Methyl farnesoate plays a dual role in regulating Drosophila metamorphosis
Corpus allatum (CA) ablation results in juvenile hormone (JH) deficiency and pupal lethality in Drosophila. The fly CA produces and releases three sesquiterpenoid hormones: JH III bisepoxide (JHB3), JH III, and methyl farnesoate (MF). In the whole body extracts, MF is the most abundant sesquiterpeno...
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creator | Wen, Di Rivera-Perez, Crisalejandra Abdou, Mohamed Jia, Qiangqiang He, Qianyu Liu, Xi Zyaan, Ola Xu, Jingjing Bendena, William G Tobe, Stephen S Noriega, Fernando G Palli, Subba R Wang, Jian Li, Sheng |
description | Corpus allatum (CA) ablation results in juvenile hormone (JH) deficiency and pupal lethality in Drosophila. The fly CA produces and releases three sesquiterpenoid hormones: JH III bisepoxide (JHB3), JH III, and methyl farnesoate (MF). In the whole body extracts, MF is the most abundant sesquiterpenoid, followed by JHB3 and JH III. Knockout of JH acid methyl transferase (jhamt) did not result in lethality; it decreased biosynthesis of JHB3, but MF biosynthesis was not affected. RNAi-mediated reduction of 3-hydroxy-3-methylglutaryl CoA reductase (hmgcr) expression in the CA decreased biosynthesis and titers of the three sesquiterpenoids, resulting in partial lethality. Reducing hmgcr expression in the CA of the jhamt mutant further decreased MF titer to a very low level, and caused complete lethality. JH III, JHB3, and MF function through Met and Gce, the two JH receptors, and induce expression of Kr-h1, a JH primary-response gene. As well, a portion of MF is converted to JHB3 in the hemolymph or peripheral tissues. Topical application of JHB3, JH III, or MF precluded lethality in JH-deficient animals, but not in the Met gce double mutant. Taken together, these experiments show that MF is produced by the larval CA and released into the hemolymph, from where it exerts its anti-metamorphic effects indirectly after conversion to JHB3, as well as acting as a hormone itself through the two JH receptors, Met and Gce. |
doi_str_mv | 10.1371/journal.pgen.1005038 |
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The fly CA produces and releases three sesquiterpenoid hormones: JH III bisepoxide (JHB3), JH III, and methyl farnesoate (MF). In the whole body extracts, MF is the most abundant sesquiterpenoid, followed by JHB3 and JH III. Knockout of JH acid methyl transferase (jhamt) did not result in lethality; it decreased biosynthesis of JHB3, but MF biosynthesis was not affected. RNAi-mediated reduction of 3-hydroxy-3-methylglutaryl CoA reductase (hmgcr) expression in the CA decreased biosynthesis and titers of the three sesquiterpenoids, resulting in partial lethality. Reducing hmgcr expression in the CA of the jhamt mutant further decreased MF titer to a very low level, and caused complete lethality. JH III, JHB3, and MF function through Met and Gce, the two JH receptors, and induce expression of Kr-h1, a JH primary-response gene. As well, a portion of MF is converted to JHB3 in the hemolymph or peripheral tissues. Topical application of JHB3, JH III, or MF precluded lethality in JH-deficient animals, but not in the Met gce double mutant. Taken together, these experiments show that MF is produced by the larval CA and released into the hemolymph, from where it exerts its anti-metamorphic effects indirectly after conversion to JHB3, as well as acting as a hormone itself through the two JH receptors, Met and Gce.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1005038</identifier><identifier>PMID: 25774983</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acids ; Animals ; Basic Helix-Loop-Helix Transcription Factors - genetics ; Basic Helix-Loop-Helix Transcription Factors - metabolism ; Biosynthesis ; Corpora Allata - growth & development ; Corpora Allata - metabolism ; Drosophila ; Drosophila melanogaster - genetics ; Drosophila melanogaster - growth & development ; Drosophila Proteins - biosynthesis ; Drosophila Proteins - genetics ; Drosophila Proteins - metabolism ; Enzymes ; Experiments ; Fatty Acids, Monounsaturated - metabolism ; Fatty Acids, Unsaturated - biosynthesis ; Fatty Acids, Unsaturated - genetics ; Fatty Acids, Unsaturated - metabolism ; Genetic aspects ; Hydroxymethylglutaryl CoA Reductases - biosynthesis ; Hydroxymethylglutaryl CoA Reductases - genetics ; Identification and classification ; Insects ; Kruppel-Like Transcription Factors - genetics ; Kruppel-Like Transcription Factors - metabolism ; Larva ; Metamorphosis, Biological - genetics ; Methyltransferases - biosynthesis ; Methyltransferases - genetics ; Physiological aspects ; Protein synthesis ; Pupa ; Terpenoids ; Transcription Factors - genetics ; Transcription Factors - metabolism</subject><ispartof>PLoS genetics, 2015-03, Vol.11 (3), p.e1005038-e1005038</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Wen et al 2015 Wen et al</rights><rights>2015 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Metamorphosis. PLoS Genet 11(3): e1005038. doi:10.1371/journal.pgen.1005038</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c764t-3fce51e6fcc3f12b8010c0fcdeb63ac8eb6a3514fb61e9ff8e3200d9636090ef3</citedby><cites>FETCH-LOGICAL-c764t-3fce51e6fcc3f12b8010c0fcdeb63ac8eb6a3514fb61e9ff8e3200d9636090ef3</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/PMC4361637/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4361637/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,729,782,786,866,887,2106,2932,23875,27933,27934,53800,53802</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25774983$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Schoofs, Liliane</contributor><creatorcontrib>Wen, Di</creatorcontrib><creatorcontrib>Rivera-Perez, Crisalejandra</creatorcontrib><creatorcontrib>Abdou, Mohamed</creatorcontrib><creatorcontrib>Jia, Qiangqiang</creatorcontrib><creatorcontrib>He, Qianyu</creatorcontrib><creatorcontrib>Liu, Xi</creatorcontrib><creatorcontrib>Zyaan, Ola</creatorcontrib><creatorcontrib>Xu, Jingjing</creatorcontrib><creatorcontrib>Bendena, William G</creatorcontrib><creatorcontrib>Tobe, Stephen S</creatorcontrib><creatorcontrib>Noriega, Fernando G</creatorcontrib><creatorcontrib>Palli, Subba R</creatorcontrib><creatorcontrib>Wang, Jian</creatorcontrib><creatorcontrib>Li, Sheng</creatorcontrib><title>Methyl farnesoate plays a dual role in regulating Drosophila metamorphosis</title><title>PLoS genetics</title><addtitle>PLoS Genet</addtitle><description>Corpus allatum (CA) ablation results in juvenile hormone (JH) deficiency and pupal lethality in Drosophila. The fly CA produces and releases three sesquiterpenoid hormones: JH III bisepoxide (JHB3), JH III, and methyl farnesoate (MF). In the whole body extracts, MF is the most abundant sesquiterpenoid, followed by JHB3 and JH III. Knockout of JH acid methyl transferase (jhamt) did not result in lethality; it decreased biosynthesis of JHB3, but MF biosynthesis was not affected. RNAi-mediated reduction of 3-hydroxy-3-methylglutaryl CoA reductase (hmgcr) expression in the CA decreased biosynthesis and titers of the three sesquiterpenoids, resulting in partial lethality. Reducing hmgcr expression in the CA of the jhamt mutant further decreased MF titer to a very low level, and caused complete lethality. JH III, JHB3, and MF function through Met and Gce, the two JH receptors, and induce expression of Kr-h1, a JH primary-response gene. As well, a portion of MF is converted to JHB3 in the hemolymph or peripheral tissues. Topical application of JHB3, JH III, or MF precluded lethality in JH-deficient animals, but not in the Met gce double mutant. Taken together, these experiments show that MF is produced by the larval CA and released into the hemolymph, from where it exerts its anti-metamorphic effects indirectly after conversion to JHB3, as well as acting as a hormone itself through the two JH receptors, Met and Gce.</description><subject>Acids</subject><subject>Animals</subject><subject>Basic Helix-Loop-Helix Transcription Factors - genetics</subject><subject>Basic Helix-Loop-Helix Transcription Factors - metabolism</subject><subject>Biosynthesis</subject><subject>Corpora Allata - growth & development</subject><subject>Corpora Allata - metabolism</subject><subject>Drosophila</subject><subject>Drosophila melanogaster - genetics</subject><subject>Drosophila melanogaster - growth & development</subject><subject>Drosophila Proteins - biosynthesis</subject><subject>Drosophila Proteins - genetics</subject><subject>Drosophila Proteins - metabolism</subject><subject>Enzymes</subject><subject>Experiments</subject><subject>Fatty