The Pseudomonas aeruginosa quorum-sensing signal molecule N-(3-oxododecanoyl)-L-homoserine lactone has immunomodulatory activity
Diverse gram-negative bacterial cells communicate with each other by using diffusible N-acyl homoserine lactone (AHL) signal molecules to coordinate gene expression with cell population density. Accumulation of AHLs above a threshold concentration renders the population "quorate," and the...
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| Veröffentlicht in: | Infection and immunity 1998, Vol.66 (1), p.36-42 |
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| creator | TELFORD, G WHEELER, D WILLIAMS, P TOMKINS, P. T APPLEBY, P SEWELL, H STEWART, G. S. A. B BYCROFT, B. W PRITCHARD, D. I |
| description | Diverse gram-negative bacterial cells communicate with each other by using diffusible N-acyl homoserine lactone (AHL) signal molecules to coordinate gene expression with cell population density. Accumulation of AHLs above a threshold concentration renders the population "quorate," and the appropriate target gene is activated. In pathogenic bacteria, such as Pseudomonas aeruginosa, AHL-mediated quorum sensing is involved in the regulation of multiple virulence determinants. We therefore sought to determine whether the immune system is capable of responding to these bacterial signal molecules. Consequently the immunomodulatory properties of the AHLs N-(3-oxododecanoyl)-L-homoserine lactone (OdDHL) and N-(3-oxohexanoyl)-L-homoserine lactone (OHHL) were evaluated in murine and human leukocyte immunoassays in vitro. OdDHL, but not OHHL, inhibited lymphocyte proliferation and tumor necrosis factor alpha production by lipopolysaccharide-stimulated macrophages. Furthermore, OdDHL simultaneously and potently down-regulated the production of IL-12, a Th-1-supportive cytokine. At high concentrations (>7 x 10(-5) M) OdDHL inhibited antibody production by keyhole limpet hemocyanin-stimulated spleen cells, but at lower concentrations ( |
| doi_str_mv | 10.1128/iai.66.1.36-42.1998 |
| format | Article |
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T ; APPLEBY, P ; SEWELL, H ; STEWART, G. S. A. B ; BYCROFT, B. W ; PRITCHARD, D. I</creator><creatorcontrib>TELFORD, G ; WHEELER, D ; WILLIAMS, P ; TOMKINS, P. T ; APPLEBY, P ; SEWELL, H ; STEWART, G. S. A. B ; BYCROFT, B. W ; PRITCHARD, D. I</creatorcontrib><description>Diverse gram-negative bacterial cells communicate with each other by using diffusible N-acyl homoserine lactone (AHL) signal molecules to coordinate gene expression with cell population density. Accumulation of AHLs above a threshold concentration renders the population "quorate," and the appropriate target gene is activated. In pathogenic bacteria, such as Pseudomonas aeruginosa, AHL-mediated quorum sensing is involved in the regulation of multiple virulence determinants. We therefore sought to determine whether the immune system is capable of responding to these bacterial signal molecules. Consequently the immunomodulatory properties of the AHLs N-(3-oxododecanoyl)-L-homoserine lactone (OdDHL) and N-(3-oxohexanoyl)-L-homoserine lactone (OHHL) were evaluated in murine and human leukocyte immunoassays in vitro. OdDHL, but not OHHL, inhibited lymphocyte proliferation and tumor necrosis factor alpha production by lipopolysaccharide-stimulated macrophages. Furthermore, OdDHL simultaneously and potently down-regulated the production of IL-12, a Th-1-supportive cytokine. At high concentrations (>7 x 10(-5) M) OdDHL inhibited antibody production by keyhole limpet hemocyanin-stimulated spleen cells, but at lower concentrations (<7 x 10(-5) M), antibody production was stimulated, apparently by increasing the proportion of the immunoglobulin G1 (IgG1) isotype. OdDHL also promoted IgE production by interleukin-4-stimulated human peripheral blood mononuclear cells. These data indicate that OdDHL may influence the Th-1-Th-2 balance in the infected host and suggest that, in addition to regulating the expression of virulence determinants, OdDHL may contribute to the pathogenesis of P. aeruginosa infections by functioning as a virulence determinant per se.