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Crosstalk between Gut Microbiota and Dietary Lipids Aggravates WAT Inflammation through TLR Signaling
Open accessAbstract
Dietary lipids may influence the abundance of circulating inflammatory microbial factors. Hence, inflammation in white adipose tissue (WAT) induced by dietary lipids may be partly dependent on their interaction with the gut microbiota. Here, we show that mice fed lard for 11 weeks have increased Toll-like receptor (TLR) activation and WAT inflammation and reduced insulin sensitivity compared with mice fed fish oil and that phenotypic differences between the dietary groups can be partly attributed to differences in microbiota composition. Trif(-/-) and Myd88(-/-) mice are protected against lard-induced WAT inflammation and impaired insulin sensitivity. Experiments in germ-free mice show that an interaction between gut microbiota and saturated lipids promotes WAT inflammation independent of adiposity. Finally, we demonstrate that the chemokine CCL2 contributes to microbiota-induced WAT inflammation in lard-fed mice. These results indicate that gut microbiota exacerbates metabolic inflammation through TLR signaling upon challenge with a diet rich in saturated lipids.
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In the citing paper
“Saturated and unsaturated fats have profoundly different effects on the gut microbiota, and the altered microbiota that results from feeding unsaturated fats can offer protection from lard-induced weight gain44.”
From Diet–microbiota interactions as moderators of human metabolism (2016) · cites this paper as [44]
In the citing paper
“germ-free mice that are fed a high-fat diet with less sucrose are only partly protected against obesity44”
From Diet–microbiota interactions as moderators of human metabolism (2016) · cites this paper as [44]
In the citing paper
“A switch to a diet rich in saturated fatty acids shifts the composition of the microbiota44.”
From Diet–microbiota interactions as moderators of human metabolism (2016) · cites this paper as [44]
In the citing paper
“Similarly, increased levels of Bilophila and a reduced abundance of Desulfovibrio were observed in mice that were fed lard compared with fish oil as a source of fat44.”
From Diet–microbiota interactions as moderators of human metabolism (2016) · cites this paper as [44]
In the citing paper
“Latest data implied that omega-3 PUFAs modulate the intestinal microbiota composition and help normalize it after disrupting environmental stress [166,168].”
From The Role of Microbiota-Gut-Brain Axis in Neuropsychiatric and Neurological Disorders (2021) · cites this paper as [168]
In the citing paper
“In a rodent study, animals fed lard showed increases in Bacteroides and displayed signs of metabolic dysfunction.”
From The athletic gut microbiota (2020) · cites this paper as [229]
In the citing paper
“In contrast, animals fed fish oil showed increased levels of lactic acid bacteria and were protected from metabolic dysfunction [229].”
From The athletic gut microbiota (2020) · cites this paper as [229]
In the citing paper
“The gut microbiota has been shown to differ between mice fed diets that are high or low in fat and between diets that contain equal amounts of fat but from different sources [10–13] (Fig. 1).”
From Dietary lipids, gut microbiota and lipid metabolism (2019) · cites this paper as [10]
In the citing paper
“In another study where mice fed a high-fat diet containing lard, rich in saturated fat, were compared to mice fed a isocaloric high-fat diet containing fish oil, rich in n-3 PUFA, it was found that phylogenetic diversity and abundance of the beneficial bacteria Akkermansia muciniphila, Lactobacillus and Bifidobacterium were lower in mice on a lard diet [10].”
From Dietary lipids, gut microbiota and lipid metabolism (2019) · cites this paper as [10]
In the citing paper
“Transplantation of cecum microbiota into germ-free (GF) mice showed that the diet-induced differences in host phenotype were partly caused by the gut microbiota.”
From Dietary lipids, gut microbiota and lipid metabolism (2019) · cites this paper as [10]
In the citing paper
“The lard diet also reduced insulin sensitivity and increased inflammation in white adipose tissue (WAT) through activation of Toll-like receptor 4 (TLR4) signaling.”
From Dietary lipids, gut microbiota and lipid metabolism (2019) · cites this paper as [10]
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Resveratrol-Induced White Adipose Tissue Browning in Obese Mice by Remodeling Fecal Microbiota
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“Louis, MI, USA) administered by oral gavage once a day for 3 days [56].”
