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Oral immune priming with Bacillus thuringiensis induces a shift in the gene expression of Tribolium castaneum larvae

BACKGROUND: The phenomenon of immune priming, i.e. enhanced protection following a secondary exposure to a pathogen, has now been demonstrated in a wide range of invertebrate species. Despite accumulating phenotypic evidence, knowledge of its mechanistic underpinnings is currently very limited. Here...

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Autores principales: Greenwood, Jenny M., Milutinović, Barbara, Peuß, Robert, Behrens, Sarah, Esser, Daniela, Rosenstiel, Philip, Schulenburg, Hinrich, Kurtz, Joachim
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5405463/
https://www.ncbi.nlm.nih.gov/pubmed/28446171
http://dx.doi.org/10.1186/s12864-017-3705-7
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author Greenwood, Jenny M.
Milutinović, Barbara
Peuß, Robert
Behrens, Sarah
Esser, Daniela
Rosenstiel, Philip
Schulenburg, Hinrich
Kurtz, Joachim
author_facet Greenwood, Jenny M.
Milutinović, Barbara
Peuß, Robert
Behrens, Sarah
Esser, Daniela
Rosenstiel, Philip
Schulenburg, Hinrich
Kurtz, Joachim
author_sort Greenwood, Jenny M.
collection PubMed
description BACKGROUND: The phenomenon of immune priming, i.e. enhanced protection following a secondary exposure to a pathogen, has now been demonstrated in a wide range of invertebrate species. Despite accumulating phenotypic evidence, knowledge of its mechanistic underpinnings is currently very limited. Here we used the system of the red flour beetle, Tribolium castaneum and the insect pathogen Bacillus thuringiensis (Bt) to further our molecular understanding of the oral immune priming phenomenon. We addressed how ingestion of bacterial cues (derived from spore supernatants) of an orally pathogenic and non-pathogenic Bt strain affects gene expression upon later challenge exposure, using a whole-transcriptome sequencing approach. RESULTS: Whereas gene expression of individuals primed with the orally non-pathogenic strain showed minor changes to controls, we found that priming with the pathogenic strain induced regulation of a large set of distinct genes, many of which are known immune candidates. Intriguingly, the immune repertoire activated upon priming and subsequent challenge qualitatively differed from the one mounted upon infection with Bt without previous priming. Moreover, a large subset of priming-specific genes showed an inverse regulation compared to their regulation upon challenge only. CONCLUSIONS: Our data demonstrate that gene expression upon infection is strongly affected by previous immune priming. We hypothesise that this shift in gene expression indicates activation of a more targeted and efficient response towards a previously encountered pathogen, in anticipation of potential secondary encounter. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-017-3705-7) contains supplementary material, which is available to authorized users.
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spelling pubmed-54054632017-04-27 Oral immune priming with Bacillus thuringiensis induces a shift in the gene expression of Tribolium castaneum larvae Greenwood, Jenny M. Milutinović, Barbara Peuß, Robert Behrens, Sarah Esser, Daniela Rosenstiel, Philip Schulenburg, Hinrich Kurtz, Joachim BMC Genomics Research Article BACKGROUND: The phenomenon of immune priming, i.e. enhanced protection following a secondary exposure to a pathogen, has now been demonstrated in a wide range of invertebrate species. Despite accumulating phenotypic evidence, knowledge of its mechanistic underpinnings is currently very limited. Here we used the system of the red flour beetle, Tribolium castaneum and the insect pathogen Bacillus thuringiensis (Bt) to further our molecular understanding of the oral immune priming phenomenon. We addressed how ingestion of bacterial cues (derived from spore supernatants) of an orally pathogenic and non-pathogenic Bt strain affects gene expression upon later challenge exposure, using a whole-transcriptome sequencing approach. RESULTS: Whereas gene expression of individuals primed with the orally non-pathogenic strain showed minor changes to controls, we found that priming with the pathogenic strain induced regulation of a large set of distinct genes, many of which are known immune candidates. Intriguingly, the immune repertoire activated upon priming and subsequent challenge qualitatively differed from the one mounted upon infection with Bt without previous priming. Moreover, a large subset of priming-specific genes showed an inverse regulation compared to their regulation upon challenge only. CONCLUSIONS: Our data demonstrate that gene expression upon infection is strongly affected by previous immune priming. We hypothesise that this shift in gene expression indicates activation of a more targeted and efficient response towards a previously encountered pathogen, in anticipation of potential secondary encounter. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-017-3705-7) contains supplementary material, which is available to authorized users. BioMed Central 2017-04-26 /pmc/articles/PMC5405463/ /pubmed/28446171 http://dx.doi.org/10.1186/s12864-017-3705-7 Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Greenwood, Jenny M.
Milutinović, Barbara
Peuß, Robert
Behrens, Sarah
Esser, Daniela
Rosenstiel, Philip
Schulenburg, Hinrich
Kurtz, Joachim
Oral immune priming with Bacillus thuringiensis induces a shift in the gene expression of Tribolium castaneum larvae
title Oral immune priming with Bacillus thuringiensis induces a shift in the gene expression of Tribolium castaneum larvae
title_full Oral immune priming with Bacillus thuringiensis induces a shift in the gene expression of Tribolium castaneum larvae
title_fullStr Oral immune priming with Bacillus thuringiensis induces a shift in the gene expression of Tribolium castaneum larvae
title_full_unstemmed Oral immune priming with Bacillus thuringiensis induces a shift in the gene expression of Tribolium castaneum larvae
title_short Oral immune priming with Bacillus thuringiensis induces a shift in the gene expression of Tribolium castaneum larvae
title_sort oral immune priming with bacillus thuringiensis induces a shift in the gene expression of tribolium castaneum larvae
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5405463/
https://www.ncbi.nlm.nih.gov/pubmed/28446171
http://dx.doi.org/10.1186/s12864-017-3705-7
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