Dietary soyasaponin attenuates 2,4‐dinitrofluorobenzene‐induced contact hypersensitivity via gut microbiota in mice
Summary Soyasaponins (SSs) are abundant in soybeans and display inhibitory activity against contact hypersensitivity (CHS), which is often used as a mouse model for allergic contact dermatitis (ACD); however, their therapeutic mechanisms remain unknown. Here, we attempted to clarify the role of gut...
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| Veröffentlicht in: | Clinical and experimental immunology 2019-01, Vol.195 (1), p.86-95 |
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Soyasaponins (SSs) are abundant in soybeans and display inhibitory activity against contact hypersensitivity (CHS), which is often used as a mouse model for allergic contact dermatitis (ACD); however, their therapeutic mechanisms remain unknown. Here, we attempted to clarify the role of gut microbiota in the inhibition of CHS by dietary soyasaponins. For antibiotic treatment, mice were administered a mixture of ciprofloxacin and metronidazole or vancomycin. These antibiotics and SSs were given to mice via drinking water 3‐weeks prior to CHS induction with 2,4‐dinitrofluorobenzene, and the mice were analysed for ear swelling, tissue oedema, infiltration of Gr‐1‐positive immune cells, the composition of faecal microbiota and regulatory T (Treg) cells. The soyasaponin diets attenuated ear swelling and tissue oedema, and reduced the number of Gr‐1‐positive cells infiltrating ear tissues. CHS caused changes in the structure of the gut microbiota, but dietary SSs blocked the changes in the microbiota composition. Ciprofloxacin and metronidazole treatments significantly enhanced the severity of CHS symptoms, whereas vancomycin treatment blocked the suppressive effect of dietary SSs on CHS. These antibiotic treatments differed in their effects on the gut microbiota composition. Treg cells in auricular lymph node and spleen increased under SS‐enriched diets, but this increase was blocked by vancomycin treatment. These results suggest that dietary SSs exert their inhibitory activity on CHS via the gut microbiota in mice, suggesting that dietary supplementation with SSs may have beneficial effects on ACD patients, but that the gut microbiota is a critical determinant of the therapeutic value of dietary SSs.
"Vancomycin treatment alters the gut microbiota composition and reduces regulatory T (Treg) cells in soyasaponin (SS)‐treated mice with contact hypersensitivity (CHS). The gut microbiota composition was analysed by sequencing the bacterial 16S ribosomal RNA gene, indicating principal component analysis (PCA) (a) and taxonomic distribution (b) at the family level. Treg cells in auricular lymph node (c) and spleen (d). CC, CHS control group; VC, vancomycin‐treated group; SS, SS‐treated group; VS, vancomycin and SS‐treated group. The data are presented as the means ± SEM; *P |
| doi_str_mv | 10.1111/cei.13212 |
| format | Article |
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Soyasaponins (SSs) are abundant in soybeans and display inhibitory activity against contact hypersensitivity (CHS), which is often used as a mouse model for allergic contact dermatitis (ACD); however, their therapeutic mechanisms remain unknown. Here, we attempted to clarify the role of gut microbiota in the inhibition of CHS by dietary soyasaponins. For antibiotic treatment, mice were administered a mixture of ciprofloxacin and metronidazole or vancomycin. These antibiotics and SSs were given to mice via drinking water 3‐weeks prior to CHS induction with 2,4‐dinitrofluorobenzene, and the mice were analysed for ear swelling, tissue oedema, infiltration of Gr‐1‐positive immune cells, the composition of faecal microbiota and regulatory T (Treg) cells. The soyasaponin diets attenuated ear swelling and tissue oedema, and reduced the number of Gr‐1‐positive cells infiltrating ear tissues. CHS caused changes in the structure of the gut microbiota, but dietary SSs blocked the changes in the microbiota composition. Ciprofloxacin and metronidazole treatments significantly enhanced the severity of CHS symptoms, whereas vancomycin treatment blocked the suppressive effect of dietary SSs on CHS. These antibiotic treatments differed in their effects on the gut microbiota composition. Treg cells in auricular lymph node and spleen increased under SS‐enriched diets, but this increase was blocked by vancomycin treatment. These results suggest that dietary SSs exert their inhibitory activity on CHS via the gut microbiota in mice, suggesting that dietary supplementation with SSs may have beneficial effects on ACD patients, but that the gut microbiota is a critical determinant of the therapeutic value of dietary SSs.
