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Recognition of nonself is necessary to activate Drosophila's immune response against an insect parasite
Innate immune responses can be activated by pathogen-associated molecular patterns (PAMPs), danger signals released by damaged tissues, or the absence of self-molecules that inhibit immunity. As PAMPs are typically conserved across broad groups of pathogens but absent from the host, it is unclear wh...
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Published in: | BMC biology 2024-04, Vol.22 (1), p.89-89, Article 89 |
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description | Innate immune responses can be activated by pathogen-associated molecular patterns (PAMPs), danger signals released by damaged tissues, or the absence of self-molecules that inhibit immunity. As PAMPs are typically conserved across broad groups of pathogens but absent from the host, it is unclear whether they allow hosts to recognize parasites that are phylogenetically similar to themselves, such as parasitoid wasps infecting insects.
Parasitoids must penetrate the cuticle of Drosophila larvae to inject their eggs. In line with previous results, we found that the danger signal of wounding triggers the differentiation of specialized immune cells called lamellocytes. However, using oil droplets to mimic infection by a parasitoid wasp egg, we found that this does not activate the melanization response. This aspect of the immune response also requires exposure to parasite molecules. The unidentified factor enhances the transcriptional response in hemocytes and induces a specific response in the fat body.
We conclude that a combination of danger signals and the recognition of nonself molecules is required to activate Drosophila's immune response against parasitic insects. |
doi_str_mv | 10.1186/s12915-024-01886-1 |
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Parasitoids must penetrate the cuticle of Drosophila larvae to inject their eggs. In line with previous results, we found that the danger signal of wounding triggers the differentiation of specialized immune cells called lamellocytes. However, using oil droplets to mimic infection by a parasitoid wasp egg, we found that this does not activate the melanization response. This aspect of the immune response also requires exposure to parasite molecules. The unidentified factor enhances the transcriptional response in hemocytes and induces a specific response in the fat body.
We conclude that a combination of danger signals and the recognition of nonself molecules is required to activate Drosophila's immune response against parasitic insects.</description><identifier>ISSN: 1741-7007</identifier><identifier>EISSN: 1741-7007</identifier><identifier>DOI: 10.1186/s12915-024-01886-1</identifier><identifier>PMID: 38644510</identifier><language>eng</language><publisher>England: BioMed Central Ltd</publisher><subject>Analysis ; Animals ; Cell differentiation ; Control ; Defence mechanisms ; Diseases and pests ; Drosophila ; Drosophila - immunology ; Drosophila - parasitology ; Drosophila melanogaster ; Drosophila melanogaster - immunology ; Drosophila melanogaster - parasitology ; Drosophila melanogaster - physiology ; Eggs ; Fat body ; Females ; Fruit flies ; Genetic aspects ; Growth ; Hemocytes ; Hemocytes - immunology ; Host-Parasite Interactions - immunology ; Identification and classification ; Immune recognition ; Immune response ; Immune system ; Immunity ; Immunity, Innate ; Infections ; Innate immunity ; Insects ; Larva - immunology ; Larva - parasitology ; Larvae ; Melanization ; Parasites ; Parasitoid wasps ; Parasitoids ; Pathogens ; Phylogeny ; Proteins ; Recognition ; Scientific equipment and supplies industry ; Tomatoes ; Wasps ; Wasps - physiology ; Wounding</subject><ispartof>BMC biology, 2024-04, Vol.22 (1), p.89-89, Article 89</ispartof><rights>2024. The Author(s).</rights><rights>COPYRIGHT 2024 BioMed Central Ltd.</rights><rights>2024. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>The Author(s) 2024</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c583t-b73ef8d2a8d0f49c825448d7b00a1c34b6d2bb187db1a8724abc9bcf6478dc973</cites><orcidid>0000-0001-7470-8157</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/3054143175/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/3054143175?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,25731,27901,27902,36989,36990,44566,53766,53768,74869</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38644510$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Leitão, Alexandre B</creatorcontrib><creatorcontrib>Arunkumar, Ramesh</creatorcontrib><creatorcontrib>Day, Jonathan P</creatorcontrib><creatorcontrib>Hanna, Nancy</creatorcontrib><creatorcontrib>Devi, Aarathi</creatorcontrib><creatorcontrib>Hayes, Matthew P</creatorcontrib><creatorcontrib>Jiggins, Francis M</creatorcontrib><title>Recognition of nonself is necessary to activate Drosophila's immune response against an insect parasite</title><title>BMC biology</title><addtitle>BMC Biol</addtitle><description>Innate immune responses can be activated by pathogen-associated molecular patterns (PAMPs), danger signals released by damaged tissues, or the absence of self-molecules that inhibit immunity. As PAMPs are typically conserved across broad groups of pathogens but absent from the host, it is unclear whether they allow hosts to recognize parasites that are phylogenetically similar to themselves, such as parasitoid wasps infecting insects.
