The gut microbiota elicits a profound metabolic reorientation in the mouse jejunal mucosa during conventionalisation

Aidy, Sahar El; Merrifield, Claire A; Derrien, Muriel; Baarlen, Peter van; Hooiveld, Guido; Levenez, Florence; Doré, Joël; Dekker, Jan; Holmes, Elaine; Claus, Sandrine P.; Reijngoud, Dirk-Jan; Kleerebezem, Michiel

doi:10.1136/gutjnl-2011-301955

Cited by 113 publications

(106 citation statements)

References 51 publications

(54 reference statements)

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“…A recent report on establishment of mouse intestinal microbiota also suggests that during the early stages of development typical pathobionts, in this case Helicobacter and Sphingomonas, are able to colonize despite activation of innate immunity. 47,48 Similar to our zebrafish data, development of adaptive immunity (from day 4-7) in these conventionalized mice coincided with decreased abundance of these pathobionts. We hypothesize that these (host-specific) pathobionts (such as Helicobacter, Sphingomonas and Vibrio spp.)…”

Section: Discussionsupporting

confidence: 85%

T lymphocytes control microbial composition by regulating the abundance of Vibrio in the zebrafish gut

et al. 2014

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Abbreviations: wpf: weeks post fertilization.Dysbiosis of the intestinal microbial community is considered a risk factor for development of chronic intestinal inflammation as well as other diseases such as diabetes, obesity and even cancer. Study of the innate and adaptive immune pathways controlling bacterial colonization has however proven difficult in rodents, considering the extensive cross-talk between bacteria and innate and adaptive immunity. Here, we used the zebrafish to study innate and adaptive immune processes controlling the microbial community. Zebrafish lack a functional adaptive immune system in the first weeks of life, enabling study of the innate immune system in the absence of adaptive immunity. We show that in wild type zebrafish, the initial lack of adaptive immunity associates with overgrowth of Vibrio species (a group encompassing fish and human pathogens), which is overcome upon adaptive immune development. In Rag1-deficient zebrafish (lacking adaptive immunity) Vibrio abundance remains high, suggesting that adaptive immune processes indeed control Vibrio species. Using cell transfer experiments, we confirm that adoptive transfer of T lymphocytes, but not B lymphocytes into Rag1-deficient recipients suppresses outgrowth of Vibrio. In addition, ex vivo exposure of intestinal T lymphocytes to Rag1-deficient microbiota results in increased interferon-gamma expression by these T lymphocytes, compared to exposure to wild type microbiota. In conclusion, we show that T lymphocytes control microbial composition by effectively suppressing the outgrowth of Vibrio species in the zebrafish intestine.

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Section: Discussionsupporting

confidence: 85%

T lymphocytes control microbial composition by regulating the abundance of Vibrio in the zebrafish gut

et al. 2014

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“…The number of GCs transiently increases in the jejunum of germfree mice conventionalized with fecal microbiota derived from conventionally raised mice (46). The number of GCs decreased in the ileum of pigs infected with F4 ϩ ETEC but not in pigs pretreated with BLS mix.…”

Section: Discussionmentioning

confidence: 98%

Oral Administration of a Select Mixture of Bacillus Probiotics Affects the Gut Microbiota and Goblet Cell Function following Escherichia coli Challenge in Newly Weaned Pigs of Genotype MUC4 That Are Supposed To Be Enterotoxigenic E. coli F4ab/ac Receptor Negative

