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

Author

Listed:
  • Antonio Molinaro

    (Wallenberg Laboratory, Department of Molecular and Clinical Medicine and Sahlgrenska Center for Cardiovascular and Metabolic Research, University of Gothenburg
    Department of Medicine, Sahlgrenska University Hospital)

  • Pierre Bel Lassen

    (INSERM, Nutrition and Obesities; Systemic Approaches (NutriOmics), Sorbonne Université
    Assistance Publique Hôpitaux de Paris, Pitie-Salpêtrière Hospital, Nutrition department, CRNH Ile de France)

  • 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
    Integromics Unit, Institute of Cardiometabolism and Nutrition)

  • 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
    Center for Microbiology)

  • Nicolas Pons

    (Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay)

  • Edi Prifti

    (Integromics Unit, Institute of Cardiometabolism and Nutrition
    Unité de Modélisation Mathématique et Informatique des Systèmes Complexes, UMMISCO)

  • 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
    Center for Microbiology)

  • 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
    Genomic and Environmental Medicine, National Heart & Lung Institute, Faculty of Medicine, Imperial College London)

  • Jeroen Raes

    (Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay
    Laboratory of Molecular Bacteriology, Department of Microbiology and Immunology, Rega Institute)

  • 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
    Molecular Medicine Partnership Unit, University of Heidelberg and 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
    Assistance Publique Hôpitaux de Paris, Pitie-Salpêtrière Hospital, Nutrition department, CRNH Ile de France)

  • Karine Clément

    (INSERM, Nutrition and Obesities; Systemic Approaches (NutriOmics), Sorbonne Université
    Assistance Publique Hôpitaux de Paris, Pitie-Salpêtrière Hospital, Nutrition department, CRNH Ile de France)

  • Fredrik Bäckhed

    (Wallenberg Laboratory, Department of Molecular and Clinical Medicine and Sahlgrenska Center for Cardiovascular and Metabolic Research, University of Gothenburg
    Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen
    Department of Clinical Physiology, Region Västra Götaland, Sahlgrenska University Hospital)

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.

Suggested Citation

  • 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 Marq, 2020. "Imidazole propionate is increased in diabetes and associated with dietary patterns and altered microbial ecology," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-19589-w
    DOI: 10.1038/s41467-020-19589-w
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    Cited by:

    1. M. C. Rühlemann & C. Bang & J. F. Gogarten & B. M. Hermes & M. Groussin & S. Waschina & M. Poyet & M. Ulrich & C. Akoua-Koffi & T. Deschner & J. J. Muyembe-Tamfum & M. M. Robbins & M. Surbeck & R. M. , 2024. "Functional host-specific adaptation of the intestinal microbiome in hominids," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

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