Effects of nonpathogenic bacteria on cytokine secretion by human intestinal mucosa

Borruel, Natalia; Casellas, Francesc; Antolı́n, Maria; Llopis, Marta; Carol, Mónica; Espíin, Eloy; Naval, Javier; Guarner, Francisco; Malagelada, Juan R.

doi:10.1111/j.1572-0241.2003.07384.x

Cited by 122 publications

(26 citation statements)

References 19 publications

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“…However, in line with our results, experiments with human intestinal mucosal explants have shown that TNF, IL-8, and IL-10 are produced in response to E. coli but not in response to Lactobacillus casei (11). Furthermore, the gut mucosal DCs predominantly consist of myeloid DCs, which presumably are of monocyte origin (7).…”

Section: Discussionsupporting

confidence: 89%

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Pattern of Cytokine Responses to Gram-Positive and Gram-Negative Commensal Bacteria Is Profoundly Changed when Monocytes Differentiate into Dendritic Cells

Karlsson¹,

Larsson²,

Wold

et al. 2004

Infect Immun

119

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The normal gastrointestinal bacterial flora is crucial for the maturation of acquired immunity via effects on antigen-presenting cells (APCs). Here we investigated how two types of APCs, monocytes and dendritic cells (DCs), react to different bacterial strains typical of the commensal intestinal microflora. Purified human monocytes and monocyte-derived DCs were stimulated with UV-inactivated gram-positive (Lactobacillus plantarum and Bifidobacterium adolescentis) and gram-negative (Escherichia coli and Veillonella parvula) bacterial strains. Monocytes produced higher levels of interleukin 12p70 (IL-12p70) and tumor necrosis factor (TNF), as detected by an enzyme-linked immunosorbent assay, in response to L. plantarum than in response to E. coli and V. parvula. In contrast, DCs secreted large amounts of IL-12p70, TNF, IL-6, and IL-10 in response to E. coli and V. parvula but were practically unresponsive to L. plantarum and B. adolescentis. The lack of a response to the gram-positive strains correlated with lower surface expression of Toll-like receptor 2 (TLR2) on DCs than on monocytes. The surface expression of TLR4 on DCs was undetectable when it was analyzed by flow cytometry, but blocking this receptor decreased the TNF production in response to V. parvula, indicating that TLR4 is expressed at a low density on DCs. Gamma interferon increased the expression of TLR4 on DCs and also potentiated the cytokine response to the gram-negative strains. Our results indicate that when monocytes differentiate into DCs, their ability to respond to different commensal bacteria dramatically changes, and they become unresponsive to probiotic gram-positive bacteria. These results may have important implications for the abilities of different groups of commensal bacteria to regulate mucosal and systemic immunity.

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Section: Discussionsupporting

confidence: 89%

“…lectins (11). Nevertheless, microbes are likely to be recognized by a complex combination of receptors, which by acting together decide the outcome of the response.…”

Section: Discussionmentioning

confidence: 99%

Pattern of Cytokine Responses to Gram-Positive and Gram-Negative Commensal Bacteria Is Profoundly Changed when Monocytes Differentiate into Dendritic Cells

Karlsson¹,

Larsson²,

Wold

et al. 2004

Infect Immun

119

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show abstract

“…Decreased levels of Bifi dobacterium and Lactobacillus strains have been described in fecal samples, whereas raised counts of Enterococcus and Bacteroides species are found in infl amed mucosa of patients with IBD. High levels of infl ammatory cytokines (TNF-α and IL-1β) and IL-8 are produced by infl amed colonic mucosa of both UC and CD patients, [65][66][67][68][69] while the role of autoantibodies remains to be determined. 70 In addition, lamina propria T cells from IBD patients secrete elevated levels of IL-6, and IL-6/STAT-3 signaling is upregulated.…”

Section: Probiotics In Infl Ammatory Diseases Of the Bowelmentioning

confidence: 99%

“…[67][68][69] Downregulation of IL-6, which can exhibit antiapoptotic activity, may play a role in this process. 69 Indeed, in a mouse model of chronic colitis, treatment with neutralizing IL-6 receptor antibodies prevented macroscopic signs of infl ammation in the colon while markedly increasing the number of lamina propria CD4+ T cells undergoing apoptosis.…”

