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  • Cytolethal distending toxin induces the formation of transient messenger-rich ribonucleoprotein nuclear invaginations in surviving cells

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    Author(s)
    Azzi-Martin, Lamia
    He, Wencan
    Pere-Vedrenne, Christelle
    Korolik, Victoria
    Alix, Chloe
    Prochazkova-Carlotti, Martina
    Morel, Jean-Luc
    Le Roux-Goglin, Emilie
    Lehours, Philippe
    Djavaheri-Mergny, Mojgan
    Grosset, Christophe F
    Varon, Christine
    Dubus, Pierre
    Menard, Armelle
    Griffith University Author(s)
    Korolik, Victoria
    Year published
    2019
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    Abstract
    Humans are frequently exposed to bacterial genotoxins involved in digestive cancers, colibactin and Cytolethal Distending Toxin (CDT), the latter being secreted by many pathogenic bacteria. Our aim was to evaluate the effects induced by these genotoxins on nuclear remodeling in the context of cell survival. Helicobacter infected mice, coculture experiments with CDT- and colibactin-secreting bacteria and hepatic, intestinal and gastric cells, and xenograft mouse-derived models were used to assess the nuclear remodeling in vitro and in vivo. Our results showed that CDT and colibactin induced-nuclear remodeling can be associated ...
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    Humans are frequently exposed to bacterial genotoxins involved in digestive cancers, colibactin and Cytolethal Distending Toxin (CDT), the latter being secreted by many pathogenic bacteria. Our aim was to evaluate the effects induced by these genotoxins on nuclear remodeling in the context of cell survival. Helicobacter infected mice, coculture experiments with CDT- and colibactin-secreting bacteria and hepatic, intestinal and gastric cells, and xenograft mouse-derived models were used to assess the nuclear remodeling in vitro and in vivo. Our results showed that CDT and colibactin induced-nuclear remodeling can be associated with the formation of deep cytoplasmic invaginations in the nucleus of giant cells. These structures, observed both in vivo and in vitro, correspond to nucleoplasmic reticulum (NR). The core of the NR was found to concentrate ribosomes, proteins involved in mRNA translation, polyadenylated RNA and the main components of the complex mCRD involved in mRNA turnover. These structures are active sites of mRNA translation, correlated with a high degree of ploidy, and involve MAPK and calcium signaling. Additional data show that insulation and concentration of these adaptive ribonucleoprotein particles within the nucleus are dynamic, transient and protect the cell until the genotoxic stress is relieved. Bacterial genotoxins-induced NR would be a privileged gateway for selected mRNA to be preferably transported therein for local translation. These findings offer new insights into the context of NR formation, a common feature of many cancers, which not only appears in response to therapies-induced DNA damage but also earlier in response to genotoxic bacteria.
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    Journal Title
    PLOS Pathogens
    Volume
    15
    Issue
    9
    DOI
    https://doi.org/10.1371/journal.ppat.1007921
    Copyright Statement
    © 2019 Azzi-Martin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
    Subject
    Microbiology
    Immunology
    Medical microbiology
    Science & Technology
    Life Sciences & Biomedicine
    Parasitology
    Virology
    Publication URI
    http://hdl.handle.net/10072/388943
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    • Journal articles

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