</description><identifier>ISSN: 0019-9567</identifier><identifier>EISSN: 1098-5522</identifier><identifier>DOI: 10.1128/iai.66.1.36-42.1998</identifier><identifier>PMID: 9423836</identifier><identifier>CODEN: INFIBR</identifier><language>eng</language><publisher>Washington, DC: American Society for Microbiology</publisher><subject>4-Butyrolactone - analogs & derivatives ; 4-Butyrolactone - biosynthesis ; 4-Butyrolactone - immunology ; 4-Butyrolactone - isolation & purification ; Adjuvants, Immunologic ; Amino Acid Sequence ; Animals ; Bacteriology ; Biological and medical sciences ; Cell Division ; Cells, Cultured ; Concanavalin A - immunology ; Cytotoxicity Tests, Immunologic ; Female ; Fundamental and applied biological sciences. Psychology ; Fundamental immunology ; Hemocyanins - immunology ; Homoserine - analogs & derivatives ; Homoserine - biosynthesis ; Homoserine - immunology ; Homoserine - isolation & purification ; Host Response and Inflammation ; Humans ; Immunobiology ; Immunoglobulin E - biosynthesis ; Immunoglobulin G - biosynthesis ; Interleukin-12 - metabolism ; Interleukin-4 - immunology ; Jurkat Cells ; Leukocytes, Mononuclear - metabolism ; Lipopolysaccharides - immunology ; Lymphocytes - cytology ; Lymphocytes - immunology ; Lymphocytes - metabolism ; Macrophages - metabolism ; Macrophages, Peritoneal - immunology ; Macrophages, Peritoneal - metabolism ; Mice ; Mice, Inbred BALB C ; Microbiology ; Modulation of the immune response (stimulation, suppression) ; Molecular Sequence Data ; Pathogenicity, virulence, toxins, bacteriocins, pyrogens, host-bacteria relations, miscellaneous strains ; Protein-Tyrosine Kinases - metabolism ; Pseudomonas aeruginosa - immunology ; Pseudomonas aeruginosa - pathogenicity ; Signal Transduction - immunology ; Spleen - cytology ; Spleen - immunology ; Tumor Necrosis Factor-alpha - metabolism ; Virulence - immunology</subject><ispartof>Infection and immunity, 1998, Vol.66 (1), p.36-42</ispartof><rights>1998 INIST-CNRS</rights><rights>Copyright © 1998, American Society for Microbiology 1998</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3438-a010886ad9b90312f486d2db973140f4c005f19bdee9f0b4fda37037565207143</citedby><cites>FETCH-LOGICAL-c3438-a010886ad9b90312f486d2db973140f4c005f19bdee9f0b4fda37037565207143</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC107855/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC107855/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,725,778,782,883,3177,4012,27906,27907,27908,53774,53776</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=2127076$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/9423836$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>TELFORD, G</creatorcontrib><creatorcontrib>WHEELER, D</creatorcontrib><creatorcontrib>WILLIAMS, P</creatorcontrib><creatorcontrib>TOMKINS, P. T</creatorcontrib><creatorcontrib>APPLEBY, P</creatorcontrib><creatorcontrib>SEWELL, H</creatorcontrib><creatorcontrib>STEWART, G. S. A. B</creatorcontrib><creatorcontrib>BYCROFT, B. W</creatorcontrib><creatorcontrib>PRITCHARD, D. I</creatorcontrib><title>The Pseudomonas aeruginosa quorum-sensing signal molecule N-(3-oxododecanoyl)-L-homoserine lactone has immunomodulatory activity</title><title>Infection and immunity</title><addtitle>Infect Immun</addtitle><description>Diverse gram-negative bacterial cells communicate with each other by using diffusible N-acyl homoserine lactone (AHL) signal molecules to coordinate gene expression with cell population density. Accumulation of AHLs above a threshold concentration renders the population "quorate," and the appropriate target gene is activated. In pathogenic bacteria, such as Pseudomonas aeruginosa, AHL-mediated quorum sensing is involved in the regulation of multiple virulence determinants. We therefore sought to determine whether the immune system is capable of responding to these bacterial signal molecules. Consequently the immunomodulatory properties of the AHLs N-(3-oxododecanoyl)-L-homoserine lactone (OdDHL) and