Cited by 798Gut microbiota and healthAdipokines, Inflammation, and Metabolic DiseasesOral microbiology and periodontitis research

Akkermansia muciniphila inversely correlates with the onset of inflammation, altered adipose tissue metabolism and metabolic disorders during obesity in mice

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Schneeberger, Marc, Everard, Amandine, Gómez-Valadés, Alicia G., Matamoros, Sébastien, Ramírez, Sara, Delzenne, Nathalie M., Gomis, Ramon, Claret, Marc +1 more·2015·Scientific Reports

Abstract

Recent evidence indicates that the gut microbiota plays a key role in the pathophysiology of obesity. Indeed, diet-induced obesity (DIO) has been associated to substantial changes in gut microbiota composition in rodent models. In the context of obesity, enhanced adiposity is accompanied by low-grade inflammation of this tissue but the exact link with gut microbial community remains unknown. In this report, we studied the consequences of high-fat diet (HFD) administration on metabolic parameters and gut microbiota composition over different periods of time. We found that Akkermansia muciniphila abundance was strongly and negatively affected by age and HFD feeding and to a lower extend Bilophila wadsworthia was the only taxa following an opposite trend. Different approaches, including multifactorial analysis, showed that these changes in Akkermansia muciniphila were robustly correlated with the expression of lipid metabolism and inflammation markers in adipose tissue, as well as several circulating parameters (i.e., glucose, insulin, triglycerides, leptin) from DIO mice. Thus, our data shows the existence of a link between gut Akkermansia muciniphila abundance and adipose tissue homeostasis on the onset of obesity, thus reinforcing the beneficial role of this bacterium on metabolism.

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Crossref · 10.1038/srep16643

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  • Akkermansia muciniphila suggests great potential for the treatment of obesity.

    “Akkermansia muciniphila undergoes changes according to the diet consumed, modulates the intestinal microbiota, changes inflammatory conditions in adipose tissue, and improves metabolic parameters, like body weight, adiposity, inflammation markers and biochemical parameters, which suggests a great potential for the treatment of obesity (74).”

    From Kefir and Intestinal Microbiota Modulation: Implications in Human Health (2021) · cites this paper as [74]

    The Discussion (page unavailable) reports that A. muciniphila abundance changes with diet and is associated with adipose-tissue inflammation and metabolic measures in mice. It also cites studies in which administering the bacterium mitigated weight and fat-mass gain, supporting the suggestion of obesity-treatment potential. But this study primarily establishes correlations; it does not show that A. muciniphila itself modulates the wider gut microbiota or improves every listed parameter. (LLM, conf=0.84)

    Experimental — accuracy not yet measured
  • Akkermansia muciniphila modulates intestinal microbiota, changes inflammatory conditions in adipose tissue, and improves metabolic parameters such as body weight, adiposity, inflammation markers, and biochemical parameters.

    “Akkermansia muciniphila undergoes changes according to the diet consumed, modulates the intestinal microbiota, changes inflammatory conditions in adipose tissue, and improves metabolic parameters, like body weight, adiposity, inflammation markers and biochemical parameters, which suggests a great potential for the treatment of obesity (74).”

    From Kefir and Intestinal Microbiota Modulation: Implications in Human Health (2021) · cites this paper as [74]

    The Results and Discussion (page not provided) link Akkermansia muciniphila abundance in high-fat-diet-fed mice to adipose-tissue inflammation and metabolic markers; the Discussion also reports prior studies in which its administration mitigated weight and fat-mass gain. But this paper's findings are correlations, not evidence that the bacterium itself modulates the intestinal microbiota or causes the listed improvements. The Discussion says a direct effect on adipose-tissue function warrants further investigation. (LLM, conf=0.88)

    Experimental — accuracy not yet measured
  • Schneeberger et al. found that the abundance of A. muciniphila progressively decreases with HFD feeding and is inversely correlated with WAT inflammation and serum concentrations of leptin and insulin.

