Microbially Produced Imidazole Propionate Impairs Insulin Signaling through mTORC1
Interactions between the gut microbiota, diet, and the host potentially contribute to the development of metabolic diseases. Here, we identify imidazole propionate as a microbially produced histidine-derived metabolite that is present at higher concentrations in subjects with versus without type 2 d...
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| Published in | Cell Vol. 175; no. 4; pp. 947 - 961.e17 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.11.2018
|
| Subjects | |
| Online Access | Get full text |
| ISSN | 0092-8674 1097-4172 1097-4172 |
| DOI | 10.1016/j.cell.2018.09.055 |
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| Abstract | Interactions between the gut microbiota, diet, and the host potentially contribute to the development of metabolic diseases. Here, we identify imidazole propionate as a microbially produced histidine-derived metabolite that is present at higher concentrations in subjects with versus without type 2 diabetes. We show that imidazole propionate is produced from histidine in a gut simulator at higher concentrations when using fecal microbiota from subjects with versus without type 2 diabetes and that it impairs glucose tolerance when administered to mice. We further show that imidazole propionate impairs insulin signaling at the level of insulin receptor substrate through the activation of p38γ MAPK, which promotes p62 phosphorylation and, subsequently, activation of mechanistic target of rapamycin complex 1 (mTORC1). We also demonstrate increased activation of p62 and mTORC1 in liver from subjects with type 2 diabetes. Our findings indicate that the microbial metabolite imidazole propionate may contribute to the pathogenesis of type 2 diabetes.
[Display omitted]
•Imidazole propionate levels are increased in subjects with type 2 diabetes (T2D)•Imidazole propionate is produced from histidine by T2D-associated bacteria•Imidazole propionate impairs glucose tolerance and insulin signaling•Imidazole propionate inhibits IRS via activation of p38γ/p62/mTORC1
Imidazole propionate, a metabolite produced by the gut microbiota, is elevated in type 2 diabetes and can directly impair glucose tolerance and insulin signaling. |
|---|---|
| AbstractList | Interactions between the gut microbiota, diet, and the host potentially contribute to the development of metabolic diseases. Here, we identify imidazole propionate as a microbially produced histidine-derived metabolite that is present at higher concentrations in subjects with versus without type 2 diabetes. We show that imidazole propionate is produced from histidine in a gut simulator at higher concentrations when using fecal microbiota from subjects with versus without type 2 diabetes and that it impairs glucose tolerance when administered to mice. We further show that imidazole propionate impairs insulin signaling at the level of insulin receptor substrate through the activation of p38γ MAPK, which promotes p62 phosphorylation and, subsequently, activation of mechanistic target of rapamycin complex 1 (mTORC1). We also demonstrate increased activation of p62 and mTORC1 in liver from subjects with type 2 diabetes. Our findings indicate that the microbial metabolite imidazole propionate may contribute to the pathogenesis of type 2 diabetes.
