Prostaglandin signals from adult germline stem cells delay somatic ageing of Caenorhabditis elegans
A moderate reduction in body temperature can induce a remarkable lifespan extension. Here we examine the link between cold temperature, germline fitness and organismal longevity. We show that low temperature reduces age-associated exhaustion of germline stem cells (GSCs) in Caenorhabditis elegans ,...
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Veröffentlicht in: | Nature metabolism 2019-08, Vol.1 (8), p.790-810 |
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description | A moderate reduction in body temperature can induce a remarkable lifespan extension. Here we examine the link between cold temperature, germline fitness and organismal longevity. We show that low temperature reduces age-associated exhaustion of germline stem cells (GSCs) in
Caenorhabditis elegans
, a process modulated by thermosensory neurons. Notably, robust self-renewal of adult GSCs delays reproductive ageing and is required for extended lifespan at cold temperatures (10 °C, 15 °C). These cells release prostaglandin E2 (PGE2) to induce
cbs-1
expression in the intestine, increasing the somatic production of hydrogen sulfide, a gaseous signalling molecule that prolongs lifespan. Loss of adult GSCs reduces intestinal
cbs-1
expression and cold-induced longevity, whereas application of exogenous PGE2 rescues these phenotypes. Importantly, tissue-specific intestinal overexpression of
cbs-1
mimics cold-temperature conditions and extends longevity even at warm temperatures (25 °C). Thus, our results indicate that GSCs communicate with somatic tissues to coordinate extended reproductive capacity with longevity.
Although germline removal normally extends
Caenorhabditis elegans
lifespan, Lee et al. show that low temperature does not extend lifespan in germline-lacking mutant worms. Cold temperatures (10 °C, 15 °C) delay germline stem cell exhaustion, releasing prostaglandin E2 hormone, which induces
cbs-1
in the intestine to produce hydrogen sulfide and prolong lifespan. |
doi_str_mv | 10.1038/s42255-019-0097-9 |
format | Article |
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Caenorhabditis elegans
, a process modulated by thermosensory neurons. Notably, robust self-renewal of adult GSCs delays reproductive ageing and is required for extended lifespan at cold temperatures (10 °C, 15 °C). These cells release prostaglandin E2 (PGE2) to induce
cbs-1
expression in the intestine, increasing the somatic production of hydrogen sulfide, a gaseous signalling molecule that prolongs lifespan. Loss of adult GSCs reduces intestinal
cbs-1
expression and cold-induced longevity, whereas application of exogenous PGE2 rescues these phenotypes. Importantly, tissue-specific intestinal overexpression of
cbs-1
mimics cold-temperature conditions and extends longevity even at warm temperatures (25 °C). Thus, our results indicate that GSCs communicate with somatic tissues to coordinate extended reproductive capacity with longevity.
Although germline removal normally extends
Caenorhabditis elegans
lifespan, Lee et al. show that low temperature does not extend lifespan in germline-lacking mutant worms. Cold temperatures (10 °C, 15 °C) delay germline stem cell exhaustion, releasing prostaglandin E2 hormone, which induces
cbs-1
in the intestine to produce hydrogen sulfide and prolong lifespan.</description><identifier>ISSN: 2522-5812</identifier><identifier>EISSN: 2522-5812</identifier><identifier>DOI: 10.1038/s42255-019-0097-9</identifier><identifier>PMID: 31485561</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>38 ; 38/89 ; 38/91 ; 59 ; 631/208 ; 631/443/7 ; 631/532 ; 631/80 ; 64/11 ; 82/1 ; 82/51 ; 82/58 ; 96/100 ; 96/63 ; Biomedical and Life Sciences ; Life Sciences</subject><ispartof>Nature metabolism, 2019-08, Vol.1 (8), p.790-810</ispartof><rights>The Author(s), under exclusive licence to Springer Nature Limited 