{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,29]],"date-time":"2026-10-29T17:47:49Z","timestamp":1793296069187,"version":"4.5.0"},"reference-count":55,"publisher":"Elsevier BV","issue":"5","license":[{"start":{"date-parts":[[2022,8,1]],"date-time":"2022-08-01T00:00:00Z","timestamp":1659312000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2022,8,1]],"date-time":"2022-08-01T00:00:00Z","timestamp":1659312000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2022,6,21]],"date-time":"2022-06-21T00:00:00Z","timestamp":1655769600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["mucosalimmunology.org","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Mucosal Immunology"],"published-print":{"date-parts":[[2022,8]]},"DOI":"10.1038\/s41385-022-00535-6","type":"journal-article","created":{"date-parts":[[2022,6,21]],"date-time":"2022-06-21T15:39:56Z","timestamp":1655825996000},"page":"1028-1039","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":13,"title":["S100A4 exerts robust mucosal adjuvant activity for co-administered antigens in mice"],"prefix":"10.1016","volume":"15","author":[{"given":"Arka","family":"Sen Chaudhuri","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yu-Wen","family":"Yeh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Olifan","family":"Zewdie","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nga Shan","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jia-Bin","family":"Sun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tao","family":"Jin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bin","family":"Wei","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jan","family":"Holmgren","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3925-0296","authenticated-orcid":false,"given":"Zou","family":"Xiang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1038\/s41385-022-00535-6_bib1","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1111\/cei.13285","article-title":"Mucosal vaccines and technology","volume":"196","author":"Miquel-Clopes","year":"2019","journal-title":"Clin. Exp. Immunol."},{"key":"10.1038\/s41385-022-00535-6_bib2","doi-asserted-by":"crossref","first-page":"1636","DOI":"10.1016\/j.immuni.2021.07.017","article-title":"Accelerated COVID-19 vaccine development: milestones, lessons, and prospects","volume":"54","author":"Bok","year":"2021","journal-title":"Immunity"},{"key":"10.1038\/s41385-022-00535-6_bib3","doi-asserted-by":"crossref","first-page":"1070","DOI":"10.1080\/21645515.2015.1114195","article-title":"Induction of mucosal immunity through systemic immunization: Phantom or reality?","volume":"12","author":"Su","year":"2016","journal-title":"Hum. Vaccin. Immunother."},{"key":"10.1038\/s41385-022-00535-6_bib4","doi-asserted-by":"crossref","first-page":"118813","DOI":"10.1016\/j.ijpharm.2019.118813","article-title":"Nasal route for vaccine and drug delivery: features and current opportunities","volume":"572","author":"Lobaina Mato","year":"2019","journal-title":"Int. J. Pharm."},{"key":"10.1038\/s41385-022-00535-6_bib5","doi-asserted-by":"crossref","first-page":"1119","DOI":"10.3389\/fimmu.2017.01119","article-title":"Deficiency in Calcium-Binding Protein S100A4 Impairs the Adjuvant Action of Cholera Toxin","volume":"8","author":"Sun","year":"2017","journal-title":"Front. Immunol."},{"key":"10.1038\/s41385-022-00535-6_bib6","doi-asserted-by":"crossref","first-page":"1551","DOI":"10.1007\/s00018-013-1400-7","article-title":"Joining S100 proteins and migration: for better or for worse, in sickness and in health","volume":"71","author":"Gross","year":"2014","journal-title":"Cell. Mol. Life Sci."},{"key":"10.1038\/s41385-022-00535-6_bib7","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1083\/jcb.130.2.393","article-title":"Identification and characterization of a fibroblast marker: FSP1","volume":"130","author":"Strutz","year":"1995","journal-title":"J. Cell Biol."