Microbial Metalloproteinases Mediate Sensing of Invading Pathogens and Activate Innate Immune Responses in the Lepidopteran Model Host Galleria mellonella
Thermolysin-like metalloproteinases such as aureolysin, pseudolysin, and bacillolysin represent virulence factors of diverse bacterial pathogens. Recently, we discovered that injection of thermolysin into larvae of the greater wax moth, Galleria mellonella, mediated strong immune responses. Thermoly...
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| Veröffentlicht in: | Infection and Immunity 2007-01, Vol.75 (1), p.175-183 |
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| creator | Altincicek, Boran Linder, Monica Linder, Dietmar Preissner, Klaus T Vilcinskas, Andreas |
| description | Thermolysin-like metalloproteinases such as aureolysin, pseudolysin, and bacillolysin represent virulence factors of diverse bacterial pathogens. Recently, we discovered that injection of thermolysin into larvae of the greater wax moth, Galleria mellonella, mediated strong immune responses. Thermolysin-mediated proteolysis of hemolymph proteins yielded a variety of small-sized ( |
| doi_str_mv | 10.1128/IAI.01385-06 |
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Recently, we discovered that injection of thermolysin into larvae of the greater wax moth, Galleria mellonella, mediated strong immune responses. Thermolysin-mediated proteolysis of hemolymph proteins yielded a variety of small-sized (<3 kDa) protein fragments (protfrags) that are potent elicitors of innate immune responses. In this study, we report the activation of a serine proteinase cascade by thermolysin, as described for bacterial lipopolysaccharides (LPS), that results in subsequent prophenoloxidase activation leading to melanization, an elementary immune defense reaction of insects. Quantitative real-time reverse transcription-PCR analyses of the expression of immune-related genes encoding the inducible metalloproteinase inhibitor, gallerimycin, and lysozyme demonstrated increased transcriptional rates after challenge with purified protfrags similar to rates after challenge with LPS. Additionally, we determined the induction of a similar spectrum of immune-responsive proteins that were secreted into the hemolymph by using comparative proteomic analyses of hemolymph proteins from untreated larvae and from larvae that were challenged with either protfrags or LPS. Since G. mellonella was recently established as a valuable pathogenicity model for Cryptococcus neoformans infection, the present results add to our understanding of the mechanisms of immune responses in G. mellonella. The obtained results support the proposed danger model, which suggests that the immune system senses endogenous alarm signals during infection besides recognition of microbial pattern molecules.</description><identifier>ISSN: 0019-9567</identifier><identifier>EISSN: 1098-5522</identifier><identifier>DOI: 10.1128/IAI.01385-06</identifier><identifier>PMID: 17074843</identifier><identifier>CODEN: INFIBR</identifier><language>eng</language><publisher>Washington, DC: American Society for Microbiology</publisher><subject>Animals ; Biological and medical sciences ; Cryptococcus neoformans ; Electrophoresis, Gel, Two-Dimensional ; Enzyme Activation ; Fundamental and applied biological sciences. Psychology ; Galleria mellonella ; Gene Expression ; Hemolymph - immunology ; Hemolymph - metabolism ; Host Response and Inflammation ; Immunity, Innate ; Larva ; Lepidoptera ; Lepidoptera - immunology ; Lepidoptera - microbiology ; Lipopolysaccharides - immunology ; Metalloendopeptidases - immunology ; Metalloendopeptidases - metabolism ; Microbiology ; Models, Immunological ; Oligopeptides - immunology ; Oligopeptides - metabolism ; Reverse Transcriptase Polymerase Chain Reaction ; Serine Endopeptidases - immunology ; Serine Endopeptidases - metabolism ; Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization ; Thermolysin - immunology ; Thermolysin - metabolism</subject><ispartof>Infection and Immunity, 2007-01, Vol.75 (1), p.175-183</ispartof><rights>2007 INIST-CNRS</rights><rights>Copyright © 2007, American Society for Microbiology 2007</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c535t-e2b685a476309fde83fc95fe92fa09167a333657449075b4c8bf5c383c6ff3</citedby><cites>FETCH-LOGICAL-c535t-e2b685a476309fde83fc95fe92fa09167a333657449075b4c8bf5c383c6ff3</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/PMC1828416/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC1828416/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,724,777,781,882,3175,3176,27905,27906,53772,53774</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=18614911$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/17074843$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Altincicek, Boran</creatorcontrib><creatorcontrib>Linder, Monica</creatorcontrib><creatorcontrib>Linder, Dietmar</creatorcontrib><creatorcontrib>Preissner, Klaus T</creatorcontrib><creatorcontrib>Vilcinskas, Andreas</creatorcontrib><title>Microbial