Food-derived sensory cues modulate longevity via distinct neuroendocrine insulin-like peptides
Environmental fluctuations influence organismal aging by affecting various regulatory systems. One such system involves sensory neurons, which affect life span in many species. However, how sensory neurons coordinate organismal aging in response to changes in environmental signals remains elusive. H...
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| Veröffentlicht in: | Genes & development 2016-05, Vol.30 (9), p.1047-1057 |
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| creator | Artan, Murat Jeong, Dae-Eun Lee, Dongyeop Kim, Young-Il Son, Heehwa G Husain, Zahabiya Kim, Jinmahn Altintas, Ozlem Kim, Kyuhyung Alcedo, Joy Lee, Seung-Jae V |
| description | Environmental fluctuations influence organismal aging by affecting various regulatory systems. One such system involves sensory neurons, which affect life span in many species. However, how sensory neurons coordinate organismal aging in response to changes in environmental signals remains elusive. Here, we found that a subset of sensory neurons shortens Caenorhabditis elegans' life span by differentially regulating the expression of a specific insulin-like peptide (ILP), INS-6. Notably, treatment with food-derived cues or optogenetic activation of sensory neurons significantly increases ins-6 expression and decreases life span. INS-6 in turn relays the longevity signals to nonneuronal tissues by decreasing the activity of the transcription factor DAF-16/FOXO. Together, our study delineates a mechanism through which environmental sensory cues regulate aging rates by modulating the activities of specific sensory neurons and ILPs. |
| doi_str_mv | 10.1101/gad.279448.116 |
| format | Article |
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One such system involves sensory neurons, which affect life span in many species. However, how sensory neurons coordinate organismal aging in response to changes in environmental signals remains elusive. Here, we found that a subset of sensory neurons shortens Caenorhabditis elegans' life span by differentially regulating the expression of a specific insulin-like peptide (ILP), INS-6. Notably, treatment with food-derived cues or optogenetic activation of sensory neurons significantly increases ins-6 expression and decreases life span. INS-6 in turn relays the longevity signals to nonneuronal tissues by decreasing the activity of the transcription factor DAF-16/FOXO. Together, our study delineates a mechanism through which environmental sensory cues regulate aging rates by modulating the activities of specific sensory neurons and ILPs.</description><identifier>ISSN: 0890-9369</identifier><identifier>EISSN: 1549-5477</identifier><identifier>DOI: 10.1101/gad.279448.116</identifier><identifier>PMID: 27125673</identifier><language>eng</language><publisher>United States: Cold Spring Harbor Laboratory Press</publisher><subject>Caenorhabditis elegans ; Caenorhabditis elegans Proteins - genetics ; Caenorhabditis elegans Proteins - metabolism ; Cues ; Environment ; Food ; Forkhead Transcription Factors - genetics ; Forkhead Transcription Factors - metabolism ; Gene Expression Regulation ; Insulin - genetics ; Insulin - metabolism ; Longevity - genetics ; Optogenetics ; Peptide Hormones - genetics ; Peptide Hormones - metabolism ; Research Paper ; Sensory Receptor Cells - physiology ; Signal Transduction</subject><ispartof>Genes & development, 2016-05, Vol.30 (9), p.1047-1057</ispartof><rights>2016 Artan et al.; Published by Cold Spring Harbor Laboratory Press.</rights><rights>2016</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c489t-4016b4fb40d036146b322e83e65bd27899994d1e3fe3cf84192d89cf3cbbe7d93</citedby><cites>FETCH-LOGICAL-c489t-4016b4fb40d036146b322e83e65bd27899994d1e3fe3cf84192d89cf3cbbe7d93</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/PMC4863736/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4863736/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27125673$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Artan, Murat</creatorcontrib><creatorcontrib>Jeong, Dae-Eun</creatorcontrib><creatorcontrib>Lee, Dongyeop</creatorcontrib><creatorcontrib>Kim, Young-Il</creatorcontrib><creatorcontrib>Son, Heehwa G</creatorcontrib><creatorcontrib>Husain, Zahabiya</creatorcontrib><creatorcontrib>Kim, Jinmahn</creatorcontrib><creatorcontrib>Altintas, Ozlem</creatorcontrib><creatorcontrib>Kim, Kyuhyung</creatorcontrib><creatorcontrib>Alcedo, Joy</creatorcontrib><creatorcontrib>Lee, Seung-Jae V</creatorcontrib><title>Food-derived sensory cues modulate longevity via distinct neuroendocrine insulin-like peptides</title><title>Genes & development</title><addtitle>Genes Dev</addtitle><description>Environmental fluctuations influence organismal aging by affecting various regulatory systems. One such system involves sensory neurons, which affect life span in many species. However, how sensory neurons coordinate organismal aging in response to changes in environmental signals remains elusive. Here, we found that a subset of sensory neurons shortens Caenorhabditis elegans' life span by differentially regulating the expression of a specific insulin-like peptide (ILP), INS-6. Notably, treatment with food-derived cues or optogenetic activation of sensory neurons significantly increases ins-6 expression and decreases life span. INS-6 in turn relays the longevity signals to nonneuronal tissues by decreasing the activity of the transcription factor DAF-16/FOXO. Together, our study delineates a mechanism through which environmental sensory cues regulate aging rates by modulating the activities of specific sensory neurons and ILPs.