Enhanced Antiinflammatory Capacity of a Lactobacillus plantarum Mutant Synthesizing Modified Teichoic Acids
Teichoic acids (TAs), and especially lipoteichoic acids (LTAs), are one of the main immunostimulatory components of pathogenic Gram-positive bacteria. Their contribution to the immunomodulatory properties of commensal bacteria and especially of lactic acid bacteria has not yet been investigated in d...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2005-07, Vol.102 (29), p.10321-10326 |
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| creator | Grangette, Corinne Nutten, Sophie Palumbo, Emmanuelle Morath, Siegfried Hermann, Corinna Dewulf, Joelle Pot, Bruno Hartung, Thomas Hols, Pascal Mercenier, Annick Klaenhammer, Todd R. |
| description | Teichoic acids (TAs), and especially lipoteichoic acids (LTAs), are one of the main immunostimulatory components of pathogenic Gram-positive bacteria. Their contribution to the immunomodulatory properties of commensal bacteria and especially of lactic acid bacteria has not yet been investigated in detail. To evaluate the role of TAs in the interaction between lactic acid bacteria and the immune system, we analyzed the antiinflammatory properties of a mutant of Lactobacillus plantarum NCIMB8826 affected in the TA biosynthesis pathway both in vitro (mononuclear cells stimulation) and in vivo (murine model of colitis). This Dlt-mutant was found to incorporate much less D-Ala in its TAs than the WT strain. This defect significantly impacted the immunomodulation reactions induced by the bacterium, as shown by a dramatically reduced secretion of proinflammatory cytokines by peripheral blood mononuclear cells and monocytes stimulated by the Dlt-mutant as compared with the parental strain. Concomitantly, a significant increase in IL-10 production was stimulated by the Dlt-mutant in comparison with the WT strain. Moreover, the proinflammatory capacity of L. plantarum-purified LTA was found to be Toll-like receptor 2-dependent. Consistent with the in vitro results, the Dlt-mutant was significantly more protective in a murine colitis model than its WT counterpart. The results indicated that composition of LTA within the whole-cell context of L. plantarum can modulate proinflammatory or antiinflammatory immune responses. |
| doi_str_mv | 10.1073/pnas.0504084102 |
| format | Article |
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Their contribution to the immunomodulatory properties of commensal bacteria and especially of lactic acid bacteria has not yet been investigated in detail. To evaluate the role of TAs in the interaction between lactic acid bacteria and the immune system, we analyzed the antiinflammatory properties of a mutant of Lactobacillus plantarum NCIMB8826 affected in the TA biosynthesis pathway both in vitro (mononuclear cells stimulation) and in vivo (murine model of colitis). This Dlt-mutant was found to incorporate much less D-Ala in its TAs than the WT strain. This defect significantly impacted the immunomodulation reactions induced by the bacterium, as shown by a dramatically reduced secretion of proinflammatory cytokines by peripheral blood mononuclear cells and monocytes stimulated by the Dlt-mutant as compared with the parental strain. Concomitantly, a significant increase in IL-10 production was stimulated by the Dlt-mutant in comparison with the WT strain. Moreover, the proinflammatory capacity of L. plantarum-purified LTA was found to be Toll-like receptor 2-dependent. Consistent with the in vitro results, the Dlt-mutant was significantly more protective in a murine colitis model than its WT counterpart. The results indicated that composition of LTA within the whole-cell context of L. plantarum can modulate proinflammatory or antiinflammatory immune responses.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.0504084102</identifier><identifier>PMID: 15985548</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Analysis of Variance ; Animals ; Anti-Inflammatory Agents - therapeutic use ; Antiinflammatories ; Bacteria ; Biological Sciences ; Bone marrow cells ; Cloning, Molecular ; Colitis ; Colitis - drug therapy ; Colitis - metabolism ; Cytokines ; Cytokines - metabolism ; DNA Primers ; Genetic Vectors - genetics ; Humans ; Immune system ; Immunologic Factors - therapeutic use ; Immunology ; Lactobacillus plantarum - genetics ; Lactobacillus plantarum - immunology ; Lactobacillus plantarum - metabolism ; Leukocytes, Mononuclear - metabolism ; Lipopolysaccharides - biosynthesis ; Lipopolysaccharides - therapeutic use ; Membrane Transport Proteins - genetics ; Mice ; Mice, Inbred BALB C ; Microbiology ; Monocytes ; Mutation ; Mutation - genetics ; Pathogens ; Saliva - microbiology ; Secretion ; Teichoic acids ; Teichoic Acids - biosynthesis ; Teichoic Acids - therapeutic use</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2005-07, Vol.102 (29), p.10321-10326</ispartof><rights>Copyright 1993/2005 The National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Jul 19, 2005</rights><rights>Copyright © 2005, The National Academy of Sciences 2005</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4442-6b7639103835376293e14e0070992f810a2882f072099dc41e31d4434d5abca3</citedby><cites>FETCH-LOGICAL-c4442-6b7639103835376293e14e0070992f810a2882f072099dc41e31d4434d5abca3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/102/29.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/3375974$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/3375974$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27901,27902,53766,53768,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/15985548$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Grangette, Corinne</creatorcontrib><creatorcontrib>Nutten, Sophie</creatorcontrib><creatorcontrib>Palumbo, Emmanuelle</creatorcontrib><creatorcontrib>Morath, Siegfried</creatorcontrib><creatorcontrib>Hermann, Corinna</creatorcontrib><creatorcontrib>Dewulf, Joelle</creatorcontrib><creatorcontrib>Pot, Bruno</creatorcontrib><creatorcontrib>Hartung, Thomas</creatorcontrib><creatorcontrib>Hols, Pascal</creatorcontrib><creatorcontrib>Mercenier, Annick</creatorcontrib><creatorcontrib>Klaenhammer, Todd R.</creatorcontrib><title>Enhanced Antiinflammatory Capacity of a Lactobacillus plantarum Mutant Synthesizing Modified Teichoic Acids</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Teichoic acids (TAs), and especially lipoteichoic acids (LTAs), are one of the main immunostimulatory components of pathogenic Gram-positive bacteria. Their contribution to the immunomodulatory properties of commensal bacteria and especially of lactic acid bacteria has not yet been investigated in detail. To evaluate the role of TAs in the interaction between lactic acid bacteria and the immune system, we analyzed the antiinflammatory properties of a mutant of Lactobacillus plantarum NCIMB8826 affected in the TA biosynthesis pathway both in vitro (mononuclear cells stimulation) and in vivo (murine model of colitis). This Dlt-mutant was found to incorporate much less D-Ala in its TAs than the WT strain. This defect significantly impacted the immunomodulation reactions induced by the bacterium, as shown by a dramatically reduced secretion of proinflammatory cytokines by peripheral blood mononuclear cells and monocytes stimulated by the Dlt-mutant as compared with the parental strain. Concomitantly, a significant increase in IL-10 production was stimulated by the Dlt-mutant in comparison with the WT strain. Moreover, the proinflammatory capacity of L. plantarum-purified LTA was found to be Toll-like receptor 2-dependent. Consistent with the in vitro results, the Dlt-mutant was significantly more protective in a murine colitis model than its WT counterpart. The results indicated that composition of LTA within the whole-cell context of L. plantarum can modulate proinflammatory or antiinflammatory immune responses.</description><subject>Analysis of Variance</subject><subject>Animals</subject><subject>Anti-Inflammatory Agents - therapeutic use</subject><subject>Antiinflammatories</subject><subject>Bacteria</subject><subject>Biological Sciences</subject><subject>Bone marrow cells</subject><subject>Cloning, Molecular</subject><subject>Colitis</subject><subject>Colitis - drug therapy</subject><subject>Colitis - metabolism</subject><subject>Cytokines</subject><subject>Cytokines - metabolism</subject><subject>DNA Primers</subject><subject>Genetic Vectors - genetics</subject><subject>Humans</subject><subject>Immune system</subject><subject>Immunologic Factors - therapeutic use</subject><subject>Immunology</subject><subject>Lactobacillus plantarum - genetics</subject><subject>Lactobacillus plantarum - immunology</subject><subject>Lactobacillus plantarum - metabolism</subject><subject>Leukocytes, Mononuclear - metabolism</subject><subject>Lipopolysaccharides - biosynthesis</subject><subject>Lipopolysaccharides - therapeutic use</subject><subject>Membrane Transport Proteins - genetics</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Microbiology</subject><subject>Monocytes</subject><subject>Mutation</subject><subject>Mutation - genetics</subject><subject>Pathogens</subject><subject>Saliva - microbiology</subject><subject>Secretion</subject><subject>Teichoic acids</subject><subject>Teichoic Acids - biosynthesis</subject><subject>Teichoic Acids - therapeutic use</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2005</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkk1vEzEQhi0EoqFw5oKQxQGJw7bjj13bl0pRVD6kVBzI3XK83sZh1w5rLyL8ehwlaoBLTzMaP_PKM-8g9JrAFQHBrnfBpCuogYPkBOgTNCOgSNVwBU_RDICKSnLKL9CLlLYAoGoJz9EFqZWsay5n6Ptt2JhgXYvnIXsfut4Mg8lx3OOF2Rnr8x7HDhu8NDbHdSn0_ZTwrjchm3Ea8N2US4q_7UPeuOR_-3CP72LrO180V87bTfQWz61v00v0rDN9cq9O8RKtPt6uFp-r5ddPXxbzZWU557Rq1qJhigCTrGaioYo5wh2AAKVoJwkYKiXtQNBSaC0njpGWc8bb2qytYZfo5ii7m9aDa60LeTS93o1-MONeR-P1vy_Bb_R9_KkJEYIpKALvTwJj_DG5lPXgk3V9mdnFKelGQtlfQx4FiWi4aBQr4Lv_wG2cxlCWoCkQTljNmwJdHyE7xpRG1z18mYA-uK0Pbuuz26Xj7d-TnvmTvQX4cAIOnWc5qqkqgVGiu6nvs_uVC4sfYQvy5ohsU7mQB4YxUSvB2R-SjMfH</recordid><startdate>20050719</startdate><enddate>20050719</enddate><creator>Grangette, Corinne</creator><creator>Nutten, Sophie</creator><creator>Palumbo, Emmanuelle</creator><creator>Morath, Siegfried</creator><creator>Hermann, Corinna</creator><creator>Dewulf, Joelle</creator><creator>Pot, Bruno</creator><creator>Hartung, Thomas</creator><creator>Hols, Pascal</creator><creator>Mercenier, Annick</creator><creator>Klaenhammer, Todd R.</creator><general>National Academy of Sciences</general><general>National Acad Sciences</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20050719</creationdate><title>Enhanced Antiinflammatory Capacity of a Lactobacillus plantarum Mutant Synthesizing Modified Teichoic Acids</title><author>Grangette, Corinne ; 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Their contribution to the immunomodulatory properties of commensal bacteria and especially of lactic acid bacteria has not yet been investigated in detail. To evaluate the role of TAs in the interaction between lactic acid bacteria and the immune system, we analyzed the antiinflammatory properties of a mutant of Lactobacillus plantarum NCIMB8826 affected in the TA biosynthesis pathway both in vitro (mononuclear cells stimulation) and in vivo (murine model of colitis). This Dlt-mutant was found to incorporate much less D-Ala in its TAs than the WT strain. This defect significantly impacted the immunomodulation reactions induced by the bacterium, as shown by a dramatically reduced secretion of proinflammatory cytokines by peripheral blood mononuclear cells and monocytes stimulated by the Dlt-mutant as compared with the parental strain. Concomitantly, a significant increase in IL-10 production was stimulated by the Dlt-mutant in comparison with the WT strain. Moreover, the proinflammatory capacity of L. plantarum-purified LTA was found to be Toll-like receptor 2-dependent. Consistent with the in vitro results, the Dlt-mutant was significantly more protective in a murine colitis model than its WT counterpart. The results indicated that composition of LTA within the whole-cell context of L. plantarum can modulate proinflammatory or antiinflammatory immune responses.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>15985548</pmid><doi>10.1073/pnas.0504084102</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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| source | Jstor Complete Legacy; MEDLINE; PubMed Central; Alma/SFX Local Collection; Free Full-Text Journals in Chemistry |
| subjects | Analysis of Variance Animals Anti-Inflammatory Agents - therapeutic use Antiinflammatories Bacteria Biological Sciences Bone marrow cells Cloning, Molecular Colitis Colitis - drug therapy Colitis - metabolism Cytokines Cytokines - metabolism DNA Primers Genetic Vectors - genetics Humans Immune system Immunologic Factors - therapeutic use Immunology Lactobacillus plantarum - genetics Lactobacillus plantarum - immunology Lactobacillus plantarum - metabolism Leukocytes, Mononuclear - metabolism Lipopolysaccharides - biosynthesis Lipopolysaccharides - therapeutic use Membrane Transport Proteins - genetics Mice Mice, Inbred BALB C Microbiology Monocytes Mutation Mutation - genetics Pathogens Saliva - microbiology Secretion Teichoic acids Teichoic Acids - biosynthesis Teichoic Acids - therapeutic use |
| title | Enhanced Antiinflammatory Capacity of a Lactobacillus plantarum Mutant Synthesizing Modified Teichoic Acids |
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