{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,22]],"date-time":"2026-07-22T17:13:53Z","timestamp":1784740433831,"version":"3.55.0"},"reference-count":27,"publisher":"Oxford University Press (OUP)","issue":"4","license":[{"start":{"date-parts":[[2024,3,23]],"date-time":"2024-03-23T00:00:00Z","timestamp":1711152000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/501100001691","name":"JSPS","doi-asserted-by":"publisher","award":["20K08846"],"award-info":[{"award-number":["20K08846"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"JSPS","doi-asserted-by":"publisher","award":["21K08287"],"award-info":[{"award-number":["21K08287"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"JSPS","doi-asserted-by":"publisher","award":["22K08338"],"award-info":[{"award-number":["22K08338"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"JSPS","doi-asserted-by":"publisher","award":["22K11786"],"award-info":[{"award-number":["22K11786"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"JSPS","doi-asserted-by":"publisher","award":["22K09553"],"award-info":[{"award-number":["22K09553"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001691","name":"JSPS","doi-asserted-by":"publisher","award":["22K08339"],"award-info":[{"award-number":["22K08339"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2024,4,8]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>It is a problem that influenza virus infection increases susceptibility to secondary bacterial infection in lungs leading to lethal pneumonia. We previously reported that exopolysaccharides (EPS) derived from Lactobacillus delbrueckii ssp. bulgaricus OLL1073R-1 (OLL1073R-1) could prevent against influenza virus infection followed by secondary bacterial infection in vitro. Therefore, the present study assessed whether EPS derived OLL1073R-1 protects the alveolar epithelial barrier disfunction caused by influenza virus infection. After A549 cells treated with EPS or without EPS were infected influenza virus A\/Puerto Rico\/8\/34 (IFV) for 12\u00a0h, the levels of tight junction genes expression and inflammatory genes expression were measured by reverse transcription polymerase chain reaction. As results, EPS treatment could protect against low-titer IFV infection, but not high-titer IFV infection, followed by suppression of the increased expression of inflammatory cytokine gene levels and recovery of the decrease in the expression level of ZO-1 gene that was caused by low-titer IFV infection, leading to an improvement trend in the barrier function. Our findings showed that EPS derived from OLL1073R-1 could inhibit low-titer IFV infection leading to maintenance of the epithelial barrier function through the suppression of inflammatory cytokine genes expression.<\/jats:p>","DOI":"10.1093\/lambio\/ovae029","type":"journal-article","created":{"date-parts":[[2024,3,22]],"date-time":"2024-03-22T07:27:53Z","timestamp":1711092473000},"source":"Crossref","is-referenced-by-count":2,"title":["<i>In vitro<\/i> investigation of the effects of <i>Lactobacillus delbrueckii<\/i> ssp. <i>bulgaricus<\/i> OLL1073R-1 exopolysaccharides on tight junction damage caused by influenza virus infection"],"prefix":"10.1093","volume":"77","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4892-9778","authenticated-orcid":false,"given":"Hiroki","family":"Ishikawa","sequence":"first","affiliation":[{"name":"Department of Microbiology and Immunology, Showa University School of Medicine , Shinagawa-ku, Tokyo, 142-8555 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yoshihiro","family":"Kuno","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, Showa University School of Medicine , Shinagawa-ku, Tokyo, 142-8555 , Japan"},{"name":"Division of Nephrology, Department of Medicine, Showa University School of Medicine , Shinagawa-ku, Tokyo, 142-8666 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Takehiro","family":"Yokoo","sequence":"additional","affiliation":[{"name":"Food Microbiology and Function Research Laboratories, R&D Division, Meiji Co., Ltd , Hachioji, Tokyo, 192-0919 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ryuichi","family":"Nagashima","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, Showa University School of Medicine , Shinagawa-ku, Tokyo, 142-8555 , Japan"},{"name":"Division of Immunology, Department of Biosciences, Kitasato University School of Science , Sagamihara, Kanagawa, 252-0373 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Takashi","family":"Takaki","sequence":"additional","affiliation":[{"name":"Division of Electron Microscopy,Showa University , Shinagawa-ku, Tokyo, 142-8555 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hiraku","family":"Sasaki","sequence":"additional","affiliation":[{"name":"Department of Health Science, Faculty of Health and Sports Science, Juntendo University , Inzai, Chiba, 270-1695 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chikara","family":"Kohda","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, Showa