FoxO is a critical regulator of stem cell maintenance in immortal Hydra
Hydra ’s unlimited life span has long attracted attention from natural scientists. The reason for that phenomenon is the indefinite self-renewal capacity of its stem cells. The underlying molecular mechanisms have yet to be explored. Here, by comparing the transcriptomes of Hydra ’s stem cells follo...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2012-11, Vol.109 (48), p.19697-19702 |
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| container_title | Proceedings of the National Academy of Sciences - PNAS |
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| creator | Boehm, Anna-Marei Khalturin, Konstantin Anton-Erxleben, Friederike Hemmrich, Georg Klostermeier, Ulrich C Lopez-Quintero, Javier A Oberg, Hans-Heinrich Puchert, Malte Rosenstiel, Philip Wittlieb, Jörg Bosch, Thomas C. G |
| description | Hydra ’s unlimited life span has long attracted attention from natural scientists. The reason for that phenomenon is the indefinite self-renewal capacity of its stem cells. The underlying molecular mechanisms have yet to be explored. Here, by comparing the transcriptomes of Hydra ’s stem cells followed by functional analysis using transgenic polyps, we identified the transcription factor forkhead box O (FoxO) as one of the critical drivers of this continuous self-renewal. foxO overexpression increased interstitial stem cell and progenitor cell proliferation and activated stem cell genes in terminally differentiated somatic cells. foxO down-regulation led to an increase in the number of terminally differentiated cells, resulting in a drastically reduced population growth rate. In addition, it caused down-regulation of stem cell genes and antimicrobial peptide (AMP) expression. These findings contribute to a molecular understanding of Hydra ’s immortality, indicate an evolutionarily conserved role of FoxO in controlling longevity from Hydra to humans, and have implications for understanding cellular aging. |
| doi_str_mv | 10.1073/pnas.1209714109 |
| format | Article |
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Here, by comparing the transcriptomes of Hydra ’s stem cells followed by functional analysis using transgenic polyps, we identified the transcription factor forkhead box O (FoxO) as one of the critical drivers of this continuous self-renewal. foxO overexpression increased interstitial stem cell and progenitor cell proliferation and activated stem cell genes in terminally differentiated somatic cells. foxO down-regulation led to an increase in the number of terminally differentiated cells, resulting in a drastically reduced population growth rate. In addition, it caused down-regulation of stem cell genes and antimicrobial peptide (AMP) expression. These findings contribute to a molecular understanding of Hydra ’s immortality, indicate an evolutionarily conserved role of FoxO in controlling longevity from Hydra to humans, and have implications for understanding cellular aging.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1209714109</identifier><identifier>PMID: 23150562</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>adenosine monophosphate ; Animals ; Animals, Genetically Modified ; antimicrobial peptides ; Aquatic life ; Biological Sciences ; Cell growth ; Cell Lineage ; Cell lines ; cell proliferation ; Epithelial cells ; Evolution ; Forkhead Transcription Factors - genetics ; Forkhead Transcription Factors - physiology ; Gene expression ; gene expression regulation ; gene overexpression ; Gene Silencing ; genes ; genetically modified organisms ; humans ; Hydra ; Hydra - cytology ; Hydra - immunology ; Hydra - metabolism ; Immunity, Innate ; Interstitial cells ; Life span ; Longevity ; Molecular Sequence Data ; Neural stem cells ; Peptides ; population growth ; Proteins ; Somatic cells ; Stem cells ; Stem Cells - metabolism ; Transcription factors ; transcriptome</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2012-11, Vol.109 (48), p.19697-19702</ispartof><rights>copyright © 1993-2008 National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Nov 27, 2012</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c492t-93517e82b24a703f6ecd8fc6c68b75a728b547e41aa165be0d90acdb7487e4453</citedby><cites>FETCH-LOGICAL-c492t-93517e82b24a703f6ecd8fc6c68b75a728b547e41aa165be0d90acdb7487e4453</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/109/48.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/41830278$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/41830278$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,803,885,27923,27924,53790,53792,58016,58249</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23150562$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Boehm, Anna-Marei</creatorcontrib><creatorcontrib>Khalturin, Konstantin</creatorcontrib><creatorcontrib>Anton-Erxleben, Friederike</creatorcontrib><creatorcontrib>Hemmrich, Georg</creatorcontrib><creatorcontrib>Klostermeier, Ulrich C</creatorcontrib><creatorcontrib>Lopez-Quintero, Javier A</creatorcontrib><creatorcontrib>Oberg, Hans-Heinrich</creatorcontrib><creatorcontrib>Puchert, Malte</creatorcontrib><creatorcontrib>Rosenstiel, Philip</creatorcontrib><creatorcontrib>Wittlieb, Jörg</creatorcontrib><creatorcontrib>Bosch, Thomas