Abstract
Endoplasmic reticulum stress (ERS) is a protective response to restore protein homeostasis by activating the unfolded protein response (UPR). However, UPR can trigger cell death under severe and/or persistently high ERS. The NLRP3 inflammasome is a complex of multiple proteins that activates the secretion of the proinflammatory cytokine IL-1β in a caspase-1-dependent manner to participate in the regulation of inflammation. The NLRP3 inflammasome involvement in ERS-induced inflammation has not been completely described. The intersection of ERS with multiple inflammatory pathways can initiate and aggravate chronic diseases. Accumulating evidence suggests that ERS-induced activation of NLRP3 inflammasome is the pathological basis of various inflammatory diseases. In this review, we have discussed the networks between ERS and NLRP3 inflammasome, with the view to identifying novel therapeutic targets in inflammatory diseases.
Key points
• Endoplasmic reticulum stress (ERS) is an important factor for the activation of the NLRP3 inflammasomes that results in pathological processes.
• ERS can activate the NLRP3 inflammasome to induce inflammatory responses via oxidative stress, calcium homeostasis, and NF-κB activation.
• The interactions between ERS and NLRP3 inflammasome are associated with inflammation, which represent a potential therapeutic opportunity of inflammatory diseases.
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References
Abais JM, Xia M, Zhang Y, Boini KM, Li PL (2015) Redox regulation of NLRP3 inflammasomes: ROS as trigger or effector? Antioxid Redox Signal 22(13):1111–1129. https://doi.org/10.1089/ars.2014.5994
Bronner DN, Abuaita BH, Chen X, Fitzgerald KA, Nunez G, He Y, Yin XM, O'Riordan MX (2015) Endoplasmic reticulum stress activates the inflammasome via NLRP3- and caspase-2-driven mitochondrial damage. Immunity 43(3):451–462. https://doi.org/10.1016/j.immuni.2015.08.008
Burgos-Moron E, Abad-Jimenez Z, Maranon AM, Iannantuoni F, Escribano-Lopez I, Lopez-Domenech S, Salom C, Jover A, Mora V, Roldan I, Sola E, Rocha M, Victor VM (2019) Relationship between oxidative stress, ER stress, and inflammation in type 2 diabetes: the battle continues. J Clin Med 8(9). https://doi.org/10.3390/jcm8091385
Cao SS, Kaufman RJ (2014) Endoplasmic reticulum stress and oxidative stress in cell fate decision and human disease. Antioxid Redox Signal 21(3):396–413. https://doi.org/10.1089/ars.2014.5851
Chalour N, Maoui A, Rat P, Massicot F, Dutot M, Faussat AM, Devevre E, Limb A, Warnet JM, Treton J, Dinet V, Mascarelli F (2018) AbetaPP-induced UPR transcriptomic signature of glial cells to oxidative stress as an adaptive mechanism to preserve cell function and survival. Curr Alzheimer Res 15(7):643–654. https://doi.org/10.2174/1567205015666180119101832
Chaudhari N, Talwar P, Parimisetty A, Lefebvre d'Hellencourt C, Ravanan P (2014) A molecular web: endoplasmic reticulum stress, inflammation, and oxidative stress. Front Cell Neurosci 8:213. https://doi.org/10.3389/fncel.2014.00213
Chen J, Zhang M, Zhu M, Gu J, Song J, Cui L, Liu D, Ning Q, Jia X, Feng L (2018a) Paeoniflorin prevents endoplasmic reticulum stress-associated inflammation in lipopolysaccharide-stimulated human umbilical vein endothelial cells via the IRE1alpha/NF-kappaB signaling pathway. Food Funct 9(4):2386–2397. https://doi.org/10.1039/c7fo01406f
