The Transplantation of ω3 PUFA–Altered Gut Microbiota of fat-1 Mice to Wild-Type Littermates Prevents Obesity and Associated Metabolic Disorders

Bidu, Célia; Escoula, Quentin; Bellenger, Sandrine; Spor, Aymé; Galan, Maxime; Geissler, Audrey; Bouchot, André; Dardevet, Dominique; Morio, Béatrice; Cani, Patrice D.; Lagrost, Laurent; Narce, Michel; Bellenger, Jérôme

doi:10.2337/db17-1488

Cited by 92Gut microbiota and healthFatty Acid Research and HealthDiet, Metabolism, and Disease

The Transplantation of ω3 PUFA–Altered Gut Microbiota of fat-1 Mice to Wild-Type Littermates Prevents Obesity and Associated Metabolic Disorders

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Bidu, Célia, Escoula, Quentin, Bellenger, Sandrine, Spor, Aymé, Galan, Maxime, Geissler, Audrey, Bouchot, André, Dardevet, Dominique +5 more·2018·Diabetes

DOI 10.2337/db17-1488

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Abstract

Altering the gut microbiome may be beneficial to the host and recently arose as a promising strategy to manage obesity. Here, we investigated the relative contribution of ω3 polyunsaturated fatty acid (PUFA)–mediated alterations in the microbiota to metabolic parameter changes in mice. Four groups were compared: male fat-1 transgenic mice (with constitutive production of ω3 PUFAs) and male wild-type (WT) littermates fed an obesogenic (high fat/high sucrose [HFHS]) or a control diet. Unlike WT mice, HFHS-fed fat-1 mice were protected against obesity, glucose intolerance, and hepatic steatosis. Unlike WT mice, fat-1 mice maintained a normal barrier function, resulting in a significantly lower metabolic endotoxemia. The fat-1 mice displayed greater phylogenic diversity in the cecum, and fecal microbiota transplantation from fat-1 to WT mice was able to reverse weight gain and to normalize glucose tolerance and intestinal permeability. We concluded that the ω3 PUFA–mediated alteration of gut microbiota contributed to the prevention of metabolic syndrome in fat-1 mice. It occurred independently of changes in the PUFA content of host tissues and may represent a promising strategy to prevent metabolic disease and preserve a lean phenotype.

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Transgenic mice that constitutively produce ω3 polyunsaturated fatty acids possess a microbiome with enhanced phylogenetic diversity that offers protection against metabolic consequences of a high-saturated-fat, high-sugar diet.
“transgenic mice that constitutively produce ω3 polyunsaturated fatty acids possess a microbiome with enhanced phylogenetic diversity that offers protection against the metabolic consequences of a high-saturated-fat, high-sugar diet (32).”
From The gut microbiota at the intersection of diet and human health (2018) · cites this paper as [32]
Lipid-mediated effects on the microbiota depend on lipid type and source.
“lipid-mediated effects on the microbiota are dependent on the lipid type and source.”
From The gut microbiota at the intersection of diet and human health (2018) · cites this paper as [32]

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Multi-omic analysis in transgenic mice implicates omega-6/omega-3 fatty acid imbalance as a risk factor for chronic disease
Kaliannan, K., Li, X., Wang, B., Pan, Q., Chen, C., Hao, L., Xie, S., & Kang, J. X. (2019) · Communications Biology · doi:10.1038/s42003-019-0521-4 · Cited by 88 · see citing works
Dietary Fish, Fish Nutrients, and Immune Function: A Review
Mendivil, C. O. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2020.617652 · Cited by 84 · see citing works
Regulation of Adaptive Thermogenesis and Browning by Prebiotics and Postbiotics
Reynés, B., Palou, M., Rodríguez, A. M., & Palou, A. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2018.01908 · Cited by 82 · see citing works
“In this model, the microbiota modulation by ω3 PUFA improves the metabolic profile of high fat (HF) diet fed mice which are protected against obesity, also maintaining a normal gut barrier function and with reduced metabolic endotoxemia (Bidu et al., 2018).”
