{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T17:49:07Z","timestamp":1790617747646,"version":"4.1.0"},"reference-count":47,"publisher":"Rockefeller University Press","issue":"10","license":[{"start":{"date-parts":[[2019,9,19]],"date-time":"2019-09-19T00:00:00Z","timestamp":1568851200000},"content-version":"vor","delay-in-days":762,"URL":"http:\/\/www.rupress.org\/terms\/"},{"start":{"date-parts":[[2018,4,2]],"date-time":"2018-04-02T00:00:00Z","timestamp":1522627200000},"content-version":"vor","delay-in-days":227,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-sa\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["DK30104150003"],"award-info":[{"award-number":["DK30104150003"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["DK30104150035"],"award-info":[{"award-number":["DK30104150035"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002858","name":"China Postdoctoral Science Foundation","doi-asserted-by":"publisher","award":["2014M560340"],"award-info":[{"award-number":["2014M560340"]}],"id":[{"id":"10.13039\/501100002858","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["rupress.org"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2017,10,2]]},"abstract":"<jats:p>Although genetic polymorphisms in the LRRK2 gene are associated with a variety of diseases, the physiological function of LRRK2 remains poorly understood. In this study, we report a crucial role for LRRK2 in the activation of the NLRC4 inflammasome during host defense against Salmonella enteric serovar Typhimurium infection. LRRK2 deficiency reduced caspase-1 activation and IL-1\u03b2 secretion in response to NLRC4 inflammasome activators in macrophages. Lrrk2\u2212\/\u2212 mice exhibited impaired clearance of pathogens after acute S. Typhimurium infection. Mechanistically, LRRK2 formed a complex with NLRC4 in the macrophages, and the formation of the LRRK2\u2013NLRC4 complex led to the phosphorylation of NLRC4 at Ser533. Importantly, the kinase activity of LRRK2 is required for optimal NLRC4 inflammasome activation. Collectively, our study reveals an important role for LRRK2 in the host defense by promoting NLRC4 inflammasome activation.<\/jats:p>","DOI":"10.1084\/jem.20170014","type":"journal-article","created":{"date-parts":[[2017,8,18]],"date-time":"2017-08-18T14:10:15Z","timestamp":1503065415000},"page":"3051-3066","update-policy":"https:\/\/doi.org\/10.1084\/jem.crossmarkpolicy","source":"Crossref","is-referenced-by-count":165,"title":["LRRK2 promotes the activation of NLRC4 inflammasome during <i>Salmonella<\/i> Typhimurium infection"],"prefix":"10.1084","volume":"214","author":[{"given":"Weiwei","family":"Liu","sequence":"first","affiliation":[{"name":"Shanghai Institute of Immunology, Shanghai Jiao Tong University School of Medicine, Shanghai, China 1"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xia\u2019nan","family":"Liu","sequence":"additional","affiliation":[{"name":"Shanghai Institute of Immunology, Shanghai Jiao Tong University School of Medicine, Shanghai, China 1"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yu","family":"Li","sequence":"additional","affiliation":[{"name":"Shanghai Institute of Immunology, Shanghai Jiao Tong University School of Medicine, Shanghai, China 1"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Junjie","family":"Zhao","sequence":"additional","affiliation":[{"name":"Department of Immunology, Cleveland Clinic, Cleveland, OH 3"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhenshan","family":"Liu","sequence":"additional","affiliation":[{"name":"Shanghai Institute of Immunology, Shanghai Jiao Tong University School of Medicine, Shanghai, China 1"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhuqin","family":"Hu","sequence":"additional","affiliation":[{"name":"Shanghai Institute of Immunology, Shanghai Jiao Tong University School of Medicine, Shanghai, China 1"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ying","family":"Wang","sequence":"additional","affiliation":[{"name":"Shanghai Institute of Immunology, Shanghai Jiao Tong University School of Medicine, Shanghai, China 1"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0849-3797","authenticated-orcid":true,"given":"Yufeng","family":"Yao","sequence":"additional","affiliation":[{"name":"Department