Chen D, Dixon BJ, Doycheva DM, Li B, Zhang Y, Hu Q, He Y, Guo Z, Nowrangi D, Flores J, Filippov V, Zhang JH, Tang J (2018b) IRE1alpha inhibition decreased TXNIP/NLRP3 inflammasome activation through miR-17-5p after neonatal hypoxic-ischemic brain injury in rats. J Neuroinflammation 15(1):32–18. https://doi.org/10.1186/s12974-018-1077-9
Chovatiya R, Medzhitov R (2014) Stress, inflammation, and defense of homeostasis. Mol Cell 54(2):281–288. https://doi.org/10.1016/j.molcel.2014.03.030
Cubillos-Ruiz JR, Bettigole SE, Glimcher LH (2017) Tumorigenic and immunosuppressive effects of endoplasmic reticulum stress in cancer. Cell 168(4):692–706. https://doi.org/10.1016/j.cell.2016.12.004
Cullinan SB, Diehl JA (2006) Coordination of ER and oxidative stress signaling: the PERK/Nrf2 signaling pathway. Int J Biochem Cell Biol 38(3):317–332. https://doi.org/10.1016/j.biocel.2005.09.018
Cullinan SB, Zhang D, Hannink M, Arvisais E, Kaufman RJ, Diehl JA (2003) Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. Mol Cell Biol 23(20):7198–7209. https://doi.org/10.1128/mcb.23.20.7198-7209.2003
Dostert C, Petrilli V, Van Bruggen R, Steele C, Mossman BT, Tschopp J (2008) Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 320(5876):674–677. https://doi.org/10.1126/science.1156995
Du RH, Tan J, Yan N, Wang L, Qiao C, Ding JH, Lu M, Hu G (2014) Kir6.2 knockout aggravates lipopolysaccharide-induced mouse liver injury via enhancing NLRP3 inflammasome activation. J Gastroenterol 49(4):727–736. https://doi.org/10.1007/s00535-013-0823-0
Duewell P, Kono H, Rayner KJ, Sirois CM, Vladimer G, Bauernfeind FG, Abela GS, Franchi L, Nunez G, Schnurr M, Espevik T, Lien E, Fitzgerald KA, Rock KL, Moore KJ, Wright SD, Hornung V, Latz E (2010) NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 464(7293):1357–1361. https://doi.org/10.1038/nature08938
Farag NS, Breitinger U, Breitinger HG, El Azizi MA (2020) Viroporins and inflammasomes: a key to understand virus-induced inflammation. Int J Biochem Cell Biol 122:105738. https://doi.org/10.1016/j.biocel.2020.105738
Forouhan M, Mori K, Boot-Handford RP (2018) Paradoxical roles of ATF6alpha and ATF6beta in modulating disease severity caused by mutations in collagen X. Matrix Biol 70:50–71. https://doi.org/10.1016/j.matbio.2018.03.004
Frakes AE, Dillin A (2017) The UPR(ER): sensor and coordinator of organismal homeostasis. Mol Cell 66(6):761–771. https://doi.org/10.1016/j.molcel.2017.05.031
Garg AD, Kaczmarek A, Krysko O, Vandenabeele P, Krysko DV, Agostinis P (2012) ER stress-induced inflammation: does it aid or impede disease progression? Trends Mol Med 18(10):589–598. https://doi.org/10.1016/j.molmed.2012.06.010
Ghosh R, Colon-Negron K, Papa FR (2019) Endoplasmic reticulum stress, degeneration of pancreatic islet beta-cells, and therapeutic modulation of the unfolded protein response in diabetes. Mol Metab 27s:S60–s68. https://doi.org/10.1016/j.molmet.2019.06.012
Gomez-Suaga P, Bravo-San Pedro JM, Gonzalez-Polo RA, Fuentes JM, Niso-Santano M (2018) ER-mitochondria signaling in Parkinson’s disease. Cell Death Dis 9(3):337–312. https://doi.org/10.1038/s41419-017-0079-3
Gong T, Yang Y, Jin T, Jiang W, Zhou R (2018) Orchestration of NLRP3 inflammasome activation by ion fluxes. Trends Immunol 39(5):393–406. https://doi.org/10.1016/j.it.2018.01.009
