{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T21:09:38Z","timestamp":1791407378601,"version":"4.3.3"},"reference-count":41,"publisher":"Springer Science and Business Media LLC","issue":"3","license":[{"start":{"date-parts":[[2015,9,21]],"date-time":"2015-09-21T00:00:00Z","timestamp":1442793600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"},{"start":{"date-parts":[[2015,9,21]],"date-time":"2015-09-21T00:00:00Z","timestamp":1442793600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Cell Mol Immunol"],"published-print":{"date-parts":[[2016,5]]},"DOI":"10.1038\/cmi.2015.82","type":"journal-article","created":{"date-parts":[[2015,9,21]],"date-time":"2015-09-21T08:41:54Z","timestamp":1442824914000},"page":"401-408","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":52,"title":["Olfactory ecto-mesenchymal stem cells possess immunoregulatory function and suppress autoimmune arthritis"],"prefix":"10.1038","volume":"13","author":[{"given":"Ke","family":"Rui","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhijiang","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jie","family":"Tian","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiang","family":"Lin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaohui","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jie","family":"Ma","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xinyi","family":"Tang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huaxi","family":"Xu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liwei","family":"Lu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shengjun","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2015,9,21]]},"reference":[{"key":"BFcmi201582_CR1","doi-asserted-by":"publisher","first-page":"2990","DOI":"10.1089\/scd.2013.0204","volume":"22","author":"M Di Trapani","year":"2013","unstructured":"Di Trapani M, Bassi G, Ricciardi M, Fontana E, Bifari F, Pacelli L et al. Comparative study of immune regulatory properties of stem cells derived from different tissues. Stem Cells Dev 2013; 22: 2990\u20133002.","journal-title":"Stem Cells Dev"},{"key":"BFcmi201582_CR2","doi-asserted-by":"publisher","first-page":"315","DOI":"10.1080\/14653240600855905","volume":"8","author":"M Dominici","year":"2006","unstructured":"Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8: 315\u2013317.","journal-title":"Cytotherapy"},{"key":"BFcmi201582_CR3","doi-asserted-by":"publisher","first-page":"216","DOI":"10.1038\/cdd.2013.158","volume":"21","author":"S Ma","year":"2014","unstructured":"Ma S, Xie N, Li W, Yuan B, Shi Y, Wang Y . Immunobiology of mesenchymal stem cells. Cell Death Differ 2014; 21: 216\u2013225.","journal-title":"Cell Death Differ"},{"key":"BFcmi201582_CR4","doi-asserted-by":"publisher","first-page":"3499","DOI":"10.1182\/blood-2007-02-069716","volume":"110","author":"AJ Nauta","year":"2007","unstructured":"Nauta AJ, Fibbe WE . Immunomodulatory properties of mesenchymal stromal cells. Blood 2007; 110: 3499\u20133506.","journal-title":"Blood"},{"key":"BFcmi201582_CR5","doi-asserted-by":"publisher","first-page":"269","DOI":"10.4067\/S0716-97602012000300008","volume":"45","author":"FE Figueroa","year":"2012","unstructured":"Figueroa FE, Carrion F, Villanueva S, Khoury M . Mesenchymal stem cell treatment for autoimmune diseases: a critical review. Biol Res 2012; 45: 269\u2013277.","journal-title":"Biol Res"},{"key":"BFcmi201582_CR6","doi-asserted-by":"publisher","first-page":"60","DOI":"10.4317\/jced.51186","volume":"6","author":"JA Vina","year":"2014","unstructured":"Vina JA, El-Alami M, Gambini J, Borras C, Vina J, Penarrocha MA . Application of mesenchymal stem cells in bone regenerative procedures in oral implantology. A literature