The DOI matches its Crossref record; 267 of the 267 references it cites were found in a registry or an index.
The intestinal microbiota fuelling metabolic inflammation
Abstract
Low-grade inflammation is the hallmark of metabolic disorders such as obesity, type 2 diabetes and nonalcoholic fatty liver disease. Emerging evidence indicates that these disorders are characterized by alterations in the intestinal microbiota composition and its metabolites, which translocate from the gut across a disrupted intestinal barrier to affect various metabolic organs, such as the liver and adipose tissue, thereby contributing to metabolic inflammation. Here, we discuss some of the recently identified mechanisms that showcase the role of the intestinal microbiota and barrier dysfunction in metabolic inflammation. We propose a concept by which the gut microbiota fuels metabolic inflammation and dysregulation.
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“Growing evidence shows that gut microbiome-derived metabolites can reach systemic circulation through the gut barrier and fuel metabolic inflammation.179”
From Interaction between microbiota and immunity in health and disease (2020) · cites this paper as [179]
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Items 201–267 of 267
Wang, Y., Liu, Y., Sidhu, A., Ma, Z., McClain, C. J., & Feng, W. (2012) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00024.2012 · Cited by 238
Muramyl Dipeptide-Based Postbiotics Mitigate Obesity-Induced Insulin Resistance via IRF4
Cavallari, J. F., Fullerton, M. D., Duggan, B. M., Foley, K. P., Denou, E., Smith, B. K., Desjardins, E. M., Henriksbo, B. D., Kim, K. J., Tuinema, B. R., et al. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.03.021 · Cited by 237
Tang, W. H. W., Wang, Z., Li, X. S., Fan, Y., Li, D. S., Wu, Y., & Hazen, S. L. (2016) · Clinical Chemistry · doi:10.1373/clinchem.2016.263640 · Cited by 234
Fabbiano, S., Suárez-Zamorano, N., Chevalier, C., Lazarević, V., Kieser, S., Rigo, D., Léo, S., Veyrat‐Durebex, C., Gaïa, N., Maresca, M., et al. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.08.005 · Cited by 233
Seganfredo, F. B., Blume, C. A., Moehlecke, M., Giongo, A., Casagrande, D. S., Spolidoro, J. V. N., Padoin, A. V., Schaan, B. D., & Mottin, C. C. (2017) · Obesity Reviews · doi:10.1111/obr.12541 · Cited by 228
Martínez-López, M., Iborra, S., Conde-Garrosa, R., Mastrangelo, A., Danne, C., Mann, E. R., Reid, D. M., Gaboriau-Routhiau, V., Chaparro, M., Lorenzo, M. P., et al. (2019) · Immunity · doi:10.1016/j.immuni.2018.12.020 · Cited by 228
Suzuki, T., & Hara, H. (2010) · Nutrition & Metabolism · doi:10.1186/1743-7075-7-19 · Cited by 224
Amar, J., Lange, C., Payros, G., Garret, C., Chabo, C., Lantieri, O., Courtney, M., Marre, M., Charles, M.-A. A., Balkau, B., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0054461 · Cited by 222
Association between microbiota-dependent metabolite trimethylamine-N-oxide and type 2 diabetes
Shan, Z., Sun, T., Huang, H., Chen, S., Chen, L., Luo, C., Yang, W., Yang, X., Yao, P., Cheng, J., et al. (2017) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.117.157107 · Cited by 210
Geng, L., Liao, B., Jin, L., Huang, Z. P., Triggle, C. R., Ding, H., Zhang, J., Huang, Y., Lin, Z., & Xu, A. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.02.014 · Cited by 208
