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Drosophila immune priming to Enterococcus faecalis relies on immune tolerance rather than resistance

Innate immune priming increases an organism’s survival of a second infection after an initial, non-lethal infection. We used Drosophila melanogaster and an insect-derived strain of Enterococcus faecalis to study transcriptional control of priming. In contrast to other pathogens, the enhanced surviva...

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Autores principales: Cabrera, Kevin, Hoard, Duncan S., Gibson, Olivia, Martinez, Daniel I., Wunderlich, Zeba
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10446173/
https://www.ncbi.nlm.nih.gov/pubmed/37566589
http://dx.doi.org/10.1371/journal.ppat.1011567
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author Cabrera, Kevin
Hoard, Duncan S.
Gibson, Olivia
Martinez, Daniel I.
Wunderlich, Zeba
author_facet Cabrera, Kevin
Hoard, Duncan S.
Gibson, Olivia
Martinez, Daniel I.
Wunderlich, Zeba
author_sort Cabrera, Kevin
collection PubMed
description Innate immune priming increases an organism’s survival of a second infection after an initial, non-lethal infection. We used Drosophila melanogaster and an insect-derived strain of Enterococcus faecalis to study transcriptional control of priming. In contrast to other pathogens, the enhanced survival in primed animals does not correlate with decreased E. faecalis load. Further analysis shows that primed organisms tolerate, rather than resist infection. Using RNA-seq of immune tissues, we found many genes were upregulated in only primed flies, suggesting a distinct transcriptional program in response to initial and secondary infections. In contrast, few genes continuously express throughout the experiment or more efficiently re-activate upon reinfection. Priming experiments in immune deficient mutants revealed Imd is largely dispensable for responding to a single infection but needed to fully prime. Together, this indicates the fly’s innate immune response is plastic—differing in immune strategy, transcriptional program, and pathway use depending on infection history.
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spelling pubmed-104461732023-08-24 Drosophila immune priming to Enterococcus faecalis relies on immune tolerance rather than resistance Cabrera, Kevin Hoard, Duncan S. Gibson, Olivia Martinez, Daniel I. Wunderlich, Zeba PLoS Pathog Research Article Innate immune priming increases an organism’s survival of a second infection after an initial, non-lethal infection. We used Drosophila melanogaster and an insect-derived strain of Enterococcus faecalis to study transcriptional control of priming. In contrast to other pathogens, the enhanced survival in primed animals does not correlate with decreased E. faecalis load. Further analysis shows that primed organisms tolerate, rather than resist infection. Using RNA-seq of immune tissues, we found many genes were upregulated in only primed flies, suggesting a distinct transcriptional program in response to initial and secondary infections. In contrast, few genes continuously express throughout the experiment or more efficiently re-activate upon reinfection. Priming experiments in immune deficient mutants revealed Imd is largely dispensable for responding to a single infection but needed to fully prime. Together, this indicates the fly’s innate immune response is plastic—differing in immune strategy, transcriptional program, and pathway use depending on infection history. Public Library of Science 2023-08-11 /pmc/articles/PMC10446173/ /pubmed/37566589 http://dx.doi.org/10.1371/journal.ppat.1011567 Text en © 2023 Cabrera et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Cabrera, Kevin
Hoard, Duncan S.
Gibson, Olivia
Martinez, Daniel I.
Wunderlich, Zeba
Drosophila immune priming to Enterococcus faecalis relies on immune tolerance rather than resistance
title Drosophila immune priming to Enterococcus faecalis relies on immune tolerance rather than resistance
title_full Drosophila immune priming to Enterococcus faecalis relies on immune tolerance rather than resistance
title_fullStr Drosophila immune priming to Enterococcus faecalis relies on immune tolerance rather than resistance
title_full_unstemmed Drosophila immune priming to Enterococcus faecalis relies on immune tolerance rather than resistance
title_short Drosophila immune priming to Enterococcus faecalis relies on immune tolerance rather than resistance
title_sort drosophila immune priming to enterococcus faecalis relies on immune tolerance rather than resistance
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10446173/
https://www.ncbi.nlm.nih.gov/pubmed/37566589
http://dx.doi.org/10.1371/journal.ppat.1011567
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