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c386t-c1a8e4323c18853ed14cc05c4bf92e411c3382ad886dd6431a9edab1dae9ae7a3</citedby><cites>FETCH-LOGICAL-c386t-c1a8e4323c18853ed14cc05c4bf92e411c3382ad886dd6431a9edab1dae9ae7a3</cites><orcidid>0000-0002-5472-3517 ; 0000-0002-0801-0743</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/s42255-019-0097-9$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s42255-019-0097-9$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,776,780,881,27903,27904,41467,42536,51297</link.rule.ids></links><search><creatorcontrib>Lee, Hyun Ju</creatorcontrib><creatorcontrib>Noormohammadi, Alireza</creatorcontrib><creatorcontrib>Koyuncu, Seda</creatorcontrib><creatorcontrib>Calculli, Giuseppe</creatorcontrib><creatorcontrib>Simic, Milos S.</creatorcontrib><creatorcontrib>Herholz, Marija</creatorcontrib><creatorcontrib>Trifunovic, Aleksandra</creatorcontrib><creatorcontrib>Vilchez, David</creatorcontrib><title>Prostaglandin signals from adult germline stem cells delay somatic ageing of Caenorhabditis elegans</title><title>Nature metabolism</title><addtitle>Nat Metab</addtitle><description>A moderate reduction in body temperature can induce a remarkable lifespan extension. Here we examine the link between cold temperature, germline fitness and organismal longevity. We show that low temperature reduces age-associated exhaustion of germline stem cells (GSCs) in
Caenorhabditis elegans
, a process modulated by thermosensory neurons. Notably, robust self-renewal of adult GSCs delays reproductive ageing and is required for extended lifespan at cold temperatures (10 °C, 15 °C). These cells release prostaglandin E2 (PGE2) to induce
cbs-1
expression in the intestine, increasing the somatic production of hydrogen sulfide, a gaseous signalling molecule that prolongs lifespan. Loss of adult GSCs reduces intestinal
cbs-1
expression and cold-induced longevity, whereas application of exogenous PGE2 rescues these phenotypes. Importantly, tissue-specific intestinal overexpression of
cbs-1
mimics cold-temperature conditions and extends longevity even at warm temperatures (25 °C). Thus, our results indicate that GSCs communicate with somatic tissues to coordinate extended reproductive capacity with longevity.
Although germline removal normally extends
Caenorhabditis elegans
lifespan, Lee et al. show that low temperature does not extend lifespan in germline-lacking mutant worms. Cold temperatures (10 °C, 15 °C) delay germline stem cell exhaustion, releasing prostaglandin E2 hormone, which induces
cbs-1
in the intestine to produce hydrogen sulfide and prolong lifespan.</description><subject>38</subject><subject>38/89</subject><subject>38/91</subject><subject>59</subject><subject>631/208</subject><subject>631/443/7</subject><subject>631/532</subject><subject>631/80</subject><subject>64/11</subject><subject>82/1</subject><subject>82/51</subject><subject>82/58</subject><subject>96/100</subject><subject>96/63</subject><subject>Biomedical and Life Sciences</subject><subject>Life Sciences</subject><issn>2522-5812</issn><issn>2522-5812</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><recordid>eNp9kE1LxDAQQIMoKuv-AG_5A9VMknbTiyCLXyDoQc9hNpl2s7SpJF1h_71dVkQvnmZg5r3DY-wSxBUIZa6zlrIsCwF1IUS9KOojdi5LKYvSgDz-tZ-xec4bIYQE0CDrU3amQJuyrOCcudc05BHbDqMPkefQRuwyb9LQc_TbbuQtpb4LkXgeqeeOuunsqcMdz0OPY3AcWwqx5UPDl0hxSGtc-TCGzKmjFmO-YCfNJKX595yx9_u7t-Vj8fzy8LS8fS6cMtVYOEBDWknlwJhSkQftnCidXjW1JA3glDISvTGV95VWgDV5XIFHqpEWqGbs5uD92K568o7imLCzHyn0mHZ2wGD_XmJY23b4tNVCVnpRTwI4CNwUJSdqflgQdh_dHqLbKbrdR7d7Rh6YPP3GKZbdDNu0j_gP9AVFN4ac</recordid><startdate>20190801</startdate><enddate>20190801</enddate><creator>Lee, Hyun Ju</creator><creator>Noormohammadi, Alireza</creator><creator>Koyuncu, Seda</creator><creator>Calculli, Giuseppe</creator><creator>Simic, Milos S.