of Immunology and Microbiology, Shanghai Jiao Tong University School of Medicine, Shanghai, China 2"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aaron W.","family":"Miller","sequence":"additional","affiliation":[{"name":"Department of Immunology, Cleveland Clinic, Cleveland, OH 3"},{"name":"Department of Urology, Cleveland Clinic, Cleveland, OH 4"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bing","family":"Su","sequence":"additional","affiliation":[{"name":"Shanghai Institute of Immunology, Shanghai Jiao Tong University School of Medicine, Shanghai, China 1"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mark R.","family":"Cookson","sequence":"additional","affiliation":[{"name":"Cell Biology and Gene Expression Section, Laboratory of Neurogenetics, National Institute on Aging, Bethesda, MD 5"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4872-9525","authenticated-orcid":true,"given":"Xiaoxia","family":"Li","sequence":"additional","affiliation":[{"name":"Department of Immunology, Cleveland Clinic, Cleveland, OH 3"},{"name":"Department of Molecular Medicine, Cleveland Clinic Lerner College of Medicine, Case Western Reserve University, Cleveland, OH 6"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5621-8912","authenticated-orcid":true,"given":"Zizhen","family":"Kang","sequence":"additional","affiliation":[{"name":"Shanghai Institute of Immunology, Shanghai Jiao Tong University School of Medicine, Shanghai, China 1"},{"name":"Department of Immunology, Cleveland Clinic, Cleveland, OH 3"},{"name":"Department of Molecular Medicine, Cleveland Clinic Lerner College of Medicine, Case Western Reserve University, Cleveland, OH 6"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"291","published-online":{"date-parts":[[2017,8,18]]},"reference":[{"key":"2023072603355472500_bib1","doi-asserted-by":"publisher","first-page":"35217","DOI":"10.1074\/jbc.M604933200","article-title":"Regulation of Legionella phagosome maturation and infection through flagellin and host Ipaf","volume":"281","author":"Amer","year":"2006","journal-title":"J. Biol. Chem."},{"key":"2023072603355472500_bib2","doi-asserted-by":"publisher","first-page":"246","DOI":"10.1038\/ng.764","article-title":"Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47","volume":"43","author":"Anderson","year":"2011","journal-title":"Nat. Genet."},{"key":"2023072603355472500_bib3","first-page":"116","article-title":"Association between sporadic Parkinson disease and interleukin-1\u03b2 -511 gene polymorphisms in the Turkish population","volume":"21","author":"Arman","year":"2010","journal-title":"Eur. Cytokine Netw."},{"key":"2023072603355472500_bib4","doi-asserted-by":"publisher","first-page":"955","DOI":"10.1038\/ng.175","article-title":"Genome-wide association defines more than 30 distinct susceptibility loci for Crohn\u2019s disease","volume":"40","author":"Barrett","year":"2008","journal-title":"Nat. Genet."},{"key":"2023072603355472500_bib5","doi-asserted-by":"publisher","first-page":"1745","DOI":"10.1084\/jem.20100257","article-title":"Redundant roles for inflammasome receptors NLRP3 and NLRC4 in host defense against Salmonella","volume":"207","author":"Broz","year":"2010","journal-title":"J. Exp. Med."},{"key":"2023072603355472500_bib6","doi-asserted-by":"publisher","first-page":"1981","DOI":"10.1128\/IAI.01382-08","article-title":"Asc and Ipaf Inflammasomes direct distinct pathways for caspase-1 activation in response to Legionella pneumophila","volume":"77","author":"Case","year":"2009","journal-title":"Infect. Immun."},{"key":"2023072603355472500_bib7","doi-asserted-by":"publisher","first-page":"570","DOI":"10.1016\/j.celrep.2014.06.028","article-title":"The neutrophil NLRC4 inflammasome selectively promotes IL-1\u03b2 maturation without pyroptosis during acute Salmonella challenge","volume":"8","author":"Chen","year":"2014","journal-title":"Cell Reports."},{"key":"2023072603355472500_bib8","doi-asserted-by":"publisher","first-page":"5827","DOI":"10.1038\/ncomms6827","article-title":"Phosphorylation of LRRK2 by casein kinase 1\u03b1 regulates trans-Golgi clustering via differential interaction with ARHGEF7","volume":"5","author":"Chia","year":"2014","journal-title":"Nat. Commun."