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Original Research

Ox-LDL Causes Endothelial Cell Injury Through ASK1/NLRP3-Mediated Inflammasome Activation via Endoplasmic Reticulum Stress

, , , ORCID Icon &
Pages 731-744 | Published online: 24 Feb 2020

References

  • RahmanMS, WoollardK. Atherosclerosis. Adv Exp Med Biol. 2017;1003:121–144.28667557
  • CancelLM, EbongEE, MensahS, HirschbergC, TarbellJM. Endothelial glycocalyx, apoptosis and inflammation in an atherosclerotic mouse model. Atherosclerosis. 2016;252:136–146. doi:10.1016/j.atherosclerosis.2016.07.93027529818
  • OuH, HuangZ, MoZ, XiaoJ. The characteristics and roles of advanced oxidation protein products in atherosclerosis. Cardiovasc Toxicol. 2017;17:1–12. doi:10.1007/s12012-016-9377-827350146
  • ChistiakovDA, BobryshevYV, OrekhovAN. Macrophage-mediated cholesterol handling in atherosclerosis. J Cell Mol Med. 2016;20:17–28. doi:10.1111/jcmm.1268926493158
  • ChistiakovDA, MelnichenkoAA, OrekhovAN, BobryshevYV. Paraoxonase and atherosclerosis-related cardiovascular diseases. Biochimie. 2017;132:19–27. doi:10.1016/j.biochi.2016.10.01027771368
  • FuY, ZhaoY, HuangB. Tribbles homolog 1 enhances cholesterol efflux from oxidized low-density lipoprotein-loaded THP-1 macrophages. Exp Ther Med. 2017;14:862–866. doi:10.3892/etm.2017.455128673011
  • LuoY, DuanH, QianY, et al. Macrophagic CD146 promotes foam cell formation and retention during atherosclerosis. Cell Res. 2017;27:352–372. doi:10.1038/cr.2017.828084332
  • BerrymanCE, FlemingJA, Kris-EthertonPM. Inclusion of almonds in a cholesterol-lowering diet improves plasma HDL subspecies and cholesterol efflux to serum in normal-weight individuals with elevated LDL cholesterol. J Nutr. 2017;147:1517–1523. doi:10.3945/jn.116.24512628615375
  • CaoSS, LuoKL, ShiL. Endoplasmic reticulum stress interacts with inflammation in human diseases. J Cell Physiol. 2016;231:288–294. doi:10.1002/jcp.v231.226201832
  • SprenkleNT, SimsSG, SanchezCL, MearesGP. Endoplasmic reticulum stress and inflammation in the central nervous system. Mol Neurodegener. 2017;12:42. doi:10.1186/s13024-017-0183-y28545479
  • BoziLHM, TakanoAPC, CamposJC, et al. Endoplasmic reticulum stress impairs cardiomyocyte contractility through JNK-dependent upregulation of BNIP3. Int J Cardiol. 2018;272:194–201. doi:10.1016/j.ijcard.2018.08.07030173922
  • Baroja-MazoA, Martin-SanchezF, GomezAI, et al. The NLRP3 inflammasome is released as a particulate danger signal that amplifies the inflammatory response. Nat Immunol. 2014;15:738–748.24952504
  • GaidtMM, HornungV. The NLRP3 inflammasome renders cell death pro-inflammatory. J Mol Biol. 2018;430:133–141. doi:10.1016/j.jmb.2017.11.01329203171
  • BaldrighiM, MallatZ, LiX. NLRP3 inflammasome pathways in atherosclerosis. Atherosclerosis. 2017;267:127–138. doi:10.1016/j.atherosclerosis.2017.10.02729126031
  • PlaceDE, SamirP, KarkiR, BriardB, VogelP, KannegantiTD. ASK family kinases are required for optimal NLRP3 inflammasome priming. Am J Pathol. 2018;188:1021–1030. doi:10.1016/j.ajpath.2017.12.00629353059
  • FrambachS, de HaasR, SmeitinkJAM, RongenGA, RusselFGM, SchirrisTJJ. Brothers in arms: ABCA1- and ABCG1-mediated cholesterol efflux as promising targets in cardiovascular disease treatment. Pharmacol Rev. 2020;72:152–190.31831519
  • WangD, HieblV, XuT, et al. Impact of natural products on the cholesterol transporter ABCA1. J Ethnopharmacol. 2019;249:112444.31805338
  • MengXD, YaoHH, WangLM, et al. Knockdown of GAS5 inhibits atherosclerosis progression via reducing EZH2-mediated ABCA1 transcription in ApoE(-/-) mice. Mol therNucleic Acids. 2019;19:84–96. doi:10.1016/j.omtn.2019.10.034
  • Yvan-CharvetL, WangN, TallAR. Role of HDL, ABCA1, and ABCG1 transporters in cholesterol efflux and immune responses. Arterioscler Thromb Vasc Biol. 2010;30:139–143. doi:10.1161/ATVBAHA.108.17928319797709