Zhang

Zhu

Zhou

et al. 2017

Appl Environ Microbiol

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Structural disruption of the gut microbiota and impaired goblet cell function are collateral etiologic factors in enteric diseases. Low, moderate, or high doses of a Bacillus licheniformis-B. subtilis mixture (BLS mix) were orally administered to piglets of genotype MUC4 that are supposed to be F4-expressing enterotoxigenic Escherichia coli strain (F4 ϩ ETEC) F4ab/ac receptor negative (i.e., MUC4-resistant piglets) for 1 week before F4 ϩ ETEC challenge. The luminal contents were collected from the mucosa of the colon on day 8 after F4 ϩ ETEC challenge. The BLS mix attenuated E. coli-induced expansion of Bacteroides uniformis, Eubacterium eligens, Acetanaerobacterium, and Sporobacter populations. Clostridium and Turicibacter populations increased following F4 ϩ ETEC challenge in pigs pretreated with low-dose BLS mix. Lactobacillus gasseri and Lactobacillus salivarius populations increased after administration of BLS mix during E. coli infection. The beneficial effects of BLS mix were due in part to the expansion of certain Clostridium, Lactobacillus, and Turicibacter populations, with a corresponding increase in the number of goblet cells in the ileum via upregulated Atoh1 expression, in turn increasing MUC2 production and thus preserving the mucus barrier and enhancing host defenses against enteropathogenic bacteria. However, excessive BLS mix consumption may increase the risk for enteritis, partly through disruption of colonic microbial ecology, characterized by expansion of Proteobacteria and impaired goblet cell function in the ileum. Our findings suggest that oral administration of BLS mix reprograms the gut microbiota and enhances goblet cell function to ameliorate enteritis.IMPORTANCE The present study is important for improving our understanding of the protective role of probiotics against Escherichia coli infection in piglets. Structural disruption of the gut microbiota and impaired goblet cell function are collateral etiologic factors in enteric diseases. In this study, low, moderate, or high doses of a Bacillus licheniformis-B. subtilis mixture (BLS mix) were orally administered to MUC4-resistant piglets for 1 week before the F4-expressing ETEC strain (F4 ϩ ETEC) challenge. Our findings suggest that oral administration of BLS mix reprograms the gut microbiota and enhances goblet cell function to ameliorate enteritis. KEYWORDS

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“…For instance, microbial metabolites such as short-chain fatty acids (SCFA) not only are energy sources for the colonic epithelium but also affect the expression of several genes and eventually participate in hepatic de novo lipogenesis through the expression of several key enzymes, such as acetyl-coenzyme A (acetyl-CoA) carboxylase (ACC) and fatty acid synthase (FASN), and of their regulators, the carbohydrate responsive element binding protein (ChREBP) and sterol responsive element binding protein 1c (SREBP-1c) (6, 7). Importantly regarding the current work, the gut microbiota directly affects nutrients, especially fatty acids (FA), and cholesterol absorption by enterocytes (8, 9) and regulates key intestinal and metabolic functions such as insulin sensitivity, fat storage, and energy expenditure (10–12). …”

Section: Introductionmentioning

confidence: 99%

Disentangling Host-Microbiota Regulation of Lipid Secretion by Enterocytes: Insights from Commensals Lactobacillus paracasei and Escherichia coli

Tazi

Araújo

Mulet

et al. 2018

mBio

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The specific contribution of each bacterial species within a complex microbiota to the regulation of host lipid metabolism remains largely unknown. Using two model commensal microorganisms, L. paracasei and E. coli, we demonstrated that both bacterial species impacted host lipid metabolism in a diet-dependent manner and, notably, that L. paracasei-colonized mice but not E. coli-colonized mice resisted high-fat-diet-induced body weight gain. In addition, we set up cellular models of fatty acid absorption and secretion by enterocytes cocultured with bacteria and showed that, in vitro, both L. paracasei and E. coli inhibited lipid secretion, through increased intracellular fat storage and enhanced lipid catabolism, respectively.

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The gut microbiota elicits a profound metabolic reorientation in the mouse jejunal mucosa during conventionalisation

Cited by 113 publications

References 51 publications

T lymphocytes control microbial composition by regulating the abundance of Vibrio in the zebrafish gut

T lymphocytes control microbial composition by regulating the abundance of Vibrio in the zebrafish gut

Oral Administration of a Select Mixture of Bacillus Probiotics Affects the Gut Microbiota and Goblet Cell Function following Escherichia coli Challenge in Newly Weaned Pigs of Genotype MUC4 That Are Supposed To Be Enterotoxigenic E. coli F4ab/ac Receptor Negative

Disentangling Host-Microbiota Regulation of Lipid Secretion by Enterocytes: Insights from Commensals Lactobacillus paracasei and Escherichia coli

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