University School of Medicine , Shinagawa-ku, Tokyo, 142-8555 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Masayuki","family":"Iyoda","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, Showa University School of Medicine , Shinagawa-ku, Tokyo, 142-8555 , Japan"},{"name":"Division of Nephrology, Department of Medicine, Showa University School of Medicine , Shinagawa-ku, Tokyo, 142-8666 , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2024,3,23]]},"reference":[{"key":"2024041308550776100_bib1","doi-asserted-by":"crossref","first-page":"3877","DOI":"10.1007\/s00253-016-7471-2","article-title":"Exopolysaccharides produced by lactic acid bacteria: from health-promoting benefits to stress tolerance mechanisms","volume":"100","author":"Caggianiello","year":"2016","journal-title":"Appl Microbiol Biotechnol"},{"key":"2024041308550776100_bib2","doi-asserted-by":"crossref","first-page":"C1002","DOI":"10.1152\/ajpcell.00175.2005","article-title":"Inducible expression of snail selectively increases paracellular ion permeability and differentially modulates tight junction proteins","volume":"289","author":"Carrozzino","year":"2005","journal-title":"Am J Physiol Cell Physiol"},{"key":"2024041308550776100_bib3","doi-asserted-by":"crossref","first-page":"1915","DOI":"10.1002\/glia.22857","article-title":"Disruption of in vitro endothelial barrier integrity by Japanese encephalitis virus-infected astrocytes","volume":"63","author":"Chang","year":"2015","journal-title":"Glia"},{"key":"2024041308550776100_bib4","doi-asserted-by":"crossref","first-page":"1150","DOI":"10.1128\/JVI.02738-13","article-title":"Infection of pericytes in vitro by Japanese encephalitis virus disrupts the integrity of the endothelial barrier","volume":"88","author":"Chen","year":"2014","journal-title":"J Virol"},{"key":"2024041308550776100_bib5","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1016\/j.jinf.2012.04.009","article-title":"Bacterial co-infection with H1N1 infection in patients admitted with community acquired pneumonia","volume":"65","author":"Cilloniz","year":"2012","journal-title":"J Infect"},{"key":"2024041308550776100_bib6","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1111\/j.1365-2672.1989.tb05105.x","article-title":"Probiotics in man and animals","volume":"66","author":"Fuller","year":"1989","journal-title":"J Appl Bacteriol"},{"key":"2024041308550776100_bib7","doi-asserted-by":"crossref","first-page":"32","DOI":"10.21037\/atm.2017.12.18","article-title":"New insights into the mechanisms of pulmonary edema in acute lung injury","volume":"6","author":"Herrero","year":"2018","journal-title":"Ann Transl Med"},{"key":"2024041308550776100_bib8","doi-asserted-by":"crossref","first-page":"632","DOI":"10.1111\/lam.13649","article-title":"Exopolysaccharides from Lactobacillus delbrueckii ssp. bulgaricus OLL1073R-1 prevent influenza virus infection and attenuate secondary bacterial infection risk","volume":"74","author":"Ishikawa","year":"2022","journal-title":"Lett Appl Microbiol"},{"key":"2024041308550776100_bib9","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1111\/cei.13042","article-title":"Respiratory syncytial virus infection influences tight junction integrity","volume":"190","author":"Kast","year":"2017","journal-title":"Clin Exp Immunol"},{"key":"2024041308550776100_bib10","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1196\/annals.1443.020","article-title":"Toll-like receptor and RIG-I-like receptor signaling","volume":"1143","author":"Kawai","year":"2008","journal-title":"Ann N Y Acad Sci"},{"key":"2024041308550776100_bib11","doi-asserted-by":"crossref","first-page":"5702","DOI":"10.3168\/jds.2017-14151","article-title":"Exopolysaccharide from Lactobacillus plantarum LRCC5310 offers protection against rotavirus-induced diarrhea and regulates inflammatory response","volume":"101","author":"Kim","year":"2018","journal-title":"J Dairy Sci"},{"key":"2024041308550776100_bib12","doi-asserted-by":"crossref","first-page":"1335","DOI":"10.4014\/jmb.1906.06064","article-title":"Role of probiotics in human gut microbiome-associated diseases","volume":"29","author":"Kim","year":"2019","journal-title":"J Microbiol Biotechnol"},{"key":"2024041308550776100_bib13","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1167\/iovs.07-0419","article-title":"Delayed disruption of barrier function in cultured human corneal epithelial cells induced by tumor necrosis factor-alpha in a manner dependent on NF-kappaB","volume":"49","author":"Kimura","year":"2008","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"2024041308550776100_bib14","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1167\/iovs.08-2606","article-title":"Interleukin-1beta-induced disruption of barrier function in cultured human corneal epithelial