Adhesive Bifidobacterium Induced Changes in Cecal Microbiome Alleviated Constipation in Mice
Wang, L., Chen, C., Cui, S., Lee, Y. K., Wang, G., Zhao, J., Zhang, H., & Chen, W. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.01721 · Cited by 65
“Constipation is related to the changes of gut microbiota, which may disturb cross-talk between the intestinal microflora, the intestinal endocrine system, the immune system and intestinal permeability (Caesar et al., 2015; Ge et al., 2017).”
Pal, A., Al‐Shaer, A. E., Guesdon, W., Torres, M. J., Armstrong, M., Quinn, K. D., Davis, T., Reisdorph, N. A., Neufer, P. D., Spangenburg, E. E., et al. (2020) · The FASEB Journal · doi:10.1096/fj.202000830r · Cited by 65
Dietary Regulation of Gut-Brain Axis in Alzheimer’s Disease: Importance of Microbiota Metabolites
Frausto, D. M., Forsyth, C. B., Keshavarzian, A., & Voigt, R. M. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.736814 · Cited by 61
“One particular study in mice, reports that consumption of fish-derived omega-3 PUFA increases the abundance of probiotic bacteria such as Actinobacteria (Bifidobacterium and Adlercreutzia), lactic acid-producing bacteria (Lactobacillus and Streptococcus), and Verrucomicrobia (Akkermansia muciniphila) (Caesar et al., 2…”
How poverty affects diet to shape the microbiota and chronic disease
Harrison, C. A., & TAREN, D. L. (2017) · Nature reviews. Immunology · doi:10.1038/nri.2017.121 · Cited by 65
Zhang, Y., Zhang, B., Dong, L., & Chang, P. (2018) · Advances in Nutrition · doi:10.1093/advances/nmy076 · Cited by 62
“, 2015 (71) C57BL/6 mice Experimental arm:”
InfluentialAnnavajhala, M. K., Khan, S. D., Sullivan, S. B., Shah, J., Pass, L., Kister, K., Kunen, H., Chiang, V., Monnot, G., Ricupero, C. L., et al. (2020) · mSphere · doi:10.1128/msphere.00798-19 · Cited by 62
Zhang, Q., Jin, K., Chen, B., Liu, R., Cheng, S., Zhang, Y., & Lü, J. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.884579 · Cited by 65
“For example, an HFD accompanied by intestinal microbiota, especially gut pathobionts, can trigger chronic inflammation; the latter contributes to metabolic alterations such as IR (Caesar et al., 2015; Dabke et al., 2019).”
Cuciniello, R., Meo, F. D., Filosa, S., Crispi, S., & Bergamo, P. (2023) · Antioxidants · doi:10.3390/antiox12051073 · Cited by 69
Heavy arch: from inflammatory bowel diseases to metabolic disorders
Adolph, T. E., Meyer, M., Jukic, A., & Tilg, H. (2024) · Gut · doi:10.1136/gutjnl-2024-331914 · Cited by 72
“56 Collectively, these studies indicated that patients with IBD are at risk for developing MASLD, which poses a risk for a poor patient outcome.”
Altered nutrient status reprograms host inflammation and metabolic health via gut microbiota
Golonka, R. M., Xiao, X., Abokor, A. A., Joe, B., & Vijay–Kumar, M. (2020) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2020.108360 · Cited by 60
“Along with an imbalance in macrophage and other immune cell subpopulations, cyclic guanosine monophosphate signaling is disrupted in inflamed WAT due to increased cytokine production (i.e. TNFα) from NF-κB signaling, further resulting in diminished adipogenesis [165].”
InfluentialMartinou, E., Stefanova, I., Iosif, E., & Angelidi, A. M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23063339 · Cited by 64
“The systemic increase in LPS and the subsequent activation of Toll-like receptor (TLR4) results in the synthesis of inflammatory cytokines, white adipose tissue inflammation, reduced insulin sensitivity and changes in the gut microbiota [381,382].”
