Diet Rich in Simple Sugars Promotes Pro-Inflammatory Response via Gut Microbiota Alteration and TLR4 Signaling
Diet is a strong modifier of microbiome and mucosal microenvironment in the gut. Recently, components of western-type diets have been associated with metabolic and immune diseases. Here, we studied how high-sugar diet (HSD) consumption influences gut mucosal barrier and immune response under steady...
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MDPI AG
2020-12-01
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author | Alena Fajstova Natalie Galanova Stepan Coufal Jana Malkova Martin Kostovcik Martina Cermakova Helena Pelantova Marek Kuzma Blanka Sediva Tomas Hudcovic Tomas Hrncir Helena Tlaskalova-Hogenova Miloslav Kverka Klara Kostovcikova |
author_facet | Alena Fajstova Natalie Galanova Stepan Coufal Jana Malkova Martin Kostovcik Martina Cermakova Helena Pelantova Marek Kuzma Blanka Sediva Tomas Hudcovic Tomas Hrncir Helena Tlaskalova-Hogenova Miloslav Kverka Klara Kostovcikova |
author_sort | Alena Fajstova |
collection | DOAJ |
description | Diet is a strong modifier of microbiome and mucosal microenvironment in the gut. Recently, components of western-type diets have been associated with metabolic and immune diseases. Here, we studied how high-sugar diet (HSD) consumption influences gut mucosal barrier and immune response under steady state conditions and in a mouse model of acute colitis. We found that HSD significantly increased gut permeability, spleen weight, and neutrophil levels in spleens of healthy mice. Subsequent dextran sodium sulfate administration led to severe colitis. In colon, HSD significantly promoted neutrophil infiltration and increased the levels of IL-6, IL-1β, and TNF-α. Moreover, HSD-fed mice had significantly higher abundance of pathobionts, such as <i>Escherichia coli</i> and <i>Candida</i>, in fecal samples. Although germ-free mice colonized with microbiota of conventionally reared mice that consumed different diets had equally severe colitis, mice colonized with HSD microbiota showed markedly increased infiltration of neutrophils to the gut. The induction of colitis in Toll-like receptor 4 (TLR4)-deficient HSD-fed mice led to significantly milder colitis than in wild-type mice. In conclusion, our results suggested a significant role of HSD in disruption of barrier integrity and balanced mucosal and systemic immune response. In addition, these processes seemed to be highly influenced by resident potentially pathogenic microbiota or metabolites via the TLR4 signaling pathway. |
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spelling | doaj.art-d6d869a8acf44e63969a0c1c9b7b2e8e2023-11-21T01:06:05ZengMDPI AGCells2073-44092020-12-01912270110.3390/cells9122701Diet Rich in Simple Sugars Promotes Pro-Inflammatory Response via Gut Microbiota Alteration and TLR4 SignalingAlena Fajstova0Natalie Galanova1Stepan Coufal2Jana Malkova3Martin Kostovcik4Martina Cermakova5Helena Pelantova6Marek Kuzma7Blanka Sediva8Tomas Hudcovic9Tomas Hrncir10Helena Tlaskalova-Hogenova11Miloslav Kverka12Klara Kostovcikova13Laboratory of Cellular and Molecular Immunology, Institute of Microbiology of the Czech Academy of Sciences, Videnska 1083, 142 20 Prague, Czech RepublicLaboratory of Cellular and Molecular Immunology, Institute of Microbiology of the Czech Academy of Sciences, Videnska 1083, 142 20 Prague, Czech RepublicLaboratory of Cellular and Molecular Immunology, Institute of Microbiology of the Czech Academy of Sciences, Videnska 1083, 142 20 Prague, Czech RepublicLaboratory of Cellular and Molecular Immunology, Institute of Microbiology of the Czech Academy of Sciences, Videnska 1083, 142 20 Prague, Czech RepublicLaboratory of Fungal Genomics and Metabolism, Institute of Microbiology of the Czech Academy of Sciences, Videnska 1083, 142 20 Prague, Czech RepublicLaboratory of Molecular Structure Characterization, Institute of Microbiology of the Czech Academy of Sciences, Videnska 1083, 142 20 Prague, Czech RepublicLaboratory of Molecular Structure Characterization, Institute of Microbiology of the Czech Academy of