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Cited by 292Probiotics and Fermented FoodsLiver Disease Diagnosis and TreatmentGut microbiota and health

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Lactobacillus rhamnosus GG Protects against Non-Alcoholic Fatty Liver Disease in Mice

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Ritze, Yvonne, Bárdos, Gyöngyi, Claus, Anke, Ehrmann, Veronika, Bergheim, Ina, Schwiertz, Andreas, Bischoff, Stephan C.·2014·PLoS ONE
DOI 10.1371/journal.pone.0080169PMC PMC3903470
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Abstract

OBJECTIVE: Experimental evidence revealed that obesity-associated non-alcoholic fatty liver disease (NAFLD) is linked to changes in intestinal permeability and translocation of bacterial products to the liver. Hitherto, no reliable therapy is available except for weight reduction. Within this study, we examined the possible effect of the probiotic bacterial strain Lactobacillus rhamnosus GG (LGG) as protective agent against experimental NAFLD in a mouse model. METHODS: Experimental NAFLD was induced by a high-fructose diet over eight weeks in C57BL/J6 mice. Fructose was administered via the drinking water containing 30% fructose with or without LGG at a concentration resulting in approximately 5×10(7) colony forming units/g body weight. Mice were examined for changes in small intestinal microbiota, gut barrier function, lipopolysaccharide (LPS) concentrations in the portal vein, liver inflammation and fat accumulation in the liver. RESULTS: LGG increased beneficial bacteria in the distal small intestine. Moreover, LGG reduced duodenal IκB protein levels and restored the duodenal tight junction protein concentration. Portal LPS (P≤0.05) was reduced and tended to attenuate TNF-α, IL-8R and IL-1β mRNA expression in the liver feeding a high-fructose diet supplemented with LGG. Furthermore liver fat accumulation and portal alanine-aminotransferase concentrations (P≤0.05) were attenuated in mice fed the high-fructose diet and LGG. CONCLUSIONS: We show for the first time that LGG protects mice from NAFLD induced by a high-fructose diet. The underlying mechanisms of protection likely involve an increase of beneficial bacteria, restoration of gut barrier function and subsequent attenuation of liver inflammation and steatosis.

