Transcriptome responses of intestinal epithelial cells induced by membrane vesicles of Listeria monocytogenes
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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| Format: | Article |
| Language: | English |
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Elsevier
2023-01-01
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| Series: | Current Research in Microbial Sciences |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2666517423000068 |
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| author | Raman Karthikeyan Pratapa Gayathri Subbiah Ramasamy Vemparthan Suvekbala Medicharla V. Jagannadham Jeyaprakash Rajendhran |
| author_facet | Raman Karthikeyan Pratapa Gayathri Subbiah Ramasamy Vemparthan Suvekbala Medicharla V. Jagannadham Jeyaprakash Rajendhran |
| author_sort | Raman Karthikeyan |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-03-13T04:43:18Z |
| format | Article |
| id | doaj.art-4d02d007009d487cbd4cbb5cbef28056 |
| institution | Directory Open Access Journal |
| issn | 2666-5174 |
| language | English |
| last_indexed | 2024-03-13T04:43:18Z |
| publishDate | 2023-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Current Research in Microbial Sciences |
| spelling | doaj.art-4d02d007009d487cbd4cbb5cbef280562023-06-19T04:29:41ZengElsevierCurrent Research in Microbial Sciences2666-51742023-01-014100185Transcriptome responses of intestinal epithelial cells induced by membrane vesicles of Listeria monocytogenesRaman Karthikeyan0Pratapa Gayathri1Subbiah Ramasamy2Vemparthan Suvekbala3Medicharla V. Jagannadham4Jeyaprakash Rajendhran5Department of Genetics, School of Biological Sciences, Madurai Kamaraj University, Madurai, 625021, Tamil Nadu, IndiaCSIR - Centre for Cellular and Molecular Biology, Tarnaka, Hyderabad 500007, IndiaDepartment of Biochemistry, School of Biological Sciences, Madurai Kamaraj University, Madurai, 625021, Tamil Nadu, IndiaEDII-Anna Business Incubation Research Foundation, University College of Engineering, BIT Campus, Anna University, Tiruchirappalli 620024, IndiaCSIR - Centre for Cellular and Molecular Biology, Tarnaka, Hyderabad 500007, India; Corresponding authors.Department of Genetics, School of Biological Sciences, Madurai Kamaraj University, Madurai, 625021, Tamil Nadu, India; Corresponding authors.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.http://www.sciencedirect.com/science/article/pii/S2666517423000068Listeria monocytogenesMembrane vesiclesCaco-2 cellsRNA-seqSignaling pathways |
| spellingShingle | Raman Karthikeyan Pratapa Gayathri Subbiah Ramasamy Vemparthan Suvekbala Medicharla V. Jagannadham Jeyaprakash Rajendhran Transcriptome responses of intestinal epithelial cells induced by membrane vesicles of Listeria monocytogenes Current Research in Microbial Sciences Listeria monocytogenes Membrane vesicles Caco-2 cells RNA-seq Signaling pathways |
| title | Transcriptome responses of intestinal epithelial cells induced by membrane vesicles of Listeria monocytogenes |
| title_full | Transcriptome responses of intestinal epithelial cells induced by membrane vesicles of Listeria monocytogenes |
| title_fullStr | Transcriptome responses of intestinal epithelial cells induced by membrane vesicles of Listeria monocytogenes |
| title_full_unstemmed | Transcriptome responses of intestinal epithelial cells induced by membrane vesicles of Listeria monocytogenes |
| title_short | Transcriptome responses of intestinal epithelial cells induced by membrane vesicles of Listeria monocytogenes |
| title_sort | transcriptome responses of intestinal epithelial cells induced by membrane vesicles of listeria monocytogenes |
| topic | Listeria monocytogenes Membrane vesicles Caco-2 cells RNA-seq Signaling pathways |
| url | http://www.sciencedirect.com/science/article/pii/S2666517423000068 |
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