{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,14]],"date-time":"2026-07-14T22:59:37Z","timestamp":1784069977191,"version":"3.55.0"},"reference-count":67,"publisher":"Wiley","license":[{"start":{"date-parts":[[2024,10,25]],"date-time":"2024-10-25T00:00:00Z","timestamp":1729814400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/100007225","name":"Ministry of Science and Technology","doi-asserted-by":"publisher","award":["110\u20102320\u2010B\u2010038\u2010032\u2010MY3"],"award-info":[{"award-number":["110\u20102320\u2010B\u2010038\u2010032\u2010MY3"]}],"id":[{"id":"10.13039\/100007225","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007225","name":"Ministry of Science and Technology","doi-asserted-by":"publisher","award":["NSTC 113\u20102635\u2010B\u2010A49\u2010001"],"award-info":[{"award-number":["NSTC 113\u20102635\u2010B\u2010A49\u2010001"]}],"id":[{"id":"10.13039\/100007225","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007225","name":"Ministry of Science and Technology","doi-asserted-by":"publisher","award":["NSTC 113\u20102320\u2010B\u2010038\u2010066"],"award-info":[{"award-number":["NSTC 113\u20102320\u2010B\u2010038\u2010066"]}],"id":[{"id":"10.13039\/100007225","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Molecular Oral Microbiology"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Infection is a known cause of abdominal aortic aneurysm (AAA), and matrix metalloproteases\u20102 (MMP\u20102) secreted by vascular smooth muscle cells (SMCs) plays a key role in the structural disruption of the middle layer of the arteries during AAA progression. The periodontal pathogen <jats:italic>Porphyromonas gingivalis<\/jats:italic> is highly associated with the progression of periodontitis. GroEL protein of periodontal pathogens is an important virulence factor that can invade the body through either the bloodstream or digestive tract and is associated with numerous systemic diseases. Although <jats:italic>P. gingivalis<\/jats:italic> aggravates AAA by increasing the expression of MMP\u20102 in animal studies, the molecular mechanism through which <jats:italic>P. gingivalis<\/jats:italic> regulates the expression of MMP\u20102 is still unknown and requires further investigation.<\/jats:p><jats:p>In this study, we first confirmed through animal experiments that <jats:italic>P. gingivalis<\/jats:italic> GroEL promotes MMP\u20102 secretion from vascular SMCs, thereby aggravating Ang II\u2010induced aortic remodeling and AAA formation. In addition, rat vascular SMCs and A7r5 cells were used to investigate the underlying mechanisms in vitro. The results demonstrated that GroEL can promote the interaction between the K639 site of MMP\u20102 and SUMO\u20101, leading to MMP\u20102 SUMOylation, which inhibits the reoccurrence of non\u2013K639\u2010mediated monoubiquitylation. Hence, the monoubiquitylation\u2010mediated lysosomal degradation of MMP\u20102 is inhibited, consequently promoting MMP\u20102 stability and production. SUMOylation may facilitate intra\u2010endoplasmic reticulum (ER) and Golgi trafficking of MMP\u20102, thereby enhancing its transport capacity. In conclusion, this is the first report demonstrating the presence of a novel posttranslational modification, SUMOylation, in the MMP family, suggesting that <jats:italic>P. gingivalis<\/jats:italic> GroEL may exacerbate AAA formation by increasing MMP\u20102 production through SUMOylation in vascular SMCs. This study also provides a novel perspective on the role of SUMOylation in MMP\u20102\u2013induced systemic diseases.<\/jats:p>","DOI":"10.1111\/omi.12487","type":"journal-article","created":{"date-parts":[[2024,10,25]],"date-time":"2024-10-25T07:02:03Z","timestamp":1729839723000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["<i>Porphyromonas gingivalis<\/i> GroEL accelerates abdominal aortic aneurysm formation by matrix metalloproteinase\u20102 SUMOylation in vascular smooth muscle cells: A novel finding for the activation of MMP\u20102"],"prefix":"10.1111","author":[{"given":"Yi\u2010Wen","family":"Lin","sequence":"first","affiliation":[{"name":"Institute of Oral Biology National Yang Ming Chiao Tung University (Taipei Campus)  Taipei Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4939-2899","authenticated-orcid":false,"given":"Feng\u2010Yen","family":"Lin","sequence":"additional","affiliation":[{"name":"Taipei Heart Institute Taipei Medical University  Taipei Taiwan"},{"name":"Division of Cardiology and