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Celiac disease-associated Neisseria flavescens decreases mitochondrial respiration in CaCo-2 epithelial cells: Impact of Lactobacillus paracasei CBA L74 on bacterial-induced cellular imbalance.

ABSTRACT: We previously identified a Neisseria flavescens strain in the duodenum of celiac disease (CD) patients that induced immune inflammation in ex vivo duodenal mucosal explants and in CaCo-2 cells. We also found that vesicular trafficking was delayed after the CD-immunogenic P31-43 gliadin peptide-entered CaCo-2 cells and that Lactobacillus paracasei CBA L74 (L. paracasei-CBA) supernatant reduced peptide entry. In this study, we evaluated if metabolism and trafficking was altered in CD-N. flavescens-infected CaCo-2 cells and if any alteration could be mitigated by pretreating cells with L. paracasei-CBA supernatant, despite the presence of P31-43. We measured CaCo-2 bioenergetics by an extracellular flux analyser, N. flavescens and P31-43 intracellular trafficking by immunofluorescence, cellular stress by TBARS assay, and ATP by bioluminescence. We found that CD-N. flavescens colocalised more than control N. flavescens with early endocytic vesicles and more escaped autophagy thereby surviving longer in infected cells. P31-43 increased colocalisation of N. flavescens with early vesicles. Mitochondrial respiration was lower (P < .05) in CD-N. flavescens-infected cells versus not-treated CaCo-2 cells, whereas pretreatment with L. paracasei-CBA reduced CD-N. flavescens viability and improved cell bioenergetics and trafficking. In conclusion, CD-N. flavescens induces metabolic imbalance in CaCo-2 cells, and the L. paracasei-CBA probiotic could be used to correct CD-associated dysbiosis.

SUBMITTER: Labruna G

PROVIDER: S-EPMC6618323 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Celiac disease-associated Neisseria flavescens decreases mitochondrial respiration in CaCo-2 epithelial cells: Impact of Lactobacillus paracasei CBA L74 on bacterial-induced cellular imbalance.

Labruna Giuseppe G Nanayakkara Merlin M Pagliuca Chiara C Nunziato Marcella M Iaffaldano Laura L D'Argenio Valeria V Colicchio Roberta R Budelli Andrea L AL Nigro Roberto R Salvatore Paola P Barone Maria Vittoria MV Sacchetti Lucia L

Cellular microbiology 20190520 8

We previously identified a Neisseria flavescens strain in the duodenum of celiac disease (CD) patients that induced immune inflammation in ex vivo duodenal mucosal explants and in CaCo-2 cells. We also found that vesicular trafficking was delayed after the CD-immunogenic P31-43 gliadin peptide-entered CaCo-2 cells and that Lactobacillus paracasei CBA L74 (L. paracasei-CBA) supernatant reduced peptide entry. In this study, we evaluated if metabolism and trafficking was altered in CD-N. flavescens ...[more]

PMID: 31042331

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Project description:Background: Fermented foods have been proposed to prevent common infectious diseases (CIDs) in children attending day care or preschool. To investigate the efficacy of dietary supplementation with cow's skim milk fermented with the probiotic Lactobacillus paracasei CBA L74 in reducing CIDs in children attending day care or preschool. Methods: Multicenter, randomized, double-blind, placebo-controlled trial on healthy children (aged 12-48 months) consuming daily 7 grams of cow's skim milk fermented with L. paracasei CBA L74 (group A), or placebo (maltodextrins group B) attending day care or preschool during the winter season. The main outcome was the proportion of children who experienced ≥1 episode of CID during a 3-month follow-up. Fecal biomarkers of innate (α- and β-defensins, cathelicidin) and acquired immunity (secretory IgA) were also monitored. Results: A total of 126 children (71 males, 56%) with a mean (SD) age of 33 (9) months completed the study, 66 in group A and 60 in group B. At intention to treat analysis, the proportion of children presenting ≥1 CID was 60% in group A vs. 83% in group B, corresponding to an absolute risk difference (ARD) of -23% (95% CI: -37% to -9%, p < 0.01). At per-protocol-analysis (PPA), the proportion of children presenting ≥1 CID was 18% in group A vs. 40% in group B, corresponding to an absolute risk difference (ARD) of -22% (95% CI: -37% to -6%, p < 0.01). PPA showed that the proportion of children presenting ≥1 acute gastroenteritis (AGE) was significantly lower in group A (18% vs. 40%, p < 0.05). The ARD for the occurrence of ≥1 AGE was -22% (95% CI: -37% to -6%, p < 0.01) in group A. Similar findings were obtained at PPA regarding the proportion of children presenting ≥1 upper respiratory tract infection (URTI), which was significantly lower in group A (51% vs. 74%, p < 0.05), corresponding to an ARD of -23% (95% CI: -40% to -7%, p < 0.01). Significant changes in innate and acquired immunity biomarkers were observed only in subjects in group A. Conclusions: Dietary supplementation with cow's skim milk fermented with L. paracasei CBA L74 is an efficient strategy in preventing CIDs in children.

Dataset Information

Celiac disease-associated Neisseria flavescens decreases mitochondrial respiration in CaCo-2 epithelial cells: Impact of Lactobacillus paracasei CBA L74 on bacterial-induced cellular imbalance.

Publications

Celiac disease-associated Neisseria flavescens decreases mitochondrial respiration in CaCo-2 epithelial cells: Impact of Lactobacillus paracasei CBA L74 on bacterial-induced cellular imbalance.

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