},{"key":"10.1038\/s41385-022-00535-6_bib8","doi-asserted-by":"crossref","first-page":"1267","DOI":"10.1136\/gut.2008.170779","article-title":"Autoimmune pancreatitis results from loss of TGFbeta signalling in S100A4-positive dendritic cells","volume":"58","author":"Boomershine","year":"2009","journal-title":"Gut"},{"key":"10.1038\/s41385-022-00535-6_bib9","doi-asserted-by":"crossref","first-page":"2598","DOI":"10.1091\/mbc.e09-07-0609","article-title":"S100A4 regulates macrophage chemotaxis","volume":"21","author":"Li","year":"2010","journal-title":"Mol. Biol. Cell"},{"key":"10.1038\/s41385-022-00535-6_bib10","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1007\/s10555-011-9338-4","article-title":"S100A4 calcium-binding protein is key player in tumor progression and metastasis: preclinical and clinical evidence","volume":"31","author":"Mishra","year":"2012","journal-title":"Cancer Metastasis Rev."},{"key":"10.1038\/s41385-022-00535-6_bib11","doi-asserted-by":"crossref","first-page":"1301","DOI":"10.1002\/ijc.23617","article-title":"Activation of NF-kappaB by extracellular S100A4: analysis of signal transduction mechanisms and identification of target genes","volume":"123","author":"Boye","year":"2008","journal-title":"Int J. Cancer"},{"key":"10.1038\/s41385-022-00535-6_bib12","doi-asserted-by":"crossref","first-page":"1520","DOI":"10.1093\/rheumatology\/keu031","article-title":"The metastasis-associated protein S100A4 promotes the inflammatory response of mononuclear cells via the TLR4 signalling pathway in rheumatoid arthritis","volume":"53","author":"Cerezo","year":"2014","journal-title":"Rheumatol. (Oxf.)"},{"key":"10.1038\/s41385-022-00535-6_bib13","doi-asserted-by":"crossref","first-page":"24","DOI":"10.2174\/156652413804486214","article-title":"Functions of S100 proteins","volume":"13","author":"Donato","year":"2013","journal-title":"Curr. Mol. Med."},{"key":"10.1038\/s41385-022-00535-6_bib14","doi-asserted-by":"crossref","first-page":"218ra4","DOI":"10.1126\/scitranslmed.3007410","article-title":"A generally applicable translational strategy identifies S100A4 as a candidate gene in allergy","volume":"6","author":"Bruhn","year":"2014","journal-title":"Sci. Transl. Med."},{"key":"10.1038\/s41385-022-00535-6_bib15","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1038\/mi.2010.55","article-title":"Topical immunization strategies","volume":"3","author":"Czerkinsky","year":"2010","journal-title":"Mucosal. Immunol."},{"key":"10.1038\/s41385-022-00535-6_bib16","doi-asserted-by":"crossref","first-page":"eabd2223","DOI":"10.1126\/scitranslmed.abd2223","article-title":"IgA dominates the early neutralizing antibody response to SARS-CoV-2","volume":"13","author":"Sterlin","year":"2020","journal-title":"Sci. Transl. Med"},{"key":"10.1038\/s41385-022-00535-6_bib17","doi-asserted-by":"crossref","first-page":"eabf1555","DOI":"10.1126\/scitranslmed.abf1555","article-title":"Enhanced SARS-CoV-2 neutralization by dimeric IgA","volume":"13","author":"Wang","year":"2021","journal-title":"Sci. Transl. Med"},{"key":"10.1038\/s41385-022-00535-6_bib18","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1248\/bpb.b14-00398","article-title":"The effect of cilia and the mucociliary clearance on successful drug delivery","volume":"38","author":"Gizurarson","year":"2015","journal-title":"Biol. Pharm. Bull."},{"key":"10.1038\/s41385-022-00535-6_bib19","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.addr.2020.06.019","article-title":"Controlling timing and location in vaccines","volume":"158","author":"Irvine","year":"2020","journal-title":"Adv. Drug Deliv. Rev."},{"key":"10.1038\/s41385-022-00535-6_bib20","doi-asserted-by":"crossref","DOI":"10.1038\/s41467-017-02247-z","article-title":"Migratory dendritic cells acquire and present lymphatic endothelial cell-archived antigens during lymph node contraction","volume":"8","author":"Kedl","year":"2017","journal-title":"Nat. Commun."