N-(3-oxohexanoyl)-L-homoserine lactone (OHHL) were evaluated in murine and human leukocyte immunoassays in vitro. OdDHL, but not OHHL, inhibited lymphocyte proliferation and tumor necrosis factor alpha production by lipopolysaccharide-stimulated macrophages. Furthermore, OdDHL simultaneously and potently down-regulated the production of IL-12, a Th-1-supportive cytokine. At high concentrations (>7 x 10(-5) M) OdDHL inhibited antibody production by keyhole limpet hemocyanin-stimulated spleen cells, but at lower concentrations (<7 x 10(-5) M), antibody production was stimulated, apparently by increasing the proportion of the immunoglobulin G1 (IgG1) isotype. OdDHL also promoted IgE production by interleukin-4-stimulated human peripheral blood mononuclear cells. These data indicate that OdDHL may influence the Th-1-Th-2 balance in the infected host and suggest that, in addition to regulating the expression of virulence determinants, OdDHL may contribute to the pathogenesis of P. aeruginosa infections by functioning as a virulence determinant per se.</description><subject>4-Butyrolactone - analogs & derivatives</subject><subject>4-Butyrolactone - biosynthesis</subject><subject>4-Butyrolactone - immunology</subject><subject>4-Butyrolactone - isolation & purification</subject><subject>Adjuvants, Immunologic</subject><subject>Amino Acid Sequence</subject><subject>Animals</subject><subject>Bacteriology</subject><subject>Biological and medical sciences</subject><subject>Cell Division</subject><subject>Cells, Cultured</subject><subject>Concanavalin A - immunology</subject><subject>Cytotoxicity Tests, Immunologic</subject><subject>Female</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Fundamental immunology</subject><subject>Hemocyanins - immunology</subject><subject>Homoserine - analogs & derivatives</subject><subject>Homoserine - biosynthesis</subject><subject>Homoserine - immunology</subject><subject>Homoserine - isolation & purification</subject><subject>Host Response and Inflammation</subject><subject>Humans</subject><subject>Immunobiology</subject><subject>Immunoglobulin E - biosynthesis</subject><subject>Immunoglobulin G - biosynthesis</subject><subject>Interleukin-12 - metabolism</subject><subject>Interleukin-4 - immunology</subject><subject>Jurkat Cells</subject><subject>Leukocytes, Mononuclear - metabolism</subject><subject>Lipopolysaccharides - immunology</subject><subject>Lymphocytes - cytology</subject><subject>Lymphocytes - immunology</subject><subject>Lymphocytes - metabolism</subject><subject>Macrophages - metabolism</subject><subject>Macrophages, Peritoneal - immunology</subject><subject>Macrophages, Peritoneal - metabolism</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Microbiology</subject><subject>Modulation of the immune response (stimulation, suppression)</subject><subject>Molecular Sequence Data</subject><subject>Pathogenicity, virulence, toxins, bacteriocins, pyrogens, host-bacteria relations, miscellaneous strains</subject><subject>Protein-Tyrosine Kinases - metabolism</subject><subject>Pseudomonas aeruginosa - immunology</subject><subject>Pseudomonas aeruginosa - pathogenicity</subject><subject>Signal Transduction - immunology</subject><subject>Spleen - cytology</subject><subject>Spleen - immunology</subject><subject>Tumor Necrosis Factor-alpha - metabolism</subject><subject>Virulence - immunology</subject><issn>0019-9567</issn><issn>1098-5522</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>1998</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkUuLFDEUhYMoYzv6C0SohYguUuZVqWQxi2Hw0dCoi3Ed0kmqO5JKZpLKYO_86aaZptHV5fKdc-6FA8BrjHqMifjote8573FPOWSkx1KKJ2CFkRRwGAh5ClYIYQnlwMfn4EUpv9rKGBMX4EIyQgXlK_Dndu-6H8VVm-YUdem0y3XnYyq6u68p1xkWF4uPu674XdShm1NwpgbXfYPvKUy_k03WGR3TIXyAG7hvOcVlH10XtFlSm_sW6-e5xoZsDXpJ-dA15h_8cngJnk06FPfqNC_Bz8-fbm--ws33L-ub6w00lFEBNcJICK6t3EpEMZmY4JbYrRwpZmhiBqFhwnJrnZMT2rLJajoiOg58IGjEjF6Cq8fcu7qdnTUuLlkHdZf9rPNBJe3V_yT6vdqlB4XRKIah-d-d_DndV1cWNftiXAg6ulSLwrw9MsijkD4KTU6lZDedb2Ckjr2p9fVaca6wolwxoo69Ndebf987e05FNf72xHUxOkxZR-PLWUYwGdHI6V9rNKSF</recordid><startdate>1998</startdate><enddate>1998</enddate><creator>TELFORD, G</creator><creator>WHEELER, D</creator><creator>WILLIAMS, P</creator><creator>TOMKINS, P. T</creator><creator>APPLEBY, P</creator><creator>SEWELL, H</creator><creator>STEWART, G. S. A. B</creator><creator>BYCROFT, B. W</creator><creator>PRITCHARD, D. I</creator><general>American