WWP-1 is a novel modulator of the DAF-2 insulin-like signaling network involved in pore-forming toxin cellular defenses in Caenorhabditis elegans
Pore-forming toxins (PFTs) are the single largest class of bacterial virulence factors. The DAF-2 insulin/insulin-like growth factor-1 signaling pathway, which regulates lifespan and stress resistance in Caenorhabditis elegans, is known to mutate to resistance to pathogenic bacteria. However, its ro...
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| Veröffentlicht in: | PloS one 2010-03, Vol.5 (3), p.e9494-e9494 |
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| description | Pore-forming toxins (PFTs) are the single largest class of bacterial virulence factors. The DAF-2 insulin/insulin-like growth factor-1 signaling pathway, which regulates lifespan and stress resistance in Caenorhabditis elegans, is known to mutate to resistance to pathogenic bacteria. However, its role in responses against bacterial toxins and PFTs is as yet unexplored. Here we reveal that reduction of the DAF-2 insulin-like pathway confers the resistance of Caenorhabditis elegans to cytolitic crystal (Cry) PFTs produced by Bacillus thuringiensis. In contrast to the canonical DAF-2 insulin-like signaling pathway previously defined for aging and pathogenesis, the PFT response pathway diverges at 3-phosphoinositide-dependent kinase 1 (PDK-1) and appears to feed into a novel insulin-like pathway signal arm defined by the WW domain Protein 1 (WWP-1). In addition, we also find that WWP-1 not only plays an important role in the intrinsic cellular defense (INCED) against PFTs but also is involved in innate immunity against pathogenic bacteria Pseudomonas aeruginosa and in lifespan regulation. Taken together, our data suggest that WWP-1 and DAF-16 function in parallel within the fundamental DAF-2 insulin/IGF-1 signaling network to regulate fundamental cellular responses in C. elegans. |
| doi_str_mv | 10.1371/journal.pone.0009494 |
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The DAF-2 insulin/insulin-like growth factor-1 signaling pathway, which regulates lifespan and stress resistance in Caenorhabditis elegans, is known to mutate to resistance to pathogenic bacteria. However, its role in responses against bacterial toxins and PFTs is as yet unexplored. Here we reveal that reduction of the DAF-2 insulin-like pathway confers the resistance of Caenorhabditis elegans to cytolitic crystal (Cry) PFTs produced by Bacillus thuringiensis. In contrast to the canonical DAF-2 insulin-like signaling pathway previously defined for aging and pathogenesis, the PFT response pathway diverges at 3-phosphoinositide-dependent kinase 1 (PDK-1) and appears to feed into a novel insulin-like pathway signal arm defined by the WW domain Protein 1 (WWP-1). In addition, we also find that WWP-1 not only plays an important role in the intrinsic cellular defense (INCED) against PFTs but also is involved in innate immunity against pathogenic bacteria Pseudomonas aeruginosa and in lifespan regulation. Taken together, our data suggest that WWP-1 and DAF-16 function in parallel within the fundamental DAF-2 insulin/IGF-1 signaling network to regulate fundamental cellular responses in C. elegans.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0009494</identifier><identifier>PMID: 20209166</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Aging ; Animals ; Ataxia ; Autophagy ; Bacillus thuringiensis - metabolism ; Bacteria ; Biochemistry ; Caenorhabditis elegans ; Caenorhabditis elegans - metabolism ; Caenorhabditis elegans Proteins - metabolism ; Caenorhabditis elegans Proteins - physiology ; Cell Biology/Cell Signaling ; Cell Biology/Cellular Death and Stress Responses ; Cellular communication ; Developmental biology ; E coli ; Forming ; Gene Expression Regulation ; Genetics ; Genetics and Genomics/Animal Genetics ; Genetics and Genomics/Disease Models ; Gram-Positive Bacterial Infections - metabolism ; Humans ; Hypoxia ; Immunity ; Immunology/Immune Response ; Immunology/Innate Immunity ; Innate immunity ; Insulin ; Insulin - metabolism ; Insulin-like growth factor I ; Insulin-like growth factors ; Kinases ; Life span ; Medical research ; Microbial drug resistance ; Microbiology/Innate Immunity ; Models, Biological ; Molecular biology ; Mutation ; Nematodes ; Pathogenesis ; Phosphatase ; Pore formation ; Proteins ; Pseudomonas aeruginosa ; Receptor, Insulin - metabolism ; Respiration ; RNA Interference ; Signal Transduction ; Signaling ; Toxins ; Ubiquitin-Protein