 36(3), 401-414. [http://dx.doi.org/10.1016/j.immuni.2012.01.009]. [PMID:22342844].
[64]
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. Neuroinflam., 2015, 12, 190. [http://dx.doi.org/10.1186/s12974-015-0409-2]. [PMID:26475134].
[65]
Zhao, H.; Pan, P.; Yang, Y.; Ge, H.; Chen, W.; Qu, J.; Shi, J.; Cui, G.; Liu, X.; Feng, H.; Chen, Y. Endogenous hydrogen sulphide attenuates NLRP3 inflammasome-mediated neuroinflammation by suppressing the P2X7 receptor after intracerebral haemorrhage in rats. J. Neuroinflammation, 2017, 14(1), 163. [http://dx.doi.org/10.1186/s12974-017-0940-4]. [PMID:28821266].
[66]
Weng, X.; Tan, Y.; Chu, X. Wu., X.F., Liu, R., Tian., Y., Li, L., Guo, F., Ouyang, Q., Li, L. N-methyl-D-aspartic acid receptor 1 (NMDAR1) aggravates secondary inflammatory damage induced by hemin-NLRP3 pathway after intracerebral hemorrhage. Chin. J. Traumatol, 2015, 18 (5), 254-8. 26777707].
[67]
Yuan, R.; Fan, H.; Cheng, S.; Gao, W.; Xu, X.; Lv, S.; Ye, M.; Wu, M.; Zhu, X.; Zhang, Y. Silymarin prevents NLRP3 inflammasome activation and protects against intracerebral hemorrhage. Biomed. Pharmacother., 2017, 93, 308-315. [http://dx.doi.org/10.1016/j.biopha.2017.06.018]. [PMID:28651232].
[68]
Yao, S.T.; Cao, F.; Chen, J.L.; Chen, W.; Fan, R.M.; Li, G.; Zeng, Y.C.; Jiao, S.; Xia, X.P.; Han, C.; Ran, Q.S. NLRP3 is required for complement-mediated caspase-1 and IL-1beta activation in ICH. J. Mol. Neurosci., 2017, 61(3), 385-395. [http://dx.doi.org/10.1007/s12031-016-0874-9]. [PMID:27933491].
[69]
Yang, Z.; Zhong, L.; Xian, R.; Yuan, B. MicroRNA-223 regulates inflammation and brain injury via feedback to NLRP3 inflammasome after intracerebral hemorrhage. Mol. Immunol., 2015, 65(2), 267-276. [http://dx.doi.org/10.1016/j.molimm.2014.12.018]. [PMID:25710917].
[70]
Suzuki, H.; Shiba, M.; Nakatsuka, Y.; Nakano, F.; Nishikawa, H. Higher cerebrospinal fluid pH may contribute to the development of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. Transl. Stroke Res., 2017, 8(2), 165-173. [http://dx.doi.org/10.1007/s12975-016-0500-8]. [PMID:27623837].
[71]
Tso, M.K.; Macdonald, R.L. Subarachnoid hemorrhage: a review of experimental studies on the microcirculation and the neurovascular unit. Transl. Stroke Res., 2014, 5(2), 174-189. [http://dx.doi.org/10.1007/s12975-014-0323-4]. [PMID:24510780].
[72]
Mathur, A.; Hayward, J.A.; Man, S.M. molecular mechanisms of inflammasome signaling. J. Leukoc. Biol., 2018, 103(2), 233-257. [http://dx.doi.org/10.1189/jlb.3MR0617-250R]. [PMID:28855232].
[73]
Pang, J.Y.; Chen, L.; Kuai, P.; Yang, J.; Peng, Y.; Wu, Y.; Chen, M.; Vitek, P.; Chen, L.; Sun, X.; Jiang, Y. Inhibition of blood-brain barrier disruption by an apolipoprotein e-Mimetic peptide ameliorates early brain injury in experimental subarachnoid hemorrhage. Transl. Stroke Res., 2017, 8(3), 257-272. [http://dx.doi.org/10.1007/s12975-016-0507-1]. [PMID:27796945].
[74]
Hosaka, K.; Hoh, B.L. Inflammation and cerebral aneurysms. Transl. Stroke Res., 2014, 5(2), 190-198. [http://dx.doi.org/10.1007/s12975-013-0313-y]. [PMID:24323732].
[75]
Dong, Y.C.; Fan, W.; Hu, S.; Jiang, Z.; Ma, X.; Yan, C.; Deng, S.; Di, Z.; Xin, G.; Wu, Y.; Yang, R.; Reiter, J.; Liang, G. Melatonin attenuated early brain injury induced by subarachnoid hemorrhage via regulating NLRP3 inflammasome and apoptosis signaling. J. Pineal Res., 2016, 60(3), 253-262. [http://dx.doi.org/10.1111/jpi.12300]. [PMID:26639408].
[76]
Cao, S.; Shrestha, S.; Li, J.; Yu, X.; Chen, J.; Yan, F.; Ying, G.; Gu, C.; Wang, L.; Chen, G. Melatonin-mediated mitophagy protects against early brain injury after subarachnoid hemorrhage through inhibition of NLRP3 inflammasome activation. Sci. Rep., 2017, 7(1), 2417. [http://dx.doi.org/10.1038/s41598-017-02679-z]. [PMID:28546552].
[77]
Chen, S.; Ma, Q.; Krafft, P.R.; Hu, Q.; Rolland, 2nd , W.; Sherchan, P.; Zhang, J.; Tang, J.; Zhang, J.H. P2X7R/cryopyrin inflammasome axis inhibition reduces neuroinflammation after SAH. Neurobiol. Dis., 2013, 58, 296-307. [http://dx.doi.org/10.1016/j.nbd.2013.06.011]. [PMID:23816751].
[78]
Zhou, K.; Shi, L.; Wang, Z.; Zhou, J. Manaenko, A., Reis, C., Chen. S., Zhang, J. RIP1-RIP3-DRP1 pathway regulates NLRP3 inflammasome activation following subarachnoid hemorrhage. Exp. Neurol., 2017, 295, 116-124. [http://dx.doi.org/10.1016/j.expneurol.2017.06.003]. [PMID:28579326].

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