cells","volume":"50","author":"Kimura","year":"2009","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"2024041308550776100_bib15","doi-asserted-by":"crossref","first-page":"1883965","DOI":"10.1080\/21688370.2021.1883965","article-title":"Airway tight junctions as targets of viral infections","volume":"9","author":"Linfield","year":"2021","journal-title":"Tissue Barriers"},{"key":"2024041308550776100_bib16","doi-asserted-by":"crossref","first-page":"2873","DOI":"10.3168\/jds.S0022-0302(06)72560-7","article-title":"Immunomodulatory effects of polysaccharides produced by Lactobacillus delbrueckii ssp. bulgaricus OLL1073R-1","volume":"89","author":"Makino","year":"2006","journal-title":"J Dairy Sci"},{"key":"2024041308550776100_bib17","doi-asserted-by":"crossref","first-page":"915","DOI":"10.3168\/jds.2015-10376","article-title":"Enhanced natural killer cell activation by exopolysaccharides derived from yogurt fermented with Lactobacillus delbrueckii ssp. bulgaricus OLL1073R-1","volume":"99","author":"Makino","year":"2016","journal-title":"J Dairy Sci"},{"key":"2024041308550776100_bib18","first-page":"519","article-title":"In vitro and in vivo effects of Peganum harmala L. seeds extract against influenza a virus","volume":"7","author":"Moradi","year":"2017","journal-title":"Avicenna J Phytomed"},{"key":"2024041308550776100_bib19","doi-asserted-by":"crossref","first-page":"2246","DOI":"10.1016\/j.intimp.2011.09.012","article-title":"Effects of oral administration of yogurt fermented with Lactobacillus delbrueckii ssp. bulgaricus OLL1073R-1 and its exopolysaccharides against influenza virus infection in mice","volume":"11","author":"Nagai","year":"2011","journal-title":"Int Immunopharmacol"},{"key":"2024041308550776100_bib20","doi-asserted-by":"crossref","first-page":"697","DOI":"10.1016\/S0140-6736(17)30129-0","article-title":"Influenza","volume":"390","author":"Paules","year":"2017","journal-title":"Lancet"},{"key":"2024041308550776100_bib21","doi-asserted-by":"crossref","first-page":"679","DOI":"10.3390\/v12060679","article-title":"Host-pathogen responses to pandemic influenza H1N1pdm09 in a human respiratory airway model","volume":"12","author":"Pharo","year":"2020","journal-title":"Viruses"},{"key":"2024041308550776100_bib22","doi-asserted-by":"crossref","first-page":"107801","DOI":"10.1016\/j.celrep.2020.107801","article-title":"H1N1 Influenza virus cross-activates Gli1 to disrupt the intercellular junctions of alveolar epithelial cells","volume":"31","author":"Ruan","year":"2020","journal-title":"Cell Rep"},{"key":"2024041308550776100_bib23","doi-asserted-by":"crossref","first-page":"4891","DOI":"10.3390\/molecules25214891","article-title":"Probiotics in treatment of viral respiratory infections and neuroinflammatory disorders","volume":"25","author":"Shahbazi","year":"2020","journal-title":"Molecules"},{"key":"2024041308550776100_bib24","doi-asserted-by":"crossref","first-page":"954","DOI":"10.1183\/13993003.01282-2015","article-title":"Influenza virus damages the alveolar barrier by disrupting epithelial cell tight junctions","volume":"47","author":"Short","year":"2016","journal-title":"Eur Respir J"},{"key":"2024041308550776100_bib25","doi-asserted-by":"crossref","first-page":"5145","DOI":"10.3390\/v7092865","article-title":"Tight junctions go viral!","volume":"7","author":"Torres-Flores","year":"2015","journal-title":"Viruses"},{"key":"2024041308550776100_bib26","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1111\/j.1749-6632.2009.04056.x","article-title":"Roles of ZO-1 and ZO-2 in establishment of the belt-like adherens and tight junctions with paracellular permselective barrier function","volume":"1165","author":"Tsukita","year":"2009","journal-title":"Ann N Y Acad Sci"},{"key":"2024041308550776100_bib27","doi-asserted-by":"crossref","first-page":"416","DOI":"10.1016\/j.ccr.2009.03.016","article-title":"Stabilization of snail by NF-kappaB is required for inflammation-induced cell migration and invasion","volume":"15","author":"Wu","year":"2009","journal-title":"Cancer Cell"}],"container-title":["Letters in Applied Microbiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/lambio\/advance-article-pdf\/doi\/10.1093\/lambio\/ovae029\/57076054\/ovae029.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/lambio\/article-pdf\/77\/4\/ovae029\/57228053\/ovae029.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/lambio\/article-pdf\/77\/4\/ovae029\/57228053\/ovae029.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,4,13]],"date-time":"2024-04-13T08:55:21Z","timestamp":1712998521000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/lambio\/article\/doi\/10.1093\/lambio\/ovae029\/7634354"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,3,23]]},"references-count":27,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2024,4,8]]}},"URL":"https:\/\/doi.org\/10.1093\/lambio\/ovae029","relation":{},"ISSN":["1472-765X"],"issn-type":[{"value":"1472-765X","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2024,4]]},"published":{"date-parts":[[2024,3,23]]},"article-number":"ovae029"}}