{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,27]],"date-time":"2026-07-27T18:31:18Z","timestamp":1785177078090,"version":"3.55.0"},"reference-count":40,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2020,7,1]],"date-time":"2020-07-01T00:00:00Z","timestamp":1593561600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2020,7,1]],"date-time":"2020-07-01T00:00:00Z","timestamp":1593561600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2020,3,12]],"date-time":"2020-03-12T00:00:00Z","timestamp":1583971200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Journal of Orthopaedic Translation"],"published-print":{"date-parts":[[2020,7]]},"DOI":"10.1016\/j.jot.2020.03.007","type":"journal-article","created":{"date-parts":[[2020,4,23]],"date-time":"2020-04-23T17:02:28Z","timestamp":1587661348000},"page":"21-28","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":34,"special_numbering":"C","title":["Multiple umbilical cord\u2013derived MSCs administrations attenuate rat osteoarthritis progression via preserving articular cartilage superficial layer cells and inhibiting synovitis"],"prefix":"10.1016","volume":"23","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8031-0380","authenticated-orcid":false,"given":"Wei","family":"Tong","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaoguang","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Quan","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiarui","family":"Fang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yong","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zengwu","family":"Shao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuhua","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dongcheng","family":"Wu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6576-3699","authenticated-orcid":false,"given":"Xiaoming","family":"Sheng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yingze","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hongtao","family":"Tian","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"issue":"7","key":"10.1016\/j.jot.2020.03.007_bib1","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1038\/nrrheum.2014.44","article-title":"The individual and socioeconomic impact of osteoarthritis","volume":"10","author":"Hunter","year":"2014","journal-title":"Nat Rev Rheumatol"},{"issue":"11","key":"10.1016\/j.jot.2020.03.007_bib2","doi-asserted-by":"crossref","first-page":"654","DOI":"10.1038\/nrrheum.2013.138","article-title":"Towards a mechanism-based approach to pain management in osteoarthritis","volume":"9","author":"Malfait","year":"2013","journal-title":"Nat Rev Rheumatol"},{"issue":"11","key":"10.1016\/j.jot.2020.03.007_bib3","doi-asserted-by":"crossref","first-page":"1835","DOI":"10.1016\/j.joca.2014.12.016","article-title":"Inflammation and intracellular metabolism: new targets in OA","volume":"23","author":"Liu-Bryan","year":"2015","journal-title":"Osteoarthritis Cartilage"},{"key":"10.1016\/j.jot.2020.03.007_bib4","doi-asserted-by":"crossref","first-page":"16072","DOI":"10.1038\/nrdp.2016.72","article-title":"Osteoarthritis","volume":"2","author":"Martel-Pelletier","year":"2016","journal-title":"Nat Rev Dis Prim"},{"issue":"1","key":"10.1016\/j.jot.2020.03.007_bib5","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.joca.2016.08.008","article-title":"Nanoindentation modulus of murine cartilage: a sensitive indicator of the initiation and progression of post-traumatic osteoarthritis","volume":"25","author":"Doyran","year":"2017","journal-title":"Osteoarthritis Cartilage"},{"issue":"10182","key":"10.1016\/j.jot.2020.03.007_bib6","doi-asserted-by":"crossref","first-page":"1745","DOI":"10.1016\/S0140-6736(19)30417-9","article-title":"Osteoarthritis","volume":"393","author":"Hunter","year":"2019","journal-title":"Lancet"},{"issue":"2","key":"10.1016\/j.jot.2020.03.007_bib7","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1006\/abbi.1996.0461","article-title":"Association of proteoglycan degradation with catabolic cytokine and stromelysin release from cartilage cultured