Cardiovascular Research Center Taipei Medical University Hospital  Taipei Taiwan"},{"name":"Division of Cardiology, Department of Internal Medicine, School of Medicine, College of Medicine Taipei Medical University  Taipei Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ze\u2010Hao","family":"Lai","sequence":"additional","affiliation":[{"name":"Institute of Oral Biology National Yang Ming Chiao Tung University (Taipei Campus)  Taipei Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chien\u2010Sung","family":"Tsai","sequence":"additional","affiliation":[{"name":"Division of Cardiovascular Surgery, National Defense Medical Center Tri\u2010Service General Hospital  Taipei Taiwan"},{"name":"Department and Graduate Institute of Pharmacology National Defense Medical Center  Taipei Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yi\u2010Ting","family":"Tsai","sequence":"additional","affiliation":[{"name":"Division of Cardiovascular Surgery, National Defense Medical Center Tri\u2010Service General Hospital  Taipei Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yen\u2010Sung","family":"Huang","sequence":"additional","affiliation":[{"name":"Institute of Biomedical Sciences Academia Sinica  Taipei Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chen\u2010Wei","family":"Liu","sequence":"additional","affiliation":[{"name":"Department of Basic Medical Science, College of Medicine University of Arizona  Phoenix Arizona USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2024,10,25]]},"reference":[{"key":"e_1_2_11_2_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1399\u2010302X.2006.00286.x"},{"key":"e_1_2_11_3_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1600-0765.2010.01326.x"},{"key":"e_1_2_11_4_1","doi-asserted-by":"publisher","DOI":"10.1534\/genetics.112.142810"},{"key":"e_1_2_11_5_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1600\u2010051X.2009.01382.x"},{"key":"e_1_2_11_6_1","doi-asserted-by":"publisher","DOI":"10.1042\/BJ20151154"},{"key":"e_1_2_11_7_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbamcr.2010.01.003"},{"key":"e_1_2_11_8_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.274.16.10846"},{"key":"e_1_2_11_9_1","doi-asserted-by":"publisher","DOI":"10.3390\/ijms21249739"},{"key":"e_1_2_11_10_1","doi-asserted-by":"publisher","DOI":"10.3390\/cells11203296"},{"key":"e_1_2_11_11_1","doi-asserted-by":"publisher","DOI":"10.1038\/sj.cdd.4401692"},{"key":"e_1_2_11_12_1","doi-asserted-by":"publisher","DOI":"10.1074\/mcp.M116.063719"},{"key":"e_1_2_11_13_1","doi-asserted-by":"publisher","DOI":"10.1242\/jcs.114.11.2167"},{"key":"e_1_2_11_14_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0018679"},{"key":"e_1_2_11_15_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1600\u20100854.2004.00206.x"},{"key":"e_1_2_11_16_1","doi-asserted-by":"publisher","DOI":"10.1002\/jcp.21535"},{"key":"e_1_2_11_17_1","doi-asserted-by":"publisher","DOI":"10.1002\/hep.24577"},{"key":"e_1_2_11_18_1","doi-asserted-by":"publisher","DOI":"10.1093\/emboj\/17.17.5238"},{"key":"e_1_2_11_19_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev\u2010biochem\u2010061909\u2010093311"},{"key":"e_1_2_11_20_1","doi-asserted-by":"publisher","DOI":"10.3390\/vaccines8040773"},{"key":"e_1_2_11_21_1","doi-asserted-by":"publisher","DOI":"10.1038\/nrm2293"},{"key":"e_1_2_11_22_1","doi-asserted-by":"publisher","DOI":"10.1152\/physrev.00027.2001"},{"key":"e_1_2_11_23_1","doi-asserted-by":"publisher","DOI":"10.1042\/BST0351414"},{"key":"e_1_2_11_24_1","doi-asserted-by":"publisher","DOI":"10.1002\/iub.1244"},{"key":"e_1_2_11_25_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00018\u2010007\u20106413\u20107"},{"key":"e_1_2_11_26_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.tibs.2003.09.005"},{"key":"e_1_2_11_27_1","first-page":"5323","article-title":"Evidence for the involvement of MMP14 in MMP2 processing and recruitment in exosomes of corneal fibroblasts","volume":"56","author":"Han K. Y.","year":"2015","journal-title":"Investigative Ophthalmology, & Visual Science"},{"key":"e_1_2_11_28_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.molcel.2005.03.012"},{"key":"e_1_2_11_29_1","doi-asserted-by":"publisher","DOI":"10.1152\/physrev.00008.2014"},{"key":"e_1_2_11_30_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0962\u20108924(98)01491\u20103"},{"key":"e_1_2_11_31_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.cellbio.19.110701.154617"},{"key":"e_1_2_11_32_1","first-page":"384","article-title":"The