Parasitoids must penetrate the cuticle of Drosophila larvae to inject their eggs. In line with previous results, we found that the danger signal of wounding triggers the differentiation of specialized immune cells called lamellocytes. However, using oil droplets to mimic infection by a parasitoid wasp egg, we found that this does not activate the melanization response. This aspect of the immune response also requires exposure to parasite molecules. The unidentified factor enhances the transcriptional response in hemocytes and induces a specific response in the fat body.
We conclude that a combination of danger signals and the recognition of nonself molecules is required to activate Drosophila's immune response against parasitic insects.</description><subject>Analysis</subject><subject>Animals</subject><subject>Cell differentiation</subject><subject>Control</subject><subject>Defence mechanisms</subject><subject>Diseases and pests</subject><subject>Drosophila</subject><subject>Drosophila - immunology</subject><subject>Drosophila - parasitology</subject><subject>Drosophila melanogaster</subject><subject>Drosophila melanogaster - immunology</subject><subject>Drosophila melanogaster - parasitology</subject><subject>Drosophila melanogaster - physiology</subject><subject>Eggs</subject><subject>Fat body</subject><subject>Females</subject><subject>Fruit flies</subject><subject>Genetic aspects</subject><subject>Growth</subject><subject>Hemocytes</subject><subject>Hemocytes - immunology</subject><subject>Host-Parasite Interactions - immunology</subject><subject>Identification and classification</subject><subject>Immune recognition</subject><subject>Immune response</subject><subject>Immune system</subject><subject>Immunity</subject><subject>Immunity, Innate</subject><subject>Infections</subject><subject>Innate immunity</subject><subject>Insects</subject><subject>Larva - immunology</subject><subject>Larva - parasitology</subject><subject>Larvae</subject><subject>Melanization</subject><subject>Parasites</subject><subject>Parasitoid wasps</subject><subject>Parasitoids</subject><subject>Pathogens</subject><subject>Phylogeny</subject><subject>Proteins</subject><subject>Recognition</subject><subject>Scientific equipment and supplies industry</subject><subject>Tomatoes</subject><subject>Wasps</subject><subject>Wasps - physiology</subject><subject>Wounding</subject><issn>1741-7007</issn><issn>1741-7007</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNqNkk1v1DAQhiMEoqXwBzggSxyAQ4ondmLnhKrytVKlSuXjatnOJPUqsbexU8G_x9stpYs4IB_GGj_va83oLYrnQI8BZPM2QtVCXdKKlxSkbEp4UByC4FAKSsXDe_eD4kmMa0qrWgj2uDhgsuG8BnpYDBdow-BdcsGT0BMffMSxJy4SjxZj1PNPkgLRNrlrnZC8n0MMm0s36leRuGlaPJIZ42arI3rQzsdEtCe5ok1ko2cdXcKnxaNejxGf3daj4tvHD19PP5dn559Wpydnpa0lS6URDHvZVVp2tOetlVXNueyEoVSDZdw0XWUMSNEZ0FJUXBvbGts3XMjOtoIdFaudbxf0Wm1mN-UBVNBO3TTCPCg9J2dHVB2ytoNsYEzNkUErwDDWmqrqKcNGZ693O6_NYibsLPo063HPdP_Fu0s1hGsFQBmndZMdXt86zOFqwZjU5KLFcdQewxIVo5wJSRvZZvTlX-g6LLPPu8pUzYEzEPUfatB5Auf7kD-2W1N1IlqgDW0ryNTxP6h8OpycDR57l_t7gjd7gswk_JEGvcSoVl8u_p89_77PVjvW5tTEGfu75QFV2wyrXYZVzrC6ybDail7cX_ud5Hdo2S-Md-st</recordid><startdate>20240422</startdate><enddate>20240422</enddate><creator>Leitão, Alexandre B</creator><creator>Arunkumar, Ramesh</creator><creator>Day, Jonathan P</creator><creator>Hanna, Nancy</creator><creator>Devi, Aarathi</creator><creator>Hayes, Matthew P</creator><creator>Jiggins, Francis M</creator><general>BioMed Central Ltd</general><general>BioMed Central</general><general>BMC</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>4U-</scope><scope>7QG</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P64</scope><scope>PADUT</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-7470-8157</orcidid></search><sort><creationdate>20240422</creationdate><title>Recognition of nonself is necessary to activate Drosophila's immune response against an insect parasite</title><author>Leitão, Alexandre B ; Arunkumar, Ramesh ; Day, Jonathan P ; Hanna, Nancy ; Devi, Aarathi ; Hayes, Matthew P ; Jiggins, Francis M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c583t-b73ef8d2a8d0f49c825448d7b00a1c34b6d2bb187db1a8724abc9bcf6478dc973</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Analysis</topic><topic>Animals</topic><topic>Cell differentiation</topic><topic>Control</topic><topic>Defence mechanisms</topic><topic>Diseases