Distinct inflammatory and cytopathic characteristics of Escherichia coli isolates from inflammatory bowel disease patients

Stina Rikke Jensen, Hengameh Chloé Mirsepasi-Lauridsen, Anna Hammerich Thysen, Jørn Brynskov, Karen Angeliki Krogfelt, Andreas Munk Petersen, Anders Elm Pedersen, Susanne Brix

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    Abstract

    Escherichia coli (E. coli) may be implicated in the pathogenesis of inflammatory bowel disease (IBD), as implied from a higher prevalence of mucosa-associated E. coli in the gut of IBD-affected individuals. However, it is unclear whether different non-diarrheagenic E. coli spp. segregate from each other in their ability to promote intestinal inflammation. Herein we compared the inflammation-inducing properties of non-diarrheagenic LF82, 691-04A, E. coli Nissle 1917 (ECN) and eleven new intestinal isolates from different locations in five IBD patients and one healthy control. Viable E. coli were cultured with human monocyte-derived dendritic cells (moDCs) and monolayers of intestinal epithelial cells (IECs), followed by analysis of secreted cytokines, intracellular levels of reactive oxygen species and cellular death. The IBD-associated E. coli LF82 induced the same dose-dependent inflammatory cytokine profile as ECN and ten of the new E. coli isolates displayed as high level IL-12p70, IL-1β, IL-23 and TNF-α from moDCs irrespective of their site of isolation (ileum/colon/faeces), disease origin (diseased/non-diseased) or known virulence factors. Contrarily, 691-04A and one new IBD E. coli isolate induced a different cellular phenotype with enhanced killing of moDCs and IECs, coupled to elevated IL-18. The cytopathic nature of 691-04A and one other IBD E. coli isolate suggests that colonization with specific non-diarrheagenic E. coli could promote intestinal barrier leakage and profound intestinal inflammation, while LF82, ECN and the remaining non-diarrheagenic E. coli isolates hold notorious pro-inflammatory characteristics that can progress inflammation in case of intestinal barrier leakage.
    Original languageEnglish
    JournalInternational Journal of Medical Microbiology
    Volume305
    Issue number8
    Pages (from-to)925-936
    Number of pages12
    ISSN1438-4221
    DOIs
    Publication statusPublished - 2015

    Keywords

    • Cell death
    • Cytokine profile
    • Dendritic cells
    • IBD-associated E. coli
    • Inflammation

    Cite this

    Jensen, Stina Rikke ; Mirsepasi-Lauridsen, Hengameh Chloé ; Thysen, Anna Hammerich ; Brynskov, Jørn ; Krogfelt, Karen Angeliki ; Petersen, Andreas Munk ; Pedersen, Anders Elm ; Brix, Susanne . / Distinct inflammatory and cytopathic characteristics of Escherichia coli isolates from inflammatory bowel disease patients. In: International Journal of Medical Microbiology. 2015 ; Vol. 305, No. 8. pp. 925-936.
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    abstract = "Escherichia coli (E. coli) may be implicated in the pathogenesis of inflammatory bowel disease (IBD), as implied from a higher prevalence of mucosa-associated E. coli in the gut of IBD-affected individuals. However, it is unclear whether different non-diarrheagenic E. coli spp. segregate from each other in their ability to promote intestinal inflammation. Herein we compared the inflammation-inducing properties of non-diarrheagenic LF82, 691-04A, E. coli Nissle 1917 (ECN) and eleven new intestinal isolates from different locations in five IBD patients and one healthy control. Viable E. coli were cultured with human monocyte-derived dendritic cells (moDCs) and monolayers of intestinal epithelial cells (IECs), followed by analysis of secreted cytokines, intracellular levels of reactive oxygen species and cellular death. The IBD-associated E. coli LF82 induced the same dose-dependent inflammatory cytokine profile as ECN and ten of the new E. coli isolates displayed as high level IL-12p70, IL-1β, IL-23 and TNF-α from moDCs irrespective of their site of isolation (ileum/colon/faeces), disease origin (diseased/non-diseased) or known virulence factors. Contrarily, 691-04A and one new IBD E. coli isolate induced a different cellular phenotype with enhanced killing of moDCs and IECs, coupled to elevated IL-18. The cytopathic nature of 691-04A and one other IBD E. coli isolate suggests that colonization with specific non-diarrheagenic E. coli could promote intestinal barrier leakage and profound intestinal inflammation, while LF82, ECN and the remaining non-diarrheagenic E. coli isolates hold notorious pro-inflammatory characteristics that can progress inflammation in case of intestinal barrier leakage.",
    keywords = "Cell death, Cytokine profile, Dendritic cells, IBD-associated E. coli, Inflammation",
    author = "Jensen, {Stina Rikke} and Mirsepasi-Lauridsen, {Hengameh Chlo{\'e}} and Thysen, {Anna Hammerich} and J{\o}rn Brynskov and Krogfelt, {Karen Angeliki} and Petersen, {Andreas Munk} and Pedersen, {Anders Elm} and Susanne Brix",
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    Distinct inflammatory and cytopathic characteristics of Escherichia coli isolates from inflammatory bowel disease patients. / Jensen, Stina Rikke; Mirsepasi-Lauridsen, Hengameh Chloé; Thysen, Anna Hammerich; Brynskov, Jørn; Krogfelt, Karen Angeliki; Petersen, Andreas Munk; Pedersen, Anders Elm; Brix, Susanne .