"Vancomycin treatment alters the gut microbiota composition and reduces regulatory T (Treg) cells in soyasaponin (SS)‐treated mice with contact hypersensitivity (CHS). The gut microbiota composition was analysed by sequencing the bacterial 16S ribosomal RNA gene, indicating principal component analysis (PCA) (a) and taxonomic distribution (b) at the family level. Treg cells in auricular lymph node (c) and spleen (d). CC, CHS control group; VC, vancomycin‐treated group; SS, SS‐treated group; VS, vancomycin and SS‐treated group. The data are presented as the means ± SEM; *P<0.05, **P<0.01."</description><identifier>ISSN: 0009-9104</identifier><identifier>EISSN: 1365-2249</identifier><identifier>DOI: 10.1111/cei.13212</identifier><identifier>PMID: 30178467</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>allergic contact dermatitis ; Animals ; Anti-Bacterial Agents - therapeutic use ; Antibiotics ; Cells, Cultured ; Ciprofloxacin ; Contact dermatitis ; contact hypersensitivity ; Dermatitis ; Dermatitis, Allergic Contact - therapy ; Dermatitis, Contact - therapy ; Diet ; Dietary supplements ; Dinitrofluorobenzene ; Dinitrofluorobenzene - analogs & derivatives ; Disease Models, Animal ; Drinking water ; Ear ; Eczema ; Edema ; Female ; Gastrointestinal Microbiome - immunology ; Glycine max - immunology ; gut microbiota ; Humans ; Hypersensitivity ; Intestinal microflora ; Lymph nodes ; Lymphocytes T ; Metronidazole ; Mice ; Mice, Inbred BALB C ; Microbiota ; Original ; regulatory T cell ; Saponins - therapeutic use ; Soyasaponin ; Soybeans ; Spleen ; T-Lymphocytes, Regulatory - immunology ; Tissues ; Vancomycin</subject><ispartof>Clinical and experimental immunology, 2019-01, Vol.195 (1), p.86-95</ispartof><rights>2018 British Society for Immunology</rights><rights>2018 British Society for Immunology.</rights><rights>2019 British Society for Immunology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5092-b8d355537f0248a99466bd414df0321b6cb824964a3b8d5c0247df3eb40afe103</citedby><cites>FETCH-LOGICAL-c5092-b8d355537f0248a99466bd414df0321b6cb824964a3b8d5c0247df3eb40afe103</cites><orcidid>0000-0002-6105-8703</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6300654/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6300654/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30178467$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Nagano, T.</creatorcontrib><creatorcontrib>Katase, M.</creatorcontrib><creatorcontrib>Tsumura, K.</creatorcontrib><title>Dietary soyasaponin attenuates 2,4‐dinitrofluorobenzene‐induced contact hypersensitivity via gut microbiota in mice</title><title>Clinical and experimental immunology</title><addtitle>Clin Exp Immunol</addtitle><description>Summary
Soyasaponins (SSs) are abundant in soybeans and display inhibitory activity against contact hypersensitivity (CHS), which is often used as a mouse model for allergic contact dermatitis (ACD); however, their therapeutic mechanisms remain unknown. Here, we attempted to clarify the role of gut microbiota in the inhibition of CHS by dietary soyasaponins. For antibiotic treatment, mice were administered a mixture of ciprofloxacin and metronidazole or vancomycin. These antibiotics and SSs were given to mice via drinking water 3‐weeks prior to CHS induction with 2,4‐dinitrofluorobenzene, and the mice were analysed for ear swelling, tissue oedema, infiltration of Gr‐1‐positive immune cells, the composition of faecal microbiota and regulatory T (Treg) cells. The soyasaponin diets attenuated ear swelling and tissue oedema, and reduced the number of Gr‐1‐positive cells infiltrating ear tissues. CHS caused changes in the structure of the gut microbiota, but dietary SSs blocked the changes in the microbiota composition. Ciprofloxacin and metronidazole treatments significantly enhanced the severity of CHS symptoms, whereas vancomycin treatment blocked the suppressive effect of dietary SSs on CHS. These antibiotic treatments differed in their effects on the gut microbiota composition. Treg cells in auricular lymph node and spleen increased under SS‐enriched diets, but this increase was blocked by vancomycin treatment. These results suggest that dietary SSs exert their inhibitory activity on CHS via the gut microbiota in mice, suggesting that dietary supplementation with SSs may have beneficial effects on ACD patients, but that the gut microbiota is a critical determinant of the therapeutic value of dietary SSs.
