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Establishment of the immunological self in juvenile Patiria pectinifera post-metamorphosis

Ontogeny of the immune system is a fundamental immunology issue. One indicator of immune system maturation is the establishment of the immunological self, which describes the ability of the immune system to distinguish allogeneic individuals (allorecognition ability). However, the timing of immune s...

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Autores principales: Taguchi, Mizuki, Minakata, Kota, Tame, Akihiro, Furukawa, Ryohei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9763293/
https://www.ncbi.nlm.nih.gov/pubmed/36561757
http://dx.doi.org/10.3389/fimmu.2022.1056027
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author Taguchi, Mizuki
Minakata, Kota
Tame, Akihiro
Furukawa, Ryohei
author_facet Taguchi, Mizuki
Minakata, Kota
Tame, Akihiro
Furukawa, Ryohei
author_sort Taguchi, Mizuki
collection PubMed
description Ontogeny of the immune system is a fundamental immunology issue. One indicator of immune system maturation is the establishment of the immunological self, which describes the ability of the immune system to distinguish allogeneic individuals (allorecognition ability). However, the timing of immune system maturation during invertebrate ontogeny is poorly understood. In the sea star Patiria pectinifera, cells that have dissociated from the embryos and larvae are able to reconstruct larvae. This reconstruction phenomenon is possible because of a lack of allorecognition capability in the larval immune system, which facilitates the formation of an allogeneic chimera. In this study, we revealed that the adult immune cells of P. pectinifera (coelomocytes) have allorecognition ability. Based on a hypothesis that allorecognition ability is acquired before and after metamorphosis, we conducted detailed morphological observations and survival time analysis of metamorphosis-induced chimeric larvae. The results showed that all allogeneic chimeras died within approximately two weeks to one month of reaching the juvenile stage. In these chimeras, the majority of the epidermal cell layer was lost and the mesenchymal region expanded, but cell death appeared enhanced in the digestive tract. These results indicate that the immunological self of P. pectinifera is established post-metamorphosis during the juvenile stage. This is the first study to identify the timing of immune system maturation during echinodermal ontogenesis. As well as establishing P. pectinifera as an excellent model for studies on self- and non-self-recognition, this study enhances our understanding of the ontogeny of the immune system in invertebrates.
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spelling pubmed-97632932022-12-21 Establishment of the immunological self in juvenile Patiria pectinifera post-metamorphosis Taguchi, Mizuki Minakata, Kota Tame, Akihiro Furukawa, Ryohei Front Immunol Immunology Ontogeny of the immune system is a fundamental immunology issue. One indicator of immune system maturation is the establishment of the immunological self, which describes the ability of the immune system to distinguish allogeneic individuals (allorecognition ability). However, the timing of immune system maturation during invertebrate ontogeny is poorly understood. In the sea star Patiria pectinifera, cells that have dissociated from the embryos and larvae are able to reconstruct larvae. This reconstruction phenomenon is possible because of a lack of allorecognition capability in the larval immune system, which facilitates the formation of an allogeneic chimera. In this study, we revealed that the adult immune cells of P. pectinifera (coelomocytes) have allorecognition ability. Based on a hypothesis that allorecognition ability is acquired before and after metamorphosis, we conducted detailed morphological observations and survival time analysis of metamorphosis-induced chimeric larvae. The results showed that all allogeneic chimeras died within approximately two weeks to one month of reaching the juvenile stage. In these chimeras, the majority of the epidermal cell layer was lost and the mesenchymal region expanded, but cell death appeared enhanced in the digestive tract. These results indicate that the immunological self of P. pectinifera is established post-metamorphosis during the juvenile stage. This is the first study to identify the timing of immune system maturation during echinodermal ontogenesis. As well as establishing P. pectinifera as an excellent model for studies on self- and non-self-recognition, this study enhances our understanding of the ontogeny of the immune system in invertebrates. Frontiers Media S.A. 2022-12-06 /pmc/articles/PMC9763293/ /pubmed/36561757 http://dx.doi.org/10.3389/fimmu.2022.1056027 Text en Copyright © 2022 Taguchi, Minakata, Tame and Furukawa 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
Taguchi, Mizuki
Minakata, Kota
Tame, Akihiro
Furukawa, Ryohei
Establishment of the immunological self in juvenile Patiria pectinifera post-metamorphosis
title Establishment of the immunological self in juvenile Patiria pectinifera post-metamorphosis
title_full Establishment of the immunological self in juvenile Patiria pectinifera post-metamorphosis
title_fullStr Establishment of the immunological self in juvenile Patiria pectinifera post-metamorphosis
title_full_unstemmed Establishment of the immunological self in juvenile Patiria pectinifera post-metamorphosis
title_short Establishment of the immunological self in juvenile Patiria pectinifera post-metamorphosis
title_sort establishment of the immunological self in juvenile patiria pectinifera post-metamorphosis
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9763293/
https://www.ncbi.nlm.nih.gov/pubmed/36561757
http://dx.doi.org/10.3389/fimmu.2022.1056027
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