Ye, D., Li, F. Y. L., Lam, K. S. L., Li, H., Jia, W., Wang, Y., Man, K., Lo, C. M., Li, X., & Xu, A. (2012) · Gut · doi:10.1136/gutjnl-2011-300269 · Cited by 206
Genser, L., Aguanno, D., Soula, H. A., Dong, L., Barbot-Trystram, L., Assmann, K. E., Salem, J., Vaillant, J., Oppert, J., Laugerette, F., et al. (2018) · The Journal of Pathology · doi:10.1002/path.5134 · Cited by 202
High-fat-induced intestinal permeability dysfunction associated with altered fecal bile acids
Stenman, L. K. (2012) · World Journal of Gastroenterology · doi:10.3748/wjg.v18.i9.923 · Cited by 201
Park, S. H., Kim, B. I., Yun, J. W., Kim, J. W., Park, D. I., Cho, Y. K., Sung, I. K., Park, C. Y., Sohn, C. I., Jeon, W. K., et al. (2004) · Journal of Gastroenterology and Hepatology · doi:10.1111/j.1440-1746.2004.03362.x · Cited by 201
Teixeira, T. F. S., Souza, N. C., Chiarello, P. G., Franceschini, S. C. C., Bressan, J., Ferreira, C. L. D. L. F., & Pelúzio, M. D. C. G. (2012) · Clinical Nutrition · doi:10.1016/j.clnu.2012.02.009 · Cited by 200
Syed, I., Lee, J., Moraes‐Vieira, P. M., Donaldson, C. J., Sontheimer-Phelps, A., Aryal, P., Wellenstein, K., Kolar, M. J., Nelson, A. T., Siegel, D. R., et al. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.01.001 · Cited by 200
Denou, E., Lolmède, K., Garidou, L., Pomié, C., Chabo, C., Lau, T. C., Fullerton, M. D., Nigro, G., Zakaroff‐Girard, A., Luche, É., et al. (2015) · EMBO Molecular Medicine · doi:10.15252/emmm.201404169 · Cited by 197
Damms-Machado, A., Louis, S., Schnitzer, A., Volynets, V., Rings, A., Basrai, M., & Bischoff, S. C. (2017) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.116.131110 · Cited by 195
Ahuja, M., Schwartz, D. M., Tandon, M., Son, A., Zeng, M., Swaim, W., Eckhaus, M., Hoffman, V., Cui, Y., Xiao, B., et al. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.02.007 · Cited by 195
Leite, A. Z., Rodrigues, N. D. C., Gonzaga, M. I., Paiolo, J. C. C., de Souza, C. A., Stefanutto, N. A. V., Omori, W. P., Pinheiro, D. G., Brisotti, J. L., Matheucci, E., et al. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01107 · Cited by 192
Giorgio, V., Miele, L., Principessa, L., Ferretti, F., Villa, M. P., Negro, V., Grieco, A., Alisi, A., & Nobili, V. (2014) · Digestive and Liver Disease · doi:10.1016/j.dld.2014.02.010 · Cited by 188
Sellmann, C., Priebs, J., Landmann, M., Degen, C., Engstler, A. J., Jin, C. J., Gärttner, S., Spruss, A., Huber, O., & Bergheim, I. (2015) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2015.05.011 · Cited by 188
Fatkhullina, A. R., Peshkova, I. O., Dzutsev, A., Aghayev, T., McCulloch, J. A., Thovarai, V., Badger, J. H., Vats, R., Sundd, P., Tang, H., et al. (2018) · Immunity · doi:10.1016/j.immuni.2018.09.011 · Cited by 186
Jejunal T Cell Inflammation in Human Obesity Correlates with Decreased Enterocyte Insulin Signaling
Monteiro-Sepulveda, M., Touch, S., Mendes-Sá, C., André, S., Poitou, C., Allatif, O., Cotillard, A., Fohrer-Ting, H., Hubert, E.-L., Remark, R., et al. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.05.020 · Cited by 170
Fatty Acid Synthase Modulates Intestinal Barrier Function through Palmitoylation of Mucin 2
Wei, X., YANG, Z. K., Rey, F. E., Ridaura, V. K., Davidson, N. O., Gordon, J. I., & Semenkovich, C. F. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2011.12.006 · Cited by 167
High Fat Diet Causes Depletion of Intestinal Eosinophils Associated with Intestinal Permeability
