Continuous up-regulation of heat shock proteins in larvae, but not adults, of a polar insect
Antarctica's terrestrial environment is a challenge to which very few animals have adapted. The largest, free-living animal to inhabit the continent year-round is a flightless midge, Belgica antarctica. Larval midges survive the lengthy austral winter encased in ice, and when the ice melts in s...
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Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2006-09, Vol.103 (38), p.14223-14227 |
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creator | Rinehart, J.P Hayward, S.A.L Elnitsky, M.A Sandro, L.H Lee, R.E. Jr Denlinger, D.L |
description | Antarctica's terrestrial environment is a challenge to which very few animals have adapted. The largest, free-living animal to inhabit the continent year-round is a flightless midge, Belgica antarctica. Larval midges survive the lengthy austral winter encased in ice, and when the ice melts in summer, the larvae complete their 2-yr life cycle, and the wingless adults form mating aggregations while subjected to surprisingly high substrate temperatures. Here we report a dichotomy in survival strategies exploited by this insect at different stages of its life cycle. Larvae constitutively up-regulate their heat shock proteins (small hsp, hsp70, and hsp90) and maintain a high inherent tolerance to temperature stress. High or low temperature exposure does not further up-regulate these genes nor does it further enhance thermotolerance. Such "preemptive" synthesis of hsps is sufficient to prevent irreversible protein aggregation in response to a variety of common environmental stresses. Conversely, adults exhibit no constitutive up-regulation of their hsps and have a lower intrinsic tolerance to high temperatures, but their hsps can be thermally activated, resulting in enhanced thermotolerance. Thus, the midge larvae, but not the adults, have adopted the unusual strategy of expressing hsps continuously, possibly to facilitate proper protein folding in a cold habitat that is more thermally stable than that of the adults but a habitat subjected frequently to freeze-thaw episodes and bouts of pH, anoxic, and osmotic stress. |
doi_str_mv | 10.1073/pnas.0606840103 |
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Jr ; Denlinger, D.L</creator><creatorcontrib>Rinehart, J.P ; Hayward, S.A.L ; Elnitsky, M.A ; Sandro, L.H ; Lee, R.E. Jr ; Denlinger, D.L</creatorcontrib><description>Antarctica's terrestrial environment is a challenge to which very few animals have adapted. The largest, free-living animal to inhabit the continent year-round is a flightless midge, Belgica antarctica. Larval midges survive the lengthy austral winter encased in ice, and when the ice melts in summer, the larvae complete their 2-yr life cycle, and the wingless adults form mating aggregations while subjected to surprisingly high substrate temperatures. Here we report a dichotomy in survival strategies exploited by this insect at different stages of its life cycle. Larvae constitutively up-regulate their heat shock proteins (small hsp, hsp70, and hsp90) and maintain a high inherent tolerance to temperature stress. High or low temperature exposure does not further up-regulate these genes nor does it further enhance thermotolerance. Such "preemptive" synthesis of hsps is sufficient to prevent irreversible protein aggregation in response to a variety of common environmental stresses. Conversely, adults exhibit no constitutive up-regulation of their hsps and have a lower intrinsic tolerance to high temperatures, but their hsps can be thermally activated, resulting in enhanced thermotolerance. Thus, the midge larvae, but not the adults, have adopted the unusual strategy of expressing hsps continuously, possibly to facilitate proper protein folding in a cold habitat that is more thermally stable than that of the adults but a habitat subjected frequently to freeze-thaw episodes and bouts of pH, anoxic, and osmotic stress.