{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,11]],"date-time":"2026-09-11T23:16:25Z","timestamp":1789168585526,"version":"build-2803163510"},"reference-count":43,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2018,5,14]],"date-time":"2018-05-14T00:00:00Z","timestamp":1526256000000},"content-version":"unspecified","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000268","name":"Biotechnology and Biological Sciences Research Council","doi-asserted-by":"publisher","award":["BB\/M029662\/1 and BB\/M029727\/1"],"award-info":[{"award-number":["BB\/M029662\/1 and BB\/M029727\/1"]}],"id":[{"id":"10.13039\/501100000268","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000341","name":"Arthritis Research UK","doi-asserted-by":"publisher","award":["21133"],"award-info":[{"award-number":["21133"]}],"id":[{"id":"10.13039\/501100000341","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Immunol."],"DOI":"10.3389\/fimmu.2018.01016","type":"journal-article","created":{"date-parts":[[2018,5,14]],"date-time":"2018-05-14T04:11:42Z","timestamp":1526271102000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":36,"title":["Protection Against Arthritis by the Parasitic Worm Product ES-62, and Its Drug-Like Small Molecule Analogues, Is Associated With Inhibition of Osteoclastogenesis"],"prefix":"10.3389","volume":"9","author":[{"given":"James","family":"Doonan","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Felicity E.","family":"Lumb","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Miguel A.","family":"Pineda","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anuradha","family":"Tarafdar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jenny","family":"Crowe","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aneesah M.","family":"Khan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Colin J.","family":"Suckling","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Margaret M.","family":"Harnett","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"William","family":"Harnett","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2018,5,14]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"429","DOI":"10.1038\/nri2094","article-title":"Cytokines in the pathogenesis of rheumatoid arthritis","volume":"7","author":"McInnes","year":"2007","journal-title":"Nat Rev Immunol"},{"key":"B2","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1186\/ar2110","article-title":"Cells of the synovium in rheumatoid arthritis. Osteoclasts","volume":"9","author":"Schett","year":"2007","journal-title":"Arthritis Res Ther"},{"key":"B3","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1038\/bonekey.2012.59","article-title":"Osteoimmunology: the expanding role of immunoreceptors in osteoclasts and bone remodeling","volume":"1","author":"Long","year":"2012","journal-title":"Bonekey Rep"},{"key":"B4","doi-asserted-by":"publisher","first-page":"1345","DOI":"10.1172\/JCI5703","article-title":"IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis","volume":"103","author":"Kotake","year":"1999","journal-title":"J Clin Invest"},{"key":"B5","doi-asserted-by":"publisher","first-page":"250","DOI":"10.1002\/1529-0131(200002)43:2<250::AID-ANR3>3.0.CO;2-P","article-title":"Synovial tissue in rheumatoid arthritis is a source of osteoclast differentiation factor","volume":"43","author":"Gravallese","year":"2000","journal-title":"Arthritis Rheum"},{"key":"B6","doi-asserted-by":"publisher","first-page":"991","DOI":"10.1242\/jcs.063032","article-title":"Bone remodelling at a glance","volume":"124","author":"Crockett","year":"2011","journal-title":"J Cell Sci"},{"key":"B7","doi-asserted-by":"publisher","first-page":"110","DOI":"10.1196\/annals.1346.014","article-title":"M-CSF, c-Fms, and signaling in osteoclasts and their precursors","volume":"1068","author":"Ross","year":"2006","journal-title":"Ann N Y Acad Sci"},{"key":"B8","doi-asserted-by":"publisher","first-page":"941","DOI":"10.1084\/jem.20040518","article-title":"RANKL-induced