[Display omitted]
•Imidazole propionate levels are increased in subjects with type 2 diabetes (T2D)•Imidazole propionate is produced from histidine by T2D-associated bacteria•Imidazole propionate impairs glucose tolerance and insulin signaling•Imidazole propionate inhibits IRS via activation of p38γ/p62/mTORC1
Imidazole propionate, a metabolite produced by the gut microbiota, is elevated in type 2 diabetes and can directly impair glucose tolerance and insulin signaling. Interactions between the gut microbiota, diet, and the host potentially contribute to the development of metabolic diseases. Here, we identify imidazole propionate as a microbially produced histidine-derived metabolite that is present at higher concentrations in subjects with versus without type 2 diabetes. We show that imidazole propionate is produced from histidine in a gut simulator at higher concentrations when using fecal microbiota from subjects with versus without type 2 diabetes and that it impairs glucose tolerance when administered to mice. We further show that imidazole propionate impairs insulin signaling at the level of insulin receptor substrate through the activation of p38γ MAPK, which promotes p62 phosphorylation and, subsequently, activation of mechanistic target of rapamycin complex 1 (mTORC1). We also demonstrate increased activation of p62 and mTORC1 in liver from subjects with type 2 diabetes. Our findings indicate that the microbial metabolite imidazole propionate may contribute to the pathogenesis of type 2 diabetes. Interactions between the gut microbiota, diet, and the host potentially contribute to the development of metabolic diseases. Here, we identify imidazole propionate as a microbially produced histidine-derived metabolite that is present at higher concentrations in subjects with versus without type 2 diabetes. We show that imidazole propionate is produced from histidine in a gut simulator at higher concentrations when using fecal microbiota from subjects with versus without type 2 diabetes and that it impairs glucose tolerance when administered to mice. We further show that imidazole propionate impairs insulin signaling at the level of insulin receptor substrate through the activation of p38 gamma MAPK, which promotes p62 phosphorylation and, subsequently, activation of mechanistic target of rapamycin complex 1 (mTORC1). We also demonstrate increased activation of p62 and mTORC1 in liver from subjects with type 2 diabetes. Our findings indicate that the microbial metabolite imidazole propionate may contribute to the pathogenesis of type 2 diabetes. Interactions between the gut microbiota, diet, and the host potentially contribute to the development of metabolic diseases. Here, we identify imidazole propionate as a microbially produced histidine-derived metabolite that is present at higher concentrations in subjects with versus without type 2 diabetes. We show that imidazole propionate is produced from histidine in a gut simulator at higher concentrations when using fecal microbiota from subjects with versus without type 2 diabetes and that it impairs glucose tolerance when administered to mice. We further show that imidazole propionate impairs insulin signaling at the level of insulin receptor substrate through the activation of p38γ MAPK, which promotes p62 phosphorylation and, subsequently, activation of mechanistic target of rapamycin complex 1 (mTORC1). We also demonstrate increased activation of p62 and mTORC1 in liver from subjects with type 2 diabetes. Our findings indicate that the microbial metabolite imidazole propionate may contribute to the pathogenesis of type 2 diabetes.Interactions between the gut microbiota, diet, and the host potentially contribute to the development of metabolic diseases. Here, we identify imidazole propionate as a microbially produced histidine-derived metabolite that is present at higher concentrations in subjects with versus without type 2 diabetes. We show that imidazole propionate is produced from histidine in a gut simulator at higher concentrations when using fecal microbiota from subjects with versus without type 2 diabetes and that it impairs glucose tolerance when administered to mice. We further show that imidazole propionate impairs insulin signaling at the level of insulin receptor substrate through the activation of p38γ MAPK, which promotes p62 phosphorylation and, subsequently, activation of mechanistic target of rapamycin complex 1 (mTORC1). We also demonstrate increased activation of p62 and mTORC1 in liver from subjects with type 2 diabetes. Our findings indicate that the microbial metabolite imidazole propionate may contribute to the pathogenesis of type 2 diabetes. |
| Author | Khan, Muhammad Tanweer Wu, Hao de Brauw, Maurits Koh, Ara Schmidt, Caroline Hartstra, Annick Jeong, Heeyoon Olofsson, Louise E. Bäckhed, Fredrik Nieuwdorp, Max Carreras, Alba Gerdes, Victor Ståhlman, Marcus Perkins, Rosie Bergström, Göran Molinaro, Antonio Mannerås-Holm, Louise Bergh, Per-Olof |