BackgroundMethod
Omega-3 Fatty Acids and Adipose Tissue: Inflammation and Browning
Kalupahana, N. S., Goonapienuwala, B. L., & Moustaid-Moussa, N. (2020) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-122319-034142 · Cited by 72 · see citing works
Decreased ω-6:ω-3 PUFA ratio attenuates ethanol-induced alterations in intestinal homeostasis, microbiota, and liver injury
Warner, D. R., Warner, J. B., Hardesty, J., Song, Y., King, T. N., Kang, J. X., Chen, C., Xie, S., Yuan, F., Prodhan, M. A. I., et al. (2019) · Journal of Lipid Research · doi:10.1194/jlr.ra119000200 · Cited by 65 · see citing works
A high linoleic acid diet exacerbates metabolic responses and gut microbiota dysbiosis in obese rats with diabetes mellitus
Lee, H.-C., Yu, S.-C., Lo, Y.-C., Lin, I., Tung, T.-H., & Huang, S. (2019) · Food & Function · doi:10.1039/c8fo02423e · Cited by 64 · see citing works
N-3 polyunsaturated fatty acids: An innovative strategy against obesity and related metabolic disorders, intestinal alteration and gut microbiota dysbiosis
Bellenger, J., Bellenger, S., Escoula, Q., Bidu, C., & Narce, M. (2019) · Biochimie · doi:10.1016/j.biochi.2019.01.017 · Cited by 59 · see citing works
Self-citation
Beneficial Effects of Omega-3 Fatty Acids on Obesity and Related Metabolic and Chronic Inflammatory Diseases
Jerab, D., Blangero, F., da Costa, P. C. T., Alves, J. L. D. B., Kéfi, R., Jamoussi, H., Morio, B., & Eljaafari, A. (2025) · Nutrients · doi:10.3390/nu17071253 · Cited by 55 · see citing works
“Moreover, they also demonstrated that transplantation of their gut microbiota to wild-type mice prevented obesity and glucose intolerance, therefore suggesting that n -3 PUFAs may also reduce fat mass and insulin resistance by modulating the gut microbiota [37].”
Self-citation
The gut microbiota in retinal diseases
Bringer, M.-A., Gabrielle, P., Bron, A. M., Creuzot-Garcher, C. P., & Acar, N. (2021) · Experimental Eye Research · doi:10.1016/j.exer.2021.108867 · Cited by 51 · see citing works
Direct and indirect effects of lipids on microglia function
Leyrolle, Q., Layé, S., & Nadjar, A. (2019) · Neuroscience Letters · doi:10.1016/j.neulet.2019.134348 · Cited by 50 · see citing works
Improvement on metabolic syndrome in high fat diet-induced obese mice through modulation of gut microbiota by sangguayin decoction
Zheng, J., Zhang, J., Guo, Y., Cui, H., Lin, A., Hu, B., Gao, Q., Chen, Y., & Liu, H. (2019) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2019.112225 · Cited by 49 · see citing works
Effect of Dietary and Supplemental Omega‐3 Polyunsaturated Fatty Acids on Risk of Recurrent Gout Flares
Zhang, M., Zhang, Y., Terkeltaub, R. A., Chen, C. A., & Neogi, T. (2019) · Arthritis & Rheumatology · doi:10.1002/art.40896 · Cited by 47 · see citing works
The gut microbiome-prostate cancer crosstalk is modulated by dietary polyunsaturated long-chain fatty acids
Lachance, G., Robitaille, K., Laaraj, J., Gevariya, N., Varin, T. V., Feldiorean, A., Gaignier, F., Bourdeau‐Julien, I., Xu, H. W., Hallal, T., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-45332-w · Cited by 47 · see citing works
“Long-chain polyunsaturated fatty acids (PUFA), such as omega-3 fatty acids, were previously reported to cause whole-body metabolic changes that were dependent on gut microbiota 35,36 .”
Interactions Between Gut Microbiota and Acute Childhood Leukemia
Wen, Y., Jin, R., & Chen, H. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.01300 · Cited by 46 · see citing works
“…the postantibiotic gut microbiota both in human and murine was rebuilt to the initial state more quickly by autologous fecal microbiome transplantation (Suez et al., 2018), similarly to three other researches (Yan et al., 2016; Bidu et al., 2018; Smillie et al., 2018; Suez et al., 2018).”
