Diversity of Innate Immune Recognition Mechanism for Bacterial Polymeric meso-Diaminopimelic Acid-type Peptidoglycan in Insects
In Drosophila, the synthesis of antimicrobial peptides in response to microbial infections is under the control of the Toll and immune deficiency (Imd) signaling pathway. The Toll signaling pathway responds mainly to the lysine-type peptidoglycan of Gram-positive bacteria and fungal β-1,3-glucan, wh...
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| creator | Yu, Yang Park, Ji-Won Kwon, Hyun-Mi Hwang, Hyun-Ok Jang, In-Hwan Masuda, Akiko Kurokawa, Kenji Nakayama, Hiroshi Lee, Won-Jae Dohmae, Naoshi Zhang, Jinghai Lee, Bok Luel |
| description | In Drosophila, the synthesis of antimicrobial peptides in response to microbial infections is under the control of the Toll and immune deficiency (Imd) signaling pathway. The Toll signaling pathway responds mainly to the lysine-type peptidoglycan of Gram-positive bacteria and fungal β-1,3-glucan, whereas the Imd pathway responds to the meso-diaminopimelic acid (DAP)-type peptidoglycan of Gram-negative bacteria and certain Gram-positive bacilli. Recently we determined the activation mechanism of a Toll signaling pathway biochemically using a large beetle, Tenebrio molitor. However, DAP-type peptidoglycan recognition mechanism and its signaling pathway are still unclear in the fly and beetle. Here, we show that polymeric DAP-type peptidoglycan, but not its monomeric form, formed a complex with Tenebrio peptidoglycan recognition protein-SA, and this complex activated the three-step proteolytic cascade to produce processed Spätzle, a Toll receptor ligand, and induced Drosophila defensin-like antimicrobial peptide in Tenebrio larvae similarly to polymeric lysine-type peptidoglycan. Monomeric DAP-type peptidoglycan induced Drosophila diptericin-like antimicrobial peptide in Tenebrio hemocytes. In addition, both polymeric and monomeric DAP-type peptidoglycans induced expression of Tenebrio peptidoglycan recognition protein-SC2, which is DAP-type peptidoglycan-selective N-acetylmuramyl-l-alanine amidase that functions as a DAP-type peptidoglycan scavenger, appearing to function as a negative regulator of the DAP-type peptidoglycan signaling by cleaving DAP-type peptidoglycan in Tenebrio larvae. Taken together, these results demonstrate that molecular recognition mechanism for polymeric DAP-type peptidoglycan is different between Tenebrio larvae and Drosophila adults, providing biochemical evidences of biological diversity of innate immune responses in insects. |
| doi_str_mv | 10.1074/jbc.M110.144014 |
| format | Article |
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The Toll signaling pathway responds mainly to the lysine-type peptidoglycan of Gram-positive bacteria and fungal β-1,3-glucan, whereas the Imd pathway responds to the meso-diaminopimelic acid (DAP)-type peptidoglycan of Gram-negative bacteria and certain Gram-positive bacilli. Recently we determined the activation mechanism of a Toll signaling pathway biochemically using a large beetle, Tenebrio molitor. However, DAP-type peptidoglycan recognition mechanism and its signaling pathway are still unclear in the fly and beetle. Here, we show that polymeric DAP-type peptidoglycan, but not its monomeric form, formed a complex with Tenebrio peptidoglycan recognition protein-SA, and this complex activated the three-step proteolytic cascade to produce processed Spätzle, a Toll receptor ligand, and induced Drosophila defensin-like antimicrobial peptide in Tenebrio larvae similarly to polymeric lysine-type peptidoglycan. Monomeric DAP-type peptidoglycan induced Drosophila diptericin-like antimicrobial peptide in Tenebrio hemocytes. In addition, both polymeric and monomeric DAP-type peptidoglycans induced expression of Tenebrio peptidoglycan recognition protein-SC2, which is DAP-type peptidoglycan-selective N-acetylmuramyl-l-alanine amidase that functions as a DAP-type peptidoglycan scavenger, appearing to function as a negative regulator of the DAP-type peptidoglycan signaling by cleaving DAP-type peptidoglycan in Tenebrio larvae. Taken together, these results demonstrate that molecular recognition mechanism for polymeric DAP-type peptidoglycan is different between Tenebrio larvae and Drosophila adults, providing biochemical evidences of biological diversity of innate immune responses in insects.