{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,19]],"date-time":"2026-10-19T22:24:41Z","timestamp":1792448681855,"version":"4.5.0"},"reference-count":103,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,2,23]],"date-time":"2023-02-23T00:00:00Z","timestamp":1677110400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Immunol."],"abstract":"<jats:p>Ubiquitin-mediated proteasomal degradation is a post-transcriptional protein modification that is comprised of various components including the 76-amino acid protein ubiquitin (Ub), Ub-activating enzyme (E1), Ub-conjugating enzyme (E2), ubiquitin ligase (E3), deubiquitinating enzyme (DUB) and proteasome. We and others have recently provided genetic evidence showing that E3-ubiquitin ligases are associated with bone metabolism, the immune system and inflammation through ubiquitylation and subsequent degradation of their substrates. Dysregulation of the E3-ubiquitin ligase RNF146-mediated degradation of the adaptor protein 3BP2 (SH3 domain-binding protein 2) causes cherubism, an autosomal dominant disorder associated with severe inflammatory craniofacial dysmorphia syndrome in children. In this review, on the basis of our discoveries in cherubism, we summarize new insights into the roles of E3-ubiquitin ligases in the development of human disorders caused by an abnormal osteoimmune system by highlighting recent genetic evidence obtained in both human and animal model studies.<\/jats:p>","DOI":"10.3389\/fimmu.2023.1120710","type":"journal-article","created":{"date-parts":[[2023,2,23]],"date-time":"2023-02-23T12:34:11Z","timestamp":1677155651000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":16,"title":["E3-ubiquitin ligases and recent progress in osteoimmunology"],"prefix":"10.3389","volume":"14","author":[{"given":"Yosuke","family":"Asano","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yoshinori","family":"Matsumoto","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jun","family":"Wada","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robert","family":"Rottapel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,2,23]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"6948367","DOI":"10.1155\/2022\/6948367","article-title":"E3 ubiquitin ligases: Potential therapeutic targets for skeletal pathology and degeneration","volume":"2022","author":"Zeng","year":"2022","journal-title":"Stem Cells Int"},{"key":"B2","doi-asserted-by":"publisher","first-page":"10569","DOI":"10.3390\/ijms231810569","article-title":"Death of a protein: The role of E3 ubiquitin ligases in circadian rhythms of mice and flies","volume":"23","author":"Abdalla","year":"2022","journal-title":"Int J Mol Sci"},{"key":"B3","doi-asserted-by":"publisher","DOI":"10.1016\/j.tcb.2013.12.003","article-title":"Perilous journey: A tour of the ubiquitin-proteasome system","volume":"24","author":"Kleiger","year":"2014","journal-title":"Trends Cell Biol"},{"key":"B4","doi-asserted-by":"publisher","DOI":"10.1038\/ncb3358","article-title":"The increasing complexity of the ubiquitin code","volume":"18","author":"Yau","year":"2016","journal-title":"Nat Cell Biol"},{"key":"B5","doi-asserted-by":"publisher","first-page":"3712083","DOI":"10.1155\/2018\/3712083","article-title":"Deubiquitinating enzymes and bone remodeling","volume":"2018","author":"Guo","year":"2018","journal-title":"Stem Cells Int"},{"key":"B6","doi-asserted-by":"publisher","DOI":"10.1080\/13543776.2018.1549229","article-title":"A patent review of the ubiquitin ligase system: 2015-2018","volume":"28","author":"Li","year":"2018","journal-title":"Expert Opin Ther Pat"},{"key":"B7","doi-asserted-by":"publisher","first-page":"683","DOI":"10.1007\/s10555-017-9703-z","article-title":"E3 ubiquitin ligases in cancer