},{"key":"2023072603355472500_bib9","doi-asserted-by":"publisher","first-page":"791","DOI":"10.1038\/nrn2935","article-title":"The role of leucine-rich repeat kinase 2 (LRRK2) in Parkinson\u2019s disease","volume":"11","author":"Cookson","year":"2010","journal-title":"Nat. Rev. Neurosci."},{"key":"2023072603355472500_bib10","doi-asserted-by":"publisher","first-page":"42","DOI":"10.1007\/s11910-015-0564-y","article-title":"LRRK2 pathways leading to neurodegeneration","volume":"15","author":"Cookson","year":"2015","journal-title":"Curr. Neurol. Neurosci. Rep."},{"key":"2023072603355472500_bib11","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1038\/nchembio.538","article-title":"Characterization of a selective inhibitor of the Parkinson\u2019s disease kinase LRRK2","volume":"7","author":"Deng","year":"2011","journal-title":"Nat. Chem. Biol."},{"key":"2023072603355472500_bib12","doi-asserted-by":"crossref","first-page":"889","DOI":"10.1002\/mds.26529","article-title":"Increased peripheral inflammation in asymptomatic leucine-rich repeat kinase 2 mutation carriers","volume":"31","author":"Dzamko","year":"2016","journal-title":"Mov. Disord."},{"key":"2023072603355472500_bib13","doi-asserted-by":"publisher","first-page":"576","DOI":"10.1038\/ni1346","article-title":"Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1\u03b2 in salmonella-infected macrophages","volume":"7","author":"Franchi","year":"2006","journal-title":"Nat. Immunol."},{"key":"2023072603355472500_bib14","doi-asserted-by":"publisher","first-page":"1118","DOI":"10.1038\/ng.717","article-title":"Genome-wide meta-analysis increases to 71 the number of confirmed Crohn\u2019s disease susceptibility loci","volume":"42","author":"Franke","year":"2010","journal-title":"Nat. Genet."},{"key":"2023072603355472500_bib15","doi-asserted-by":"publisher","first-page":"5577","DOI":"10.4049\/jimmunol.1000548","article-title":"LRRK2 is involved in the IFN-\u03b3 response and host response to pathogens","volume":"185","author":"Gardet","year":"2010","journal-title":"J. Immunol."},{"key":"2023072603355472500_bib16","doi-asserted-by":"publisher","first-page":"1247","DOI":"10.1038\/ni.2749","article-title":"Phosphorylation of the adaptor ASC acts as a molecular switch that controls the formation of speck-like aggregates and inflammasome activity","volume":"14","author":"Hara","year":"2013","journal-title":"Nat. Immunol."},{"key":"2023072603355472500_bib17","doi-asserted-by":"publisher","first-page":"172","DOI":"10.1126\/science.1236381","article-title":"Crystal structure of NLRC4 reveals its autoinhibition mechanism","volume":"341","author":"Hu","year":"2013","journal-title":"Science."},{"key":"2023072603355472500_bib18","doi-asserted-by":"publisher","first-page":"399","DOI":"10.1126\/science.aac5489","article-title":"Structural and biochemical basis for induced self-propagation of NLRC4","volume":"350","author":"Hu","year":"2015","journal-title":"Science."},{"key":"2023072603355472500_bib19","doi-asserted-by":"publisher","first-page":"781","DOI":"10.1212\/WNL.0b013e318249f673","article-title":"The LRRK2 G2019S mutation is associated with Parkinson disease and concomitant non-skin cancers","volume":"78","author":"Inzelberg","year":"2012","journal-title":"Neurology."},{"key":"2023072603355472500_bib20","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1016\/S0092-8674(00)81092-2","article-title":"Active and inactive protein kinases: Structural basis for regulation","volume":"85","author":"Johnson","year":"1996","journal-title":"Cell."},{"key":"2023072603355472500_bib21","doi-asserted-by":"publisher","first-page":"7403","DOI":"10.1073\/pnas.1402911111","article-title":"Inflammasome activation causes dual recruitment of NLRC4 and NLRP3 to the same macromolecular complex","volume":"111","author":"Man","year":"2014","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"2023072603355472500_bib22","doi-asserted-by":"publisher","first-page":"33835","DOI":"10.1074\/jbc.274.48.33835","article-title":"ASC, a novel 22-kDa protein, aggregates during apoptosis of human promyelocytic leukemia HL-60 cells","volume":"274","author":"Masumoto","year":"1999","journal-title":"J. Biol. Chem."