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 in | Current research in microbial sciences Vol. 4 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
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Elsevier B.V
06.03.2023
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Online Access | Get full text |
ISSN | 2666-5174 2666-5174 |
DOI | 10.1016/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.
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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 |
Author_xml | – sequence: 1 givenname: Raman surname: Karthikeyan fullname: Karthikeyan, Raman organization: Department of Genetics, School of Biological Sciences, Madurai Kamaraj University, Madurai, 625021, Tamil Nadu, India – sequence: 2 givenname: Pratapa surname: Gayathri fullname: Gayathri, Pratapa organization: CSIR - Centre for Cellular and Molecular Biology, Tarnaka, Hyderabad 500007, India – sequence: 3 givenname: Subbiah surname: Ramasamy fullname: Ramasamy, Subbiah organization: Department of Biochemistry, School of Biological Sciences, Madurai Kamaraj University, Madurai, 625021, Tamil Nadu, India – sequence: 4 givenname: Vemparthan surname: Suvekbala fullname: Suvekbala, Vemparthan organization: EDII-Anna Business Incubation Research Foundation, University College of Engineering, BIT Campus, Anna University, Tiruchirappalli 620024, India – sequence: 5 givenname: Medicharla V. orcidid: 0000-0001-9371-6275 surname: Jagannadham fullname: Jagannadham, Medicharla V. email: medicharlavj@gmail.com organization: CSIR - Centre for Cellular and Molecular Biology, Tarnaka, Hyderabad 500007, India – sequence: 6 givenname: Jeyaprakash orcidid: 0000-0002-1898-1607 surname: Rajendhran fullname: Rajendhran, Jeyaprakash email: jrajendhran@gmail.com organization: Department of Genetics, School of Biological Sciences, Madurai Kamaraj University, Madurai, 625021, Tamil Nadu, India |
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Copyright | 2023 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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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... |
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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 |
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