Serotonin signaling by maternal neurons upon stress ensures progeny survival
Germ cells are vulnerable to stress. Therefore, how organisms protect their future progeny from damage in a fluctuating environment is a fundamental question in biology. We show that in Caenorhabditis elegans, serotonin released by maternal neurons during stress ensures the viability and stress resi...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2020-04-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/55246 |
| _version_ | 1828221814989389824 |
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| author | Srijit Das Felicia K Ooi Johnny Cruz Corchado Leah C Fuller Joshua A Weiner Veena Prahlad |
| author_facet | Srijit Das Felicia K Ooi Johnny Cruz Corchado Leah C Fuller Joshua A Weiner Veena Prahlad |
| author_sort | Srijit Das |
| collection | DOAJ |
| description | Germ cells are vulnerable to stress. Therefore, how organisms protect their future progeny from damage in a fluctuating environment is a fundamental question in biology. We show that in Caenorhabditis elegans, serotonin released by maternal neurons during stress ensures the viability and stress resilience of future offspring. Serotonin acts through a signal transduction pathway conserved between C. elegans and mammalian cells to enable the transcription factor HSF1 to alter chromatin in soon-to-be fertilized germ cells by recruiting the histone chaperone FACT, displacing histones, and initiating protective gene expression. Without serotonin release by maternal neurons, FACT is not recruited by HSF1 in germ cells, transcription occurs but is delayed, and progeny of stressed C. elegans mothers fail to complete development. These studies uncover a novel mechanism by which stress sensing by neurons is coupled to transcription response times of germ cells to protect future offspring. |
| first_indexed | 2024-04-12T16:45:32Z |
| format | Article |
| id | doaj.art-cefacc91422144ff8dea467d4ab32f29 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T16:45:32Z |
| publishDate | 2020-04-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-cefacc91422144ff8dea467d4ab32f292022-12-22T03:24:36ZengeLife Sciences Publications LtdeLife2050-084X2020-04-01910.7554/eLife.55246Serotonin signaling by maternal neurons upon stress ensures progeny survivalSrijit Das0https://orcid.org/0000-0002-0402-3256Felicia K Ooi1https://orcid.org/0000-0003-4766-2477Johnny Cruz Corchado2Leah C Fuller3Joshua A Weiner4https://orcid.org/0000-0002-3352-2847Veena Prahlad5https://orcid.org/0000-0002-0413-6074Department of Biology, Aging Mind and Brain Initiative, Iowa City, United StatesDepartment of Biology, Aging Mind and Brain Initiative, Iowa City, United StatesDepartment of Biology, Aging Mind and Brain Initiative, Iowa City, United StatesDepartment of Biology, Iowa City, United StatesDepartment of Biology, Iowa City, United States; Iowa Neuroscience Institute, Iowa City, United StatesDepartment of Biology, Aging Mind and Brain Initiative, Iowa City, United States; Department of Biology, Iowa City, United States; Iowa Neuroscience Institute, Iowa City, United StatesGerm cells are vulnerable to stress. Therefore, how organisms protect their future progeny from damage in a fluctuating environment is a fundamental question in biology. We show that in Caenorhabditis elegans, serotonin released by maternal neurons during stress ensures the viability and stress resilience of future offspring. Serotonin acts through a signal transduction pathway conserved between C. elegans and mammalian cells to enable the transcription factor HSF1 to alter chromatin in soon-to-be fertilized germ cells by recruiting the histone chaperone FACT, displacing histones, and initiating protective gene expression. Without serotonin release by maternal neurons, FACT is not recruited by HSF1 in germ cells, transcription occurs but is delayed, and progeny of stressed C. elegans mothers fail to complete development. These studies uncover a novel mechanism by which stress sensing by neurons is coupled to transcription response times of germ cells to protect future offspring.https://elifesciences.org/articles/55246HSF1serotonincell non-autonomousneuronal signalinghistone chaperoneepigenetic |
| spellingShingle | Srijit Das Felicia K Ooi Johnny Cruz Corchado Leah C Fuller Joshua A Weiner Veena Prahlad Serotonin signaling by maternal neurons upon stress ensures progeny survival eLife HSF1 serotonin cell non-autonomous neuronal signaling histone chaperone epigenetic |
| title | Serotonin signaling by maternal neurons upon stress ensures progeny survival |
| title_full | Serotonin signaling by maternal neurons upon stress ensures progeny survival |
| title_fullStr | Serotonin signaling by maternal neurons upon stress ensures progeny survival |
| title_full_unstemmed | Serotonin signaling by maternal neurons upon stress ensures progeny survival |
| title_short | Serotonin signaling by maternal neurons upon stress ensures progeny survival |
| title_sort | serotonin signaling by maternal neurons upon stress ensures progeny survival |
| topic | HSF1 serotonin cell non-autonomous neuronal signaling histone chaperone epigenetic |
| url | https://elifesciences.org/articles/55246 |
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