The Insulin-Like Proteins dILPs-2/5 Determine Diapause Inducibility in Drosophila
Diapause is an actively induced dormancy that has evolved in Metazoa to resist environmental stresses. In temperate regions, many diapausing insects overwinter at low temperatures by blocking embryonic, larval or adult development. Despite its Afro-tropical origin, Drosophila melanogaster migrated t...
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| Veröffentlicht in: | PloS one 2016-09, Vol.11 (9), p.e0163680-e0163680 |
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| description | Diapause is an actively induced dormancy that has evolved in Metazoa to resist environmental stresses. In temperate regions, many diapausing insects overwinter at low temperatures by blocking embryonic, larval or adult development. Despite its Afro-tropical origin, Drosophila melanogaster migrated to temperate regions of Asia and Europe where females overwinter as adults by arresting gonadal development (reproductive diapause) at temperatures |
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In temperate regions, many diapausing insects overwinter at low temperatures by blocking embryonic, larval or adult development. Despite its Afro-tropical origin, Drosophila melanogaster migrated to temperate regions of Asia and Europe where females overwinter as adults by arresting gonadal development (reproductive diapause) at temperatures <13°C. Recent work in D. melanogaster has implicated the developmental hormones dILPs-2 and/or dILP3, and dILP5, homologues of vertebrate insulin/insulin-like growth factors (IGFs), in reproductive arrest. However, polymorphisms in timeless (tim) and couch potato (cpo) dramatically affect diapause inducibility and these dILP experiments could not exclude this common genetic variation contributing to the diapause phenotype. Here, we apply an extensive genetic dissection of the insulin signaling pathway which allows us to see both enhancements and reductions in egg development that are independent of tim and cpo variations. We show that a number of manipulations dramatically enhance diapause to ~100%. These include ablating, or reducing the excitability of the insulin-producing cells (IPCs) that express dILPs-2,3,5 employing the dilp2,3,5-/- triple mutant, desensitizing insulin signaling using a chico mutation, or inhibiting dILP2 and 5 in the hemolymph by over-expressing Imaginal Morphogenesis Protein-Late 2 (Imp-L2). In addition, triple mutant dilp2,3,5-/- females maintain high levels of diapause even when temperatures are raised in adulthood to 19°C. However at 22°C, these females all show egg development revealing that the effects are conditional on temperature and not a general female sterility. In contrast, over-expression of dilps-2/5 or enhancing IPC excitability, led to levels of ovarian arrest that approached zero, underscoring dILPs-2 and 5 as key antagonists of diapause.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0163680</identifier><identifier>PMID: 27689881</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adults ; Aging ; Antagonists ; Biology ; Biology and Life Sciences ; Cell division ; Desensitization ; Diapause ; Dormancy ; Drosophila ; Drosophila melanogaster ; Earth Sciences ; Embryogenesis ; Environmental stress ; Excitability ; Females ; Gene expression ; Genetic aspects ; Genetic diversity ; Genetic engineering ; Genomes ; Growth factors ; Hemolymph ; Homology ; Hormones ; Insects ; Insulin ; Insulin-like growth factors ; Kinases ; Low temperature ; Medicine and Health Sciences ; Metazoa ; Morphogenesis ; Mutation ; Neurophysiology ; Overexpression ; Pancreatic beta cells ; Phenotypes ; Potatoes ; Proteins ; Research and Analysis Methods ; Signal transduction ; Signaling ; Solanum tuberosum ; Sterility ; Temperature effects ; Timeless protein</subject><ispartof>PloS one, 2016-09, Vol.11 (9), p.e0163680-e0163680</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Schiesari et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://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>2016 Schiesari et al 2016 Schiesari