{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,29]],"date-time":"2026-10-29T12:43:46Z","timestamp":1793277826947,"version":"4.5.0"},"reference-count":47,"publisher":"Elsevier BV","issue":"5","license":[{"start":{"date-parts":[[2023,5,1]],"date-time":"2023-05-01T00:00:00Z","timestamp":1682899200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2023,5,1]],"date-time":"2023-05-01T00:00:00Z","timestamp":1682899200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"}],"funder":[{"name":"Intramural Research Programs","award":["ZIAAR041199"],"award-info":[{"award-number":["ZIAAR041199"]}]}],"content-domain":{"domain":["ard.eular.org","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Annals of the Rheumatic Diseases"],"published-print":{"date-parts":[[2023,5]]},"DOI":"10.1136\/ard-2022-223568","type":"journal-article","created":{"date-parts":[[2023,2,3]],"date-time":"2023-02-03T13:21:10Z","timestamp":1675430470000},"page":"630-638","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":144,"title":["Neutrophil extracellular trap-associated carbamylation and histones trigger osteoclast formation in rheumatoid arthritis"],"prefix":"10.1016","volume":"82","author":[{"given":"Liam J","family":"O'Neil","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christopher B","family":"Oliveira","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xinghao","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mario","family":"Navarrete","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ana","family":"Barrera-Vargas","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Javier","family":"Merayo-Chalico","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rwan","family":"Aljahdali","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eduardo","family":"Aguirre-Aguilar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9729-4572","authenticated-orcid":false,"given":"Philip","family":"Carlucci","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2968-0815","authenticated-orcid":false,"given":"Mariana J","family":"Kaplan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7706-1464","authenticated-orcid":false,"given":"Carmelo","family":"Carmona-Rivera","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1136\/ard-2022-223568_bib1","doi-asserted-by":"crossref","first-page":"134","DOI":"10.1038\/nri.2017.105","article-title":"Neutrophil extracellular traps in immunity and disease","volume":"18","author":"Papayannopoulos","year":"2018","journal-title":"Nat Rev Immunol"},{"key":"10.1136\/ard-2022-223568_bib2","doi-asserted-by":"crossref","first-page":"2178","DOI":"10.1182\/blood-2018-11-844530","article-title":"Neutrophils and nets in modulating acute and chronic inflammation","volume":"133","author":"Castanheira","year":"2019","journal-title":"Blood"},{"key":"10.1136\/ard-2022-223568_bib3","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1038\/nrrheum.2014.80","article-title":"The multifactorial role of neutrophils in rheumatoid arthritis","volume":"10","author":"Wright","year":"2014","journal-title":"Nat Rev Rheumatol"},{"key":"10.1136\/ard-2022-223568_bib4","doi-asserted-by":"crossref","first-page":"eabd2688","DOI":"10.1126\/sciadv.abd2688","article-title":"Neutrophil-Mediated carbamylation promotes articular damage in rheumatoid arthritis","volume":"6","author":"O'Neil","year":"2020","journal-title":"Sci Adv"},{"key":"10.1136\/ard-2022-223568_bib5","doi-asserted-by":"crossref","first-page":"531","DOI":"10.1016\/j.autrev.2009.12.013","article-title":"Neutrophils in rheumatoid arthritis: more than simple final effectors","volume":"9","author":"Casc\u00e3o","year":"2010","journal-title":"Autoimmun Rev"},{"key":"10.1136\/ard-2022-223568_bib6","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/j.molmed.2018.12.008","article-title":"Neutrophils in rheumatoid