and implications for therapies","volume":"36","author":"Wang","year":"2017","journal-title":"Cancer Metastasis Rev"},{"key":"B8","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1186\/s43556-021-00043-2","article-title":"E3 ubiquitin ligases: Styles, structures and functions","volume":"2","author":"Yang","year":"2021","journal-title":"Mol Biomed"},{"key":"B9","doi-asserted-by":"publisher","DOI":"10.1038\/88832","article-title":"Mutations in the gene encoding c-abl-binding protein SH3BP2 cause cherubism","volume":"28","author":"Ueki","year":"2001","journal-title":"Nat Genet"},{"key":"B10","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1016\/j.cell.2006.10.047","article-title":"Increased myeloid cell responses to m-CSF and RANKL cause bone loss and inflammation in SH3BP2 \"cherubism\" mice","volume":"128","author":"Ueki","year":"2007","journal-title":"Cell"},{"key":"B11","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2011.10.045","article-title":"Loss of tankyrase-mediated destruction of 3BP2 is the underlying pathogenic mechanism of cherubism","volume":"147","author":"Levaot","year":"2011","journal-title":"Cell"},{"key":"B12","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2011.10.046","article-title":"Structural basis and sequence rules for substrate recognition by tankyrase explain the basis for cherubism disease","volume":"147","author":"Guettler","year":"2011","journal-title":"Cell"},{"key":"B13","doi-asserted-by":"publisher","DOI":"10.1038\/ng0298-143","article-title":"The itchy locus encodes a novel ubiquitin protein ligase that is disrupted in a18H mice","volume":"18","author":"Perry","year":"1998","journal-title":"Nat Genet"},{"key":"B14","doi-asserted-by":"publisher","DOI":"10.1016\/j.ajhg.2010.01.028","article-title":"Human ITCH E3 ubiquitin ligase deficiency causes syndromic multisystem autoimmune disease","volume":"86","author":"Lohr","year":"2010","journal-title":"Am J Hum Genet"},{"key":"B15","doi-asserted-by":"publisher","DOI":"10.1093\/hmg\/ddl425","article-title":"Itch genetically interacts with Notch1 in a mouse autoimmune disease model","volume":"15","author":"Matesic","year":"2006","journal-title":"Hum Mol Genet"},{"key":"B16","doi-asserted-by":"publisher","DOI":"10.4049\/jimmunol.179.7.4435","article-title":"Ubiquitinylation of ig beta dictates the endocytic fate of the b cell antigen receptor","volume":"179","author":"Zhang","year":"2007","journal-title":"J Immunol"},{"key":"B17","doi-asserted-by":"publisher","first-page":"185","DOI":"10.1007\/978-3-540-75203-5_9","article-title":"Itchy mice: The identification of a new pathway for the development of autoimmunity","volume":"321","author":"Matesic","year":"2008","journal-title":"Curr Top Microbiol Immunol"},{"key":"B18","doi-asserted-by":"publisher","first-page":"4273","DOI":"10.1182\/blood-2007-10-115667","article-title":"Itch-\/- alphabeta and gammadelta T cells independently contribute to autoimmunity in itchy mice","volume":"111","author":"Parravicini","year":"2008","journal-title":"Blood"},{"key":"B19","doi-asserted-by":"publisher","DOI":"10.1084\/jem.20181953","article-title":"The E3 ubiquitin ligase itch restricts antigen-driven b cell responses","volume":"216","author":"Moser","year":"2019","journal-title":"J Exp Med"},{"key":"B20","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2009.06.038","article-title":"ITCH K63-ubiquitinates the NOD2 binding protein, RIP2, to influence inflammatory signaling pathways","volume":"19","author":"Tao","year":"2009","journal-title":"Curr Biol"},{"key":"B21","doi-asserted-by":"publisher","DOI":"10.1038\/35079114","article-title":"A frameshift mutation in NOD2 associated with susceptibility to crohn's