  • StefuljJ, PanzenboeckU, BeckerT, et al. Human endothelial cells of the placental barrier efficiently deliver cholesterol to the fetal circulation via ABCA1 and ABCG1. Circ Res. 2009;104:600–608. doi:10.1161/CIRCRESAHA.108.18506619168441
  • WangX, CollinsHL, RanallettaM, FukiIV, RaderDJ. Macrophage ABCA1 and ABCG1, but not SR-BI, promote macrophage reverse cholesterol transport in vivo. J Clin Invest. 2007;117:2216–2224. doi:10.1172/JCI3205717657311
  • Yvan-CharvetL, RanallettaM, WangN, et al. Combined deficiency of ABCA1 and ABCG1 promotes foam cell accumulation and accelerates atherosclerosis in mice. J Clin Invest. 2007;117:3900–3908. doi:10.1172/JCI3337217992262
  • TanY-L, H-xO, ZhangM, et al. Tanshinone IIA promotes macrophage cholesterol efflux and attenuates atherosclerosis of apoE-/- mice by omentin-1/ABCA1 pathway. Curr Pharm Biotechnol. 2019;20:422–432. doi:10.2174/138920102066619040412521330947667
  • BrownRA, ShantsilaE, VarmaC, LipGY. Current understanding of atherogenesis. Am J Med. 2017;130:268–282. doi:10.1016/j.amjmed.2016.10.02227888053
  • GisteraA, HanssonGK. The immunology of atherosclerosis. Nat Rev Nephrol. 2017;13:368–380. doi:10.1038/nrneph.2017.5128392564
  • HoseiniZ, SepahvandF, RashidiB, SahebkarA, MasoudifarA, MirzaeiH. NLRP3 inflammasome: its regulation and involvement in atherosclerosis. J Cell Physiol. 2018;233:2116–2132. doi:10.1002/jcp.v233.328345767
  • ZeeshanHM, LeeGH, KimHR, ChaeHJ. Endoplasmic reticulum stress and associated ROS. Int J Mol Sci. 2016;17:327. doi:10.3390/ijms1703032726950115
  • MilliatF, FrançoisA, IsoirM, et al. Influence of endothelial cells on vascular smooth muscle cells phenotype after irradiation: implication in radiation-induced vascular damages. Am J Pathol. 2006;169:1484–1495. doi:10.2353/ajpath.2006.06011617003501
  • SturtzelC. Endothelial Cells. Adv Exp Med Biol. 2017;1003:71–91.28667554
  • CichonN, LachD, DziedzicA, BijakM, SalukJ. The inflammatory processes in atherogenesis. Polski Merkuriusz Lekarski. 2017;42:125–128.28333905
  • QuillardT, FranckG, MawsonT, FolcoE, LibbyP. Mechanisms of erosion of atherosclerotic plaques. Curr Opin Lipidol. 2017;28:434–441. doi:10.1097/MOL.000000000000044028682809
  • GengC, ZhangY, HidruTH, et al. Sonodynamic therapy: a potential treatment for atherosclerosis. Life Sci. 2018;207:304–313. doi:10.1016/j.lfs.2018.06.01829940244
  • ThentZC, ChakrabortyC, MahakkanukrauhP, et al. The molecular concept of atheromatous plaques. Curr Drug Targets. 2017;18:1250–1258. doi:10.2174/138945011766616050215160027138760
  • SchurmannC, RezendeF, KruseC, et al. The NADPH oxidase Nox4 has anti-atherosclerotic functions. Eur Heart J. 2015;36:3447–3456. doi:10.1093/eurheartj/ehv46026385958
  • WangY, LiL, ZhaoW, et al. Targeted therapy of atherosclerosis by a broad-spectrum reactive oxygen species scavenging nanoparticle with intrinsic anti-inflammatory activity. ACS Nano. 2018;12:8943–8960. doi:10.1021/acsnano.8b0203730114351
  • YangJ, YuJ, LiD, et al. Store-operated calcium entry-activated autophagy protects EPC proliferation via the CAMKK2-MTOR pathway in ox-LDL exposure. Autophagy. 2017;13:82–98. doi:10.1080/15548627.2016.124526127791458
  • GaoW, CuiH, LiQ, et al. Upregulation of microRNA-218 reduces cardiac microvascular endothelial cells injury induced by coronary artery disease through the inhibition of HMGB1. J Cell Physiol. 2020;235:3079–3095. doi:10.1002/jcp.2921431566720
  • QianW, CaiX, QianQ, et al. Astragaloside IV protects endothelial progenitor cells from the damage of ox-LDL via the LOX-1/NLRP3 inflammasome pathway. Drug Des Devel Ther. 2019;13:2579–2589. doi:10.2147/DDDT.S207774
