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Here, we explore the role and precise mechanism of Van-Gogh-like 2 (VANGL2) during the pathogenesis of IBD. VANGL2 decreases in IBD patients and dextran sulfate sodium (DSS)-induced colitis in mice. Myeloid VANGL2 deficiency exacerbates the progression of DSS-induced colitis in mice and specifically enhances the activation of NLRP3 inflammasome in macrophages. NLRP3-specific inhibitor MCC950 effectively alleviates DSS-induced colitis in VANGL2 deficient mice. Mechanistically, VANGL2 interacts with NLRP3 and promotes the autophagic degradation of NLRP3 through enhancing the K27-linked polyubiquitination at lysine 823 of NLRP3 by recruiting E3 ligase MARCH8, leading to optineurin (OPTN)-mediated selective autophagy. Notably, decreased VANGL2 in the peripheral blood mononuclear cells from IBD patients results in overt NLRP3 inflammasome activation and sustained inflammation. Taken together, this study demonstrates that VANGL2 acts as a repressor of IBD progression by inhibiting NLRP3 inflammasome activation and provides insights into the crosstalk between inflammation and autophagy in preventing IBD.<\/jats:p>","DOI":"10.1371\/journal.pbio.3002961","type":"journal-article","created":{"date-parts":[[2025,2,3]],"date-time":"2025-02-03T18:21:43Z","timestamp":1738606903000},"page":"e3002961","update-policy":"https:\/\/doi.org\/10.1371\/journal.pbio.corrections_policy","source":"Crossref","is-referenced-by-count":9,"title":["VANGL2 alleviates inflammatory bowel disease by recruiting the ubiquitin ligase MARCH8 to limit NLRP3 inflammasome activation through OPTN-mediated selective autophagy"],"prefix":"10.1371","volume":"23","author":[{"given":"Huaji","family":"Jiang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yingchao","family":"Xie","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhiqiang","family":"Hu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiansen","family":"Lu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiahuan","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hongyu","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ke","family":"Zeng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenqiang","family":"Peng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cheng","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Junsheng","family":"Huang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zelong","family":"Han","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaochun","family":"Bai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2491-9110","authenticated-orcid":true,"given":"Xiao","family":"Yu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2025,2,3]]},"reference":[{"key":"pbio.3002961.ref001","article-title":"behaviour, and environmental modification for the management of patients with inflammatory bowel diseases: an International Organization for Study of Inflammatory","author":"A Ana","year":"2022","journal-title":"Bowel Diseases consensus"},{"key":"pbio.3002961.ref002","doi-asserted-by":"crossref","first-page":"108176","DOI":"10.1016\/j.pharmthera.2022.108176","article-title":"Macrophage immunometabolism in inflammatory bowel diseases: From pathogenesis to therapy","volume":"238","author":"X Pan","year":"2022","journal-title":"Pharmacol Ther"},{"key":"pbio.3002961.ref003","doi-asserted-by":"crossref","first-page":"2566","DOI":"10.3389\/fimmu.2018.02566","article-title":"The Role of NLRP3 and IL-1beta in the Pathogenesis of Inflammatory Bowel Disease.","volume":"9","author":"L Mao","year":"2018","journal-title":"Front Immunol."},{"issue":"5","key":"pbio.3002961.ref004","doi-asserted-by":"crossref","first-page":"550","DOI":"10.1038\/s41590-021-00886-5","article-title":"NLRP3 inflammasome in cancer and metabolic diseases","volume":"22","author":"BR Sharma","year":"2021","journal-title":"Nat Immunol"},{"issue":"12","key":"pbio.3002961.ref005","doi-asserted-by":"crossref","first-page":"906","DOI":"10.1038\/s41419-019-2157-1","article-title":"NEK7 interacts with NLRP3 to modulate the pyroptosis in inflammatory bowel disease via NF-kappaB signaling","volume":"10","author":"X Chen","year":"2019","journal-title":"Cell Death Dis"},{"key":"pbio.3002961.ref006","doi-asserted-by":"crossref","first-page":"276","DOI":"10.3389\/fimmu.2019.00276","article-title":"NLRP3 Inflammasome and Inflammatory Bowel Disease.","volume":"10","author":"Y Zhen","year":"2019","journal-title":"Front Immunol."},{"issue":"1","key":"pbio.3002961.ref007","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1038\/ng.285","article-title":"Common variants in the NLRP3 region contribute to Crohn\u2019s disease susceptibility","volume":"41","author":"AC Villani","year":"2009","journal-title":"Nat Genet"},{"issue":"1","key":"pbio.3002961.ref008","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1080\/15548627.2019.1635384","article-title":"New insights into the interplay between autophagy, gut microbiota and inflammatory responses","volume":"16","author":"A Larabi","year":"2020","journal-title":"IBD. 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