Norepinephrine-dependently released Dr fimbriae of diffusely adhering Escherichia coli strain IH11128 promotes a mitogen-activated protein kinase ERK1/2-dependent production of pro-inflammatory cytokine, IL-8 in human intestinal Caco-2/TC7 cells

Diard, Stéphane; Moal, Vanessa Liévin-Le; Toribio, Ana Luisa; Boum, Yap; Vigier, Florence; Servin, Alain L.; Bouvet, Odile

doi:10.1016/j.micinf.2009.05.010

Cited by 9 publications

(7 citation statements)

References 33 publications

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“…This is due to the differential induction of the genes draC, which encodes the usher, and draE, which encodes the major fimbrial subunit (804). Like for Afa/Dr DAF/CEACAMs DAEC apically infecting intestinal cells, the released Dr fimbriae are able to induce hDAF-dependent phosphorylation of Erk1/2 MAPK and the production of IL-8 in fully differentiated Caco-2/TC7 cells (805). It is noteworthy that non-Afa/Dr DAEC strains are also able to induce IL-8 production in fully differentiated T84 cells (806).…”

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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“…The Dr-induced activation of Src kinases could also be related to the previously observed hDAF-dependent proinflammatory responses. Indeed, the production of interleukin-8 (IL-8) and vascular endothelial growth factor has been found to be elevated in enterocyte-like cells as a result of the recognition of hDAF by Afa/Dr hDAF fimbriae and the activation of mitogen-activated protein kinases (MAPKs) (4,5,9,10,15). Moreover, hDAF is well-known to prevent complement cascade occurring at the level of the critical C3 convertase step, thus protecting cells and tissues against complement-mediated damage.…”

Section: Discussionmentioning

confidence: 99%

Role of Src Kinases in Mobilization of Glycosylphosphatidylinositol-Anchored Decay-Accelerating Factor by Dr Fimbria-Positive Adhering Bacteria

2011

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Afa/Dr fimbriae constitute the major virulence factor of diffusely adhering Escherichia coli (Afa/Dr DAEC). After recognizing membrane-bound signaling receptors, they trigger cell responses. One of these receptors is the human decay-accelerating factor (hDAF). It has previously been reported that the binding of Afa/Dr fimbriae to hDAF quickly induces recruitment of hDAF around adhering bacteria. The aim of our study is to analyze the role of Src kinases in the Dr fimbria-induced recruitment of hDAF. Using biochemical methods and confocal microscopy followed by 3-dimensional (3D) analysis, we have shown that the activation and cell membrane targeting of Src kinases are necessary for the recruitment and organization of hDAF around adhering bacteria. We identified c-Src to be the specific kinase involved in this process. Using a set of Src-green fluorescent protein mutants, we showed that the catalytic activity and the Src homology 2 (SH2) and SH3 domains of the Src kinases are necessary for Dr fimbria-induced hDAF mobilization to occur. In addition, using mutated Dr fimbriae and a set of mutated hDAFs in which each of the complement control protein (CCP) domains had successively been deleted, we found that the aspartic acids at position 54 in the Dr fimbriae and in CCP domain 4 of hDAF played pivotal roles in the mobilization of the Src kinases and hDAF, respectively.

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“…5B) (340), and phosphorylated PI3K is recruited around Dr adhesinpositive E. coli adhering to human differentiated primary bladder cells expressing hDAF and hCEACAMs (188). Triggered by the Dr and F1845 adhesins, an hDAF-dependent activation of mitogenactivated protein kinases (MAPKs), including extracellular signalregulated kinase 1/2 (Erk1/2), p38 mitogen-activated protein kinase (p38), and stress-activated protein kinase/c-Jun N-terminal kinase SAPK/JNK (JNK), occurred in enterocyte-like Caco-2 cells and colonic T84 cells (341)(342)(343)(344)(345). Src kinase and NF-B and AKT signaling pathways are hDAF-dependently activated in C1845infected T84 cells (345).…”

