Transcriptome responses of intestinal epithelial cells induced by membrane vesicles of Listeriamonocytogenes

•We report the transcriptome profiling of Caco-2 cells upon interaction with membrane vesicles of L. monocytogenes.•Exposure of MVs to intestinal epithelial cells extensively altered the host transcriptome.•Pathway analysis confirming that MVs appears as principally responsible for the induction of...

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Published inCurrent research in microbial sciences Vol. 4
Main Authors Karthikeyan, Raman, Gayathri, Pratapa, Ramasamy, Subbiah, Suvekbala, Vemparthan, Jagannadham, Medicharla V., Rajendhran, Jeyaprakash
Format Journal Article
LanguageEnglish
Published Elsevier B.V 06.03.2023
Elsevier
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ISSN2666-5174
2666-5174
DOI10.1016/j.crmicr.2023.100185

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Abstract •We report the transcriptome profiling of Caco-2 cells upon interaction with membrane vesicles of L. monocytogenes.•Exposure of MVs to intestinal epithelial cells extensively altered the host transcriptome.•Pathway analysis confirming that MVs appears as principally responsible for the induction of immune signaling pathways.•We identified several non-coding RNAs (ncRNAs), possibly involved in the regulation of early manipulation of the host gene expression, essential for the persistence of L. monocytogenes.•The findings have opened the way for more detailed studies on the roles of membrane vesicles in the host-pathogen interaction during L. monocytogenes infection. Membrane vesicles (MVs) serve as an essential virulence factor in several pathogenic bacteria. The release of MVs by Listeria monocytogenes is only recently recognized; still, the enigmatic role of MVs in pathogenesis is yet to be established. We report the transcriptome response of Caco-2 cells upon exposure to MVs and the L. monocytogenes that leads to observe the up-regulation of autophagy-related genes in the early phase of exposure to MVs. Transcription of inflammatory cytokines is to the peak at the fourth hour of exposure. An array of differentially expressed genes was associated with actin cytoskeleton rearrangement, autophagy, cell cycle arrest, and induction of oxidative stress. At a later time point, transcriptional programs are generated upon interaction with MVs to evade innate immune signals, by modulating the expression of anti-inflammatory genes. KEGG pathway analysis is palpably confirming that MVs appear principally responsible for the induction of immune signaling pathways. Besides, MVs induced the expression of cell cycle regulatory genes, likely responsible for the ability to prolong host cell survival, thus protecting the replicative niche for L. monocytogenes. Notably, we identified several non-coding RNAs (ncRNAs), possibly involved in the regulation of early manipulation of the host gene expression, essential for the persistence of L. monocytogenes. [Display omitted]
AbstractList • We report the transcriptome profiling of Caco-2 cells upon interaction with membrane vesicles of L. monocytogenes . • Exposure of MVs to intestinal epithelial cells extensively altered the host transcriptome. • Pathway analysis confirming that MVs appears as principally responsible for the induction of immune signaling pathways. • We identified several non-coding RNAs (ncRNAs), possibly involved in the regulation of early manipulation of the host gene expression, essential for the persistence of L. monocytogenes . • The findings have opened the way for more detailed studies on the roles of membrane vesicles in the host-pathogen interaction during L. monocytogenes infection. Membrane vesicles (MVs) serve as an essential virulence factor in several pathogenic bacteria. The release of MVs by Listeria monocytogenes is only recently recognized; still, the enigmatic role of MVs in pathogenesis is yet to be established. We report the transcriptome response of Caco-2 cells upon exposure to MVs and the L. monocytogenes that leads to observe the up-regulation of autophagy-related genes in the early phase of exposure to MVs. Transcription of inflammatory cytokines is to the peak at the fourth hour of exposure. An array of differentially expressed genes was associated with actin cytoskeleton rearrangement, autophagy, cell cycle arrest, and induction of oxidative stress. At a later time point, transcriptional programs are generated upon interaction with MVs to evade innate immune signals, by modulating the expression of anti-inflammatory genes. KEGG pathway analysis is palpably confirming that MVs appear principally responsible for the induction of immune signaling pathways. Besides, MVs induced the expression of cell cycle regulatory genes, likely responsible for the ability to prolong host cell survival, thus protecting the replicative niche for L. monocytogenes . Notably, we identified several non-coding RNAs (ncRNAs), possibly involved in the regulation of early manipulation of the host gene expression, essential for the persistence of L. monocytogenes . Image, graphical abstract
•We report the transcriptome profiling of Caco-2 cells upon interaction with membrane vesicles of L. monocytogenes.•Exposure of MVs to intestinal epithelial cells extensively altered the host transcriptome.•Pathway analysis confirming that MVs appears as principally responsible for the induction of immune signaling pathways.•We identified several non-coding RNAs (ncRNAs), possibly involved in the regulation of early manipulation of the host gene expression, essential for the persistence of L. monocytogenes.•The findings have opened the way for more detailed studies on the roles of membrane vesicles in the host-pathogen interaction during L. monocytogenes infection. Membrane vesicles (MVs) serve as an essential virulence factor in several pathogenic bacteria. The release of MVs by Listeria monocytogenes is only recently recognized; still, the enigmatic role of MVs in pathogenesis is yet to be established. We report the transcriptome response of Caco-2 cells upon exposure to MVs and the L. monocytogenes that leads to observe the up-regulation of autophagy-related genes in the early phase of exposure to MVs. Transcription of inflammatory cytokines is to the peak at the fourth hour of exposure. An array of differentially expressed genes was associated with actin cytoskeleton rearrangement, autophagy, cell cycle arrest, and induction of oxidative stress. At a later time point, transcriptional programs are generated upon interaction with MVs to evade innate immune signals, by modulating the expression of anti-inflammatory genes. KEGG pathway analysis is palpably confirming that MVs appear principally responsible for the induction of immune signaling pathways. Besides, MVs induced the expression of cell cycle regulatory genes, likely responsible for the ability to prolong host cell survival, thus protecting the replicative niche for L. monocytogenes. Notably, we identified several non-coding RNAs (ncRNAs), possibly involved in the regulation of early manipulation of the host gene expression, essential for the persistence of L. monocytogenes. [Display omitted]
ArticleNumber 100185
Author Rajendhran, Jeyaprakash
Ramasamy, Subbiah
Jagannadham, Medicharla V.
Suvekbala, Vemparthan
Karthikeyan, Raman
Gayathri, Pratapa
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2023 The Authors. Published by Elsevier B.V. 2023
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Keywords Signaling pathways
Listeria monocytogenes
Membrane vesicles
Caco-2 cells
RNA-seq
Language English
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This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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Snippet •We report the transcriptome profiling of Caco-2 cells upon interaction with membrane vesicles of L. monocytogenes.•Exposure of MVs to intestinal epithelial...
• We report the transcriptome profiling of Caco-2 cells upon interaction with membrane vesicles of L. monocytogenes . • Exposure of MVs to intestinal...
SourceID pubmedcentral
elsevier
SourceType Open Access Repository
Publisher
SubjectTerms Caco-2 cells
Listeria monocytogenes
Membrane vesicles
Research Paper
RNA-seq
Signaling pathways
Title Transcriptome responses of intestinal epithelial cells induced by membrane vesicles of Listeriamonocytogenes
URI https://dx.doi.org/10.1016/j.crmicr.2023.100185
https://pubmed.ncbi.nlm.nih.gov/PMC10023947
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