Acids, Monounsaturated - metabolism</subject><subject>Fatty Acids, Unsaturated - biosynthesis</subject><subject>Fatty Acids, Unsaturated - genetics</subject><subject>Fatty Acids, Unsaturated - metabolism</subject><subject>Genetic aspects</subject><subject>Hydroxymethylglutaryl CoA Reductases - biosynthesis</subject><subject>Hydroxymethylglutaryl CoA Reductases - genetics</subject><subject>Identification and classification</subject><subject>Insects</subject><subject>Kruppel-Like Transcription Factors - genetics</subject><subject>Kruppel-Like Transcription Factors - metabolism</subject><subject>Larva</subject><subject>Metamorphosis, Biological - genetics</subject><subject>Methyltransferases - biosynthesis</subject><subject>Methyltransferases - genetics</subject><subject>Physiological aspects</subject><subject>Protein synthesis</subject><subject>Pupa</subject><subject>Terpenoids</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><issn>1553-7404</issn><issn>1553-7390</issn><issn>1553-7404</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNqVkl2P1CAUhhujcdfVf2C0iYnRixlhoJTebLJZv8asbuLXLaH00DKhpQI1zr-XcWY308QLhYtD4HlfCOfNsscYLTEp8auNm_wg7XJsYVhihApE-J3sFBcFWZQU0btH65PsQQgbhEjBq_J-drIqypJWnJxmHz5C7LY219IPEJyMkI9WbkMu82aSNvfOQm6G3EM7WRnN0OavvQtu7IyVeQ9R9s6PnQsmPMzuaWkDPDrUs-zb2zdfL98vrq7frS8vrhaqZDQuiFZQYGBaKaLxquYII4W0aqBmRCqeiiQFprpmGCqtOZAVQk3FCEMVAk3Osqd739G6IA7fEARmPKkQL2ki1nuicXIjRm966bfCSSP-bDjfCumjURYEbzRWRQ204IrSuuQVLepVWdasolA1O6_zw21T3UOjYIhe2pnp_GQwnWjdT0EJw4yUyeDFwcC7HxOEKHoTFFgrB3DT7t2MpoH4KqHP9mgr09PMoF1yVDtcXFDMKStwWSVq-RcqzQZ6o9wA2qT9meDlTJCYCL9iK6cQxPrL5_9gP_07e_19zj4_YjuQNnbB2SkaN4Q5SPegSjELHvTtV2MkdsG_6bjYBV8cgp9kT47bdCu6STr5DRdg_iU</recordid><startdate>20150301</startdate><enddate>20150301</enddate><creator>Wen, Di</creator><creator>Rivera-Perez, Crisalejandra</creator><creator>Abdou, Mohamed</creator><creator>Jia, Qiangqiang</creator><creator>He, Qianyu</creator><creator>Liu, Xi</creator><creator>Zyaan, Ola</creator><creator>Xu, Jingjing</creator><creator>Bendena, William G</creator><creator>Tobe, Stephen S</creator><creator>Noriega, Fernando G</creator><creator>Palli, Subba R</creator><creator>Wang, Jian</creator><creator>Li, Sheng</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>ISN</scope><scope>ISR</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20150301</creationdate><title>Methyl farnesoate plays a dual role in regulating Drosophila metamorphosis</title><author>Wen, Di ; Rivera-Perez, Crisalejandra ; Abdou, Mohamed ; Jia, Qiangqiang ; He, Qianyu ; Liu, Xi ; Zyaan, Ola ; Xu, Jingjing ; Bendena, William G ; Tobe, Stephen S ; Noriega, Fernando G ; Palli, Subba R ; Wang, Jian ; Li, Sheng</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c764t-3fce51e6fcc3f12b8010c0fcdeb63ac8eb6a3514fb61e9ff8e3200d9636090ef3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Acids</topic><topic>Animals</topic><topic>Basic Helix-Loop-Helix Transcription Factors - genetics</topic><topic>Basic Helix-Loop-Helix Transcription Factors - metabolism</topic><topic>Biosynthesis</topic><topic>Corpora Allata - growth & development</topic><topic>Corpora Allata - metabolism</topic><topic>Drosophila</topic><topic>Drosophila melanogaster - genetics</topic><topic>Drosophila melanogaster - growth & development</topic><topic>Drosophila Proteins - biosynthesis</topic><topic>Drosophila Proteins - genetics</topic><topic>Drosophila Proteins - metabolism</topic><topic>Enzymes</topic><topic>Experiments</topic><topic>Fatty Acids, Monounsaturated - metabolism</topic><topic>Fatty Acids, Unsaturated - biosynthesis</topic><topic>Fatty Acids, Unsaturated - genetics</topic><topic>Fatty Acids, Unsaturated - metabolism</topic><topic>Genetic aspects</topic><topic>Hydroxymethylglutaryl CoA Reductases - biosynthesis</topic><topic>Hydroxymethylglutaryl CoA Reductases - genetics</topic><topic>Identification and classification</topic><topic>Insects</topic><topic>Kruppel-Like Transcription Factors - genetics</topic><topic>Kruppel-Like Transcription Factors - metabolism</topic><topic>Larva</topic><topic>Metamorphosis, Biological - genetics</topic><topic>Methyltransferases - biosynthesis</topic><topic>Methyltransferases - genetics</topic><topic>Physiological aspects</topic><topic>Protein synthesis</topic><topic>Pupa</topic><topic>Terpenoids</topic><topic>Transcription Factors - genetics</topic><topic>Transcription Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wen, Di</creatorcontrib><creatorcontrib>Rivera-Perez, Crisalejandra</creatorcontrib><creatorcontrib>Abdou, Mohamed</creatorcontrib><creatorcontrib>Jia, Qiangqiang</creatorcontrib><creatorcontrib>He, Qianyu</creatorcontrib><creatorcontrib>Liu, Xi</creatorcontrib><creatorcontrib>Zyaan, Ola</creatorcontrib><creatorcontrib>Xu, Jingjing</creatorcontrib><creatorcontrib>Bendena, William G</creatorcontrib><creatorcontrib>Tobe, Stephen S</creatorcontrib><creatorcontrib>Noriega, Fernando G</creatorcontrib><creatorcontrib>Palli, Subba R</creatorcontrib><creatorcontrib>Wang, Jian</creatorcontrib><creatorcontrib>Li, Sheng</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wen, Di</au><au>Rivera-Perez, Crisalejandra</au><au>Abdou, Mohamed</au><au>Jia, Qiangqiang</au><au>He, Qianyu</au><au>Liu, Xi</au><au>Zyaan, Ola</au><au>Xu, Jingjing</au><au>Bendena, William G</au><au>Tobe, Stephen S</au><au>Noriega, Fernando G</au><au>Palli, Subba R</au><au>Wang, Jian</au><au>Li, Sheng</au><au>Schoofs, Liliane</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Methyl farnesoate plays a dual role in regulating Drosophila metamorphosis</atitle><jtitle>PLoS genetics</jtitle><addtitle>PLoS Genet</addtitle><date>2015-03-01</date><risdate>2015</risdate><volume>11</volume><issue>3</issue><spage>e1005038</spage><epage>e1005038</epage><pages>e1005038-e1005038</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>Corpus allatum (CA) ablation results in juvenile hormone (JH) deficiency and pupal lethality in Drosophila. The fly CA produces and releases three sesquiterpenoid hormones: JH III bisepoxide (JHB3), JH III, and methyl farnesoate (MF). In the whole body extracts, MF is the most abundant sesquiterpenoid, followed by JHB3 and JH III. Knockout of JH acid methyl transferase (jhamt) did not result in lethality; it decreased biosynthesis of JHB3, but MF biosynthesis was not affected. RNAi-mediated reduction of 3-hydroxy-3-methylglutaryl CoA reductase (hmgcr) expression in the CA decreased biosynthesis and titers of the three sesquiterpenoids, resulting in partial lethality. Reducing hmgcr expression in the CA of the jhamt mutant further decreased MF titer to a very low level, and caused complete lethality. JH III, JHB3, and MF function through Met and Gce, the two JH receptors, and induce expression of Kr-h1, a JH primary-response gene. As well, a portion of MF is converted to JHB3 in the hemolymph or peripheral tissues. Topical application of JHB3, JH III, or MF precluded lethality in JH-deficient animals, but not in the Met gce double mutant. Taken together, these experiments show that MF is produced by the larval CA and released into the hemolymph, from where it exerts its anti-metamorphic effects indirectly after conversion to JHB3, as well as acting as a hormone itself through the two JH receptors, Met and Gce.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25774983</pmid><doi>10.1371/journal.pgen.1005038</doi><oa>free_for_read</oa></addata></record> |
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subjects | Acids Animals Basic Helix-Loop-Helix Transcription Factors - genetics Basic Helix-Loop-Helix Transcription Factors - metabolism Biosynthesis Corpora Allata - growth & development Corpora Allata - metabolism Drosophila Drosophila melanogaster - genetics Drosophila melanogaster - growth & development Drosophila Proteins - biosynthesis Drosophila Proteins - genetics Drosophila Proteins - metabolism Enzymes Experiments Fatty Acids, Monounsaturated - metabolism Fatty Acids, Unsaturated - biosynthesis Fatty Acids, Unsaturated - genetics Fatty Acids, Unsaturated - metabolism Genetic aspects Hydroxymethylglutaryl CoA Reductases - biosynthesis Hydroxymethylglutaryl CoA Reductases - genetics Identification and classification Insects Kruppel-Like Transcription Factors - genetics Kruppel-Like Transcription Factors - metabolism Larva Metamorphosis, Biological - genetics Methyltransferases - biosynthesis Methyltransferases - genetics Physiological aspects Protein synthesis Pupa Terpenoids Transcription Factors - genetics Transcription Factors - metabolism |
title | Methyl farnesoate plays a dual role in regulating Drosophila metamorphosis |
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