arthritis: breaking immune tolerance and fueling disease","volume":"25","author":"O'Neil","year":"2019","journal-title":"Trends Mol Med"},{"key":"10.1136\/ard-2022-223568_bib7","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1093\/rheumatology\/keab289","article-title":"Are neutrophil extracellular traps the link for the cross-talk between periodontitis and rheumatoid arthritis physiopathology?","volume":"61","author":"Oliveira","year":"2021","journal-title":"Rheumatology (Oxford)"},{"key":"10.1136\/ard-2022-223568_bib8","doi-asserted-by":"crossref","first-page":"e0192365","DOI":"10.1371\/journal.pone.0192365","article-title":"Circulating levels of carbamylated protein and neutrophil extracellular traps are associated with periodontitis severity in patients with rheumatoid arthritis: a pilot case-control study","volume":"13","author":"Kaneko","year":"2018","journal-title":"PLoS One"},{"key":"10.1136\/ard-2022-223568_bib9","doi-asserted-by":"crossref","first-page":"470","DOI":"10.1161\/CIRCRESAHA.119.314581","article-title":"Extracellular DNA NET-works with dire consequences for health","volume":"125","author":"Sorvillo","year":"2019","journal-title":"Circ Res"},{"key":"10.1136\/ard-2022-223568_bib10","doi-asserted-by":"crossref","first-page":"2536","DOI":"10.3389\/fimmu.2019.02536","article-title":"DAMPs and nets in sepsis","volume":"10","author":"Denning","year":"2019","journal-title":"Front Immunol"},{"key":"10.1136\/ard-2022-223568_bib11","doi-asserted-by":"crossref","first-page":"236","DOI":"10.3389\/fimmu.2016.00236","article-title":"The emerging role of nets in venous thrombosis and immunothrombosis","volume":"7","author":"Kimball","year":"2016","journal-title":"Front Immunol"},{"key":"10.1136\/ard-2022-223568_bib12","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1161\/CIRCRESAHA.117.312494","article-title":"Roles of PAD4 and netosis in experimental atherosclerosis and arterial injury: implications for superficial erosion","volume":"123","author":"Franck","year":"2018","journal-title":"Circ Res"},{"key":"10.1136\/ard-2022-223568_bib13","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1038\/nrrheum.2017.15","article-title":"Beyond citrullination: other post-translational protein modifications in rheumatoid arthritis","volume":"13","author":"Trouw","year":"2017","journal-title":"Nat Rev Rheumatol"},{"key":"10.1136\/ard-2022-223568_bib14","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1038\/nrrheum.2011.204","article-title":"The influence of AcpA status and characteristics on the course of RA","volume":"8","author":"Willemze","year":"2012","journal-title":"Nat Rev Rheumatol"},{"key":"10.1136\/ard-2022-223568_bib15","doi-asserted-by":"crossref","first-page":"17372","DOI":"10.1073\/pnas.1114465108","article-title":"Autoantibodies recognizing carbamylated proteins are present in sera of patients with rheumatoid arthritis and predict joint damage","volume":"108","author":"Shi","year":"2011","journal-title":"Proc Natl Acad Sci U S A"},{"key":"10.1136\/ard-2022-223568_bib16","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1186\/s13075-014-0515-z","article-title":"Separate and overlapping specificities in rheumatoid arthritis antibodies binding to citrulline- and homocitrulline-containing peptides related to type I and II collagen telopeptides","volume":"17","author":"Turunen","year":"2015","journal-title":"Arthritis Res Ther"},{"key":"10.1136\/ard-2022-223568_bib17","doi-asserted-by":"crossref","first-page":"416","DOI":"10.1111\/imm.12204","article-title":"Human monoclonal Fab and human plasma antibodies to carbamyl-epitopes cross-react with malondialdehyde-adducts","volume":"141","author":"Kummu","year":"2014","journal-title":"Immunology"},{"key":"10.1136\/ard-2022-223568_bib18","doi-asserted-by":"crossref","first-page":"570","DOI":"10.55563\/clinexprheumatol\/0ms5pk","article-title":"Mass-Spectrometric