Result
Into the wild: microbiome transplant studies need broader ecological reality
Greyson‐Gaito, C. J., Bartley, T., Cottenie, K., Jarvis, W. M. C., Newman, A. E. M., & Stothart, M. R. (2020) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2019.2834 · Cited by 42 · see citing works
Physical Exercise and Diet: Regulation of Gut Microbiota to Prevent and Treat Metabolic Disorders to Maintain Health
Zhang, L., Liu, Y., Xinzhou, W., & Zhang, X. (2023) · Nutrients · doi:10.3390/nu15061539 · Cited by 42 · see citing works
Gut Enterobacteriaceae and uraemic toxins - Perpetrators for ageing
Boopathi, S., Kumar, R. M. S., Priya, P. S., Haridevamuthu, B., Nayak, S. P. R. R., Chulenbayeva, L., Kushugulova, A. R., & Arockiaraj, J. (2023) · Experimental Gerontology · doi:10.1016/j.exger.2023.112088 · Cited by 40 · see citing works
Metabolic networks of the human gut microbiota
Selber‐Hnatiw, S., Sultana, T., Tse, W., Abdollahi, N., Abdullah, S., Rahbani, J. A., Alazar, D., Alrumhein, N. J., Aprikian, S., Arshad, R., et al. (2019) · Microbiology · doi:10.1099/mic.0.000853 · Cited by 37 · see citing works
Omega-3 Polyunsaturated Fatty Acids Prevent Toxoplasma gondii Infection by Inducing Autophagy via AMPK Activation
Choi, J.-W., Lee, J., Lee, J.-H., Park, B., Lee, E. J., Shin, S., Cha, G., Lee, Y., Lim, K., & Yuk, J. (2019) · Nutrients · doi:10.3390/nu11092137 · Cited by 33 · see citing works
Obesity and Its Multiple Clinical Implications between Inflammatory States and Gut Microbiotic Alterations
Milano, W., Carizzone, F., Foia, M. G., Marchese, M., Milano, M. F., Saetta, B., & Capasso, A. (2022) · Diseases · doi:10.3390/diseases11010007 · Cited by 34 · see citing works
STAT3 Signalling via the IL-6ST/gp130 Cytokine Receptor Promotes Epithelial Integrity and Intestinal Barrier Function during DSS-Induced Colitis
Pang, L., Huynh, J., Alorro, M., Li, X., Ernst, M., & Chand, A. L. (2021) · Biomedicines · doi:10.3390/biomedicines9020187 · Cited by 33 · see citing works
“Since Reg3 family antimicrobial peptides have been reported to shape the composition of the gut microbiota in metabolic diseases [44,45], our findings warrant further exploration into whether the modulation of STAT3 activity alters microbial communities in mouse models of IBD.”
Background
The adjuvant treatment role of ω-3 fatty acids by regulating gut microbiota positively in the acne vulgaris
Huang, Y., Liu, F., Lai, J., Jiang, S., Tan, X., Chen, L., Xu, Y., Xiong, X., & Deng, Y. (2024) · Journal of Dermatological Treatment · doi:10.1080/09546634.2023.2299107 · Cited by 32 · see citing works
“…(42), and play a role in the protection of the related metabolic disorders such as type 2 diabetes (43) and obesity (44) associated with unhealthy dietary habits (45), as well as decrease the level of proinflammatory mediators to reduce the occurrence of chronic low-grade inflammation (46).”
Docosahexaenoic and Eicosapentaenoic Acids Prevent Altered-Muc2 Secretion Induced by Palmitic Acid by Alleviating Endoplasmic Reticulum Stress in LS174T Goblet Cells
Escoula, Q., Bellenger, S., Narce, M., & Bellenger, J. (2019) · Nutrients · doi:10.3390/nu11092179 · Cited by 30 · see citing works
“Dietary n-3 PUFAs can notably maintain gut integrity by up-regulating the expression of tight junctions [6,30], improving the epithelial barrier function [31] and lowering permeability-induced inflammatory cytokines [32].”
BackgroundMethodInfluentialSelf-citation
Omega-3 Phospholipids from Krill Oil Enhance Intestinal Fatty Acid Oxidation More Effectively than Omega-3 Triacylglycerols in High-Fat Diet-Fed Obese Mice
Kroupova, P., van Schothorst, E. M., Keijer, J., Bunschoten, A., Vodička, M., Irodenko, I., Oseeva, M., Žáček, P., Kopecký, J., Rossmeisl, M., et al. (2020) · Nutrients · doi:10.3390/nu12072037 · Cited by 28 · see citing works
Beneficial effects of eicosapentaenoic acid on the metabolic profile of obese female mice entails upregulation of HEPEs and increased abundance of enteric Akkermansia muciniphila
Pal, A., Sun, S., Armstrong, M., Manke, J., Reisdorph, N., Adams, V. R., Kennedy, A. J., Zu, Y., Moustaïd‐Moussa, N., Carroll, I. M., et al. (2021) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2021.159059 · Cited by 24 · see citing works
n-3 polyunsaturated fatty acids in the regulation of adipose tissue browning and thermogenesis in obesity: Potential relationship with gut microbiota
Zapata, J. L., Gallardo, A., Romero, C., Valenzuela, R., Garcia-Diaz, D., Duarte-Silva, L., Bustamante, A., Gasaly, N., Gotteland, M., & Echeverría, F. (2021) · Prostaglandins Leukotrienes and Essential Fatty Acids · doi:10.1016/j.plefa.2021.102388 · Cited by 24 · see citing works
Integrated bioinformatics analysis reveals novel key biomarkers and potential candidate small molecule drugs in gestational diabetes mellitus
Alur, V. C., Raju, V., Vastrad, B. M., Tengli, A., Vastrad, C. M., & Kotrashetti, S. (2021) · Bioscience Reports · doi:10.1042/bsr20210617 · Cited by 23 · see citing works
Diet, gut microbiota, and health: a review
Zhang, L., TuoLiKen, H., Li, J., & Gao, H. (2024) · Food Science and Biotechnology · doi:10.1007/s10068-024-01759-x · Cited by 23 · see citing works
“Additionally, transgenic mice that consistently produce ω3 polyunsaturated fatty acids exhibited a microbiome with heightened phylogenetic diversity, which protected against the metabolic effects of a diet high in saturated fat and sugar (Bidu et al., 2018).”