et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c725t-7decda5b7d62835f52c7f53f3b5009f6e675d09050d304655d23570b86183b8a3</citedby><cites>FETCH-LOGICAL-c725t-7decda5b7d62835f52c7f53f3b5009f6e675d09050d304655d23570b86183b8a3</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/PMC5045170/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5045170/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27689881$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Roman, Gregg</contributor><creatorcontrib>Schiesari, Luca</creatorcontrib><creatorcontrib>Andreatta, Gabriele</creatorcontrib><creatorcontrib>Kyriacou, Charalambos P</creatorcontrib><creatorcontrib>O'Connor, Michael B</creatorcontrib><creatorcontrib>Costa, Rodolfo</creatorcontrib><title>The Insulin-Like Proteins dILPs-2/5 Determine Diapause Inducibility in Drosophila</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Diapause is an actively induced dormancy that has evolved in Metazoa to resist environmental stresses. In temperate regions, many diapausing insects overwinter at low temperatures by blocking embryonic, larval or adult development. Despite its Afro-tropical origin, Drosophila melanogaster migrated to temperate regions of Asia and Europe where females overwinter as adults by arresting gonadal development (reproductive diapause) at temperatures <13°C. Recent work in D. melanogaster has implicated the developmental hormones dILPs-2 and/or dILP3, and dILP5, homologues of vertebrate insulin/insulin-like growth factors (IGFs), in reproductive arrest. However, polymorphisms in timeless (tim) and couch potato (cpo) dramatically affect diapause inducibility and these dILP experiments could not exclude this common genetic variation contributing to the diapause phenotype. Here, we apply an extensive genetic dissection of the insulin signaling pathway which allows us to see both enhancements and reductions in egg development that are independent of tim and cpo variations. We show that a number of manipulations dramatically enhance diapause to ~100%. These include ablating, or reducing the excitability of the insulin-producing cells (IPCs) that express dILPs-2,3,5 employing the dilp2,3,5-/- triple mutant, desensitizing insulin signaling using a chico mutation, or inhibiting dILP2 and 5 in the hemolymph by over-expressing Imaginal Morphogenesis Protein-Late 2 (Imp-L2). In addition, triple mutant dilp2,3,5-/- females maintain high levels of diapause even when temperatures are raised in adulthood to 19°C. However at 22°C, these females all show egg development revealing that the effects are conditional on temperature and not a general female sterility. In contrast, over-expression of dilps-2/5 or enhancing IPC excitability, led to levels of ovarian arrest that approached zero, underscoring dILPs-2 and 5 as key antagonists of diapause.</description><subject>Adults</subject><subject>Aging</subject><subject>Antagonists</subject><subject>Biology</subject><subject>Biology and Life Sciences</subject><subject>Cell division</subject><subject>Desensitization</subject><subject>Diapause</subject><subject>Dormancy</subject><subject>Drosophila</subject><subject>Drosophila melanogaster</subject><subject>Earth Sciences</subject><subject>Embryogenesis</subject><subject>Environmental stress</subject><subject>Excitability</subject><subject>Females</subject><subject>Gene expression</subject><subject>Genetic aspects</subject><subject>Genetic diversity</subject><subject>Genetic engineering</subject><subject>Genomes</subject><subject>Growth factors</subject><subject>Hemolymph</subject><subject>Homology</subject><subject>Hormones</subject><subject>Insects</subject><subject>Insulin</subject><subject>Insulin-like growth factors</subject><subject>Kinases</subject><subject>Low temperature</subject><subject>Medicine and Health Sciences</subject><subject>Metazoa</subject><subject>Morphogenesis</subject><subject>Mutation</subject><subject>Neurophysiology</subject><subject>Overexpression</subject><subject>Pancreatic beta cells</subject><subject>Phenotypes</subject><subject>Potatoes</subject><subject>Proteins</subject><subject>Research and Analysis Methods</subject><subject>Signal transduction</subject><subject>Signaling</subject><subject>Solanum tuberosum</subject><subject>Sterility</subject><subject>Temperature effects</subject><subject>Timeless 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Insulin-Like