{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,31]],"date-time":"2026-08-31T02:19:52Z","timestamp":1788142792391,"version":"build-2803163510"},"reference-count":73,"publisher":"Wiley","license":[{"start":{"date-parts":[[2026,8,30]],"date-time":"2026-08-30T00:00:00Z","timestamp":1788048000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2026,8,30]],"date-time":"2026-08-30T00:00:00Z","timestamp":1788048000000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"content-domain":{"domain":["advanced.onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Advanced Science"],"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>\n                    Planar cell polarity (PCP) signaling is an evolutionarily conserved mechanism regulating polarized cellular and tissue behaviors in diverse morphogenetic and physiological processes. Disruption or aberrant activation of PCP signaling can cause developmental defects or promote cancer malignancy. Vangl1 and Vangl2 are redundant core PCP components, and their protein levels are tightly controlled to maintain appropriate PCP signaling. Here, we identify two deubiquitinases, USP6 and USP32, that stabilize Vangl proteins through distinct ubiquitin linkage\u2010specific mechanisms. USP6 primarily removes K33\u2010linked and multi\u2010monoubiquitin signals from plasma membrane\u2010associated Vangl2, whereas USP32 removes K48\u2010linked ubiquitin chains from Golgi\/ER\u2010localized Vangl2, thereby regulating distinct subcellular pools of Vangl2. Given that\n                    <jats:italic>USP6<\/jats:italic>\n                    was previously reported to be a hominoid\u2010specific gene originating from\n                    <jats:italic>USP32<\/jats:italic>\n                    , our findings suggest evolutionary refinement in PCP regulation. Consistent with these biochemical functions, genetic interaction studies demonstrate that\n                    <jats:italic>Usp32<\/jats:italic>\n                    cooperates with\n                    <jats:italic>Vangl<\/jats:italic>\n                    genes to regulate PCP signaling during mouse embryogenesis. In pancreatic ductal adenocarcinoma, USP32 and VANGL1 are markedly upregulated and functionally promote cancer cell migration and metastasis. USP32 enhances metastatic behavior by stabilizing VANGL1 proteins. Together, our findings uncover a previously unrecognized regulatory mechanism of PCP signaling through USP6\/USP32\u2010mediated deubiquitination of Vangl proteins and highlight its roles in both developmental morphogenesis and cancer progression.\n                  <\/jats:p>","DOI":"10.1002\/advs.77496","type":"journal-article","created":{"date-parts":[[2026,8,31]],"date-time":"2026-08-31T02:03:36Z","timestamp":1788141816000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Deubiquitination of Vangl by USP6 and USP32 Regulates Planar Cell Polarity Signaling"],"prefix":"10.1002","author":[{"given":"Fangzi","family":"Zha","sequence":"first","affiliation":[{"name":"School of Biomedical Sciences Faculty of Medicine The Chinese University of Hong Kong  Hong Kong SAR China"},{"name":"Shenzhen Research Institute The Chinese University of Hong Kong  Shenzhen China"},{"name":"School of Biomedical Sciences Li Ka Shing Faculty of Medicine The University of Hong Kong  Hong Kong SAR China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1444-3510","authenticated-orcid":false,"given":"Di","family":"Feng","sequence":"additional","affiliation":[{"name":"School of Biomedical Sciences Faculty of Medicine The Chinese University of Hong Kong  Hong Kong SAR China"},{"name":"Shenzhen Research Institute The Chinese University of Hong Kong  Shenzhen China"},{"name":"School of Biomedical Sciences Li Ka Shing Faculty of Medicine The University of Hong Kong  Hong Kong SAR China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ziru","family":"Xue","sequence":"additional","affiliation":[{"name":"Shanghai Key Laboratory of Cancer Systems Regulation and Clinical Translation Shanghai Cancer Institute Renji Hospital School of Medicine Shanghai Jiao Tong University  