GroEL protein of Porphyromonas gingivalis regulates atherogenic phenomena in endothelial cells mediated by upregulating toll\u2010like receptor 4 expression","volume":"8","author":"Huang C. Y.","year":"2016","journal-title":"American journal of translational research"},{"key":"e_1_2_11_33_1","doi-asserted-by":"publisher","DOI":"10.1016\/S1065\u20106995(03)00167\u20107"},{"key":"e_1_2_11_34_1","doi-asserted-by":"publisher","DOI":"10.1046\/j.1432\u20101033.2002.03317.x"},{"key":"e_1_2_11_35_1","doi-asserted-by":"publisher","DOI":"10.3109\/14756366.2016.1161620"},{"key":"e_1_2_11_36_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0071794"},{"key":"e_1_2_11_37_1","doi-asserted-by":"publisher","DOI":"10.1038\/s12276\u2010019\u20100286\u20103"},{"key":"e_1_2_11_38_1","doi-asserted-by":"publisher","DOI":"10.1161\/ATVBAHA.112.300432"},{"key":"e_1_2_11_39_1","doi-asserted-by":"publisher","DOI":"10.1242\/jcs.052761"},{"key":"e_1_2_11_40_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00018\u2010012\u20101214\u2010z"},{"key":"e_1_2_11_41_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbadis.2017.01.018"},{"key":"e_1_2_11_42_1","doi-asserted-by":"publisher","DOI":"10.18632\/oncotarget.10494"},{"key":"e_1_2_11_43_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0102450"},{"key":"e_1_2_11_44_1","doi-asserted-by":"publisher","DOI":"10.1111\/omi.12083"},{"key":"e_1_2_11_45_1","doi-asserted-by":"publisher","DOI":"10.3389\/fcvm.2023.1199804"},{"key":"e_1_2_11_46_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ejvs.2016.07.004"},{"key":"e_1_2_11_47_1","doi-asserted-by":"publisher","DOI":"10.3390\/ijms20123077"},{"key":"e_1_2_11_48_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00418\u2010018\u20101689\u20102"},{"key":"e_1_2_11_49_1","doi-asserted-by":"publisher","DOI":"10.1093\/cvr\/cvp155"},{"key":"e_1_2_11_50_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cardiores.2005.12.002"},{"key":"e_1_2_11_51_1","doi-asserted-by":"publisher","DOI":"10.1177\/1747493019834191"},{"key":"e_1_2_11_52_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbrc.2005.09.090"},{"key":"e_1_2_11_53_1","doi-asserted-by":"publisher","DOI":"10.1189\/jlb.1006629"},{"key":"e_1_2_11_54_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41467\u2010021\u201025033\u20104"},{"key":"e_1_2_11_55_1","doi-asserted-by":"publisher","DOI":"10.1177\/0003319718821243"},{"key":"e_1_2_11_56_1","doi-asserted-by":"publisher","DOI":"10.1096\/fj.06\u20107938com"},{"key":"e_1_2_11_57_1","doi-asserted-by":"publisher","DOI":"10.1002\/elps.201900100"},{"key":"e_1_2_11_58_1","doi-asserted-by":"publisher","DOI":"10.1093\/jxb\/ery295"},{"key":"e_1_2_11_59_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41368\u2010019\u20100054\u20101"},{"key":"e_1_2_11_60_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.X800009200"},{"key":"e_1_2_11_61_1","doi-asserted-by":"publisher","DOI":"10.1042\/BST0380046"},{"key":"e_1_2_11_62_1","doi-asserted-by":"publisher","DOI":"10.1067\/mva.2001.116966"},{"key":"e_1_2_11_63_1","doi-asserted-by":"publisher","DOI":"10.4049\/jimmunol.0803164"},{"key":"e_1_2_11_64_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.matbio.2015.02.007"},{"key":"e_1_2_11_65_1","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2020.609161"},{"key":"e_1_2_11_66_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.mi.45.100191.001505"},{"key":"e_1_2_11_67_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41392\u2010022\u201000966\u20104"},{"key":"e_1_2_11_68_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.canlet.2012.10.026"}],"container-title":["Molecular Oral Microbiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/omi.12487","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,10,25]],"date-time":"2024-10-25T07:02:09Z","timestamp":1729839729000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/omi.12487"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,10,25]]},"references-count":67,"alternative-id":["10.1111\/omi.12487"],"URL":"https:\/\/doi.org\/10.1111\/omi.12487","archive":["Portico"],"relation":{},"ISSN":["2041-1006","2041-1014"],"issn-type":[{"value":"2041-1006","type":"print"},{"value":"2041-1014","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,10,25]]},"assertion":[{"value":"2024-08-12","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2024-09-26","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2024-10-25","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"omi.12487"}}