    “Schneeberger et al. found that the abundance of A. muciniphila progressively decrease with HFD feeding and is inversely correlated with WAT inflammation and serum concentrations of leptin and insulin (Schneeberger et al., 2015).”

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Research works printed but not linked: 34

  1. Everard A. et al. Microbiome of prebiotic-treated mice reveals novel targets involved in host response during obesity. The ISME journal 8, 2116– 2130, doi: 10.1038/ismej.2014.45 (2014). 24694712 PMC4163056 · DOI · Paper page
  2. Everard A., Matamoros S., Geurts L., Delzenne N. M. & Cani P. D. Saccharomyces boulardii Administration Changes Gut Microbiota and Reduces Hepatic Steatosis, Low-Grade Inflammation, and Fat Mass in Obese and Type 2 Diabetic db/db Mice. mBio 5, doi: 10.1128/mBio.01011-14 (2014). PMC4056549 24917595 · DOI
  3. Everard A. et al. Intestinal epithelial MyD88 is a sensor switching host metabolism towards obesity according to nutritional status. Nature communications 5, 5648, doi: 10.1038/ncomms6648 (2014). PMC4268705 25476696 · DOI
  4. Cotillard A. et al. Dietary intervention impact on gut microbial gene richness. Nature 500, 585– 588, doi: 10.1038/nature12480 (2013). 23985875 · DOI · Paper page
  5. Tremaroli V. & Backhed F. Functional interactions between the gut microbiota and host metabolism. Nature 489, 242– 249, doi: 10.1038/nature11552 (2012). 22972297 · DOI · Paper page
  6. Cani P. D. et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56, 1761– 1772 (2007). 17456850
  7. Cani P. D. et al. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 50, 2374– 2383 (2007). 17823788
  8. Turnbaugh P. J., Backhed F., Fulton L. & Gordon J. I. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host.Microbe 3, 213– 223 (2008). 18407065 PMC3687783
  9. Serino M. et al. Metabolic adaptation to a high-fat diet is associated with a change in the gut microbiota. Gut 61, 543– 553, doi: 10.1136/gutjnl-2011-301012 (2012). 22110050 PMC3292714 · DOI
  10. Everard A. et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci USA 110, 9066– 9071, doi: 10.1073/pnas.1219451110 (2013). 23671105 PMC3670398 · DOI · Paper page
  11. Wang J. H., Bose S., Kim H. G., Han K. S. & Kim H. Fermented Rhizoma Atractylodis Macrocephalae alleviates high fat diet-induced obesity in association with regulation of intestinal permeability and microbiota in rats. Scientific reports 5, 8391, doi: 10.1038/srep08391 (2015). 25684573 PMC4329570 · DOI
  12. Dewulf E. M. et al. Inulin-type fructans with prebiotic properties counteract GPR43 overexpression and PPARgamma-related adipogenesis in the white adipose tissue of high-fat diet-fed mice. J. Nutr. Biochem. 22, 712– 722 (2011). 21115338
  13. Neyrinck A. M. et al. Curcuma longa Extract Associated with White Pepper Lessens High Fat Diet-Induced Inflammation in Subcutaneous Adipose Tissue. PLoS One 8, 0081252 (2013). PMC3834320 24260564
  14. Neyrinck A. M. et al. Polyphenol-rich extract of pomegranate peel alleviates tissue inflammation and hypercholesterolaemia in high-fat diet-induced obese mice: potential implication of the gut microbiota. The British journal of nutrition 109, 802– 809, doi: 10.1017/S0007114512002206 (2013). 22676910 · DOI
  15. Qiu Y. et al. Eosinophils and type 2 cytokine signaling in macrophages orchestrate development of functional beige fat. Cell 157, 1292– 1308, doi: 10.1016/j.cell.2014.03.066 (2014). 24906148 PMC4129510 · DOI
  16. Rao R. R. et al. Meteorin-like Is a Hormone that Regulates Immune-Adipose Interactions to Increase Beige Fat Thermogenesis. Cell 157, 1279– 1291, doi: 10.1016/j.cell.2014.03.065 (2014). 24906147 PMC4131287 · DOI · Paper page
  17. Muccioli G. G. et al. The endocannabinoid system links gut microbiota to adipogenesis. Mol. Syst. Biol. 6, 392 (2010). 20664638 PMC2925525