Johnson, A. M. F., Costanzo, A. E., Gareau, M. G., Armando, A. M., Quehenberger, O., Jameson, J., & Olefsky, J. M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0122195 · Cited by 164
Ghosh, S. S., Bie, J., Wang, J., & Ghosh, S. (2014) · PLoS ONE · doi:10.1371/journal.pone.0108577 · Cited by 162
Microbiome, trimethylamine N-oxide, and cardiometabolic disease
Tang, W. H. W., & Hazen, S. L. (2017) · Translational Research · doi:10.1016/j.trsl.2016.07.007 · Cited by 160
Molecular and Cellular Basis of Microflora-Host Interactions1,
Winkler, P., Ghadimi, D., Schrezenmeir, J., & Kraehenbühl, J.-P. (2007) · Journal of Nutrition · doi:10.1093/jn/137.3.756s · Cited by 158
Circulating microbiome in blood of different circulatory compartments
Schierwagen, R., Silva, M. C. A., Madsen, M. S. A., Kolbe, C. C., Meyer, C. H., Thomas, D., Uschner, F. E., Magdaleno, F., Jansen, C., Pohlmann, A., et al. (2018) · Gut · doi:10.1136/gutjnl-2018-316227 · Cited by 157
The Gordian Knot of dysbiosis, obesity and NAFLD
Mehal, W. Z. (2013) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2013.146 · Cited by 156
Darnaud, M., Santos, A. D., Gonzalez, P., Augui, S., Lacoste, C., Desterke, C., Hertogh, G. D., Valentino, E., Braun, E. J., Zheng, J., et al. (2017) · Gastroenterology · doi:10.1053/j.gastro.2017.11.003 · Cited by 152
Lymphotoxin regulates commensal responses to enable diet-induced obesity
Upadhyay, V., Poroyko, V. A., Kim, T.-J., Devkota, S., Fu, S., Liu, D., Tumanov, A. V., Koroleva, E. P., Deng, L., Nagler‐Anderson, C., et al. (2012) · Nature Immunology · doi:10.1038/ni.2403 · Cited by 145
The circulating microbiome signature and inferred functional metagenomics in alcoholic hepatitis
Puri, P., Liangpunsakul, S., Christensen, J. E., Shah, V. H., Kamath, P. S., Gores, G. J., Walker, S., Comerford, M., Katz, B. P., Borst, A. J., et al. (2017) · Hepatology · doi:10.1002/hep.29623 · Cited by 128
Zimmermann, E., Anty, R., Tordjman, J., Verrijken, A., Gual, P., Tran, A., Iannelli, A., Gugenheim, J., Bédossa, P., Francque, S., et al. (2011) · Journal of Hepatology · doi:10.1016/j.jhep.2010.12.017 · Cited by 123
Ngo, V. L., Abo, H., Maxim, E., Harusato, A., Geem, D., Contreras, O. M., Merlin, D., Gewirtz, A. T., Nusrat, A., & Denning, T. L. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1718902115 · Cited by 123
Kotas, M. E., & Locksley, R. M. (2018) · Immunity · doi:10.1016/j.immuni.2018.06.002 · Cited by 123
Luche, É., Cousin, B., Garidou, L., Sérino, M., Waget, A., Barreau, C., André, M., Valet, P., Courtney, M., Casteilla, L., et al. (2013) · Molecular Metabolism · doi:10.1016/j.molmet.2013.06.005 · Cited by 115
Peptidoglycan from the gut microbiota governs the lifespan of circulating phagocytes at homeostasis
Hergott, C. A., Roche, A. M., Tamashiro, E., Clarke, T. B., Bailey, A., Laughlin, A. L., Bushman, F. D., & Weiser, J. N. (2016) · Blood · doi:10.1182/blood-2015-10-675173 · Cited by 115
Pihlajamäki, J., Kuulasmaa, T., Kamińska, D., Simonen, M., Kärjä, V. J., Grönlund, S., Käkelä, P., Pääkkönen, M. E., Kainulainen, S., Punnonen, K. R. A., et al. (2011) · Journal of Hepatology · doi:10.1016/j.jhep.2011.10.005 · Cited by 109
Epithelial IL-23R Signaling Licenses Protective IL-22 Responses in Intestinal Inflammation
Aden, K., Rehman, A., Falk‐Paulsen, M., Sécher, T., Kuiper, J. W., Tran, F., Pfeuffer, S., Sheibani‐Tezerji, R., Breuer, A., Luzius, A., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.07.054 · Cited by 107