C. G</creatorcontrib><title>FoxO is a critical regulator of stem cell maintenance in immortal Hydra</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Hydra ’s unlimited life span has long attracted attention from natural scientists. The reason for that phenomenon is the indefinite self-renewal capacity of its stem cells. The underlying molecular mechanisms have yet to be explored. Here, by comparing the transcriptomes of Hydra ’s stem cells followed by functional analysis using transgenic polyps, we identified the transcription factor forkhead box O (FoxO) as one of the critical drivers of this continuous self-renewal. foxO overexpression increased interstitial stem cell and progenitor cell proliferation and activated stem cell genes in terminally differentiated somatic cells. foxO down-regulation led to an increase in the number of terminally differentiated cells, resulting in a drastically reduced population growth rate. In addition, it caused down-regulation of stem cell genes and antimicrobial peptide (AMP) expression. These findings contribute to a molecular understanding of Hydra ’s immortality, indicate an evolutionarily conserved role of FoxO in controlling longevity from Hydra to humans, and have implications for understanding cellular aging.</description><subject>adenosine monophosphate</subject><subject>Animals</subject><subject>Animals, Genetically Modified</subject><subject>antimicrobial peptides</subject><subject>Aquatic life</subject><subject>Biological Sciences</subject><subject>Cell growth</subject><subject>Cell Lineage</subject><subject>Cell lines</subject><subject>cell proliferation</subject><subject>Epithelial cells</subject><subject>Evolution</subject><subject>Forkhead Transcription Factors - genetics</subject><subject>Forkhead Transcription Factors - physiology</subject><subject>Gene expression</subject><subject>gene expression regulation</subject><subject>gene overexpression</subject><subject>Gene Silencing</subject><subject>genes</subject><subject>genetically modified organisms</subject><subject>humans</subject><subject>Hydra</subject><subject>Hydra - cytology</subject><subject>Hydra - immunology</subject><subject>Hydra - metabolism</subject><subject>Immunity, Innate</subject><subject>Interstitial cells</subject><subject>Life span</subject><subject>Longevity</subject><subject>Molecular Sequence Data</subject><subject>Neural stem cells</subject><subject>Peptides</subject><subject>population growth</subject><subject>Proteins</subject><subject>Somatic cells</subject><subject>Stem cells</subject><subject>Stem Cells - metabolism</subject><subject>Transcription factors</subject><subject>transcriptome</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkc1v1DAQxS0EokvhzAmwxIVL2vFHYvtSCVW0RarUA_RsTRxn8SqJFztB9L_Hyy5b4GJLfr95nqdHyGsGZwyUON9OmM8YB6OYZGCekFU5WdVIA0_JCoCrSksuT8iLnDcAYGoNz8kJF6yGuuErcn0Vf97RkClSl8IcHA40-fUy4BwTjT3Nsx-p88NARwzT7CecnKdhomEcY5oLfvPQJXxJnvU4ZP_qcJ-S-6tPXy9vqtu768-XH28rJw2fKyNqprzmLZeoQPSNd53uXeMa3aoaFddtLZWXDJE1deuhM4Cua5XU5VXW4pRc7H23Szv6zvlpTjjYbQojpgcbMdh_lSl8s-v4w5aPmZKsGHw4GKT4ffF5tmPIu3w4-bhkyzgHZbgAXtD3_6GbuKSpxPtNNcIIDYU631MuxZyT74_LMLC7kuyuJPtYUpl4-3eGI_-nlQLQA7CbfLQzVmrLTGNUQd7skU0uRR0ZyXTZXOmiv9vrPUaL6xSyvf_CgTUATICsmfgFMEOqGw</recordid><startdate>20121127</startdate><enddate>20121127</enddate><creator>Boehm, Anna-Marei</creator><creator>Khalturin, Konstantin</creator><creator>Anton-Erxleben, Friederike</creator><creator>Hemmrich, Georg</creator><creator>Klostermeier, Ulrich C</creator><creator>Lopez-Quintero, Javier A</creator><creator>Oberg, Hans-Heinrich</creator><creator>Puchert, Malte</creator><creator>Rosenstiel, Philip</creator><creator>Wittlieb, Jörg</creator><creator>Bosch, Thomas C. 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Here, by comparing the transcriptomes of Hydra ’s stem cells followed by functional analysis using transgenic polyps, we identified the transcription factor forkhead box O (FoxO) as one of the critical drivers of this continuous self-renewal. foxO overexpression increased interstitial stem cell and progenitor cell proliferation and activated stem cell genes in terminally differentiated somatic cells. foxO down-regulation led to an increase in the number of terminally differentiated cells, resulting in a drastically reduced population growth rate. In addition, it caused down-regulation of stem cell genes and antimicrobial peptide (AMP) expression. 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| subjects | adenosine monophosphate Animals Animals, Genetically Modified antimicrobial peptides Aquatic life Biological Sciences Cell growth Cell Lineage Cell lines cell proliferation Epithelial cells Evolution Forkhead Transcription Factors - genetics Forkhead Transcription Factors - physiology Gene expression gene expression regulation gene overexpression Gene Silencing genes genetically modified organisms humans Hydra Hydra - cytology Hydra - immunology Hydra - metabolism Immunity, Innate Interstitial cells Life span Longevity Molecular Sequence Data Neural stem cells Peptides population growth Proteins Somatic cells Stem cells Stem Cells - metabolism Transcription factors transcriptome |
| title | FoxO is a critical regulator of stem cell maintenance in immortal Hydra |
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