  18. Geurts L. et al. Adipose tissue NAPE-PLD controls fat mass development by altering the browning process and gut microbiota. Nature communications 6, 6495, doi: 10.1038/ncomms7495 (2015). PMC4382707 25757720 · DOI
  19. Wueest S., Yang X., Liu J., Schoenle E. J. & Konrad D. Inverse regulation of basal lipolysis in perigonadal and mesenteric fat depots in mice. American journal of physiology. Endocrinology and metabolism 302, E153– 160, doi: 10.1152/ajpendo.00338.2011 (2012). 21989031 PMC3774557 · DOI
  20. Stanton M. C. et al. Inflammatory Signals shift from adipose to liver during high fat feeding and influence the development of steatohepatitis in mice. J Inflamm (Lond) 8, 8, doi: 10.1186/1476-9255-8-8 (2011). 21410952 PMC3070617 · DOI
  21. Shin N. R. et al. An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut 63, 727– 735, doi: 10.1136/gutjnl-2012-303839 (2014). 23804561 · DOI · Paper page
  22. Kim H. et al. Modulation of the intestinal microbiota is associated with lower plasma cholesterol and weight gain in hamsters fed chardonnay grape seed flour. J Agric Food Chem 63, 1460– 1467, doi: 10.1021/jf5026373 (2015). 25598538 · DOI
  23. Dewulf E. M. et al. Insight into the prebiotic concept: lessons from an exploratory, double blind intervention study with inulin-type fructans in obese women. Gut, doi: 10.1136/gutjnl-2012-303304 (2012). PMC3711491 23135760 · DOI · Paper page
  24. Cani P. D. & Van Hul M. Novel opportunities for next-generation probiotics targeting metabolic syndrome. Curr Opin Biotechnol 32, 21– 27, doi: 10.1016/j.copbio.2014.10.006 (2015). 25448228 · DOI · Paper page
  25. Parks B. W. et al. Genetic control of obesity and gut microbiota composition in response to high-fat, high-sucrose diet in mice. Cell Metab 17, 141– 152, doi: 10.1016/j.cmet.2012.12.007 (2013). 23312289 PMC3545283 · DOI · Paper page
  26. Carmody R. N. et al. Diet dominates host genotype in shaping the murine gut microbiota. Cell host & microbe 17, 72- 84, doi: 10.1016/j.chom.2014.11.010 (2015). 25532804 PMC4297240 · DOI · Paper page
  27. Hamilton M. K., Boudry G., Lemay D. G. & Raybould H. E. Changes in intestinal barrier function and gut microbiota in high-fat diet-fed rats are dynamic and region dependent. American journal of physiology. Gastrointestinal and liver physiology 308, G840– 851, doi: 10.1152/ajpgi.00029.2015 (2015). 25747351 PMC4437018 · DOI
  28. Dao M. C. et al. Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology. Gut, doi: 10.1136/gutjnl-2014-308778 (2015). 26100928 · DOI · Paper page
  29. Everard A. et al. Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice. Diabetes 60, 2775– 2786 (2011). 21933985 PMC3198091
  30. Collado M. C., Derrien M., Isolauri E., de Vos W. M. & Salminen S. Intestinal integrity and Akkermansia muciniphila, a mucin-degrading member of the intestinal microbiota present in infants, adults, and the elderly. Appl Environ Microbiol 73, 7767– 7770, doi: 10.1128/AEM.01477-07 (2007). 17933936 PMC2168041 · DOI · Paper page
  31. Sonoyama K. et al. Response of gut microbiota to fasting and hibernation in Syrian hamsters. Appl Environ Microbiol 75, 6451– 6456, doi: 10.1128/AEM.00692-09 (2009). 19700553 PMC2765128 · DOI
  32. Remely M. et al. Increased gut microbiota diversity and abundance of Faecalibacterium prausnitzii and Akkermansia after fasting: a pilot study. Wiener klinische Wochenschrift, doi: 10.1007/s00508-015-0755-1 (2015). PMC4452615 25763563 · DOI
  33. Claret M. et al. AMPK is essential for energy homeostasis regulation and glucose sensing by POMC and AgRP neurons. J.Clin.Invest 117, 2325– 2336 (2007). PMC1934578 17671657
  34. Dewulf E. M. et al. Insight into the prebiotic concept: lessons from an exploratory, double blind intervention study with inulin-type fructans in obese women. Gut 62, 1112– 1121, doi: 10.1136/gutjnl-2012-303304 (2013). PMC3711491 23135760 · DOI · Paper page