},{"key":"2023072603355472500_bib23","doi-asserted-by":"publisher","first-page":"7128","DOI":"10.1523\/JNEUROSCI.3314-15.2016","article-title":"Altered development of synapse structure and function in striatum caused by Parkinson\u2019s disease-linked LRRK2-G2019S mutation","volume":"36","author":"Matikainen-Ankney","year":"2016","journal-title":"J. Neurosci."},{"key":"2023072603355472500_bib24","doi-asserted-by":"publisher","first-page":"1541","DOI":"10.1073\/pnas.1417945112","article-title":"Flagellin-induced NLRC4 phosphorylation primes the inflammasome for activation by NAIP5","volume":"112","author":"Matusiak","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"2023072603355472500_bib25","doi-asserted-by":"publisher","first-page":"1136","DOI":"10.1038\/ni.1960","article-title":"Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria","volume":"11","author":"Miao","year":"2010","journal-title":"Nat. Immunol."},{"key":"2023072603355472500_bib26","doi-asserted-by":"publisher","first-page":"3076","DOI":"10.1073\/pnas.0913087107","article-title":"Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome","volume":"107","author":"Miao","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA."},{"key":"2023072603355472500_bib27","doi-asserted-by":"publisher","first-page":"661","DOI":"10.1016\/j.molcel.2004.08.024","article-title":"Regulation of protein kinases: Controlling activity through activation segment conformation","volume":"15","author":"Nolen","year":"2004","journal-title":"Mol. Cell."},{"key":"2023072603355472500_bib28","doi-asserted-by":"publisher","first-page":"595","DOI":"10.1016\/j.neuron.2004.10.023","article-title":"Cloning of the gene containing mutations that cause PARK8-linked Parkinson\u2019s disease","volume":"44","author":"Pais\u00e1n-Ru\u00edz","year":"2004","journal-title":"Neuron."},{"key":"2023072603355472500_bib29","doi-asserted-by":"publisher","first-page":"1880","DOI":"10.1093\/brain\/awn101","article-title":"Central and systemic IL-1 exacerbates neurodegeneration and motor symptoms in a model of Parkinson\u2019s disease","volume":"131","author":"Pott Godoy","year":"2008","journal-title":"Brain."},{"key":"2023072603355472500_bib30","doi-asserted-by":"publisher","first-page":"539","DOI":"10.1038\/nature11429","article-title":"Phosphorylation of NLRC4 is critical for inflammasome activation","volume":"490","author":"Qu","year":"2012","journal-title":"Nature."},{"key":"2023072603355472500_bib31","doi-asserted-by":"publisher","first-page":"877","DOI":"10.1084\/jem.20132234","article-title":"NLRP3 recruitment by NLRC4 during Salmonella infection","volume":"213","author":"Qu","year":"2016","journal-title":"J. Exp. Med."},{"key":"2023072603355472500_bib32","doi-asserted-by":"publisher","first-page":"5625","DOI":"10.1016\/j.bmcl.2012.06.104","article-title":"GSK2578215A; A potent and highly selective 2-arylmethyloxy-5-substitutent-N-arylbenzamide LRRK2 kinase inhibitor","volume":"22","author":"Reith","year":"2012","journal-title":"Bioorg. Med. Chem. Lett."},{"key":"2023072603355472500_bib33","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.jneuroim.2013.09.020","article-title":"The innate and adaptive immunological aspects in neurodegenerative diseases","volume":"269","author":"Rodrigues","year":"2014","journal-title":"J. Neuroimmunol."},{"key":"2023072603355472500_bib34","doi-asserted-by":"publisher","first-page":"20","DOI":"10.1186\/1741-7015-10-20","article-title":"Is inhibition of kinase activity the only therapeutic strategy for LRRK2-associated Parkinson\u2019s disease?","volume":"10","author":"Rudenko","year":"2012","journal-title":"BMC Med."},{"key":"2023072603355472500_bib35","doi-asserted-by":"publisher","first-page":"e1368","DOI":"10.1038\/cddis.2014.320","article-title":"The LRRK2 inhibitor GSK2578215A induces protective autophagy in SH-SY5Y cells: involvement of Drp-1-mediated mitochondrial fission and mitochondrial-derived ROS signaling","volume":"5","author":"Saez-Atienzar","year":"2014","journal-title":"Cell Death Dis."