Goodall JC, Wu C, Zhang Y, McNeill L, Ellis L, Saudek V, Gaston JS (2010) Endoplasmic reticulum stress-induced transcription factor, CHOP, is crucial for dendritic cell IL-23 expression. Proc Natl Acad Sci U S A 107(41):17698–17703. https://doi.org/10.1073/pnas.1011736107
Guo FJ, Xiong Z, Lu X, Ye M, Han X, Jiang R (2014) ATF6 upregulates XBP1S and inhibits ER stress-mediated apoptosis in osteoarthritis cartilage. Cell Signal 26(2):332–342. https://doi.org/10.1016/j.cellsig.2013.11.018
Guo M, An F, Yu H, Wei X, Hong M, Lu Y (2017) Comparative effects of schisandrin A, B, and C on Propionibacterium acnes-induced, NLRP3 inflammasome activation-mediated IL-1beta secretion and pyroptosis. Biomed Pharmacother 96:129–136. https://doi.org/10.1016/j.biopha.2017.09.097
Guthrie LN, Abiraman K, Plyler ES, Sprenkle NT, Gibson SA, McFarland BC, Rajbhandari R, Rowse AL, Benveniste EN, Meares GP (2016) Attenuation of PKR-like ER kinase (PERK) signaling selectively controls endoplasmic reticulum stress-induced inflammation without compromising immunological responses. J Biol Chem 291(30):15830–15840. https://doi.org/10.1074/jbc.M116.738021
Han CY, Rho HS, Kim A, Kim TH, Jang K, Jun DW, Kim JW, Kim B, Kim SG (2018) FXR inhibits endoplasmic reticulum stress-induced NLRP3 inflammasome in hepatocytes and ameliorates liver injury. Cell Rep 24(11):2985–2999. https://doi.org/10.1016/j.celrep.2018.07.068
He X, Mekasha S, Mavrogiorgos N, Fitzgerald KA, Lien E, Ingalls RR (2010) Inflammation and fibrosis during Chlamydia pneumoniae infection is regulated by IL-1 and the NLRP3/ASC inflammasome. J Immunol 184(10):5743–5754. https://doi.org/10.4049/jimmunol.0903937
He Y, Hara H, Nunez G (2016) Mechanism and regulation of NLRP3 Inflammasome activation. Trends Biochem Sci 41(12):1012–1021. https://doi.org/10.1016/j.tibs.2016.09.002
Hise AG, Tomalka J, Ganesan S, Patel K, Hall BA, Brown GD, Fitzgerald KA (2009) An essential role for the NLRP3 inflammasome in host defense against the human fungal pathogen Candida albicans. Cell Host Microbe 5(5):487–497. https://doi.org/10.1016/j.chom.2009.05.002
Hornung V, Bauernfeind F, Halle A, Samstad EO, Kono H, Rock KL, Fitzgerald KA, Latz E (2008) Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol 9(8):847–856. https://doi.org/10.1038/ni.1631
Hu X, Li D, Wang J, Guo J, Li Y, Cao Y, Zhang N, Fu Y (2018) Melatonin inhibits endoplasmic reticulum stress-associated TXNIP/NLRP3 inflammasome activation in lipopolysaccharide-induced endometritis in mice. Int Immunopharmacol 64:101–109. https://doi.org/10.1016/j.intimp.2018.08.028
Iannitti RG, Napolioni V, Oikonomou V, De Luca A, Galosi C, Pariano M, Massi-Benedetti C, Borghi M, Puccetti M, Lucidi V, Colombo C, Fiscarelli E, Lass-Florl C, Majo F, Cariani L, Russo M, Porcaro L, Ricciotti G, Ellemunter H, Ratclif L, De Benedictis FM, Talesa VN, Dinarello CA, van de Veerdonk FL, Romani L (2016) IL-1 receptor antagonist ameliorates inflammasome-dependent inflammation in murine and human cystic fibrosis. Nat Commun 7:10791. https://doi.org/10.1038/ncomms10791
Inagi R, Ishimoto Y, Nangaku M (2014) Proteostasis in endoplasmic reticulum--new mechanisms in kidney disease. Nat Rev Nephrol 10(7):369–378. https://doi.org/10.1038/nrneph.2014.67
Jiang Y, Wang M, Huang K, Zhang Z, Shao N, Zhang Y, Wang W, Wang S (2012) Oxidized low-density lipoprotein induces secretion of interleukin-1beta by macrophages via reactive oxygen species-dependent NLRP3 inflammasome activation. Biochem Biophys Res Commun 425(2):121–126. https://doi.org/10.1016/j.bbrc.2012.07.011