disease","volume":"411","author":"Ogura","year":"2001","journal-title":"Nature"},{"key":"B22","doi-asserted-by":"publisher","DOI":"10.1006\/mcne.1998.0677","article-title":"Atrophin-1, the DRPLA gene product, interacts with two families of WW domain-containing proteins","volume":"11","author":"Wood","year":"1998","journal-title":"Mol Cell Neurosci"},{"key":"B23","doi-asserted-by":"publisher","DOI":"10.3389\/fgene.2019.00827","article-title":"Integrating genome-wide association studies with pathway analysis and gene expression analysis highlights novel osteoarthritis risk pathways and genes","volume":"10","author":"Gao","year":"2019","journal-title":"Front Genet"},{"key":"B24","doi-asserted-by":"publisher","first-page":"2429","DOI":"10.1038\/s41467-019-10177-1","article-title":"Wwp2 maintains cartilage homeostasis through regulation of Adamts5","volume":"10","author":"Mokuda","year":"2019","journal-title":"Nat Commun"},{"key":"B25","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1038\/ncb2134","article-title":"The E3 ubiquitin ligase Wwp2 regulates craniofacial development through mono-ubiquitylation of goosecoid","volume":"13","author":"Zou","year":"2011","journal-title":"Nat Cell Biol"},{"key":"B26","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1220271110","article-title":"E3 ligase WWP2 negatively regulates TLR3-mediated innate immune response by targeting TRIF for ubiquitination and degradation","volume":"110","author":"Yang","year":"2013","journal-title":"Proc Natl Acad Sci USA"},{"key":"B27","doi-asserted-by":"publisher","DOI":"10.1128\/MCB.00218-07","article-title":"A novel regulatory mechanism of the bone morphogenetic protein (BMP) signaling pathway involving the carboxyl-terminal tail domain of BMP type II receptor","volume":"27","author":"Chan","year":"2007","journal-title":"Mol Cell Biol"},{"key":"B28","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2005.01.035","article-title":"Ubiquitin ligase Smurf1 controls osteoblast activity and bone homeostasis by targeting MEKK2 for degradation","volume":"121","author":"Yamashita","year":"2005","journal-title":"Cell"},{"key":"B29","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1186\/gm448","article-title":"Genome-wide approaches for identifying genetic risk factors for osteoporosis","volume":"5","author":"Wu","year":"2013","journal-title":"Genome Med"},{"key":"B30","doi-asserted-by":"publisher","DOI":"10.1007\/s00223-020-00668-5","article-title":"Fragile bones secondary to SMURF1 gene duplication","volume":"106","author":"Al-Rawi","year":"2020","journal-title":"Calcif Tissue Int"},{"key":"B31","doi-asserted-by":"publisher","first-page":"16009","DOI":"10.1038\/boneres.2016.9","article-title":"TGF-beta and BMP signaling in osteoblast, skeletal development, and bone formation, homeostasis and disease","volume":"4","author":"Wu","year":"2016","journal-title":"Bone Res"},{"key":"B32","doi-asserted-by":"publisher","first-page":"4901","DOI":"10.1038\/ncomms5901","article-title":"ATR\/Chk1\/Smurf1 pathway determines cell fate after DNA damage by controlling RhoB abundance","volume":"5","author":"Wang","year":"2014","journal-title":"Nat Commun"},{"key":"B33","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1002\/jcp.20694","article-title":"The cbl family proteins: Ring leaders in regulation of cell signaling","volume":"209","author":"Swaminathan","year":"2006","journal-title":"J Cell Physiol"},{"key":"B34","doi-asserted-by":"publisher","DOI":"10.1042\/BJ20050892","article-title":"C-cbl and cbl-b ubiquitin ligases: Substrate diversity and the negative regulation of signalling responses","volume":"391","author":"Thien","year":"2005","journal-title":"Biochem J"},{"key":"B35","doi-asserted-by":"publisher","first-page":"294","DOI":"10.1038\/35067100","article-title":"Cbl: Many adaptations