Neonatal intake of Omega-3 fatty acids enhances lipid oxidation in adipocyte precursors
Varshney, R., Das, S., Trahan, G. D., Farriester, J. W., Mullen, G. P., Kyere-Davies, G., Presby, D. M., Houck, J. A., Webb, P. G., Dzieciątkowska, M., et al. (2022) · iScience · doi:10.1016/j.isci.2022.105750 · Cited by 19 · see citing works
“Others have identified n3 PUFA as mediators of improved microbiome diversity that, when transplanted into naive hosts, protects against diet-induced obesity and metabolic dysfunction.(81) Altogether, numerous n6-and n3-derived bioactive lipids within neonatal circulation likely act together to establish a metabolic ph…”
Background
Effect of Atkins versus a low-fat diet on gut microbiota, and cardiometabolic markers in obese women following an energy-restricted diet: Randomized, crossover trial
Tehrani, L. H.-G., Mousavi, S. N., Chiti, H., & Afshar, D. (2022) · Nutrition Metabolism and Cardiovascular Diseases · doi:10.1016/j.numecd.2022.04.007 · Cited by 19 · see citing works
Maternal Fat-1 Transgene Protects Offspring from Excess Weight Gain, Oxidative Stress, and Reduced Fatty Acid Oxidation in Response to High-Fat Diet
Boyle, K. E., Magill-Collins, M., Newsom, S. A., Janssen, R. C., & Friedman, J. E. (2020) · Nutrients · doi:10.3390/nu12030767 · Cited by 17 · see citing works
Human periodontitis-associated salivary microbiome affects the immune response of diabetic mice
He, J., Shen, X., Fu, D., Yang, Y., Xiong, K., Жао, Л., Xie, H., Pelekos, G., & Li, Y. (2022) · Journal of Oral Microbiology · doi:10.1080/20002297.2022.2107814 · Cited by 16 · see citing works
Egg oil from Portunus trituberculatus alleviated obesity and regulated gut microbiota in mice
Hu, S., Yang, H., Gao, X., Li, S., Jiang, W., & Liu, Y. (2020) · Scientific Reports · doi:10.1038/s41598-020-65199-3 · Cited by 17 · see citing works
Decreased Tissue Omega-6/Omega-3 Fatty Acid Ratio Prevents Chemotherapy-Induced Gastrointestinal Toxicity Associated with Alterations of Gut Microbiome
Kaliannan, K., Donnell, S. O., Murphy, K., Stanton, C., Kang, C., Wang, B., Li, X., Bhan, A. K., & Kang, J. X. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23105332 · Cited by 17 · see citing works
Sandalwood seed oil improves insulin sensitivity in high-fat/high-sucrose diet-fed rats associated with altered intestinal microbiota and its metabolites
Gao, X., Zhang, H., Li, K., Shi, Y., Guo, X., Wang, L., & Li, D. (2021) · Food & Function · doi:10.1039/d1fo02239c · Cited by 16 · see citing works
The transplantation of the gut microbiome of fat-1 mice protects against colonic mucus layer disruption and endoplasmic reticulum stress induced by high fat diet
Bourragat, A., Escoula, Q., Bellenger, S., Zemb, O., Beaumont, M., Chaumonnot, K., Farine, J., Jacotot, E., Bonnotte, A., Avoscan, L., et al. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2356270 · Cited by 16 · see citing works
“32,39 To determine whether the gut microbiome of omega-3 PUFAs-enriched mice may improve obesity-related traits in HFD-fed mice, the cecal microbiome of fat-1 mice was transferred to WT mice fed a CTL or HFD without any prior antibiotic treatment.”
