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One characteristic feature of all SUMO proteins is the presence of a highly divergent intrinsically disordered region at their N-terminus. In this study, we examine the role of this N-terminal region of SUMO proteins in SUMO\u2013SIM interactions required for the formation of nuclear bodies by the promyelocytic leukemia (PML) protein (PML-NBs). We demonstrate that the N-terminal region of SUMO1 functions in a paralog specific manner as an auto-inhibition domain by blocking its binding to the phosphorylated SIMs of PML and Daxx. Interestingly, we find that this auto-inhibition in SUMO1 is relieved by zinc, and structurally show that zinc stabilizes the complex between SUMO1 and a phospho-mimetic form of the SIM of PML. In addition, we demonstrate that increasing cellular zinc levels enhances PML-NB formation in senescent cells. Taken together, these results provide important insights into a paralog specific function of SUMO1, and suggest that zinc levels could play a crucial role in regulating SUMO1-SIM interactions required for PML-NB formation and function.<\/jats:p>","DOI":"10.1093\/nar\/gkac620","type":"journal-article","created":{"date-parts":[[2022,7,24]],"date-time":"2022-07-24T09:19:30Z","timestamp":1658654370000},"page":"8331-8348","source":"Crossref","is-referenced-by-count":18,"title":["Zinc controls PML nuclear body formation through regulation of a paralog specific auto-inhibition in SUMO1"],"prefix":"10.1093","volume":"50","author":[{"given":"Mathieu","family":"Lussier-Price","sequence":"first","affiliation":[{"name":"D\u00e9partement de Biochimie et M\u00e9dicine Mol\u00e9culaire, Universit\u00e9 de Montr\u00e9al , Montr\u00e9al, QC, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haytham M","family":"Wahba","sequence":"additional","affiliation":[{"name":"D\u00e9partement de Biochimie et M\u00e9dicine Mol\u00e9culaire, Universit\u00e9 de Montr\u00e9al , Montr\u00e9al, QC, Canada"},{"name":"Department of Biochemistry, Beni-Suef University , Beni-Suef, Egypt"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xavier H","family":"Mascle","sequence":"additional","affiliation":[{"name":"D\u00e9partement de Biochimie et M\u00e9dicine Mol\u00e9culaire, Universit\u00e9 de Montr\u00e9al , Montr\u00e9al, QC, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laurent","family":"Cappadocia","sequence":"additional","affiliation":[{"name":"D\u00e9partement de Biochimie et M\u00e9dicine Mol\u00e9culaire, Universit\u00e9 de Montr\u00e9al , Montr\u00e9al, QC, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Veronique","family":"Bourdeau","sequence":"additional","affiliation":[{"name":"D\u00e9partement de Biochimie et M\u00e9dicine Mol\u00e9culaire, Universit\u00e9 de Montr\u00e9al , Montr\u00e9al, QC, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christina","family":"Gagnon","sequence":"additional","affiliation":[{"name":"D\u00e9partement de Biochimie et M\u00e9dicine Mol\u00e9culaire, Universit\u00e9 de Montr\u00e9al , Montr\u00e9al, QC, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sebastian","family":"Igelmann","sequence":"additional","affiliation":[{"name":"D\u00e9partement de Biochimie et M\u00e9dicine Mol\u00e9culaire, Universit\u00e9 de Montr\u00e9al , Montr\u00e9al, QC, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8434-4171","authenticated-orcid":false,"given":"Kazuyasu","family":"Sakaguchi","sequence":"additional","affiliation":[{"name":"Department of Chemistry, Faculty of Science, Hokkaido University , Sapporo, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2146-618X","authenticated-orcid":false,"given":"Gerardo","family":"Ferbeyre","sequence":"additional","affiliation":[{"name":"D\u00e9partement de Biochimie et M\u00e9dicine Mol\u00e9culaire, Universit\u00e9 de Montr\u00e9al , Montr\u00e9al, QC, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3543-1914","authenticated-orcid":false,"given":"James\u00a0G","family":"Omichinski","sequence":"additional","affiliation":[{"name":"D\u00e9partement de Biochimie et M\u00e9dicine Mol\u00e9culaire, Universit\u00e9 de Montr\u00e9al , Montr\u00e9al, QC, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2022,7,25]]},"reference":[{"key":"2022081200022102000_B1","doi-asserted-by":"crossref","first-page":"550","DOI":"10.1038\/sj.embor.7400980","article-title":"SUMO junction-what's your function? 