{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,23]],"date-time":"2026-08-23T14:00:01Z","timestamp":1787493601525,"version":"build-2736575974"},"reference-count":76,"publisher":"The Company of Biologists","issue":"8","license":[{"start":{"date-parts":[[2026,8,7]],"date-time":"2026-08-07T00:00:00Z","timestamp":1786060800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"crossref","award":["RGPIN-2020-07205"],"award-info":[{"award-number":["RGPIN-2020-07205"]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100000024","name":"Canadian Institutes of Health Research","doi-asserted-by":"crossref","award":["MOP 136802"],"award-info":[{"award-number":["MOP 136802"]}],"id":[{"id":"10.13039\/501100000024","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100000196","name":"Canada Foundation for Innovation","doi-asserted-by":"crossref","award":["30017"],"award-info":[{"award-number":["30017"]}],"id":[{"id":"10.13039\/501100000196","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100008985","name":"Diab\u00e8te Qu\u00e9bec","doi-asserted-by":"crossref","id":[{"id":"10.13039\/100008985","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100005242","name":"Universit\u00e9 de Montr\u00e9al","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100005242","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2026,8,15]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>E3 ubiquitin ligases include hundreds of members that can regulate the half-life of other proteins but also modulate their cellular localization and functions. While MARCH1 appears to target principally immune cell components, such as MHC class II molecules and the co-stimulatory molecule CD86, the repertory of its targets remains to be fully documented. Here, we adapted a proximity-dependent biotin identification (BioID)-based screening approach in live HEK293 cells. We transfected a fusion protein consisting of mouse MARCH1 linked to YFP at its N-terminus and to the biotin ligase of Aquifex aeolicus at its C-terminus. Upon transient overexpression in the presence of biotin, we could recover biotinylated proteins that are presumably found within 10\u2005nm of MARCH1. CD98 and CD71, two previously described targets of MARCH1, were identified. Of 16 other biotinylated proteins identified by semi-quantitative mass spectrometry, ten were tested directly by flow cytometry to monitor their expression in the presence or absence of transfected MARCH1. SNAT2 was particularly sensitive to the presence of MARCH1 and was found to be ubiquitinated on western blots. Thus, BioID2 is an effective mean of characterizing the interactome of MARCH1, and the identification of SNAT2 suggests a role of this ubiquitin ligase in cellular metabolism.<\/jats:p>","DOI":"10.1242\/bio.061700","type":"journal-article","created":{"date-parts":[[2026,7,20]],"date-time":"2026-07-20T08:33:30Z","timestamp":1784536410000},"source":"Crossref","is-referenced-by-count":1,"title":["A proximity ligation screen identifies SNAT2 as a novel target of the MARCH1 E3 ubiquitin ligase"],"prefix":"10.1242","volume":"15","author":[{"given":"Renaud","family":"Balthazard","sequence":"first","affiliation":[{"name":"Universit\u00e9 de Montr\u00e9al 1 Laboratoire d'immunologie mol\u00e9culaire , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]},{"name":"Universit\u00e9 de Montr\u00e9al 2 D\u00e9partement de microbiologie, infectiologie et immunologie , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]},{"name":"Institut Courtois d'innovation biom\u00e9dicale (CI2B) 3 , Facult\u00e9 de m\u00e9decine , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]},{"name":"Universit\u00e9 de Montr\u00e9al 3 , Facult\u00e9 de m\u00e9decine , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0004-2687-6905","authenticated-orcid":false,"given":"William","family":"Mitchell","sequence":"additional","affiliation":[{"name":"Universit\u00e9 de Montr\u00e9al 1 Laboratoire d'immunologie mol\u00e9culaire , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]},{"name":"Universit\u00e9 de Montr\u00e9al 2 D\u00e9partement de microbiologie, infectiologie et immunologie , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]},{"name":"Institut Courtois d'innovation biom\u00e9dicale (CI2B) 3 , Facult\u00e9 de m\u00e9decine , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]},{"name":"Universit\u00e9 de Montr\u00e9al 3 , Facult\u00e9 de m\u00e9decine , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maxime","family":"Raymond","sequence":"additional","affiliation":[{"name":"Universit\u00e9 de Montr\u00e9al 1 Laboratoire d'immunologie mol\u00e9culaire , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]},{"name":"Universit\u00e9 de Montr\u00e9al 2 D\u00e9partement de microbiologie, infectiologie et immunologie , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]},{"name":"Institut Courtois d'innovation biom\u00e9dicale (CI2B) 3 , Facult\u00e9 de m\u00e9decine , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]},{"name":"Universit\u00e9 