Proteins dILPs-2/5 Determine Diapause Inducibility in Drosophila</title><author>Schiesari, Luca ; Andreatta, Gabriele ; Kyriacou, Charalambos P ; O'Connor, Michael B ; Costa, Rodolfo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c725t-7decda5b7d62835f52c7f53f3b5009f6e675d09050d304655d23570b86183b8a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Adults</topic><topic>Aging</topic><topic>Antagonists</topic><topic>Biology</topic><topic>Biology and Life Sciences</topic><topic>Cell division</topic><topic>Desensitization</topic><topic>Diapause</topic><topic>Dormancy</topic><topic>Drosophila</topic><topic>Drosophila melanogaster</topic><topic>Earth Sciences</topic><topic>Embryogenesis</topic><topic>Environmental stress</topic><topic>Excitability</topic><topic>Females</topic><topic>Gene expression</topic><topic>Genetic aspects</topic><topic>Genetic 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Rodolfo</au><au>Roman, Gregg</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Insulin-Like Proteins dILPs-2/5 Determine Diapause Inducibility in Drosophila</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2016-09-30</date><risdate>2016</risdate><volume>11</volume><issue>9</issue><spage>e0163680</spage><epage>e0163680</epage><pages>e0163680-e0163680</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Diapause is an actively induced dormancy that has evolved in Metazoa to resist environmental stresses. In temperate regions, many diapausing insects overwinter at low temperatures by blocking embryonic, larval or adult development. Despite its Afro-tropical origin, Drosophila melanogaster migrated to temperate regions of Asia and Europe where females overwinter as adults by arresting gonadal development (reproductive diapause) at temperatures <13°C. Recent work in D. melanogaster has implicated the developmental hormones dILPs-2 and/or dILP3, and dILP5, homologues of vertebrate insulin/insulin-like growth factors (IGFs), in reproductive arrest. However, polymorphisms in timeless (tim) and couch potato (cpo) dramatically affect diapause inducibility and these dILP experiments could not exclude this common genetic variation contributing to the diapause phenotype. Here, we apply an extensive genetic dissection of the insulin signaling pathway which allows us to see both enhancements and reductions in egg development that are independent of tim and cpo variations. We show that a number of manipulations dramatically enhance diapause to ~100%. These include ablating, or reducing the excitability of the insulin-producing cells (IPCs) that express dILPs-2,3,5 employing the dilp2,3,5-/- triple mutant, desensitizing insulin signaling using a chico mutation, or inhibiting dILP2 and 5 in the hemolymph by over-expressing Imaginal Morphogenesis Protein-Late 2 (Imp-L2). In addition, triple mutant dilp2,3,5-/- females maintain high levels of diapause even when temperatures are raised in adulthood to 19°C. However at 22°C, these females all show egg development revealing that the effects are conditional on temperature and not a general female sterility. In contrast, over-expression of dilps-2/5 or enhancing IPC excitability, led to levels of ovarian arrest that approached zero, underscoring dILPs-2 and 5 as key antagonists of diapause.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>27689881</pmid><doi>10.1371/journal.pone.0163680</doi><tpages>e0163680</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Adults Aging Antagonists Biology Biology and Life Sciences Cell division Desensitization Diapause Dormancy Drosophila Drosophila melanogaster Earth Sciences Embryogenesis Environmental stress Excitability Females Gene expression Genetic aspects Genetic diversity Genetic engineering Genomes Growth factors Hemolymph Homology Hormones Insects Insulin Insulin-like growth factors Kinases Low temperature Medicine and Health Sciences Metazoa Morphogenesis Mutation Neurophysiology Overexpression Pancreatic beta cells Phenotypes Potatoes Proteins Research and Analysis Methods Signal transduction Signaling Solanum tuberosum Sterility Temperature effects Timeless protein |
| title | The Insulin-Like Proteins dILPs-2/5 Determine Diapause Inducibility in Drosophila |
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