Molecular phenomics and metagenomics of hepatic steatosis in non-diabetic obese women
Open accessAbstract
Hepatic steatosis is a multifactorial condition that is often observed in obese patients and is a prelude to non-alcoholic fatty liver disease. Here, we combine shotgun sequencing of fecal metagenomes with molecular phenomics (hepatic transcriptome and plasma and urine metabolomes) in two well-characterized cohorts of morbidly obese women recruited to the FLORINASH study. We reveal molecular networks linking the gut microbiome and the host phenome to hepatic steatosis. Patients with steatosis have low microbial gene richness and increased genetic potential for the processing of dietary lipids and endotoxin biosynthesis (notably from Proteobacteria), hepatic inflammation and dysregulation of aromatic and branched-chain amino acid metabolism. We demonstrated that fecal microbiota transplants and chronic treatment with phenylacetic acid, a microbial product of aromatic amino acid metabolism, successfully trigger steatosis and branched-chain amino acid metabolism. Molecular phenomic signatures were predictive (area under the curve = 87%) and consistent with the gut microbiome having an effect on the steatosis phenome (>75% shared variation) and, therefore, actionable via microbiome-based therapies. Metabolic activity of specific human gut microorganisms contributes to liver steatosis in obese women.
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PIEZO1 positively correlated with genes encoding collagens such as COL1A1, COL3A1, and COL6A1 in human liver transcription profiling datasets.
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From Stiffness sensing via Piezo1 enhances macrophage efferocytosis and promotes the resolution of liver fibrosis (2024) · cites this paper as [15]
Multi-faceted studies using different methods and research platforms can enable more mechanistic understandings of associations between microbes and host phenotypes.
“An additional advantage of multi-faceted studies using different methods and research platforms is that they can enable more mechanistic understandings of associations between microbes and host phenotypes 37-39 .”
From Human microbiome myths and misconceptions (2023) · cites this paper as [37]
Studies in cohorts of morbidly obese women confirmed the increase in Gram-negative proteobacteria and linked steatosis occurrence with alterations in aromatic and branched-chain amino acid metabolism.
“Studies performed in cohorts of morbidly obese women confirmed the increased in Gram- proteobacteria and linked, for the first time, steatosis occurrence with alterations in aromatic and branched-chain amino acid metabolism [233].”
From Gut-pancreas-liver Axis as a target for treatment of NAFLD/NASH (2020) · cites this paper as [233]
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Kadar, H., Dubus, J., Dutot, J., Hedjazi, L., Srinivasa, S., Fitch, K., Grinspoon, S., Nicholson, J., Dumas, M., & Gauguier, D. (2016) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2016.03.029 · Cited by 13 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Gut microbiota in human metabolic health and disease
Fan, Y., & Pedersen, O. (2021) · Nature Reviews Microbiology · doi:10.1038/s41579-020-0433-9 · Cited by 4,724 · see citing works
MAFLD: a consensus-driven proposed nomenclature for metabolic associated fatty liver disease
Eslam, M., Sanyal, A. J., George, J., Sanyal, A., Neuschwander-Tetri, B., Tiribelli, C., Kleiner, D. E., Brunt, E., Bugianesi, E., Yki-Järvinen, H., et al. (2020) · Gastroenterology · doi:10.1053/j.gastro.2019.11.312 · Cited by 3,286 · see citing works
The gut-liver axis in liver disease: Pathophysiological basis for therapy
Albillos, A., de Gottardi, A., & Rescigno, M. (2020) · Journal of Hepatology · doi:10.1016/j.jhep.2019.10.003 · Cited by 2,166 · see citing works