},{"key":"10.1038\/s41385-022-00535-6_bib21","doi-asserted-by":"crossref","first-page":"eaal2094","DOI":"10.1126\/scitranslmed.aal2094","article-title":"Vaccine priming is restricted to draining lymph nodes and controlled by adjuvant-mediated antigen uptake","volume":"9","author":"Liang","year":"2017","journal-title":"Sci. Transl. Med"},{"key":"10.1038\/s41385-022-00535-6_bib22","doi-asserted-by":"crossref","first-page":"2214","DOI":"10.3389\/fimmu.2019.02214","article-title":"Adjuvants Enhance the Induction of Germinal Center and Antibody Secreting Cells in Spleen and Their Persistence in Bone Marrow of Neonatal Mice","volume":"10","author":"Aradottir Pind","year":"2019","journal-title":"Front. Immunol."},{"key":"10.1038\/s41385-022-00535-6_bib23","doi-asserted-by":"crossref","first-page":"1357","DOI":"10.1586\/erv.10.136","article-title":"Is the choice of vaccine adjuvant critical for long-term memory development?","volume":"9","author":"Lycke","year":"2010","journal-title":"Expert Rev. Vaccines"},{"key":"10.1038\/s41385-022-00535-6_bib24","doi-asserted-by":"crossref","first-page":"1108","DOI":"10.4049\/jimmunol.158.3.1108","article-title":"Mouse CD38 is down-regulated on germinal center B cells and mature plasma cells","volume":"158","author":"Oliver","year":"1997","journal-title":"J. Immunol."},{"key":"10.1038\/s41385-022-00535-6_bib25","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1038\/s41590-020-0598-4","article-title":"Germinal center B cells selectively oxidize fatty acids for energy while conducting minimal glycolysis","volume":"21","author":"Weisel","year":"2020","journal-title":"Nat. Immunol."},{"key":"10.1038\/s41385-022-00535-6_bib26","doi-asserted-by":"crossref","first-page":"1529","DOI":"10.3389\/fimmu.2019.01529","article-title":"Targeting Conventional Dendritic Cells to Fine-Tune Antibody Responses","volume":"10","author":"Tesfaye","year":"2019","journal-title":"Front. Immunol."},{"key":"10.1038\/s41385-022-00535-6_bib27","doi-asserted-by":"crossref","first-page":"269","DOI":"10.3389\/fimmu.2019.00269","article-title":"Requirement for Cyclic AMP\/Protein Kinase A-Dependent Canonical NFkappaB Signaling in the Adjuvant Action of Cholera Toxin and Its Non-toxic Derivative mmCT","volume":"10","author":"Terrinoni","year":"2019","journal-title":"Front. Immunol."},{"key":"10.1038\/s41385-022-00535-6_bib28","doi-asserted-by":"crossref","first-page":"97","DOI":"10.5483\/BMBRep.2017.50.2.170","article-title":"Extracellular S100A4 negatively regulates osteoblast function by activating the NF-kappaB pathway","volume":"50","author":"Kim","year":"2017","journal-title":"BMB Rep."},{"key":"10.1038\/s41385-022-00535-6_bib29","doi-asserted-by":"crossref","first-page":"5487","DOI":"10.1038\/sj.onc.1207720","article-title":"Extracellular S100A4(mts1) stimulates invasive growth of mouse endothelial cells and modulates MMP-13 matrix metalloproteinase activity","volume":"23","author":"Schmidt-Hansen","year":"2004","journal-title":"Oncogene"},{"key":"10.1038\/s41385-022-00535-6_bib30","doi-asserted-by":"crossref","first-page":"e63012","DOI":"10.1371\/journal.pone.0063012","article-title":"Common interactions between S100A4 and S100A9 defined by a novel chemical probe","volume":"8","author":"Bjork","year":"2013","journal-title":"PLoS ONE"},{"key":"10.1038\/s41385-022-00535-6_bib31","doi-asserted-by":"crossref","first-page":"2874","DOI":"10.3389\/fimmu.2018.02874","article-title":"Adjuvants Enhancing Cross-Presentation by Dendritic Cells: The Key to More Effective Vaccines?","volume":"9","author":"Ho","year":"2018","journal-title":"Front. Immunol."},{"key":"10.1038\/s41385-022-00535-6_bib32","doi-asserted-by":"crossref","first-page":"2431","DOI":"10.1016\/S0264-410X(02)00155-X","article-title":"A dilemma for mucosal vaccination: efficacy versus toxicity using enterotoxin-based adjuvants","volume":"20","author":"Fujihashi","year":"2002","journal-title":"Vaccine"},{"key":"10.1038\/s41385-022-00535-6_bib33","doi-asserted-by":"crossref","first-page":"592","DOI":"10.1038\/nri3251","article-title":"Recent progress in mucosal vaccine development: potential and limitations","volume":"12","author":"Lycke","year":"2012","journal-title":"Nat. Rev. Immunol."