Section: Probiotics In Infl Ammatory Diseases Of the Bowelmentioning

confidence: 99%

Probiotics and immunity

et al. 2009

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Probiotics are defi ned as live microorganisms that, when administered in adequate amounts, confer a health benefi t on the host, including the gastrointestinal tract. While this benefi cial effect was originally thought to stem from improvements in the intestinal microbial balance, there is now substantial evidence that probiotics can also provide benefi ts by modulating immune functions. In animal models, probiotic supplementation is able to provide protection from spontaneous and chemically induced colitis by downregulating infl ammatory cytokines or inducing regulatory mechanisms in a strain-specifi c manner. In animal models of allergen sensitization and murine models of asthma and allergic rhinitis, orally administered probiotics can straindependently decrease allergen-specifi c IgE production, in part by modulating systemic cytokine production. Certain probiotics have been shown to decrease airway hyperresponsiveness and infl ammation by inducing regulatory mechanisms. Promising results have been obtained with probiotics in the treatment of human infl ammatory diseases of the intestine and in the prevention and treatment of atopic eczema in neonates and infants. However, the fi ndings are too variable to allow fi rm conclusions as to the effectiveness of specifi c probiotics in these conditions.

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“…A strain of Lactobacillus casei, DN-114 001, has been shown to decrease the secretion of TNF-␣ from the inflammed ileum of Crohn's disease patients (8,9). The beneficial effect of probiotics is proposed to be due, at least in part, to interference with the innate immune system and possibly the orientation of adaptive immunity.…”

mentioning

confidence: 99%

Anti-Inflammatory Effect of Lactobacillus casei on Shigella-Infected Human Intestinal Epithelial Cells

Tien

Girardin

Regnault

et al. 2006

The Journal of Immunology

277

113

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Shigella invades the human intestinal mucosa, thus causing bacillary dysentery, an acute recto-colitis responsible for lethal complications, mostly in infants and toddlers. Conversely, commensal bacteria live in a mutualistic relationship with the intestinal mucosa that is characterized by homeostatic control of innate responses, thereby contributing to tolerance to the flora. Cross-talk established between commensals and the intestinal epithelium mediate this active process, the mechanisms of which remain largely uncharacterized. Probiotics such as Lactobacillus casei belong to a subclass of these commensals that modulate mucosal innate responses and possibly display anti-inflammatory properties. We analyzed whether L. casei could attenuate the pro-inflammatory signaling induced by Shigella flexneri after invasion of the epithelial lining. Cultured epithelial cells were infected with L. casei, followed by a challenge with S. flexneri. Using macroarray DNA chips, we observed that L. casei down-regulated the transcription of a number of genes encoding pro-inflammatory effectors such as cytokines and chemokines and adherence molecules induced by invasive S. flexneri. This resulted in an anti-inflammatory effect that appeared mediated by the inhibition of the NF-κB pathway, particularly through stabilization of I-κBα. In a time-course experiment using GeneChip hybridization analysis, the expression of many genes involved in ubiquitination and proteasome processes were modulated during L. casei treatment. Thus, L. casei has developed a sophisticated means to maintain intestinal homeostasis through a process that involves manipulation of the ubiquitin/proteasome pathway upstream of I-κBα.

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Effects of nonpathogenic bacteria on cytokine secretion by human intestinal mucosa

Abstract: Nonpathogenic bacteria interact with human intestinal mucosa and can induce changes in cytokine production that are strain specific.

Cited by 122 publications

References 19 publications

Pattern of Cytokine Responses to Gram-Positive and Gram-Negative Commensal Bacteria Is Profoundly Changed when Monocytes Differentiate into Dendritic Cells

Pattern of Cytokine Responses to Gram-Positive and Gram-Negative Commensal Bacteria Is Profoundly Changed when Monocytes Differentiate into Dendritic Cells

Probiotics and immunity

Anti-Inflammatory Effect of Lactobacillus casei on Shigella-Infected Human Intestinal Epithelial Cells

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