MethodResultSelf-citation
Comparative Analyses of Scylla olivacea Gut Microbiota Composition and Function Suggest the Capacity for Polyunsaturated Fatty Acid Biosynthesis
Lau, N., Ting, S. Y., Sam, K., Janaranjani, M., Wong, S. C., Wu, X., Waiho, K., Fazhan, H., & Shu‐Chien, A. C. (2022) · Microbial Ecology · doi:10.1007/s00248-022-02046-0 · Cited by 16 · see citing works
Dual expression of transgenic delta-5 and delta-6 desaturase in tilapia alters gut microbiota and enhances resistance to Vibrio vulnificus infection
Chiang, K.-Y., Lin, W., Tsai, T.-Y., Lin, C., Huang, S.-J., Huang, C., Wu, S.-H., Ken, C., Gong, H., Chen, J., et al. (2020) · PLoS ONE · doi:10.1371/journal.pone.0236601 · Cited by 14 · see citing works
Comparing Transgenic Production to Supplementation of ω-3 PUFA Reveals Distinct But Overlapping Mechanisms Underlying Protection Against Metabolic and Hepatic Disorders
Daniel, N., Barz, M. L., Mitchell, P. L., Varin, T. V., Bourdeau‐Julien, I., Farabos, D., Pilon, G., Gauthier, J., Garofalo, C., Kang, J. X., et al. (2022) · Function · doi:10.1093/function/zqac069 · Cited by 14 · see citing works
Dietary Patterns, Gut Microbiota Remodeling, and Cardiometabolic Disease
Guiducci, L., Nicolini, G., & Forini, F. (2023) · Metabolites · doi:10.3390/metabo13060760 · Cited by 12 · see citing works
Effect of Dietary Supplementation with Omega-3 Fatty Acid on the Generation of Regulatory T Lymphocytes and on Antioxidant Parameters and Markers of Oxidative Stress in the Liver Tissue of IL−10 Knockout Mice
Campanari, D. D., Cipriano, U. G., Fraga‐Silva, T. F. D. C., Ramalho, L. N. Z., Ovídio, P. P., Júnior, A. A. J., Bonato, V. L. D., & Ferriolli, E. (2024) · Nutrients · doi:10.3390/nu16050634 · Cited by 10 · see citing works
“It is worth mentioning that the duration and amount of lipids added to the diet of supplemented animals may explain differences between the animals’ weight gain in relation to previous studies, since when there is an increase in the amount of lipids, animals tend to gain weight [33,34].”
Result
The endoplasmic reticulum stress protein GRP94 modulates cathepsin L activity in M2 macrophages in conditions of obesity-associated inflammation and contributes to their pro-inflammatory profile
Wang, F., Baverel, V., Chaumonnot, K., Bourragat, A., Bellenger, J., Bellenger, S., Zhou, W., Narce, M., Garrido, C., & Kohli, É. (2024) · International Journal of Obesity · doi:10.1038/s41366-024-01478-7 · Cited by 9 · see citing works
Self-citation
The relationship between n-3 polyunsaturated fatty acids and telomere: A review on proposed nutritional treatment against metabolic syndrome and potential signaling pathways
Wu, Y., Zhang, Y., & Jiao, J. (2022) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2022.2142196 · Cited by 8 · see citing works
“Fat-1 transgenic mice fed with a high fat and high sucrose diet are protected against obesity, hepatic steatosis, and glucose intolerance compared to wide type mice, and results remain consistent when fecal microbiota is transplanted from fat-1 to wide type mice (Bidu et al. 2018).”
Background
Resolvin E1 Derived from Eicosapentaenoic Acid Prevents Hyperinsulinemia and Hyperglycemia in a Host Genetic Manner
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) · Digital Commons - University of South Florida (University of South Florida) · Cited by 8 · see citing works
Effects of increasing n3:n6 ratio by replacing extruded soybeans with extruded flaxseed on dry matter intake, rumen fluid bacteria, and liver lipid metabolism in transition cows
Liu, X., Zhang, X., He, Q., Sun, X., Wang, W., & Li, S. (2025) · BMC Microbiology · doi:10.1186/s12866-024-03733-3 · Cited by 7 · see citing works
“By increasing n-3/n-6 PUFA ratios in the diet, gram-negative Enterobacteriaceae growth can be reduced, Bifidobacterium and Akker-mansia growth can be improved, and lipopolysaccharide (LPS) production can be reduced, thereby preventing gut barrier inflammation [16, 17].”
