دورية أكاديمية
Priming of NLRP3 inflammasome activation by Msn kinase MINK1 in macrophages.
| العنوان: | Priming of NLRP3 inflammasome activation by Msn kinase MINK1 in macrophages. |
|---|---|
| المؤلفون: | Zhu K; Institute of Immunology and Department of Rheumatology, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, 310058, P. R. China.; Zhejiang University-University of Edinburgh Institute, Zhejiang University School of Medicine, Haining, 314400, P. R. China.; Department of Medical Microbiology and Parasitology, Zhejiang University School of Medicine, Hangzhou, 310058, P. R. China., Jin X; Institute of Immunology and Department of Rheumatology, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, 310058, P. R. China., Chi Z; Department of Immunology, Zhejiang University School of Medicine, Hangzhou, 310058, P. R. China., Chen S; Department of Immunology, Zhejiang University School of Medicine, Hangzhou, 310058, P. R. China.; Department of Colorectal Surgery, The Second Affiliated Hospital, Hangzhou, 310058, P. R. China., Wu S; Medical College, Lishui University, Lishui, 323000, P. R. China., Sloan RD; Zhejiang University-University of Edinburgh Institute, Zhejiang University School of Medicine, Haining, 314400, P. R. China.; Infection Medicine, School of Biomedical Sciences, The University of Edinburgh, Edinburgh, EH16 4SB, Scotland, UK., Lin X; Department of Medical Microbiology and Parasitology, Zhejiang University School of Medicine, Hangzhou, 310058, P. R. China., Neculai D; Department of Cell Biology, Zhejiang University School of Medicine, Hangzhou, 310058, P. R. China., Wang D; Department of Immunology, Zhejiang University School of Medicine, Hangzhou, 310058, P. R. China., Hu H; Department of Pathology and Pathophysiology, Zhejiang University School of Medicine, Hangzhou, 310058, P. R. China., Lu L; Institute of Immunology and Department of Rheumatology, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, 310058, P. R. China. lu_linrong@zju.edu.cn.; Zhejiang University-University of Edinburgh Institute, Zhejiang University School of Medicine, Haining, 314400, P. R. China. lu_linrong@zju.edu.cn.; Dr. Li Dak Sum and Yip Yio Chin Center for Stem Cells and Regenerative Medicine, Zhejiang University School of Medicine, Hangzhou, 310058, P. R. China. lu_linrong@zju.edu.cn. |
| المصدر: | Cellular & molecular immunology [Cell Mol Immunol] 2021 Oct; Vol. 18 (10), pp. 2372-2382. Date of Electronic Publication: 2021 Sep 03. |
| نوع المنشور: | Journal Article; Research Support, Non-U.S. Gov't |
| اللغة: | English |
| بيانات الدورية: | Publisher: Chinese Society of Immunology;; _b Nature Pub. Group Country of Publication: China NLM ID: 101242872 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 2042-0226 (Electronic) Linking ISSN: 16727681 NLM ISO Abbreviation: Cell Mol Immunol Subsets: MEDLINE |
| أسماء مطبوعة: | Original Publication: Beijing, China : Tokyo, Japan : Chinese Society of Immunology; Nature Pub. Group, 2010- |
| مواضيع طبية MeSH: | Inflammasomes* , NLR Family, Pyrin Domain-Containing 3 Protein*, Animals ; Inflammation ; Macrophages ; Mice ; Reactive Oxygen Species |
