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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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“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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“GF mice that lack any exposure to living pathogenic or nonpathogenic microorganisms provide an attractive model to investigate the role of the composition and function of intestinal microbiota on the development of obesity (6).”
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“84, 85 Citizens of high-income countries have less diverse microbiota than do huntergatherers.”
Western diets, gut dysbiosis, and metabolic diseases: Are they linked?
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“Germ-free mice receiving FMT of lard-induced microbiota experiences more weight and had elevated macrophage-2 staining in white adipose tissue (WAT) than the mice receiving fish oil-induced microbiota, despite all mice being maintained on a lard diet for 3 weeks.(31)”
InfluentialInterplay between food and gut microbiota in health and disease
Danneskiold‐Samsøe, N. B., Barros, H. D. D. F. Q., dos Santos, R., Bicas, J. L., Cazarin, C. B. B., Madsen, L., Kristiansen, K., Pastore, G. M., Brix, S., & Maróstica, M. R. (2018) · Food Research International · doi:10.1016/j.foodres.2018.07.043 · Cited by 278
The Mouse Microbiome Is Required for Sex-Specific Diurnal Rhythms of Gene Expression and Metabolism
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The Role of Lipids in Parkinson’s Disease
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“The exposure of AT to LPS depends on the lipid content, the type of lipids in the diet, and the gut permeability to LPS((18)).”
InfluentialNon-alcoholic fatty liver and the gut microbiota
Bashiardes, S., Shapiro, H., Rozin, S., Shibolet, O., & Elinav, E. (2016) · Molecular Metabolism · doi:10.1016/j.molmet.2016.06.003 · Cited by 241
“Keywords NAFLD; NASH; Microbiome; Liver”
Gut Microbiota Metabolism and Interaction with Food Components
Vernocchi, P., CHIERICO, F. D., & Putignani, L. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21103688 · Cited by 242
Spiljar, M., Merkler, D., & Trajkovski, M. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01353 · Cited by 219
“This chemokine contributes to a microbiota-induced macrophage accumulation and WAT inflammation in lard-fed mice (40).”
Influence of Early Life, Diet, and the Environment on the Microbiome
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“For example, a recent study found that mice fed lard fat had a higher abundance of Bacteroides and Bilophila, whereas mice fed fish oil–derived fat had higher levels of Akkermansia and Lactobaccillus.71 The mice on a lard fat diet also had higher toll-like receptor activation and white adipose tissue inflammation, in…”
InfluentialRegulation of energy balance by a gut–brain axis and involvement of the gut microbiota
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Dietary fat and gut microbiota interactions determine diet-induced obesity in mice
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Gut Microbiota, Host Organism, and Diet Trialogue in Diabetes and Obesity
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“Moreover, lard-fed mice exhibited white adipose tissue inflammation and impaired insulin sensitivity compared to fish oil-fed mice (111).”
Gut-associated IgA+ immune cells regulate obesity-related insulin resistance
Luck, H., Khan, S. M., Kim, J. H., Copeland, J. K., Revelo, X. S., Tsai, S. J., Chakraborty, M., Cheng, K., Chan, Y. T., Nøhr, M. K., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-11370-y · Cited by 210
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Gut microbiota influences pathological angiogenesis in obesity‐driven choroidal neovascularization
Andriessen, E. M., Wilson, A. M., Mawambo, G., Dejda, A., Miloudi, K., Sennlaub, F., & Sapieha, P. (2016) · EMBO Molecular Medicine · doi:10.15252/emmm.201606531 · Cited by 201
“…provoke low-grade inflammation (Cani et al, 2008), insulin resistance (Cani et al, 2007), augmented cardiovascular risk (Manco et al, 2010), fatty liver disease (Brun et al, 2007), white adipose tissue inflammation (Caesar et al, 2015), and retinopathy of prematurity (ROP) (Tremblay et al, 2013).”
Gut microbiota and colorectal cancer
Gao, R., Gao, Z., Huang, L., & Qin, H. (2017) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-016-2881-8 · Cited by 205
“The crosstalk mechanism between dietary lipids and gut microbiota is based on the TLR signal pathway [116].”
Interaction between gut microbiota and toll-like receptor: from immunity to metabolism
Yiu, J. H. C., Dorweiler, B., & Woo, C. W. (2016) · Journal of Molecular Medicine · doi:10.1007/s00109-016-1474-4 · Cited by 202
Epigenetic Regulation at the Interplay Between Gut Microbiota and Host Metabolism
Miro-Blanch, J., & Yanes, O. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00638 · Cited by 195
On phagocytes and macular degeneration
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Gut microbiota bridges dietary nutrients and host immunity
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“Moreover, a lower dietary n-6/n-3 PUFA ratio decreases the expression of TLR4 in gastro-cnemius muscle in comparison with dietary SFAs (Liu et al., 2013).”
InfluentialWestern diets and chronic diseases
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Emerging Priorities for Microbiome Research
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“(2015) similarly reported little confidence in the estimated effects to recommend probiotic use for allergy prevention in children from 21 RCTs due to poor quality.”
Microbiome-Mediated Effects of the Mediterranean Diet on Inflammation
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“Acutely, both saturated fat and unsaturated fat facilitate LPS translocation; however, chronically, metabolic endotoxemia was more pronounced in the high-saturated fat group, which may be due to long-term changes in the GI microbiota including an increase of Akkermansia muciniphila, whichwas only enriched in the fish…”
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Diet and microbiota linked in health and disease
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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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