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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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Innate Immune Signaling in Nonalcoholic Fatty Liver Disease and Cardiovascular Diseases
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Carco, C., Young, W., Gearry, R. B., Talley, N. J., McNabb, W. C., & Roy, N. C. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.00468 · Cited by 105
Gut Microbiota and Lifestyle Interventions in NAFLD
Houghton, D., Stewart, C. J., Day, C. P., & Trenell, M. I. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17040447 · Cited by 99
“Increased endotoxemia and inflammation in human [85–87] and animal studies [81,88–90] further suggests insulin resistance to be a key to the development of NAFLD and NASH [90,91].”
Nutrition, the visceral immune system, and the evolutionary origins of pathogenic obesity
West‐Eberhard, M. J. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1809046116 · Cited by 102
Fiber, Fat, and Colorectal Cancer: New Insight into Modifiable Dietary Risk Factors
Ocvirk, S., Wilson, A. S., Appolonia, C. N., Thomas, T. K., & O’Keefe, S. J. (2019) · Current Gastroenterology Reports · doi:10.1007/s11894-019-0725-2 · Cited by 104
Moossavi, S., Atakora, F., Miliku, K., Sepehri, S., Robertson, B., Duan, Q., Becker, A. B., Mandhane, P. J., Turvey, S. E., Moraes, T. J., et al. (2019) · Frontiers in Nutrition · doi:10.3389/fnut.2019.00058 · Cited by 105
“However, these correlations have not been examined while controlling for maternal fish oil supplement use, which modifies milk n3-PUFA concentrations (26) and might also influence microbiota (27).”
Wu, H., Ni, X., Xu, Q., Wang, Q., Li, X., & Hua, J. (2020) · Journal of Gastroenterology and Hepatology · doi:10.1111/jgh.15025 · Cited by 101
Herreweghen, F. V., den Abbeele, P. V., Mulder, T. D., Weirdt, R. D., Geirnaert, A., Hernandez‐Sanabria, E., Vilchez‐Vargas, R., Jáuregui, R., Pieper, D. H., Belzer, C., et al. (2016) · Beneficial Microbes · doi:10.3920/bm2016.0013 · Cited by 97
Rampelli, S., Guenther, K., Turroni, S., Wolters, M., Veidebaum, T., Kourides, Y. A., Molnár, D., Lissner, L., Benítez‐Páez, A., Sanz, Y., et al. (2018) · Communications Biology · doi:10.1038/s42003-018-0221-5 · Cited by 107
Diet Alters Entero-Mammary Signaling to Regulate the Breast Microbiome and Tumorigenesis
Soto‐Pantoja, D. R., Gaber, M. K., Arnone, A. A., Bronson, S. M., Cruz‐Diaz, N., Wilson, A. S., Clear, K. Y. J., Ramirez, M. U., Kucera, G. L., Levine, E. A., et al. (2021) · Cancer Research · doi:10.1158/0008-5472.can-20-2983 · Cited by 97
Versatile Triad Alliance: Bile Acid, Taurine and Microbiota
Duszka, K. (2022) · Cells · doi:10.3390/cells11152337 · Cited by 101
“High-saturated fat diet-triggered increase in BAs production may result in enriching for BAs-tolerant taxa in the families Ruminococcaceae and Lachnospiraceae, as well as the genera Bacteroides and Bilophila, that have previously been associated with host inflammation [120,212,214].”
Robertson, R. C., Kaliannan, K., Strain, C., Ross, R. P., Stanton, C., & Kang, J. X. (2018) · Microbiome · doi:10.1186/s40168-018-0476-6 · Cited by 96
“As has been reported previously, this inflammatory phenotype is induced by a disturbed microbiota [19, 44].”
Impact of a Healthy Dietary Pattern on Gut Microbiota and Systemic Inflammation in Humans
Telle‐Hansen, V. H., Holven, K. B., & Ulven, S. M. (2018) · Nutrients · doi:10.3390/nu10111783 · Cited by 102
“Fecal transplantation from mice given PUFA to those given SFA were sufficient to reverse inflammation [31].”
Shen, N., Caixàs, A., Ahlers, M., Patel, K., Gao, Z., Dutia, R., Blaser, M. J., Clemente, J. C., & Laferrère, B. (2019) · Surgery for Obesity and Related Diseases · doi:10.1016/j.soard.2019.05.038 · Cited by 94
“(Figure 2C) Akkermansia, via Toll-like receptors[8], may be a mediator of the ameliorated glucose metabolism and decreased inflammation after surgery.”
Gut microbiome interventions in human health and diseases
Nie, P., Li, Z., Wang, Y., Zhang, Y., Zhao, M., Luo, J., Du, S., Deng, Z., Chen, J., Wang, Y., et al. (2019) · Medicinal Research Reviews · doi:10.1002/med.21584 · Cited by 94
“Increased levels of circulating LPS in saturated fat‐fed mice activate TLR signaling and expression of the chemokine CCL2, which recruits macrophages and induces inflammation in WIT.167”
Fecal Microbial Transplantation and Its Potential Application in Cardiometabolic Syndrome
Leshem, A., Horesh, N., & Elinav, E. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01341 · Cited by 96
“These conflicting reports may stem from experimental differences in dietary macronutrients, namely fat/protein/fibers source and content (77, 84, 85).”
Wu, Y., Ma, N., Song, P., He, T., Levesque, C. L., Bai, Y., Zhang, A., & Ma, X. (2019) · Journal of Nutrition · doi:10.1093/jn/nxz102 · Cited by 94
“The bloom of Akkermansia that belongs to mucindegrading bacterium alleviates inflammation in the gut of rodents and improves metabolic health and protects the host against obesity (29, 30).”