DC-STAMP is essential for osteoclastogenesis","volume":"200","author":"Kukita","year":"2004","journal-title":"J Exp Med"},{"key":"B9","doi-asserted-by":"publisher","first-page":"159","DOI":"10.1016\/j.bone.2004.09.020","article-title":"Impaired bone resorption in cathepsin K-deficient mice is partially compensated for by enhanced osteoclastogenesis and increased expression of other proteases via an increased RANKL\/OPG ratio","volume":"36","author":"Kiviranta","year":"2005","journal-title":"Bone"},{"key":"B10","doi-asserted-by":"publisher","first-page":"889","DOI":"10.1016\/S1534-5807(02)00369-6","article-title":"Induction and activation of the transcription factor NFATc1 (NFAT2) Integrate RANKL signaling in terminal differentiation of osteoclasts","volume":"3","author":"Takayanagi","year":"2002","journal-title":"Dev Cell"},{"key":"B11","doi-asserted-by":"publisher","first-page":"874","DOI":"10.3892\/ijmm.2013.1258","article-title":"A crucial role for reactive oxygen species in macrophage colony-stimulating factor-induced RANK expression in osteoclastic differentiation","volume":"31","author":"Nakanishi","year":"2013","journal-title":"Int J Mol Med"},{"key":"B12","doi-asserted-by":"publisher","first-page":"852","DOI":"10.1182\/blood-2004-09-3662","article-title":"A crucial role for reactive oxygen species in RANKL-induced osteoclast differentiation","volume":"106","author":"Lee","year":"2005","journal-title":"Blood"},{"key":"B13","doi-asserted-by":"publisher","DOI":"10.3904\/kjim.2016.329","article-title":"N-acetyl-l-cysteine controls osteoclastogenesis through regulating Th17 differentiation and RANKL in rheumatoid arthritis","author":"Kim","year":"2017","journal-title":"Korean J Intern Med"},{"key":"B14","doi-asserted-by":"publisher","first-page":"2127","DOI":"10.4049\/jimmunol.171.4.2127","article-title":"A novel therapeutic approach targeting articular inflammation using the filarial nematode-derived phosphorylcholine-containing glycoprotein ES-62","volume":"171","author":"McInnes","year":"2003","journal-title":"J Immunol"},{"key":"B15","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1016\/S0167-4889(01)00101-X","article-title":"Modulation of the host immune system by phosphorylcholine-containing glycoproteins secreted by parasitic filarial nematodes","volume":"1539","author":"Harnett","year":"2001","journal-title":"Biochim Biophys Acta"},{"key":"B16","doi-asserted-by":"publisher","first-page":"1492","DOI":"10.1002\/art.38392","article-title":"ES-62 protects against collagen-induced arthritis by resetting interleukin-22 toward resolution of inflammation in the joints","volume":"66","author":"Pineda","year":"2014","journal-title":"Arthritis Rheumatol"},{"key":"B17","doi-asserted-by":"publisher","first-page":"3168","DOI":"10.1002\/art.34581","article-title":"The parasitic helminth product ES-62 suppresses pathogenesis in collagen-induced arthritis by targeting the interleukin-17-producing cellular network at multiple sites","volume":"64","author":"Pineda","year":"2012","journal-title":"Arthritis Rheum"},{"key":"B18","doi-asserted-by":"publisher","first-page":"9982","DOI":"10.1021\/jm401251p","article-title":"Designing anti-inflammatory drugs from parasitic worms: a synthetic small molecule analogue of the Acanthocheilonema viteae product ES-62 prevents development of collagen-induced arthritis","volume":"56","author":"Al-Riyami","year":"2013","journal-title":"J Med Chem"},{"key":"B19","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1016\/j.jaut.2015.04.005","article-title":"Prophylactic and therapeutic treatment with a synthetic analogue of a parasitic worm product prevents experimental arthritis and inhibits IL-1\u03b2 production via NRF2-mediated counter-regulation of the inflammasome","volume":"60","author":"Rzepecka","year":"2015","journal-title":"J Autoimmun"},{"key":"B20","doi-asserted-by":"publisher","first-page":"1704","DOI":"10.1038\/s41598-017-01651-1","article-title":"Dendritic cells provide a therapeutic target for synthetic