Society for Microbiology</general><scope>IQODW</scope><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>7QL</scope><scope>7T5</scope><scope>C1K</scope><scope>H94</scope><scope>5PM</scope></search><sort><creationdate>1998</creationdate><title>The Pseudomonas aeruginosa quorum-sensing signal molecule N-(3-oxododecanoyl)-L-homoserine lactone has immunomodulatory activity</title><author>TELFORD, G ; WHEELER, D ; WILLIAMS, P ; TOMKINS, P. T ; APPLEBY, P ; SEWELL, H ; STEWART, G. S. A. B ; BYCROFT, B. W ; PRITCHARD, D. I</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3438-a010886ad9b90312f486d2db973140f4c005f19bdee9f0b4fda37037565207143</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>1998</creationdate><topic>4-Butyrolactone - analogs & derivatives</topic><topic>4-Butyrolactone - biosynthesis</topic><topic>4-Butyrolactone - immunology</topic><topic>4-Butyrolactone - isolation & purification</topic><topic>Adjuvants, Immunologic</topic><topic>Amino Acid Sequence</topic><topic>Animals</topic><topic>Bacteriology</topic><topic>Biological and medical sciences</topic><topic>Cell Division</topic><topic>Cells, Cultured</topic><topic>Concanavalin A - immunology</topic><topic>Cytotoxicity Tests, Immunologic</topic><topic>Female</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Fundamental immunology</topic><topic>Hemocyanins - immunology</topic><topic>Homoserine - analogs & derivatives</topic><topic>Homoserine - biosynthesis</topic><topic>Homoserine - immunology</topic><topic>Homoserine - isolation & purification</topic><topic>Host Response and Inflammation</topic><topic>Humans</topic><topic>Immunobiology</topic><topic>Immunoglobulin E - biosynthesis</topic><topic>Immunoglobulin G - biosynthesis</topic><topic>Interleukin-12 - metabolism</topic><topic>Interleukin-4 - immunology</topic><topic>Jurkat Cells</topic><topic>Leukocytes, Mononuclear - metabolism</topic><topic>Lipopolysaccharides - immunology</topic><topic>Lymphocytes - cytology</topic><topic>Lymphocytes - immunology</topic><topic>Lymphocytes - metabolism</topic><topic>Macrophages - metabolism</topic><topic>Macrophages, Peritoneal - immunology</topic><topic>Macrophages, Peritoneal - metabolism</topic><topic>Mice</topic><topic>Mice, Inbred BALB C</topic><topic>Microbiology</topic><topic>Modulation of the immune response (stimulation, suppression)</topic><topic>Molecular Sequence Data</topic><topic>Pathogenicity, virulence, toxins, bacteriocins, pyrogens, host-bacteria relations, miscellaneous strains</topic><topic>Protein-Tyrosine Kinases - metabolism</topic><topic>Pseudomonas aeruginosa - immunology</topic><topic>Pseudomonas aeruginosa - pathogenicity</topic><topic>Signal Transduction - immunology</topic><topic>Spleen - cytology</topic><topic>Spleen - immunology</topic><topic>Tumor Necrosis Factor-alpha - metabolism</topic><topic>Virulence - immunology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>TELFORD, G</creatorcontrib><creatorcontrib>WHEELER, D</creatorcontrib><creatorcontrib>WILLIAMS, P</creatorcontrib><creatorcontrib>TOMKINS, P. 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I</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Immunology Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Infection and immunity</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>TELFORD, G</au><au>WHEELER, D</au><au>WILLIAMS, P</au><au>TOMKINS, P. T</au><au>APPLEBY, P</au><au>SEWELL, H</au><au>STEWART, G. S. A. B</au><au>BYCROFT, B. W</au><au>PRITCHARD, D. I</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Pseudomonas aeruginosa quorum-sensing signal molecule N-(3-oxododecanoyl)-L-homoserine lactone has immunomodulatory activity</atitle><jtitle>Infection and immunity</jtitle><addtitle>Infect