Mechanisms and disease consequences of nonalcoholic fatty liver disease
Loomba, R., Friedman, S. L., & Shulman, G. I. (2021) · Cell · doi:10.1016/j.cell.2021.04.015 · Cited by 2,002 · see citing works
Gut microbial metabolites in obesity, NAFLD and T2DM
Canfora, E. E., Meex, R. C. R., Venema, K., & Blaak, E. E. (2019) · Nature Reviews Endocrinology · doi:10.1038/s41574-019-0156-z · Cited by 1,493 · see citing works
The integrative biology of type 2 diabetes
Roden, M., & Shulman, G. I. (2019) · Nature · doi:10.1038/s41586-019-1797-8 · Cited by 1,167 · see citing works
Dietary lipids, gut microbiota and lipid metabolism
Schoeler, M., & Caesar, R. (2019) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-019-09512-0 · Cited by 1,163 · see citing works
The intestinal microbiota fuelling metabolic inflammation
Tilg, H., Zmora, N., Adolph, T. E., & Elinav, E. (2020) · Nature Reviews Immunology · doi:10.1038/s41577-019-0198-4 · Cited by 1,089 · see citing works
Diet-microbiota interactions and personalized nutrition
Kolodziejczyk, A. A., Zheng, D., & Elinav, E. (2019) · Nature Reviews Microbiology · doi:10.1038/s41579-019-0256-8 · Cited by 879 · see citing works
The gut–liver axis and gut microbiota in health and liver disease
Hsu, C. L., & Schnabl, B. (2023) · Nature Reviews Microbiology · doi:10.1038/s41579-023-00904-3 · Cited by 737 · see citing works
The role of the microbiome in NAFLD and NASH
Kolodziejczyk, A. A., Zheng, D., Shibolet, O., & Elinav, E. (2019) · EMBO Molecular Medicine · doi:10.15252/emmm.201809302 · Cited by 523 · see citing works
Gut microbiome, liver immunology, and liver diseases
Wang, R., Tang, R., Li, B., Ma, X., Schnabl, B., & Tilg, H. (2021) · Cellular & Molecular Immunology · doi:10.1038/s41423-020-00592-6 · Cited by 466 · see citing works
Gut Bacteria and Neurotransmitters
Dicks, L. M. T. (2022) · Microorganisms · doi:10.3390/microorganisms10091838 · Cited by 482 · see citing works
Metabolomics and lipidomics in NAFLD: biomarkers and non-invasive diagnostic tests
Masoodi, M., Gastaldelli, A., Hyötyläinen, T., Arretxe, E., Alonso, C., Gaggini, M., Brosnan, J., Anstee, Q. M., Millet, O., Ortiz, P., et al. (2021) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-021-00502-9 · Cited by 451 · see citing works
Metabolically healthy versus metabolically unhealthy obesity
Iacobini, C., Pugliese, G., Blasetti Fantauzzi, C., Federici, M., & Menini, S. (2019) · Metabolism · doi:10.1016/j.metabol.2018.11.009 · Cited by 453 · see citing works
Self-citationGut Microbiome Fermentation Determines the Efficacy of Exercise for Diabetes Prevention
Liu, Y., Wang, Y., Ni, Y., Cheung, C. K. Y., Lam, K. S. L., Wang, Y., Xia, Z., Ye, D., Guo, J., Tse, M. A., et al. (2020) · Cell Metabolism · doi:10.1016/j.cmet.2019.11.001 · Cited by 405 · see citing works
RETRACTED ARTICLE: Role of the gut microbiome in chronic diseases: a narrative review
Vijay, A., & Valdes, A. M. (2022) · European Journal of Clinical Nutrition · doi:10.1038/s41430-021-00991-6 · Cited by 361 · see citing works
RetractedChu, H., Duan, Y., Yang, L., & Schnabl, B. (2019) · Gut · doi:10.1136/gutjnl-2018-316307 · Cited by 354 · see citing works
A Gut Microbiome Signature for Cirrhosis Due to Nonalcoholic Fatty Liver Disease
Caussy, C., Tripathi, A., Humphrey, G., Bassirian, S., Singh, S., Faulkner, C., Bettencourt, R., Rizo, E., Richards, L., Xu, Z. Z., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09455-9 · Cited by 338 · see citing works
Gut reactions: Breaking down xenobiotic–microbiome interactions
Clarke, G., Sandhu, K. V., Griffin, B. T., Dinan, T. G., Cryan, J. F., & Hyland, N. P. (2019) · Pharmacological Reviews · doi:10.1124/pr.118.015768 · Cited by 319 · see citing works
A faecal microbiota signature with high specificity for pancreatic cancer