small molecule analogues of the parasitic worm product, ES-62","volume":"7","author":"Lumb","year":"2017","journal-title":"Sci Rep"},{"key":"B21","doi-asserted-by":"publisher","first-page":"518","DOI":"10.1136\/ard.2007.073502","article-title":"The phosphorycholine moiety of the filarial nematode immunomodulator ES-62 is responsible for its anti-inflammatory action in arthritis","volume":"67","author":"Harnett","year":"2008","journal-title":"Ann Rheum Dis"},{"key":"B22","doi-asserted-by":"publisher","first-page":"308","DOI":"10.14800\/ics.308","article-title":"The parasitic worm product ES-62 up-regulates IL-22 production by \u03b3\u03b4 T cells in the murine model of collagen-induced arthritis","volume":"1","author":"Harnett","year":"2014","journal-title":"Inflamm Cell Signal"},{"key":"B23","doi-asserted-by":"publisher","first-page":"3089","DOI":"10.4049\/jimmunol.1601441","article-title":"Glucose-dependent insulinotropic polypeptide receptor deficiency leads to impaired bone marrow hematopoiesis","volume":"198","author":"Mantelmacher","year":"2017","journal-title":"J Immunol"},{"key":"B24","doi-asserted-by":"publisher","first-page":"4592","DOI":"10.1172\/JCI60920","article-title":"Inflammatory arthritis increases mouse osteoclast precursors with myeloid suppressor function","volume":"122","author":"Charles","year":"2012","journal-title":"J Clin Invest"},{"key":"B25","doi-asserted-by":"publisher","first-page":"491","DOI":"10.1111\/j.1365-2567.2004.01993.x","article-title":"In vivo exposure of murine dendritic cell and macrophage bone marrow progenitors to the phosphorylcholine-containing filarial nematode glycoprotein ES-62 polarizes their differentiation to an anti-inflammatory phenotype","volume":"113","author":"Goodridge","year":"2004","journal-title":"Immunology"},{"key":"B26","doi-asserted-by":"publisher","first-page":"e2104","DOI":"10.1371\/journal.pone.0002104","article-title":"Complex dynamics of osteoclast formation and death in long-term cultures","volume":"3","author":"Akchurin","year":"2008","journal-title":"PLoS One"},{"key":"B27","doi-asserted-by":"crossref","first-page":"3233","DOI":"10.1242\/jcs.108.10.3233","article-title":"Multinucleated cells can continuously generate mononucleated cells in the absence of mitosis: a study of cells of the avian osteoclast lineage","volume":"108","author":"Solari","year":"1995","journal-title":"J Cell Sci"},{"key":"B28","doi-asserted-by":"publisher","first-page":"1269","DOI":"10.1038\/nprot.2007.173","article-title":"Collagen-induced arthritis","volume":"2","author":"Brand","year":"2007","journal-title":"Nat Protoc"},{"key":"B29","doi-asserted-by":"publisher","first-page":"1023","DOI":"10.1002\/art.39004","article-title":"The parasitic worm product ES-62 targets myeloid differentiation factor 88-dependent effector mechanisms to suppress antinuclear antibody production and proteinuria in MRL\/lpr mice","volume":"67","author":"Rodgers David","year":"2015","journal-title":"Arthritis Rheumatol"},{"key":"B30","doi-asserted-by":"publisher","first-page":"176","DOI":"10.1210\/me.2007-0237","article-title":"NFATc1 induces osteoclast fusion via up-regulation of Atp6v0d2 and the dendritic cell-specific transmembrane protein (DC-STAMP)","volume":"22","author":"Kim","year":"2008","journal-title":"Mol Endocrinol"},{"key":"B31","doi-asserted-by":"publisher","first-page":"1617","DOI":"10.1177\/00220345990780100601","article-title":"Autocrine regulation of osteoclast formation and bone resorption by IL-1\u03b1 and TNF\u03b1","volume":"78","author":"Tani-Ishii","year":"1999","journal-title":"J Dent Res"},{"key":"B32","doi-asserted-by":"publisher","first-page":"23009","DOI":"10.1074\/jbc.M113.478545","article-title":"The Keap1\/Nrf2 protein axis plays a role in osteoclast differentiation by regulating intracellular reactive oxygen species signaling","volume":"288","author":"Kanzaki","year":"2013","journal-title":"J Biol Chem"},{"key":"B33","doi-asserted-by":"publisher","first-page":"666","DOI":"10.1016\/j.jaci.2016.07.007","article-title":"Regulation