| Author_xml | – sequence: 1 givenname: Ara surname: Koh fullname: Koh, Ara organization: Department of Molecular and Clinical Medicine/Wallenberg Laboratory, Institute of Medicine, University of Gothenburg and Sahlgrenska University Hospital, Gothenburg, Sweden – sequence: 2 givenname: Antonio surname: Molinaro fullname: Molinaro, Antonio organization: Department of Molecular and Clinical Medicine/Wallenberg Laboratory, Institute of Medicine, University of Gothenburg and Sahlgrenska University Hospital, Gothenburg, Sweden – sequence: 3 givenname: Marcus surname: Ståhlman fullname: Ståhlman, Marcus organization: Department of Molecular and Clinical Medicine/Wallenberg Laboratory, Institute of Medicine, University of Gothenburg and Sahlgrenska University Hospital, Gothenburg, Sweden – sequence: 4 givenname: Muhammad Tanweer surname: Khan fullname: Khan, Muhammad Tanweer organization: Department of Molecular and Clinical Medicine/Wallenberg Laboratory, Institute of Medicine, University of Gothenburg and Sahlgrenska University Hospital, Gothenburg, Sweden – sequence: 5 givenname: Caroline surname: Schmidt fullname: Schmidt, Caroline organization: Department of Molecular and Clinical Medicine/Wallenberg Laboratory, Institute of Medicine, University of Gothenburg and Sahlgrenska University Hospital, Gothenburg, Sweden – sequence: 6 givenname: Louise surname: Mannerås-Holm fullname: Mannerås-Holm, Louise organization: Department of Molecular and Clinical Medicine/Wallenberg Laboratory, Institute of Medicine, University of Gothenburg and Sahlgrenska University Hospital, Gothenburg, Sweden – sequence: 7 givenname: Hao surname: Wu fullname: Wu, Hao organization: Department of Molecular and Clinical Medicine/Wallenberg Laboratory, Institute of Medicine, University of Gothenburg and Sahlgrenska University Hospital, Gothenburg, Sweden – sequence: 8 givenname: Alba surname: Carreras fullname: Carreras, Alba organization: Department of Molecular and Clinical Medicine/Wallenberg Laboratory, Institute of Medicine, University of Gothenburg and Sahlgrenska University Hospital, Gothenburg, Sweden – sequence: 9 givenname: Heeyoon surname: Jeong fullname: Jeong, Heeyoon organization: Department of Life Sciences, Pohang University of Science and Technology, Pohang 37673, Republic of Korea – sequence: 10 givenname: Louise E. surname: Olofsson fullname: Olofsson, Louise E. organization: Department of Molecular and Clinical Medicine/Wallenberg Laboratory, Institute of Medicine, University of Gothenburg and Sahlgrenska University Hospital, Gothenburg, Sweden – sequence: 11 givenname: Per-Olof surname: Bergh fullname: Bergh, Per-Olof organization: Department of Molecular and Clinical Medicine/Wallenberg Laboratory, Institute of Medicine, University of Gothenburg and Sahlgrenska University Hospital, Gothenburg, Sweden – sequence: 12 givenname: Victor surname: Gerdes fullname: Gerdes, Victor organization: Slotervaart Hospital, Amsterdam, the Netherlands – sequence: 13 givenname: Annick surname: Hartstra fullname: Hartstra, Annick organization: Department of Vascular Medicine, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlands – sequence: 14 givenname: Maurits surname: de Brauw fullname: de Brauw, Maurits organization: Slotervaart Hospital, Amsterdam, the Netherlands – sequence: 15 givenname: Rosie surname: Perkins fullname: Perkins, Rosie organization: Department of Molecular and Clinical Medicine/Wallenberg Laboratory, Institute of Medicine, University of Gothenburg and Sahlgrenska University Hospital, Gothenburg, Sweden – sequence: 16 givenname: Max surname: Nieuwdorp fullname: Nieuwdorp, Max organization: Department of Molecular and Clinical Medicine/Wallenberg Laboratory, Institute of Medicine, University of Gothenburg and Sahlgrenska University Hospital, Gothenburg, Sweden – sequence: 17 givenname: Göran surname: Bergström fullname: Bergström, Göran organization: Department of Molecular and Clinical Medicine/Wallenberg Laboratory, Institute of Medicine, University of Gothenburg and Sahlgrenska University Hospital, Gothenburg, Sweden – sequence: 18 givenname: Fredrik surname: Bäckhed fullname: Bäckhed, Fredrik email: fredrik@wlab.gu.se organization: Department of Molecular and Clinical Medicine/Wallenberg Laboratory, Institute of Medicine, University of Gothenburg and Sahlgrenska University Hospital, Gothenburg, Sweden |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30401435$$D View this record in MEDLINE/PubMed https://gup.ub.gu.se/publication/274697$$DView record from Swedish Publication Index |
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| Title | Microbially Produced Imidazole Propionate Impairs Insulin Signaling through mTORC1 |
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