Cano, R., Bermúdez, V., Galbán, N., Garrido, B., Santeliz, R., Gotera, M. P., Durán, P., Boscan, A., Carbonell, A., Durán‐Agüero, S., et al. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25169118 · Cited by 65
The microbiome-adipose tissue axis in systemic metabolism
Lundgren, P., & Thaiss, C. A. (2020) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00304.2019 · Cited by 62
Microbially produced vitamin B12 contributes to the lipid-lowering effect of silymarin
Sun, W., Hua, S., Li, X., Shen, L., Wu, H., & Ji, H. (2023) · Nature Communications · doi:10.1038/s41467-023-36079-x · Cited by 60
Krautkramer, K. A., Dhillon, R. S., Denu, J. M., & Carey, H. V. (2017) · Translational research · doi:10.1016/j.trsl.2017.08.005 · Cited by 61
Gut microbiota as the critical correlation of polycystic ovary syndrome and type 2 diabetes mellitus
Duan, L., An, X., Zhang, Y., Jin, D., Zhao, S., Zhou, R., Duan, Y., Zhang, Y., Liu, X., & Lian, F. (2021) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2021.112094 · Cited by 65
Are We What We Eat? Impact of Diet on the Gut–Brain Axis in Parkinson’s Disease
Alfonsetti, M., Castelli, V., & d’Angelo, M. (2022) · Nutrients · doi:10.3390/nu14020380 · Cited by 61
“There are no clinical studies demonstrating an alteration of gut microbiota upon high-unsaturated fat diets; however, in vivo studies (on mice) reported an increase in in Actinobacteria (Bifidobacterium and Adlercreutzia), lactic acid bacteria (Lactobacillus and Streptococcus), and Verrucomicrobia (Akkermansia mucinip…”
Cross-Talk Between Gut Microbiota and Adipose Tissues in Obesity and Related Metabolic Diseases
Wu, D., Wang, H., Xie, L., & Hu, F. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.908868 · Cited by 62
“Unsaturated lipids were reported to decrease body weight gain, increase Firmicutes to Bacteroidetes ratio and promote a healthier metabolic phenotype, while saturated lipids aggravate WAT inflammation and promote a higher degree of obesity, which is partly attributed to distinct gut microbiota richness and diversity (…”
Regulatory mechanisms of macrophage polarization in adipose tissue
Pan, D., Guo, L., Jiang, C., Hu, J., & Hu, X. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1149366 · Cited by 64
“In obese AT, fatty acid-binding Fetuin-A acts as an endogenous ligand of TLR4 to promote inflammation and IR (53).”
Diabetes-associated microbiota in fa/fa rats is modified by Roux-en-Y gastric bypass
Arora, T., Seyfried, F., Docherty, N. G., Tremaroli, V., le Roux, C. W., Perkins, R., & Bäckhed, F. (2017) · The ISME Journal · doi:10.1038/ismej.2017.70 · Cited by 60
“Quality-filtered 454 pyrosequencing and Illumina reads from both experiments were analyzed using the QIIME (Quantitative Insights Into Microbial Ecology) software package (Caporaso et al., 2010a; version 1.9.1) as described previously (Caesar et al., 2015).”
InfluentialSelf-citationSuratt, B. T., Ubags, N. D. J., Rastogi, D., Tantisira, K. G., Marsland, B. J., Petrache, I., Allen, J. B., Bates, J. H. T., Holguín, F., McCormack, M. C., et al. (2017) · Annals of the American Thoracic Society · doi:10.1513/annalsats.201703-263ws · Cited by 58
Targeting the gut microbiota by dietary nutrients: A new avenue for human health
Li, D., Wang, P., Wang, P., Hu, X., & Chen, F. (2017) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2017.1363708 · Cited by 60
“…and metabolites, which further pass through the intestinal epithelium and regulate the physiological functions of various organs of the host. polyunsaturated fatty acids) have increased abundance of beneficial bacteria such as Lactobacillus and Akkermansia muciniphila (Caesar et al., 2015).”