| مستخلص: | The nucleotide-binding domain, leucine-rich-repeat containing family, pyrin domain-containing 3 (NLRP3) inflammasome is essential in inflammation and inflammatory disorders. Phosphorylation at various sites on NLRP3 differentially regulates inflammasome activation. The Ser725 phosphorylation site on NLRP3 is depicted in multiple inflammasome activation scenarios, but the importance and regulation of this site has not been clarified. The present study revealed that the phosphorylation of Ser725 was an essential step for the priming of the NLRP3 inflammasome in macrophages. We also showed that Ser725 was directly phosphorylated by misshapen (Msn)/NIK-related kinase 1 (MINK1), depending on the direct interaction between MINK1 and the NLRP3 LRR domain. MINK1 deficiency reduced NLRP3 activation and suppressed inflammatory responses in mouse models of acute sepsis and peritonitis. Reactive oxygen species (ROS) upregulated the kinase activity of MINK1 and subsequently promoted inflammasome priming via NLRP3 Ser725 phosphorylation. Eliminating ROS suppressed NLRP3 activation and reduced sepsis and peritonitis symptoms in a MINK1-dependent manner. Altogether, our study reveals a direct regulation of the NLRP3 inflammasome by Msn family kinase MINK1 and suggests that modulation of MINK1 activity is a potential intervention strategy for inflammasome-related diseases. (© 2021. The Author(s), under exclusive licence to CSI and USTC.) |
| References: | Davis BK, Wen H, Ting JP. The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu Rev Immunol. 2011;29:707–35. (PMID: 21219188406731710.1146/annurev-immunol-031210-101405) Evavold CL, Kagan JC. Inflammasomes: threat-assessment organelles of the innate immune system. Immunity. 2019;51:609–24. (PMID: 31473100680109310.1016/j.immuni.2019.08.005) He Y, Hara H, Nunez G. Mechanism and regulation of NLRP3 inflammasome activation. Trends Biochem Sci. 2016;41:1012–21. (PMID: 27669650512393910.1016/j.tibs.2016.09.002) Broz P. Inflammasomes in host defense and autoimmunity. Chimia. 2016;70:853–5. (PMID: 2866135510.2533/chimia.2016.853) Broz P. Inflammasomes: intracellular detection of extracellular bacteria. Cell Res. 2016;26:859–60. (PMID: 27283800497332810.1038/cr.2016.67) Baroja-Mazo A, Martin-Sanchez F, Gomez AI, Martinez CM, Amores-Iniesta J, Compan V, et al. The NLRP3 inflammasome is released as a particulate danger signal that amplifies the inflammatory response. Nat Immunol. 2014;15:738–48. (PMID: 2495250410.1038/ni.2919) Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature. 2006;440:237–41. (PMID: 1640788910.1038/nature04516) Schroder K, Zhou R, Tschopp J. The NLRP3 inflammasome: a sensor for metabolic danger? Science. 2010;327:296–300. (PMID: 2007524510.1126/science.1184003) Wen H, Gris D, Lei Y, Jha S, Zhang L, Huang MT, et al. Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat Immunol. 2011;12:408–15. (PMID: 21478880409039110.1038/ni.2022) Kummer JA, Broekhuizen R, Everett H, Agostini L, Kuijk L, Martinon F, et al. Inflammasome components NALP 1 and 3 show distinct but separate expression profiles in human tissues suggesting a site-specific role in the inflammatory response. J Histochem Cytochem. 2007;55:443–52. (PMID: 1716440910.1369/jhc.6A7101.2006) Broz P, Dixit VM. Inflammasomes: mechanism of assembly, regulation and signalling. Nat Rev Immunol. 2016;16:407–20. (PMID: 2729196410.1038/nri.2016.58) Carta S, Tassi S, Pettinati I, Delfino L, Dinarello CA, Rubartelli A. The rate of interleukin-1beta secretion in different myeloid cells varies with the extent of redox response to Toll-like receptor triggering. J Biol Chem. 2011;286:27069–80. (PMID: 21628463314930010.1074/jbc.M110.203398) Swanson KV, Deng M, Ting JP. The NLRP3 inflammasome: molecular activation and regulation to therapeutics. Nat Rev Immunol. 