Junjappa RP, Patil P, Bhattarai KR, Kim HR, Chae HJ (2018) IRE1alpha implications in endoplasmic reticulum stress-mediated development and pathogenesis of autoimmune diseases. Front Immunol 9:1289. https://doi.org/10.3389/fimmu.2018.01289
Kanak MA, Shahbazov R, Yoshimatsu G, Levy MF, Lawrence MC, Naziruddin B (2017) A small molecule inhibitor of NFkappaB blocks ER stress and the NLRP3 inflammasome and prevents progression of pancreatitis. J Gastroenterol 52(3):352–365. https://doi.org/10.1007/s00535-016-1238-5
Kang MJ, Jo SG, Kim DJ, Park JH (2017) NLRP3 inflammasome mediates interleukin-1beta production in immune cells in response to Acinetobacter baumannii and contributes to pulmonary inflammation in mice. Immunology 150(4):495–505. https://doi.org/10.1111/imm.12704
Kaushik DK, Gupta M, Kumawat KL, Basu A (2012) NLRP3 inflammasome: key mediator of neuroinflammation in murine Japanese encephalitis. PLoS One 7(2):e32270. https://doi.org/10.1371/journal.pone.0032270
Keestra-Gounder AM, Byndloss MX, Seyffert N, Young BM, Chavez-Arroyo A, Tsai AY, Cevallos SA, Winter MG, Pham OH, Tiffany CR, de Jong MF, Kerrinnes T, Ravindran R, Luciw PA, McSorley SJ, Baumler AJ, Tsolis RM (2016) NOD1 and NOD2 signalling links ER stress with inflammation. Nature 532(7599):394–397. https://doi.org/10.1038/nature17631
Kim S, Joe Y, Jeong SO, Zheng M, Back SH, Park SW, Ryter SW, Chung HT (2014) Endoplasmic reticulum stress is sufficient for the induction of IL-1beta production via activation of the NF-kappaB and inflammasome pathways. Innate Immun 20(8):799–815. https://doi.org/10.1177/1753425913508593
Kim S, Joe Y, Kim HJ, Kim YS, Jeong SO, Pae HO, Ryter SW, Surh YJ, Chung HT (2015) Endoplasmic reticulum stress-induced IRE1alpha activation mediates cross-talk of GSK-3beta and XBP-1 to regulate inflammatory cytokine production. J Immunol 194(9):4498–4506. https://doi.org/10.4049/jimmunol.1401399
Kim YG, Kim SM, Kim KP, Lee SH, Moon JY (2019) The role of inflammasome-dependent and Inflammasome-independent NLRP3 in the kidney. Cells 8(11). https://doi.org/10.3390/cells8111389
Kistowska M, Gehrke S, Jankovic D, Kerl K, Fettelschoss A, Feldmeyer L, Fenini G, Kolios A, Navarini A, Ganceviciene R, Schauber J, Contassot E, French LE (2014) IL-1beta drives inflammatory responses to propionibacterium acnes in vitro and in vivo. J Invest Dermatol 134(3):677–685. https://doi.org/10.1038/jid.2013.438
Lebeaupin C, Proics E, de Bieville CH, Rousseau D, Bonnafous S, Patouraux S, Adam G, Lavallard VJ, Rovere C, Le Thuc O, Saint-Paul MC, Anty R, Schneck AS, Iannelli A, Gugenheim J, Tran A, Gual P, Bailly-Maitre B (2015) ER stress induces NLRP3 inflammasome activation and hepatocyte death. Cell Death Dis 6:e1879. https://doi.org/10.1038/cddis.2015.248
Lee S, Kim GL, Kim NY, Kim SJ, Ghosh P, Rhee DK (2018) ATF3 stimulates IL-17A by regulating intracellular Ca(2+)/ROS-dependent IL-1beta activation during Streptococcus pneumoniae infection. Front Immunol 9:1954. https://doi.org/10.3389/fimmu.2018.01954
Lencer WI, DeLuca H, Grey MJ, Cho JA (2015) Innate immunity at mucosal surfaces: the IRE1-RIDD-RIG-I pathway. Trends Immunol 36(7):401–409. https://doi.org/10.1016/j.it.2015.05.006