with fibronectin fragments","volume":"334","author":"Homandberg","year":"1996","journal-title":"Arch Biochem Biophys"},{"issue":"2","key":"10.1016\/j.jot.2020.03.007_bib8","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1177\/1759720X12467868","article-title":"Role of inflammation in the pathogenesis of osteoarthritis: latest findings and interpretations","volume":"5","author":"Sokolove","year":"2013","journal-title":"Ther Adv Musculoskelet Dis"},{"issue":"3","key":"10.1016\/j.jot.2020.03.007_bib9","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1002\/bdrc.20050","article-title":"Mechanisms of synovial joint and articular cartilage formation: recent advances, but many lingering mysteries","volume":"75","author":"Pacifici","year":"2005","journal-title":"Birth Defects Res C Embryo Today"},{"issue":"4","key":"10.1016\/j.jot.2020.03.007_bib10","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1002\/(SICI)1097-0029(19970515)37:4<271::AID-JEMT3>3.0.CO;2-O","article-title":"Ultrastructure of adult human articular cartilage matrix after cryotechnical processing","volume":"37","author":"Hunziker","year":"1997","journal-title":"Microsc Res Tech"},{"issue":"Pt 6","key":"10.1016\/j.jot.2020.03.007_bib11","doi-asserted-by":"crossref","first-page":"889","DOI":"10.1242\/jcs.00912","article-title":"The surface of articular cartilage contains a progenitor cell population","volume":"117","author":"Dowthwaite","year":"2004","journal-title":"J Cell Sci"},{"issue":"5","key":"10.1016\/j.jot.2020.03.007_bib12","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1002\/stem.2975","article-title":"Periarticular mesenchymal progenitors initiate and contribute to secondary ossification center formation during mouse long bone development","volume":"37","author":"Tong","year":"2019","journal-title":"Stem Cell"},{"issue":"5","key":"10.1016\/j.jot.2020.03.007_bib13","doi-asserted-by":"crossref","first-page":"1261","DOI":"10.1002\/art.39030","article-title":"Identification of a Prg4-expressing articular cartilage progenitor cell population in mice","volume":"67","author":"Kozhemyakina","year":"2015","journal-title":"Arthritis Rheum"},{"issue":"6","key":"10.1016\/j.jot.2020.03.007_bib14","doi-asserted-by":"crossref","first-page":"617","DOI":"10.1089\/ten.teb.2010.0191","article-title":"Articular cartilage: structure and regeneration","volume":"16","author":"Becerra","year":"2010","journal-title":"Tissue Eng B Rev"},{"issue":"1","key":"10.1016\/j.jot.2020.03.007_bib15","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.joca.2005.07.014","article-title":"Osteoarthritis cartilage histopathology: grading and staging","volume":"14","author":"Pritzker","year":"2006","journal-title":"Osteoarthritis Cartilage"},{"issue":"1","key":"10.1016\/j.jot.2020.03.007_bib16","doi-asserted-by":"crossref","first-page":"26","DOI":"10.3109\/14653249.2011.605119","article-title":"Comparison of chemokine and receptor gene expression between Wharton's jelly and bone marrow-derived mesenchymal stromal cells","volume":"14","author":"Balasubramanian","year":"2012","journal-title":"Cytotherapy"},{"issue":"3","key":"10.1016\/j.jot.2020.03.007_bib17","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1002\/sctm.18-0053","article-title":"Umbilical cord-derived mesenchymal stromal cells (MSCs) for knee osteoarthritis: repeated MSC dosing is superior to a single MSC dose and to hyaluronic acid in a controlled randomized phase I\/II trial","volume":"8","author":"Matas","year":"2019","journal-title":"Stem Cells Transl Med"},{"issue":"2","key":"10.1016\/j.jot.2020.03.007_bib18","first-page":"71","article-title":"Human umbilical cord-derived mesenchymal stem cells reduce monosodium iodoacetate-induced apoptosis in cartilage","volume":"30","author":"Chang","year":"2018","journal-title":"Ci Ji Yi Xue Za Zhi"},{"issue":"10","key":"10.1016\/j.jot.2020.03.007_bib19","doi-asserted-by":"crossref","first-page":"1109","DOI":"10.5966\/sctm.2015-0022","article-title":"Chorion mesenchymal stem cells show superior differentiation, immunosuppressive, and angiogenic potentials