  • WangM, LiuY, LiC, ZhangY, ZhouX, LuC. Long noncoding RNA OIP5-AS1 accelerates the ox-LDL mediated vascular endothelial cells apoptosis through targeting GSK-3beta via recruiting EZH2. Am J Transl Res. 2019;11:1827–1834.30972206
  • JiG, SongX, WangL, LiZ, DongH. Golgi apparatus fragmentation participates in oxidized low-density lipoprotein-induced endothelial cell injury. J Cell Biochem. 2019;120. doi:10.1002/jcb.29205
  • CaiT, CuiX, ZhangK, ZhangA, LiuB, MuJJ. LncRNA TNK2-AS1 regulated ox-LDL-stimulated HASMC proliferation and migration via modulating VEGFA and FGF1 expression by sponging miR-150-5p. J Cell Mol Med. 2019;23:7289–7298. doi:10.1111/jcmm.1457531468685
  • BaoMH, LiGY, HuangXS, TangL, DongLP, LiJM. Long noncoding RNA LINC00657 acting as a miR-590-3p sponge to facilitate low concentration oxidized low-density lipoprotein-induced angiogenesis. Mol Pharmacol. 2018;93:368–375. doi:10.1124/mol.117.11065029436491
  • QiuJ, WangG, ZhengY, HuJ, PengQ, YinT. Coordination of Id1 and p53 activation by oxidized LDL regulates endothelial cell proliferation and migration. Ann Biomed Eng. 2011;39:2869–2878. doi:10.1007/s10439-011-0382-621870248
  • ZhangC, AdamosC, OhMJ, et al. oxLDL induces endothelial cell proliferation via Rho/ROCK/Akt/p27(kip1) signaling: opposite effects of oxLDL and cholesterol loading. Am J Physiol Cell Physiol. 2017;313:C340–c351. doi:10.1152/ajpcell.00249.201628701359
  • ZhuH, XiaM, HouM, et al. Ox-LDL plays dual effect in modulating expression of inflammatory molecules through LOX-1 pathway in human umbilical vein endothelial cells. Front Biosci. 2005;10:2585–2594. doi:10.2741/172215970520
  • ZhongZ, Sanchez-LopezE, KarinM. Autophagy, NLRP3 inflammasome and auto-inflammatory/immune diseases. Clin Exp Rheumatol. 2016;34:12–16.27586797
  • RhoadsJP, LukensJR, WilhelmAJ, et al. Oxidized low-density lipoprotein immune complex priming of the Nlrp3 inflammasome involves TLR and FcgammaR cooperation and is dependent on CARD9. J Immunol. 2017;198:2105–2114. doi:10.4049/jimmunol.160156328130494
  • DuewellP, KonoH, RaynerKJ, et al. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature. 2010;464:1357–1361. doi:10.1038/nature0893820428172
  • RajamakiK, LappalainenJ, OorniK, et al. Cholesterol crystals activate the NLRP3 inflammasome in human macrophages: a novel link between cholesterol metabolism and inflammation. PLoS One. 2010;5:e11765. doi:10.1371/journal.pone.001176520668705
  • ChenL, YaoQ, XuS, WangH, QuP. Inhibition of the NLRP3 inflammasome attenuates foam cell formation of THP-1 macrophages by suppressing ox-LDL uptake and promoting cholesterol efflux. Biochem Biophys Res Commun. 2018;495:382–387. doi:10.1016/j.bbrc.2017.11.02529122594
  • WesterterpM, FotakisP, OuimetM, et al. Cholesterol efflux pathways suppress inflammasome activation, NETosis, and atherogenesis. Circulation. 2018;138:898–912. doi:10.1161/CIRCULATIONAHA.117.03263629588315
  • LiuY, YinG, SurapisitchatJ, BerkBC, MinW. Laminar flow inhibits TNF-induced ASK1 activation by preventing dissociation of ASK1 from its inhibitor 14-3-3. J Clin Invest. 2001;107:917–923. doi:10.1172/JCI1194711285311
  • TarteyS, GurungP, DasariTK, BurtonA, KannegantiTD. ASK1/2 signaling promotes inflammation in a mouse model of neutrophilic dermatosis. J Clin Invest. 2018;128:2042–2047.29629899
  • SakauchiC, WakatsukiH, IchijoH, HattoriK. Pleiotropic properties of ASK1. Biochim Biophys Acta Gen Subj. 2017;1861:3030–3038. doi:10.1016/j.bbagen.2016.09.028
  • TangSY, WanYP, WuYM. Death domain associated protein (Daxx), a multi-functional protein. Cell Mol Biol Lett. 2015;20:788–797. doi:10.1515/cmble-2015-004826540225
  • YamadaS, NoguchiH, TanimotoA. Critical and diverse in vivo roles of apoptosis signal-regulating kinase 1 in animal models of atherosclerosis and cholestatic liver injury. Histol Histopathol. 2017;32:11840.
