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Mated Progeny Production Is a Biomarker of Aging in Caenorhabditis elegans
Abstract The relationships between reproduction and aging are important for understanding the mechanisms of aging and evaluating evolutionary theories of aging. To investigate the effects of progeny production on reproductive and somatic aging, we conducted longitudinal studies of Caenorhabditis ele...
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Published in: | G3 : genes - genomes - genetics 2013-12, Vol.3 (12), p.2219-2232 |
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creator | Pickett, Christopher L Dietrich, Nicholas Chen, Junfang Xiong, Chengjie Kornfeld, Kerry |
description | Abstract
The relationships between reproduction and aging are important for understanding the mechanisms of aging and evaluating evolutionary theories of aging. To investigate the effects of progeny production on reproductive and somatic aging, we conducted longitudinal studies of Caenorhabditis elegans hermaphrodites. For mated wild-type animals that were not sperm limited and survived past the end of the reproductive period, high levels of cross-progeny production were positively correlated with delayed reproductive and somatic aging. In this group of animals, individuals that generated more cross progeny also reproduced and lived longer than individuals that generated fewer cross progeny. These results indicate that progeny production does not accelerate reproductive or somatic aging. This longitudinal study demonstrated that cumulative cross progeny production through day four is an early-stage biomarker that is a positive predictor of longevity. Furthermore, in mated animals, high levels of early cross progeny production were positively correlated with high levels of late cross progeny production, indicating that early progeny production does not accelerate reproductive aging. The relationships between progeny production and aging were further evaluated by comparing self-fertile hermaphrodites that generated relatively few self progeny with mated hermaphrodites that generated many cross progeny. The timing of age-related somatic degeneration was similar in these groups, suggesting progeny production does not accelerate somatic aging. These studies rigorously define relationships between progeny production, reproductive aging, and somatic aging and identify new biomarkers of C. elegans aging. These results indicate that some mechanisms or pathways control age-related degeneration of both reproductive and somatic tissues in C. elegans. |
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The relationships between reproduction and aging are important for understanding the mechanisms of aging and evaluating evolutionary theories of aging. To investigate the effects of progeny production on reproductive and somatic aging, we conducted longitudinal studies of Caenorhabditis elegans hermaphrodites. For mated wild-type animals that were not sperm limited and survived past the end of the reproductive period, high levels of cross-progeny production were positively correlated with delayed reproductive and somatic aging. In this group of animals, individuals that generated more cross progeny also reproduced and lived longer than individuals that generated fewer cross progeny. These results indicate that progeny production does not accelerate reproductive or somatic aging. This longitudinal study demonstrated that cumulative cross progeny production through day four is an early-stage biomarker that is a positive predictor of longevity. Furthermore, in mated animals, high levels of early cross progeny production were positively correlated with high levels of late cross progeny production, indicating that early progeny production does not accelerate reproductive aging. The relationships between progeny production and aging were further evaluated by comparing self-fertile hermaphrodites that generated relatively few self progeny with mated hermaphrodites that generated many cross progeny. The timing of age-related somatic degeneration was similar in these groups, suggesting progeny production does not accelerate somatic aging. These studies rigorously define relationships between progeny production, reproductive aging, and somatic aging and identify new biomarkers of C. elegans aging. These results indicate that some mechanisms or pathways control age-related degeneration of both reproductive and somatic tissues in C. elegans.