de Montr\u00e9al 3 , Facult\u00e9 de m\u00e9decine , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Arnau","family":"Ballestero Vidal","sequence":"additional","affiliation":[{"name":"Universit\u00e9 de Montr\u00e9al 1 Laboratoire d'immunologie mol\u00e9culaire , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]},{"name":"Universit\u00e9 de Montr\u00e9al 2 D\u00e9partement de microbiologie, infectiologie et immunologie , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]},{"name":"Institut Courtois d'innovation biom\u00e9dicale (CI2B) 3 , Facult\u00e9 de m\u00e9decine , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]},{"name":"Universit\u00e9 de Montr\u00e9al 3 , Facult\u00e9 de m\u00e9decine , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dominic G.","family":"Roy","sequence":"additional","affiliation":[{"name":"Universit\u00e9 de Montr\u00e9al 2 D\u00e9partement de microbiologie, infectiologie et immunologie , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]},{"name":"Centre de recherche du Centre hospitalier de l'Universit\u00e9 de Montr\u00e9al (CR-CHUM) 4 , Montr\u00e9al H2X 0A9 ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Libia Cecilia","family":"Palma Zambrano","sequence":"additional","affiliation":[{"name":"Universit\u00e9 de Montr\u00e9al 1 Laboratoire d'immunologie mol\u00e9culaire , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]},{"name":"Universit\u00e9 de Montr\u00e9al 2 D\u00e9partement de microbiologie, infectiologie et immunologie , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]},{"name":"Institut Courtois d'innovation biom\u00e9dicale (CI2B) 3 , Facult\u00e9 de m\u00e9decine , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]},{"name":"Universit\u00e9 de Montr\u00e9al 3 , Facult\u00e9 de m\u00e9decine , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mohamed Abdelwafi","family":"Moulefera","sequence":"additional","affiliation":[{"name":"Universit\u00e9 de Montr\u00e9al 1 Laboratoire d'immunologie mol\u00e9culaire , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]},{"name":"Universit\u00e9 de Montr\u00e9al 2 D\u00e9partement de microbiologie, infectiologie et immunologie , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]},{"name":"Institut Courtois d'innovation biom\u00e9dicale (CI2B) 3 , Facult\u00e9 de m\u00e9decine , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]},{"name":"Universit\u00e9 de Montr\u00e9al 3 , Facult\u00e9 de m\u00e9decine , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Denis","family":"Faubert","sequence":"additional","affiliation":[{"name":"Institut de recherches cliniques de Montr\u00e9al 5 , Montr\u00e9al H2W 1R7 ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sarah","family":"Pasquin","sequence":"additional","affiliation":[{"name":"Institut Courtois d'innovation biom\u00e9dicale (CI2B) 3 , Facult\u00e9 de m\u00e9decine , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]},{"name":"Universit\u00e9 de Montr\u00e9al 3 , Facult\u00e9 de m\u00e9decine , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]},{"name":"Universit\u00e9 de Montr\u00e9al 6 D\u00e9partement de pharmacologie et physiologie , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jean-Fran\u00e7ois","family":"Gauchat","sequence":"additional","affiliation":[{"name":"Institut Courtois d'innovation biom\u00e9dicale (CI2B) 3 , Facult\u00e9 de m\u00e9decine , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]},{"name":"Universit\u00e9 de Montr\u00e9al 3 , Facult\u00e9 de m\u00e9decine , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]},{"name":"Universit\u00e9 de Montr\u00e9al 6 D\u00e9partement de pharmacologie et physiologie , , Montr\u00e9al H3T 1J4 ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0790-9634","authenticated-orcid":false,"given":"Jacques","family":"Thibodeau","sequence":"additional","affiliation":[{"name":"Universit\u00e9 de Montr\u00e9al 1 Laboratoire d'immunologie mol\u00e9culaire , , Montr\u00e9al H3T 1J4 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Cell Sci."},{"key":"2026080705062026600_BIO061700C2","doi-asserted-by":"publisher","first-page":"539","DOI":"10.1111\/j.1471-4159.2009.05979.x","article-title":"An IRBIT homologue lacks binding activity to inositol 1,4,5-trisphosphate receptor due to the unique N-terminal appendage","volume":"109","author":"Ando","year":"2009","journal-title":"J. Neurochem."},{"key":"2026080705062026600_BIO061700C3","doi-asserted-by":"publisher","first-page":"102325","DOI":"10.1016\/j.coi.2023.102325","article-title":"Regulation of MHC class II and CD86 expression by March-I in immunity and disease","volume":"82","author":"Bandola-Simon","year":"2023","journal-title":"Curr. Opin. Immunol."},{"key":"2026080705062026600_BIO061700C4","doi-asserted-by":"publisher","first-page":"993","DOI":"10.1084\/jem.20151682","article-title":"Ubiquitin-mediated fluctuations in MHC class II facilitate efficient germinal center B cell responses","volume":"213","author":"Bannard","year":"2016","journal-title":"J. Exp. Med."