},{"key":"10.1038\/s41385-022-00535-6_bib34","first-page":"153","article-title":"Cholera toxin - a foe & a friend","volume":"133","author":"Sanchez","year":"2011","journal-title":"Indian J. Med. Res."},{"key":"10.1038\/s41385-022-00535-6_bib35","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1016\/j.coph.2018.03.015","article-title":"ADP-ribosylating enterotoxins as vaccine adjuvants","volume":"41","author":"Lycke","year":"2018","journal-title":"Curr. Opin. Pharm."},{"key":"10.1038\/s41385-022-00535-6_bib36","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1038\/cmi.2016.34","article-title":"HMGB1, IL-1alpha, IL-33 and S100 proteins: dual-function alarmins","volume":"14","author":"Bertheloot","year":"2017","journal-title":"Cell Mol. Immunol."},{"key":"10.1038\/s41385-022-00535-6_bib37","doi-asserted-by":"crossref","first-page":"422","DOI":"10.3389\/fimmu.2015.00422","article-title":"DAMPs from Cell Death to New Life","volume":"6","author":"Venereau","year":"2015","journal-title":"Front. Immunol."},{"key":"10.1038\/s41385-022-00535-6_bib38","doi-asserted-by":"crossref","first-page":"309","DOI":"10.3389\/fimmu.2014.00309","article-title":"Emerging Concepts about NAIP\/NLRC4 Inflammasomes","volume":"5","author":"Lage","year":"2014","journal-title":"Front. Immunol."},{"key":"10.1038\/s41385-022-00535-6_bib39","doi-asserted-by":"crossref","first-page":"252","DOI":"10.3390\/pathogens9040252","article-title":"Inflammasomes as Targets for Adjuvants","volume":"9","author":"Ivanov","year":"2020","journal-title":"Pathogens"},{"key":"10.1038\/s41385-022-00535-6_bib40","doi-asserted-by":"crossref","first-page":"771","DOI":"10.3109\/1061186X.2010.523790","article-title":"Nasal vaccine innovation","volume":"18","author":"Jabbal-Gill","year":"2010","journal-title":"J. Drug Target"},{"key":"10.1038\/s41385-022-00535-6_bib41","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1016\/j.biotechadv.2009.06.007","article-title":"Application of chitosan microspheres for nasal delivery of vaccines","volume":"27","author":"Kang","year":"2009","journal-title":"Biotechnol. Adv."},{"key":"10.1038\/s41385-022-00535-6_bib42","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1042\/BC20100120","article-title":"Ciliary beat co-ordination by calcium","volume":"103","author":"Schmid","year":"2011","journal-title":"Biol. Cell"},{"key":"10.1038\/s41385-022-00535-6_bib43","doi-asserted-by":"crossref","first-page":"2270","DOI":"10.4049\/jimmunol.180.4.2270","article-title":"Maturing dendritic cells depend on RAGE for in vivo homing to lymph nodes","volume":"180","author":"Manfredi","year":"2008","journal-title":"J. Immunol."},{"key":"10.1038\/s41385-022-00535-6_bib44","doi-asserted-by":"crossref","first-page":"2823","DOI":"10.1016\/j.celrep.2019.10.091","article-title":"S100A4 Protein Is Essential for the Development of Mature Microfold Cells in Peyer's Patches","volume":"29","author":"Kunimura","year":"2019","journal-title":"Cell Rep."},{"key":"10.1038\/s41385-022-00535-6_bib45","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/j.coi.2017.03.006","article-title":"Plasma cell and memory B cell differentiation from the germinal center","volume":"45","author":"Suan","year":"2017","journal-title":"Curr. Opin. Immunol."},{"key":"10.1038\/s41385-022-00535-6_bib46","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1111\/imr.12756","article-title":"B cell primary immune responses","volume":"288","author":"Shlomchik","year":"2019","journal-title":"Immunol. Rev."},{"key":"10.1038\/s41385-022-00535-6_bib47","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1038\/s41556-018-0217-x","article-title":"Metabolism as a guiding force for immunity","volume":"21","author":"Jung","year":"2019","journal-title":"Nat. Cell Biol."