Imidazole propionate is increased in diabetes and associated with dietary patterns and altered microbial ecology

Antonio Molinaro, Pierre Bel Lassen, Marcus Henricsson, Hao Wu, Solia Adriouch, Eugeni Belda, Rima Chakaroun, Trine Nielsen, Per-Olof Bergh, Christine Rouault, Sébastien André, Florian Marquet, Fabrizio Andreelli, Joe-Elie Salem, Karen Assmann, Jean-Philippe Bastard, Sofia Forslund, Emmanuelle Le Chatelier, Gwen Falony, Nicolas Pons, Edi Prifti, Benoit Quinquis, Hugo Roume, Sara Vieira-Silva, Tue H. Hansen, Helle Krogh Pedersen, Christian Lewinter, Nadja B. Sønderskov, Lars Køber, Henrik Vestergaard, Torben Hansen, Jean-Daniel Zucker, Pilar Galan, Marc-Emmanuel Dumas, Jeroen Raes, Jean-Michel Oppert, Ivica Letunic, Jens Nielsen, Peer Bork, S. Dusko Ehrlich, Michael Stumvoll, Oluf Pedersen, Judith Aron-Wisnewsky, Karine Clément () and Fredrik Bäckhed ()
Additional contact information
Antonio Molinaro: Wallenberg Laboratory, Department of Molecular and Clinical Medicine and Sahlgrenska Center for Cardiovascular and Metabolic Research, University of Gothenburg
Pierre Bel Lassen: INSERM, Nutrition and Obesities; Systemic Approaches (NutriOmics), Sorbonne Université
Marcus Henricsson: Wallenberg Laboratory, Department of Molecular and Clinical Medicine and Sahlgrenska Center for Cardiovascular and Metabolic Research, University of Gothenburg
Hao Wu: Wallenberg Laboratory, Department of Molecular and Clinical Medicine and Sahlgrenska Center for Cardiovascular and Metabolic Research, University of Gothenburg
Solia Adriouch: INSERM, Nutrition and Obesities; Systemic Approaches (NutriOmics), Sorbonne Université
Eugeni Belda: INSERM, Nutrition and Obesities; Systemic Approaches (NutriOmics), Sorbonne Université
Rima Chakaroun: Medical Department III - Endocrinology, Nephrology, Rheumatology, University of Leipzig Medical Center
Trine Nielsen: Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen
Per-Olof Bergh: Wallenberg Laboratory, Department of Molecular and Clinical Medicine and Sahlgrenska Center for Cardiovascular and Metabolic Research, University of Gothenburg
Christine Rouault: INSERM, Nutrition and Obesities; Systemic Approaches (NutriOmics), Sorbonne Université
Sébastien André: INSERM, Nutrition and Obesities; Systemic Approaches (NutriOmics), Sorbonne Université
Florian Marquet: INSERM, Nutrition and Obesities; Systemic Approaches (NutriOmics), Sorbonne Université
Fabrizio Andreelli: INSERM, Nutrition and Obesities; Systemic Approaches (NutriOmics), Sorbonne Université
Joe-Elie Salem: Assistance Publique Hôpitaux de Paris, Clinical Investigation Center Paris East
Karen Assmann: INSERM, Nutrition and Obesities; Systemic Approaches (NutriOmics), Sorbonne Université
Jean-Philippe Bastard: Assistance Publique Hôpitaux de Paris, Biochemistry and Hormonology Department, Tenon Hospital
Sofia Forslund: Experimental and Clinical Research Center, A Cooperation of Charité-Universitätsmedizin and the Max-Delbrück Center
Emmanuelle Le Chatelier: Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay
Gwen Falony: Laboratory of Molecular Bacteriology, Department of Microbiology and Immunology, Rega Institute
Nicolas Pons: Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay
Edi Prifti: Integromics Unit, Institute of Cardiometabolism and Nutrition
Benoit Quinquis: Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay
Hugo Roume: Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay
Sara Vieira-Silva: Laboratory of Molecular Bacteriology, Department of Microbiology and Immunology, Rega Institute
Tue H. Hansen: Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen
Helle Krogh Pedersen: Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen
Christian Lewinter: Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen
Nadja B. Sønderskov: Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen
Lars Køber: Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen
Henrik Vestergaard: Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen
Torben Hansen: Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen
Jean-Daniel Zucker: Unité de Modélisation Mathématique et Informatique des Systèmes Complexes, UMMISCO
Pilar Galan: Sorbonne Paris Cité Epidemiology and Statistics Research Centre (CRESS), U1153 Inserm, U1125, Inra, Cnam, University of Paris 13, Nutritional Epidemiology Research Team (EREN)
Marc-Emmanuel Dumas: Computational and Systems Medicine, Department of Metabolism, Digestion and Reproduction, Faculty of Medicine, Imperial College London
Jeroen Raes: Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay
Jean-Michel Oppert: Assistance Publique Hôpitaux de Paris, Pitie-Salpêtrière Hospital, Nutrition department, CRNH Ile de France
Ivica Letunic: Biobyte Solutions GmbH
Jens Nielsen: Department of Biology and Biological Engineering, Chalmers University of Technology
Peer Bork: Structural and Computational Biology, European Molecular Biology Laboratory
S. Dusko Ehrlich: Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay
Michael Stumvoll: Medical Department III - Endocrinology, Nephrology, Rheumatology, University of Leipzig Medical Center
Oluf Pedersen: Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen
Judith Aron-Wisnewsky: INSERM, Nutrition and Obesities; Systemic Approaches (NutriOmics), Sorbonne Université
Karine Clément: INSERM, Nutrition and Obesities; Systemic Approaches (NutriOmics), Sorbonne Université
Fredrik Bäckhed: Wallenberg Laboratory, Department of Molecular and Clinical Medicine and Sahlgrenska Center for Cardiovascular and Metabolic Research, University of Gothenburg

Nature Communications, 2020, vol. 11, issue 1, 1-10

Abstract: Abstract Microbiota-host-diet interactions contribute to the development of metabolic diseases. Imidazole propionate is a novel microbially produced metabolite from histidine, which impairs glucose metabolism. Here, we show that subjects with prediabetes and diabetes in the MetaCardis cohort from three European countries have elevated serum imidazole propionate levels. Furthermore, imidazole propionate levels were increased in subjects with low bacterial gene richness and Bacteroides 2 enterotype, which have previously been associated with obesity. The Bacteroides 2 enterotype was also associated with increased abundance of the genes involved in imidazole propionate biosynthesis from dietary histidine. Since patients and controls did not differ in their histidine dietary intake, the elevated levels of imidazole propionate in type 2 diabetes likely reflects altered microbial metabolism of histidine, rather than histidine intake per se. Thus the microbiota may contribute to type 2 diabetes by generating imidazole propionate that can modulate host inflammation and metabolism.

Date: 2020
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DOI: 10.1038/s41467-020-19589-w

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