Section: Receptor Clustering and Cell Signalingmentioning

confidence: 99%

“…Sperandio et al (469), observing that an EHEC luxS mutant responds to a eukaryotic cell signal activating the expression of its virulence genes, have identified epinephrine as promoting a "language" by which bacteria and host cells communicate. Diard et al (343,470) have demonstrated that norepinephrine is involved in Afa/Dr DAEC pathogenesis. In the wild-type strain IH11128, the thermoregulated production of Dr adhesin, which is optimal during the logarithmic phase of anaerobic growth, has been found to be accompanied by a release of Dr fimbriae without cell lysis (470).…”

Section: Intestinal Tract Infectionmentioning

confidence: 99%

“…Norepinephrine increases the Dr adhesin release by affecting the production of the fimbrial subunits. Indeed, norepinephrine promotes the differential induction of genes draC and draE by a regulatory mechanism; i.e., the level of the draE transcript is highly increased, while expression of draC transcript is increased to a lesser extent, relative to basal expression (343). Like with the wild-type IH11128 (341), the released Dr adhesin induces the phosphorylation of Erk1/2, in turn promoting the production of IL-8 in enterocyte-like Caco-2/ TC7 cells (343).…”

Section: Intestinal Tract Infectionmentioning

confidence: 99%

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Pathogenesis of Human Diffusely Adhering Escherichia coli Expressing Afa/Dr Adhesins (Afa/Dr DAEC): Current Insights and Future Challenges

Servin

2014

Clin Microbiol Rev

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SUMMARY The pathogenicity and clinical pertinence of diffusely adhering Escherichia coli expressing the Afa/Dr adhesins (Afa/Dr DAEC) in urinary tract infections (UTIs) and pregnancy complications are well established. In contrast, the implication of intestinal Afa/Dr DAEC in diarrhea is still under debate. These strains are age dependently involved in diarrhea in children, are apparently not involved in diarrhea in adults, and can also be asymptomatic intestinal microbiota strains in children and adult. This comprehensive review analyzes the epidemiology and diagnosis and highlights recent progress which has improved the understanding of Afa/Dr DAEC pathogenesis. Here, I summarize the roles of Afa/Dr DAEC virulence factors, including Afa/Dr adhesins, flagella, Sat toxin, and pks island products, in the development of specific mechanisms of pathogenicity. In intestinal epithelial polarized cells, the Afa/Dr adhesins trigger cell membrane receptor clustering and activation of the linked cell signaling pathways, promote structural and functional cell lesions and injuries in intestinal barrier, induce proinflammatory responses, create angiogenesis, instigate epithelial-mesenchymal transition-like events, and lead to pks -dependent DNA damage. UTI-associated Afa/Dr DAEC strains, following adhesin-membrane receptor cell interactions and activation of associated lipid raft-dependent cell signaling pathways, internalize in a microtubule-dependent manner within urinary tract epithelial cells, develop a particular intracellular lifestyle, and trigger a toxin-dependent cell detachment. In response to Afa/Dr DAEC infection, the host epithelial cells generate antibacterial defense responses. Finally, I discuss a hypothetical role of intestinal Afa/Dr DAEC strains that can act as “silent pathogens” with the capacity to emerge as “pathobionts” for the development of inflammatory bowel disease and intestinal carcinogenesis.

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Norepinephrine-dependently released Dr fimbriae of diffusely adhering Escherichia coli strain IH11128 promotes a mitogen-activated protein kinase ERK1/2-dependent production of pro-inflammatory cytokine, IL-8 in human intestinal Caco-2/TC7 cells

Cited by 9 publications

References 33 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

Role of Src Kinases in Mobilization of Glycosylphosphatidylinositol-Anchored Decay-Accelerating Factor by Dr Fimbria-Positive Adhering Bacteria

Pathogenesis of Human Diffusely Adhering Escherichia coli Expressing Afa/Dr Adhesins (Afa/Dr DAEC): Current Insights and Future Challenges

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