  • ZhengS, LongL, LiY, et al. A novel ASK inhibitor AGI-1067 inhibits TLR-4-mediated activation of ASK1 by preventing dissociation of thioredoxin from ASK1. Cardiovasc Pharm Open Access. 2015;4. doi:10.4172/2329-6607.1000132
  • ZhangH, LiuQ, LinJL, et al. Recombinant human thioredoxin-1 protects macrophages from oxidized low-density lipoprotein-induced foam cell formation and cell apoptosis. Biomol Ther. 2018;26:121–129. doi:10.4062/biomolther.2016.275
  • HuYB, WuX, QinXF, WangL, PanPH. Role of endoplasmic reticulum stress in silica-induced apoptosis in RAW264.7 cells. Biomed Environ Sci. 2017;30:591–600. doi:10.3967/bes2017.07828807099
  • DongY, FernandesC, LiuY, et al. Role of endoplasmic reticulum stress signalling in diabetic endothelial dysfunction and atherosclerosis. Diabetes Vasc Dis Res. 2017;14:14–23. doi:10.1177/1479164116666762
  • IvanovaEA, OrekhovAN. The role of endoplasmic reticulum stress and unfolded protein response in atherosclerosis. Int J Mol Sci. 2016;17:193.
  • GuoC, MaR, LiuX, et al. Silica nanoparticles promote oxLDL-induced macrophage lipid accumulation and apoptosis via endoplasmic reticulum stress signaling. Scie Total Environ. 2018;570:631–632.
  • YaoS, TianH, MiaoC, et al. D4F alleviates macrophage-derived foam cell apoptosis by inhibiting CD36 expression and ER stress-CHOP pathway. J Lipid Res. 2015;56:836–847. doi:10.1194/jlr.M05540025635126
  • StarosylaSA, VolynetsGP, LukashovSS, et al. Identification of apoptosis signal-regulating kinase 1 (ASK1) inhibitors among the derivatives of benzothiazol-2-yl-3-hydroxy-5-phenyl-1,5-dihydro-pyrrol-2-one. Bioorg Med Chem. 2015;23:2489–2497. doi:10.1016/j.bmc.2015.03.05625882527
  • ZengT, PengL, ChaoH, et al. IRE1alpha-TRAF2-ASK1 complex-mediated endoplasmic reticulum stress and mitochondrial dysfunction contribute to CXC195-induced apoptosis in human bladder carcinoma T24 cells. Biochem Biophys Res Commun. 2015;460:530–536. doi:10.1016/j.bbrc.2015.03.06425797626
  • BronnerDN, AbuaitaBH, ChenX, et al. Endoplasmic reticulum stress activates the inflammasome via NLRP3- and Caspase-2-driven mitochondrial damage. Immunity. 2015;43:451–462. doi:10.1016/j.immuni.2015.08.00826341399
  • LiJ, WangY, WangY, et al. Pharmacological activation of AMPK prevents Drp1-mediated mitochondrial fission and alleviates endoplasmic reticulum stress-associated endothelial dysfunction. J Mol Cell Cardiol. 2015;86:62–74. doi:10.1016/j.yjmcc.2015.07.01026196303
  • YuanX, ZhengY, ChenC, WangC. Anisodamine inhibits endoplasmic reticulum stress-associated TXNIP/NLRP3 inflammasome activation in rhabdomyolysis-induced acute kidney injury. Apoptosis. 2017;22:1524–1531. doi:10.1007/s10495-017-1414-y28918467