Cargando…

Dietary restriction and gonadal signaling differentially regulate post‐development quality control functions in Caenorhabditis elegans

Protein homeostasis is remodeled early in Caenorhabditis elegans adulthood, resulting in a sharp decline in folding capacity and reduced ability to cope with chronic and acute stress. Endocrine signals from the reproductive system can ameliorate this proteostatic collapse and reshape the quality con...

Descripción completa

Detalles Bibliográficos
Autores principales: Shpigel, Nufar, Shemesh, Netta, Kishner, Mor, Ben‐Zvi, Anat
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6413660/
https://www.ncbi.nlm.nih.gov/pubmed/30648346
http://dx.doi.org/10.1111/acel.12891
_version_ 1783402863134769152
author Shpigel, Nufar
Shemesh, Netta
Kishner, Mor
Ben‐Zvi, Anat
author_facet Shpigel, Nufar
Shemesh, Netta
Kishner, Mor
Ben‐Zvi, Anat
author_sort Shpigel, Nufar
collection PubMed
description Protein homeostasis is remodeled early in Caenorhabditis elegans adulthood, resulting in a sharp decline in folding capacity and reduced ability to cope with chronic and acute stress. Endocrine signals from the reproductive system can ameliorate this proteostatic collapse and reshape the quality control network. Given that environmental conditions, such as food availability, impact reproductive success, we asked whether conditions of dietary restriction (DR) can also reverse the decline in quality control function at the transition to adulthood, and if so, whether gonadal signaling and dietary signaling remodel the quality control network in a similar or different manner. For this, we employed the eat‐2 genetic model and bacterial deprivation protocol. We found that animals under DR maintained heat shock response activation and high protein folding capacity during adulthood. However, while gonadal signaling required DAF‐16, DR‐associated rescue of quality control functions required the antagonistic transcription factor, PQM‐1. Bioinformatic analyses supported a role for DAF‐16 in acute stress responses and a role for PQM‐1 in cellular maintenance and chronic stress. Comparing the stress activation and folding capacities of dietary‐ and gonadal‐signaling mutant animals confirmed this prediction and demonstrated that each differentially impacts cellular quality control capabilities. These data suggest that the functional mode of cellular quality control networks can be differentially remodeled, affecting an organism's ability to respond to acute and chronic stresses during adulthood.
format Online
Article
Text
id pubmed-6413660
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher John Wiley and Sons Inc.
record_format MEDLINE/PubMed
spelling pubmed-64136602019-04-01 Dietary restriction and gonadal signaling differentially regulate post‐development quality control functions in Caenorhabditis elegans Shpigel, Nufar Shemesh, Netta Kishner, Mor Ben‐Zvi, Anat Aging Cell Original Papers Protein homeostasis is remodeled early in Caenorhabditis elegans adulthood, resulting in a sharp decline in folding capacity and reduced ability to cope with chronic and acute stress. Endocrine signals from the reproductive system can ameliorate this proteostatic collapse and reshape the quality control network. Given that environmental conditions, such as food availability, impact reproductive success, we asked whether conditions of dietary restriction (DR) can also reverse the decline in quality control function at the transition to adulthood, and if so, whether gonadal signaling and dietary signaling remodel the quality control network in a similar or different manner. For this, we employed the eat‐2 genetic model and bacterial deprivation protocol. We found that animals under DR maintained heat shock response activation and high protein folding capacity during adulthood. However, while gonadal signaling required DAF‐16, DR‐associated rescue of quality control functions required the antagonistic transcription factor, PQM‐1. Bioinformatic analyses supported a role for DAF‐16 in acute stress responses and a role for PQM‐1 in cellular maintenance and chronic stress. Comparing the stress activation and folding capacities of dietary‐ and gonadal‐signaling mutant animals confirmed this prediction and demonstrated that each differentially impacts cellular quality control capabilities. These data suggest that the functional mode of cellular quality control networks can be differentially remodeled, affecting an organism's ability to respond to acute and chronic stresses during adulthood. John Wiley and Sons Inc. 2019-01-15 2019-04 /pmc/articles/PMC6413660/ /pubmed/30648346 http://dx.doi.org/10.1111/acel.12891 Text en © 2018 The Authors. Aging Cell published by the Anatomical Society and John Wiley & Sons Ltd. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Papers
Shpigel, Nufar
Shemesh, Netta
Kishner, Mor
Ben‐Zvi, Anat
Dietary restriction and gonadal signaling differentially regulate post‐development quality control functions in Caenorhabditis elegans
title Dietary restriction and gonadal signaling differentially regulate post‐development quality control functions in Caenorhabditis elegans
title_full Dietary restriction and gonadal signaling differentially regulate post‐development quality control functions in Caenorhabditis elegans
title_fullStr Dietary restriction and gonadal signaling differentially regulate post‐development quality control functions in Caenorhabditis elegans
title_full_unstemmed Dietary restriction and gonadal signaling differentially regulate post‐development quality control functions in Caenorhabditis elegans
title_short Dietary restriction and gonadal signaling differentially regulate post‐development quality control functions in Caenorhabditis elegans
title_sort dietary restriction and gonadal signaling differentially regulate post‐development quality control functions in caenorhabditis elegans
topic Original Papers
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6413660/
https://www.ncbi.nlm.nih.gov/pubmed/30648346
http://dx.doi.org/10.1111/acel.12891
work_keys_str_mv AT shpigelnufar dietaryrestrictionandgonadalsignalingdifferentiallyregulatepostdevelopmentqualitycontrolfunctionsincaenorhabditiselegans
AT shemeshnetta dietaryrestrictionandgonadalsignalingdifferentiallyregulatepostdevelopmentqualitycontrolfunctionsincaenorhabditiselegans
AT kishnermor dietaryrestrictionandgonadalsignalingdifferentiallyregulatepostdevelopmentqualitycontrolfunctionsincaenorhabditiselegans
AT benzvianat dietaryrestrictionandgonadalsignalingdifferentiallyregulatepostdevelopmentqualitycontrolfunctionsincaenorhabditiselegans