</description><identifier>ISSN: 0021-9258</identifier><identifier>EISSN: 1083-351X</identifier><identifier>DOI: 10.1074/jbc.M110.144014</identifier><identifier>PMID: 20702416</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Amidase ; Animals ; Antimicrobial peptides ; b-1,3-Glucan ; Bacteria ; Bacteria - immunology ; Bacteria - metabolism ; Base Sequence ; beta -1,3-Glucan ; Biological diversity ; Carrier Proteins - genetics ; Carrier Proteins - immunology ; Carrier Proteins - metabolism ; Cell Wall ; Defensins - biosynthesis ; Defensins - genetics ; Defensins - immunology ; Diaminopimelic Acid ; Drosophila ; Drosophila melanogaster ; Drosophila Proteins - genetics ; Drosophila Proteins - immunology ; Drosophila Proteins - metabolism ; Gram-negative bacteria ; Gram-positive bacilli ; Gram-positive bacteria ; Hemocytes ; Humoral Response ; Imd Pathway ; Immune response ; Immunity, Innate - physiology ; Immunology ; Infection ; Innate Immunity ; Insect ; Insect Proteins - genetics ; Insect Proteins - immunology ; Insect Proteins - metabolism ; Larvae ; Molecular Sequence Data ; Pattern Recognition Receptor ; Peptidoglycan ; Peptidoglycan - immunology ; Peptidoglycan - metabolism ; peptidoglycans ; PGRP ; Proteolysis ; Signal Transduction ; Species Specificity ; Tenebrio ; Tenebrio - genetics ; Tenebrio - immunology ; Tenebrio - metabolism ; Tenebrio - microbiology ; Tenebrio molitor ; Toll Receptors</subject><ispartof>The Journal of biological chemistry, 2010-10, Vol.285 (43), p.32937-32945</ispartof><rights>2010 © 2010 ASBMB. Currently published by Elsevier Inc; originally published by American Society for Biochemistry and Molecular Biology.</rights><rights>2010 by The American Society for Biochemistry and Molecular Biology, Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c642t-7d3803f9a69e1b32065031acb1add4b3535e159bf34fd0ab10a8e6b293dbb42b3</citedby><cites>FETCH-LOGICAL-c642t-7d3803f9a69e1b32065031acb1add4b3535e159bf34fd0ab10a8e6b293dbb42b3</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/PMC2963372/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2963372/$$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/20702416$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yu, Yang</creatorcontrib><creatorcontrib>Park, Ji-Won</creatorcontrib><creatorcontrib>Kwon, Hyun-Mi</creatorcontrib><creatorcontrib>Hwang, Hyun-Ok</creatorcontrib><creatorcontrib>Jang, In-Hwan</creatorcontrib><creatorcontrib>Masuda, Akiko</creatorcontrib><creatorcontrib>Kurokawa, Kenji</creatorcontrib><creatorcontrib>Nakayama, Hiroshi</creatorcontrib><creatorcontrib>Lee, Won-Jae</creatorcontrib><creatorcontrib>Dohmae, Naoshi</creatorcontrib><creatorcontrib>Zhang, Jinghai</creatorcontrib><creatorcontrib>Lee, Bok Luel</creatorcontrib><title>Diversity of Innate Immune Recognition Mechanism for Bacterial Polymeric meso-Diaminopimelic Acid-type Peptidoglycan in Insects</title><title>The Journal of biological chemistry</title><addtitle>J Biol Chem</addtitle><description>In Drosophila, the synthesis of antimicrobial peptides in response to microbial infections is under the control of the Toll and immune deficiency (Imd) signaling pathway. The Toll signaling pathway responds mainly to the lysine-type peptidoglycan of Gram-positive bacteria and fungal β-1,3-glucan, whereas the Imd pathway responds to the meso-diaminopimelic acid (DAP)-type peptidoglycan of Gram-negative bacteria and certain Gram-positive bacilli. Recently we determined the activation mechanism of a Toll signaling pathway biochemically using a large beetle, Tenebrio molitor. However, DAP-type peptidoglycan recognition mechanism