Sciences, Videnska 1083, 142 20 Prague, Czech RepublicLaboratory of Molecular Structure Characterization, Institute of Microbiology of the Czech Academy of Sciences, Videnska 1083, 142 20 Prague, Czech RepublicLaboratory of Molecular Structure Characterization, Institute of Microbiology of the Czech Academy of Sciences, Videnska 1083, 142 20 Prague, Czech RepublicLaboratory of Gnotobiology, Institute of Microbiology of the Czech Academy of Sciences, Doly 183, 549 22 Novy Hradek, Czech RepublicLaboratory of Gnotobiology, Institute of Microbiology of the Czech Academy of Sciences, Doly 183, 549 22 Novy Hradek, Czech RepublicLaboratory of Cellular and Molecular Immunology, Institute of Microbiology of the Czech Academy of Sciences, Videnska 1083, 142 20 Prague, Czech RepublicLaboratory of Cellular and Molecular Immunology, Institute of Microbiology of the Czech Academy of Sciences, Videnska 1083, 142 20 Prague, Czech RepublicLaboratory of Cellular and Molecular Immunology, Institute of Microbiology of the Czech Academy of Sciences, Videnska 1083, 142 20 Prague, Czech RepublicDiet is a strong modifier of microbiome and mucosal microenvironment in the gut. Recently, components of western-type diets have been associated with metabolic and immune diseases. Here, we studied how high-sugar diet (HSD) consumption influences gut mucosal barrier and immune response under steady state conditions and in a mouse model of acute colitis. We found that HSD significantly increased gut permeability, spleen weight, and neutrophil levels in spleens of healthy mice. Subsequent dextran sodium sulfate administration led to severe colitis. In colon, HSD significantly promoted neutrophil infiltration and increased the levels of IL-6, IL-1β, and TNF-α. Moreover, HSD-fed mice had significantly higher abundance of pathobionts, such as <i>Escherichia coli</i> and <i>Candida</i>, in fecal samples. Although germ-free mice colonized with microbiota of conventionally reared mice that consumed different diets had equally severe colitis, mice colonized with HSD microbiota showed markedly increased infiltration of neutrophils to the gut. The induction of colitis in Toll-like receptor 4 (TLR4)-deficient HSD-fed mice led to significantly milder colitis than in wild-type mice. In conclusion, our results suggested a significant role of HSD in disruption of barrier integrity and balanced mucosal and systemic immune response. In addition, these processes seemed to be highly influenced by resident potentially pathogenic microbiota or metabolites via the TLR4 signaling pathway.https://www.mdpi.com/2073-4409/9/12/2701inflammatory bowel diseasesneutrophilsmetabolitesmicrobiomemucosal barrierhigh-sugar diet |
spellingShingle | Alena Fajstova Natalie Galanova Stepan Coufal Jana Malkova Martin Kostovcik Martina Cermakova Helena Pelantova Marek Kuzma Blanka Sediva Tomas Hudcovic Tomas Hrncir Helena Tlaskalova-Hogenova Miloslav Kverka Klara Kostovcikova Diet Rich in Simple Sugars Promotes Pro-Inflammatory Response via Gut Microbiota Alteration and TLR4 Signaling Cells inflammatory bowel diseases neutrophils metabolites microbiome mucosal barrier high-sugar diet |
title | Diet Rich in Simple Sugars Promotes Pro-Inflammatory Response via Gut Microbiota Alteration and TLR4 Signaling |
title_full | Diet Rich in Simple Sugars Promotes Pro-Inflammatory Response via Gut Microbiota Alteration and TLR4 Signaling |
title_fullStr | Diet Rich in Simple Sugars Promotes Pro-Inflammatory Response via Gut Microbiota Alteration and TLR4 Signaling |
title_full_unstemmed | Diet Rich in Simple Sugars Promotes Pro-Inflammatory Response via Gut Microbiota Alteration and TLR4 Signaling |
title_short | Diet Rich in Simple Sugars Promotes Pro-Inflammatory Response via Gut Microbiota Alteration and TLR4 Signaling |
title_sort | diet rich in simple sugars promotes pro inflammatory response via gut microbiota alteration and tlr4 signaling |
topic | inflammatory bowel diseases neutrophils metabolites microbiome mucosal barrier high-sugar diet |
url | https://www.mdpi.com/2073-4409/9/12/2701 |
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