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Authors
Schneeberger, M., Everard, A., Gómez-Valadés, A. G., Matamoros, S., Ramírez, S., Delzenne, N. M., Gomis, R., Claret, M., & Cani, P. D.
Affiliations
  • Centro de Investigación Biomédica en Red Diabetes y Enfermedades Metabólicas Asociadas (ES)
  • Walloon Excellence in Lifesciences and Biotechnology (BE)
  • Consorci Institut D'Investigacions Biomediques August Pi I Sunyer (ES)
Corresponding author
  • Claret, Marc
  • Cani, Patrice D.
Venue
Scientific Reports
Published
2015-11-13
Volume
5
Issue
1
Pages
16643-16643
ISSN
2045-2322 (ISSN-L)
OpenAlex
W2206854629
Cited by
798
References
10
Citations by year
2026: 37 · 2025: 47 · 2024: 63 · 2023: 70 · 2022: 88 · 2021: 101 · 2020: 106 · 2019: 101 · 2018: 84 · 2017: 69 · 2016: 31
FWCI
26.65
Type
journal article
Language
en
Open access
Locations
  • Scientific Reports (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Digital Access to Libraries (submittedVersion, other-oa)
  • Dipòsit Digital de la Universitat de Barcelona (Universitat de Barcelona) (submittedVersion, cc-by-nc-nd)
  • RECERCAT (Consorci de Serveis Universitaris de Catalunya) (submittedVersion, cc-by-nc-nd)
Funders
  • European Commission (267248)
  • Fonds De La Recherche Scientifique - FNRS (12/17-047, WELBIO-CR-2012S-02R, T.0138.14, 3.4579.11)
  • Generalitat de Catalunya (2014 SGR 659)
  • Fédération Wallonie-Bruxelles
  • Ministerio de Ciencia e Innovación
  • Walloon excellence in life sciences and biotechnology
  • Instituto de Salud Carlos III (PI13/01500, PI13/01604)
  • European Regional Development Fund
  • FP7 Ideas: European Research Council (336452)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
  • Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
Keywords
Akkermansia muciniphila, gut microbiota, diet-induced obesity, high-fat diet, adipose tissue inflammation, adipose tissue lipid metabolism, low-grade inflammation, Bilophila wadsworthia, metabolic disorders, insulin, leptin, triglycerides, age-related changes
MeSH terms
Gastrointestinal Microbiome, Adipose Tissue, Age Factors, Animals, Bacteria, Homeostasis, Inflammation, Male, Metabolic Diseases, Mice, Inbred C57BL, Obesity, RNA, Ribosomal, 16S, Species Specificity, Time Factors, Gene Expression, Reverse Transcriptase Polymerase Chain Reaction, Gastrointestinal Tract, Bilophila, Lipid Metabolism, Host-Pathogen Interactions, Bacterial Load, Diet, High-Fat, Verrucomicrobia

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