Maternal Linoleic Acid Overconsumption Alters Offspring Gut and Adipose Tissue Homeostasis in Young but Not Older Adult Rats
Marchix, J., Alain, C., Gall‐David, S. L., Acuña-Amador, L., Druart, C., Delzenne, N. M., Barloy-Hubler, F., Legrand, P., & Boudry, G. (2020) · Nutrients · doi:10.3390/nu12113451 · Cited by 7 · see citing works
16S rRNA and transcriptome analysis of the FOS-mediated alleviation of Aeromonas hydrophila-induced intestinal damage in Megalobrama amblycephala
Jiang, D., Li, S., Liang, Y., Xu, R., Qi, Q., Wang, B., & Zhang, C. (2023) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2023.127040 · Cited by 7 · see citing works
Ileum Gene Expression in Response to Acute Systemic Inflammation in Mice Chronically Fed Ethanol: Beneficial Effects of Elevated Tissue n-3 PUFAs
Hardesty, J., Warner, J. B., Song, Y., Rouchka, E. C., McClain, C. J., Warner, D. R., & Kirpich, I. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22041582 · Cited by 7 · see citing works
“Similarly, transgenic mice that endogenously produce n-3 PUFAs from n6 PUFAs (fat-1 mice [5]) have reduced intestinal permeability when fed a hypercaloric diet [6] and are also protected from colitis [7].”
Background
Intestinal microbiota mediates the beneficial effects of n-3 polyunsaturated fatty acids during dietary obesity,
Bellenger, J., Bellenger, S., Bourragat, A., Escoula, Q., Weill, P., & Narce, M. (2021) · OCL · doi:10.1051/ocl/2021006 · Cited by 7 · see citing works
Self-citation
Omega-3 polyunsaturated fatty acids and gut microbiota
Hull, M. A., & Sun, H. (2025) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0000000000001176 · Cited by 4 · see citing works
Heterogeneity in the response to n-3 polyunsaturated fatty acids
Shaikh, S. R., & Bazinet, R. P. (2023) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0000000000000930 · Cited by 4 · see citing works
“There is compelling evidence that long-chain n-3 PUFAs specifically control the composition and function of the gut microbiome of rodents and humans [11,12].”
Background
Microbial Community and Metabolome Analysis of the Porcine Intestinal Damage Model Induced by the IPEC-J2 Cell Culture-Adapted Porcine Deltacoronavirus (PDCoV) Infection
Shi, Y., Li, B., Cheng, J., Tao, J., Tang, P., Jiao, J., & Liu, H. (2024) · Microorganisms · doi:10.3390/microorganisms12050874 · Cited by 3 · see citing works
“Any damage to these barriers can facilitate the entry of bacteria or viruses into the host’s body, enabling their passage into the bloodstream and ultimately leading to systemic damage [21].”
Background
The gut microbiota improves reproductive dysfunction in obese mice by suppressing the NLRP3/ASC/caspase-1 axis
Huang, H., Zhou, T., He, F., Wen, B., Yang, Y., Zhong, W., Wang, Q., & Li, . (2024) · Future Microbiology · doi:10.1080/17460913.2024.2386867 · Cited by 4 · see citing works
Do Endogenously Produced and Dietary ω-3 Fatty Acids Act Differently?
Calder, P. C. (2023) · Function · doi:10.1093/function/zqad009 · Cited by 3 · see citing works
Increased Akkermansia abundance is associated with increased colonic mucosal ω-3 fatty acids and decreased colonic mucosal PGE 2 concentrations following healthy dietary pattern interventionsPreprint
Rifkin, S. B., Sen, A., Turgeon, D. K., Chan, R., Ruffin, M. T., Brenner, D. E., Schloss, P. D., & Djurić, Z. (2021) · medRxiv · doi:10.1101/2021.10.11.21264748 · Cited by 3 · see citing works
Generation of Codon-Optimized Fad3 Gene Transgenic Bovine That Produce More n-3 Polyunsaturated Fatty Acids
Su, G., Wei, Z., Bai, C., Li, D., Zhao, X., Liu, X., Song, L., Zhang, L., Li, G., & Yang, L. (2025) · Animals · doi:10.3390/ani15010093 · Cited by 2 · see citing works
Fructose malabsorption induces dysbiosis and increases anxiety in male human and animal models
Coursan, A., Polve, D., Leroi, A., Monnoye, M., Roussin, L., Benatar, C., Tavolacci, M., Quillard‐Muraine, M., Maccarone, M., Guérin, O., et al. (2025) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2025.106221 · Cited by 3 · see citing works
Self-citation
Effet des acides gras polyinsaturés oméga-3 sur le tissu adipeux blanc
Brun, A., Pinel, A., & Capel, F. (2024) · Cahiers de Nutrition et de Diététique · doi:10.1016/j.cnd.2024.05.004 · Cited by 1 · see citing works
Anti-Obesogenic Effects of Culinary Herbs Through Modulation of Inflammation and Metabolic Pathways
Winiarska‐Mieczan, A., Tomczyk‐Warunek, A., Jachimowicz-Rogowska, K., Kwiecień, M., Czernecki, T., Lis, M., & Kazimierczak, W. (2026) · Nutrients · doi:10.3390/nu18060993 · Cited by 1 · see citing works
“…PUFAs enhance intestinal alkaline phosphatase production and secretion, which induces changes in the gut bacterial composition that reduce lipopolysaccharide production and intestinal permeability, thereby lowering metabolic endotoxaemia and inflammation, as demonstrated in mice studies [111].”