of the host immune system by helminth parasites","volume":"138","author":"Maizels","year":"2016","journal-title":"J Allergy Clin Immunol"},{"key":"B34","doi-asserted-by":"publisher","first-page":"11596","DOI":"10.1038\/ncomms11596","article-title":"Th2 and eosinophil responses suppress inflammatory arthritis","volume":"7","author":"Chen","year":"2016","journal-title":"Nat Commun"},{"key":"B35","doi-asserted-by":"publisher","first-page":"457","DOI":"10.1111\/imm.12208","article-title":"Protection against collagen-induced arthritis in mice afforded by the parasitic worm product, ES-62, is associated with restoration of the levels of interleukin-10-producing B cells and reduced plasma cell infiltration of the joints","volume":"141","author":"Rodgers","year":"2014","journal-title":"Immunology"},{"key":"B36","doi-asserted-by":"crossref","first-page":"284","DOI":"10.4049\/jimmunol.174.1.284","article-title":"Immunomodulation via novel use of TLR4 by the filarial nematode phosphorylcholine-containing secreted product, ES-62","volume":"174","author":"Goodridge","year":"2005","journal-title":"J Immunol"},{"key":"B37","doi-asserted-by":"publisher","first-page":"801","DOI":"10.1016\/j.immuni.2006.04.008","article-title":"Toll-like receptors on hematopoietic progenitor cells stimulate innate immune system replenishment","volume":"24","author":"Nagai","year":"2006","journal-title":"Immunity"},{"key":"B38","doi-asserted-by":"publisher","first-page":"1399","DOI":"10.1016\/j.ijpara.2005.05.012","article-title":"A glycoprotein from Spirometra erinaceieuropaei plerocercoids suppresses osteoclastogenesis and proinflammatory cytokine gene expression","volume":"35","author":"Kina","year":"2005","journal-title":"Int J Parasitol"},{"key":"B39","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1080\/08916934.2016.1261837","article-title":"Inflammatory arthritis and systemic bone loss are attenuated by gastrointestinal helminth parasites","volume":"50","author":"Sarter","year":"2017","journal-title":"Autoimmunity"},{"key":"B40","doi-asserted-by":"publisher","first-page":"1573","DOI":"10.1016\/j.jprot.2011.06.002","article-title":"Proteomic analysis of secretory products from the model gastrointestinal nematode Heligmosomoides polygyrus reveals dominance of venom allergen-like (VAL) proteins","volume":"74","author":"Hewitson","year":"2011","journal-title":"J Proteomics"},{"key":"B41","doi-asserted-by":"crossref","first-page":"4829","DOI":"10.4049\/jimmunol.151.9.4829","article-title":"Inhibition of murine B cell proliferation and down-regulation of protein kinase C levels by a phosphorylcholine-containing filarial excretory-secretory product","volume":"151","author":"Harnett","year":"1993","journal-title":"J Immunol"},{"key":"B42","doi-asserted-by":"publisher","first-page":"443","DOI":"10.1126\/science.7939685","article-title":"c-Fos: a key regulator of osteoclast-macrophage lineage determination and bone remodeling","volume":"266","author":"Grigoriadis","year":"1994","journal-title":"Science"},{"key":"B43","doi-asserted-by":"publisher","first-page":"789","DOI":"10.1016\/j.freeradbiomed.2013.08.005","article-title":"Nrf2 deficiency induces oxidative stress and promotes RANKL-induced osteoclast differentiation","volume":"65","author":"Hyeon","year":"2013","journal-title":"Free Radic Biol Med"}],"container-title":["Frontiers in Immunology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fimmu.2018.01016\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,9,2]],"date-time":"2023-09-02T16:03:56Z","timestamp":1693670636000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fimmu.2018.01016\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,5,14]]},"references-count":43,"alternative-id":["10.3389\/fimmu.2018.01016"],"URL":"https:\/\/doi.org\/10.3389\/fimmu.2018.01016","relation":{},"ISSN":["1664-3224"],"issn-type":[{"value":"1664-3224","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,5,14]]},"article-number":"1016"}}