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Figure 1 Lactobacillus rhamnosus GG ameliorates fructose-induced hepatic fatty acid accumulation. Representative Oil-Red-O (A) and hematoxilin & eosin (B) stainings showing fat accumulation in the liver. Abbreviations: C, control diet; F, high-fructose diet; CLGG, control diet with Lactobacillus rhamnosus GG (LGG) supplementation; FLGG, F with LGG supplementation.
Figure 1 Lactobacillus rhamnosus GG ameliorates fructose-induced hepatic fatty acid accumulation. Representative Oil-Red-O (A) and hematoxilin & eosin (B) stainings showing fat accumulation in the liver. Abbreviations: C, control diet; F, high-fructose diet; CLGG, control diet with Lactobacillus rhamnosus GG (LGG) supplementation; FLGG, F with LGG supplementation.CC BY · PubMed Central
Figure 2 Lactobacillus rhamnosus GG modulates fructose-induced hepatic fatty acid metabolism. Hepatic ChREBP (A), ACC1 (B) and FAS (C) mRNA expression was measured. Concentrations of triglycerides in the liver were analysed (D). Data are shown as means ± SEM (**P<0.01; ***P<0.001; n = 4–6). Abbreviations: see Figure 1; ChREBP, carbohydrate response element-binding protein; ACC1, acetyl-CoA carboxylase 1; FAS, fatty acid synthase.
Figure 2 Lactobacillus rhamnosus GG modulates fructose-induced hepatic fatty acid metabolism. Hepatic ChREBP (A), ACC1 (B) and FAS (C) mRNA expression was measured. Concentrations of triglycerides in the liver were analysed (D). Data are shown as means ± SEM (**P<0.01; ***P<0.001; n = 4–6). Abbreviations: see Figure 1; ChREBP, carbohydrate response element-binding protein; ACC1, acetyl-CoA carboxylase 1; FAS, fatty acid synthase.CC BY · PubMed Central
Figure 3 Lactobacillus rhamnosus GG ameliorates fructose-induced liver inflammation. Hepatic TNF-α (A), IL-1β (B) and IL-8R (C) mRNA expression was measured. Data are shown as means ± SEM (*P<0.05; n = 4–6). Abbreviations: see Figure 1; TNF-α, tumor necorsis factor alpha; IL-1β, interleukin 1 beta; IL-8R, interleukin 8 receptor.
Figure 3 Lactobacillus rhamnosus GG ameliorates fructose-induced liver inflammation. Hepatic TNF-α (A), IL-1β (B) and IL-8R (C) mRNA expression was measured. Data are shown as means ± SEM (*P<0.05; n = 4–6). Abbreviations: see Figure 1; TNF-α, tumor necorsis factor alpha; IL-1β, interleukin 1 beta; IL-8R, interleukin 8 receptor.CC BY · PubMed Central
Figure 4 Lactobacillus rhamnosus GG improves markers of intestinal barrier function. The tight junction molecules occludin (A), and claudin-1 (B), as well as the inflammatory marker pIκB kinase (C) were analysed in the proximal intestine. Representative western blots and quantitative analyses of the blots are shown (A–C). LPS in portal plasma was measured (D). Data are shown as means ± SEM (*P<0.05, **P<0.01; n = 4–6). Abbreviations: see Figure 1; LPS; lipopolysaccharides.
Figure 4 Lactobacillus rhamnosus GG improves markers of intestinal barrier function. The tight junction molecules occludin (A), and claudin-1 (B), as well as the inflammatory marker pIκB kinase (C) were analysed in the proximal intestine. Representative western blots and quantitative analyses of the blots are shown (A–C). LPS in portal plasma was measured (D). Data are shown as means ± SEM (*P<0.05, **P<0.01; n = 4–6). Abbreviations: see Figure 1; LPS; lipopolysaccharides.CC BY · PubMed Central
Figure 5 Lactobacillus rhamnosus GG elevates bacterial numbers in the distal small intestine. Total bacterial numbers (A), LGG numbers (B), the phyla Firmicutes (C), and Bacteriodetes (D) were measured via qPCR. Data are shown as means ± SEM (**P<0.01, ***P<0.001; n = 5–6). Abbreviations: see Figure 1.
Figure 5 Lactobacillus rhamnosus GG elevates bacterial numbers in the distal small intestine. Total bacterial numbers (A), LGG numbers (B), the phyla Firmicutes (C), and Bacteriodetes (D) were measured via qPCR. Data are shown as means ± SEM (**P<0.01, ***P<0.001; n = 5–6). Abbreviations: see Figure 1.CC BY · PubMed Central
Figure 6 Lactobacillus rhamnosus GG improves diet-induced NAFLD. LGG ameliorates high-fructose diet-induced NAFLD via modulation of the intestinal microbiota. LGG products e.g. lactate may increase butyrate producing Firmicutes leading to an improved intestinal barrier and reduced portal plasma LPS concentrations as well as a decreased inflammation and fatty acid accumulation in the liver. Abbreviations: NAFLD, non-alcoholic fatty liver disease; LPS, lipopolysaccharides.
Figure 6 Lactobacillus rhamnosus GG improves diet-induced NAFLD. LGG ameliorates high-fructose diet-induced NAFLD via modulation of the intestinal microbiota. LGG products e.g. lactate may increase butyrate producing Firmicutes leading to an improved intestinal barrier and reduced portal plasma LPS concentrations as well as a decreased inflammation and fatty acid accumulation in the liver. Abbreviations: NAFLD, non-alcoholic fatty liver disease; LPS, lipopolysaccharides.CC BY · PubMed Central

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Metadata

Authors
Ritze, Y., Bárdos, G., Claus, A., Ehrmann, V., Bergheim, I., Schwiertz, A., & Bischoff, S. C.
Affiliations
  • University of Hohenheim (DE)
  • Institut für Mikroökologie (DE)
Corresponding author
Bischoff, Stephan C.
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2014-01-27
Volume
9
Issue
1
Pages
e80169
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0080169
PMC
PMC3903470
OpenAlex
W2009514456
Semantic Scholar
ae2ffaa03bd783feff42333b9541e6a8e65206e6
Cited by
292
References
51
Citations by year
2026: 13 · 2025: 16 · 2024: 28 · 2023: 26 · 2022: 27 · 2021: 23 · 2020: 38 · 2019: 23 · 2018: 19 · 2017: 24 · 2016: 24 · 2015: 20 · 2014: 11
FWCI
37.75
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Danone
  • Bundesministerium für Bildung und Forschung (01GI0843, FKZ: 01GI0843)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
  • Health Sciences › Medicine › Hepatology › Liver Disease Diagnosis and Treatment
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Keywords
Lactobacillus rhamnosus GG, non-alcoholic fatty liver disease, probiotics, high-fructose diet, intestinal permeability, intestinal barrier, lipopolysaccharide, gut microbiota, liver inflammation, hepatic steatosis, tight junctions, obesity
MeSH terms
Alanine Transaminase, Analysis of Variance, Animals, Dextrans, Fatty Liver, Fructose, Humans, Immunohistochemistry, Intestine, Small, Mice, Inbred C57BL, Permeability, DNA Primers, Caco-2 Cells, Probiotics, Mice, Lacticaseibacillus rhamnosus, Real-Time Polymerase Chain Reaction, Non-alcoholic Fatty Liver Disease

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