Ligases - metabolism ; Ubiquitin-Protein Ligases - physiology ; Virulence ; Virulence (Microbiology) ; Virulence Factors ; Worms</subject><ispartof>PloS one, 2010-03, Vol.5 (3), p.e9494-e9494</ispartof><rights>COPYRIGHT 2010 Public Library of Science</rights><rights>2010 Chen et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Chen et al. 2010</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c757t-44728406e0673cccadb1917f33e968705e1e1b7c00c17281c5b04251fbbd227a3</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2830483/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2830483/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20209166$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chen, Chang-Shi</creatorcontrib><creatorcontrib>Bellier, Audrey</creatorcontrib><creatorcontrib>Kao, Cheng-Yuan</creatorcontrib><creatorcontrib>Yang, Ya-Luen</creatorcontrib><creatorcontrib>Chen, Huan-Da</creatorcontrib><creatorcontrib>Los, Ferdinand C O</creatorcontrib><creatorcontrib>Aroian, Raffi V</creatorcontrib><title>WWP-1 is a novel modulator of the DAF-2 insulin-like signaling network involved in pore-forming toxin cellular defenses in Caenorhabditis elegans</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Pore-forming toxins (PFTs) are the single largest class of bacterial virulence factors. The DAF-2 insulin/insulin-like growth factor-1 signaling pathway, which regulates lifespan and stress resistance in Caenorhabditis elegans, is known to mutate to resistance to pathogenic bacteria. However, its role in responses against bacterial toxins and PFTs is as yet unexplored. Here we reveal that reduction of the DAF-2 insulin-like pathway confers the resistance of Caenorhabditis elegans to cytolitic crystal (Cry) PFTs produced by Bacillus thuringiensis. In contrast to the canonical DAF-2 insulin-like signaling pathway previously defined for aging and pathogenesis, the PFT response pathway diverges at 3-phosphoinositide-dependent kinase 1 (PDK-1) and appears to feed into a novel insulin-like pathway signal arm defined by the WW domain Protein 1 (WWP-1). In addition, we also find that WWP-1 not only plays an important role in the intrinsic cellular defense (INCED) against PFTs but also is involved in innate immunity against pathogenic bacteria Pseudomonas aeruginosa and in lifespan regulation. Taken together, our data suggest that WWP-1 and DAF-16 function in parallel within the fundamental DAF-2 insulin/IGF-1 signaling network to regulate fundamental cellular responses in C. elegans.</description><subject>Aging</subject><subject>Animals</subject><subject>Ataxia</subject><subject>Autophagy</subject><subject>Bacillus thuringiensis - metabolism</subject><subject>Bacteria</subject><subject>Biochemistry</subject><subject>Caenorhabditis elegans</subject><subject>Caenorhabditis elegans - metabolism</subject><subject>Caenorhabditis elegans Proteins - metabolism</subject><subject>Caenorhabditis elegans Proteins - physiology</subject><subject>Cell Biology/Cell Signaling</subject><subject>Cell Biology/Cellular Death and Stress Responses</subject><subject>Cellular communication</subject><subject>Developmental biology</subject><subject>E coli</subject><subject>Forming</subject><subject>Gene Expression Regulation</subject><subject>Genetics</subject><subject>Genetics and Genomics/Animal Genetics</subject><subject>Genetics and Genomics/Disease Models</subject><subject>Gram-Positive Bacterial Infections - 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metabolism</subject><subject>Ubiquitin-Protein Ligases - physiology</subject><subject>Virulence</subject><subject>Virulence (Microbiology)</subject><subject>Virulence Factors</subject><subject>Worms</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNk11v0zAUhiMEYqPwDxBEQgJxkeKvxMkNUjUYTJo0xNcuLcc5Sd25drGdMn4G_xiXdlOLdoF8Yev4Oe-xX_tk2VOMpphy_GbhRm-lma6chSlCqGENu5cd44aSoiKI3t9bH2WPQlggVNK6qh5mRwQR1OCqOs5-X15-KnCuQy5z69Zg8qXrRiOj87nr8ziH_N3stCC5tmE02hZGX0Ee9JBKazvkFuJP56_S9tqZNXRpka-ch6J3frkBortOIQXGJFWfd9CDDRA23IkE6_xctp2O6QBgYJA2PM4e9NIEeLKbJ9m30_dfTz4W5xcfzk5m54XiJY8FY5zUDFWAKk6VUrJrcYN5Tyk0Vc1RCRhwyxVCCicSq7JFjJS4b9uOEC7pJHu-1V0ZF8TOzSAwqRvGksNlIs62ROfkQqy8Xkr_Szipxd-A84OQPmplQJS07yusgCgODGretkjWVQe8VKSt2iZpvd1VG9sldAps9NIciB7uWD0Xg1sLUlPEapoEXu0EvPsxQohiqcPGVmnBjUFwSsua0bJK5It_yLsvt6MGmc6vbe9SWbXRFDPGaYMRS8ZOsukdVBodLLVKP6_XKX6Q8PogITERruMgxxDE2ZfP_89efD9kX-6xc5AmzoMzY9TOhkOQbUHlXQge-luPMRKbxrlxQ2waR-waJ6U923-f26SbTqF_ALzJFAw</recordid><startdate>20100302</startdate><enddate>20100302</enddate><creator>Chen, Chang-Shi</creator><creator>Bellier, Audrey</creator><creator>Kao, Cheng-Yuan</creator><creator>Yang, Ya-Luen</creator><creator>Chen, Huan-Da</creator><creator>Los, Ferdinand