Yersiniabactin-Producing Adherent/Invasive Escherichia coli Promotes Inflammation-Associated Fibrosis in Gnotobiotic
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              Il10
              <sup>−/−</sup>
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            Mice

Ellermann, Melissa; Gharaibeh, Raad Z.; Fulbright, Laura E.; Dogan, Belgin; Moore, Lyndsey N; Broberg, Christopher A.; Lopez, Lacey R.; Rothemich, Aaron; Herzog, Jeremy; Rogala, Allison R.; Gordon, Ilyssa O.; Rieder, Florian; Brouwer, Cory; Simpson, Kenneth W.; Jobin, Christian; Sartor, R. Balfour; Arthur, Janelle C.

doi:10.1128/iai.00587-19

Cited by 40 publications

(60 citation statements)

References 61 publications

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“…To evaluate the utility of our nanopore pipeline for complex biological samples, we performed in vivo colonization studies using a well-established IBD mouse model [3,[10][11][30][31][32]. We first determined if these human-derived strains and murine-derived NC101 could colonize and persist in mice, in the presence of a competing microbiota.…”

Section: In Vivo Colonization Studiesmentioning

confidence: 99%

Long-read sequencing to interrogate strain-level variation among adherent-invasiveEscherichia coliisolated from human intestinal tissue

Wang

Bleich

Zarmer

et al. 2020

Preprint

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Adherent-invasive Escherichia coli (AIEC) are a pathovar linked to inflammatory bowel diseases (IBD), especially Crohn's disease, and colorectal cancer. AIEC have no known molecular or genomic markers, but instead are defined by in vitro functional attributes.Futhermore, it is unknown if strains classified as AIEC truly colonize intestinal tissues better than non-AIEC strains. To evaluate strain-level variation among tissue-associated E. coli, we must develop a sequencing approach capable of long reads and with the ability to exclude mammalian DNA. We also must evaluate genomic variation among strains that have demonstrated ability to colonize intestinal tissues. Here we have assembled complete genomes using ultra-long-read nanopore sequencing for a model AIEC strain, NC101, and seven strains isolated from the intestinal mucosa of Crohn's disease and non-Crohn's tissues. We show these strains can colonize the intestinal tissue in a Crohn's disease mouse model and induce varying levels of inflammatory cytokines from cultured macrophages. We demonstrate these strains can be quantified and distinguished in the presence of 99.5% mammalian DNA and from within a fecal population. Analysis of global genomic structure and specific sequence variation within the ribosomal RNA operon provides a framework for efficiently tracking strain-level variation of closely-related E. coli and likely other commensal/pathogenic bacteria impacting intestinal inflammation in mice and IBD patients.

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Section: In Vivo Colonization Studiesmentioning

confidence: 99%

Long-read sequencing to interrogate strain-level variation among adherent-invasiveEscherichia coliisolated from human intestinal tissue

Wang

Bleich

Zarmer

et al. 2020

Preprint

Self Cite

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“…Within the same line, applying TFF2 does reduce inflammatory indexes in a hapten colitis rodent model and has even been suggested as a therapeutic scaffold for inflammatory bowel disease treatment [28]. Importantly, TFF2 treatment reduces fibrosis (subepithelial collagen deposition) in a murine model of chronic allergic airways disease [2], which could indicate a reduced fibrogenesis in tissues undergoing inflammation [29,30]. Thus, TFF2 effects are not limited to an anti-inflammatory effect but would also reduce the tissue fibrosis.…”

mentioning

confidence: 99%

Trefoil Factor Family Member 2 (TFF2) as an Inflammatory-Induced and Anti-Inflammatory Tissue Repair Factor

Ghanemi

Yoshioka

St‐Amand

2020

Animals

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“…Most of the genes involved in Ybt biosynthesis are grouped in a gene cluster 61,62 . In addition to Yersinia species, many Enterobacteriaceae also produce Ybt, including both pathogenic and commensal E. coli 46,[63][64][65] . Ybt is well known for scavenging iron in vivo 66 , and plays a critical role in Y. pestis virulence 61 .…”

Section: Discussionmentioning

confidence: 99%

“…Ybt is well known for scavenging iron in vivo 66 , and plays a critical role in Y. pestis virulence 61 . Moreover, Ybt reduces reactive oxygen species formation in phagocytes by scavenging iron and preventing Haber-Weiss reactions 67 , as well as contributes to intestinal fibrosis 63 , indicating that Ybt modulates the host immune response. Incidentally, a product of the ybt gene cluster has been proposed to enable zinc acquisition by Y. pestis 40 , although direct binding of Ybt to zinc was not described in two independent studies 39,41 .…”

Section: Discussionmentioning

confidence: 99%

Siderophore-mediated zinc acquisition enhances enterobacterial colonization of the inflamed gut

Zhi

Behnsen

Aron

et al. 2020

Preprint

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Zinc is an essential cofactor for bacterial metabolism, and many Enterobacteriaceae express the zinc transporters ZnuABC and ZupT to acquire this metal in the host. Unexpectedly, the probiotic bacterium Escherichia coli Nissle 1917 exhibited appreciable growth in zinc-limited media even when these transporters were deleted. By utilizing in vitro and in vivo studies, as well as native spray metal infusion mass spectrometry and ion identity molecular networking, we discovered that Nissle utilizes yersiniabactin as a zincophore. Indeed, yersiniabactin enables Nissle to scavenge zinc in zinc-limited media, to resist calprotectin-mediated zinc sequestration, and to thrive in the inflamed gut. Moreover, we discovered that yersiniabactin’s affinity for iron or zinc changes in a pH-dependent manner, with higher affinity for zinc as the pH increased. Altogether, we demonstrate that siderophore metal affinity can be influenced by the local environment and reveal a mechanism of zinc acquisition available to many commensal and pathogenic Enterobacteriaceae.

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Yersiniabactin-Producing Adherent/Invasive Escherichia coli Promotes Inflammation-Associated Fibrosis in Gnotobiotic Il10 ^−/− Mice

Cited by 40 publications

References 61 publications

Long-read sequencing to interrogate strain-level variation among adherent-invasiveEscherichia coliisolated from human intestinal tissue

Long-read sequencing to interrogate strain-level variation among adherent-invasiveEscherichia coliisolated from human intestinal tissue

Trefoil Factor Family Member 2 (TFF2) as an Inflammatory-Induced and Anti-Inflammatory Tissue Repair Factor

Siderophore-mediated zinc acquisition enhances enterobacterial colonization of the inflamed gut

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Yersiniabactin-Producing Adherent/Invasive Escherichia coli Promotes Inflammation-Associated Fibrosis in Gnotobiotic Il10 −/− Mice

Cited by 40 publications

References 61 publications

Long-read sequencing to interrogate strain-level variation among adherent-invasiveEscherichia coliisolated from human intestinal tissue

Long-read sequencing to interrogate strain-level variation among adherent-invasiveEscherichia coliisolated from human intestinal tissue

Trefoil Factor Family Member 2 (TFF2) as an Inflammatory-Induced and Anti-Inflammatory Tissue Repair Factor

Siderophore-mediated zinc acquisition enhances enterobacterial colonization of the inflamed gut

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Product

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Yersiniabactin-Producing Adherent/Invasive Escherichia coli Promotes Inflammation-Associated Fibrosis in Gnotobiotic Il10 ^−/− Mice