to regulate protein tyrosine kinases","volume":"2","author":"Thien","year":"2001","journal-title":"Nat Rev Mol Cell Biol"},{"key":"B36","doi-asserted-by":"publisher","DOI":"10.1093\/hmg\/ddx177","article-title":"Epigenome-wide association study of rheumatoid arthritis identifies differentially methylated loci in b cells","volume":"26","author":"Julia","year":"2017","journal-title":"Hum Mol Genet"},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.1158\/1078-0432.CCR-13-2490","article-title":"Molecular pathways: Cbl proteins in tumorigenesis and antitumor immunity-opportunities for cancer treatment","volume":"21","author":"Liyasova","year":"2015","journal-title":"Clin Cancer Res"},{"key":"B38","doi-asserted-by":"publisher","DOI":"10.1038\/ni0901-870","article-title":"Proteolysis-independent regulation of PI3K by cbl-b-mediated ubiquitination in T cells","volume":"2","author":"Fang","year":"2001","journal-title":"Nat Immunol"},{"key":"B39","doi-asserted-by":"publisher","DOI":"10.4049\/jimmunol.1303077","article-title":"A multiple sclerosis-associated variant of CBLB links genetic risk with type I IFN function","volume":"193","author":"Sturner","year":"2014","journal-title":"J Immunol"},{"key":"B40","doi-asserted-by":"publisher","DOI":"10.1038\/ng.479","article-title":"Genetic variants at CD28, PRDM1 and CD2\/CD58 are associated with rheumatoid arthritis risk","volume":"41","author":"Raychaudhuri","year":"2009","journal-title":"Nat Genet"},{"key":"B41","doi-asserted-by":"publisher","DOI":"10.1101\/gad.13.8.1015","article-title":"TRAF6 deficiency results in osteopetrosis and defective interleukin-1, CD40, and LPS signaling","volume":"13","author":"Lomaga","year":"1999","journal-title":"Genes Dev"},{"key":"B42","doi-asserted-by":"publisher","DOI":"10.1016\/j.febslet.2012.09.009","article-title":"Structural insight into the interaction of ADP-ribose with the PARP WWE domains","volume":"586","author":"He","year":"2012","journal-title":"FEBS Lett"},{"key":"B43","doi-asserted-by":"publisher","DOI":"10.1101\/gad.182618.111","article-title":"Recognition of the iso-ADP-ribose moiety in poly(ADP-ribose) by WWE domains suggests a general mechanism for poly(ADP-ribosyl)ation-dependent ubiquitination","volume":"26","author":"Wang","year":"2012","journal-title":"Genes Dev"},{"key":"B44","doi-asserted-by":"publisher","DOI":"10.1038\/nature13826","article-title":"Allosteric activation of the RNF146 ubiquitin ligase by a poly(ADP-ribosyl)ation signal","volume":"517","author":"DaRosa","year":"2015","journal-title":"Nature"},{"key":"B45","doi-asserted-by":"publisher","DOI":"10.1126\/science.8438166","article-title":"Identification of a ten-amino acid proline-rich SH3 binding site","volume":"259","author":"Ren","year":"1993","journal-title":"Science"},{"key":"B46","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1242\/jcs.175521","article-title":"Multifunctional abl kinases in health and disease","volume":"129","author":"Khatri","year":"2016","journal-title":"J Cell Sci"},{"key":"B47","doi-asserted-by":"publisher","DOI":"10.1302\/0301-620X.32B3.334","article-title":"Cherubism\u2013familial fibrous dysplasia of the jaws","author":"Jones","year":"1950","journal-title":"J Bone Joint Surg Br volume"},{"key":"B48","doi-asserted-by":"publisher","DOI":"10.1172\/JCI45843","article-title":"3BP2-deficient mice are osteoporotic with impaired osteoblast and osteoclast functions","volume":"121","author":"Levaot","year":"2011","journal-title":"J Clin Invest"},{"key":"B49","doi-asserted-by":"publisher","DOI":"10.1172\/JCI87802","article-title":"Reciprocal stabilization of ABL and TAZ regulates osteoblastogenesis through transcription factor RUNX2","volume":"126","author":"Matsumoto","year":"2016","journal-title":"J Clin