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

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 upo...

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Autores principales: Karthikeyan, Raman, Gayathri, Pratapa, Ramasamy, Subbiah, Suvekbala, Vemparthan, Jagannadham, Medicharla V., Rajendhran, Jeyaprakash
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10023947/
https://www.ncbi.nlm.nih.gov/pubmed/36942003
http://dx.doi.org/10.1016/j.crmicr.2023.100185
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author Karthikeyan, Raman
Gayathri, Pratapa
Ramasamy, Subbiah
Suvekbala, Vemparthan
Jagannadham, Medicharla V.
Rajendhran, Jeyaprakash
author_facet Karthikeyan, Raman
Gayathri, Pratapa
Ramasamy, Subbiah
Suvekbala, Vemparthan
Jagannadham, Medicharla V.
Rajendhran, Jeyaprakash
author_sort Karthikeyan, Raman
collection PubMed
description 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.
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spelling pubmed-100239472023-03-19 Transcriptome responses of intestinal epithelial cells induced by membrane vesicles of Listeriamonocytogenes Karthikeyan, Raman Gayathri, Pratapa Ramasamy, Subbiah Suvekbala, Vemparthan Jagannadham, Medicharla V. Rajendhran, Jeyaprakash Curr Res Microb Sci Research Paper 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. Elsevier 2023-03-06 /pmc/articles/PMC10023947/ /pubmed/36942003 http://dx.doi.org/10.1016/j.crmicr.2023.100185 Text en © 2023 The Authors. Published by Elsevier B.V. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Research Paper
Karthikeyan, Raman
Gayathri, Pratapa
Ramasamy, Subbiah
Suvekbala, Vemparthan
Jagannadham, Medicharla V.
Rajendhran, Jeyaprakash
Transcriptome responses of intestinal epithelial cells induced by membrane vesicles of Listeriamonocytogenes
title Transcriptome responses of intestinal epithelial cells induced by membrane vesicles of Listeriamonocytogenes
title_full Transcriptome responses of intestinal epithelial cells induced by membrane vesicles of Listeriamonocytogenes
title_fullStr Transcriptome responses of intestinal epithelial cells induced by membrane vesicles of Listeriamonocytogenes
title_full_unstemmed Transcriptome responses of intestinal epithelial cells induced by membrane vesicles of Listeriamonocytogenes
title_short Transcriptome responses of intestinal epithelial cells induced by membrane vesicles of Listeriamonocytogenes
title_sort transcriptome responses of intestinal epithelial cells induced by membrane vesicles of listeriamonocytogenes
topic Research Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10023947/
https://www.ncbi.nlm.nih.gov/pubmed/36942003
http://dx.doi.org/10.1016/j.crmicr.2023.100185
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