Genetics of human longevity within an eco-evolutionary nature-nurture framework
Giuliani, C., Garagnani, P., & Franceschi, C. (2018) · Circulation Research · doi:10.1161/circresaha.118.312562 · Cited by 92
Interaction between dietary lipids and gut microbiota regulates hepatic cholesterol metabolism
Caesar, R., Nygrén, H., Orešič, M., & Bäckhed, F. (2016) · Journal of Lipid Research · doi:10.1194/jlr.m065847 · Cited by 94
Self-citationGut microbiome and lipid metabolism
Wang, Z., Koonen, D. P. Y., Hofker, M. H., & Fu, J. (2016) · Current Opinion in Lipidology · doi:10.1097/mol.0000000000000308 · Cited by 95
The Metabolic Role and Therapeutic Potential of the Microbiome
Olofsson, L. E., & Bäckhed, F. (2022) · Endocrine Reviews · doi:10.1210/endrev/bnac004 · Cited by 99
Self-citationToll-like receptors and metabolic (dysfunction)-associated fatty liver disease
Khanmohammadi, S., & Kuchay, M. S. (2022) · Pharmacological Research · doi:10.1016/j.phrs.2022.106507 · Cited by 95
Diet-induced gut dysbiosis and inflammation: Key drivers of obesity-driven NASH
Kang, G. G., Trevaskis, N. L., Murphy, A. J., & Febbraio, M. A. (2023) · iScience · doi:10.1016/j.isci.2022.105905 · Cited by 94
“Whereas fish oil-derived lipids reversed these effects by increasing Bifidobacterium—known to reduce LPS levels—favoring a nonobese and anti-inflammatory bacterial composition.(135) These findings demonstrate that”
Interactions Between Food and Gut Microbiota: Impact on Human Health
Wu, Y., Wan, J., Choe, U., Pham, Q., Schoene, N. W., He, Q., Li, B., Yu, L. L., & Wang, T. T. Y. (2019) · Annual Review of Food Science and Technology · doi:10.1146/annurev-food-032818-121303 · Cited by 96
Adipose Tissue Development and Expansion from the Womb to Adolescence: An Overview
Orsso, C. E., Colin-Ramírez, E., Field, C. J., Madsen, K. L., Prado, C. M. M., & Haqq, A. M. (2020) · Nutrients · doi:10.3390/nu12092735 · Cited by 103
The Impact of Diet on Immunity and Respiratory Diseases
Wypych, T. P., Marsland, B. J., & Ubags, N. D. J. (2017) · Annals of the American Thoracic Society · doi:10.1513/annalsats.201703-255aw · Cited by 91
Zhuang, P., Zhang, Y., Shou, Q., Li, H., Zhu, Y., He, L., Chen, J., & Jiao, J. (2020) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201900946 · Cited by 94
Nutrition Regulates Innate Immunity in Health and Disease
Nobs, S. P., Zmora, N., & Elinav, E. (2020) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-120919-094440 · Cited by 93
Li, Z., Hu, G.-A., Zhu, L., Sun, Z., Jiang, Y., Gao, M., & Zhan, X. (2021) · BMC Microbiology · doi:10.1186/s12866-021-02111-7 · Cited by 96
“12 acids[52] could increase the abundance of in vivo A.”
Griffin, C. A., Eter, L., Lanzetta, N., Abrishami, S., Varghese, M., McKernan, K. E., Muir, L. A., Lane, J., Lumeng, C. N.-K., & Singer, K. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra117.001526 · Cited by 88
“Whereas this direct effect of fatty acids on hematopoietic progenitors is novel, it is probably one of many factors altered with HFD, given that increased endotoxins (46) and microbiota changes have also been demonstrated to enhance ATM recruitment via TLR4 (47).”
Terzo, S., Mulè, F., Caldara, G., Baldassano, S., Puleio, R., Vitale, M., Cassata, G., Ferrantelli, V., & Amato, A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21010365 · Cited by 89
“The gut microbiota might induce inflammation in visceral adipose tissue via the LPS and TLR4 signaling pathways with an increased macrophage infiltration and release of a variety of pro-inflammatory mediators, which in turn recruit additional macrophages to further propagate the chronic inflammatory status [51,52].”
Immunological contributions to adipose tissue homeostasis
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Major shifts in gut microbiota during development and its relationship to growth in ostriches
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“A. muciniphila has also been negatively correlated with obesity, diabetes and in‐ flammatory gut diseases in mice and humans, as well as with body weight in chickens (Caesar et al., 2015; Derrien, Belzer, & de Vos, 2017; Everard et al., 2013; Han et al., 2016; Schneeberger et al., 2015).”
The role of the gut microbiome and diet in the pathogenesis of non-alcoholic fatty liver disease
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“Ingestion of longchained saturated fats, compared to short-chained unsaturated fats, are associated with a more pronounced reduction in phylogenetic diversity and beneficial bacteria.(102) The mechanisms by which dietary fatty acids affect the gut microbiome are not well defined.”
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“Recent studies have linked dysbiosis associated with a lard-based HFD to metabolic inflammation, whereby leaked gut microbial products stimulate adipocyte TLR4, MyD88, and TLR adaptor molecule 1 (TRIF) signaling, to facilitate CCL2-mediated immune cell inflammation in adipose tissue (40).”
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“The nature of the dietary fat also matters, since changes in gut microbiota induced by HFD differ depending on whether the fat is derived from lard versus fish oil (37).”
Sterilized bifidobacteria suppressed fat accumulation and blood glucose level
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Gut microbiome response to a modern Paleolithic diet in a Western lifestyle context
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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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