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Broad Ultrastructural and Transcriptomic Changes Underlie the Multinucleated Giant Hemocyte Mediated Innate Immune Response against Parasitoids
Multinucleated giant hemocytes (MGHs) represent a novel type of blood cell in insects that participate in a highly efficient immune response against parasitoid wasps involving isolation and killing of the parasite. Previously, we showed that circulating MGHs have high motility and the interaction wi...
Autores principales: | , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
S. Karger AG
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9275024/ https://www.ncbi.nlm.nih.gov/pubmed/34864742 http://dx.doi.org/10.1159/000520110 |
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author | Cinege, Gyöngyi Magyar, Lilla B. Kovács, Attila L. Lerner, Zita Juhász, Gábor Lukacsovich, David Winterer, Jochen Lukacsovich, Tamás Hegedűs, Zoltán Kurucz, Éva Hultmark, Dan Földy, Csaba Andó, István |
author_facet | Cinege, Gyöngyi Magyar, Lilla B. Kovács, Attila L. Lerner, Zita Juhász, Gábor Lukacsovich, David Winterer, Jochen Lukacsovich, Tamás Hegedűs, Zoltán Kurucz, Éva Hultmark, Dan Földy, Csaba Andó, István |
author_sort | Cinege, Gyöngyi |
collection | PubMed |
description | Multinucleated giant hemocytes (MGHs) represent a novel type of blood cell in insects that participate in a highly efficient immune response against parasitoid wasps involving isolation and killing of the parasite. Previously, we showed that circulating MGHs have high motility and the interaction with the parasitoid rapidly triggers encapsulation. However, structural and molecular mechanisms behind these processes remained elusive. Here, we used detailed ultrastructural analysis and live cell imaging of MGHs to study encapsulation in Drosophila ananassae after parasitoid wasp infection. We found dynamic structural changes, mainly driven by the formation of diverse vesicular systems and newly developed complex intracytoplasmic membrane structures, and abundant generation of giant cell exosomes in MGHs. In addition, we used RNA sequencing to study the transcriptomic profile of MGHs and activated plasmatocytes 72 h after infection, as well as the uninduced blood cells. This revealed that differentiation of MGHs was accompanied by broad changes in gene expression. Consistent with the observed structural changes, transcripts related to vesicular function, cytoskeletal organization, and adhesion were enriched in MGHs. In addition, several orphan genes encoding for hemolysin-like proteins, pore-forming toxins of prokaryotic origin, were expressed at high level, which may be important for parasitoid elimination. Our results reveal coordinated molecular and structural changes in the course of MGH differentiation and parasitoid encapsulation, providing a mechanistic model for a powerful innate immune response. |
format | Online Article Text |
id | pubmed-9275024 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | S. Karger AG |
record_format | MEDLINE/PubMed |
spelling | pubmed-92750242022-08-16 Broad Ultrastructural and Transcriptomic Changes Underlie the Multinucleated Giant Hemocyte Mediated Innate Immune Response against Parasitoids Cinege, Gyöngyi Magyar, Lilla B. Kovács, Attila L. Lerner, Zita Juhász, Gábor Lukacsovich, David Winterer, Jochen Lukacsovich, Tamás Hegedűs, Zoltán Kurucz, Éva Hultmark, Dan Földy, Csaba Andó, István J Innate Immun Research Article Multinucleated giant hemocytes (MGHs) represent a novel type of blood cell in insects that participate in a highly efficient immune response against parasitoid wasps involving isolation and killing of the parasite. Previously, we showed that circulating MGHs have high motility and the interaction with the parasitoid rapidly triggers encapsulation. However, structural and molecular mechanisms behind these processes remained elusive. Here, we used detailed ultrastructural analysis and live cell imaging of MGHs to study encapsulation in Drosophila ananassae after parasitoid wasp infection. We found dynamic structural changes, mainly driven by the formation of diverse vesicular systems and newly developed complex intracytoplasmic membrane structures, and abundant generation of giant cell exosomes in MGHs. In addition, we used RNA sequencing to study the transcriptomic profile of MGHs and activated plasmatocytes 72 h after infection, as well as the uninduced blood cells. This revealed that differentiation of MGHs was accompanied by broad changes in gene expression. Consistent with the observed structural changes, transcripts related to vesicular function, cytoskeletal organization, and adhesion were enriched in MGHs. In addition, several orphan genes encoding for hemolysin-like proteins, pore-forming toxins of prokaryotic origin, were expressed at high level, which may be important for parasitoid elimination. Our results reveal coordinated molecular and structural changes in the course of MGH differentiation and parasitoid encapsulation, providing a mechanistic model for a powerful innate immune response. S. Karger AG 2021-12-03 /pmc/articles/PMC9275024/ /pubmed/34864742 http://dx.doi.org/10.1159/000520110 Text en Copyright © 2021 by The Author(s). Published by S. Karger AG, Basel https://creativecommons.org/licenses/by-nc/4.0/This article is licensed under the Creative Commons Attribution-NonCommercial 4.0 International License (CC BY-NC). Usage and distribution for commercial purposes requires written permission. Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug. Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements. |
spellingShingle | Research Article Cinege, Gyöngyi Magyar, Lilla B. Kovács, Attila L. Lerner, Zita Juhász, Gábor Lukacsovich, David Winterer, Jochen Lukacsovich, Tamás Hegedűs, Zoltán Kurucz, Éva Hultmark, Dan Földy, Csaba Andó, István Broad Ultrastructural and Transcriptomic Changes Underlie the Multinucleated Giant Hemocyte Mediated Innate Immune Response against Parasitoids |
title | Broad Ultrastructural and Transcriptomic Changes Underlie the Multinucleated Giant Hemocyte Mediated Innate Immune Response against Parasitoids |
title_full | Broad Ultrastructural and Transcriptomic Changes Underlie the Multinucleated Giant Hemocyte Mediated Innate Immune Response against Parasitoids |
title_fullStr | Broad Ultrastructural and Transcriptomic Changes Underlie the Multinucleated Giant Hemocyte Mediated Innate Immune Response against Parasitoids |
title_full_unstemmed | Broad Ultrastructural and Transcriptomic Changes Underlie the Multinucleated Giant Hemocyte Mediated Innate Immune Response against Parasitoids |
title_short | Broad Ultrastructural and Transcriptomic Changes Underlie the Multinucleated Giant Hemocyte Mediated Innate Immune Response against Parasitoids |
title_sort | broad ultrastructural and transcriptomic changes underlie the multinucleated giant hemocyte mediated innate immune response against parasitoids |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9275024/ https://www.ncbi.nlm.nih.gov/pubmed/34864742 http://dx.doi.org/10.1159/000520110 |
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