C O</creator><creator>Aroian, Raffi V</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20100302</creationdate><title>WWP-1 is a novel modulator of the DAF-2 insulin-like signaling network involved in pore-forming toxin cellular defenses in Caenorhabditis elegans</title><author>Chen, Chang-Shi ; Bellier, Audrey ; Kao, Cheng-Yuan ; Yang, Ya-Luen ; Chen, Huan-Da ; Los, Ferdinand C O ; Aroian, Raffi V</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c757t-44728406e0673cccadb1917f33e968705e1e1b7c00c17281c5b04251fbbd227a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Aging</topic><topic>Animals</topic><topic>Ataxia</topic><topic>Autophagy</topic><topic>Bacillus thuringiensis - 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The DAF-2 insulin/insulin-like growth factor-1 signaling pathway, which regulates lifespan and stress resistance in Caenorhabditis elegans, is known to mutate to resistance to pathogenic bacteria. However, its role in responses against bacterial toxins and PFTs is as yet unexplored. Here we reveal that reduction of the DAF-2 insulin-like pathway confers the resistance of Caenorhabditis elegans to cytolitic crystal (Cry) PFTs produced by Bacillus thuringiensis. In contrast to the canonical DAF-2 insulin-like signaling pathway previously defined for aging and pathogenesis, the PFT response pathway diverges at 3-phosphoinositide-dependent kinase 1 (PDK-1) and appears to feed into a novel insulin-like pathway signal arm defined by the WW domain Protein 1 (WWP-1). In addition, we also find that WWP-1 not only plays an important role in the intrinsic cellular defense (INCED) against PFTs but also is involved in innate immunity against pathogenic bacteria Pseudomonas aeruginosa and in lifespan regulation. Taken together, our data suggest that WWP-1 and DAF-16 function in parallel within the fundamental DAF-2 insulin/IGF-1 signaling network to regulate fundamental cellular responses in C. elegans.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>20209166</pmid><doi>10.1371/journal.pone.0009494</doi><tpages>e9494</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | PloS one, 2010-03, Vol.5 (3), p.e9494-e9494 |
| issn | 1932-6203 1932-6203 |
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| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Aging Animals Ataxia Autophagy Bacillus thuringiensis - metabolism Bacteria Biochemistry Caenorhabditis elegans Caenorhabditis elegans - metabolism Caenorhabditis elegans Proteins - metabolism Caenorhabditis elegans Proteins - physiology Cell Biology/Cell Signaling Cell Biology/Cellular Death and Stress Responses Cellular communication Developmental biology E coli Forming Gene Expression Regulation Genetics Genetics and Genomics/Animal Genetics Genetics and Genomics/Disease Models Gram-Positive Bacterial Infections - metabolism Humans Hypoxia Immunity Immunology/Immune Response Immunology/Innate Immunity Innate immunity Insulin Insulin - metabolism Insulin-like growth factor I Insulin-like growth factors Kinases Life span Medical research Microbial drug resistance Microbiology/Innate Immunity Models, Biological Molecular biology Mutation Nematodes Pathogenesis Phosphatase Pore formation Proteins Pseudomonas aeruginosa Receptor, Insulin - metabolism Respiration RNA Interference Signal Transduction Signaling Toxins Ubiquitin-Protein Ligases - metabolism Ubiquitin-Protein Ligases - physiology Virulence Virulence (Microbiology) Virulence Factors Worms |
| title | WWP-1 is a novel modulator of the DAF-2 insulin-like signaling network involved in pore-forming toxin cellular defenses in Caenorhabditis elegans |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-09T12%3A21%3A05IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=WWP-1%20is%20a%20novel%20modulator%20of%20the%20DAF-2%20insulin-like%20signaling%20network%20involved%20in%20pore-forming%20toxin%20cellular%20defenses%20in%20Caenorhabditis%20elegans&rft.jtitle=PloS%20one&rft.au=Chen,%20Chang-Shi&rft.date=2010-03-02&rft.volume=5&rft.issue=3&rft.spage=e9494&rft.epage=e9494&rft.pages=e9494-e9494&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0009494&rft_dat=%3Cgale_plos_%3EA473910467%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1289441375&rft_id=info:pmid/20209166&rft_galeid=A473910467&rft_doaj_id=oai_doaj_org_article_53ff61ce2c7e4e87bb0a86de75c2b6b9&rfr_iscdi=true |