},{"key":"10.1038\/s41385-022-00535-6_bib48","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/j.isci.2018.07.005","article-title":"Initial B Cell Activation Induces Metabolic Reprogramming and Mitochondrial Remodeling","volume":"5","author":"Waters","year":"2018","journal-title":"iScience"},{"key":"10.1038\/s41385-022-00535-6_bib49","doi-asserted-by":"crossref","first-page":"528","DOI":"10.2353\/ajpath.2010.090526","article-title":"S100A4 and metastasis: a small actor playing many roles","volume":"176","author":"Boye","year":"2010","journal-title":"Am. J. Pathol."},{"key":"10.1038\/s41385-022-00535-6_bib50","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1080\/15384101.2017.1415678","article-title":"The role of S100A4 protein in anticancer cytotoxicity: its presence is required on the surface of CD(4+)CD(25+)PGRPs(+)S100A4(+) lymphocyte and undesirable on the surface of target cells","volume":"17","author":"Dukhanina","year":"2018","journal-title":"Cell Cycle"},{"key":"10.1038\/s41385-022-00535-6_bib51","doi-asserted-by":"crossref","first-page":"3670","DOI":"10.1038\/sj.onc.1207420","article-title":"Cancer predisposition in mice deficient for the metastasis-associated Mts1(S100A4) gene","volume":"23","author":"C","year":"2004","journal-title":"Oncogene"},{"key":"10.1038\/s41385-022-00535-6_bib52","doi-asserted-by":"crossref","first-page":"294","DOI":"10.1016\/j.tibtech.2011.02.004","article-title":"Pathogen-associated molecular patterns on biomaterials: a paradigm for engineering new vaccines","volume":"29","author":"Demento","year":"2011","journal-title":"Trends Biotechnol."},{"key":"10.1038\/s41385-022-00535-6_bib53","doi-asserted-by":"crossref","first-page":"1260","DOI":"10.1593\/neo.121554","article-title":"Anti-S100A4 antibody suppresses metastasis formation by blocking stroma cell invasion","volume":"14","author":"Klingelhofer","year":"2012","journal-title":"Neoplasia"},{"key":"10.1038\/s41385-022-00535-6_bib54","doi-asserted-by":"crossref","first-page":"804","DOI":"10.4049\/jimmunol.145.3.804","article-title":"Generation of class I MHC-restricted T-T hybridomas","volume":"145","author":"Rock","year":"1990","journal-title":"J. Immunol."},{"key":"10.1038\/s41385-022-00535-6_bib55","doi-asserted-by":"crossref","first-page":"85","DOI":"10.5099\/aj120100085","article-title":"The Use of Principal Component Analysis in MALDI-TOF MS: a Powerful Tool for Establishing a Mini-optimized Proteomic Profile","volume":"4","author":"Shao","year":"2012","journal-title":"Am. J. Biomed. Sci."}],"container-title":["Mucosal Immunology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41385-022-00535-6.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41385-022-00535-6","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S1933021922000204?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S1933021922000204?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41385-022-00535-6.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,30]],"date-time":"2025-10-30T13:09:16Z","timestamp":1761829756000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S1933021922000204"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,8]]},"references-count":55,"journal-issue":{"issue":"5","published-print":{"date-parts":[[2022,8]]}},"alternative-id":["S1933021922000204"],"URL":"https:\/\/doi.org\/10.1038\/s41385-022-00535-6","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2022.01.04.474916","asserted-by":"object"}]},"ISSN":["1933-0219"],"issn-type":[{"value":"1933-0219","type":"print"}],"subject":[],"published":{"date-parts":[[2022,8]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"S100A4 exerts robust mucosal adjuvant activity for co-administered antigens in mice","name":"articletitle","label":"Article Title"},{"value":"Mucosal Immunology","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1038\/s41385-022-00535-6","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"Copyright \u00a9 2022 The Authors. Published by Elsevier Inc.","name":"copyright","label":"Copyright"}]}}