Self-citationBrignardello, J., Morales, P., Díaz-Bautista, E., Romero, J., Brunser, O., & Gotteland, M. (2010) · Alimentary Pharmacology & Therapeutics · doi:10.1111/j.1365-2036.2010.04475.x · Cited by 103
Houghton, D., Hardy, T., Stewart, C. J., Errington, L., Day, C. P., Trenell, M. I., & Avery, L. (2018) · Diabetologia · doi:10.1007/s00125-018-4632-0 · Cited by 97
Pang, J., Xu, W., Zhang, X., Wong, G. L., Chan, A. W. H., Chan, H., Tse, C., Shu, S. S., Choi, P. C., Chan, H. L., et al. (2017) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.14119 · Cited by 91
Chan, K. L., Tam, T. H., Boroumand, P., Prescott, D., Costford, S. R., Escalante, N. K., Fine, N., Tu, Y., Robertson, S. J., Prabaharan, D., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.02.027 · Cited by 88
Compartmentalized Antimicrobial Defenses in Response to Flagellin
Vijayan, A., Rumbo, M., Carnoy, C., & Sirard, J. (2017) · Trends in Microbiology · doi:10.1016/j.tim.2017.10.008 · Cited by 85
Abnormal intestinal permeability to sugars in diabetes mellitus
Mooradian, A. D., Morley, J. E., Levine, A. S., Prigge, W. F., & Gebhard, R. L. (1986) · Diabetologia · doi:10.1007/bf00454879 · Cited by 81
Verbeek, J., Lannoo, M., Pirinen, E., Ryu, D., Spincemaille, P., Elst, I. V., Windmolders, P., Thevissen, K., Cammue, B. P. A., van Pelt, J. F., et al. (2014) · Gut · doi:10.1136/gutjnl-2014-306748 · Cited by 79
Plasma concentration of trimethylamine-N-oxide and risk of gestational diabetes mellitus
Li, P., Zhong, C., Li, S., Sun, T., Huang, H., Chen, X., Zhu, Y., Hu, X., Peng, X., Zhang, X., et al. (2018) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqy116 · Cited by 78
Golden, J. M., Escobar, O. H., Nguyen, M. V. L., Mallicote, M. U., Kavarian, P., Frey, M. R., & Gayer, C. P. (2018) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00354.2017 · Cited by 69
Intestinal Ralstonia pickettii augments glucose intolerance in obesity
Udayappan, S. D., Kovatcheva‐Datchary, P., Bakker, G. J., Havik, S. R., Herrema, H., Cani, P. D., Bouter, K. E. C., Belzer, C., Witjes, J. J., Vrieze, A., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0181693 · Cited by 68
Endotoxemia unrequired in the pathogenesis of pediatric nonalcoholic steatohepatitis
Yuan, J., Baker, S. S., Liu, W., Alkhouri, R. H., Baker, R. D., Xie, J., Ji, G., & Zhu, L. (2013) · Journal of Gastroenterology and Hepatology · doi:10.1111/jgh.12510 · Cited by 64
Chiang, C.-H., Huang, C., Chan, W., Chen, J., & Leu, H. (2010) · Clinical Biochemistry · doi:10.1016/j.clinbiochem.2010.09.003 · Cited by 64
Effect of total starvation and very low calorie diets on intestinal permeability in man
Elia, M., Gören, A., Behrens, R. H., Barber, R. W., & Neale, G. (1987) · Clinical Science · doi:10.1042/cs0730205 · Cited by 54
Probiotic carbohydrates reduce intestinal permeability and inflammation in metabolic diseases
Strowski, M. Z., & Wiedenmann, B. J. (2009) · Gut · doi:10.1136/gut.2009.179325 · Cited by 45
Li, Y., Zheng, J., Hu, Y., Hou, H., Hao, S., Liu, N., & Wang, Y. (2017) · Pharmacognosy Magazine · doi:10.4103/pm.pm_584_16 · Cited by 43
Jin, X. (2007) · World Journal of Gastroenterology · doi:10.3748/wjg.v13.i11.1732 · Cited by 41
Impact of Bariatric Surgery on White Adipose Tissue Inflammation
Labrecque, J., Laforest, S., Michaud, A., Biertho, L. D., & Tchernof, A. (2017) · Canadian Journal of Diabetes · doi:10.1016/j.jcjd.2016.12.003 · Cited by 40