identification of carbamylated proteins present in the joints of rheumatoid arthritis patients and controls","volume":"39","author":"Verheul","year":"2021","journal-title":"Clin Exp Rheumatol"},{"key":"10.1136\/ard-2022-223568_bib19","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1136\/annrheumdis-2015-208870","article-title":"The association between anti-carbamylated protein (anti-carp) antibodies and radiographic progression in early rheumatoid arthritis: a study exploring replication and the added value to AcpA and rheumatoid factor","volume":"76","author":"Ajeganova","year":"2017","journal-title":"Ann Rheum Dis"},{"key":"10.1136\/ard-2022-223568_bib20","doi-asserted-by":"crossref","first-page":"1930","DOI":"10.1093\/rheumatology\/kev250","article-title":"Anti-carbamylated protein antibodies in rheumatoid arthritis patients of Asian descent","volume":"54","author":"Verheul","year":"2015","journal-title":"Rheumatology (Oxford)"},{"key":"10.1136\/ard-2022-223568_bib21","doi-asserted-by":"crossref","first-page":"e0180144","DOI":"10.1371\/journal.pone.0180144","article-title":"Anti-carbamylated protein autoantibodies associated with mortality in Spanish rheumatoid arthritis patients","volume":"12","author":"Vidal-Bralo","year":"2017","journal-title":"PLoS One"},{"key":"10.1136\/ard-2022-223568_bib22","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1186\/s12891-017-1563-8","article-title":"Association between antibodies to carbamylated proteins and subclinical atherosclerosis in rheumatoid arthritis patients","volume":"18","author":"Spinelli","year":"2017","journal-title":"BMC Musculoskelet Disord"},{"key":"10.1136\/ard-2022-223568_bib23","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1172\/JCI116179","article-title":"Macrophage colony-stimulating factor is indispensable for both proliferation and differentiation of osteoclast progenitors","volume":"91","author":"Tanaka","year":"1993","journal-title":"J Clin Invest"},{"key":"10.1136\/ard-2022-223568_bib24","doi-asserted-by":"crossref","first-page":"2226","DOI":"10.1089\/ten.tea.2012.0469","article-title":"Pi3K\/Akt pathway involvement in the osteogenic effects of osteoclast culture supernatants on preosteoblast cells","volume":"19","author":"Chen","year":"2013","journal-title":"Tissue Eng Part A"},{"key":"10.1136\/ard-2022-223568_bib25","doi-asserted-by":"crossref","first-page":"937","DOI":"10.3389\/fimmu.2019.00937","article-title":"Hematopoietic or osteoclast-specific deletion of syk leads to increased bone mass in experimental mice","volume":"10","author":"Csete","year":"2019","journal-title":"Front Immunol"},{"key":"10.1136\/ard-2022-223568_bib26","doi-asserted-by":"crossref","first-page":"713","DOI":"10.1038\/bonekey.2015.82","article-title":"The regulation of osteoclast differentiation by wnt signals","volume":"4","author":"Kobayashi","year":"2015","journal-title":"Bonekey Rep"},{"key":"10.1136\/ard-2022-223568_bib27","doi-asserted-by":"crossref","first-page":"44347","DOI":"10.1074\/jbc.M202009200","article-title":"A RANK\/TRAF6-dependent signal transduction pathway is essential for osteoclast cytoskeletal organization and resorptive function","volume":"277","author":"Armstrong","year":"2002","journal-title":"J Biol Chem"},{"key":"10.1136\/ard-2022-223568_bib28","doi-asserted-by":"crossref","first-page":"e0131041","DOI":"10.1371\/journal.pone.0131041","article-title":"Cxcl8 and CCL20 enhance osteoclastogenesis via modulation of cytokine production by human primary osteoblasts","volume":"10","author":"Pathak","year":"2015","journal-title":"PLoS One"},{"key":"10.1136\/ard-2022-223568_bib29","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1038\/nri.2016.124","article-title":"The immunopathogenesis of seropositive