</description><subject>Caenorhabditis elegans</subject><subject>Caenorhabditis elegans Proteins - genetics</subject><subject>Caenorhabditis elegans Proteins - metabolism</subject><subject>Cues</subject><subject>Environment</subject><subject>Food</subject><subject>Forkhead Transcription Factors - genetics</subject><subject>Forkhead Transcription Factors - metabolism</subject><subject>Gene Expression Regulation</subject><subject>Insulin - genetics</subject><subject>Insulin - metabolism</subject><subject>Longevity - genetics</subject><subject>Optogenetics</subject><subject>Peptide Hormones - genetics</subject><subject>Peptide Hormones - metabolism</subject><subject>Research Paper</subject><subject>Sensory Receptor Cells - physiology</subject><subject>Signal Transduction</subject><issn>0890-9369</issn><issn>1549-5477</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkUtLxDAUhYMoOj62LiVLNx2TJs1jI4j4ggE3ujW0ye0Y7SRj0g7Mv7cyOujOu7lc7uFwDh9Cp5RMKSX0Yl67aSk152q8xQ6a0IrrouJS7qIJUZoUmgl9gA5zfiOECCLEPjooJS0rIdkEvdzG6AoHya_A4Qwhx7TGdoCMF9ENXd0D7mKYw8r3a7zyNXY-9z7YHgcYUoTgok0-APYhD50PReffAS9h2XsH-RjttXWX4eR7H6Hn25un6_ti9nj3cH01KyxXui84oaLhbcOJI0xQLhpWlqAYiKpxpVR6HO4osBaYbRWnunRK25bZpgHpNDtClxvf5dAswFkIfao7s0x-Uae1ibU3fz_Bv5p5XBmuBJNMjAbn3wYpfozte7Pw2ULX1QHikA2VmmguZCX_IVWSK1IyNkqnG6lNMecE7TYRJeaLnxn5mQ2_8f6Kcfa7x1b-A4x9AiCKmSc</recordid><startdate>20160501</startdate><enddate>20160501</enddate><creator>Artan, Murat</creator><creator>Jeong, Dae-Eun</creator><creator>Lee, Dongyeop</creator><creator>Kim, Young-Il</creator><creator>Son, Heehwa G</creator><creator>Husain, Zahabiya</creator><creator>Kim, Jinmahn</creator><creator>Altintas, Ozlem</creator><creator>Kim, Kyuhyung</creator><creator>Alcedo, Joy</creator><creator>Lee, Seung-Jae V</creator><general>Cold Spring Harbor Laboratory Press</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>7X8</scope><scope>7TK</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>5PM</scope></search><sort><creationdate>20160501</creationdate><title>Food-derived sensory cues modulate longevity via distinct neuroendocrine insulin-like peptides</title><author>Artan, Murat ; Jeong, Dae-Eun ; Lee, Dongyeop ; Kim, Young-Il ; Son, Heehwa G ; Husain, Zahabiya ; Kim, Jinmahn ; Altintas, Ozlem ; Kim, Kyuhyung ; Alcedo, Joy ; Lee, Seung-Jae V</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c489t-4016b4fb40d036146b322e83e65bd27899994d1e3fe3cf84192d89cf3cbbe7d93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Caenorhabditis elegans</topic><topic>Caenorhabditis elegans Proteins - genetics</topic><topic>Caenorhabditis elegans Proteins - metabolism</topic><topic>Cues</topic><topic>Environment</topic><topic>Food</topic><topic>Forkhead Transcription Factors - genetics</topic><topic>Forkhead Transcription Factors - metabolism</topic><topic>Gene Expression Regulation</topic><topic>Insulin - genetics</topic><topic>Insulin - metabolism</topic><topic>Longevity - genetics</topic><topic>Optogenetics</topic><topic>Peptide Hormones - genetics</topic><topic>Peptide Hormones - metabolism</topic><topic>Research Paper</topic><topic>Sensory Receptor Cells - physiology</topic><topic>Signal Transduction</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Artan, Murat</creatorcontrib><creatorcontrib>Jeong, Dae-Eun</creatorcontrib><creatorcontrib>Lee, Dongyeop</creatorcontrib><creatorcontrib>Kim, Young-Il</creatorcontrib><creatorcontrib>Son, Heehwa G</creatorcontrib><creatorcontrib>Husain, Zahabiya</creatorcontrib><creatorcontrib>Kim, Jinmahn</creatorcontrib><creatorcontrib>Altintas, Ozlem</creatorcontrib><creatorcontrib>Kim, Kyuhyung</creatorcontrib><creatorcontrib>Alcedo, Joy</creatorcontrib><creatorcontrib>Lee, Seung-Jae V</creatorcontrib><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>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Genes & development</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Artan, Murat</au><au>Jeong, Dae-Eun</au><au>Lee, Dongyeop</au><au>Kim, Young-Il</au><au>Son, Heehwa G</au><au>Husain, Zahabiya</au><au>Kim, Jinmahn</au><au>Altintas, Ozlem</au><au>Kim, Kyuhyung</au><au>Alcedo, Joy</au><au>Lee, Seung-Jae V</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Food-derived sensory cues modulate longevity via distinct neuroendocrine insulin-like peptides</atitle><jtitle>Genes & development</jtitle><addtitle>Genes Dev</addtitle><date>2016-05-01</date><risdate>2016</risdate><volume>30</volume><issue>9</issue><spage>1047</spage><epage>1057</epage><pages>1047-1057</pages><issn>0890-9369</issn><eissn>1549-5477</eissn><abstract>Environmental fluctuations influence organismal aging by affecting various regulatory systems. 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| subjects | Caenorhabditis elegans Caenorhabditis elegans Proteins - genetics Caenorhabditis elegans Proteins - metabolism Cues Environment Food Forkhead Transcription Factors - genetics Forkhead Transcription Factors - metabolism Gene Expression Regulation Insulin - genetics Insulin - metabolism Longevity - genetics Optogenetics Peptide Hormones - genetics Peptide Hormones - metabolism Research Paper Sensory Receptor Cells - physiology Signal Transduction |
| title | Food-derived sensory cues modulate longevity via distinct neuroendocrine insulin-like peptides |
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