and its signaling pathway are still unclear in the fly and beetle. Here, we show that polymeric DAP-type peptidoglycan, but not its monomeric form, formed a complex with Tenebrio peptidoglycan recognition protein-SA, and this complex activated the three-step proteolytic cascade to produce processed Spätzle, a Toll receptor ligand, and induced Drosophila defensin-like antimicrobial peptide in Tenebrio larvae similarly to polymeric lysine-type peptidoglycan. Monomeric DAP-type peptidoglycan induced Drosophila diptericin-like antimicrobial peptide in Tenebrio hemocytes. In addition, both polymeric and monomeric DAP-type peptidoglycans induced expression of Tenebrio peptidoglycan recognition protein-SC2, which is DAP-type peptidoglycan-selective N-acetylmuramyl-l-alanine amidase that functions as a DAP-type peptidoglycan scavenger, appearing to function as a negative regulator of the DAP-type peptidoglycan signaling by cleaving DAP-type peptidoglycan in Tenebrio larvae. Taken together, these results demonstrate that molecular recognition mechanism for polymeric DAP-type peptidoglycan is different between Tenebrio larvae and Drosophila adults, providing biochemical evidences of biological diversity of innate immune responses in insects.</description><subject>Amidase</subject><subject>Animals</subject><subject>Antimicrobial peptides</subject><subject>b-1,3-Glucan</subject><subject>Bacteria</subject><subject>Bacteria - immunology</subject><subject>Bacteria - metabolism</subject><subject>Base Sequence</subject><subject>beta -1,3-Glucan</subject><subject>Biological diversity</subject><subject>Carrier Proteins - genetics</subject><subject>Carrier Proteins - immunology</subject><subject>Carrier Proteins - metabolism</subject><subject>Cell Wall</subject><subject>Defensins - biosynthesis</subject><subject>Defensins - genetics</subject><subject>Defensins - immunology</subject><subject>Diaminopimelic Acid</subject><subject>Drosophila</subject><subject>Drosophila melanogaster</subject><subject>Drosophila Proteins - genetics</subject><subject>Drosophila Proteins - immunology</subject><subject>Drosophila Proteins - metabolism</subject><subject>Gram-negative bacteria</subject><subject>Gram-positive bacilli</subject><subject>Gram-positive bacteria</subject><subject>Hemocytes</subject><subject>Humoral Response</subject><subject>Imd Pathway</subject><subject>Immune response</subject><subject>Immunity, Innate - physiology</subject><subject>Immunology</subject><subject>Infection</subject><subject>Innate Immunity</subject><subject>Insect</subject><subject>Insect Proteins - genetics</subject><subject>Insect Proteins - immunology</subject><subject>Insect Proteins - metabolism</subject><subject>Larvae</subject><subject>Molecular Sequence Data</subject><subject>Pattern Recognition Receptor</subject><subject>Peptidoglycan</subject><subject>Peptidoglycan - immunology</subject><subject>Peptidoglycan - metabolism</subject><subject>peptidoglycans</subject><subject>PGRP</subject><subject>Proteolysis</subject><subject>Signal Transduction</subject><subject>Species Specificity</subject><subject>Tenebrio</subject><subject>Tenebrio - genetics</subject><subject>Tenebrio - immunology</subject><subject>Tenebrio - metabolism</subject><subject>Tenebrio - microbiology</subject><subject>Tenebrio molitor</subject><subject>Toll Receptors</subject><issn>0021-9258</issn><issn>1083-351X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkjtvFDEUhUcIRJZATQfuqCbxax5ukELCY6VEREAkOsv23NncaMbe2LMrTZW_Hq82RFAgcOPXd8-1dU5RvGb0iNFGHt9Yd3TBdjspKZNPigWjrShFxX4-LRaUclYqXrUHxYuUbmgeUrHnxQGnDeWS1Yvi7gy3EBNOMwk9WXpvJiDLcdx4IN_AhZXHCYMnF-Cujcc0kj5E8sG4CSKagVyGYR7z0pERUijP0IzowxpHGPLZicOunOY1kEtYT9iF1TA74wn63CqBm9LL4llvhgSvHubD4urTxx-nX8rzr5-Xpyfnpasln8qmEy0VvTK1AmYFp3VFBTPOMtN10opKVMAqZXsh-44ay6hpobZcic5aya04LN7vddcbO0LnwE_RDHodcTRx1sGg_vPG47Veha3mqhai4Vng3YNADLcbSJMeMTkYBuMhbJJuGyWbRjH1H6RkGeT1P8mmUkxkd3fk8Z50MaQUoX98OaN6lwSdk6B3SdD7JOSKN79_-JH_ZX0G3u6B3gRtVhGTvvrOKROUtaqtKc2E2hOQjdkiRJ0cgnfQYcze6S7gX9vfAx28zkI</recordid><startdate>20101022</startdate><enddate>20101022</enddate><creator>Yu, Yang</creator><creator>Park, Ji-Won</creator><creator>Kwon, Hyun-Mi</creator><creator>Hwang, Hyun-Ok</creator><creator>Jang, In-Hwan</creator><creator>Masuda, Akiko</creator><creator>Kurokawa, Kenji</creator><creator>Nakayama, Hiroshi</creator><creator>Lee, Won-Jae</creator><creator>Dohmae, Naoshi</creator><creator>Zhang, Jinghai</creator><creator>Lee, Bok Luel</creator><general>Elsevier Inc</general><general>American Society for Biochemistry and Molecular Biology</general><scope>6I.