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Commun."},{"key":"2022081200022102000_B66","doi-asserted-by":"crossref","first-page":"6183","DOI":"10.1128\/MCB.22.17.6183-6198.2002","article-title":"Gamma interferon and cadmium treatments modulate eukaryotic initiation factor 4E-dependent mRNA transport of cyclin D1 in a PML-dependent manner","volume":"22","author":"Topisirovic","year":"2002","journal-title":"Mol. Cell. Biol."},{"key":"2022081200022102000_B67","first-page":"365","article-title":"PML isoforms in response to arsenic: high-resolution analysis of PML body structure and degradation","volume":"127","author":"Hands","year":"2014","journal-title":"J. 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Biochem."},{"key":"2022081200022102000_B73","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1083\/jcb.130.1.1","article-title":"Molecular characterization of NDP52, a novel protein of the nuclear domain 10, which is redistributed upon virus infection and interferon treatment","volume":"130","author":"Korioth","year":"1995","journal-title":"J. Cell Biol."},{"key":"2022081200022102000_B74","doi-asserted-by":"crossref","first-page":"1419","DOI":"10.1039\/c9mt00102f","article-title":"Integrity of zinc finger motifs in PML protein is necessary for inducing its degradation by antimony","volume":"11","author":"Yang","year":"2019","journal-title":"Metallomics"},{"key":"2022081200022102000_B75","doi-asserted-by":"crossref","first-page":"4308","DOI":"10.1182\/blood.V92.11.4308","article-title":"Trivalent antimonials induce degradation of the PML-RAR oncoprotein and reorganization of the promyelocytic leukemia nuclear bodies in acute promyelocytic leukemia NB4 cells","volume":"92","author":"M\u00fcller","year":"1998","journal-title":"Blood"},{"key":"2022081200022102000_B76","doi-asserted-by":"crossref","first-page":"651","DOI":"10.1016\/j.cell.2016.06.010","article-title":"Compositional control of phase-separated cellular bodies","volume":"166","author":"Banani","year":"2016","journal-title":"Cell"},{"key":"2022081200022102000_B77","doi-asserted-by":"crossref","first-page":"2878","DOI":"10.1039\/C3DT52810C","article-title":"Structural and computational insights into the versatility of cadmium binding to proteins","volume":"43","author":"Friedman","year":"2014","journal-title":"Dalton Trans."},{"key":"2022081200022102000_B78","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0300-483X(80)90107-9","article-title":"The interaction of cadmium and certain other metal ions with proteins and nucleic acids","volume":"16","author":"Jacobson","year":"1980","journal-title":"Toxicology"},{"key":"2022081200022102000_B79","doi-asserted-by":"crossref","first-page":"7769","DOI":"10.1021\/cr300015c","article-title":"Arsenic binding to proteins","volume":"113","author":"Shen","year":"2013","journal-title":"Chem. Rev."},{"key":"2022081200022102000_B80","doi-asserted-by":"crossref","first-page":"873","DOI":"10.1021\/tx034053g","article-title":"Interaction of trivalent arsenicals with metallothionein","volume":"16","author":"Jiang","year":"2003","journal-title":"Chem. Res. Toxicol."},{"key":"2022081200022102000_B81","doi-asserted-by":"crossref","first-page":"3173","DOI":"10.1021\/pr0603699","article-title":"Zinc through the three domains of life","volume":"5","author":"Andreini","year":"2006","journal-title":"J. Proteome Res."},{"key":"2022081200022102000_B82","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1093\/annonc\/mdj019","article-title":"Treatment of acute promyelocytic leukemia with arsenic trioxide without ATRA and\/or chemotherapy","volume":"17","author":"Ghavamzadeh","year":"2006","journal-title":"Ann. Oncol."