Invest"},{"key":"B50","doi-asserted-by":"publisher","DOI":"10.3389\/fonc.2021.665273","article-title":"RUNX2 phosphorylation by tyrosine kinase ABL promotes breast cancer invasion","volume":"11","author":"He","year":"2021","journal-title":"Front Oncol"},{"key":"B51","doi-asserted-by":"publisher","DOI":"10.1172\/JCI90527","article-title":"RANKL coordinates multiple osteoclastogenic pathways by regulating expression of ubiquitin ligase RNF146","volume":"127","author":"Matsumoto","year":"2017","journal-title":"J Clin Invest"},{"key":"B52","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.201207142","article-title":"Canonical wnt signaling inhibits osteoclastogenesis independent of osteoprotegerin","volume":"200","author":"Albers","year":"2013","journal-title":"J Cell Biol"},{"key":"B53","doi-asserted-by":"publisher","DOI":"10.4049\/jimmunol.1102836","article-title":"TREM2 and beta-catenin regulate bone homeostasis by controlling the rate of osteoclastogenesis","volume":"188","author":"Otero","year":"2012","journal-title":"J Immunol"},{"key":"B54","doi-asserted-by":"publisher","DOI":"10.1128\/MCB.05980-11","article-title":"Biphasic and dosage-dependent regulation of osteoclastogenesis by beta-catenin","volume":"31","author":"Wei","year":"2011","journal-title":"Mol Cell Biol"},{"key":"B55","doi-asserted-by":"publisher","DOI":"10.1172\/JCI92233","article-title":"Ubiquitin ligase RNF146 coordinates bone dynamics and energy metabolism","volume":"127","author":"Matsumoto","year":"2017","journal-title":"J Clin Invest"},{"key":"B56","article-title":"Cleidocranial dysplasia: Clinical and molecular genetics","volume":"36","author":"Mundlos","year":"1999","journal-title":"J Med Genet"},{"key":"B57","article-title":"Sur la dysostose cl\u00e9ido-cranienne h\u00e9r\u00e9ditaire","volume":"6","author":"Marie","year":"1898","journal-title":"Rev Neurol"},{"key":"B58","doi-asserted-by":"publisher","DOI":"10.1016\/S0092-8674(00)80260-3","article-title":"Mutations involving the transcription factor CBFA1 cause cleidocranial dysplasia","volume":"89","author":"Mundlos","year":"1997","journal-title":"Cell."},{"key":"B59","doi-asserted-by":"publisher","DOI":"10.1038\/ng0797-307","article-title":"Missense mutations abolishing DNA binding of the osteoblast-specific transcription factor OSF2\/CBFA1 in cleidocranial dysplasia","volume":"16","author":"Lee","year":"1997","journal-title":"Nat Genet"},{"key":"B60","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1007\/978-1-62703-989-5_1","article-title":"Overview of skeletal development","volume":"1130","author":"Kobayashi","year":"2014","journal-title":"Methods Mol Biol"},{"key":"B61","doi-asserted-by":"publisher","DOI":"10.1016\/s0092-8674(00)80257-3","article-title":"Osf2\/Cbfa1: a transcriptional activator of osteoblast differentiation","volume":"89","author":"Ducy","year":"1997","journal-title":"Cell"},{"key":"B62","doi-asserted-by":"publisher","DOI":"10.1016\/s0092-8674(00)80258-5","article-title":"Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts","volume":"89","author":"Komori","year":"1997","journal-title":"Cell"},{"key":"B63","doi-asserted-by":"publisher","DOI":"10.1002\/humu.21298","article-title":"Deletions of the RUNX2 gene are present in about 10% of individuals with cleidocranial dysplasia","volume":"31","author":"Ott","year":"2010","journal-title":"Hum Mutat"},{"key":"B64","doi-asserted-by":"publisher","first-page":"e140869","DOI":"10.1172\/JCI140869","article-title":"Tankyrase represses autoinflammation through the attenuation of TLR2 signaling","volume":"132","author":"Matsumoto","year":"2022","journal-title":"J Clin Invest"},{"key":"B65","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.88.13.5582","article-title":"G Alpha 12 and G alpha 13 