InfluentialShapiro, H., Suez, J., & Elinav, E. (2017) · Journal of Diabetes · doi:10.1111/1753-0407.12501 · Cited by 56
“The metabolic effect was transferrable to GF mice, whereas gut microbiota from fish-oil diet-fed mice given to lard-fed mice counteracted the metabolic phenotype, suggesting that diet has a major effect on microbial composition, which, in turn, modulates adipose tissue inflammation and adiposity.(81)”
Pharmacologic and Nonpharmacologic Therapies for the Gut Microbiota in Type 2 Diabetes
Caesar, R. (2019) · Canadian Journal of Diabetes · doi:10.1016/j.jcjd.2019.01.007 · Cited by 57
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“Mice fed saturated fats had an increased activation of TLR, which was at least partially mediated by gut microbiota, leading to white adipose tissue inflammation [76].”
Deficiency of essential dietary n-3 PUFA disrupts the caecal microbiome and metabolome in mice
Robertson, R., Oriach, C. S., Murphy, K., Moloney, G., Cryan, J., Dinan, T., Ross, R., & Stanton, C. (2017) · British Journal of Nutrition · doi:10.1017/s0007114517002999 · Cited by 50
“(11) have shown that a diet containing fi sh oil, rich in n -3 PUFA, reverses adipose tissue in fl ammation through toll-like receptor signalling, which is mediated through comprehensive changes in gut microbiota composition.”
Exploring the microbiome in health and disease
Scotti, E., Boué, S., Sasso, G. L., Zanetti, F., Belcastro, V., Poussin, C., Sierro, N., Battey, J. N. D., Gimalac, A., Ivanov, N. V., et al. (2017) · Toxicology Research and Application · doi:10.1177/2397847317741884 · Cited by 56
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Metadata
- Authors
- Caesar, R., Tremaroli, V., Kovatcheva-Datchary, P., Cani, P. D., & Bäckhed, F.
- Affiliations
- University of Gothenburg (SE)
- Walloon Excellence in Lifesciences and Biotechnology (BE)
- University of Copenhagen (DK)
- Corresponding author
- Caesar, Robert
- Bäckhed, Fredrik
- Venue
- Cell Metabolism
- Publisher
- Elsevier BV
- Published
- 2015-10
- Volume
- 22
- Issue
- 4
- Pages
- 658-668
- ISSN
- 1550-4131 (ISSN-L)
- PMC
- PMC4598654
- OpenAlex
- W2096736123
- Cited by
- 960
- References
- 51
- Citations by year
- 2026: 43 · 2025: 52 · 2024: 76 · 2023: 89 · 2022: 124 · 2021: 109 · 2020: 114 · 2019: 105 · 2018: 88 · 2017: 85 · 2016: 59 · 2015: 12
- FWCI
- 35.30
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Cell Metabolism (publishedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, cc-by-nc-nd)
- Digital Access to Libraries (submittedVersion, other-oa)
- Funders
- Stiftelsen för Strategisk Forskning
- Fonds De La Recherche Scientifique - FNRS (WELBIO-CR-2012S-02R)
- Knut och Alice Wallenbergs Stiftelse
- Novo Nordisk
- Vetenskapsrådet
- Göteborgs Universitet
- Novo Nordisk Fonden (NNF13OC0008163)
- Walloon excellence in life sciences and biotechnology
- Wageningen University and Research
- Uppsala Multidisciplinary Center for Advanced Computational Science
- FP7 Food, Agriculture and Fisheries, Biotechnology
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- gut microbiota, dietary fat, white adipose tissue inflammation, Toll-like receptor signaling, lard, fish oil, saturated fatty acids, insulin sensitivity, metabolic inflammation, CCL2 chemokine, MyD88, TRIF, germ-free mice
- MeSH terms
- Gastrointestinal Microbiome, Animals, Bacteria, Body Weight, DNA, Bacterial, Fish Oils, Inflammation, Male, Mice, Inbred C57BL, Phylogeny, Signal Transduction, Mice, Knockout, Chemokine CCL2, Adaptor Proteins, Vesicular Transport, Gastrointestinal Tract, Toll-Like Receptors, Mice, Adipose Tissue, White, Myeloid Differentiation Factor 88, Diet, High-Fat
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