"Vancomycin treatment alters the gut microbiota composition and reduces regulatory T (Treg) cells in soyasaponin (SS)‐treated mice with contact hypersensitivity (CHS). The gut microbiota composition was analysed by sequencing the bacterial 16S ribosomal RNA gene, indicating principal component analysis (PCA) (a) and taxonomic distribution (b) at the family level. Treg cells in auricular lymph node (c) and spleen (d). CC, CHS control group; VC, vancomycin‐treated group; SS, SS‐treated group; VS, vancomycin and SS‐treated group. The data are presented as the means ± SEM; *P<0.05, **P<0.01."</description><subject>allergic contact dermatitis</subject><subject>Animals</subject><subject>Anti-Bacterial Agents - therapeutic use</subject><subject>Antibiotics</subject><subject>Cells, Cultured</subject><subject>Ciprofloxacin</subject><subject>Contact dermatitis</subject><subject>contact hypersensitivity</subject><subject>Dermatitis</subject><subject>Dermatitis, Allergic Contact - therapy</subject><subject>Dermatitis, Contact - therapy</subject><subject>Diet</subject><subject>Dietary supplements</subject><subject>Dinitrofluorobenzene</subject><subject>Dinitrofluorobenzene - analogs & derivatives</subject><subject>Disease Models, Animal</subject><subject>Drinking water</subject><subject>Ear</subject><subject>Eczema</subject><subject>Edema</subject><subject>Female</subject><subject>Gastrointestinal Microbiome - immunology</subject><subject>Glycine max - immunology</subject><subject>gut microbiota</subject><subject>Humans</subject><subject>Hypersensitivity</subject><subject>Intestinal microflora</subject><subject>Lymph nodes</subject><subject>Lymphocytes T</subject><subject>Metronidazole</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Microbiota</subject><subject>Original</subject><subject>regulatory T cell</subject><subject>Saponins - therapeutic use</subject><subject>Soyasaponin</subject><subject>Soybeans</subject><subject>Spleen</subject><subject>T-Lymphocytes, Regulatory - immunology</subject><subject>Tissues</subject><subject>Vancomycin</subject><issn>0009-9104</issn><issn>1365-2249</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kU1uFDEQhS1ERIbAggsgS6yQ6MT_071BiiYBIkViA2vL7a5OHM3Yg-2eqFnlCJyRk1AwSQQLvLHK_vyqnh8hrzg75rhOPIRjLgUXT8iCS6MbIVT3lCwYY13TcaYOyfNSbrA0xohn5FAyvmyVWS7I7VmA6vJMS5pdcdsUQ6SuVoiTq1CoeKd-3v0YQgw1p3E9pZx6iN8hAh6HOEweBupTrM5Xej1vIReIJdSwC3Wmu-Do1VTpJnh8F1J1FOWxghfkYHTrAi_v9yPy9cP5l9Wn5vLzx4vV6WXjNetE07eD1FrL5ciEal3XKWP6QXE1jAwN98b3LXo1yklEtUdqOYwSesXcCJzJI_J-r7ud-g0MHmLNbm23OWzQtU0u2H9vYri2V2lnjcTf0goF3twL5PRtglLtTZpyxJmt4LpVTOhWIvV2T6HPUjKMjx04s78zspiR_ZMRsq__HumRfAgFgZM9cBvWMP9fya7OL_aSvwDLcaBR</recordid><startdate>201901</startdate><enddate>201901</enddate><creator>Nagano, T.</creator><creator>Katase, M.</creator><creator>Tsumura, K.</creator><general>Oxford University Press</general><general>John Wiley and Sons Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7T5</scope><scope>7U9</scope><scope>H94</scope><scope>M7N</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-6105-8703</orcidid></search><sort><creationdate>201901</creationdate><title>Dietary soyasaponin attenuates 2,4‐dinitrofluorobenzene‐induced contact hypersensitivity via gut microbiota in mice</title><author>Nagano, T. ; Katase, M. ; Tsumura, K.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5092-b8d355537f0248a99466bd414df0321b6cb824964a3b8d5c0247df3eb40afe103</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>allergic contact dermatitis</topic><topic>Animals</topic><topic>Anti-Bacterial Agents - therapeutic use</topic><topic>Antibiotics</topic><topic>Cells, Cultured</topic><topic>Ciprofloxacin</topic><topic>Contact dermatitis</topic><topic>contact hypersensitivity</topic><topic>Dermatitis</topic><topic>Dermatitis, Allergic Contact - therapy</topic><topic>Dermatitis, Contact - therapy</topic><topic>Diet</topic><topic>Dietary supplements</topic><topic>Dinitrofluorobenzene</topic><topic>Dinitrofluorobenzene - analogs & derivatives</topic><topic>Disease Models, Animal</topic><topic>Drinking water</topic><topic>Ear</topic><topic>Eczema</topic><topic>Edema</topic><topic>Female</topic><topic>Gastrointestinal Microbiome - immunology</topic><topic>Glycine max - immunology</topic><topic>gut microbiota</topic><topic>Humans</topic><topic>Hypersensitivity</topic><topic>Intestinal microflora</topic><topic>Lymph nodes</topic><topic>Lymphocytes T</topic><topic>Metronidazole</topic><topic>Mice</topic><topic>Mice, Inbred BALB C</topic><topic>Microbiota</topic><topic>Original</topic><topic>regulatory T cell</topic><topic>Saponins - therapeutic use</topic><topic>Soyasaponin</topic><topic>Soybeans</topic><topic>Spleen</topic><topic>T-Lymphocytes, Regulatory - immunology</topic><topic>Tissues</topic><topic>Vancomycin</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Nagano, T.