},{"key":"2023072603355472500_bib36","doi-asserted-by":"crossref","first-page":"2536","DOI":"10.1002\/mds.23314","article-title":"LRRK2 G2019S mutations are associated with an increased cancer risk in Parkinson disease","volume":"25","author":"Saunders-Pullman","year":"2010","journal-title":"Mov. Disord."},{"key":"2023072603355472500_bib37","doi-asserted-by":"publisher","first-page":"821","DOI":"10.1016\/j.cell.2010.01.040","article-title":"The inflammasomes","volume":"140","author":"Schroder","year":"2010","journal-title":"Cell."},{"key":"2023072603355472500_bib38","doi-asserted-by":"publisher","first-page":"660","DOI":"10.1038\/nature15514","article-title":"Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death","volume":"526","author":"Shi","year":"2015","journal-title":"Nature."},{"key":"2023072603355472500_bib39","doi-asserted-by":"publisher","first-page":"3235","DOI":"10.1084\/jem.20071239","article-title":"Immune recognition of Pseudomonas aeruginosa mediated by the IPAF\/NLRC4 inflammasome","volume":"204","author":"Sutterwala","year":"2007","journal-title":"J. Exp. Med."},{"key":"2023072603355472500_bib40","doi-asserted-by":"publisher","first-page":"e111","DOI":"10.1371\/journal.ppat.0030111","article-title":"Differential regulation of caspase-1 activation, pyroptosis, and autophagy via Ipaf and ASC in Shigella-infected macrophages","volume":"3","author":"Suzuki","year":"2007","journal-title":"PLoS Pathog."},{"key":"2023072603355472500_bib41","doi-asserted-by":"publisher","first-page":"84","DOI":"10.1016\/j.coi.2015.01.010","article-title":"The NAIP\/NLRC4 inflammasomes","volume":"32","author":"Vance","year":"2015","journal-title":"Curr. Opin. Immunol."},{"key":"2023072603355472500_bib42","doi-asserted-by":"publisher","first-page":"836","DOI":"10.1001\/archneur.64.6.836","article-title":"Inflammatory cytokine gene polymorphisms and increased risk of Parkinson disease","volume":"64","author":"Wahner","year":"2007","journal-title":"Arch. Neurol."},{"key":"2023072603355472500_bib43","doi-asserted-by":"publisher","first-page":"2609","DOI":"10.1056\/NEJMoa0903753","article-title":"Genomewide association study of leprosy","volume":"361","author":"Zhang","year":"2009","journal-title":"N. Engl. J. Med."},{"key":"2023072603355472500_bib44","doi-asserted-by":"publisher","first-page":"404","DOI":"10.1126\/science.aac5789","article-title":"Cryo-EM structure of the activated NAIP2-NLRC4 inflammasome reveals nucleated polymerization","volume":"350","author":"Zhang","year":"2015","journal-title":"Science."},{"key":"2023072603355472500_bib45","doi-asserted-by":"publisher","first-page":"918","DOI":"10.1038\/ni.3233","article-title":"Commensal bacteria direct selective cargo sorting to promote symbiosis","volume":"16","author":"Zhang","year":"2015","journal-title":"Nat. Immunol."},{"key":"2023072603355472500_bib46","doi-asserted-by":"publisher","first-page":"596","DOI":"10.1038\/nature10510","article-title":"The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus","volume":"477","author":"Zhao","year":"2011","journal-title":"Nature."},{"key":"2023072603355472500_bib47","doi-asserted-by":"publisher","first-page":"601","DOI":"10.1016\/j.neuron.2004.11.005","article-title":"Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology","volume":"44","author":"Zimprich","year":"2004","journal-title":"Neuron."}],"container-title":["Journal of Experimental Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/rupress.org\/jem\/article-pdf\/214\/10\/3051\/1756278\/jem_20170014.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/rupress.org\/jem\/article-pdf\/214\/10\/3051\/1756278\/jem_20170014.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,7,26]],"date-time":"2023-07-26T03:37:42Z","timestamp":1690342662000},"score":1,"resource":{"primary":{"URL":"https:\/\/rupress.org\/jem\/article\/214\/10\/3051\/42244\/LRRK2-promotes-the-activation-of-NLRC4"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,8,18]]},"references-count":47,"journal-issue":{"issue":"10","published-print":{"date-parts":[[2017,10,2]]}},"URL":"https:\/\/doi.org\/10.1084\/jem.20170014","relation":{},"ISSN":["0022-1007","1540-9538"],"issn-type":[{"value":"0022-1007","type":"print"},{"value":"1540-9538","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,8,18]]}}}