review. J Clin Exp Dent 2014; 6: 60\u201365.","journal-title":"J Clin Exp Dent"},{"key":"BFcmi201582_CR7","doi-asserted-by":"crossref","first-page":"942","DOI":"10.1002\/jor.21065","volume":"28","author":"EA Breitbart","year":"2010","unstructured":"Breitbart EA, Meade S, Azad V, Yeh S, Al-Zube L, Lee YS et al. Mesenchymal stem cells accelerate bone allograft incorporation in the presence of diabetes mellitus. J Orthop Res 2010; 28: 942\u2013949.","journal-title":"J Orthop Res"},{"key":"BFcmi201582_CR8","doi-asserted-by":"publisher","first-page":"505","DOI":"10.1093\/qjmed\/hcu033","volume":"107","author":"JJ El-Jawhari","year":"2014","unstructured":"El-Jawhari JJ, El-Sherbiny YM, Jones EA, McGonagle D . Mesenchymal stem cells, autoimmunity and rheumatoid arthritis. QJM 2014; 107: 505\u2013514.","journal-title":"QJM"},{"key":"BFcmi201582_CR9","doi-asserted-by":"publisher","first-page":"993","DOI":"10.4049\/jimmunol.0900803","volume":"183","author":"P Fiorina","year":"2009","unstructured":"Fiorina P, Jurewicz M, Augello A, Vergani A, Dada S, La Rosa S et al. Immunomodulatory function of bone marrow-derived mesenchymal stem cells in experimental autoimmune type 1 diabetes. J Immunol 2009; 183: 993\u20131004.","journal-title":"J Immunol"},{"key":"BFcmi201582_CR10","doi-asserted-by":"publisher","first-page":"417","DOI":"10.1038\/cmi.2008.52","volume":"5","author":"K Zhou","year":"2008","unstructured":"Zhou K, Zhang H, Jin O, Feng X, Yao G, Hou Y et al. Transplantation of human bone marrow mesenchymal stem cell ameliorates the autoimmune pathogenesis in MRL\/lpr mice. Cell Mol Immunol 2008; 5: 417\u2013424.","journal-title":"Cell Mol Immunol"},{"key":"BFcmi201582_CR11","doi-asserted-by":"publisher","first-page":"14","DOI":"10.4103\/0973-6247.59386","volume":"4","author":"P Shetty","year":"2010","unstructured":"Shetty P, Cooper K, Viswanathan C . Comparison of proliferative and multilineage differentiation potentials of cord matrix, cord blood, and bone marrow mesenchymal stem cells. Asian J Transfus Sci 2010; 4: 14\u201324.","journal-title":"Asian J Transfus Sci"},{"key":"BFcmi201582_CR12","doi-asserted-by":"publisher","first-page":"853","DOI":"10.1089\/scd.2009.0267","volume":"19","author":"B Delorme","year":"2010","unstructured":"Delorme B, Nivet E, Gaillard J, Haupl T, Ringe J, Deveze A et al. The human nose harbors a niche of olfactory ecto-mesenchymal stem cells displaying neurogenic and osteogenic properties. Stem Cells Dev 2010; 19: 853\u2013866.","journal-title":"Stem Cells Dev"},{"key":"BFcmi201582_CR13","doi-asserted-by":"publisher","first-page":"742","DOI":"10.1089\/scd.2011.0419","volume":"21","author":"S Hauser","year":"2012","unstructured":"Hauser S, Widera D, Qunneis F, Muller J, Zander C, Greiner J et al. Isolation of novel multipotent neural crest-derived stem cells from adult human inferior turbinate. Stem Cells Dev 2012; 21: 742\u2013756.","journal-title":"Stem Cells Dev"},{"key":"BFcmi201582_CR14","doi-asserted-by":"publisher","first-page":"2808","DOI":"10.1172\/JCI44489","volume":"121","author":"E Nivet","year":"2011","unstructured":"Nivet E, Vignes M, Girard SD, Pierrisnard C, Baril N, Dev\u00e8ze A et al. Engraftment of human nasal olfactory stem cells restores neuroplasticity in mice with hippocampal lesions. J Clin Invest 2011; 121: 2808\u20132820.","journal-title":"J Clin Invest"},{"key":"BFcmi201582_CR15","doi-asserted-by":"publisher","first-page":"673","DOI":"10.1016\/j.scr.2014.02.010","volume":"12","author":"JC Stamegna","year":"2014","unstructured":"Stamegna JC, Girard SD, Veron A, Sicard G, Khrestchatisky M, Feron F et al. A unique method for the isolation of nasal olfactory stem cells in living rats. Stem Cell Res 2014; 12: 673-\u2013679.","journal-title":"Stem