Impact of fecal microbiota transplantation on lipid parameters in patients with metabolic syndrome: a meta-analysis
Wang, L., Liu, Z. H., Fan, F., Zhang, L., & Li, J. (2026) · BMC Gastroenterology · doi:10.1186/s12876-026-05037-4 · Cited by 1 · see citing works
Dietary Fatty Acids, Gut Microbiome, and Gut–Brain Communication: A Current Perspective
Anand, S. K., Sukrutha, S. K., Shilpa, B. R., & Nagarathna, A. (2022) · Nutritional neurosciences · doi:10.1007/978-981-19-4530-4_8 · Cited by 1 · see citing works
Effect of feeding a dried distillers’ grains with solubles diet on the metabolism of the intestinal wall in Guanling crossbred cattle: a preliminary assessment
Luo, X., Zhang, T., Xu, D., Zhu, M., Zhang, J., Zhang, R., He, G., Chen, Z., Mei, S., BiJun, Z., et al. (2024) · Frontiers in Veterinary Science · doi:10.3389/fvets.2023.1223088 · Cited by 1 · see citing works
Liver disease
McClain, C. J., Smart, L., Safadi, S., & Kirpich, I. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-818460-8.00026-5 · Cited by 1 · see citing works
Eicosapentaenoic Acid Prevents Obesity‐induced Metabolic Impairments through The Host‐genetic Dependent Effects of Resolvin E1
Pal, A., Al‐Shaer, A. E., Guesdon, W., Torres, M. J., Armstrong, M., Quinn, K. D., Reisdorph, N. A., Neufer, P. D., & Shaikh, S. R. (2020) · The FASEB Journal · doi:10.1096/fasebj.2020.34.s1.09373 · Cited by 1 · see citing works
Introduction to the International Symposium on Lipid Science and Health and research progress in lipid science and health
Wei, F., Zheng, M., Deng, Q., Wan, X., Xu, J., Gong, Y., Chen, H., & Huang, F. (2021) · Oil Crop Science · doi:10.1016/j.ocsci.2021.09.002
Multi-Omics Analysis to the Alleviation of Aeromonas Hydrophila-Induced Intestinal-Barrier Damage by the Application of Fos in Megalobrama AmblycephalaPreprint
Jiang, D., Li, S., Liang, Y., Xu, R., qi, Q., & Zhang, C. (2022) · SSRN Electronic Journal · doi:10.2139/ssrn.4177782
EPA and Mixed Omega-3 Fatty Acids: Impact on Dyslipidemia and Cardiovascular Events in Patients with Diabetes
Ganda, O. P., Busch, R. S., Nelson, J. R., & Philip, S. (2023) · Contemporary diabetes · doi:10.1007/978-3-031-26681-2_25
Additional file 4 of Eicosapentaenoic and docosahexaenoic acids attenuate hyperglycemia through the microbiome-gut-organs axis in db/db mice
Zhuang, P., Li, H., Jia, W. P., Shou, Q., Zhu, Y., Mao, L., Wang, W., Wu, F. H., Chen, X., Wan, X., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16606932
Additional file 5 of Eicosapentaenoic and docosahexaenoic acids attenuate hyperglycemia through the microbiome-gut-organs axis in db/db mice
Zhuang, P., Li, H., Jia, W. P., Shou, Q., Zhu, Y., Mao, L., Wang, W., Wu, F. H., Chen, X., Wan, X., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16606935
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“” Baseline characteristics (#2) were clearly described in nine studies (Hsu et al. 2020; Asano et al. 2020; Barouei et al. 2017; Bidu et al. 2018; Du Preez et al. 2019; Durand et al. 2020; Horne et al. 2020; Kumar et al. 2016; Yang et al. 2019), earning a “ LOW ” risk of bias grade, with the…”
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Additional file 2 of Eicosapentaenoic and docosahexaenoic acids attenuate hyperglycemia through the microbiome-gut-organs axis in db/db mice
Zhuang, P., Li, H., Jia, W., Shou, Q., Zhu, Y., Mao, L., Wang, W., Wu, F., Chen, X., Wan, X., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16606926
