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Modulatory upregulation of an insulin peptide gene by different pathogens in C. elegans
When an animal is infected, its innate immune response needs to be tightly regulated across tissues and coordinated with other aspects of organismal physiology. Previous studies with Caenorhabditis elegans have demonstrated that insulin-like peptide genes are differentially expressed in response to...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Taylor & Francis
2018
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5955453/ https://www.ncbi.nlm.nih.gov/pubmed/29405821 http://dx.doi.org/10.1080/21505594.2018.1433969 |
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author | Lee, Song-Hua Omi, Shizue Thakur, Nishant Taffoni, Clara Belougne, Jérôme Engelmann, Ilka Ewbank, Jonathan J. Pujol, Nathalie |
author_facet | Lee, Song-Hua Omi, Shizue Thakur, Nishant Taffoni, Clara Belougne, Jérôme Engelmann, Ilka Ewbank, Jonathan J. Pujol, Nathalie |
author_sort | Lee, Song-Hua |
collection | PubMed |
description | When an animal is infected, its innate immune response needs to be tightly regulated across tissues and coordinated with other aspects of organismal physiology. Previous studies with Caenorhabditis elegans have demonstrated that insulin-like peptide genes are differentially expressed in response to different pathogens. They represent prime candidates for conveying signals between tissues upon infection. Here, we focused on one such gene, ins-11 and its potential role in mediating cross-tissue regulation of innate immune genes. While diverse bacterial intestinal infections can trigger the up-regulation of ins-11 in the intestine, we show that epidermal infection with the fungus Drechmeria coniospora triggers an upregulation of ins-11 in the epidermis. Using the Shigella virulence factor OpsF, a MAP kinase inhibitor, we found that in both cases, ins-11 expression is controlled cell autonomously by p38 MAPK, but via distinct transcription factors, STA-2/STAT in the epidermis and HLH-30/TFEB in the intestine. We established that ins-11, and the insulin signaling pathway more generally, are not involved in the regulation of antimicrobial peptide gene expression in the epidermis. The up-regulation of ins-11 in the epidermis does, however, affect intestinal gene expression in a complex manner, and has a deleterious effect on longevity. These results support a model in which insulin signaling, via ins-11, contributes to the coordination of the organismal response to infection, influencing the allocation of resources in an infected animal. |
format | Online Article Text |
id | pubmed-5955453 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2018 |
publisher | Taylor & Francis |
record_format | MEDLINE/PubMed |
spelling | pubmed-59554532018-05-21 Modulatory upregulation of an insulin peptide gene by different pathogens in C. elegans Lee, Song-Hua Omi, Shizue Thakur, Nishant Taffoni, Clara Belougne, Jérôme Engelmann, Ilka Ewbank, Jonathan J. Pujol, Nathalie Virulence Research Paper When an animal is infected, its innate immune response needs to be tightly regulated across tissues and coordinated with other aspects of organismal physiology. Previous studies with Caenorhabditis elegans have demonstrated that insulin-like peptide genes are differentially expressed in response to different pathogens. They represent prime candidates for conveying signals between tissues upon infection. Here, we focused on one such gene, ins-11 and its potential role in mediating cross-tissue regulation of innate immune genes. While diverse bacterial intestinal infections can trigger the up-regulation of ins-11 in the intestine, we show that epidermal infection with the fungus Drechmeria coniospora triggers an upregulation of ins-11 in the epidermis. Using the Shigella virulence factor OpsF, a MAP kinase inhibitor, we found that in both cases, ins-11 expression is controlled cell autonomously by p38 MAPK, but via distinct transcription factors, STA-2/STAT in the epidermis and HLH-30/TFEB in the intestine. We established that ins-11, and the insulin signaling pathway more generally, are not involved in the regulation of antimicrobial peptide gene expression in the epidermis. The up-regulation of ins-11 in the epidermis does, however, affect intestinal gene expression in a complex manner, and has a deleterious effect on longevity. These results support a model in which insulin signaling, via ins-11, contributes to the coordination of the organismal response to infection, influencing the allocation of resources in an infected animal. Taylor & Francis 2018-03-19 /pmc/articles/PMC5955453/ /pubmed/29405821 http://dx.doi.org/10.1080/21505594.2018.1433969 Text en © 2018 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Research Paper Lee, Song-Hua Omi, Shizue Thakur, Nishant Taffoni, Clara Belougne, Jérôme Engelmann, Ilka Ewbank, Jonathan J. Pujol, Nathalie Modulatory upregulation of an insulin peptide gene by different pathogens in C. elegans |
title | Modulatory upregulation of an insulin peptide gene by different pathogens in C. elegans |
title_full | Modulatory upregulation of an insulin peptide gene by different pathogens in C. elegans |
title_fullStr | Modulatory upregulation of an insulin peptide gene by different pathogens in C. elegans |
title_full_unstemmed | Modulatory upregulation of an insulin peptide gene by different pathogens in C. elegans |
title_short | Modulatory upregulation of an insulin peptide gene by different pathogens in C. elegans |
title_sort | modulatory upregulation of an insulin peptide gene by different pathogens in c. elegans |
topic | Research Paper |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5955453/ https://www.ncbi.nlm.nih.gov/pubmed/29405821 http://dx.doi.org/10.1080/21505594.2018.1433969 |
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