Cell Res"},{"key":"BFcmi201582_CR16","doi-asserted-by":"publisher","first-page":"13","DOI":"10.22203\/eCM.v023a02","volume":"23","author":"E Birmingham","year":"2012","unstructured":"Birmingham E, Niebur GL, McHugh PE, Shaw G, Barry FP, McNamara LM . Osteogenic differentiation of mesenchymal stem cells is regulated by osteocyte and osteoblast cells in a simplified bone niche. Eur Cell Mater 2012; 23: 13\u201327.","journal-title":"Eur Cell Mater"},{"key":"BFcmi201582_CR17","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1038\/nprot.2010.189","volume":"6","author":"MT Yang","year":"2011","unstructured":"Yang MT, Fu J, Wang YK, Desai RA, Chen CS . Assaying stem cell mechanobiology on microfabricated elastomeric substrates with geometrically modulated rigidity. Nat Protoc 2011; 6: 187\u2013213.","journal-title":"Nat Protoc"},{"key":"BFcmi201582_CR18","doi-asserted-by":"publisher","first-page":"3564","DOI":"10.1002\/art.34637","volume":"64","author":"J Deng","year":"2012","unstructured":"Deng J, Liu Y, Yang M, Wang S, Zhang M, Wang X et al. Leptin exacerbates collagen-induced arthritis via enhancement of Th17 cell response. Arthritis Rheum 2012; 64: 3564\u20133573.","journal-title":"Arthritis Rheum"},{"key":"BFcmi201582_CR19","doi-asserted-by":"publisher","first-page":"1269","DOI":"10.1038\/nprot.2007.173","volume":"2","author":"DD Brand","year":"2007","unstructured":"Brand DD, Latham KA, Rosloniec EF . Collagen-induced arthritis. Nat Protoc 2007; 2: 1269\u20131275.","journal-title":"Nat Protoc"},{"key":"BFcmi201582_CR20","doi-asserted-by":"publisher","first-page":"296","DOI":"10.1038\/cmi.2011.2","volume":"8","author":"C Carnrot","year":"2011","unstructured":"Carnrot C, Prokopec KE, Rasbo K, Karlsson MC, Kleinau S . Marginal zone B cells are naturally reactive to collagen type II and are involved in the initiation of the immune response in collagen-induced arthritis. Cell Mol Immunol 2011; 8: 296\u2013304.","journal-title":"Cell Mol Immunol"},{"key":"BFcmi201582_CR21","doi-asserted-by":"publisher","first-page":"645","DOI":"10.1016\/j.freeradbiomed.2007.04.026","volume":"43","author":"NS Bryan","year":"2007","unstructured":"Bryan NS, Grisham MB . Methods to detect nitric oxide and its metabolites in biological samples. Free Radic Biol Med 2007; 43: 645\u2013657.","journal-title":"Free Radic Biol Med"},{"key":"BFcmi201582_CR22","doi-asserted-by":"publisher","first-page":"266","DOI":"10.1016\/j.actbio.2014.11.027","volume":"13","author":"SA Johnstone","year":"2015","unstructured":"Johnstone SA, Liley M, Dalby MJ, Barnett SC . Comparison of human olfactory and skeletal MSCs using osteogenic nanotopography to demonstrate bone-specific bioactivity of the surfaces. Acta Biomater 2015; 13: 266\u2013276.","journal-title":"Acta Biomater"},{"key":"BFcmi201582_CR23","doi-asserted-by":"publisher","first-page":"368","DOI":"10.1002\/glia.22440","volume":"61","author":"SL Lindsay","year":"2013","unstructured":"Lindsay SL, Johnstone SA, Mountford JC, Sheikh S, Allan DB, Clark L et al. Human mesenchymal stem cells isolated from olfactory biopsies but not bone enhance CNS myelination in vitro. Glia 2013; 61: 368\u2013382.","journal-title":"Glia"},{"key":"BFcmi201582_CR24","doi-asserted-by":"crossref","unstructured":"Huang Y-S, Li IH, Chueh S-H, Hueng D-Y, Tai M-C, Liang C-M et al. Mesenchymal stem cells from rat olfactory bulbs can differentiate into cells with cardiomyocyte characteristics. J Tissue Eng Regen Med 2013.","DOI":"10.1002\/term.1684"},{"key":"BFcmi201582_CR25","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1038\/icb.2012.60","volume":"91","author":"SP Burr","year":"2013","unstructured":"Burr SP, Dazzi F, Garden OA . Mesenchymal stromal cells and regulatory T cells: the Yin and Yang of peripheral tolerance? Immunol Cell Biol 2013; 91: 12\u201318.","journal-title":"Immunol Cell Biol"},{"key":"BFcmi201582_CR26","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1016\/j.stem.2007.11.014","volume":"2","author":"G Ren","year":"2008","unstructured":"Ren G, Zhang L, Zhao X, Xu G, Zhang Y, Roberts AI et al. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2008; 2: 141\u2013150.","journal-title":"Cell Stem Cell"},{"key":"BFcmi201582_CR27","doi-asserted-by":"publisher","first-page":"433","DOI":"10.1111\/j.1365-2567.2006.02321.x","volume":"117","author":"A Taylor","year":"2006","unstructured":"Taylor A, Verhagen J, Blaser K, Akdis M, Akdis CA . Mechanisms of immune suppression by interleukin-10 and transforming growth factor-beta: the role of T regulatory cells. Immunology 2006; 117: 433\u2013442.","journal-title":"Immunology"},{"key":"BFcmi201582_CR28","doi-asserted-by":"crossref","unstructured":"Liechtenstein T, Dufait I, Bricogne C, Lanna A, Pen J, Breckpot K et al. PD-L1\/PD-1 co-stimulation, a brake for T cell activation and a T cell differentiation signal. J Clin Cell Immunol 2012; S12.","DOI":"10.6064\/2012\/694137"},{"key":"BFcmi201582_CR29","doi-asserted-by":"publisher","first-page":"1175","DOI":"10.1002\/art.22511","volume":"56","author":"A Augello","year":"2007","unstructured":"Augello A, Tasso R, Negrini SM, Cancedda R, Pennesi G . Cell therapy using allogeneic bone marrow mesenchymal stem cells prevents tissue damage in collagen-induced arthritis. Arthritis Rheum 2007; 56: 1175\u20131186.","journal-title":"Arthritis Rheum"},{"key":"BFcmi201582_CR30","doi-asserted-by":"publisher","first-page":"978","DOI":"10.1053\/j.gastro.2008.11.041","volume":"136","author":"MA Gonz\u00e1lez","year":"2009","unstructured":"Gonz\u00e1lez MA, Gonzalez\u2013Rey E, Rico L, B\u00fcscher D, Delgado M . Adipose-derived mesenchymal stem cells alleviate experimental colitis by inhibiting inflammatory and autoimmune responses. Gastroenterology 2009; 136: 978\u2013989.","journal-title":"Gastroenterology"},{"key":"BFcmi201582_CR31","doi-asserted-by":"publisher","first-page":"I96","DOI":"10.1136\/ard.58.2008.i96","volume":"58","author":"B Bresnihan","year":"1999","unstructured":"Bresnihan B . Treatment of rheumatoid arthritis with interleukin 1 receptor antagonist. Ann Rheum Dis 1999; 58: I96\u2013I98.","journal-title":"Ann Rheum Dis"},{"key":"BFcmi201582_CR32","first-page":"CD003785","volume":"2002","author":"B Blumenauer","year":"2002","unstructured":"Blumenauer B, Judd M, Wells G, Burls A, Cranney A, Hochberg M et al. Infliximab for the treatment of rheumatoid arthritis. Cochrane Database Syst Rev 2002; 2002: CD003785.","journal-title":"Cochrane Database Syst Rev"},{"key":"BFcmi201582_CR33","doi-asserted-by":"publisher","first-page":"1761","DOI":"10.1002\/art.20303","volume":"50","author":"N Nishimoto","year":"2004","unstructured":"Nishimoto N, Yoshizaki K, Miyasaka N, Yamamoto K, Kawai S, Takeuchi T et al. Treatment of rheumatoid arthritis with humanized anti-interleukin-6 receptor antibody: a multicenter, double-blind, placebo-controlled trial. Arthritis Rheum 2004; 50: 1761\u20131769.","journal-title":"Arthritis Rheum"},{"key":"BFcmi201582_CR34","doi-asserted-by":"publisher","first-page":"280","DOI":"10.1124\/pr.114.009639","volume":"67","author":"S Siebert","year":"2015","unstructured":"Siebert S, Tsoukas A, Robertson J, McInnes I . Cytokines as therapeutic targets in rheumatoid arthritis and other inflammatory diseases. Pharmacol Rev 2015; 67: 280\u2013309.","journal-title":"Pharmacol Rev"},{"key":"BFcmi201582_CR35","volume-title":"The Role of Bone Marrow-derived Stem Cells in Lung Regeneration and Repair","author":"EK Sage","year":"2008","unstructured":"Sage EK, Loebinger MR, Polak J, Janes SM . The Role of Bone Marrow-derived Stem Cells in Lung Regeneration and Repair. Cambridge, MA: StemBook, 2008."