subunits define a fourth class of G protein alpha subunits","volume":"88","author":"Strathmann","year":"1991","journal-title":"Proc Natl Acad Sci USA"},{"key":"B66","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2019.01058","article-title":"Myo1f, an unconventional long-tailed myosin, is a new partner for the adaptor 3BP2 involved in mast cell migration","volume":"10","author":"Navines-Ferrer","year":"2019","journal-title":"Front Immunol"},{"key":"B67","doi-asserted-by":"publisher","DOI":"10.1128\/MCB.01014-06","article-title":"The 3BP2 adapter protein is required for optimal b-cell activation and thymus-independent type 2 humoral response","volume":"27","author":"Chen","year":"2007","journal-title":"Mol Cell Biol"},{"key":"B68","doi-asserted-by":"publisher","DOI":"10.1016\/j.celrep.2018.06.075","article-title":"Timed regulation of 3BP2 induction is critical for sustaining CD8(+) T cell expansion and differentiation","volume":"24","author":"Dimitriou","year":"2018","journal-title":"Cell Rep"},{"key":"B69","doi-asserted-by":"publisher","DOI":"10.1002\/art.38975","article-title":"Loss of SH3 domain-binding protein 2 function suppresses bone destruction in tumor necrosis factor-driven and collagen-induced arthritis in mice","volume":"67","author":"Mukai","year":"2015","journal-title":"Arthritis Rheumatol"},{"key":"B70","doi-asserted-by":"publisher","DOI":"10.1002\/jbmr.2295","article-title":"SH3BP2 cherubism mutation potentiates TNF-alpha-induced osteoclastogenesis via NFATc1 and TNF-alpha-mediated inflammatory bone loss","volume":"29","author":"Mukai","year":"2014","journal-title":"J Bone Miner Res"},{"key":"B71","doi-asserted-by":"publisher","first-page":"4898","DOI":"10.1038\/s41467-019-12910-2","article-title":"Tankyrase inhibition preserves osteoarthritic cartilage by coordinating cartilage matrix anabolism via effects on SOX9 PARylation","volume":"10","author":"Kim","year":"2019","journal-title":"Nat Commun"},{"key":"B72","doi-asserted-by":"publisher","first-page":"3079","DOI":"10.3390\/cancers13123079","article-title":"Targeting the ubiquitin-proteasome system for cancer therapeutics by small-molecule inhibitors","volume":"13","author":"LaPlante","year":"2021","journal-title":"Cancers (Basel)"},{"key":"B73","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1038\/s41392-020-0107-0","article-title":"The role of ubiquitination in tumorigenesis and targeted drug discovery","volume":"5","author":"Deng","year":"2020","journal-title":"Signal Transduct Target Ther"},{"key":"B74","doi-asserted-by":"publisher","DOI":"10.55563\/clinexprheumatol\/qf55h8","article-title":"Pharmacologic inhibition of PARP5, but not that of PARP1 or 2, promotes cytokine production and osteoclastogenesis through different pathways","author":"Asano","year":"2023","journal-title":"Clin Exp Rheumatol"},{"key":"B75","doi-asserted-by":"publisher","DOI":"10.1096\/fj.201902697RR","article-title":"JAK3 restrains inflammatory responses and protects against periodontal disease through Wnt3a signaling","volume":"34","author":"Lu","year":"2020","journal-title":"FASEB J"},{"key":"B76","doi-asserted-by":"publisher","DOI":"10.1172\/JCI138234","article-title":"HUWE1 mediates inflammasome activation and promotes host defense against bacterial infection","volume":"130","author":"Guo","year":"2020","journal-title":"J Clin Invest"},{"key":"B77","doi-asserted-by":"publisher","DOI":"10.1093\/intimm\/dxq470","article-title":"Anti-arthritic effect of E3 ubiquitin ligase, c-MIR, expression in the joints","volume":"23","author":"Toyomoto","year":"2011","journal-title":"Int Immunol"},{"key":"B78","doi-asserted-by":"publisher","DOI":"10.4049\/jimmunol.1900925","article-title":"Cullin 3 is crucial for pro-b cell proliferation, interacts with CD22, and