Camargo, A., Jiménez-Lucena, R., Alcala-Diaz, J. F., Rangel-Zúñiga, O. A., García‐Carpintero, S., López-Moreno, J., Blanco-Rojo, R., Delgado‐Lista, J., Pérez‐Martínez, P., van Ommen, B., et al. (2018) · Clinical Nutrition · doi:10.1016/j.clnu.2018.03.016 · Cited by 38
Role of MAIT cells in the immunopathogenesis of inflammatory diseases: New players in old game
Kumar, V., & Ahmad, A. (2017) · International Reviews of Immunology · doi:10.1080/08830185.2017.1380199 · Cited by 36
Liang, H., Lum, H., Alvarez, A. V., Garduño‐García, J. D. J., Daniel, B. J., & Musi, N. (2018) · PLoS ONE · doi:10.1371/journal.pone.0195810 · Cited by 33
Mohammed, N., Tang, L., Jahangiri, A., de Villiers, W. J. S., & Eckhardt, E. R. M. (2012) · Metabolism · doi:10.1016/j.metabol.2012.02.007 · Cited by 32
Satoh, M., & Iwabuchi, K. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01314 · Cited by 26
Li, X., Zhaoyan, Z., Zhang, S., et al. (2017) · Pharmacognosy Magazine · doi:10.4103/pm.pm_256_16 · Cited by 24
Adipose tissue microbiota in humans: an open issue
Zulian, A., Cancello, R., Cesana, E., Rizzi, E., Consolandi, C., Severgnini, M., Panizzo, V., Blasio, A. M. D., Micheletto, G., & Invitti, C. (2016) · International Journal of Obesity · doi:10.1038/ijo.2016.111 · Cited by 23
Pamir, N., McMillen, T. S., Edgel, K. A., Kim, F., & LeBoeuf, R. C. (2012) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00447.2011 · Cited by 17
The signposts and winding roads to immunity and inflammation
Kanneganti, T. (2019) · Nature reviews. Immunology · doi:10.1038/s41577-018-0108-1 · Cited by 5
Research works printed but not linked: 2
- Wen, H. et al. Fatty acid–induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat. Immunol. 12, 408–415 (2011). · DOI · Paper page
- Henao-Mejia, J. et al. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature 482, 179–185 (2012). · DOI · Paper page
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Stefan, N., & Cusi, K. (2022) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(22)00003-1 · Cited by 593
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Self-citation
Metadata
- Authors
- Tilg, H., Zmora, N., Adolph, T. E., & Elinav, E.
- Affiliations
- Innsbruck Medical University (AT)
- Tel Aviv Sourasky Medical Center (IL)
- German Cancer Research Center (DE)
- Corresponding author
- Tilg, Herbert
- Elinav, Eran
- Venue
- Nature Reviews Immunology
- Published
- 2019-08-06
- Volume
- 20
- Issue
- 1
- Pages
- 40-54
- ISSN
- 1474-1733 (ISSN-L)
- 1474-1741
- OpenAlex
- W2965140029
- Semantic Scholar
- 075fe4860874305da0e6be3e1bf99792c631d395
- Cited by
- 1,089
- References
- 267
- Citations by year
- 2026: 149 · 2025: 152 · 2024: 169 · 2023: 162 · 2022: 184 · 2021: 171 · 2020: 88 · 2019: 12
- FWCI
- 10.31
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Nature reviews. Immunology (publishedVersion)
- PubMed (publishedVersion)
- 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
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- gut microbiota, metabolic inflammation, low-grade inflammation, obesity, type 2 diabetes, non-alcoholic fatty liver disease, intestinal barrier dysfunction, microbial metabolites, adipose tissue, liver
- MeSH terms
- Gastrointestinal Microbiome, Animals, Chronic Disease, Humans, Inflammation, Intestinal Mucosa, Metabolic Diseases, Dysbiosis
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