Liang Y, Fan C, Yan X, Lu X, Jiang H, Di S, Ma Z, Feng Y, Zhang Z, Feng P, Feng X, Feng J, Jin F (2019) Berberine ameliorates lipopolysaccharide-induced acute lung injury via the PERK-mediated Nrf2/HO-1 signaling axis. Phytother Res 33(1):130–148. https://doi.org/10.1002/ptr.6206
Lin Y, Yang Y (2019) MiR-24 inhibits inflammatory responses in LPS-induced acute lung injury of neonatal rats through targeting NLRP3. Pathol Res Pract 215(4):683–688. https://doi.org/10.1016/j.prp.2018.12.028
Liu Q, Zhang D, Hu D, Zhou X, Zhou Y (2018) The role of mitochondria in NLRP3 inflammasome activation. Mol Immunol 103:115–124. https://doi.org/10.1016/j.molimm.2018.09.010
Ma X, Dai Z, Sun K, Zhang Y, Chen J, Yang Y, Tso P, Wu G, Wu Z (2017) Intestinal epithelial cell endoplasmic reticulum stress and inflammatory bowel disease pathogenesis: an update review. Front Immunol 8:1271. https://doi.org/10.3389/fimmu.2017.01271
MacPherson M, Westbom C, Kogan H, Shukla A (2017) Actin polymerization plays a significant role in asbestos-induced inflammasome activation in mesothelial cells in vitro. Histochem Cell Biol 147(5):595–604. https://doi.org/10.1007/s00418-016-1530-8
Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J (2006) Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440(7081):237–241. https://doi.org/10.1038/nature04516
Martinon F, Chen X, Lee AH, Glimcher LH (2010) TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat Immunol 11(5):411–418. https://doi.org/10.1038/ni.1857
Meares GP, Liu Y, Rajbhandari R, Qin H, Nozell SE, Mobley JA, Corbett JA, Benveniste EN (2014) PERK-dependent activation of JAK1 and STAT3 contributes to endoplasmic reticulum stress-induced inflammation. Mol Cell Biol 34(20):3911–3925. https://doi.org/10.1128/mcb.00980-14
Mendez JM, Kolora LD, Lemon JS, Dupree SL, Keestra-Gounder AM (2019) Activation of the endoplasmic reticulum stress response impacts the NOD1 signaling pathway. Infect Immun 87(8). https://doi.org/10.1128/iai.00826-18
Mijosek V, Lasitschka F, Warth A, Zabeck H, Dalpke AH, Weitnauer M (2016) Endoplasmic reticulum stress is a danger signal promoting innate inflammatory responses in bronchial epithelial cells. J Innate Immun 8(5):464–478. https://doi.org/10.1159/000447668
Mogilenko DA, Haas JT, L'Homme L, Fleury S, Quemener S, Levavasseur M, Becquart C, Wartelle J, Bogomolova A, Pineau L, Molendi-Coste O, Lancel S, Dehondt H, Gheeraert C, Melchior A, Dewas C, Nikitin A, Pic S, Rabhi N, Annicotte JS, Oyadomari S, Velasco-Hernandez T, Cammenga J, Foretz M, Viollet B, Vukovic M, Villacreces A, Kranc K, Carmeliet P, Marot G, Boulter A, Tavernier S, Berod L, Longhi MP, Paget C, Janssens S, Staumont-Salle D, Aksoy E, Staels B, Dombrowicz D (2019) Metabolic and innate immune cues merge into a specific inflammatory response via the UPR. Cell 177(5):1201–1216.e19. https://doi.org/10.1016/j.cell.2019.03.018
Mohammed-Ali Z, Cruz GL, Dickhout JG (2015) Crosstalk between the unfolded protein response and NF-kappaB-mediated inflammation in the progression of chronic kidney disease. J Immunol Res 2015:428508. https://doi.org/10.1155/2015/428508
Murakami T, Ockinger J, Yu J, Byles V, McColl A, Hofer AM, Horng T (2012) Critical role for calcium mobilization in activation of the NLRP3 inflammasome. Proc Natl Acad Sci U S A 109(28):11282–11287. https://doi.org/10.1073/pnas.1117765109