rheumatoid arthritis: from triggering to targeting","volume":"17","author":"Malmstr\u00f6m","year":"2017","journal-title":"Nat Rev Immunol"},{"key":"10.1136\/ard-2022-223568_bib30","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/S8756-3282(03)00086-3","article-title":"Interleukin-8 stimulation of osteoclastogenesis and bone resorption is a mechanism for the increased osteolysis of metastatic bone disease","volume":"33","author":"Bendre","year":"2003","journal-title":"Bone"},{"key":"10.1136\/ard-2022-223568_bib31","first-page":"2329","article-title":"Upregulation of interleukin-8 and activin A induces osteoclastogenesis in ameloblastoma","volume":"43","author":"Liu","year":"2019","journal-title":"Int J Mol Med"},{"key":"10.1136\/ard-2022-223568_bib32","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1186\/s12865-021-00409-9","article-title":"Lipopolysaccharide- TLR-4 axis regulates osteoclastogenesis independent of RANKL\/RANK signaling","volume":"22","author":"AlQranei","year":"2021","journal-title":"BMC Immunol"},{"key":"10.1136\/ard-2022-223568_bib33","doi-asserted-by":"crossref","first-page":"107602","DOI":"10.1016\/j.celrep.2020.107602","article-title":"Histones, DNA, and citrullination promote neutrophil extracellular trap inflammation by regulating the localization and activation of TLR4","volume":"31","author":"Tsourouktsoglou","year":"2020","journal-title":"Cell Rep"},{"key":"10.1136\/ard-2022-223568_bib34","doi-asserted-by":"crossref","first-page":"1915","DOI":"10.1136\/annrheumdis-2017-211300","article-title":"Molecular basis for increased susceptibility of Indigenous North Americans to seropositive rheumatoid arthritis","volume":"76","author":"Scally","year":"2017","journal-title":"Ann Rheum Dis"},{"key":"10.1136\/ard-2022-223568_bib35","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1016\/S8756-3282(99)00210-0","article-title":"Osteoblasts\/stromal cells stimulate osteoclast activation through expression of osteoclast differentiation factor\/RANKL but not macrophage colony-stimulating factor: receptor activator of NF-kappa B ligand","volume":"25","author":"Udagawa","year":"1999","journal-title":"Bone"},{"key":"10.1136\/ard-2022-223568_bib36","doi-asserted-by":"crossref","first-page":"715997","DOI":"10.3389\/fimmu.2021.715997","article-title":"Anti-carbamylated LL37 antibodies promote pathogenic bone resorption in rheumatoid arthritis","volume":"12","author":"O'Neil","year":"2021","journal-title":"Front Immunol"},{"key":"10.1136\/ard-2022-223568_bib37","doi-asserted-by":"crossref","first-page":"234","DOI":"10.3389\/fmed.2017.00234","article-title":"Key triggers of osteoclast-related diseases and available strategies for targeted therapies: a review","volume":"4","author":"Bi","year":"2017","journal-title":"Front Med (Lausanne)"},{"key":"10.1136\/ard-2022-223568_bib38","doi-asserted-by":"crossref","first-page":"2626","DOI":"10.4049\/jimmunol.1003930","article-title":"Extracellular histones are mediators of death through TLR2 and TLR4 in mouse fatal liver injury","volume":"187","author":"Xu","year":"2011","journal-title":"J Immunol"},{"key":"10.1136\/ard-2022-223568_bib39","doi-asserted-by":"crossref","first-page":"1317","DOI":"10.1016\/j.biocel.2007.11.008","article-title":"Neutrophil serine proteases fine-tune the inflammatory response","volume":"40","author":"Pham","year":"2008","journal-title":"Int J Biochem Cell Biol"},{"key":"10.1136\/ard-2022-223568_bib40","doi-asserted-by":"crossref","first-page":"e139388","DOI":"10.1172\/jci.insight.139388","article-title":"Neutrophil extracellular traps mediate articular cartilage damage and enhance cartilage component immunogenicity in rheumatoid arthritis","volume":"5","author":"Carmona-Rivera","year":"2020","journal-title":"JCI