Additional file 3 of Eicosapentaenoic and docosahexaenoic acids attenuate hyperglycemia through the microbiome-gut-organs axis in db/db mice
Zhuang, P., Li, H., Jia, W., Shou, Q., Zhu, Y., Mao, L., Wang, W., Wu, F., Chen, X., Wan, X., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16606929
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Intestinal microbiota mediates the beneficial effects of n-3 polyunsaturated fatty acids during dietary obesity,
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The transplantation of the gut microbiome of fat-1 mice protects against colonic mucus layer disruption and endoplasmic reticulum stress induced by high fat diet
Bourragat, A., Escoula, Q., Bellenger, S., Zemb, O., Beaumont, M., Chaumonnot, K., Farine, J., Jacotot, E., Bonnotte, A., Avoscan, L., et al. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2356270 · Cited by 16 · see citing works
Self-citation

Authors: Bidu, C., Escoula, Q., Bellenger, S., Spor, A., Galan, M., Geissler, A., Bouchot, A., Dardevet, D., Morio, B., Cani, P. D., Lagrost, L., Narce, M., & Bellenger, J.
Affiliations: Inserm (FR)
Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR)
Centre de Coopération Internationale en Recherche Agronomique pour le Développement (FR)
Université de Bourgogne (FR)
Université Clermont Auvergne (FR)
Lyon 1 Université (FR)
Walloon Excellence in Lifesciences and Biotechnology (BE)
Corresponding author: Narce, Michel
ORCID: Bellenger, Sandrine
Spor, Aymé
Galan, Maxime
Dardevet, Dominique
Morio, Béatrice
Cani, Patrice D.
Lagrost, Laurent
Narce, Michel
Bellenger, Jérôme
Venue: Diabetes
Publisher: American Diabetes Association
Published: 2018-05-23
Volume: 67
Issue: 8
Pages: 1512-1523
ISSN: 0012-1797 (ISSN-L)
1939-327X
DOI: 10.2337/db17-1488
OpenAlex: W2803278092
Cited by: 90
References: 57
Citations by year: 2026: 3 · 2025: 9 · 2024: 10 · 2023: 11 · 2022: 10 · 2021: 14 · 2020: 14 · 2019: 16 · 2018: 3
FWCI: 4.35
Type: journal article
Language: en
Update notices: correction (2019-01-01)
Open access: green
hdl.handle.net
Licence: other-oa
www.diabetesjournals.org/content/license (vor, 58 d)
Locations: Diabetes (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion)
Digital Access to Libraries (Université catholique de Louvain (UCL), l'Université de Namur (UNamur) and the Université Saint-Louis (USL-B)) (submittedVersion, other-oa)
Funders: Agence Nationale de la Recherche (ANR-11-LABX-0021)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Health Sciences › Nursing › Nutrition and Dietetics › Fatty Acid Research and Health
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diet, Metabolism, and Disease
Keywords: omega-3 polyunsaturated fatty acids, fat-1 transgenic mice, gut microbiota, fecal microbiota transplantation, obesity prevention, metabolic syndrome, impaired glucose tolerance, hepatic steatosis, intestinal permeability, endotoxemia, high-fat high-sugar diet, host-microbiota interactions
MeSH terms: Gastrointestinal Microbiome, Fecal Microbiota Transplantation, Diet, Carbohydrate Loading, Animals, Insulin Resistance, Intestinal Mucosa, Intestines, Liver, Male, Mice, Transgenic, Obesity, Permeability, Phylogeny, Fatty Acids, Omega-3, Cadherins, Glucose Intolerance, Muscle, Skeletal, Dietary Sucrose, Endotoxemia, Diet, High-Fat, Dysbiosis, Non-alcoholic Fatty Liver Disease

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The Transplantation of ω3 PUFA–Altered Gut Microbiota of fat-1 Mice to Wild-Type Littermates Prevents Obesity and Associated Metabolic Disorders

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