in comparison with haploidentical maternal placental cells","volume":"4","author":"Gonz\u00e1lez","year":"2015","journal-title":"Stem Cells Transl Med"},{"issue":"9","key":"10.1016\/j.jot.2020.03.007_bib20","doi-asserted-by":"crossref","first-page":"1670","DOI":"10.1002\/art.1780400917","article-title":"Mono-iodoacetate-induced experimental osteoarthritis: a dose-response study of loss of mobility, morphology, and biochemistry","volume":"40","author":"Guingamp","year":"1997","journal-title":"Arthritis Rheum"},{"issue":"12","key":"10.1016\/j.jot.2020.03.007_bib21","doi-asserted-by":"crossref","first-page":"1739","DOI":"10.1038\/labinvest.2011.144","article-title":"Roles of beta-catenin signaling in phenotypic expression and proliferation of articular cartilage superficial zone cells","volume":"91","author":"Yasuhara","year":"2011","journal-title":"Lab Invest"},{"issue":"8","key":"10.1016\/j.jot.2020.03.007_bib22","doi-asserted-by":"crossref","first-page":"949","DOI":"10.1016\/j.joca.2012.05.001","article-title":"Histopathology of naturally occurring and surgically induced osteoarthritis in mice","volume":"20","author":"McNulty","year":"2012","journal-title":"Osteoarthritis Cartilage"},{"issue":"8","key":"10.1016\/j.jot.2020.03.007_bib23","doi-asserted-by":"crossref","first-page":"2173","DOI":"10.1002\/art.11094","article-title":"Inflammation and angiogenesis in osteoarthritis","volume":"48","author":"Haywood","year":"2003","journal-title":"Arthritis Rheum"},{"issue":"7","key":"10.1016\/j.jot.2020.03.007_bib24","first-page":"1534","volume":"99","author":"Billinghurst","year":"1997","journal-title":"Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage"},{"issue":"7033","key":"10.1016\/j.jot.2020.03.007_bib25","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1038\/nature03369","article-title":"Deletion of active ADAMTS5 prevents cartilage degradation in a murine model of osteoarthritis","volume":"434","author":"Glasson","year":"2005","journal-title":"Nature"},{"issue":"50","key":"10.1016\/j.jot.2020.03.007_bib26","doi-asserted-by":"crossref","first-page":"14360","DOI":"10.1073\/pnas.1608938113","article-title":"EGFR signaling is critical for maintaining the superficial layer of articular cartilage and preventing osteoarthritis initiation","volume":"113","author":"Jia","year":"2016","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"6","key":"10.1016\/j.jot.2020.03.007_bib27","doi-asserted-by":"crossref","first-page":"728","DOI":"10.1016\/j.joca.2011.02.014","article-title":"T helper cells promote disease progression of osteoarthritis by inducing macrophage inflammatory protein-1\u03b3","volume":"19","author":"Shen","year":"2011","journal-title":"Osteoarthritis Cartilage"},{"issue":"1","key":"10.1016\/j.jot.2020.03.007_bib28","doi-asserted-by":"crossref","first-page":"3451","DOI":"10.1038\/s41598-017-03759-w","article-title":"IL-6 secretion in osteoarthritis patients is mediated by chondrocyte-synovial fibroblast cross-talk and is enhanced by obesity","volume":"7","author":"Pearson","year":"2017","journal-title":"Sci Rep"},{"issue":"12","key":"10.1016\/j.jot.2020.03.007_bib29","doi-asserted-by":"crossref","first-page":"3464","DOI":"10.1002\/art.11365","article-title":"Stem cell therapy in a caprine model of osteoarthritis","volume":"48","author":"Murphy","year":"2003","journal-title":"Arthritis Rheum"},{"issue":"6","key":"10.1016\/j.jot.2020.03.007_bib30","first-page":"1376","volume":"37","author":"Kuroda","year":"2019","journal-title":"Intra-articular autologous uncultured adipose-derived stromal cell transplantation inhibited the progression of cartilage degeneration"},{"issue":"9","key":"10.1016\/j.jot.2020.03.007_bib31","doi-asserted-by":"crossref","first-page":"2153","DOI":"10.1111\/jcmm.13138","article-title":"A comparative assessment of adipose-derived stem cells from subcutaneous and visceral fat as a potential cell source for knee osteoarthritis treatment,","volume":"21","author":"Tang","year":"2017","journal-title":"J Cell Mol