Kartal, E., Schmidt, T. S. B., Molina-Montes, E., Rodríguez-Perales, S., Wirbel, J., Maistrenko, O. M., Akanni, W. A., Alashkar Alhamwe, B., Alves, R. J., Carrato, A., et al. (2022) · Gut · doi:10.1136/gutjnl-2021-324755 · Cited by 290 · see citing works
D’Amato, A., Di Cesare Mannelli, L., Lucarini, E., Man, A. L., Le Gall, G., Branca, J. J. V., Ghelardini, C., Amedei, A., Bertelli, E., Regoli, M., et al. (2020) · Microbiome · doi:10.1186/s40168-020-00914-w · Cited by 269 · see citing works
Self-citationSharpton, S. R., Schnabl, B., Knight, R., & Loomba, R. (2021) · Cell Metabolism · doi:10.1016/j.cmet.2020.11.010 · Cited by 194 · see citing works
Human microbiome myths and misconceptions
Walker, A. W., & Hoyles, L. (2023) · Nature Microbiology · doi:10.1038/s41564-023-01426-7 · Cited by 163 · see citing works
Self-citationAoki, R., Onuki, M., Hattori, K., Ito, M., Yamada, T., Kamikado, K., Kim, Y.-G., Nakamoto, N., Kimura, I., Clarke, J. M., et al. (2021) · Microbiome · doi:10.1186/s40168-021-01125-7 · Cited by 167 · see citing works
Risk assessment with gut microbiome and metabolite markers in NAFLD development
Leung, H., Long, X., Ni, Y., Qian, L., Nychas, E., Siliceo, S. L., Pohl, D., Hanhineva, K., Liu, Y., Xu, A., et al. (2022) · Science Translational Medicine · doi:10.1126/scitranslmed.abk0855 · Cited by 152 · see citing works
Wang, Y., Wang, J., Zhang, J., Wang, Y., Wang, Y., Kang, H., Zhao, W., Bai, W., Miao, N., & Wang, J. (2024) · Science Advances · doi:10.1126/sciadv.adj3289 · Cited by 131 · see citing works
The need for an integrated multi-OMICs approach in microbiome science in the food system
Ferrocino, I., Rantsiou, K., McClure, R., Kostic, T., de Souza, R. S. C., Lange, L., FitzGerald, J., Kriaa, A., Cotter, P., Maguin, E., et al. (2023) · Comprehensive Reviews in Food Science and Food Safety · doi:10.1111/1541-4337.13103 · Cited by 110 · see citing works
The Commensal Microbe V eillonella as a Marker for Response to an FGF19 Analog in NASH
Loomba, R., Ling, L., Dinh, D. M., DePaoli, A. M., Lieu, H. D., Harrison, S. A., & Sanyal, A. J. (2021) · Hepatology · doi:10.1002/hep.31523 · Cited by 88 · see citing works
Rational combination therapy for NASH: Insights from clinical trials and error
Ratziu, V., & Charlton, M. (2023) · Journal of Hepatology · doi:10.1016/j.jhep.2022.12.025 · Cited by 71 · see citing works
Gut-pancreas-liver Axis as a target for treatment of NAFLD/NASH
Svegliati-Baroni, G., Patrício, B., Lioci, G., Macedo, M. P., & Gastaldelli, A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21165820 · Cited by 66 · see citing works
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Self-citationTargeting nonalcoholic fatty liver disease via gut microbiome-centered therapies
Koning, M., Herrema, H., Nieuwdorp, M., & Meijnikman, A. S. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2226922 · Cited by 56 · see citing works
Milbank, E., Díaz-Trelles, R., Dragano, N., Latorre, J., Mukthavaram, R., Mayneris-Perxachs, J., Ortega, F., Federici, M., Burcelin, R., Karmali, P. P., et al. (2023) · Pharmacological Research · doi:10.1016/j.phrs.2022.106562 · Cited by 26 · see citing works
Self-citationAdvancements in MAFLD Modeling with Human Cell and Organoid Models
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- Authors
- Hoyles, L., Fernández-Real, J.-M., Federici, M., Serino, M., Abbott, J., Charpentier, J., Heymes, C., Luque, J. L., Anthony, E., Barton, R. H., Chilloux, J., Myridakis, A., Martinez-Gili, L., Moreno-Navarrete, J. M., Benhamed, F., Azalbert, V., Blasco-Baque, V., Puig, J., Xifra, G., Ricart, W., Tomlinson, C., Woodbridge, M., Cardellini, M., Davato, F., Cardolini, I., Porzio, O., Gentileschi, P., Lopez, F., Foufelle, F., Butcher, S. A., Holmes, E., Nicholson, J. K., Postic, C., Burcelin, R., & Dumas, M.-E.