</description><identifier>ISSN: 2160-1836</identifier><identifier>EISSN: 2160-1836</identifier><identifier>DOI: 10.1534/g3.113.008664</identifier><identifier>PMID: 24142929</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Aging - physiology ; Animals ; Biomarkers ; Caenorhabditis elegans - physiology ; Caenorhabditis elegans Proteins - genetics ; Disorders of Sex Development ; DNA-Binding Proteins - genetics ; Female ; Investigations ; Male ; Reproduction - genetics ; Reproduction - physiology ; Sexual Behavior, Animal ; Transcription Factors - genetics</subject><ispartof>G3 : genes - genomes - genetics, 2013-12, Vol.3 (12), p.2219-2232</ispartof><rights>2013 Pickett et al. 2013</rights><rights>Copyright © 2013 Pickett 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c381t-dd348ad1c9fb351db0f9f6fd856c9f2520c90c7460294b21eb958756237fb1bf3</citedby><cites>FETCH-LOGICAL-c381t-dd348ad1c9fb351db0f9f6fd856c9f2520c90c7460294b21eb958756237fb1bf3</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/PMC3852384/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3852384/$$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/24142929$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Pickett, Christopher L</creatorcontrib><creatorcontrib>Dietrich, Nicholas</creatorcontrib><creatorcontrib>Chen, Junfang</creatorcontrib><creatorcontrib>Xiong, Chengjie</creatorcontrib><creatorcontrib>Kornfeld, Kerry</creatorcontrib><title>Mated Progeny Production Is a Biomarker of Aging in Caenorhabditis elegans</title><title>G3 : genes - genomes - genetics</title><addtitle>G3 (Bethesda)</addtitle><description>Abstract
The relationships between reproduction and aging are important for understanding the mechanisms of aging and evaluating evolutionary theories of aging. To investigate the effects of progeny production on reproductive and somatic aging, we conducted longitudinal studies of Caenorhabditis elegans hermaphrodites. For mated wild-type animals that were not sperm limited and survived past the end of the reproductive period, high levels of cross-progeny production were positively correlated with delayed reproductive and somatic aging. In this group of animals, individuals that generated more cross progeny also reproduced and lived longer than individuals that generated fewer cross progeny. These results indicate that progeny production does not accelerate reproductive or somatic aging. This longitudinal study demonstrated that cumulative cross progeny production through day four is an early-stage biomarker that is a positive predictor of longevity. Furthermore, in mated animals, high levels of early cross progeny production were positively correlated with high levels of late cross progeny production, indicating that early progeny production does not accelerate reproductive aging. The relationships between progeny production and aging were further evaluated by comparing self-fertile hermaphrodites that generated relatively few self progeny with mated hermaphrodites that generated many cross progeny. The timing of age-related somatic degeneration was similar in these groups, suggesting progeny production does not accelerate somatic aging. These studies rigorously define relationships between progeny production, reproductive aging, and somatic aging and identify new biomarkers of C. elegans aging. These results indicate that some mechanisms or pathways control age-related degeneration of both reproductive and somatic tissues in C. elegans.</description><subject>Aging - physiology</subject><subject>Animals</subject><subject>Biomarkers</subject><subject>Caenorhabditis elegans - physiology</subject><subject>Caenorhabditis elegans Proteins - genetics</subject><subject>Disorders of Sex Development</subject><subject>DNA-Binding Proteins - genetics</subject><subject>Female</subject><subject>Investigations</subject><subject>Male</subject><subject>Reproduction - genetics</subject><subject>Reproduction - physiology</subject><subject>Sexual Behavior, Animal</subject><subject>Transcription Factors - genetics</subject><issn>2160-1836</issn><issn>2160-1836</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><recordid>eNqFkbtPwzAQxi0EAlQ6siKPLCl-11mQoOJRBIIBZsuJ7dSQ2sVOkPjvCSqPMnHLne5--u50HwCHGE0wp-ykoROM6QQhKQTbAvsEC1RgScX2Rr0Hxjk_oyE4HzCxC_YIw4yUpNwHN3e6swY-pNjY8P6ZTV93PgY4z1DDcx-XOr3YBKODZ40PDfQBzrQNMS10ZXznM7StbXTIB2DH6Tbb8VcegafLi8fZdXF7fzWfnd0WNZW4K4yhTGqD69JVlGNTIVc64YzkYmgRTlBdonrKBCIlqwi2VcnllAtCp67ClaMjcLrWXfXV0prahi7pVq2SH059V1F79XcS_EI18U1RyQmVbBA4_hJI8bW3uVNLn2vbtjrY2GeFmZgKyqjAA1qs0TrFnJN1P2swUp8WqIaqwQK1tmDgjzZv-6G_H_67O_arf7Q-ANLkjXI</recordid><startdate>20131209</startdate><enddate>20131209</enddate><creator>Pickett, Christopher