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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...

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Autores principales: Das, Srijit, Ooi, Felicia K, Cruz Corchado, Johnny, Fuller, Leah C, Weiner, Joshua A, Prahlad, Veena
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7237211/
https://www.ncbi.nlm.nih.gov/pubmed/32324136
http://dx.doi.org/10.7554/eLife.55246
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author Das, Srijit
Ooi, Felicia K
Cruz Corchado, Johnny
Fuller, Leah C
Weiner, Joshua A
Prahlad, Veena
author_facet Das, Srijit
Ooi, Felicia K
Cruz Corchado, Johnny
Fuller, Leah C
Weiner, Joshua A
Prahlad, Veena
author_sort Das, Srijit
collection PubMed
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.
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spelling pubmed-72372112020-05-20 Serotonin signaling by maternal neurons upon stress ensures progeny survival Das, Srijit Ooi, Felicia K Cruz Corchado, Johnny Fuller, Leah C Weiner, Joshua A Prahlad, Veena eLife Cell Biology 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. eLife Sciences Publications, Ltd 2020-04-23 /pmc/articles/PMC7237211/ /pubmed/32324136 http://dx.doi.org/10.7554/eLife.55246 Text en © 2020, Das et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Das, Srijit
Ooi, Felicia K
Cruz Corchado, Johnny
Fuller, Leah C
Weiner, Joshua A
Prahlad, Veena
Serotonin signaling by maternal neurons upon stress ensures progeny survival
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 Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7237211/
https://www.ncbi.nlm.nih.gov/pubmed/32324136
http://dx.doi.org/10.7554/eLife.55246
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