2019;19:477–89. (PMID: 31036962780724210.1038/s41577-019-0165-0) Song N, Liu ZS, Xue W, Bai ZF, Wang QY, Dai J, et al. NLRP3 phosphorylation is an essential priming event for inflammasome activation. Mol Cell. 2017;68:185–97. e6. (PMID: 2894331510.1016/j.molcel.2017.08.017) Guo C, Xie S, Chi Z, Zhang J, Liu Y, Zhang L, et al. Bile acids control inflammation and metabolic disorder through inhibition of NLRP3 inflammasome. Immunity. 2016;45:802–16. (PMID: 2769261010.1016/j.immuni.2016.09.008) Chi Z, Chen S, Xu T, Zhen W, Yu W, Jiang D, et al. Histone deacetylase 3 couples mitochondria to drive IL-1beta-dependent inflammation by configuring fatty acid oxidation. Mol Cell. 2020;80:43–58. (PMID: 3293710010.1016/j.molcel.2020.08.015) Stutz A, Kolbe CC, Stahl R, Horvath GL, Franklin BS, van Ray O, et al. NLRP3 inflammasome assembly is regulated by phosphorylation of the pyrin domain. J Exp Med. 2017;214:1725–36. (PMID: 28465465546099610.1084/jem.20160933) Spalinger MR, Kasper S, Gottier C, Lang S, Atrott K, Vavricka SR, et al. NLRP3 tyrosine phosphorylation is controlled by protein tyrosine phosphatase PTPN22. J Clin Investig. 2016;126:4388. (PMID: 27801679509691410.1172/JCI90897) Huang Y, Wang H, Hao Y, Lin H, Dong M, Ye J, et al. Myeloid PTEN promotes chemotherapy-induced NLRP3-inflammasome activation and antitumour immunity. Nat Cell Biol. 2020;22:716–27. (PMID: 3236704710.1038/s41556-020-0510-3) Dan I, Watanabe NM, Kobayashi T, Yamashita-Suzuki K, Fukagaya Y, Kajikawa E, et al. Molecular cloning of MINK, a novel member of mammalian GCK family kinases, which is up-regulated during postnatal mouse cerebral development. FEBS Lett. 2000;469:19–23. (PMID: 1070874810.1016/S0014-5793(00)01247-3) Dan I, Watanabe NM, Kusumi A. The Ste20 group kinases as regulators of MAP kinase cascades. Trends Cell Biol. 2001;11:220–30. (PMID: 1131661110.1016/S0962-8924(01)01980-8) Leong SY, Ong BK, Chu JJ. The role of misshapen NCK-related kinase (MINK), a novel Ste20 family kinase, in the IRES-mediated protein translation of human enterovirus 71. PLoS Pathog. 2015;11:e1004686. (PMID: 25747578435205610.1371/journal.ppat.1004686) Nicke B, Bastien J, Khanna SJ, Warne PH, Cowling V, Cook SJ, et al. Involvement of MINK, a Ste20 family kinase, in Ras oncogene-induced growth arrest in human ovarian surface epithelial cells. Mol Cell. 2005;20:673–85. (PMID: 1633759210.1016/j.molcel.2005.10.038) Larhammar M, Huntwork-Rodriguez S, Rudhard Y, Sengupta-Ghosh A, Lewcock JW. The Ste20 family kinases MAP4K4, MINK1, and TNIK converge to regulate stress-induced JNK signaling in neurons. J Neurosci. 2017;37:11074–84. (PMID: 28993483659680810.1523/JNEUROSCI.0905-17.2017) Hussain NK, Hsin H, Huganir RL, Sheng M. MINK and TNIK differentially act on Rap2-mediated signal transduction to regulate neuronal structure and AMPA receptor function. J Neurosci. 2010;30:14786–94. (PMID: 21048137307094310.1523/JNEUROSCI.4124-10.2010) McCarty N, Paust S, Ikizawa K, Dan I, Li X, Cantor H. Signaling by the kinase MINK is essential in the negative selection of autoreactive thymocytes. Nat Immunol. 2005;6:65–72. (PMID: 1560864210.1038/ni1145) Yue M, Luo D, Yu S, Liu P, Zhou Q, Hu M, et al. Misshapen/NIK-related kinase (MINK1) is involved in platelet function, hemostasis, and thrombus formation. Blood. 2016;127:927–37. (PMID: 2659871710.1182/blood-2015-07-659185) Meng Z, Moroishi T, Mottier-Pavie V, Plouffe SW, Hansen CG, Hong AW, et al. MAP4K family kinases act in parallel to MST1/2 to activate LATS1/2 in the Hippo pathway. Nat Commun. 