controls CD22 internalization on b cells","volume":"204","author":"Meyer","year":"2020","journal-title":"J Immunol"},{"key":"B79","doi-asserted-by":"publisher","DOI":"10.1038\/bjc.2014.259","article-title":"Role of Fbxw7 in the maintenance of normal stem cells and cancer-initiating cells","volume":"111","author":"Takeishi","year":"2014","journal-title":"Br J Cancer"},{"key":"B80","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1038\/nrc2290","article-title":"FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation","volume":"8","author":"Welcker","year":"2008","journal-title":"Nat Rev Cancer"},{"key":"B81","doi-asserted-by":"publisher","DOI":"10.1038\/ncb2183","article-title":"Nde1-mediated inhibition of ciliogenesis affects cell cycle re-entry","volume":"13","author":"Kim","year":"2011","journal-title":"Nat Cell Biol"},{"key":"B82","doi-asserted-by":"publisher","first-page":"1066","DOI":"10.1038\/s42003-021-02504-4","article-title":"FBW7 couples structural integrity with functional output of primary cilia","volume":"4","author":"Petsouki","year":"2021","journal-title":"Commun Biol"},{"key":"B83","doi-asserted-by":"publisher","DOI":"10.1093\/jb\/mvj160","article-title":"A novel family of membrane-bound E3 ubiquitin ligases","volume":"140","author":"Ohmura-Hoshino","year":"2006","journal-title":"J Biochem"},{"key":"B84","doi-asserted-by":"crossref","DOI":"10.4049\/jimmunol.143.3.913","article-title":"Involvement of class II MHC molecules in the LPS-induction of IL-1\/TNF secretions by human monocytes. quantitative differences at the polymorphic level","volume":"143","author":"Santamaria","year":"1989","journal-title":"J Immunol"},{"key":"B85","doi-asserted-by":"publisher","DOI":"10.1084\/jem.20092203","article-title":"CD83 increases MHC II and CD86 on dendritic cells by opposing IL-10-driven MARCH1-mediated ubiquitination and degradation","volume":"208","author":"Tze","year":"2011","journal-title":"J Exp Med"},{"key":"B86","doi-asserted-by":"publisher","DOI":"10.1002\/eji.200737902","article-title":"Interleukin-10-induced MARCH1 mediates intracellular sequestration of MHC class II in monocytes","volume":"38","author":"Thibodeau","year":"2008","journal-title":"Eur J Immunol"},{"key":"B87","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0037330","article-title":"Francisella tularensis elicits IL-10 via a PGE(2)-inducible factor, to drive macrophage MARCH1 expression and class II down-regulation","volume":"7","author":"Hunt","year":"2012","journal-title":"PloS One"},{"key":"B88","doi-asserted-by":"publisher","DOI":"10.4049\/jimmunol.1601168","article-title":"MARCH1 E3 ubiquitin ligase dampens the innate inflammatory response by modulating monocyte functions in mice","volume":"198","author":"Galbas","year":"2017","journal-title":"J Immunol"},{"key":"B89","doi-asserted-by":"publisher","DOI":"10.1006\/jmbi.2001.4448","article-title":"Identification of muscle specific ring finger proteins as potential regulators of the titin kinase domain","volume":"306","author":"Centner","year":"2001","journal-title":"J Mol Biol"},{"key":"B90","doi-asserted-by":"publisher","DOI":"10.1152\/ajpendo.00204.2014","article-title":"Skeletal muscle atrophy and the E3 ubiquitin ligases MuRF1 and MAFbx\/atrogin-1","volume":"307","author":"Bodine","year":"2014","journal-title":"Am J Physiol Endocrinol Metab"},{"key":"B91","doi-asserted-by":"publisher","DOI":"10.1126\/science.1065874","article-title":"Identification of ubiquitin ligases required for skeletal muscle atrophy","volume":"294","author":"Bodine","year":"2001","journal-title":"Science."