Murphy N, Grehan B, Lynch MA (2014) Glial uptake of amyloid beta induces NLRP3 inflammasome formation via cathepsin-dependent degradation of NLRP10. NeuroMolecular Med 16(1):205–215. https://doi.org/10.1007/s12017-013-8274-6
Namgaladze D, Khodzhaeva V, Brune B (2019) ER-mitochondria communication in cells of the innate immune system. Cells 8(9). https://doi.org/10.3390/cells8091088
Ochoa CD, Wu RF, Terada LS (2018) ROS signaling and ER stress in cardiovascular disease. Mol Asp Med 63:18–29. https://doi.org/10.1016/j.mam.2018.03.002
Oslowski CM, Hara T, O'Sullivan-Murphy B, Kanekura K, Lu S, Hara M, Ishigaki S, Zhu LJ, Hayashi E, Hui ST, Greiner D, Kaufman RJ, Bortell R, Urano F (2012) Thioredoxin-interacting protein mediates ER stress-induced beta cell death through initiation of the inflammasome. Cell Metab 16(2):265–273. https://doi.org/10.1016/j.cmet.2012.07.005
Papaioannou A, Higa A, Jegou G, Jouan F, Pineau R, Saas L, Avril T, Pluquet O, Chevet E (2018) Alterations of EDEM1 functions enhance ATF6 pro-survival signaling. FEBS J 285(22):4146–4164. https://doi.org/10.1111/febs.14669
Pereira CA, Carlos D, Ferreira NS, Silva JF, Zanotto CZ, Zamboni DS, Garcia VD, Ventura DF, Silva JS, Tostes RC (2019) Mitochondrial DNA promotes NLRP3 inflammasome activation and contributes to endothelial dysfunction and inflammation in type 1 diabetes. Front Physiol 10:1557. https://doi.org/10.3389/fphys.2019.01557
Rajamaki K, Lappalainen J, Oorni K, Valimaki E, Matikainen S, Kovanen PT, Eklund KK (2010) Cholesterol crystals activate the NLRP3 inflammasome in human macrophages: a novel link between cholesterol metabolism and inflammation. PLoS One 5(7):e11765. https://doi.org/10.1371/journal.pone.0011765
Rao J, Yue S, Fu Y, Zhu J, Wang X, Busuttil RW, Kupiec-Weglinski JW, Lu L, Zhai Y (2014) ATF6 mediates a pro-inflammatory synergy between ER stress and TLR activation in the pathogenesis of liver ischemia-reperfusion injury. Am J Transplant 14(7):1552–1561. https://doi.org/10.1111/ajt.12711
Robblee MM, Kim CC, Porter Abate J, Valdearcos M, Sandlund KL, Shenoy MK, Volmer R, Iwawaki T, Koliwad SK (2016) Saturated fatty acids engage an IRE1alpha-dependent pathway to activate the NLRP3 inflammasome in myeloid cells. Cell Rep 14(11):2611–2623. https://doi.org/10.1016/j.celrep.2016.02.053
Rosen DA, Seki SM, Fernandez-Castaneda A, Beiter RM, Eccles JD, Woodfolk JA, Gaultier A (2019) Modulation of the sigma-1 receptor-IRE1 pathway is beneficial in preclinical models of inflammation and sepsis. Sci Transl Med 11(478). https://doi.org/10.1126/scitranslmed.aau5266
Sagar V, Vatapalli R, Lysy B, Pamarthy S, Anker JF, Rodriguez Y, Han H, Unno K, Stadler WM, Catalona WJ, Hussain M, Gill PS, Abdulkadir SA (2019) EPHB4 inhibition activates ER stress to promote immunogenic cell death of prostate cancer cells. Cell Death Dis 10(11):801. https://doi.org/10.1038/s41419-019-2042-y
Saito A, Imaizumi K (2018) Unfolded protein response-dependent communication and contact among endoplasmic reticulum, mitochondria, and plasma membrane. Int J Mol Sci 19(10). https://doi.org/10.3390/ijms19103215
Samstad EO, Niyonzima N, Nymo S, Aune MH, Ryan L, Bakke SS, Lappegard KT, Brekke OL, Lambris JD, Damas JK, Latz E, Mollnes TE, Espevik T (2014) Cholesterol crystals induce complement-dependent inflammasome activation and cytokine release. J Immunol 192(6):2837–2845. https://doi.org/10.4049/jimmunol.1302484