</scope><scope>AAFTH</scope><scope>FBQ</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>7X8</scope><scope>7QL</scope><scope>7SS</scope><scope>7T5</scope><scope>C1K</scope><scope>H94</scope><scope>7T7</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>5PM</scope></search><sort><creationdate>20101022</creationdate><title>Diversity of Innate Immune Recognition Mechanism for Bacterial Polymeric meso-Diaminopimelic Acid-type Peptidoglycan in Insects</title><author>Yu, Yang ; Park, Ji-Won ; Kwon, Hyun-Mi ; Hwang, Hyun-Ok ; Jang, In-Hwan ; Masuda, Akiko ; Kurokawa, Kenji ; Nakayama, Hiroshi ; Lee, Won-Jae ; Dohmae, Naoshi ; Zhang, Jinghai ; Lee, Bok Luel</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c642t-7d3803f9a69e1b32065031acb1add4b3535e159bf34fd0ab10a8e6b293dbb42b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Amidase</topic><topic>Animals</topic><topic>Antimicrobial peptides</topic><topic>b-1,3-Glucan</topic><topic>Bacteria</topic><topic>Bacteria - immunology</topic><topic>Bacteria - metabolism</topic><topic>Base Sequence</topic><topic>beta -1,3-Glucan</topic><topic>Biological diversity</topic><topic>Carrier Proteins - genetics</topic><topic>Carrier Proteins - immunology</topic><topic>Carrier Proteins - metabolism</topic><topic>Cell Wall</topic><topic>Defensins - biosynthesis</topic><topic>Defensins - genetics</topic><topic>Defensins - immunology</topic><topic>Diaminopimelic Acid</topic><topic>Drosophila</topic><topic>Drosophila melanogaster</topic><topic>Drosophila Proteins - genetics</topic><topic>Drosophila Proteins - immunology</topic><topic>Drosophila Proteins - metabolism</topic><topic>Gram-negative bacteria</topic><topic>Gram-positive bacilli</topic><topic>Gram-positive bacteria</topic><topic>Hemocytes</topic><topic>Humoral Response</topic><topic>Imd Pathway</topic><topic>Immune response</topic><topic>Immunity, Innate - physiology</topic><topic>Immunology</topic><topic>Infection</topic><topic>Innate Immunity</topic><topic>Insect</topic><topic>Insect Proteins - genetics</topic><topic>Insect Proteins - immunology</topic><topic>Insect Proteins - metabolism</topic><topic>Larvae</topic><topic>Molecular Sequence Data</topic><topic>Pattern Recognition Receptor</topic><topic>Peptidoglycan</topic><topic>Peptidoglycan - immunology</topic><topic>Peptidoglycan - metabolism</topic><topic>peptidoglycans</topic><topic>PGRP</topic><topic>Proteolysis</topic><topic>Signal Transduction</topic><topic>Species Specificity</topic><topic>Tenebrio</topic><topic>Tenebrio - genetics</topic><topic>Tenebrio - immunology</topic><topic>Tenebrio - metabolism</topic><topic>Tenebrio - microbiology</topic><topic>Tenebrio molitor</topic><topic>Toll Receptors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yu, Yang</creatorcontrib><creatorcontrib>Park, Ji-Won</creatorcontrib><creatorcontrib>Kwon, Hyun-Mi</creatorcontrib><creatorcontrib>Hwang, Hyun-Ok</creatorcontrib><creatorcontrib>Jang, In-Hwan</creatorcontrib><creatorcontrib>Masuda, Akiko</creatorcontrib><creatorcontrib>Kurokawa, Kenji</creatorcontrib><creatorcontrib>Nakayama, Hiroshi</creatorcontrib><creatorcontrib>Lee, Won-Jae</creatorcontrib><creatorcontrib>Dohmae, Naoshi</creatorcontrib><creatorcontrib>Zhang, Jinghai</creatorcontrib><creatorcontrib>Lee, Bok Luel</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of biological chemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yu, Yang</au><au>Park, Ji-Won</au><au>Kwon, Hyun-Mi</au><au>Hwang, Hyun-Ok</au><au>Jang, In-Hwan</au><au>Masuda, Akiko</au><au>Kurokawa, Kenji</au><au>Nakayama, Hiroshi</au><au>Lee, Won-Jae</au><au>Dohmae, Naoshi</au><au>Zhang, Jinghai</au><au>Lee, Bok Luel</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Diversity of Innate Immune Recognition Mechanism for Bacterial Polymeric meso-Diaminopimelic Acid-type Peptidoglycan in Insects</atitle><jtitle>The Journal of biological chemistry</jtitle><addtitle>J Biol Chem</addtitle><date>2010-10-22</date><risdate>2010</risdate><volume>285</volume><issue>43</issue><spage>32937</spage><epage>32945</epage><pages>32937-32945</pages><issn>0021-9258</issn><eissn>1083-351X</eissn><abstract>In Drosophila, the synthesis of antimicrobial peptides in response to microbial infections is under the control of the Toll and immune deficiency (Imd) signaling pathway. The Toll signaling pathway responds mainly to the lysine-type peptidoglycan of Gram-positive bacteria and fungal β-1,3-glucan, whereas the Imd pathway responds to the meso-diaminopimelic acid (DAP)-type peptidoglycan of Gram-negative bacteria and certain Gram-positive bacilli. Recently we determined the activation mechanism of a Toll signaling pathway biochemically using a large beetle, Tenebrio molitor. However, DAP-type peptidoglycan recognition mechanism and its signaling pathway are still unclear in the fly and beetle. Here, we show that polymeric DAP-type peptidoglycan, but not its monomeric form, formed a complex with Tenebrio peptidoglycan recognition protein-SA, and this complex activated the three-step proteolytic cascade to produce processed Spätzle, a Toll receptor ligand, and induced Drosophila defensin-like antimicrobial peptide in Tenebrio larvae similarly to polymeric lysine-type peptidoglycan. Monomeric DAP-type peptidoglycan induced Drosophila diptericin-like antimicrobial peptide in Tenebrio hemocytes. In addition, both polymeric and monomeric DAP-type peptidoglycans induced expression of Tenebrio peptidoglycan recognition protein-SC2, which is DAP-type peptidoglycan-selective N-acetylmuramyl-l-alanine amidase that functions as a DAP-type peptidoglycan scavenger, appearing to function as a negative regulator of the DAP-type peptidoglycan signaling by cleaving DAP-type peptidoglycan in Tenebrio larvae. Taken together, these results demonstrate that molecular recognition mechanism for polymeric DAP-type peptidoglycan is different between Tenebrio larvae and Drosophila adults, providing biochemical evidences of biological diversity of innate immune responses in insects.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>20702416</pmid><doi>10.1074/jbc.M110.144014</doi><tpages>9</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Amidase Animals Antimicrobial peptides b-1,3-Glucan Bacteria Bacteria - immunology Bacteria - metabolism Base Sequence beta -1,3-Glucan Biological diversity Carrier Proteins - genetics Carrier Proteins - immunology Carrier Proteins - metabolism Cell Wall Defensins - biosynthesis Defensins - genetics Defensins - immunology Diaminopimelic Acid Drosophila Drosophila melanogaster Drosophila Proteins - genetics Drosophila Proteins - immunology Drosophila Proteins - metabolism Gram-negative bacteria Gram-positive bacilli Gram-positive bacteria Hemocytes Humoral Response Imd Pathway Immune response Immunity, Innate - physiology Immunology Infection Innate Immunity Insect Insect Proteins - genetics Insect Proteins - immunology Insect Proteins - metabolism Larvae Molecular Sequence Data Pattern Recognition Receptor Peptidoglycan Peptidoglycan - immunology Peptidoglycan - metabolism peptidoglycans PGRP Proteolysis Signal Transduction Species Specificity Tenebrio Tenebrio - genetics Tenebrio - immunology Tenebrio - metabolism Tenebrio - microbiology Tenebrio molitor Toll Receptors |
| title | Diversity of Innate Immune Recognition Mechanism for Bacterial Polymeric meso-Diaminopimelic Acid-type Peptidoglycan in Insects |
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