L</creator><creator>Dietrich, Nicholas</creator><creator>Chen, Junfang</creator><creator>Xiong, Chengjie</creator><creator>Kornfeld, Kerry</creator><general>Oxford University Press</general><general>Genetics Society of America</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>5PM</scope></search><sort><creationdate>20131209</creationdate><title>Mated Progeny Production Is a Biomarker of Aging in Caenorhabditis elegans</title><author>Pickett, Christopher L ; Dietrich, Nicholas ; Chen, Junfang ; Xiong, Chengjie ; Kornfeld, Kerry</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c381t-dd348ad1c9fb351db0f9f6fd856c9f2520c90c7460294b21eb958756237fb1bf3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Aging - physiology</topic><topic>Animals</topic><topic>Biomarkers</topic><topic>Caenorhabditis elegans - physiology</topic><topic>Caenorhabditis elegans Proteins - genetics</topic><topic>Disorders of Sex Development</topic><topic>DNA-Binding Proteins - genetics</topic><topic>Female</topic><topic>Investigations</topic><topic>Male</topic><topic>Reproduction - genetics</topic><topic>Reproduction - physiology</topic><topic>Sexual Behavior, Animal</topic><topic>Transcription Factors - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Pickett, Christopher L</creatorcontrib><creatorcontrib>Dietrich, Nicholas</creatorcontrib><creatorcontrib>Chen, Junfang</creatorcontrib><creatorcontrib>Xiong, Chengjie</creatorcontrib><creatorcontrib>Kornfeld, Kerry</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>PubMed Central (Full Participant titles)</collection><jtitle>G3 : genes - genomes - genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Pickett, Christopher L</au><au>Dietrich, Nicholas</au><au>Chen, Junfang</au><au>Xiong, Chengjie</au><au>Kornfeld, Kerry</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Mated Progeny Production Is a Biomarker of Aging in Caenorhabditis elegans</atitle><jtitle>G3 : genes - genomes - genetics</jtitle><addtitle>G3 (Bethesda)</addtitle><date>2013-12-09</date><risdate>2013</risdate><volume>3</volume><issue>12</issue><spage>2219</spage><epage>2232</epage><pages>2219-2232</pages><issn>2160-1836</issn><eissn>2160-1836</eissn><abstract>Abstract
The relationships between reproduction and aging are important for understanding the mechanisms of aging and evaluating evolutionary theories of aging. To investigate the effects of progeny production on reproductive and somatic aging, we conducted longitudinal studies of Caenorhabditis elegans hermaphrodites. For mated wild-type animals that were not sperm limited and survived past the end of the reproductive period, high levels of cross-progeny production were positively correlated with delayed reproductive and somatic aging. In this group of animals, individuals that generated more cross progeny also reproduced and lived longer than individuals that generated fewer cross progeny. These results indicate that progeny production does not accelerate reproductive or somatic aging. This longitudinal study demonstrated that cumulative cross progeny production through day four is an early-stage biomarker that is a positive predictor of longevity. Furthermore, in mated animals, high levels of early cross progeny production were positively correlated with high levels of late cross progeny production, indicating that early progeny production does not accelerate reproductive aging. The relationships between progeny production and aging were further evaluated by comparing self-fertile hermaphrodites that generated relatively few self progeny with mated hermaphrodites that generated many cross progeny. The timing of age-related somatic degeneration was similar in these groups, suggesting progeny production does not accelerate somatic aging. These studies rigorously define relationships between progeny production, reproductive aging, and somatic aging and identify new biomarkers of C. elegans aging. These results indicate that some mechanisms or pathways control age-related degeneration of both reproductive and somatic tissues in C. elegans.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>24142929</pmid><doi>10.1534/g3.113.008664</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Aging - physiology Animals Biomarkers Caenorhabditis elegans - physiology Caenorhabditis elegans Proteins - genetics Disorders of Sex Development DNA-Binding Proteins - genetics Female Investigations Male Reproduction - genetics Reproduction - physiology Sexual Behavior, Animal Transcription Factors - genetics |
title | Mated Progeny Production Is a Biomarker of Aging in Caenorhabditis elegans |
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