</creatorcontrib><creatorcontrib>Katase, M.</creatorcontrib><creatorcontrib>Tsumura, K.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Immunology Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Clinical and experimental immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Nagano, T.</au><au>Katase, M.</au><au>Tsumura, K.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dietary soyasaponin attenuates 2,4‐dinitrofluorobenzene‐induced contact hypersensitivity via gut microbiota in mice</atitle><jtitle>Clinical and experimental immunology</jtitle><addtitle>Clin Exp Immunol</addtitle><date>2019-01</date><risdate>2019</risdate><volume>195</volume><issue>1</issue><spage>86</spage><epage>95</epage><pages>86-95</pages><issn>0009-9104</issn><eissn>1365-2249</eissn><abstract>Summary
Soyasaponins (SSs) are abundant in soybeans and display inhibitory activity against contact hypersensitivity (CHS), which is often used as a mouse model for allergic contact dermatitis (ACD); however, their therapeutic mechanisms remain unknown. Here, we attempted to clarify the role of gut microbiota in the inhibition of CHS by dietary soyasaponins. For antibiotic treatment, mice were administered a mixture of ciprofloxacin and metronidazole or vancomycin. These antibiotics and SSs were given to mice via drinking water 3‐weeks prior to CHS induction with 2,4‐dinitrofluorobenzene, and the mice were analysed for ear swelling, tissue oedema, infiltration of Gr‐1‐positive immune cells, the composition of faecal microbiota and regulatory T (Treg) cells. The soyasaponin diets attenuated ear swelling and tissue oedema, and reduced the number of Gr‐1‐positive cells infiltrating ear tissues. CHS caused changes in the structure of the gut microbiota, but dietary SSs blocked the changes in the microbiota composition. Ciprofloxacin and metronidazole treatments significantly enhanced the severity of CHS symptoms, whereas vancomycin treatment blocked the suppressive effect of dietary SSs on CHS. These antibiotic treatments differed in their effects on the gut microbiota composition. Treg cells in auricular lymph node and spleen increased under SS‐enriched diets, but this increase was blocked by vancomycin treatment. These results suggest that dietary SSs exert their inhibitory activity on CHS via the gut microbiota in mice, suggesting that dietary supplementation with SSs may have beneficial effects on ACD patients, but that the gut microbiota is a critical determinant of the therapeutic value of dietary SSs.
"Vancomycin treatment alters the gut microbiota composition and reduces regulatory T (Treg) cells in soyasaponin (SS)‐treated mice with contact hypersensitivity (CHS). The gut microbiota composition was analysed by sequencing the bacterial 16S ribosomal RNA gene, indicating principal component analysis (PCA) (a) and taxonomic distribution (b) at the family level. Treg cells in auricular lymph node (c) and spleen (d). CC, CHS control group; VC, vancomycin‐treated group; SS, SS‐treated group; VS, vancomycin and SS‐treated group. The data are presented as the means ± SEM; *P<0.05, **P<0.01."</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>30178467</pmid><doi>10.1111/cei.13212</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0002-6105-8703</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | allergic contact dermatitis Animals Anti-Bacterial Agents - therapeutic use Antibiotics Cells, Cultured Ciprofloxacin Contact dermatitis contact hypersensitivity Dermatitis Dermatitis, Allergic Contact - therapy Dermatitis, Contact - therapy Diet Dietary supplements Dinitrofluorobenzene Dinitrofluorobenzene - analogs & derivatives Disease Models, Animal Drinking water Ear Eczema Edema Female Gastrointestinal Microbiome - immunology Glycine max - immunology gut microbiota Humans Hypersensitivity Intestinal microflora Lymph nodes Lymphocytes T Metronidazole Mice Mice, Inbred BALB C Microbiota Original regulatory T cell Saponins - therapeutic use Soyasaponin Soybeans Spleen T-Lymphocytes, Regulatory - immunology Tissues Vancomycin |
| title | Dietary soyasaponin attenuates 2,4‐dinitrofluorobenzene‐induced contact hypersensitivity via gut microbiota in mice |
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