Med"},{"issue":"7","key":"10.1016\/j.jot.2020.03.007_bib32","doi-asserted-by":"crossref","first-page":"847","DOI":"10.5966\/sctm.2015-0245","article-title":"Adipose mesenchymal stromal cell-based therapy for severe osteoarthritis of the knee: a phase I dose-escalation trial","volume":"5","author":"Pers","year":"2016","journal-title":"Stem cells Transl Med"},{"issue":"3","key":"10.1016\/j.jot.2020.03.007_bib33","first-page":"4474","article-title":"The human umbilical cord stem cells improve the viability of OA degenerated chondrocytes,","volume":"17","author":"Wang","year":"2018","journal-title":"Mol Med Rep"},{"issue":"6","key":"10.1016\/j.jot.2020.03.007_bib34","first-page":"1229","article-title":"MSC therapy for osteoarthritis: an unfinished story","volume":"37","author":"Barry","year":"2019"},{"issue":"6","key":"10.1016\/j.jot.2020.03.007_bib35","doi-asserted-by":"crossref","first-page":"1384","DOI":"10.1634\/stemcells.2006-0709","article-title":"Comparison of proliferative and multilineage differentiation potential of human mesenchymal stem cells derived from umbilical cord and bone marrow","volume":"25","author":"Baksh","year":"2007","journal-title":"Stem Cell"},{"key":"10.1016\/j.jot.2020.03.007_bib36","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1186\/1478-811X-9-12","article-title":"Different populations and sources of human mesenchymal stem cells (MSC): a comparison of adult and neonatal tissue-derived MSC","volume":"9","author":"Hass","year":"2011","journal-title":"Cell Commun Signal"},{"issue":"4","key":"10.1016\/j.jot.2020.03.007_bib37","doi-asserted-by":"crossref","first-page":"206","DOI":"10.1038\/nrrheum.2014.200","article-title":"Origin and function of cartilage stem\/progenitor cells in osteoarthritis","volume":"11","author":"Jiang","year":"2015","journal-title":"Nat Rev Rheumatol"},{"issue":"1","key":"10.1016\/j.jot.2020.03.007_bib38","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1186\/s13075-017-1229-9","article-title":"Synovitis in osteoarthritis: current understanding with therapeutic implications","volume":"19","author":"Mathiessen","year":"2017","journal-title":"Arthritis Res Ther"},{"issue":"5","key":"10.1016\/j.jot.2020.03.007_bib39","doi-asserted-by":"crossref","first-page":"1399","DOI":"10.7150\/thno.21072","article-title":"Mesenchymal stem cells-derived exosomes are more immunosuppressive than microparticles in inflammatory arthritis","volume":"8","author":"Cosenza","year":"2018","journal-title":"Theranostics"},{"issue":"1\u20132","key":"10.1016\/j.jot.2020.03.007_bib40","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1016\/S0304-3959(03)00012-5","article-title":"Injection of nerve growth factor into human masseter muscle evokes long-lasting mechanical allodynia and hyperalgesia","volume":"104","author":"Svensson","year":"2003","journal-title":"Pain"}],"container-title":["Journal of Orthopaedic Translation"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S2214031X20300371?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S2214031X20300371?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,11,1]],"date-time":"2025-11-01T10:42:03Z","timestamp":1761993723000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S2214031X20300371"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,7]]},"references-count":40,"alternative-id":["S2214031X20300371"],"URL":"https:\/\/doi.org\/10.1016\/j.jot.2020.03.007","relation":{},"ISSN":["2214-031X"],"issn-type":[{"value":"2214-031X","type":"print"}],"subject":[],"published":{"date-parts":[[2020,7]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Multiple umbilical cord\u2013derived MSCs administrations attenuate rat osteoarthritis progression via preserving articular cartilage superficial layer cells and inhibiting synovitis","name":"articletitle","label":"Article Title"},{"value":"Journal of Orthopaedic Translation","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.jot.2020.03.007","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2020 The Authors. Published by Elsevier (Singapore) Pte Ltd on behalf of Chinese Speaking Orthopaedic Society.","name":"copyright","label":"Copyright"}]}}