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.0606840103</identifier><identifier>PMID: 16968769</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>adult insects ; Aggregation ; air temperature ; Animal behavior ; Animals ; Antarctic Regions ; Antarctica ; Belgica antarctica ; Biological Sciences ; Chironomidae - genetics ; Chironomidae - physiology ; cold tolerance ; Entomology ; Environment ; gene expression ; Gene Expression Regulation, Developmental ; gene induction ; genes ; heat ; heat shock proteins ; heat tolerance ; High temperature ; HSP70 Heat-Shock Proteins - genetics ; HSP70 Heat-Shock Proteins - metabolism ; imagos ; Insect larvae ; Insect Proteins - genetics ; Insect Proteins - metabolism ; Insects ; Larva - physiology ; Larvae ; Life Cycle Stages ; Life cycles ; Low temperature ; Midges ; Molecular Sequence Data ; nucleotide sequences ; Proteins ; Shock heating ; Survival Rate ; Temperature ; Up regulation ; Wildlife habitats</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2006-09, Vol.103 (38), p.14223-14227</ispartof><rights>Copyright 2006 National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Sep 19, 2006</rights><rights>2006 by The National Academy of Sciences of the USA 2006</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c585t-f12ba10b9c132177f33d7c57bfbd5ec756e99769afef3be198ef7c179c444c1d3</citedby><cites>FETCH-LOGICAL-c585t-f12ba10b9c132177f33d7c57bfbd5ec756e99769afef3be198ef7c179c444c1d3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/103/38.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/30052013$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/30052013$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,725,778,782,801,883,27907,27908,53774,53776,58000,58233</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/16968769$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Rinehart, J.P</creatorcontrib><creatorcontrib>Hayward, S.A.L</creatorcontrib><creatorcontrib>Elnitsky, M.A</creatorcontrib><creatorcontrib>Sandro, L.H</creatorcontrib><creatorcontrib>Lee, R.E. Jr</creatorcontrib><creatorcontrib>Denlinger, D.L</creatorcontrib><title>Continuous up-regulation of heat shock proteins in larvae, but not adults, of a polar insect</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Antarctica's terrestrial environment is a challenge to which very few animals have adapted. The largest, free-living animal to inhabit the continent year-round is a flightless midge, Belgica antarctica. Larval midges survive the lengthy austral winter encased in ice, and when the ice melts in summer, the larvae complete their 2-yr life cycle, and the wingless adults form mating aggregations while subjected to surprisingly high substrate temperatures. Here we report a dichotomy in survival strategies exploited by this insect at different stages of its life cycle. Larvae constitutively up-regulate their heat shock proteins (small hsp, hsp70, and hsp90) and maintain a high inherent tolerance to temperature stress. High or low temperature exposure does not further up-regulate these genes nor does it further enhance thermotolerance. Such "preemptive" synthesis of hsps is sufficient to prevent irreversible protein aggregation in response to a variety of common environmental stresses. Conversely, adults exhibit no constitutive up-regulation of their hsps and have a lower intrinsic tolerance to high temperatures, but their hsps can be thermally activated, resulting in enhanced thermotolerance. Thus, the midge larvae, but not the adults, have adopted the unusual strategy of expressing hsps continuously, possibly to facilitate proper protein folding in a cold habitat that is more thermally stable than that of the adults but a habitat subjected frequently to freeze-thaw episodes and bouts of pH, anoxic, and osmotic stress.