},{"key":"BFcmi201582_CR36","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1007\/s00441-013-1585-y","volume":"353","author":"K Unsicker","year":"2013","unstructured":"Unsicker K . Neurotrophic molecules in the treatment of neurodegenerative disease with focus on the retina: status and perspectives. Cell Tissue Res 2013; 353: 205\u2013218.","journal-title":"Cell Tissue Res"},{"key":"BFcmi201582_CR37","doi-asserted-by":"publisher","first-page":"32","DOI":"10.1038\/icb.2012.64","volume":"91","author":"SA Jacobs","year":"2013","unstructured":"Jacobs SA, Roobrouck VD, Verfaillie CM, Van Gool SW . Immunological characteristics of human mesenchymal stem cells and multipotent adult progenitor cells. Immunol Cell Biol 2013; 91: 32\u201339.","journal-title":"Immunol Cell Biol"},{"key":"BFcmi201582_CR38","first-page":"216806","volume":"2014","author":"R Haddad","year":"2014","unstructured":"Haddad R, Saldanha-Araujo F . Mechanisms of T-cell immunosuppression by mesenchymal stromal cells: what do we know so far? BioMed Res Int 2014; 2014: 216806.","journal-title":"BioMed Res Int"},{"key":"BFcmi201582_CR39","doi-asserted-by":"publisher","first-page":"583","DOI":"10.1002\/jcb.1174","volume":"82","author":"SM Mueller","year":"2001","unstructured":"Mueller SM, Glowacki J . Age-related decline in the osteogenic potential of human bone marrow cells cultured in three-dimensional collagen sponges. J Cell Biochem 2001; 82: 583\u2013590.","journal-title":"J Cell Biochem"},{"key":"BFcmi201582_CR40","doi-asserted-by":"publisher","first-page":"561","DOI":"10.1002\/jcp.20890","volume":"210","author":"SY Lee","year":"2007","unstructured":"Lee SY, Miwa M, Sakai Y, Kuroda R, Matsumoto T, Iwakura T et al. In vitro multipotentiality and characterization of human unfractured traumatic hemarthrosis-derived progenitor cells: a potential cell source for tissue repair. J Cell Physiol 2007; 210: 561\u2013566.","journal-title":"J Cell Physiol"},{"key":"BFcmi201582_CR41","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1007\/978-1-62703-574-3_10","volume":"1059","author":"F F\u00e9ron","year":"2013","unstructured":"F\u00e9ron F, Perry C, Girard SD, Mackay-Sim A . Isolation of adult stem cells from the human olfactory mucosa. Methods Mol Biol 2013; 1059: 107\u2013114","journal-title":"Methods Mol Biol"}],"container-title":["Cellular &amp; Molecular Immunology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/cmi201582.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/cmi201582","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/cmi201582.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,3]],"date-time":"2023-01-03T11:06:12Z","timestamp":1672743972000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/cmi201582"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2015,9,21]]},"references-count":41,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2016,5]]}},"alternative-id":["BFcmi201582"],"URL":"https:\/\/doi.org\/10.1038\/cmi.2015.82","relation":{},"ISSN":["1672-7681","2042-0226"],"issn-type":[{"value":"1672-7681","type":"print"},{"value":"2042-0226","type":"electronic"}],"subject":[],"published":{"date-parts":[[2015,9,21]]},"assertion":[{"value":"18 May 2015","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"3 August 2015","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"3 August 2015","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"21 September 2015","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare that no conflicts of interest exist.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}]}}