and pests</topic><topic>Drosophila</topic><topic>Drosophila - immunology</topic><topic>Drosophila - parasitology</topic><topic>Drosophila melanogaster</topic><topic>Drosophila melanogaster - immunology</topic><topic>Drosophila melanogaster - parasitology</topic><topic>Drosophila melanogaster - physiology</topic><topic>Eggs</topic><topic>Fat body</topic><topic>Females</topic><topic>Fruit flies</topic><topic>Genetic aspects</topic><topic>Growth</topic><topic>Hemocytes</topic><topic>Hemocytes - immunology</topic><topic>Host-Parasite Interactions - immunology</topic><topic>Identification and classification</topic><topic>Immune recognition</topic><topic>Immune response</topic><topic>Immune system</topic><topic>Immunity</topic><topic>Immunity, Innate</topic><topic>Infections</topic><topic>Innate immunity</topic><topic>Insects</topic><topic>Larva - immunology</topic><topic>Larva - parasitology</topic><topic>Larvae</topic><topic>Melanization</topic><topic>Parasites</topic><topic>Parasitoid wasps</topic><topic>Parasitoids</topic><topic>Pathogens</topic><topic>Phylogeny</topic><topic>Proteins</topic><topic>Recognition</topic><topic>Scientific equipment and supplies industry</topic><topic>Tomatoes</topic><topic>Wasps</topic><topic>Wasps - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>BMC biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Leitão, Alexandre B</au><au>Arunkumar, Ramesh</au><au>Day, Jonathan P</au><au>Hanna, Nancy</au><au>Devi, Aarathi</au><au>Hayes, Matthew P</au><au>Jiggins, Francis M</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Recognition of nonself is necessary to activate Drosophila's immune response against an insect parasite</atitle><jtitle>BMC biology</jtitle><addtitle>BMC Biol</addtitle><date>2024-04-22</date><risdate>2024</risdate><volume>22</volume><issue>1</issue><spage>89</spage><epage>89</epage><pages>89-89</pages><artnum>89</artnum><issn>1741-7007</issn><eissn>1741-7007</eissn><abstract>Innate immune responses can be activated by pathogen-associated molecular patterns (PAMPs), danger signals released by damaged tissues, or the absence of self-molecules that inhibit immunity. As PAMPs are typically conserved across broad groups of pathogens but absent from the host, it is unclear whether they allow hosts to recognize parasites that are phylogenetically similar to themselves, such as parasitoid wasps infecting insects.
Parasitoids must penetrate the cuticle of Drosophila larvae to inject their eggs. In line with previous results, we found that the danger signal of wounding triggers the differentiation of specialized immune cells called lamellocytes. However, using oil droplets to mimic infection by a parasitoid wasp egg, we found that this does not activate the melanization response. This aspect of the immune response also requires exposure to parasite molecules. The unidentified factor enhances the transcriptional response in hemocytes and induces a specific response in the fat body.
We conclude that a combination of danger signals and the recognition of nonself molecules is required to activate Drosophila's immune response against parasitic insects.</abstract><cop>England</cop><pub>BioMed Central Ltd</pub><pmid>38644510</pmid><doi>10.1186/s12915-024-01886-1</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0001-7470-8157</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Analysis Animals Cell differentiation Control Defence mechanisms Diseases and pests Drosophila Drosophila - immunology Drosophila - parasitology Drosophila melanogaster Drosophila melanogaster - immunology Drosophila melanogaster - parasitology Drosophila melanogaster - physiology Eggs Fat body Females Fruit flies Genetic aspects Growth Hemocytes Hemocytes - immunology Host-Parasite Interactions - immunology Identification and classification Immune recognition Immune response Immune system Immunity Immunity, Innate Infections Innate immunity Insects Larva - immunology Larva - parasitology Larvae Melanization Parasites Parasitoid wasps Parasitoids Pathogens Phylogeny Proteins Recognition Scientific equipment and supplies industry Tomatoes Wasps Wasps - physiology Wounding |
title | Recognition of nonself is necessary to activate Drosophila's immune response against an insect parasite |
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