Immun</addtitle><date>1998</date><risdate>1998</risdate><volume>66</volume><issue>1</issue><spage>36</spage><epage>42</epage><pages>36-42</pages><issn>0019-9567</issn><eissn>1098-5522</eissn><coden>INFIBR</coden><abstract>Diverse gram-negative bacterial cells communicate with each other by using diffusible N-acyl homoserine lactone (AHL) signal molecules to coordinate gene expression with cell population density. Accumulation of AHLs above a threshold concentration renders the population "quorate," and the appropriate target gene is activated. In pathogenic bacteria, such as Pseudomonas aeruginosa, AHL-mediated quorum sensing is involved in the regulation of multiple virulence determinants. We therefore sought to determine whether the immune system is capable of responding to these bacterial signal molecules. Consequently the immunomodulatory properties of the AHLs N-(3-oxododecanoyl)-L-homoserine lactone (OdDHL) and N-(3-oxohexanoyl)-L-homoserine lactone (OHHL) were evaluated in murine and human leukocyte immunoassays in vitro. OdDHL, but not OHHL, inhibited lymphocyte proliferation and tumor necrosis factor alpha production by lipopolysaccharide-stimulated macrophages. Furthermore, OdDHL simultaneously and potently down-regulated the production of IL-12, a Th-1-supportive cytokine. At high concentrations (>7 x 10(-5) M) OdDHL inhibited antibody production by keyhole limpet hemocyanin-stimulated spleen cells, but at lower concentrations (<7 x 10(-5) M), antibody production was stimulated, apparently by increasing the proportion of the immunoglobulin G1 (IgG1) isotype. OdDHL also promoted IgE production by interleukin-4-stimulated human peripheral blood mononuclear cells. These data indicate that OdDHL may influence the Th-1-Th-2 balance in the infected host and suggest that, in addition to regulating the expression of virulence determinants, OdDHL may contribute to the pathogenesis of P. aeruginosa infections by functioning as a virulence determinant per se.</abstract><cop>Washington, DC</cop><pub>American Society for Microbiology</pub><pmid>9423836</pmid><doi>10.1128/iai.66.1.36-42.1998</doi><tpages>7</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Infection and immunity, 1998, Vol.66 (1), p.36-42 |
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| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_107855 |
| source | American Society for Microbiology; MEDLINE; EZB-FREE-00999 freely available EZB journals; PubMed Central |
| subjects | 4-Butyrolactone - analogs & derivatives 4-Butyrolactone - biosynthesis 4-Butyrolactone - immunology 4-Butyrolactone - isolation & purification Adjuvants, Immunologic Amino Acid Sequence Animals Bacteriology Biological and medical sciences Cell Division Cells, Cultured Concanavalin A - immunology Cytotoxicity Tests, Immunologic Female Fundamental and applied biological sciences. Psychology Fundamental immunology Hemocyanins - immunology Homoserine - analogs & derivatives Homoserine - biosynthesis Homoserine - immunology Homoserine - isolation & purification Host Response and Inflammation Humans Immunobiology Immunoglobulin E - biosynthesis Immunoglobulin G - biosynthesis Interleukin-12 - metabolism Interleukin-4 - immunology Jurkat Cells Leukocytes, Mononuclear - metabolism Lipopolysaccharides - immunology Lymphocytes - cytology Lymphocytes - immunology Lymphocytes - metabolism Macrophages - metabolism Macrophages, Peritoneal - immunology Macrophages, Peritoneal - metabolism Mice Mice, Inbred BALB C Microbiology Modulation of the immune response (stimulation, suppression) Molecular Sequence Data Pathogenicity, virulence, toxins, bacteriocins, pyrogens, host-bacteria relations, miscellaneous strains Protein-Tyrosine Kinases - metabolism Pseudomonas aeruginosa - immunology Pseudomonas aeruginosa - pathogenicity Signal Transduction - immunology Spleen - cytology Spleen - immunology Tumor Necrosis Factor-alpha - metabolism Virulence - immunology |
| title | The Pseudomonas aeruginosa quorum-sensing signal molecule N-(3-oxododecanoyl)-L-homoserine lactone has immunomodulatory activity |
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