},{"key":"2026080705062026600_BIO061700C5","doi-asserted-by":"publisher","first-page":"2966","DOI":"10.4049\/jimmunol.1101643","article-title":"Ubiquitination of CD86 is a key mechanism in regulating antigen presentation by dendritic cells","volume":"187","author":"Baravalle","year":"2011","journal-title":"J. Immunol."},{"key":"2026080705062026600_BIO061700C6","doi-asserted-by":"publisher","first-page":"1009","DOI":"10.1016\/j.celrep.2017.10.002","article-title":"Dendritic cell amiloride-sensitive channels mediate sodium-induced inflammation and hypertension","volume":"21","author":"Barbaro","year":"2017","journal-title":"Cell Rep."},{"key":"2026080705062026600_BIO061700C7","doi-asserted-by":"publisher","first-page":"7656","DOI":"10.1038\/s41467-023-43326-8","article-title":"BioE3 identifies specific substrates of ubiquitin E3 ligases","volume":"14","author":"Barroso-Gomila","year":"2023","journal-title":"Nat. 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Virol."},{"key":"2026080705062026600_BIO061700C9","doi-asserted-by":"publisher","first-page":"e107","DOI":"10.1371\/journal.ppat.0020107","article-title":"Quantitative membrane proteomics reveals new cellular targets of viral immune modulators","volume":"2","author":"Bartee","year":"2006","journal-title":"PLoS Pathog."},{"key":"2026080705062026600_BIO061700C10","doi-asserted-by":"publisher","first-page":"e15132","DOI":"10.1371\/journal.pone.0015132","article-title":"Membrane-Associated RING-CH proteins associate with Bap31 and target CD81 and CD44 to lysosomes","volume":"5","author":"Bartee","year":"2010","journal-title":"PLoS ONE"},{"key":"2026080705062026600_BIO061700C11","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1016\/j.nbt.2016.12.002","article-title":"Overview of the membrane-associated RING-CH (MARCH) E3 ligase family","volume":"38","author":"Bauer","year":"2017","journal-title":"N. Biotechnol."},{"key":"2026080705062026600_BIO061700C12","doi-asserted-by":"publisher","first-page":"4959","DOI":"10.4049\/jimmunol.1102708","article-title":"Autoregulation of MARCH1 expression by dimerization and autoubiquitination","volume":"188","author":"Bourgeois-Daigneault","year":"2012","journal-title":"J. Immunol."},{"key":"2026080705062026600_BIO061700C13","doi-asserted-by":"publisher","first-page":"880","DOI":"10.1038\/nbt.4201","article-title":"Efficient proximity labeling in living cells and organisms with TurboID","volume":"36","author":"Branon","year":"2018","journal-title":"Nat. Biotechnol."},{"key":"2026080705062026600_BIO061700C14","doi-asserted-by":"publisher","first-page":"1719","DOI":"10.1074\/mcp.M800410-MCP200","article-title":"A label-free quantitative proteomics strategy to identify E3 ubiquitin ligase substrates targeted to proteasome degradation","volume":"8","author":"Burande","year":"2009","journal-title":"Mol. Cell. 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Cell"},{"key":"2026080705062026600_BIO061700C27","doi-asserted-by":"publisher","first-page":"2798","DOI":"10.1242\/jcs.119909","article-title":"Membrane-associated RING-CH (MARCH) 8 mediates the ubiquitination and lysosomal degradation of the transferrin receptor","volume":"126","author":"Fujita","year":"2013","journal-title":"J. Cell Sci."},{"key":"2026080705062026600_BIO061700C28","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1016\/j.cyto.2012.03.015","article-title":"MARCH1 down-regulation in IL-10-activated B cells increases MHC class II expression","volume":"59","author":"Galbas","year":"2012","journal-title":"Cytokine"},{"key":"2026080705062026600_BIO061700C29","doi-asserted-by":"publisher","first-page":"1518","DOI":"10.1111\/j.1600-0854.2009.00948.x","article-title":"Sorting of MHC class II molecules into exosomes through a ubiquitin-independent pathway","volume":"10","author":"Gauvreau","year":"2009","journal-title":"Traffic"},{"key":"2026080705062026600_BIO061700C30","doi-asserted-by":"publisher","first-page":"200","DOI":"10.1038\/s41586-023-06299-8","article-title":"SLC38A2 and glutamine signalling in cDC1s dictate anti-tumour immunity","volume":"620","author":"Guo","year":"2023","journal-title":"Nature"},{"key":"2026080705062026600_BIO061700C31","doi-asserted-by":"publisher","first-page":"424","DOI":"10.3390\/cells13050424","article-title":"CD112 supports lymphatic migration of human dermal dendritic cells","volume":"13","author":"Haghayegh Jahromi","year":"2024","journal-title":"Cells"},{"key":"2026080705062026600_BIO061700C32","doi-asserted-by":"publisher","first-page":"135","DOI":"10.33160\/yam.2020.08.001","article-title":"Regulatory mechanism of SNAP23 in phagosome formation and maturation","volume":"63","author":"Hatsuzawa","year":"2020","journal-title":"Yonago Acta Med."},{"key":"2026080705062026600_BIO061700C33","doi-asserted-by":"publisher","first-page":"425","DOI":"10.1146\/annurev.biochem.67.1.425","article-title":"The ubiquitin system","volume":"67","author":"Hershko","year":"1998","journal-title":"Annu. 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