</description><subject>adult insects</subject><subject>Aggregation</subject><subject>air temperature</subject><subject>Animal behavior</subject><subject>Animals</subject><subject>Antarctic Regions</subject><subject>Antarctica</subject><subject>Belgica antarctica</subject><subject>Biological Sciences</subject><subject>Chironomidae - genetics</subject><subject>Chironomidae - physiology</subject><subject>cold tolerance</subject><subject>Entomology</subject><subject>Environment</subject><subject>gene expression</subject><subject>Gene Expression Regulation, Developmental</subject><subject>gene induction</subject><subject>genes</subject><subject>heat</subject><subject>heat shock proteins</subject><subject>heat tolerance</subject><subject>High temperature</subject><subject>HSP70 Heat-Shock Proteins - genetics</subject><subject>HSP70 Heat-Shock Proteins - metabolism</subject><subject>imagos</subject><subject>Insect larvae</subject><subject>Insect Proteins - genetics</subject><subject>Insect Proteins - metabolism</subject><subject>Insects</subject><subject>Larva - physiology</subject><subject>Larvae</subject><subject>Life Cycle Stages</subject><subject>Life cycles</subject><subject>Low temperature</subject><subject>Midges</subject><subject>Molecular Sequence Data</subject><subject>nucleotide sequences</subject><subject>Proteins</subject><subject>Shock heating</subject><subject>Survival Rate</subject><subject>Temperature</subject><subject>Up regulation</subject><subject>Wildlife habitats</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2006</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkkuLFDEUhQtRnHZ07UoNLgRhauamkspjI0jjCwZc6OyEkEon3dVWJzVJatB_b4puptVNr7I43znce3Oq6jmGSwycXI1ep0tgwAQFDORBtcAgcc2ohIfVAqDhtaANPauepLQFANkKeFydYSaZ4Ewuqh_L4HPvpzAlNI11tOtp0LkPHgWHNlZnlDbB_ERjDNn2PqHeo0HHO20vUDdl5ENGejUNOV3MDo3GUORCJWvy0-qR00Oyzw7veXXz8cP35ef6-uunL8v317VpRZtrh5tOY-ikwaTBnDtCVty0vHPdqrWGt8xKWabVzjrSWSyFddxgLg2l1OAVOa_e7XPHqdvZlbE-Rz2oMfY7HX-roHv1r-L7jVqHO4VbKSURJeDNISCG28mmrHZ9MnYYtLflMooJwXGZ4CRIOZGCsNOJWBLMKG8L-Po_cBum6Mu5VAOYcE4xK9DVHjIxpBStu98Ng5qLoOYiqGMRiuPl3yc58oefLwA6ALPzGEcUEQrTppkz3p5AlJuGIdtfubAv9uw25RDvYQLQzmsU_dVedzoovY59UjffZgWAs4Y2jPwBRqra-g</recordid><startdate>20060919</startdate><enddate>20060919</enddate><creator>Rinehart, J.P</creator><creator>Hayward, S.A.L</creator><creator>Elnitsky, M.A</creator><creator>Sandro, L.H</creator><creator>Lee, R.E. 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Here we report a dichotomy in survival strategies exploited by this insect at different stages of its life cycle. Larvae constitutively up-regulate their heat shock proteins (small hsp, hsp70, and hsp90) and maintain a high inherent tolerance to temperature stress. High or low temperature exposure does not further up-regulate these genes nor does it further enhance thermotolerance. Such "preemptive" synthesis of hsps is sufficient to prevent irreversible protein aggregation in response to a variety of common environmental stresses. Conversely, adults exhibit no constitutive up-regulation of their hsps and have a lower intrinsic tolerance to high temperatures, but their hsps can be thermally activated, resulting in enhanced thermotolerance. Thus, the midge larvae, but not the adults, have adopted the unusual strategy of expressing hsps continuously, possibly to facilitate proper protein folding in a cold habitat that is more thermally stable than that of the adults but a habitat subjected frequently to freeze-thaw episodes and bouts of pH, anoxic, and osmotic stress.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>16968769</pmid><doi>10.1073/pnas.0606840103</doi><tpages>5</tpages><oa>free_for_read</oa></addata></record> |
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subjects | adult insects Aggregation air temperature Animal behavior Animals Antarctic Regions Antarctica Belgica antarctica Biological Sciences Chironomidae - genetics Chironomidae - physiology cold tolerance Entomology Environment gene expression Gene Expression Regulation, Developmental gene induction genes heat heat shock proteins heat tolerance High temperature HSP70 Heat-Shock Proteins - genetics HSP70 Heat-Shock Proteins - metabolism imagos Insect larvae Insect Proteins - genetics Insect Proteins - metabolism Insects Larva - physiology Larvae Life Cycle Stages Life cycles Low temperature Midges Molecular Sequence Data nucleotide sequences Proteins Shock heating Survival Rate Temperature Up regulation Wildlife habitats |
title | Continuous up-regulation of heat shock proteins in larvae, but not adults, of a polar insect |
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