Singh M, Kumari B, Yadav UCS (2019) Regulation of oxidized LDL-induced inflammatory process through NLRP3 inflammasome activation by the deubiquitinating enzyme BRCC36. Inflamm Res 68(12):999–1010. https://doi.org/10.1007/s00011-019-01281-5
Song MJ, Malhi H (2019) The unfolded protein response and hepatic lipid metabolism in non alcoholic fatty liver disease. Pharmacol Ther 203:107401. https://doi.org/10.1016/j.pharmthera.2019.107401
Sun Z, Brodsky JL (2019) Protein quality control in the secretory pathway. J Cell Biol 218(10):3171–3187. https://doi.org/10.1083/jcb.201906047
Sundaram A, Appathurai S, Plumb R, Mariappan M (2018) Dynamic changes in complexes of IRE1alpha, PERK, and ATF6alpha during endoplasmic reticulum stress. Mol Biol Cell 29(11):1376–1388. https://doi.org/10.1091/mbc.E17-10-0594
Talty A, Deegan S, Ljujic M, Mnich K, Naicker SD, Quandt D, Zeng Q, Patterson JB, Gorman AM, Griffin MD, Samali A, Logue SE (2019) Inhibition of IRE1alpha RNase activity reduces NLRP3 inflammasome assembly and processing of pro-IL1beta. Cell Death Dis 10(9):622–611. https://doi.org/10.1038/s41419-019-1847-z
Tam AB, Koong AC, Niwa M (2014) Ire1 has distinct catalytic mechanisms for XBP1/HAC1 splicing and RIDD. Cell Rep 9(3):850–858. https://doi.org/10.1016/j.celrep.2014.09.016
Thoudam T, Jeon JH, Ha CM, Lee IK (2016) Role of mitochondria-associated endoplasmic reticulum membrane in inflammation-mediated metabolic diseases. Mediat Inflamm 2016:1851420. https://doi.org/10.1155/2016/1851420
Tu BP, Weissman JS (2004) Oxidative protein folding in eukaryotes: mechanisms and consequences. J Cell Biol 164(3):341–346. https://doi.org/10.1083/jcb.200311055
Tufanli O, Telkoparan Akillilar P, Acosta-Alvear D, Kocaturk B, Onat UI, Hamid SM, Cimen I, Walter P, Weber C, Erbay E (2017) Targeting IRE1 with small molecules counteracts progression of atherosclerosis. Proc Natl Acad Sci U S A 114(8):E1395–e1404. https://doi.org/10.1073/pnas.1621188114
Urra H, Hetz C (2014) A novel ER stress-independent function of the UPR in angiogenesis. Mol Cell 54(4):542–544. https://doi.org/10.1016/j.molcel.2014.05.013
Vekich JA, Belmont PJ, Thuerauf DJ, Glembotski CC (2012) Protein disulfide isomerase-associated 6 is an ATF6-inducible ER stress response protein that protects cardiac myocytes from ischemia/reperfusion-mediated cell death. J Mol Cell Cardiol 53(2):259–267. https://doi.org/10.1016/j.yjmcc.2012.05.005
Wang K, Yao Y, Zhu X, Zhang K, Zhou F, Zhu L (2017) Amyloid beta induces NLRP3 inflammasome activation in retinal pigment epithelial cells via NADPH oxidase- and mitochondria-dependent ROS production. J Biochem Mol Toxicol 31(6). https://doi.org/10.1002/jbt.21887
Wang W, Li G, De W, Luo Z, Pan P, Tian M, Wang Y, Xiao F, Li A, Wu K, Liu X, Rao L, Liu F, Liu Y, Wu J (2018) Zika virus infection induces host inflammatory responses by facilitating NLRP3 inflammasome assembly and interleukin-1beta secretion. Nat Commun 9(1):106. https://doi.org/10.1038/s41467-017-02645-3
Wang G, Xue Y, Wang Y, Dong F, Shen M, Zong R, Liu Z, Li C (2019) The role of autophagy in the pathogenesis of exposure keratitis. J Cell Mol Med 23(6):4217–4228. https://doi.org/10.1111/jcmm.14310
Weber K, Schilling JD (2014) Lysosomes integrate metabolic-inflammatory cross-talk in primary macrophage inflammasome activation. J Biol Chem 289(13):9158–9171. https://doi.org/10.1074/jbc.M113.531202