Shanghai China"},{"name":"School of Health Science and Engineering University of Shanghai for Science and Technology  Shanghai China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhiying","family":"Liu","sequence":"additional","affiliation":[{"name":"School of Biomedical Sciences Faculty of Medicine The Chinese University of Hong Kong  Hong Kong SAR China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaochen","family":"Lin","sequence":"additional","affiliation":[{"name":"School of Biomedical Sciences Faculty of Medicine The Chinese University of Hong Kong  Hong Kong SAR China"},{"name":"School of Biomedical Sciences Li Ka Shing Faculty of Medicine The University of Hong Kong  Hong Kong SAR China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhe","family":"Wang","sequence":"additional","affiliation":[{"name":"School of Biomedical Sciences Faculty of Medicine The Chinese University of Hong Kong  Hong Kong SAR China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ling","family":"Xu","sequence":"additional","affiliation":[{"name":"School of Biomedical Sciences Li Ka Shing Faculty of Medicine The University of Hong Kong  Hong Kong SAR China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6336-6657","authenticated-orcid":false,"given":"Jasper Fuk Woo","family":"Chan","sequence":"additional","affiliation":[{"name":"Department of Microbiology School of Clinical Medicine Li Ka Shing Faculty of Medicine The University of Hong Kong  Hong Kong SAR China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3471-8534","authenticated-orcid":false,"given":"Martin","family":"Cheung","sequence":"additional","affiliation":[{"name":"School of Biomedical Sciences Li Ka Shing Faculty of Medicine The University of Hong Kong  Hong Kong SAR China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael Shing Yan","family":"Huen","sequence":"additional","affiliation":[{"name":"School of Biomedical Sciences Li Ka Shing Faculty of Medicine The University of Hong Kong  Hong Kong SAR China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5539-599X","authenticated-orcid":false,"given":"Yusong","family":"Guo","sequence":"additional","affiliation":[{"name":"Division of Life Science Hong Kong University of Science and Technology  Hong Kong SAR China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6430-3340","authenticated-orcid":false,"given":"Kui Ming","family":"Chan","sequence":"additional","affiliation":[{"name":"Department of Biomedical Sciences College of Biomedicine City University of Hong Kong  Hong Kong SAR China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yun","family":"Liu","sequence":"additional","affiliation":[{"name":"Shanghai Key Laboratory of Cancer Systems Regulation and Clinical Translation Shanghai Cancer Institute Renji Hospital School of Medicine Shanghai Jiao Tong University  Shanghai China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8684-5199","authenticated-orcid":false,"given":"Bo","family":"Gao","sequence":"additional","affiliation":[{"name":"School of Biomedical Sciences Faculty of Medicine The Chinese University of Hong Kong  Hong Kong SAR China"},{"name":"Shenzhen Research Institute The Chinese University of Hong Kong  Shenzhen China"},{"name":"Key Laboratory of Regenerative Medicine Ministry of Education School of Biomedical Sciences Faculty of Medicine The Chinese University of Hong Kong  Hong Kong SAR China"},{"name":"Kunming Institute of Zoology \u2013 The Chinese University of Hong Kong (KIZ\u2010CUHK) Joint Laboratory of Bioresources and Molecular Research of Common Diseases The Chinese University of Hong Kong  Hong Kong SAR China"},{"name":"Centre for Translational Stem Cell Biology  Hong Kong SAR China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,8,30]]},"reference":[{"issue":"4","key":"e_1_2_9_2_1","doi-asserted-by":"crossref","first-page":"647","DOI":"10.1242\/dev.02772","article-title":"Tissue\/Planar Cell Polarity in Vertebrates: New Insights and New Questions","volume":"134","author":"Wang Y.","year":"2007","journal-title":"Development"},{"issue":"1","key":"e_1_2_9_3_1","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1016\/j.devcel.2011.06.011","article-title":"Planar Cell Polarity: Coordinating Morphogenetic Cell Behaviors with Embryonic Polarity","volume":"21","author":"Gray R. 