- Affiliations
- Imperial College London (GB)
- University of Rome Tor Vergata (IT)
- Université Toulouse III - Paul Sabatier (FR)
- Centre National de la Recherche Scientifique (FR)
- Universitat de Girona (ES)
- Centre de Recherche des Cordeliers (FR)
- Corresponding author
- Federici, Massimo
- Burcelin, Rémy
- Dumas, Marc-Emmanuel
- ORCID
- Hoyles, Lesley
- Federici, Massimo
- Serino, Matteo
- Abbott, James
- Heymes, Christophe
- Luque, Jèssica Latorre
- Barton, Richard H.
- Chilloux, Julien
- Myridakis, Antonis
- Martinez-Gili, Laura
- Benhamed, Fadila
- Puig, Josep
- Ricart, Wifredo
- Tomlinson, Christopher
- Woodbridge, Mark
- Cardellini, Marina
- Porzio, Ottavia
- Gentileschi, Paolo
- Lopez, Frédéric
- Foufelle, Fabienne
- Butcher, Sarah A.
- Holmes, Elaine
- Nicholson, Jeremy K.
- Postic, Catherine
- Burcelin, Rémy
- Dumas, Marc-Emmanuel
- Venue
- Nature Medicine
- Published
- 2018-06-25
- Volume
- 24
- Issue
- 7
- Pages
- 1070-1080
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- PMC
- PMC6140997
- OpenAlex
- W2790364467
- Semantic Scholar
- 95928b78c00de22480cf16a53a5c05b9c288d335
- Cited by
- 720
- References
- 80
- Citations by year
- 2026: 54 · 2025: 79 · 2024: 104 · 2023: 103 · 2022: 86 · 2021: 112 · 2020: 99 · 2019: 52 · 2018: 29
- FWCI
- 26.15
- Type
- journal article
- Language
- en
- Update notices
- correction (2018-08-09)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Medicine (publishedVersion)
- PubMed (publishedVersion)
- Discovery Research Portal (University of Dundee) (publishedVersion)
- Nottingham Trent University's Institutional Repository (Nottingham Trent Repository) (acceptedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- HAL (submittedVersion)
- HAL (submittedVersion, other-oa)
- Cineca Institutional Research Information System (Tor Vergata University) (submittedVersion)
- Cineca Institutional Research Information System (Tor Vergata University) (submittedVersion, other-oa)
- Spiral (Imperial College London) (submittedVersion)
- Funders
- Agence Nationale de la Recherche (ANR-09-GENO-0032)
- Medical Research Council (MR/M501797/1, MR/L01632X/1)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Epidemiology › Liver Disease Diagnosis and Treatment
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diet, Metabolism, and Disease
- Keywords
- hepatic steatosis, non-diabetic obesity, non-alcoholic fatty liver disease, gut microbiota, fecal microbiota transplantation, phenylacetic acid, branched-chain amino acid metabolism, aromatic amino acid metabolism, Proteobacteria, liver transcriptome, plasma metabolome, urinary metabolome, liver inflammation, women, microbiota-based therapy
- MeSH terms
- Fecal Microbiota Transplantation, Animals, Cells, Cultured, Diabetes Mellitus, Female, Humans, Obesity, Phenotype, Cohort Studies, Confounding Factors, Epidemiologic, Hepatocytes, Mice, Metabolomics, Metabolome, Metagenomics, Transcriptome, Microbiota, Non-alcoholic Fatty Liver Disease
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