Wen Y, Shi Y (2016) Alum: an old dog with new tricks. Emerg Microbes Infect 5:e25. https://doi.org/10.1038/emi.2016.40
Yang Z, Liu Q, Shi H, Jiang X, Wang S, Lu Y, Zhang J, Huang X, Yu A (2018) Interleukin 17A exacerbates ER-stress-mediated inflammation of macrophages following ICH. Mol Immunol 101:38–45. https://doi.org/10.1016/j.molimm.2018.05.020
Young SK, Shao Y, Bidwell JP, Wek RC (2016) Nuclear matrix protein 4 is a novel regulator of ribosome biogenesis and controls the unfolded protein response via repression of Gadd34 expression. J Biol Chem 291(26):13780–13788. https://doi.org/10.1074/jbc.M116.729830
Yu X, Lan P, Hou X, Han Q, Lu N, Li T, Jiao C, Zhang J, Zhang C, Tian Z (2017) HBV inhibits LPS-induced NLRP3 inflammasome activation and IL-1beta production via suppressing the NF-kappaB pathway and ROS production. J Hepatol 66(4):693–702. https://doi.org/10.1016/j.jhep.2016.12.018
Yue Y, Stanojlovic M, Lin Y, Karsenty G, Lin W (2019) Oligodendrocyte-specific ATF4 inactivation does not influence the development of EAE. J Neuroinflammation 16(1):23. https://doi.org/10.1186/s12974-019-1415-6
Yuliana A, Daijo A, Jheng HF, Kwon J, Nomura W, Takahashi H, Ara T, Kawada T, Goto T (2019) Endoplasmic reticulum stress impaired uncoupling protein 1 expression via the suppression of peroxisome proliferator-activated receptor gamma binding activity in mice beige adipocytes. Int J Mol Sci 20(2). https://doi.org/10.3390/ijms20020274
Zhang H, Zhao C, Wang S, Huang Y, Wang H, Zhao J, Yang N (2015) Anti-dsDNA antibodies induce inflammation via endoplasmic reticulum stress in human mesangial cells. J Transl Med 13:178. https://doi.org/10.1186/s12967-015-0536-7
Zhang Q, Lenardo MJ, Baltimore D (2017) 30 years of NF-kappaB: a blossoming of relevance to human pathobiology. Cell 168(1–2):37–57. https://doi.org/10.1016/j.cell.2016.12.012
Zhong Z, Liang S, Sanchez-Lopez E, He F, Shalapour S, Lin XJ, Wong J, Ding S, Seki E, Schnabl B, Hevener AL, Greenberg HB, Kisseleva T, Karin M (2018) New mitochondrial DNA synthesis enables NLRP3 inflammasome activation. Nature 560(7717):198–203. https://doi.org/10.1038/s41586-018-0372-z
Zhou R, Tardivel A, Thorens B, Choi I, Tschopp J (2010) Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat Immunol 11(2):136–140. https://doi.org/10.1038/ni.1831
Acknowledgments
Thanks to everyone who helped me in the past three years, and thank my boyfriend to accompany me through those difficult times.
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This study was supported by the National Natural Science Foundation of China (No 81201331) and Major special projects of the Hunan Provincial Health and Family Planning Commission (A2017011).
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Wrote the paper: Wei Li and Ting Cao. Revised the paper: Chunyi Luo, Xiangping Zhou, and Jialun Jia. Critically revised the manuscript for important intellectual content: Xinhua Xiao and Shuangquan Liu. All authors read and approved the final manuscript.
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Li, W., Cao, T., Luo, C. et al. Crosstalk between ER stress, NLRP3 inflammasome, and inflammation. Appl Microbiol Biotechnol 104, 6129–6140 (2020). https://doi.org/10.1007/s00253-020-10614-y
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DOI: https://doi.org/10.1007/s00253-020-10614-y