2015;6:8357. (PMID: 2643744310.1038/ncomms9357) Moroishi T, Hayashi T, Pan WW, Fujita Y, Holt MV, Qin J, et al. The Hippo pathway kinases LATS1/2 suppress cancer immunity. Cell. 2016;167:1525–39. (PMID: 27912060551241810.1016/j.cell.2016.11.005) Fu G, Xu Q, Qiu Y, Jin X, Xu T, Dong S, et al. Suppression of Th17 cell differentiation by misshapen/NIK-related kinase MINK1. J Exp Med. 2017;214:1453–69. (PMID: 28400474541333010.1084/jem.20161120) Bauernfeind FG, Horvath G, Stutz A, Alnemri ES, MacDonald K, Speert D, et al. Cutting edge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J Immunol. 2009;183:787–91. (PMID: 1957082210.4049/jimmunol.0901363) Sutterwala FS, Ogura Y, Zamboni DS, Roy CR, Flavell RA. NALP3: a key player in caspase-1 activation. J Endotoxin Res. 2006;12:251–6. (PMID: 1695397810.1177/09680519060120040701) Hornung V, Bauernfeind F, Halle A, Samstad EO, Kono H, Rock KL, et al. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol. 2008;9:847–56. (PMID: 18604214283478410.1038/ni.1631) Hyodo T, Ito S, Hasegawa H, Asano E, Maeda M, Urano T, et al. Misshapen-like kinase 1 (MINK1) is a novel component of striatin-interacting phosphatase and kinase (STRIPAK) and is required for the completion of cytokinesis. J Biol Chem. 2012;287:25019–29. (PMID: 22665485340814310.1074/jbc.M112.372342) Kaneko S, Chen X, Lu P, Yao X, Wright TG, Rajurkar M, et al. Smad inhibition by the Ste20 kinase misshapen. Proc Natl Acad Sci USA. 2011;108:11127–32. (PMID: 21690388313137910.1073/pnas.1104128108) Liu X, Pichulik T, Wolz OO, Dang TM, Stutz A, Dillen C, et al. Human NACHT, LRR, and PYD domain-containing protein 3 (NLRP3) inflammasome activity is regulated by and potentially targetable through Bruton tyrosine kinase. J Allergy Clin Immunol. 2017;140:1054–67. (PMID: 2821643410.1016/j.jaci.2017.01.017) Martinez GJ. MINK1: the missing link between ROS and its inhibition of Th17 cells. J Exp Med. 2017;214:1205–6. (PMID: 28420734541334210.1084/jem.20170571) Zhou R, Yazdi AS, Menu P, Tschopp J. A role for mitochondria in NLRP3 inflammasome activation. Nature. 2011;469:221–5. (PMID: 2112431510.1038/nature09663) Tschopp J, Schroder K. NLRP3 inflammasome activation: the convergence of multiple signalling pathways on ROS production? Nat Rev Immunol. 2010;10:210–5. (PMID: 2016831810.1038/nri2725) Du K, Ramachandran A, Weemhoff JL, Woolbright BL, Jaeschke AH, Chao X, et al. Mito-tempo protects against acute liver injury but induces limited secondary apoptosis during the late phase of acetaminophen hepatotoxicity. Arch Toxicol. 2019;93:163–78. (PMID: 3032431310.1007/s00204-018-2331-8) Iyer SS, He Q, Janczy JR, Elliott EI, Zhong Z, Olivier AK, et al. Mitochondrial cardiolipin is required for Nlrp3 inflammasome activation. Immunity. 2013;39:311–23. (PMID: 23954133377928510.1016/j.immuni.2013.08.001) Dan Dunn J, Alvarez LA, Zhang X, Soldati T. Reactive oxygen species and mitochondria: a nexus of cellular homeostasis. Redox Biol. 2015;6:472–85. (PMID: 10.1016/j.redox.2015.09.005) Liu T, Wang L, Liang P, Wang X, Liu Y, Cai J, et al. USP19 suppresses inflammation and promotes M2-like macrophage polarization by manipulating NLRP3 function via autophagy. Cell Mol Immunol. 2020. https://doi.org/10.1038/s41423-020-00567-7 . Bauernfeind F, Bartok E, Rieger A, Franchi L, Nunez G, Hornung V. Cutting edge: reactive oxygen species inhibitors block priming, but not activation, of the NLRP3 inflammasome. J Immunol. 