},{"key":"B92","doi-asserted-by":"publisher","first-page":"eaay8203","DOI":"10.1126\/scisignal.aay8203","article-title":"Myeloma cells shift osteoblastogenesis to adipogenesis by inhibiting the ubiquitin ligase MURF1 in mesenchymal stem cells","volume":"13","author":"Liu","year":"2020","journal-title":"Sci Signal"},{"key":"B93","doi-asserted-by":"publisher","DOI":"10.1016\/j.immuni.2008.09.003","article-title":"The adaptor protein MITA links virus-sensing receptors to IRF3 transcription factor activation","volume":"29","author":"Zhong","year":"2008","journal-title":"Immunity"},{"key":"B94","doi-asserted-by":"publisher","DOI":"10.1038\/nature07317","article-title":"STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling","volume":"455","author":"Ishikawa","year":"2008","journal-title":"Nature"},{"key":"B95","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1008387","article-title":"RNF90 negatively regulates cellular antiviral responses by targeting MITA for degradation","volume":"16","author":"Yang","year":"2020","journal-title":"PloS Pathog"},{"key":"B96","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2018.02882","article-title":"SAG\/RBX2 E3 ubiquitin ligase differentially regulates inflammatory responses of myeloid cell subsets","volume":"9","author":"Xiong","year":"2018","journal-title":"Front Immunol"},{"key":"B97","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.RA117.001267","article-title":"The endoplasmic reticulum-resident E3 ubiquitin ligase Hrd1 controls a critical checkpoint in b cell development in mice","volume":"293","author":"Yang","year":"2018","journal-title":"J Biol Chem"},{"key":"B98","doi-asserted-by":"publisher","first-page":"595","DOI":"10.1038\/nm.3111","article-title":"Peli1 promotes microglia-mediated CNS inflammation by regulating Traf3 degradation","volume":"19","author":"Xiao","year":"2013","journal-title":"Nat Med"},{"key":"B99","doi-asserted-by":"publisher","DOI":"10.1038\/s41423-021-00660-5","article-title":"The ubiquitin ligase Peli1 inhibits ICOS and thereby tfh-mediated immunity","volume":"18","author":"Huang","year":"2021","journal-title":"Cell Mol Immunol"},{"key":"B100","doi-asserted-by":"publisher","DOI":"10.1038\/nri2413","article-title":"TRIM family proteins and their emerging roles in innate immunity","volume":"8","author":"Ozato","year":"2008","journal-title":"Nat Rev Immunol"},{"key":"B101","doi-asserted-by":"publisher","DOI":"10.4049\/jimmunol.1500859","article-title":"TRIM38 negatively regulates TLR3\/4-mediated innate immune and inflammatory responses by two sequential and distinct mechanisms","volume":"195","author":"Hu","year":"2015","journal-title":"J Immunol"},{"key":"B102","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1016\/j.bbrc.2021.03.147","article-title":"TRIM37 negatively regulates inflammatory responses induced by virus infection via controlling TRAF6 ubiquitination","volume":"556","author":"Zhao","year":"2021","journal-title":"Biochem Biophys Res Commun"},{"key":"B103","doi-asserted-by":"publisher","DOI":"10.1002\/eji.201747129","article-title":"Myc binding protein 2 suppresses M2-like phenotypes in macrophages during zymosan-induced inflammation in mice","volume":"48","author":"Pierre","year":"2018","journal-title":"Eur J Immunol"}],"container-title":["Frontiers in Immunology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fimmu.2023.1120710\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,2,23]],"date-time":"2023-02-23T12:34:15Z","timestamp":1677155655000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fimmu.2023.1120710\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,2,23]]},"references-count":103,"alternative-id":["10.3389\/fimmu.2023.1120710"],"URL":"https:\/\/doi.org\/10.3389\/fimmu.2023.1120710","relation":{},"ISSN":["1664-3224"],"issn-type":[{"value":"1664-3224","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,2,23]]},"article-number":"1120710"}}