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M.","year":"2012","journal-title":"Molecular and Cellular Biology"},{"issue":"8","key":"e_1_2_9_23_1","doi-asserted-by":"crossref","first-page":"1693","DOI":"10.1242\/dev.089656","article-title":"A Cul\u20103\u2010BTB Ubiquitylation Pathway Regulates Junctional Levels and Asymmetry of Core Planar Polarity Proteins","volume":"140","author":"Strutt H.","year":"2013","journal-title":"Development"},{"issue":"1","key":"e_1_2_9_24_1","doi-asserted-by":"crossref","first-page":"4832","DOI":"10.1038\/ncomms5832","article-title":"The Ubiquitin Ligase PDZRN3 Is Required for Vascular Morphogenesis through Wnt\/Planar Cell Polarity Signalling","volume":"5","author":"Sewduth R. N.","year":"2014","journal-title":"Nature Communications"},{"issue":"5","key":"e_1_2_9_25_1","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pgen.1005259","article-title":"Clustering and Negative Feedback by Endocytosis in Planar Cell Polarity Signaling Is Modulated by Ubiquitinylation of Prickle","volume":"11","author":"Cho B.","year":"2015","journal-title":"PLOS Genetics"},{"issue":"2","key":"e_1_2_9_26_1","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1016\/j.celrep.2016.06.010","article-title":"Frizzled\u2010Induced Van Gogh Phosphorylation by CK1\u03b5 Promotes Asymmetric Localization of Core PCP Factors in Drosophila","volume":"16","author":"Kelly L. K.","year":"2016","journal-title":"Cell Reports"},{"issue":"36","key":"e_1_2_9_27_1","doi-asserted-by":"crossref","first-page":"5158","DOI":"10.1038\/onc.2017.126","article-title":"Suppression of Planar Cell Polarity Signaling and Migration in Glioblastoma by Nrdp1\u2010mediated Dvl Polyubiquitination","volume":"36","author":"Wald J. 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M.","year":"2023","journal-title":"Dis Model Mech"},{"issue":"29","key":"e_1_2_9_35_1","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.2400569121","article-title":"Stearoylation Cycle Regulates the Cell Surface Distribution of the PCP Protein Vangl2","volume":"121","author":"Ying J.","year":"2024","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"1","key":"e_1_2_9_36_1","doi-asserted-by":"crossref","first-page":"7219","DOI":"10.1038\/s41467-025-62400-x","article-title":"FGF Receptor Modulates Planar Cell Polarity in the Neuroectoderm via Vangl2 Tyrosine Phosphorylation","volume":"16","author":"Chuykin I.","year":"2025","journal-title":"Nature Communications"},{"issue":"8","key":"e_1_2_9_37_1","doi-asserted-by":"crossref","DOI":"10.1242\/dev.163824","article-title":"Coordinated Directional Outgrowth and Pattern Formation by Integration of Wnt5a and Fgf Signaling in Planar Cell Polarity","volume":"145","author":"Gao B.","year":"2018","journal-title":"Development"},{"issue":"20","key":"e_1_2_9_38_1","doi-asserted-by":"crossref","DOI":"10.21769\/BioProtoc.4533","article-title":"Analysis of the Ubiquitination and Phosphorylation of Vangl Proteins","volume":"12","author":"Feng D.","year":"2022","journal-title":"Bio Protoc"},{"key":"e_1_2_9_39_1","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.65759","article-title":"RNF43 inhibits WNT5A\u2010driven Signaling and Suppresses Melanoma Invasion and Resistance to the Targeted Therapy","volume":"10","author":"Radaszkiewicz T.","year":"2021","journal-title":"Elife"},{"issue":"8","key":"e_1_2_9_40_1","doi-asserted-by":"crossref","first-page":"550","DOI":"10.1038\/nrm2731","article-title":"Breaking the Chains: Structure and Function of the Deubiquitinases","volume":"10","author":"Komander D.","year":"2009","journal-title":"Nature Reviews Molecular Cell Biology"},{"issue":"1","key":"e_1_2_9_41_1","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1146\/annurev-biochem-061516-044916","article-title":"Mechanisms of Deubiquitinase Specificity and Regulation","volume":"86","author":"Mevissen T. 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