mRNA decapping is an evolutionarily conserved modulator of neuroendocrine signaling that controls development and ageing
Eukaryotic 5’−3’ mRNA decay plays important roles during development and in response to stress, regulating gene expression post-transcriptionally. In Caenorhabditis elegans, deficiency of DCAP-1/DCP1, the essential co-factor of the major cytoplasmic mRNA decapping enzyme, impacts normal development,...
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| Format: | Article |
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eLife Sciences Publications Ltd
2020-05-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/53757 |
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| author | Fivos Borbolis John Rallis George Kanatouris Nikolitsa Kokla Antonis Karamalegkos Christina Vasileiou Katerina M Vakaloglou George Diallinas Dimitrios J Stravopodis Christos G Zervas Popi Syntichaki |
| author_facet | Fivos Borbolis John Rallis George Kanatouris Nikolitsa Kokla Antonis Karamalegkos Christina Vasileiou Katerina M Vakaloglou George Diallinas Dimitrios J Stravopodis Christos G Zervas Popi Syntichaki |
| author_sort | Fivos Borbolis |
| collection | DOAJ |
| description | Eukaryotic 5’−3’ mRNA decay plays important roles during development and in response to stress, regulating gene expression post-transcriptionally. In Caenorhabditis elegans, deficiency of DCAP-1/DCP1, the essential co-factor of the major cytoplasmic mRNA decapping enzyme, impacts normal development, stress survival and ageing. Here, we show that overexpression of dcap-1 in neurons of worms is sufficient to increase lifespan through the function of the insulin/IGF-like signaling and its effector DAF-16/FOXO transcription factor. Neuronal DCAP-1 affects basal levels of INS-7, an ageing-related insulin-like peptide, which acts in the intestine to determine lifespan. Short-lived dcap-1 mutants exhibit a neurosecretion-dependent upregulation of intestinal ins-7 transcription, and diminished nuclear localization of DAF-16/FOXO. Moreover, neuronal overexpression of DCP1 in Drosophila melanogaster confers longevity in adults, while neuronal DCP1 deficiency shortens lifespan and affects wing morphogenesis, cell non-autonomously. Our genetic analysis in two model-organisms suggests a critical and conserved function of DCAP-1/DCP1 in developmental events and lifespan modulation. |
| first_indexed | 2024-04-12T12:04:36Z |
| format | Article |
| id | doaj.art-70b7733d7efd4e01b0d12cb392e90b83 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T12:04:36Z |
| publishDate | 2020-05-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-70b7733d7efd4e01b0d12cb392e90b832022-12-22T03:33:45ZengeLife Sciences Publications LtdeLife2050-084X2020-05-01910.7554/eLife.53757mRNA decapping is an evolutionarily conserved modulator of neuroendocrine signaling that controls development and ageingFivos Borbolis0https://orcid.org/0000-0001-6559-1356John Rallis1George Kanatouris2Nikolitsa Kokla3Antonis Karamalegkos4Christina Vasileiou5Katerina M Vakaloglou6George Diallinas7https://orcid.org/0000-0002-3426-726XDimitrios J Stravopodis8Christos G Zervas9https://orcid.org/0000-0003-0531-9515Popi Syntichaki10https://orcid.org/0000-0001-9536-8905Biomedical Research Foundation of the Academy of Athens, Center of Basic Research, Athens, Greece; Department of Biology, School of Science, National and Kapodistrian University of Athens, Athens, GreeceBiomedical Research Foundation of the Academy of Athens, Center of Basic Research, Athens, Greece; Department of Biology, School of Science, National and Kapodistrian University of Athens, Athens, GreeceBiomedical Research Foundation of the Academy of Athens, Center of Basic Research, Athens, Greece; Department of Biology, School of Science, National and Kapodistrian University of Athens, Athens, GreeceBiomedical Research Foundation of the Academy of Athens, Center of Basic Research, Athens, Greece; Department of Biology, School of Science, National and Kapodistrian University of Athens, Athens, GreeceBiomedical Research Foundation of the Academy of Athens, Center of Basic Research, Athens, Greece; Department of Biology, School of Science, National and Kapodistrian University of Athens, Athens, GreeceBiomedical Research Foundation of the Academy of Athens, Center of Basic Research, Athens, Greece; Department of Molecular Biology and Genetics, Democritus University of Thrace, Alex/polis, GreeceBiomedical Research Foundation of the Academy of Athens, Center of Basic Research, Athens, GreeceDepartment of Biology, School of Science, National and Kapodistrian University of Athens, Athens, GreeceDepartment of Biology, School of Science, National and Kapodistrian University of Athens, Athens, GreeceBiomedical Research Foundation of the Academy of Athens, Center of Basic Research, Athens, GreeceBiomedical Research Foundation of the Academy of Athens, Center of Basic Research, Athens, GreeceEukaryotic 5’−3’ mRNA decay plays important roles during development and in response to stress, regulating gene expression post-transcriptionally. In Caenorhabditis elegans, deficiency of DCAP-1/DCP1, the essential co-factor of the major cytoplasmic mRNA decapping enzyme, impacts normal development, stress survival and ageing. Here, we show that overexpression of dcap-1 in neurons of worms is sufficient to increase lifespan through the function of the insulin/IGF-like signaling and its effector DAF-16/FOXO transcription factor. Neuronal DCAP-1 affects basal levels of INS-7, an ageing-related insulin-like peptide, which acts in the intestine to determine lifespan. Short-lived dcap-1 mutants exhibit a neurosecretion-dependent upregulation of intestinal ins-7 transcription, and diminished nuclear localization of DAF-16/FOXO. Moreover, neuronal overexpression of DCP1 in Drosophila melanogaster confers longevity in adults, while neuronal DCP1 deficiency shortens lifespan and affects wing morphogenesis, cell non-autonomously. Our genetic analysis in two model-organisms suggests a critical and conserved function of DCAP-1/DCP1 in developmental events and lifespan modulation.https://elifesciences.org/articles/53757Caenorhabditis elegansDrosophila melanogasterDCAP-1/DCP1iongevityins-7wing development |
| spellingShingle | Fivos Borbolis John Rallis George Kanatouris Nikolitsa Kokla Antonis Karamalegkos Christina Vasileiou Katerina M Vakaloglou George Diallinas Dimitrios J Stravopodis Christos G Zervas Popi Syntichaki mRNA decapping is an evolutionarily conserved modulator of neuroendocrine signaling that controls development and ageing eLife Caenorhabditis elegans Drosophila melanogaster DCAP-1/DCP1 iongevity ins-7 wing development |
| title | mRNA decapping is an evolutionarily conserved modulator of neuroendocrine signaling that controls development and ageing |
| title_full | mRNA decapping is an evolutionarily conserved modulator of neuroendocrine signaling that controls development and ageing |
| title_fullStr | mRNA decapping is an evolutionarily conserved modulator of neuroendocrine signaling that controls development and ageing |
| title_full_unstemmed | mRNA decapping is an evolutionarily conserved modulator of neuroendocrine signaling that controls development and ageing |
| title_short | mRNA decapping is an evolutionarily conserved modulator of neuroendocrine signaling that controls development and ageing |
| title_sort | mrna decapping is an evolutionarily conserved modulator of neuroendocrine signaling that controls development and ageing |
| topic | Caenorhabditis elegans Drosophila melanogaster DCAP-1/DCP1 iongevity ins-7 wing development |
| url | https://elifesciences.org/articles/53757 |
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