Insight"},{"key":"10.1136\/ard-2022-223568_bib41","doi-asserted-by":"crossref","first-page":"411","DOI":"10.4049\/jimmunol.0803729","article-title":"Neutrophil elastase represses IL-8\/CXCL8 synthesis in human airway smooth muscle cells through induction of NF-kappa B repressing factor","volume":"183","author":"Ho","year":"2009","journal-title":"J Immunol"},{"key":"10.1136\/ard-2022-223568_bib42","doi-asserted-by":"crossref","first-page":"3021","DOI":"10.1093\/eurheartj\/ehu111","article-title":"Carbamylated low-density lipoprotein induces endothelial dysfunction","volume":"35","author":"Speer","year":"2014","journal-title":"Eur Heart J"},{"key":"10.1136\/ard-2022-223568_bib43","doi-asserted-by":"crossref","first-page":"826","DOI":"10.1161\/01.ATV.0000258795.75121.8a","article-title":"Carbamylated low-density lipoprotein induces monocyte adhesion to endothelial cells through intercellular adhesion molecule-1 and vascular cell adhesion molecule-1","volume":"27","author":"Apostolov","year":"2007","journal-title":"Arterioscler Thromb Vasc Biol"},{"key":"10.1136\/ard-2022-223568_bib44","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1186\/s13075-020-02354-1","article-title":"Clinical predictors of multiple failure to biological therapy in patients with rheumatoid arthritis","volume":"22","author":"Novella-Navarro","year":"2020","journal-title":"Arthritis Res Ther"},{"key":"10.1136\/ard-2022-223568_bib45","doi-asserted-by":"crossref","first-page":"656","DOI":"10.1038\/nrrheum.2012.153","article-title":"Bone erosion in rheumatoid arthritis: mechanisms, diagnosis and treatment","volume":"8","author":"Schett","year":"2012","journal-title":"Nat Rev Rheumatol"},{"key":"10.1136\/ard-2022-223568_bib46","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1038\/s41584-022-00786-4","article-title":"From risk to chronicity: evolution of autoreactive B cell and antibody responses in rheumatoid arthritis","volume":"18","author":"Scherer","year":"2022","journal-title":"Nat Rev Rheumatol"},{"key":"10.1136\/ard-2022-223568_bib47","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1038\/s41467-020-20279-w","article-title":"Site-specific incorporation of citrulline into proteins in mammalian cells","volume":"12","author":"Mondal","year":"2021","journal-title":"Nat Commun"}],"container-title":["Annals of the Rheumatic Diseases"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0003496724084620?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0003496724084620?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/syndication.highwire.org\/content\/doi\/10.1136\/ard-2022-223568","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,1,5]],"date-time":"2025-01-05T03:19:27Z","timestamp":1736047167000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0003496724084620"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,5]]},"references-count":47,"journal-issue":{"issue":"5","published-print":{"date-parts":[[2023,5]]}},"alternative-id":["S0003496724084620"],"URL":"https:\/\/doi.org\/10.1136\/ard-2022-223568","relation":{},"ISSN":["0003-4967"],"issn-type":[{"value":"0003-4967","type":"print"}],"subject":[],"published":{"date-parts":[[2023,5]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Neutrophil extracellular trap-associated carbamylation and histones trigger osteoclast formation in rheumatoid arthritis","name":"articletitle","label":"Article Title"},{"value":"Annals of the Rheumatic Diseases","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1136\/ard-2022-223568","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"Copyright \u00a9 2023 \u00a9 Author(s) (or their employer(s)) 2023. No commercial re-use. See rights and permissions. Published by Elsevier Inc. Published by Elsevier B.V. All rights are reserved, including those for text and data mining, AI training, and similar technologies.","name":"copyright","label":"Copyright"}]}}