</creator><creator>Herholz, Marija</creator><creator>Trifunovic, Aleksandra</creator><creator>Vilchez, David</creator><general>Nature Publishing Group UK</general><scope>AAYXX</scope><scope>CITATION</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-5472-3517</orcidid><orcidid>https://orcid.org/0000-0002-0801-0743</orcidid></search><sort><creationdate>20190801</creationdate><title>Prostaglandin signals from adult germline stem cells delay somatic ageing of Caenorhabditis elegans</title><author>Lee, Hyun Ju ; Noormohammadi, Alireza ; Koyuncu, Seda ; Calculli, Giuseppe ; Simic, Milos S. ; Herholz, Marija ; Trifunovic, Aleksandra ; Vilchez, David</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c386t-c1a8e4323c18853ed14cc05c4bf92e411c3382ad886dd6431a9edab1dae9ae7a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>38</topic><topic>38/89</topic><topic>38/91</topic><topic>59</topic><topic>631/208</topic><topic>631/443/7</topic><topic>631/532</topic><topic>631/80</topic><topic>64/11</topic><topic>82/1</topic><topic>82/51</topic><topic>82/58</topic><topic>96/100</topic><topic>96/63</topic><topic>Biomedical and Life Sciences</topic><topic>Life Sciences</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lee, Hyun Ju</creatorcontrib><creatorcontrib>Noormohammadi, Alireza</creatorcontrib><creatorcontrib>Koyuncu, Seda</creatorcontrib><creatorcontrib>Calculli, Giuseppe</creatorcontrib><creatorcontrib>Simic, Milos S.</creatorcontrib><creatorcontrib>Herholz, Marija</creatorcontrib><creatorcontrib>Trifunovic, Aleksandra</creatorcontrib><creatorcontrib>Vilchez, David</creatorcontrib><collection>CrossRef</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Nature metabolism</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lee, Hyun Ju</au><au>Noormohammadi, Alireza</au><au>Koyuncu, Seda</au><au>Calculli, Giuseppe</au><au>Simic, Milos S.</au><au>Herholz, Marija</au><au>Trifunovic, Aleksandra</au><au>Vilchez, David</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Prostaglandin signals from adult germline stem cells delay somatic ageing of Caenorhabditis elegans</atitle><jtitle>Nature metabolism</jtitle><stitle>Nat Metab</stitle><date>2019-08-01</date><risdate>2019</risdate><volume>1</volume><issue>8</issue><spage>790</spage><epage>810</epage><pages>790-810</pages><issn>2522-5812</issn><eissn>2522-5812</eissn><abstract>A moderate reduction in body temperature can induce a remarkable lifespan extension. Here we examine the link between cold temperature, germline fitness and organismal longevity. We show that low temperature reduces age-associated exhaustion of germline stem cells (GSCs) in
Caenorhabditis elegans
, a process modulated by thermosensory neurons. Notably, robust self-renewal of adult GSCs delays reproductive ageing and is required for extended lifespan at cold temperatures (10 °C, 15 °C). These cells release prostaglandin E2 (PGE2) to induce
cbs-1
expression in the intestine, increasing the somatic production of hydrogen sulfide, a gaseous signalling molecule that prolongs lifespan. Loss of adult GSCs reduces intestinal
cbs-1
expression and cold-induced longevity, whereas application of exogenous PGE2 rescues these phenotypes. Importantly, tissue-specific intestinal overexpression of
cbs-1
mimics cold-temperature conditions and extends longevity even at warm temperatures (25 °C). Thus, our results indicate that GSCs communicate with somatic tissues to coordinate extended reproductive capacity with longevity.
Although germline removal normally extends
Caenorhabditis elegans
lifespan, Lee et al. show that low temperature does not extend lifespan in germline-lacking mutant worms. Cold temperatures (10 °C, 15 °C) delay germline stem cell exhaustion, releasing prostaglandin E2 hormone, which induces
cbs-1
in the intestine to produce hydrogen sulfide and prolong lifespan.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>31485561</pmid><doi>10.1038/s42255-019-0097-9</doi><tpages>21</tpages><orcidid>https://orcid.org/0000-0002-5472-3517</orcidid><orcidid>https://orcid.org/0000-0002-0801-0743</orcidid><oa>free_for_read</oa></addata></record> |
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title | Prostaglandin signals from adult germline stem cells delay somatic ageing of Caenorhabditis elegans |
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