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Food perception without ingestion leads to metabolic changes and irreversible developmental arrest in C. elegans

BACKGROUND: Developmental physiology is very sensitive to nutrient availability. For instance, in the nematode Caenorhabditis elegans, newly hatched L1-stage larvae require food to initiate postembryonic development. In addition, larvae arrested in the dauer diapause, a non-feeding state of developm...

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Autores principales: Kaplan, Rebecca E. W., Webster, Amy K., Chitrakar, Rojin, Dent, Joseph A., Baugh, L. Ryan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6176503/
https://www.ncbi.nlm.nih.gov/pubmed/30296941
http://dx.doi.org/10.1186/s12915-018-0579-3
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author Kaplan, Rebecca E. W.
Webster, Amy K.
Chitrakar, Rojin
Dent, Joseph A.
Baugh, L. Ryan
author_facet Kaplan, Rebecca E. W.
Webster, Amy K.
Chitrakar, Rojin
Dent, Joseph A.
Baugh, L. Ryan
author_sort Kaplan, Rebecca E. W.
collection PubMed
description BACKGROUND: Developmental physiology is very sensitive to nutrient availability. For instance, in the nematode Caenorhabditis elegans, newly hatched L1-stage larvae require food to initiate postembryonic development. In addition, larvae arrested in the dauer diapause, a non-feeding state of developmental arrest that occurs during the L3 stage, initiate recovery when exposed to food. Despite the essential role of food in C. elegans development, the contribution of food perception versus ingestion on physiology has not been delineated. RESULTS: We used a pharmacological approach to uncouple the effects of food (bacteria) perception and ingestion in C. elegans. Perception was not sufficient to promote postembryonic development in L1-stage larvae. However, L1 larvae exposed to food without ingestion failed to develop upon return to normal culture conditions, instead displaying an irreversible arrest phenotype. Inhibition of gene expression during perception rescued subsequent development, demonstrating that the response to perception without feeding is deleterious. Perception altered DAF-16/FOXO subcellular localization, reflecting activation of insulin/IGF signaling (IIS). The insulin-like peptide daf-28 was specifically required, suggesting perception in chemosensory neurons, where it is expressed, regulates peptide synthesis and possibly secretion. However, genetic manipulation of IIS did not modify the irreversible arrest phenotype caused by food perception, revealing that wild-type function of the IIS pathway is not required to produce this phenotype and that other pathways affected by perception of food in the absence of its ingestion are likely to be involved. Gene expression and Nile red staining showed that food perception could alter lipid metabolism and storage. We found that starved larvae sense environmental polypeptides, with similar molecular and developmental effects as perception of bacteria. Environmental polypeptides also promoted recovery from dauer diapause, suggesting that perception of polypeptides plays an important role in the life history of free-living nematodes. CONCLUSIONS: We conclude that actual ingestion of food is required to initiate postembryonic development in C. elegans. We also conclude that polypeptides are perceived as a food-associated cue in this and likely other animals, initiating a signaling and gene regulatory cascade that alters metabolism in anticipation of feeding and development, but that this response is detrimental if feeding does not occur. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12915-018-0579-3) contains supplementary material, which is available to authorized users.
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spelling pubmed-61765032018-10-18 Food perception without ingestion leads to metabolic changes and irreversible developmental arrest in C. elegans Kaplan, Rebecca E. W. Webster, Amy K. Chitrakar, Rojin Dent, Joseph A. Baugh, L. Ryan BMC Biol Research Article BACKGROUND: Developmental physiology is very sensitive to nutrient availability. For instance, in the nematode Caenorhabditis elegans, newly hatched L1-stage larvae require food to initiate postembryonic development. In addition, larvae arrested in the dauer diapause, a non-feeding state of developmental arrest that occurs during the L3 stage, initiate recovery when exposed to food. Despite the essential role of food in C. elegans development, the contribution of food perception versus ingestion on physiology has not been delineated. RESULTS: We used a pharmacological approach to uncouple the effects of food (bacteria) perception and ingestion in C. elegans. Perception was not sufficient to promote postembryonic development in L1-stage larvae. However, L1 larvae exposed to food without ingestion failed to develop upon return to normal culture conditions, instead displaying an irreversible arrest phenotype. Inhibition of gene expression during perception rescued subsequent development, demonstrating that the response to perception without feeding is deleterious. Perception altered DAF-16/FOXO subcellular localization, reflecting activation of insulin/IGF signaling (IIS). The insulin-like peptide daf-28 was specifically required, suggesting perception in chemosensory neurons, where it is expressed, regulates peptide synthesis and possibly secretion. However, genetic manipulation of IIS did not modify the irreversible arrest phenotype caused by food perception, revealing that wild-type function of the IIS pathway is not required to produce this phenotype and that other pathways affected by perception of food in the absence of its ingestion are likely to be involved. Gene expression and Nile red staining showed that food perception could alter lipid metabolism and storage. We found that starved larvae sense environmental polypeptides, with similar molecular and developmental effects as perception of bacteria. Environmental polypeptides also promoted recovery from dauer diapause, suggesting that perception of polypeptides plays an important role in the life history of free-living nematodes. CONCLUSIONS: We conclude that actual ingestion of food is required to initiate postembryonic development in C. elegans. We also conclude that polypeptides are perceived as a food-associated cue in this and likely other animals, initiating a signaling and gene regulatory cascade that alters metabolism in anticipation of feeding and development, but that this response is detrimental if feeding does not occur. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12915-018-0579-3) contains supplementary material, which is available to authorized users. BioMed Central 2018-10-08 /pmc/articles/PMC6176503/ /pubmed/30296941 http://dx.doi.org/10.1186/s12915-018-0579-3 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Kaplan, Rebecca E. W.
Webster, Amy K.
Chitrakar, Rojin
Dent, Joseph A.
Baugh, L. Ryan
Food perception without ingestion leads to metabolic changes and irreversible developmental arrest in C. elegans
title Food perception without ingestion leads to metabolic changes and irreversible developmental arrest in C. elegans
title_full Food perception without ingestion leads to metabolic changes and irreversible developmental arrest in C. elegans
title_fullStr Food perception without ingestion leads to metabolic changes and irreversible developmental arrest in C. elegans
title_full_unstemmed Food perception without ingestion leads to metabolic changes and irreversible developmental arrest in C. elegans
title_short Food perception without ingestion leads to metabolic changes and irreversible developmental arrest in C. elegans
title_sort food perception without ingestion leads to metabolic changes and irreversible developmental arrest in c. elegans
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6176503/
https://www.ncbi.nlm.nih.gov/pubmed/30296941
http://dx.doi.org/10.1186/s12915-018-0579-3
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