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Environmental stress and nanoplastics’ effects on Ciona robusta: regulation of immune/stress-related genes and induction of innate memory in pharynx and gut

In addition to circulating haemocytes, the immune system of the solitary ascidian Ciona robusta relies on two organs, the pharynx and the gut, and encompasses a wide array of immune and stress-related genes. How the pharynx and the gut of C. robusta react and adapt to environmental stress was assess...

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Autores principales: Marino, Rita, Melillo, Daniela, Italiani, Paola, Boraschi, Diana
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10258323/
https://www.ncbi.nlm.nih.gov/pubmed/37313415
http://dx.doi.org/10.3389/fimmu.2023.1176982
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author Marino, Rita
Melillo, Daniela
Italiani, Paola
Boraschi, Diana
author_facet Marino, Rita
Melillo, Daniela
Italiani, Paola
Boraschi, Diana
author_sort Marino, Rita
collection PubMed
description In addition to circulating haemocytes, the immune system of the solitary ascidian Ciona robusta relies on two organs, the pharynx and the gut, and encompasses a wide array of immune and stress-related genes. How the pharynx and the gut of C. robusta react and adapt to environmental stress was assessed upon short or long exposure to hypoxia/starvation in the absence or in the presence of polystyrene nanoplastics. We show that the immune response to stress is very different between the two organs, suggesting an organ-specific immune adaptation to the environmental changes. Notably, the presence of nanoplastics appears to alter the gene modulation induced by hypoxia/starvation in both organs, resulting in a partial increase in gene up-regulation in the pharynx and a less evident response to stress in the gut. We have also assessed whether the hypoxia/starvation stress could induce innate memory, measured as gene expression in response to a subsequent challenge with the bacterial agent LPS. Exposure to stress one week before challenge induced a substantial change in the response to LPS, with a general decrease of gene expression in the pharynx and a strong increase in the gut. Co-exposure with nanoplastics only partially modulated the stress-induced memory response to LPS, without substantially changing the stress-dependent gene expression profile in either organ. Overall, the presence of nanoplastics in the marine environment seems able to decrease the immune response of C. robusta to stressful conditions, hypothetically implying a reduced capacity to adapt to environmental changes, but only partially affects the stress-dependent induction of innate memory and subsequent responses to infectious challenges.
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spelling pubmed-102583232023-06-13 Environmental stress and nanoplastics’ effects on Ciona robusta: regulation of immune/stress-related genes and induction of innate memory in pharynx and gut Marino, Rita Melillo, Daniela Italiani, Paola Boraschi, Diana Front Immunol Immunology In addition to circulating haemocytes, the immune system of the solitary ascidian Ciona robusta relies on two organs, the pharynx and the gut, and encompasses a wide array of immune and stress-related genes. How the pharynx and the gut of C. robusta react and adapt to environmental stress was assessed upon short or long exposure to hypoxia/starvation in the absence or in the presence of polystyrene nanoplastics. We show that the immune response to stress is very different between the two organs, suggesting an organ-specific immune adaptation to the environmental changes. Notably, the presence of nanoplastics appears to alter the gene modulation induced by hypoxia/starvation in both organs, resulting in a partial increase in gene up-regulation in the pharynx and a less evident response to stress in the gut. We have also assessed whether the hypoxia/starvation stress could induce innate memory, measured as gene expression in response to a subsequent challenge with the bacterial agent LPS. Exposure to stress one week before challenge induced a substantial change in the response to LPS, with a general decrease of gene expression in the pharynx and a strong increase in the gut. Co-exposure with nanoplastics only partially modulated the stress-induced memory response to LPS, without substantially changing the stress-dependent gene expression profile in either organ. Overall, the presence of nanoplastics in the marine environment seems able to decrease the immune response of C. robusta to stressful conditions, hypothetically implying a reduced capacity to adapt to environmental changes, but only partially affects the stress-dependent induction of innate memory and subsequent responses to infectious challenges. Frontiers Media S.A. 2023-05-29 /pmc/articles/PMC10258323/ /pubmed/37313415 http://dx.doi.org/10.3389/fimmu.2023.1176982 Text en Copyright © 2023 Marino, Melillo, Italiani and Boraschi https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
Marino, Rita
Melillo, Daniela
Italiani, Paola
Boraschi, Diana
Environmental stress and nanoplastics’ effects on Ciona robusta: regulation of immune/stress-related genes and induction of innate memory in pharynx and gut
title Environmental stress and nanoplastics’ effects on Ciona robusta: regulation of immune/stress-related genes and induction of innate memory in pharynx and gut
title_full Environmental stress and nanoplastics’ effects on Ciona robusta: regulation of immune/stress-related genes and induction of innate memory in pharynx and gut
title_fullStr Environmental stress and nanoplastics’ effects on Ciona robusta: regulation of immune/stress-related genes and induction of innate memory in pharynx and gut
title_full_unstemmed Environmental stress and nanoplastics’ effects on Ciona robusta: regulation of immune/stress-related genes and induction of innate memory in pharynx and gut
title_short Environmental stress and nanoplastics’ effects on Ciona robusta: regulation of immune/stress-related genes and induction of innate memory in pharynx and gut
title_sort environmental stress and nanoplastics’ effects on ciona robusta: regulation of immune/stress-related genes and induction of innate memory in pharynx and gut
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10258323/
https://www.ncbi.nlm.nih.gov/pubmed/37313415
http://dx.doi.org/10.3389/fimmu.2023.1176982
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