    In: International Journal of Medical Microbiology, Vol. 305, No. 8, 2015, p. 925-936.

    Research output: Contribution to journalJournal articleResearchpeer-review

    TY - JOUR

    T1 - Distinct inflammatory and cytopathic characteristics of Escherichia coli isolates from inflammatory bowel disease patients

    AU - Jensen, Stina Rikke

    AU - Mirsepasi-Lauridsen, Hengameh Chloé

    AU - Thysen, Anna Hammerich

    AU - Brynskov, Jørn

    AU - Krogfelt, Karen Angeliki

    AU - Petersen, Andreas Munk

    AU - Pedersen, Anders Elm

    AU - Brix, Susanne

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    AB - Escherichia coli (E. coli) may be implicated in the pathogenesis of inflammatory bowel disease (IBD), as implied from a higher prevalence of mucosa-associated E. coli in the gut of IBD-affected individuals. However, it is unclear whether different non-diarrheagenic E. coli spp. segregate from each other in their ability to promote intestinal inflammation. Herein we compared the inflammation-inducing properties of non-diarrheagenic LF82, 691-04A, E. coli Nissle 1917 (ECN) and eleven new intestinal isolates from different locations in five IBD patients and one healthy control. Viable E. coli were cultured with human monocyte-derived dendritic cells (moDCs) and monolayers of intestinal epithelial cells (IECs), followed by analysis of secreted cytokines, intracellular levels of reactive oxygen species and cellular death. The IBD-associated E. coli LF82 induced the same dose-dependent inflammatory cytokine profile as ECN and ten of the new E. coli isolates displayed as high level IL-12p70, IL-1β, IL-23 and TNF-α from moDCs irrespective of their site of isolation (ileum/colon/faeces), disease origin (diseased/non-diseased) or known virulence factors. Contrarily, 691-04A and one new IBD E. coli isolate induced a different cellular phenotype with enhanced killing of moDCs and IECs, coupled to elevated IL-18. The cytopathic nature of 691-04A and one other IBD E. coli isolate suggests that colonization with specific non-diarrheagenic E. coli could promote intestinal barrier leakage and profound intestinal inflammation, while LF82, ECN and the remaining non-diarrheagenic E. coli isolates hold notorious pro-inflammatory characteristics that can progress inflammation in case of intestinal barrier leakage.

    KW - Cell death

    KW - Cytokine profile

    KW - Dendritic cells

    KW - IBD-associated E. coli

    KW - Inflammation

    U2 - 10.1016/j.ijmm.2015.10.002

    DO - 10.1016/j.ijmm.2015.10.002

    M3 - Journal article

    VL - 305

    SP - 925

    EP - 936

    JO - International Journal of Medical Microbiology

    JF - International Journal of Medical Microbiology

    SN - 1438-4221

    IS - 8

    ER -