Campylobacter jejuni Outer Membrane Vesicles Play an Important Role in Bacterial Interactions with Human Intestinal Epithelial Cells

Elmi, Abdi; Watson, E.D.; Sandu, Pamela; Gundogdu, Ozan; Mills, Dominic C.; Inglis, Neil F.; Manson, Erin; Imrie, Lisa; Bajaj-Elliott, Mona; Wren, Brendan W.; Smith, David George Emslie; Dorrell, Nick

doi:10.1128/iai.00161-12

Cited by 141 publications

(198 citation statements)

References 79 publications

(91 reference statements)

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“…In fully differentiated Caco-2 and T84 cells, C. jejuni induces strong IL-8 secretion (723). C. jejuni-produced OMVs containing a large set of bacterial proteins, including CDT, exert a cytotoxic activity and induce lipid raft-dependent IL-8 production in fully differentiated T84 cells (724). Infection of fully differentiated T84 cells with C. jejuni upregulated DCs and T-cell chemokine gene transcription and secretion through the activation of NF-B signaling, but this is independent of TLR5 activation by flagellin (725).…”

Section: Host Cellular Defense Responsesmentioning

confidence: 99%

Pathogenesis of Human Enterovirulent Bacteria: Lessons from Cultured, Fully Differentiated Human Colon Cancer Cell Lines

Moal

Servin

2013

Microbiol Mol Biol Rev

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SUMMARY Hosts are protected from attack by potentially harmful enteric microorganisms, viruses, and parasites by the polarized fully differentiated epithelial cells that make up the epithelium, providing a physical and functional barrier. Enterovirulent bacteria interact with the epithelial polarized cells lining the intestinal barrier, and some invade the cells. A better understanding of the cross talk between enterovirulent bacteria and the polarized intestinal cells has resulted in the identification of essential enterovirulent bacterial structures and virulence gene products playing pivotal roles in pathogenesis. Cultured animal cell lines and cultured human nonintestinal, undifferentiated epithelial cells have been extensively used for understanding the mechanisms by which some human enterovirulent bacteria induce intestinal disorders. Human colon carcinoma cell lines which are able to express in culture the functional and structural characteristics of mature enterocytes and goblet cells have been established, mimicking structurally and functionally an intestinal epithelial barrier. Moreover, Caco-2-derived M-like cells have been established, mimicking the bacterial capture property of M cells of Peyer's patches. This review intends to analyze the cellular and molecular mechanisms of pathogenesis of human enterovirulent bacteria observed in infected cultured human colon carcinoma enterocyte-like HT-29 subpopulations, enterocyte-like Caco-2 and clone cells, the colonic T84 cell line, HT-29 mucus-secreting cell subpopulations, and Caco-2-derived M-like cells, including cell association, cell entry, intracellular lifestyle, structural lesions at the brush border, functional lesions in enterocytes and goblet cells, functional and structural lesions at the junctional domain, and host cellular defense responses.

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Section: Host Cellular Defense Responsesmentioning

confidence: 99%

Pathogenesis of Human Enterovirulent Bacteria: Lessons from Cultured, Fully Differentiated Human Colon Cancer Cell Lines

Moal

Servin

2013

Microbiol Mol Biol Rev

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“…Since HPA improves the growth of C. jejuni, we reasoned that it could be degraded by the bacterium. As Cj0511 is a protease (42) that is known to be secreted in outer membrane vesicles (OMVs) (43) and is abundant in a C. jejuni strain that colonizes chickens efficiently (44), we hypothesized that it is involved in the response to pancreatic amylase. Determination of the amount of secreted carbohydrate showed that the increased secretion seen in the WT strain in response to stimulation with HPA was absent in a cj0511 mutant (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Since Cj0511 does not appear to degrade pancreatic amylase, we conclude that it is involved at a later stage in the molecular mechanism; elucidation of its precise role requires further research. Previous studies have shown that Cj0511 is expressed in the absence of pancreatic amylase (43), suggesting that its expression is constitutive. It will be interesting in future work to see if Cj0511 levels are increased in the presence of pancreatic amylase.…”

Section: Figmentioning

confidence: 99%

“…The fact that HPA enhances the growth of C. jejuni suggested that it may be used as a nutrient source, and Cj0511, predicted to be a serine protease of the C-terminal protease (CTP) family and known to be secreted in OMVs (43), seemed a likely candidate for degrading pancreatic amylase. Our data show that a cj0511 mutant did not display the response to HPA, a phenotype that was restored in a complemented strain, confirming the role of Cj0511 specifically.…”

Section: Figmentioning

confidence: 99%

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Pancreatic Amylase Is an Environmental Signal for Regulation of Biofilm Formation and Host Interaction in Campylobacter jejuni

et al. 2015

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f Campylobacter jejuni is a commensal bacterium in the intestines of animals and birds and a major cause of food-borne gastroenteritis in humans worldwide. Here we show that exposure to pancreatic amylase leads to secretion of an ␣-dextran by C. jejuni and that a secreted protease, Cj0511, is required. Exposure of C. jejuni to pancreatic amylase promotes biofilm formation in vitro, increases interaction with human epithelial cell lines, increases virulence in the Galleria mellonella infection model, and promotes colonization of the chicken ileum. We also show that exposure to pancreatic amylase protects C. jejuni from stress conditions in vitro, suggesting that the induced ␣-dextran may be important during transmission between hosts. This is the first evidence that pancreatic amylase functions as an interkingdom signal in an enteric microorganism.

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“…After attachment, the luminal contents of the OMVs are delivered into the periplasmic space of the recipient. OMVs enter eukaryotic cells through a variety of mechanisms: direct membrane fusion (28,34,35), lipid rafts (36), receptor-mediated endocytosis (19,37), and caveolin-mediated endocytosis (38)(39)(40)(41)(42). These modes of entry potentially constrain the functions of OMVs as public goods in interdomain contexts.…”

mentioning

confidence: 99%

Spheres of Hope, Packets of Doom: the Good and Bad of Outer Membrane Vesicles in Interspecies and Ecological Dynamics

Lynch

Alegado

2017

J Bacteriol

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Outer membrane vesicles (OMVs) are proteoliposome nanoparticles ubiquitously produced by Gram-negative bacteria. Typically bearing a composition similar to those of the outer membrane and periplasm of the cells from which they are derived, OMVs package an array of proteins, lipids, and nucleic acids. Once considered inconsequential by-products of bacterial growth, OMVs have since been demonstrated to mediate cellular stress relief, promote horizontal gene transfer and antimicrobial activity, and elicit metazoan inflammation. Recently, OMVs have gained appreciation as critical moderators of interorganismal dynamics. In this review, we focus on recent progress toward understanding the functions of OMVs with regard to symbiosis and ecological contexts, and we propose potential avenues for future OMV studies.

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Campylobacter jejuni Outer Membrane Vesicles Play an Important Role in Bacterial Interactions with Human Intestinal Epithelial Cells

Cited by 141 publications

References 79 publications

Pathogenesis of Human Enterovirulent Bacteria: Lessons from Cultured, Fully Differentiated Human Colon Cancer Cell Lines

Pathogenesis of Human Enterovirulent Bacteria: Lessons from Cultured, Fully Differentiated Human Colon Cancer Cell Lines

Pancreatic Amylase Is an Environmental Signal for Regulation of Biofilm Formation and Host Interaction in Campylobacter jejuni

Spheres of Hope, Packets of Doom: the Good and Bad of Outer Membrane Vesicles in Interspecies and Ecological Dynamics

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