Metalloproteinases Mediate Sensing of Invading Pathogens and Activate Innate Immune Responses in the Lepidopteran Model Host Galleria mellonella</title><title>Infection and Immunity</title><addtitle>Infect Immun</addtitle><description>Thermolysin-like metalloproteinases such as aureolysin, pseudolysin, and bacillolysin represent virulence factors of diverse bacterial pathogens. Recently, we discovered that injection of thermolysin into larvae of the greater wax moth, Galleria mellonella, mediated strong immune responses. Thermolysin-mediated proteolysis of hemolymph proteins yielded a variety of small-sized (<3 kDa) protein fragments (protfrags) that are potent elicitors of innate immune responses. In this study, we report the activation of a serine proteinase cascade by thermolysin, as described for bacterial lipopolysaccharides (LPS), that results in subsequent prophenoloxidase activation leading to melanization, an elementary immune defense reaction of insects. Quantitative real-time reverse transcription-PCR analyses of the expression of immune-related genes encoding the inducible metalloproteinase inhibitor, gallerimycin, and lysozyme demonstrated increased transcriptional rates after challenge with purified protfrags similar to rates after challenge with LPS. Additionally, we determined the induction of a similar spectrum of immune-responsive proteins that were secreted into the hemolymph by using comparative proteomic analyses of hemolymph proteins from untreated larvae and from larvae that were challenged with either protfrags or LPS. Since G. mellonella was recently established as a valuable pathogenicity model for Cryptococcus neoformans infection, the present results add to our understanding of the mechanisms of immune responses in G. mellonella. The obtained results support the proposed danger model, which suggests that the immune system senses endogenous alarm signals during infection besides recognition of microbial pattern molecules.</description><subject>Animals</subject><subject>Biological and medical sciences</subject><subject>Cryptococcus neoformans</subject><subject>Electrophoresis, Gel, Two-Dimensional</subject><subject>Enzyme Activation</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Galleria mellonella</subject><subject>Gene Expression</subject><subject>Hemolymph - immunology</subject><subject>Hemolymph - metabolism</subject><subject>Host Response and Inflammation</subject><subject>Immunity, Innate</subject><subject>Larva</subject><subject>Lepidoptera</subject><subject>Lepidoptera - immunology</subject><subject>Lepidoptera - microbiology</subject><subject>Lipopolysaccharides - immunology</subject><subject>Metalloendopeptidases - immunology</subject><subject>Metalloendopeptidases - metabolism</subject><subject>Microbiology</subject><subject>Models, Immunological</subject><subject>Oligopeptides - immunology</subject><subject>Oligopeptides - metabolism</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>Serine Endopeptidases - immunology</subject><subject>Serine Endopeptidases - metabolism</subject><subject>Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization</subject><subject>Thermolysin - immunology</subject><subject>Thermolysin - metabolism</subject><issn>0019-9567</issn><issn>1098-5522</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2007</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkc1uEzEUhUcIRENgxxq8oSum2OP_DVJUlTZSIlALa8uZuU6MZuzpeBLEq_C0eJqIwoqNr-376fj4nqJ4TfAFIZX6sFwsLzChipdYPClmBGtVcl5VT4sZxkSXmgt5VrxI6Xs-MsbU8-KMSCyZYnRW_Fr7eogbb1u0htG2beyHOIIPNkHKV423I6A7CMmHLYoOLcPBNtP-ix13cZsbyIYGLerRHyZ0GcJD6bp9AHQLqY9hkvIBjTtAK-h9E_sRBhvQOjbQopuYRnSdn4bBW9RB9hDyYl8Wz5xtE7w61Xlx--nq6-VNufp8vbxcrMqaUz6WUG2E4pZJQbF2DSjqas0d6MpZrImQllIquGRMY8k3rFYbx2uqaC2co_Pi41G03286aGoI42Bb0w--s8NPE603_3aC35ltPBiiKsWIyALnJ4Eh3u8hjabzqZ78B4j7ZISiSisu_wsSrQWT2eu8eH8EczApDeD-uCHYTJGbHLl5iNzgycCbv3_wCJ8yzsC7E2BTbVuXJ1_79MgpQZgmJHPoyO38dvfDD2Bs6ozPE5DckKzHM_L2iDgbjd0OWebbXZWt4OyLykrQ31g_y3Y</recordid><startdate>20070101</startdate><enddate>20070101</enddate><creator>Altincicek, Boran</creator><creator>Linder, Monica</creator><creator>Linder, Dietmar</creator><creator>Preissner, Klaus T</creator><creator>Vilcinskas, Andreas</creator><general>American Society for Microbiology</general><scope>FBQ</scope><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>7SS</scope><scope>7T5</scope><scope>7T7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20070101</creationdate><title>Microbial Metalloproteinases Mediate Sensing of Invading Pathogens and Activate Innate Immune Responses in the Lepidopteran Model Host Galleria mellonella</title><author>Altincicek, Boran ; Linder, Monica ; Linder, Dietmar ; Preissner, Klaus T ; Vilcinskas, Andreas</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c535t-e2b685a476309fde83fc95fe92fa09167a333657449075b4c8bf5c383c6ff3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2007</creationdate><topic>Animals</topic><topic>Biological and medical sciences</topic><topic>Cryptococcus neoformans</topic><topic>Electrophoresis, Gel, Two-Dimensional</topic><topic>Enzyme