2011;187:613–7. (PMID: 2167713610.4049/jimmunol.1100613) Tassi S, Carta S, Delfino L, Caorsi R, Martini A, Gattorno M, et al. Altered redox state of monocytes from cryopyrin-associated periodic syndromes causes accelerated IL-1beta secretion. Proc Natl Acad Sci USA. 2010;107:9789–94. (PMID: 20445104290685110.1073/pnas.1000779107) Sanchez-Rodriguez R, Munari F, Angioni R, Venegas F, Agnellini A, Castro-Gil MP, et al. Targeting monoamine oxidase to dampen NLRP3 inflammasome activation in inflammation. Cell Mol Immunol. 2021;18:1311–3. Zhou R, Tardivel A, Thorens B, Choi I, Tschopp J. Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat Immunol. 2010;11:136–40. (PMID: 2002366210.1038/ni.1831) Park YJ, Yoon SJ, Suh HW, Kim DO, Park JR, Jung H, et al. TXNIP deficiency exacerbates endotoxic shock via the induction of excessive nitric oxide synthesis. PLoS Pathog. 2013;9:e1003646. (PMID: 24098117378975410.1371/journal.ppat.1003646) Masters SL, Dunne A, Subramanian SL, Hull RL, Tannahill GM, Sharp FA, et al. Activation of the NLRP3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1beta in type 2 diabetes. Nat Immunol. 2010;11:897–904. (PMID: 20835230310366310.1038/ni.1935) Zhao C, Gillette DD, Li X, Zhang Z, Wen H. Nuclear factor E2-related factor-2 (Nrf2) is required for NLRP3 and AIM2 inflammasome activation. J Biol Chem. 2014;289:17020–9. (PMID: 24798340405914410.1074/jbc.M114.563114) Wegiel B, Larsen R, Gallo D, Chin BY, Harris C, Mannam P, et al. Macrophages sense and kill bacteria through carbon monoxide-dependent inflammasome activation. J Clin Investig. 2014;124:4926–40. (PMID: 25295542434724410.1172/JCI72853) Jhang JJ, Yen GC. The role of Nrf2 in NLRP3 inflammasome activation. Cell Mol Immunol. 2017;14:1011–2. (PMID: 29129911571913810.1038/cmi.2017.114) Freeman TL, Swartz TH. Targeting the NLRP3 inflammasome in severe COVID-19. Front Immunol. 2020;11:1518. (PMID: 32655582732476010.3389/fimmu.2020.01518) Sharif H, Wang L, Wang WL, Magupalli VG, Andreeva L, Qiao Q, et al. Structural mechanism for NEK7-licensed activation of NLRP3 inflammasome. Nature. 2019;570:338–43. (PMID: 31189953677435110.1038/s41586-019-1295-z) Hu Z, Yan C, Liu P, Huang Z, Ma R, Zhang C, et al. Crystal structure of NLRC4 reveals its autoinhibition mechanism. Science. 2013;341:172–5. (PMID: 2376527710.1126/science.1236381) Conway P, Tyka MD, DiMaio F, Konerding DE, Baker D. Relaxation of backbone bond geometry improves protein energy landscape modeling. Protein Sci. 2014;23:47–55. (PMID: 2426521110.1002/pro.2389) Davis IW, Arendall WB 3rd, Richardson DC, Richardson JS. The backrub motion: how protein backbone shrugs when a sidechain dances. Structure. 2006;14:265–74. (PMID: 1647274610.1016/j.str.2005.10.007) Andre I, Bradley P, Wang C, Baker D. Prediction of the structure of symmetrical protein assemblies. Proc Natl Acad Sci USA. 2007;104:17656–61. (PMID: 17978193207706910.1073/pnas.0702626104) |
| فهرسة مساهمة: | Keywords: MINK1 kinase; NLRP3 inflammasome; Phosphorylation; ROS |
| المشرفين على المادة: | 0 (Inflammasomes) 0 (NLR Family, Pyrin Domain-Containing 3 Protein) 0 (Nlrp3 protein, mouse) 0 (Reactive Oxygen Species) |
| تواريخ الأحداث: | Date Created: 20210904 Date Completed: 20220331 Latest Revision: 20230205 |
| رمز التحديث: | 20240628 |
| مُعرف محوري في PubMed: | PMC8414466 |
| DOI: | 10.1038/s41423-021-00761-1 |
| PMID: | 34480147 |
| قاعدة البيانات: | MEDLINE |
Find this article in full text from Springer Verlag. 
Full Text Finder | تدمد: | 2042-0226 |
|---|---|
| DOI: | 10.1038/s41423-021-00761-1 |