},{"key":"2022081200022102000_B83","doi-asserted-by":"crossref","first-page":"1333","DOI":"10.1038\/nm.1891","article-title":"Eradication of acute promyelocytic leukemia-initiating cells through PML-RARA degradation","volume":"14","author":"Nasr","year":"2008","journal-title":"Nat. Med."},{"key":"2022081200022102000_B84","doi-asserted-by":"crossref","first-page":"2627","DOI":"10.1182\/blood-2005-08-3532","article-title":"Single-agent arsenic trioxide in the treatment of newly diagnosed acute promyelocytic leukemia: durable remissions with minimal toxicity","volume":"107","author":"Mathews","year":"2006","journal-title":"Blood"},{"key":"2022081200022102000_B85","doi-asserted-by":"crossref","first-page":"1564","DOI":"10.1039\/C8MT00202A","article-title":"Arsenic trioxide preferentially binds to the ring finger protein PML: understanding target selection of the drug","volume":"10","author":"Kaiming","year":"2018","journal-title":"Metallomics"},{"key":"2022081200022102000_B86","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1016\/j.ccr.2010.06.003","article-title":"PML\/RARA oxidation and arsenic binding initiate the antileukemia response of As2O3","volume":"18","author":"Jeanne","year":"2010","journal-title":"Cancer Cell"},{"key":"2022081200022102000_B87","doi-asserted-by":"crossref","first-page":"4227","DOI":"10.1091\/mbc.e10-05-0449","article-title":"Arsenic-induced SUMO-dependent recruitment of RNF4 into PML nuclear bodies","volume":"21","author":"Geoffroy","year":"2010","journal-title":"Mol. Biol. Cell"},{"key":"2022081200022102000_B88","doi-asserted-by":"crossref","first-page":"16595","DOI":"10.1074\/jbc.M109.006387","article-title":"Role of SUMO in RNF4-mediated promyelocytic leukemia protein (PML) degradation: sumoylation of PML and phospho-switch control of its SUMO binding domain dissected in living cells","volume":"284","author":"Percherancier","year":"2009","journal-title":"J. Biol. Chem."},{"key":"2022081200022102000_B89","doi-asserted-by":"crossref","first-page":"4455","DOI":"10.1242\/jcs.00758","article-title":"Size, position and dynamic behavior of PML nuclear bodies following cell stress as a paradigm for supramolecular trafficking and assembly","volume":"116","author":"Eskiw","year":"2003","journal-title":"J. Cell Sci."},{"key":"2022081200022102000_B90","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1242\/jcs.00253","article-title":"Heat shock and Cd2+ exposure regulate PML and Daxx release from ND10 by independent mechanisms that modify the induction of heat-shock proteins 70 and 25 differently","volume":"116","author":"Nefkens","year":"2003","journal-title":"J. Cell Sci."},{"key":"2022081200022102000_B91","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1083\/jcb.200511045","article-title":"PML clastosomes prevent nuclear accumulation of mutant ataxin-7 and other polyglutamine proteins","volume":"174","author":"Janer","year":"2006","journal-title":"J. Cell Biol."},{"key":"2022081200022102000_B92","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1021\/acs.chemrestox.6b00328","article-title":"Reactions of the Zn proteome with Cd(2+) and other xenobiotics: trafficking and toxicity","volume":"30","author":"Petering","year":"2017","journal-title":"Chem. Res. Toxicol."},{"key":"2022081200022102000_B93","doi-asserted-by":"crossref","first-page":"499","DOI":"10.4161\/19491034.2014.970104","article-title":"PML nuclear bodies: assembly and oxidative stress-sensitive sumoylation","volume":"5","author":"Sahin","year":"2014","journal-title":"Nucleus"},{"key":"2022081200022102000_B94","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1083\/jcb.201305148","article-title":"Oxidative stress-induced assembly of PML nuclear bodies controls sumoylation of partner proteins","volume":"204","author":"Sahin","year":"2014","journal-title":"J. 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