Activation</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Galleria mellonella</topic><topic>Gene Expression</topic><topic>Hemolymph - immunology</topic><topic>Hemolymph - metabolism</topic><topic>Host Response and Inflammation</topic><topic>Immunity, Innate</topic><topic>Larva</topic><topic>Lepidoptera</topic><topic>Lepidoptera - immunology</topic><topic>Lepidoptera - microbiology</topic><topic>Lipopolysaccharides - immunology</topic><topic>Metalloendopeptidases - immunology</topic><topic>Metalloendopeptidases - metabolism</topic><topic>Microbiology</topic><topic>Models, Immunological</topic><topic>Oligopeptides - immunology</topic><topic>Oligopeptides - metabolism</topic><topic>Reverse Transcriptase Polymerase Chain Reaction</topic><topic>Serine Endopeptidases - immunology</topic><topic>Serine Endopeptidases - metabolism</topic><topic>Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization</topic><topic>Thermolysin - immunology</topic><topic>Thermolysin - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Altincicek, Boran</creatorcontrib><creatorcontrib>Linder, Monica</creatorcontrib><creatorcontrib>Linder, Dietmar</creatorcontrib><creatorcontrib>Preissner, Klaus T</creatorcontrib><creatorcontrib>Vilcinskas, Andreas</creatorcontrib><collection>AGRIS</collection><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>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</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>Altincicek, Boran</au><au>Linder, Monica</au><au>Linder, Dietmar</au><au>Preissner, Klaus T</au><au>Vilcinskas, Andreas</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Microbial Metalloproteinases Mediate Sensing of Invading Pathogens and Activate Innate Immune Responses in the Lepidopteran Model Host Galleria mellonella</atitle><jtitle>Infection and Immunity</jtitle><addtitle>Infect Immun</addtitle><date>2007-01-01</date><risdate>2007</risdate><volume>75</volume><issue>1</issue><spage>175</spage><epage>183</epage><pages>175-183</pages><issn>0019-9567</issn><eissn>1098-5522</eissn><coden>INFIBR</coden><abstract>Thermolysin-like metalloproteinases such as aureolysin, pseudolysin, and bacillolysin represent virulence factors of diverse bacterial pathogens. Recently, we discovered that injection of thermolysin into larvae of the greater wax moth, Galleria mellonella, mediated strong immune responses. Thermolysin-mediated proteolysis of hemolymph proteins yielded a variety of small-sized (<3 kDa) protein fragments (protfrags) that are potent elicitors of innate immune responses. In this study, we report the activation of a serine proteinase cascade by thermolysin, as described for bacterial lipopolysaccharides (LPS), that results in subsequent prophenoloxidase activation leading to melanization, an elementary immune defense reaction of insects. Quantitative real-time reverse transcription-PCR analyses of the expression of immune-related genes encoding the inducible metalloproteinase inhibitor, gallerimycin, and lysozyme demonstrated increased transcriptional rates after challenge with purified protfrags similar to rates after challenge with LPS. Additionally, we determined the induction of a similar spectrum of immune-responsive proteins that were secreted into the hemolymph by using comparative proteomic analyses of hemolymph proteins from untreated larvae and from larvae that were challenged with either protfrags or LPS. Since G. mellonella was recently established as a valuable pathogenicity model for Cryptococcus neoformans infection, the present results add to our understanding of the mechanisms of immune responses in G. mellonella. The obtained results support the proposed danger model, which suggests that the immune system senses endogenous alarm signals during infection besides recognition of microbial pattern molecules.</abstract><cop>Washington, DC</cop><pub>American Society for Microbiology</pub><pmid>17074843</pmid><doi>10.1128/IAI.01385-06</doi><tpages>9</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Biological and medical sciences Cryptococcus neoformans Electrophoresis, Gel, Two-Dimensional Enzyme Activation Fundamental and applied biological sciences. Psychology Galleria mellonella Gene Expression Hemolymph - immunology Hemolymph - metabolism Host Response and Inflammation Immunity, Innate Larva Lepidoptera Lepidoptera - immunology Lepidoptera - microbiology Lipopolysaccharides - immunology Metalloendopeptidases - immunology Metalloendopeptidases - metabolism Microbiology Models, Immunological Oligopeptides - immunology Oligopeptides - metabolism Reverse Transcriptase Polymerase Chain Reaction Serine Endopeptidases - immunology Serine Endopeptidases - metabolism Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization Thermolysin - immunology Thermolysin - metabolism |
| title | Microbial Metalloproteinases Mediate Sensing of Invading Pathogens and Activate Innate Immune Responses in the Lepidopteran Model Host Galleria mellonella |
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